Encyclopedia of Entomology

Encyclopedia of Entomology Encyclopedia of Entomology Edited by John L. Capinera University of Florida Second Editio...

Author: John L. Capinera

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Encyclopedia of Entomology

Encyclopedia of Entomology Edited by John L. Capinera University of Florida

Second Edition

Volume 4 S–Z

Professor John L. Capinera Dept. Entomology and Nematology University of Florida Gainesville FL 32611–0620 USA

Library of Congress Control Number: 2008930112 ISBN: 978-1-4020-6242-1 This publication is available also as: Electronic publication under ISBN 978-1-4020-6359-6 and Print and electronic bundle under ISBN 978-1-4020-6360-2 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in other ways, and storage in data banks. Duplication of this publication or parts thereof is only permitted under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. © 2008 Springer Science+Business Media B.V. The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. springer.com Editor: Zuzana Bernhart, Dordrecht/ Sandra Fabiani, Heidelberg Development Editor: Sylvia Blago, Heidelberg Production Editor: le-tex publishing services oHG, Leipzig Cover Design: Frido Steinen-Broo, Spanien Printed on acid-free paper SPIN: 11757993

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Editorial Board Cyrus Abivardi Swiss Federal Institute of Technnoloy

Eugene J. Gerberg University of Florida

Donald R. Barnard United States Department of Agriculture

Donald W. Hall University of Florida

Jean-Luc Boevé Royal Belgian Institute of Natural Sciences

Marjorie A. Hoy University of Florida

Drion Boucias University of Florida

John B. Heppner Florida State Collection of Arthropods

Paul. M. Choate University of Florida

Pauline O. Lawrence University of Florida

Whitney Cranshaw Colorado State University

Heather J. McAuslane University of Florida

Thomas C. Emmel University of Florida

James L. Nation University of Florida

J. Howard Frank University of Florida

Herb Oberlander United States Department of Agriculture

Severiano F. Gayubo Universidad de Salamanca

Frank B. Peairs Colorado State University

Acknowledgments This project is the labor of many people, including some who labored diligently behind the scenes. Among those to whom I am greatly indebted for their ‘behind-the-scenes’ assistance are Pam Howell and Carole Girimont (first edition) and Pam Howell (second edition) for document processing and editing assistance; Mike Sanford, Pat Hope, and Jane Medley (first edition) and Hope Johnson (second edition) for assistance with the images, and Marsha Capinera for compiling the list of contributors. Ron Cave, Andrei Sourakov, and Lyle Buss helped greatly by supplying numerous photographs for the second edition. Howard Frank deserves special mention for his editing acumen and assistance. Drion Boucias contributed the lengthy unattributed sections on insect pathology. The unattributed biographic sketches with last names beginning with A to J were contributed by Howard Frank. All other unattributed sections were contributed by John Capinera.

Preface Some biologists have called this the ‘Age of Insects.’ Among animals, certainly the diversity of insects is unrivaled. Nearly one million species have been described to date, and some entomologists estimate that as the tropics are fully explored, we will find that there are actually more than three million insect species. The large number of insects is often attributed to the divergence of plants (angiosperms), which provide numerous hosts and places to feed, but if plant feeders are excluded from the tabulation the biodiversity of insects remains unrivaled. Virtually every environment has been exploited by these resilient organisms. Even if one dislikes insects, they are impossible to ignore, and a little knowledge about them could be indispensable should one have a ‘close encounter’ of an unpleasant kind. Insects are remarkable biological organisms. They are small enough to escape the detailed scrutiny of most people, but I have yet to meet anyone whom, once provided the opportunity to examine insects closely (through a microscope) is not completely amazed by the detail and complexity of these exquisitely designed (by natural selection) beasties. They are fascinating in function as well as form. Insects are the only invertebrates to fly, they are disproportionately strong, and their ecological adaptability defies belief. For example, some insects produce their own version of anti-freeze, which allows them to be frozen solid yet to regain normal function upon thawing. Their sensory abilities are beyond human comprehension; a male insect can sometimes locate a female by her ‘perfume’ (pheromone) from several kilometers distance. Although not normally considered intelligent, insects display surprisingly complex behaviors, and altruistic social systems that could well serve as models for human societies. Insects and their close relatives are important for many reasons besides their sheer diversity. Their effect on humans is profound. Insects are our chief competitor for food and fiber resources throughout the world. Annual crop losses of 10 to 15% are attributed to insects, with both pre-harvest and postharvest losses considerably more at times. Insects also are the principal vector of many human, animal, and plant diseases, including viruses, mollicutes, bacteria, fungi, and nematodes. The ability to transmit diseases magnifies their effect, and makes it more difficult to manage injury. Over the course of human history, insect-transmitted disease has caused untold human suffering. For example, introduction of flea-transmitted bubonic plague to Europe centuries ago killed millions of people and caused severe disruption to western civilization. Though less dramatic, mosquito-transmitted malaria kills thousands annually throughout the world, and unlike plague, which is now mostly a historical footnote, the toll continues to mount. Advances in technology, particularly the introduction of chemical insecticides, have done much to remove the threat of insect-related damage from the consciousness of most humans. Insecticides are applied preventatively to avoid pre- and post-harvest damage to crops, to our dwellings, and to our landscape. This is an oft-overlooked but remarkable achievement that has increased stability in the supply and price of resources, and in the lives of resource producers. No longer are people faced with starvation or economic ruin due to the ravages of insects; in almost all parts of the world, the ready availability of insecticides can be used to prevent massive insect population outbreaks. However, we realize increasingly that this approach is not without its own set of health, environmental and economic costs, and alleviating dependency on insecticides, or making alternatives to insecticides more readily available, has assumed greater priority.

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We are faced with an interesting dichotomy. There is a wealth of information about insects, but it is known mostly to ‘insect scientists’ (entomologists). The public (non-entomologists or 99.99% of all people) has little knowledge about insects, and poor access to vital information about these important organisms. So this encyclopedia is presented to bridge the gap – to better enable those with a need to know to find fundamental information provided by more than 450 experts in the field of entomology. We provide a broad overview of insects and their close relatives, including taxonomy, behavior, ecology, physiology, history, and management. Importantly, we provide critical links to the entomological literature, much of which presently is unavailable for search electronically. The contributors are distinguished entomologists from around the world. They hope that the availability of this encyclopedia will help others to reap the benefits of centuries of discovery, and to discover the wonders that make the study of insects so compelling. It was constructed with college and university students in mind, but others may find it a handy reference. John L. Capinera, Gainesville (Florida)

April, 2008

Highlights of the Encyclopedia of Entomology Major Taxa of Insects and Their Near Relatives Alderflies and Dobsonflies (Megaloptera) Angel Insects (Zoraptera) Bark-Lice, Book-Lice, or Psocids (Psocoptera) Beetles (Coleoptera) Bristletails (Archeognatha) Bugs (Hemiptera) Butterflies and Moths (Lepidoptera) Caddisflies (Trichoptera) Centipedes (Chilopoda) Chewing and Sucking Lice (Phthiraptera) Cockroaches (Blattodea) Diplurans (Diplura) Dragonflies and Damselflies (Odonata) Earwigs (Dermaptera) Fleas (Siphonaptera) Flies (Diptera) Gladiators (Mantophasmatodea) Grasshoppers, Katydids, and Crickets (Orthoptera) Lacewings, Antlions, and Mantispids (Neuroptera) Mayflies (Ephemeroptera) Millipedes (Diplopoda) Mites (Acari) Pillbugs and Sowbugs, or Woodlice (Isopoda) Praying Mantids (Mantodea) Proturans (Protura) Rock Crawlers (Grylloblattodea) Scorpionflies (Mecoptera) Scorpions (Scorpiones) Sea Spiders (Pycnogonida) Silverfish (Zygentoma) Snakeflies (Raphidioptera) Spiders (Araneae) Springtails (Collembola) Stick and Leaf Insects (Phasmida)

Stoneflies (Plecoptera) Stylopids (Strepsiptera) Symphylans (Symphyla) Termites (Isoptera) Thrips (Thysanoptera) Ticks (Ixodida) Wasps, Ants, Bees, and Sawflies (Hymenoptera) Webspinners (Embiidina)

Other Groups Anagrus Fairyflies (Hymenoptera: Mymaridae) Ants (Hymenoptera: Formicidae) Aphids (Hemiptera: Aphididae) Apoid Wasps (Hymenoptera: Apoidea: Spheciformes) Argasid (Soft) Ticks (Acari: Ixodida: Argasidae) Assassin Bugs, Kissing Bugs and Others (Hemiptera: Reduviidae) Bark Beetles, Dendroctonus spp. (Coleoptera: Curculionidae: Scolytinae) Bees (Hymenoptera: Apoidea: Apiformes) Bess Beetles (Coleoptera: Passalidae) Biting Midges, Culicoides (Diptera: Ceratopogonidae) Black Flies (Diptera: Simuliidae) Blister Beetles (Coleoptera: Meloidae) Bulb Mites, Rhizoglyphus (Acari: Acaridae) Burnet Moth Biology (Lepidoptera: Zygaenidae) Brush-Footed Butterflies (Lepidoptera: Nymphalidae) Butterflies (Lepidoptera: Rhopalocera) Carpenter Bees (Hymenoptera: Apidae: Xylocopinae) Carrion Beetles (Coleoptera: Silphidae) Cicadas (Hemiptera: Cicadoidea) Clearwing Moths (Lepidoptera: Sesiidae)

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Coreid Bugs and Relatives: Coreidae, Stenocepahidae, Alydidae, Rhopalidae, and Hyocephalidae (Hemiptera: Coreoidea) Crane Flies (Diptera: Tipulidae and Others) Dance Flies, Balloon Flies, Predaceous Flies (Diptera: Empidoidea, exclusive of Dolichopodidae) Darkling Beetles (Coleoptera: Tenebrionidae) Earwigflies (Mecoptera: Meropeidae) Fairyflies (Hymenoptera: Mymaridae) Fireflies (Coleoptera: Lampyridae) Flea Beetles (Coleoptera: Chrysomelidae: Alticinae) Four-Legged Mites (Eriophyoidea or Tetrapodili) Fruit Flies (Diptera: Tephritidae) Fungus Gnats (Diptera: Mycetophilidae and Others) Gall Midges (Diptera: Cecidomyiidae) Gall Wasps (Hymenoptera: Cynipidae) Giant Water Bugs (Hemiptera: Belostomatidae) Greater Fritillaries or Silverspots, Speyeria [= Argynnis] (Lepidoptera: Nymphalidae) Ground Beetles (Coleoptera: Carabidae): Taxonomy Harvester Ants, Pogonomyrmex (Hymenoptera: Formicidae) Horse Flies and Deer Flies (Diptera: Tabanidae) Jerusalem Crickets (Orthoptera: Stenopelmatidae) Jumping Spiders (Arachnida: Araneae: Salticidae) June Beetles, Phyllophaga spp. (Coleoptera: Scarabaeidae: Melolothinae: Melolothini) Katydids (Orthoptera: Tettigoniidae) Kissing Bugs (Hemiptera: Reduviidae: Triatominae) Lace Bugs (Hemiptera: Tingidae) Ladybird Beetles (Coccinellidae: Coleoptera) Leaf Beetles (Coleoptera: Chrysomelidae) Leaf-Cutting Ants (Formicidae: Myrmicinae: Attini) Leaf-Miner Flies (Diptera: Agromyzidae) Leafhoppers (Hemiptera: Cicadellidae) Longicorn, Longhorned, or Round-Headed Beetles (Coleoptera: Cerambycidae) Long-Legged Flies (Diptera: Dolichopodidae) Mantidflies (Neuroptera: Mantispidae)

Marine Insects and the Sea-Skater Halobates (Hemiptera: Gerridae) Metalmark Butterflies (Lepidoptera: Riodinidae) Microdon spp. (Diptera: Syrphidae) Minute Pirate Bugs (Hemiptera: Anthocoridae) Mosquitoes (Diptera: Culicidae) Moths (Lepidoptera: Heterocera) Nuttalliellidae (Acari) Orchid Bees (Hymenoptera: Apidae) Parasitic Hymenoptera (Hymenoptera: Parasitica) Paederus Fabricius (Coleoptera: Staphylinidae: Paederinae) Pelecinid Wasps (Hymenoptera: Pelecinidae) Periodical Cicadas, Magicicada spp. (Hemiptera: Cicadidae) Phytoseiid Mites (Acari: Phytoseiidae) Powderpost Beetles (Coleoptera: Bostrichidae: Lyctinae) Pine Tip Moths, Rhyacionia spp. (Lepidoptera: Tortricidae) Plant Bugs (Hemiptera: Miridae) Planthoppers (Hemiptera: Fulgoroidea) Plume Moths (Lepidoptera: Pterophoridae) Powderpost Beetles (Coleoptera: Bostrichidae: Lyctinae) Predatory Stink Bugs (Hemiptera: Pentatomidae: Asopinae) Riffle Beetles (Coleoptera: Elmidae) Robber Flies (Diptera: Asilidae) Rove Beetles (Coleoptera: Staphylinidae) Sac Spiders (Arachnida: Araneae: Tengellidae, Zorocratidae, Miturgidae, Anyphaenidae, Clubionidae, Liocranidae, and Corinnidae) Sap Beetles (Coleoptera: Nitidulidae) Sawflies (Hymenoptera: Symphyta) Sawflies (Hymenoptera: Tenthredinidae) Scale Insects and Mealybugs (Hemiptera: Coccoidea) Scarab Beetles (Coleoptera: Scarabaeoidea) Skin-Piercing and Blood-Feeding Moths, Calyptra spp. (Lepidoptera: Noctuidae: Calpinae) Soil Mites (Acari: Oribatida and Others) Spittlebugs (Hemiptera: Cercopoidea) Spongillaflies (Neuroptera: Sisyridae) Stilt Bugs (Hemiptera: Berytidae)


Stink Bugs (Hemiptera: Pentatomidae), Emphasizing Economic Importance Tachinid Flies (Diptera: Tachinidae) Tent Caterpillars, Malacosoma spp. (Lepidoptera: Lasiocampidae) Tiger Beetles (Coleoptera: Carabidae: Collyrinae and Cicindelinae) Termites (Isoptera) in South America Tiphiid Wasps (Hymenoptera: Tiphiidae) Treehoppers (Hemiptera: Membracidae) Underwing Moths –Catocala (Lepidoptera: Noctuidae) Velvet Ants (Hymenoptera: Mutillidae) Water Penny Beetles (Coleoptera: Psephenidae) Weevils, Billbugs, Bark Beetles, and Others (Coleoptera: Curculionoidea) Weta (Orthoptera: Anostostomatidae, Rhaphidophoridae) Whiteflies (Hemiptera: Aleyrodidae)

Morphology and Anatomy Abdomen of Hexapods Antennae of Hexapods Head of Hexapods Internal Anatomy of Insects Alimentary Canal and Digestion Legs of Hexapods Mouthparts of Hexapods Thorax of Hexapods Wings of Insects Eggs of Insects Nervous System Eyes and Vision Integument: Structure and Function Nygma Wing Coupling

Physiology Accessory Pulsatile Hearts Adipokinetic and Hypertrehalosemic Neurohormones

Alarm Pheromones Alary Muscles Alimentary Canal and Digestion Biological Clock of the German Cockroach, Blattella germanica (L.) Chordotonal Sensory Organs Corazonin Cryptobiosis Diapause Dorsal Vessel: Heart and Aorta Ecdysone Agonists, a Novel Group of Insect Growth Regulators Ecdysteroids Embryogenesis Endocrine Regulation of Insect Reproduction Eyes and Vision Fatty Acid Binding Proteins Fireflies: Control of Flashing Hemocytes in Insects: Their Morphology and Function H-Organ Immunity Integument: Structure and Function Entomopathogenic Fungi and Their Host Cuticle Juvenile Hormone Learning in Insects: Neurochemistry and Localization of Brain Function Locomotion and Muscles Metamorphosis Midgut and Insect Pathogens Multifunctional Semiochemicals Nervous System Neurological Effects of Insecticides and the Insect Nervous System Nutrition in Insects Oogenesis Pheromones Polyphenism in Insects and Juvenile Hormone (JH) Prothoracicotropic Hormone Reflex Bleeding Regulation of Sex Pheromone Production in Moths Reproduction Reselin

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Sex Attractant Pheromones Social Insect Pheromones Sound Production in the Cicadoidea Storage Proteins Storage Protein Receptors Stress-Induced Host Plant Free Amino Acids and Insects Taste and Contact Chemoreception Tracheal System and Respiratory Gas Exchange Ultrastructure of Insect Sensilla Venoms and Toxins in Insects Venoms of Ectoparasitic Wasps Venoms of Endoparasitic Wasps Vitellogenesis Water Balance

Genetics Bacteriophage WO Behavior of Insects: Genetic Analysis by Crossing and Selection Behavior: Molecular Genetic Analyses Genetic Modification of Drosophila By P Elements Genetic Sexing Genetic Transformation Genomes of Insects Homeotic Genes in Coleoptera Honey Bee Sexuality: A Historical Perspective Meiotic Drive in Insects Molecular Diagnosis Polytene Chromosomes Sex Ratio Modification by Cytoplasmic Agents Sibling Species Transgenic Arthropods for Pest Management Programs RNA Interference

Behavior Acoustic Communication in Insects Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)

Arthropod-Associated Plant Effectors (AAPEs): Elicitors and Suppressors of Crop Defense Attraction of Insects to Organic Sulfur Compounds in Plants Blister Beetle Antennal Twisting Behavior Construction Behavior of Insects Crypsis Cycloalexy Deflection Marks Deimatic Behavior Drumming Communication and Intersexual Searching Behavior of Stoneflies (Plecoptera) Environmental Influences on Behavioral Development in Insects Facultative Predators Flash Colors Glowworms Gregarious Behavior in Insects Hilltopping Host Location in Parasitic Wasps Host Plant Selection by Insects Inverted Copulation Learning in Insects Marking Insects for Studying Ecology and Behavior Mosquito Oviposition Multifunctional Semiochemicals Myrmecomorphy Myrmecophiles Parental Care in Heteroptera (Hemiptera: Heteroptera) Puddling Behavior in Butterflies Red Imported Fire Ant Territorial Behavior Reflex Bleeding Sociality of Insects Sound Production in the Cicadoidea Sphragis Spider Behavior and Value in Agricultural Landscapes Thermoregulation in Insects Vibrational Communication Visual Mating Signals Walking Stick Defensive Behavior and Regeneration of Appendages


Ecology and Evolution Adaptation of Indigenous Insects to Introduced Crops Allelochemicals Ant-Plant Interactions Aposematism Arthropod-Associated Plant Effectors (AAPEs): Elicitors and Suppressors of Crop Defense Bioclimatic Models in Entomology Biogeography Brachelytry Bromeliad Fauna Cannibalism Carnivorous Plants Carnivory and Symbiosis in the Purple Pitcher Plant Castes Cave Adapted Insects Cave Habitat Colonization Chemical Ecology of Insects Cold Tolerance in Insects Conservation of Insects Cryptobiosis Decomposer Insects Diapause Eggs of Insects Endophytic Fungi and Grass-Feeding Insects Food Habits of Insects Fossil Record of Insects Furanocoumarins Gall Formation Galápagos Islands Insects: Colonization, Structure, and Evolution Geological Time Glowworms Gregarious Behavior in Insects Ground Beetle (Coleoptera: Carabidae) Feeding Ecology Hypertely Hypericin Inquilines and Cleptoparasites

Insectivorous Plants Life Tables Mimicry Mosquito Larval Feeding Ecology Mosquito Overwintering Ecology Natural Enemy Attraction to Plant Volatiles Night Blooming Plants and Their Insect Pollinators Nutrient Content of Insects Outbreaks of Insects Overwintering in Insects Phase Polymorphism in Locusts Phylogenetics Phytotelmata Plant Extrafloral Nectaries Plant Secondary Compounds and Phytophagous Insects Pollination and Flower Visitation Pollination by Osmia Bees (Hymenoptera: Megachilidae) Pollination by Yucca Moths Pollution and Terrestrial Arthropods Polyphenism Polyacetylenes and Their Thiophene Derivatives Predation: The Role of Generalist Predators in Biodiversity and Biological Control Pyrophilous Insects Pyrrolizidine Alkaloids and Tiger Moths (Lepidoptera: Arctiidae) Retournement and Deversement of the Aedeagus in Coleoptera Rhythms of Insects Seed Predation by Insects Sexual Selection Sociality of Insects Species Concepts Speciation Processes Among Insects Symbiosis Between Planthoppers and Microorganisms Trichomes and Insects Tritrophic Interactions Water Pollution and Insects

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Microbiology and Pathology Microbial Control of Insects Microbial Control of Medically Important Insects Symbionts of Insects Symbiosis Between Planthoppers and Microorganisms Symbiotic Viruses of Parasitic Wasps Fungal Pathogens in Insects Entomopathogenic Fungi and Their Host Cuticle Midgut and Insect Pathogens Immunity Pathogens of Whiteflies (Hemiptera: Aleyrodidae) Diseases Of Grasshoppers and Locusts Nematode Parasites of Insects Nematomorphs (Nematomorpha) Entomopathogenic Nematodes and Insect Management Thrips-Parasitic Nematodes American Foulbrood Amoebae Ascosphaera apis Ascoviruses Bacillus sphaericus Bacillus thuringiensis Baculoviruses Beauveria Birnaviruses Cestodes Coelomomyces Culicinomyces Entomophthorales Entomopoxviruses (Poxviruses) Granulovirus Helicosporium Hirsutella Iridoviruses Laboulbeniales Lagenidium giganteum Lecanicillium Metarhizium Microsporidia (Phylum Microsporidia) Nosema locustae (Protozoa: Microsporidia)

Nosema disease Nomuraea Orcytes virus and other Nudiviruses Paecilomyces Paenibacillus Parvoviruses Polydnaviruses Reoviruses Rhabdoviruses Septobasidium Serratia entomophila Small RNA viruses of invertebrates Sorosporella Trichomycetes

Humans and Insects Apiculture (Beekeeping) Aquatic Entomology and Flyfishing Butterfly Counts Butterfly Gardening Careers in Entomology Collecting and Preserving Insects Common (Vernacular) Names of Insects Conservation of Insects Costs and Benefits of Insects Cultural Entomology Entomodeltiology Entomophagy: Human Consumption of Insects Forensic Entomology History and Insects Honeybee Sexuality: An Historical Perspective Identification of Insects Insects as Aphrodisiacs Invasive Species Lacquers and Dyes From Insects Literature and Insects Maggot Therapy Marking Insects for Studying Ecology and Behavior Midges as Human Food Mythology and Insects Native American Culture and Insects Popularity of Insects


Pronunciation of Scientific Names and Terms Psychiatry And Insects: Phobias and Delusions of Insect Infestations in Humans Rearing of Insects Scientific Names and Other Words From Latin and Greek Sericulture Silk Teaching and Training in Entomology: Institutional Models Teaching Entomology: A Review of Techniques

Notable and Pioneer Entomologists Abafi-Aigner, Lajos (Ludwig Aigner) Abbott, John Agassiz, Jean Louis Rodolphe Aldrovandi, Ulisse (Ulysse, Ulysses) Alexander, Charles Paul Amerasinghe, Felix P. Andrewartha, Herbert George Arnett, Jr., Ross Harold Audinet-Serville, Jean-Guillaume Audouin, Jean-Victor Barber, Herbert Spencer Bates, Henry Walter Bates, Marston Beck, Stanley Dwight Beklemishev, Vladimir NikolayevicH Bell, William J. Becquaert, Joseph Charles Berlese, Antonio Bernhauer, Max Bertram, Douglas Somerville Bíró, Lajos Blackburn, Thomas Blackwelder, Richard Elliot Blaisdell, Frank Ellsworth Blatchley, Willis Stanley Bodenheimer, Friedrich (Frederick) Simon Bohart, Richard M. Boheman, Carl Heinrich Boisduval, Jean-Baptiste Alphonse Dechauffour

Bokor, Elemér Bonnet, Charles Borgmeier, Thomas Bøving, Adam Giede Brauer, Friedrich Moritz Broun, Thomas Bruch, Carlos Brues, II, Charles Thomas Brullé, Gaspard Auguste Brunner von Wattenwyl, Carl Buffon, Georges Louis Leclerc (Comte de) Burgess, Albert Franklin Burmeister, Carl Hermann Conrad Buxton, Patrick Alfred Calvert, Philip Powell Cameron, Malcolm Candèze, Ernest Charles Auguste Carpenter, Frank Morton Carter, Herbert James Casey, Thomas Lincoln Caudell, Andrew Nelson Chagas, Carlos Justiniano Ribeiro Chaudoir, Maximilien Stanislavovitch de Champion, George Charles Chapman, Reginald Frederick Chevrolat, Louis Alexandre Auguste Chiang, Huai C. China, William Edward Chittenden, Frank Hurlbut Christophers, (Sir) Samuel Rickard Cockerell, Theodor Dru Alison Comstock, John Henry Coquillett, Daniel William Craw, Alexander Cresson, Ezra Townsend Criddle, Norman Crotch, George Robert Crowson, Roy Albert Csiki, Erno (Ernst Dietl) Curran, Charles Howard Curtis, John Cushman, Robert Asa Cuvier, (Baron) Georges Léopold Chretien Frédéric Dagobert Dahlbom, Anders Gustav

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Darlington, Jr., Philip J. Darwin, Charles Davis, William Thompson Debach, Paul Degeer, Carl (Carolus, Karl, Charles) Dejean, Pierre François Marie Auguste Dethier, Vincent Gaston Dobzhansky, Theodosius Grigorievich Donisthorpe, Horace St. John Kelly Douglas, John William Drake, Carl John Dudich, Endre Dufour, Léon Jean Marie Duponchel, Philogène August-Joseph Dyar, Harrison Grey Edwards, William Henry Eickwort, George C. Emerson, Alfred Edwards Endrödi, Sebö (Sebastian Endrödi) Endrödy-Younga, Sebastian (Sebestyén Endrödy-Younga, Sebestyén Endrödy) Erichson, Wilhelm Ferdinand Esaki, Teiso Evans, Howard Ensign Fabre, Jean-Henri Casimir Fabricius, Johann Christian Fairchild, Alexander Graham Bell Fairmaire, Léon Fall, Henry Clinton Fauvel, Charles Adolphe Albert Felt, Ephraim Porter Fenichel, Sámuel Fennah, Ronald Gordon Fernald, Charles Henry Ferris, Gordon Floyd Fischer Von Waldheim, Gotthelf Fitch, Asa Fletcher, James Foote, Richard H. Forbes, Stephen Alfred Ford, Edmund Brisco Forel, Auguste Henri Fourcroy, Antoine-François (Comte de) Frisch, K. von Frivaldszky, Imre

Frivaldszky, János Froggatt, Walter Wilson Gahan, Arthur Burton Ganglbauer, Ludwig Germar, Ernst Friedrich Ghilarov, Mercury Sergeevich Girault, Alexandre Arsène Glover, Townend Gmelin, Johann Friedrich Goeldi, Emil (Emilio) August Gorgas, William Crawford Graham, Marcus William Robert de Vere Grassi, Giovanni Battista Gravenhorst, Johan Ludwig Christian Gressitt, Judson Linsley Grote, Augustus Radcliffe Guenée, Achille Guérin-Méneville, Félix Edouard Gundlach, Johannes (Juan) Christopher Gyllenhal, Leonhard Haddow, Alexander John Hagen, Hermann August Hagen, Kenneth Sverre Hahn, Carl Wilhelm Hale Carpenter, Geoffrey Douglas Haliday, Alexander Henry Handlirsch, Anton Hansen, Viktor Harris, Thaddeus William Hatch, Melville Harrison Heer, Oswald Henneguy, Louis Félix Hennig, Willi Herman, Ottó Herrich-Schäffer, Gottlieb August Hewitt, Charles Gordon Hinton, Howard Everest Hobby, Bertram Maurice Hocking, Brian Hogstraal, Harry O. Holland, William Jacob Hope, Frederick William Hopkins, Andrew Delmar Horn, George Henry Horn, Hermann Wilhelm Walther


Horsfall, William R. Howard, Leland Ossian Hübner, Jacob Huffaker, Carl Barton Hungerford, Herbert Barker Ihering, Hermann Von Imms, Augustus Daniel Jacquelin du Val, Pierre Nicolas Camille Jeannel, René Johannsen, Oskar Augustus Jordan, Heinrich Ernst Karl Kaszab, Zoltán Kellogg, Vernon Lyman Kennedy, John S. Kershaw, John Crampton Wilkinson Kevan, Douglas Keith McEwan Kiesenwetter, Ernst August Hellmuth von Kirby, William Klee, Waldemar G. Knipling, Edward Fred Koebele, Albert Kraatz, Ernst Gustav Kring, James Burton Lamarck, Jean-Baptiste Latreille, Pierre André Lea, Arthur Mills Lea, H. Arnold LeConte, John Lawrence Leech, Hugh Bosdin Lefroy, Harold Maxwell Leng, Charles William Lepeletier, Amédée Louis Michel Lindroth, Carl H. Linnaeus, Carolus (Linné, Carl von) Linsley, Earle Gorton Loew, Hermann Lorguin, Pierre Joseph Michel Lugger, Otto Macleay (Sir) William John Macquart, Pierre Justin Marie Mallis, Arnold Mann, William M. Mannerheim, Carl Gustav von Marlatt, Charles Lester Marx, George

Maskell, William Miles Masters, George Matheson, Robert Matsumura, Shonen Mcdunnough, James Halliday Mcglashan, Charles Fayette Meigen, Johann Wilhelm Mellanby, Kenneth Melander, Axel Leonard Melsheimer, Frederick Valentine Ménétriés, Edouard Metcalf, Clell Lee Metcalf, Zeno Payne Meyrick, Edward Miller, David M’lachlan, Robert Morgan, Thomas Hunt Morrison, Herbert Knowles Morse, Albert Pitts Motschulsky, Victor Ivanovich Müller, Johann Friedrich Theodor Müller, Josef Mulsant, Etienne Needham, James George Newell, Wilmon Newman, Edward. Newsom, Leo Dale Olivier, Guillaume Antoine Ormerod, Eleanor Anne Osborn, Herbert Osten Sacken, C.R. Packard, Alpheus Spring Painter, Reginald Henry Palm, Thure Pass, Bobby Clifton Patch, Edith Marion Paykull, Gustaf Peairs, Leonard Marion Peck, William Dandridge Petrunkevitch, Alexander Pickett, Allison Deforest Pomerantsev, Boris Ivanovich Potter, Charles Prokopy, Ronald J. Provancher, (l’abbé) Léon

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Putzeys, Jules Antoine Adolphe Henri Rabb, Robert Lamar Radoshkowsky, Octavius John de Réaumur, René Antoine Ferchault Redi, Francesco Redtenbacher, Ludwig Reed, Walter. Rehn, James Abram Garfield Reitter, Edmund Remington, Charles Lee Rey, Claudius Richards, Owain Westmacott Riley, Charles Valentine Robineau-Desvoidy, Jean Baptiste Rondani, Camillo Rosen, David Ross, Herbert Holdsworth Rothschild, Miriam Roubal, Jan Sabrosky, Curtis Sahlberg, Carl Reinhold Sailer, Reece I. Sanderson, Dwight Saunders, William Saussure, Henri Louis Frederic de Say, Thomas Scheerpeltz, Otto Schneiderman, Howard Allen Schwarz, Eugene Amandus Scudder, Samuel Hubbard Selys-Longchamps, Michel Edmond de Sharp, David Shelford, Victor Ernest Signoret, Victor Antoine Silvestri, Filippo Sylveira Caldeira, João da Smirnoff, Vladimir A. Smith, John Bernhardt Smith, Harry Scott Smith, Ray F. Snodgrass, Robert Evans Snow, Francis Huntington Spielman, Andrew Stål, Carl Steinhaus, Edward Arthur

Stern, Vernon M. Swammerdam, Jan Swezey, Otto Herman Szent-Ivány, József Gyula Hubertus Thomas, Cyrus Thomson, Carl Gustav Thunberg, Carl Peter Tillyard, Robin John Torre-Bueno, José Rollin De La Townes, Jr., Henry K. Treherne, John E Uhler, Philip Reese Usinger, Robert Leslie Uvarov, (Sir) Boris Petrovich Van Den Bosch, Robert Van Duzee, Edward Payson Varley, George C Viereck, Henry Lorenz Walker, Francis Waloff, Nadejda Walsh, Benjamin Dann Walsingham, (Lord) Thomas de Gray Wasmann, Erich Wesmael, Constantin Westwood, John Obadiah Wheeler, William Morton Wiedemann, Christian Rudolph Wilhelm Wigglesworth, (Sir) Vincent Brian Williams, Carroll Milton Williston, Samuel Wendell Wirth, Willis Wagner Wolcott, George N. Wollaston, Thomas Vernon Young, Jr., David A Zeller, Philipp Christoph Zetterstedt, Johann Wilhelm Zachvatkin (Jasykov), Aleksei Alekseevich

Pest Management Integrated Pest Management (IPM) Economic Injury Level (EIL) and Economic Threshold (ET) Concepts in Pest Management


Costs and Benefits of Insects Methods for Measuring Crop Losses by Insects Sampling Arthropods Traps for Capturing Insects Scale and Hierarchy in Integrated Pest Management Phenology Models for Pest Management Agroecology Organic Agriculture Regulatory Entomology Regulations Affecting the Implementation of Regulatory Entomology Practices Invasive Species Pest Risk Analysis Mechanical Protection of Humans from Arthropod Attacks and Bites Repellents of Biting Flies Physical Management of Insect Pests Kaolin-Based Particle Films for Arthropod Control Controlled Atmosphere Technologies for Insect Control Cultural Control of Insects Plant Resistance to Insects Resistance of Solanaceous Vegetables to Insects Cover, Border and Trap Crops for Pest and Disease Management Polyculture Microbial Control of Insects Visual Attractants and Repellents in IPM Push-Pull Strategy for Insect Pest Management Area-Wide Insect Pest Management Sterile Insect Technique Filter Rearing System for Sterile Insect Technology Weeds in Crop Systems for Pest Suppression Biological Control of Weeds Weed Biological Control in Australia Biological Control of Invasive Plants in Latin America Host Specificity of Weed-Feeding Insects Foreign Exploration for Insects that Feed on Weeds Flower Strips as Conservation Areas for Pest Management

Augmentative Biological Control Classical Biological Control Conservation Biological Control Natural Enemies Important in Biological Control Mass Rearing of Natural Enemies Culture of Natural Enemies on Factitious Foods and Artificial Diets Classical Biological Control of Chestnut Gall Wasp in Japan Conservation of Ground Beetles in Annual Crops Filth Fly Parasitoids (Hymenoptera: Pteromalidae) in North America Carabid Beetles (Coleoptera: Carabidae) as Parasitoids History of Biological Control of Wheat Stem Sawflies (Hymenoptera: Cephidae) Parasitism of Lepidoptera Defoliators in Sunflower and Legume Crops, and A djacent Vegetation in the Pampas of Argentina Transmission of Plant Diseases by Insects Plant Viruses and Insects Management of Insect-Vectored Pathogens of Plants Transmission of Xylella fastidiosa Bacteria by Xylem-Feeding Insects Vectors of Phytoplasmas

Pesticides and Pesticide Application Acaricides or Miticides Boric Acid DDT Insecticides Insecticide Application: The Dose Transfer Process Food-Based Poisoned Baits for Insect Control Soil Fumigation Structural Fumigation Insecticide Bioassay Insecticide Formulation Insecticide Resistance Insecticide Toxicity

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Pesticide Hormoligosis Synergism Chronotoxicology Detoxification Mechanisms in Insects Enhanced Biodegradation of Soil-Applied Pesticides Pesticide Resistance Management Natural Products Used for Insect Control Botanical Insecticides Chinaberry, Melia azedarach, a Biopesticidal Tree Pyrethrum and Persian Insect Powder Neem Horticultural Oils Soaps as Insecticides Diatomaceous Earth Photodynamic Action in Pest Control and Medicine Neurological Effects of Insecticides and the Insect Nervous System Regulations Affecting Use of Pesticides

Pests Groups and Their Management Agricultural Crop Pests in Southeast Asia Including South China Alfalfa (Lucerne) Pests and Their Management Apple Pests and Their Management Banana Pests and Their Management Bark Beetles in The Genus Dendroctonus Cassava Pests and Their Management Citrus Pests and Their Management Coffee Pests and Their Management Crucifer Pests and Their Management Desert Locust, Schistocerca gregaria Forskål (Orthoptera: Acrididae) Plagues Grasshoppers and Locusts as Agricultural Pests Grasshoppers of the Argentine Pampas Grasshopper and Locust Pests in Africa Grasshopper and Locust Pests in Australia Grasshopper Pests in North America Gramineous Lepidopteran Stem Borders in Africa Mahogany Pests and Their Management

Maize (Corn) Pests and Their Management Mite Pests of Crops in Asia Musk Thistle Suppression Using Weevils For Biological Control Palm Insects Pests and Their Natural Enemies (Parasitoids and/or Predators) in The Middle East Potato Pests and Their Management School IPM, or Pest Management on School Grounds Shade Tree Arthropods and Their Management Small Fruit Pests and Their Management Stored Grain and Flour Insects and Their Management Sugarcane Pests and Their Management Sweetpotato Weevils and Their Eradication Programs in Japan Tropical Fruit Pests and Their Management Turfgrass Insects of the United States and Their Management Urban Entomology Vegetable Pests and Their Management Veterinary Pests and Their Management Wheat Pests and Their Management Whitefly Bioecology and Management in Latin America Wood-Attacking Insects

Medical and Veterinary Entomology African Horse Sickness Viruses Argasid (Soft) Ticks (Acari: Ixodida: Argasidae) Avian (Bird) Malaria Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) Biting Midges, Culicoides spp. (Diptera: Ceratopogonidae) Black Flies Attacking Livestock: Simulium arcticum Malloch and Simulium luggeri Nicholson & Mickel (Diptera: Simuliidae) Bluetongue Disease Bovine Hypodermosis: Phenology in Europe Brown Dog Tick, Rhipicephalus sanguineus (Latreille) (Acari: Ixodida: Ixodidae)


Cat Flea, Ctenocephalides felis felis Bouché (Siphonaptera: Pulicidae) Chagas, Carlos Justiniano Ribeiro Chagas Disease or American Trypanosomiasis Chagas Disease: Biochemistry of the Vector Chikungunya Chironomids as a Nuisance and of Medical Importance Cockroaches and Disease Dermatitis Linearis Dengue Dirofilariasis Eastern Equine Encephalitis Horse Flies and Deer flies House Fly, Musca domestica L. (Diptera: Muscidae) Human Botfly, Dermatobia hominis (Linneaus, Jr.) (Diptera: Oestridae) Human Lice Human Lymphatic Filariasis (Elephantiasis) Human Scabies Hypodermosis in Deer Japanese Encephalitis La Crosse Encephalitis Leishmaniasis Lyme Borreliosis Maggot Therapy Malaria Mechanical Protection of Humans from Arthropod Attacks and Bites Microbial Control of Medically Important Insects Mites (Acari) Mosquitoes (Diptera: Culicidae) Mosquitoes as Vectors of Viral Pathogens Mosquito Oviposition Myiasis Onchocerciasis Paederina Pederin Pathogen Transmission by Arthropods Piroplasmosis: Babesia and Theileria Reed, Walter Repellents of Biting Flies Rocky Mountain Spotted Fever

Rocky Mountain Wood Tick, Dermacentor andersoni Stiles (Acari: Ixodidae) Rodent Trypanosomiasis: A Comparison Between Trypanosoma lewisi and Trypanosoma musculi Simulium spp. Vectors of Onchocerca volvulus Skin-Piercing and Blood-Feeding Moths, Calyptra spp. (Lepidoptera: Noctuidae: Calpinae) Sleeping Sickness or African Trypanosomiasis St. Louis Encephalitis Sugar-Feeding in Blood-Feeding Flies Taiga Tick, Ixodes persulcatus Schulze (Acari: Ixodida: Ixodidae) Tick Paralysis Ticks (Ixodida) Ticks as Vectors of Pathogens Trypanosomes Tsetse Flies, Glossina spp. (Diptera: Glossinidae) Types of Pathogen Transmission by Arthropods Vector Capability of Blood-Sucking Arthropods: A Forecasting Matrix Venoms And Toxins in Insects West Nile Fever Yellow Fever

Arthropods of Economic Importance African Armyworm, Spodoptera exempta (Lepidoptera: Noctuidae) African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae) African Mahogany-Feeding Caterpillar, Heteronygmia dissimilis Aurivillius (Lepidoptera: Lymantriidae) African Pine-Feeding Grasshopper, Plagiotriptus pinivorus (Descamps) (Orthoptera: Eumastacidae) Alfalfa Leafcutting Bee, Megachile rotundata Fabricius (Hymenoptera: Megachilidae) Allegheny Mound Ant, Formica exsectoides Foretl (Hymenoptera: Formicidae)

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American Grasshopper, Schistocerca americana (Drury) (Orthoptera: Acrididae) Almond Seed Wasp, Eurytoma amygdali Enderlein (Hymenoptera: Eurytomidae) American Serpentine Leafminer, Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) Argentine Ant, Linepithema humile (Mayr), (Hymenoptera: Formicidae: Dolichoderinae) Army Cutworm, Euxoa auxiliaris (Grote) (Lepidoptera: Noctuidae) Armyworm, Pseudaletia unipuncta (Haworth) (Lepidoptera: Noctuidae) Asian Citrus Psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae) Asparagus Aphid, Brachycorynella asparagi (Mordvilko) (Hemiptera: Aphididae) Aster Leafhopper, Macrosteles quadrilineatus Forbes (Hemiptera: Cicadellidae) Australian Sheep Blowfly, Lucilia cuprina Wiedemann (Diptera: Calliphoridae) Banana Weevil, Cosmopolites sordidus (Germar) (Coleoptera: Curculionidae) Bed Bugs (Hemiptera: Cimicidae: Cimex spp.) Bee Louse, Bee Fly, or Braulid, Braula coeca Nitzsch (Diptera: Braulidae) Beet Armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) Bertha Armyworm, Mamestra configurata Walker (Lepidoptera: Noctuidae) Black Cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae) Black Fig Fly, Silba adipata McAlpine (Diptera: Lonchaeidae) Bogong moth, Agrotis infusa (Boisduval) (Lepidoptera: Noctuidae) Boll Weevil, Anthonomus grandis Boheman (Coleoptera: Curculionidae) Brown Citrus Aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae) Cabbage Aphid, Brevicoryne brassicae (L.) (Hemiptera: Aphididae) Cabbage Maggot or Cabbage Root Fly, Delia radicum (Linnaeus) (Diptera: Anthomyiidae)

Cabbage Looper, Trichoplusia ni (Hübner) (Lepidoptera Noctuidae) Cabbageworm, Pieris rapae (Linnaeus) (Lepidoptera: Pieridae) Cactus Moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) Cape Honey Bees, Apis mellifera capensis Escholtz Cassava Mealybug, Phenacoccus manihoti Matile-Ferrero (Hemiptera: Pseudococcidae) Chilli Thrips, Scirtothrips dorsalis Hood (Thysanoptera: Thripidae) Chinch Bug, Blissus leucopterus (Say) (Hemiptera: Blissidae) Cluster Fly, Pollenia rudis (Fabricius) and P. pseudorudis Rognes (Diptera: Calliphoridae) Coconut Mite, Aceria guerreronis (Acari: Eriophyidae) Coffee Berry Borer, Hypthenemus hampei (Ferrari) (Coleoptera: Curculionidae: Scolytinae) Colorado Potato Beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) Corn Delphacid, Peregrinus maidis (Ashmead) (Hemiptera: Delphacidae) Corn Earworm, Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae) Corn Leaf Aphid, Rhopalosiphum maidis (Fitch) (Hemiptera: Aphididae) Corn Leafhopper, Dalbulus maidis (Delong And Wolcott) (Hemiptera: Cicadellidae) Cotton Leafworm, Spodoptera littoralis (Boisduval) Crapemyrtle Aphid Sarucallis kahawaluokalani (Kirkaldy) (Hemiptera: Aphididae) Date Palm Stem Borer, Pseudophilus testaceus Gah. (= Jebusea hammershmidti Reiche) (Coleoptera: Cerambycidae) Diamondback Moth, Plutella xylostella (Linnaeus) (Lepidoptera: Plutellidae) Diaprepes Root Weevil, Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae)


Differential Grasshopper, Melanoplus differentialis (Thomas) (Orthoptera: Acrididae) Douglas-Fir Beetle, Dendroctonus pseudotsugae pseudotsugae Hopkins (Coleoptera: Curculionidae, Scolytinae) Driver Ants (Dorylus Subgenus Anomma) (Hymenoptera: Formicidae) Dubas Bug (Old World Date Bug), Ommatissus binotatus (Hemiptera: Tropiduchidae) Eastern Lubber Grasshopper, Romalea microptera (Beauvois) (Orthoptera: Acrididae) Elm Leaf Beetle, Xanthogaleruca (= Pyrrhalta) luteola (Müller) (Coleoptera: Chrysomelidae) Eri Silkworm, Philosamia ricini (Lepidoptera: Saturniidae) Eurasian Spruce Bark Beetle, Ips typographus Linnaeus (Coleoptera: Curculionidae, Scolytinae) European Cherry Fruit Fly Rhagoletis cerasi (Linnaeus) (Diptera: Tephritidae) European Corn Borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) European Earwig, Forficula auricularia Linnaeus (Dermaptera: Forficulidae) Face Fly, Musca autumnalis De Geer (Diptera: Muscidae) Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) Formosan Subterranean Termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae) Fruit Stalk Borer, Oryectes elegans Prell (Coleoptera: Scarabaeidae) Gamagrass Leafhopper Dalbulus quinquenotatus Delong & Nault (Hemiptera: Cicadellidae) Glassy-Winged Sharpshooter, Homalodisca vitripennis (Hemiptera: Cicadellidae) Grape Phylloxera, Daktulosphaira vitifoliae (Fitch) (Hemiptera: Aphidoidea: Phylloxeridae) Grapevine Leafhopper Complex (Hemiptera: Cicadellidae) in Cyprus

Greater Date Moth, Arenipses sabella Hmps (Lepidoptera: Pyralidae) Greenhouse Whitefly, Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) Green Peach Aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) Gypsy Moth, Lymantria dispar Linnaeus (Lepidoptera: Lymantriidae) Harlequin Bug, Murgantia histrionica (Hahn) (Hemiptera: Pentatomidae) Hazelnut and Walnut Twig Borer, Oberea linearis Linnaeus (Coleoptera: Cerambycidae) Hessian Fly, Mayetiola destructor (Say) (Diptera: Cecidomyiidae) Honey Bee, Apis mellifera Linnaeus (Hymenoptera: Apidae) Horn Fly, Haematobia irritans (L.) (Diptera: Muscidae) House Fly, Musca domestica L. (Diptera: Muscidae) Human Botfly, Dermatobia hominis (Linneaus, Jr.) (Diptera: Oestridae) Japanese Beetle, Popillia japonica Newman (Coleoptera: Scarabaeidae) Jewel Wasp, Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) Khapra Beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae) Large Milkweed Bug, Oncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae) Large Cabbage White Butterfly, Pieris brassicae (Linnaeus) (Lepidoptera: Pieridae) Larger Grain Borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) Leaf-Cutting Ants (Formicidae: Myrmicinae: Attini) Lesser Date Moth, Batrachedra amydraula Meyrick (Lepidoptera: Cosmopterygidae) Lettuce Root Aphid, Pemphigus bursarius (Linnaeus) (Hemiptera: Aphididae) Locust Borer, Megacyllene robiniae (Forster) (Coleoptera: Cerambycidae)

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Lovebug, Plecia nearctica Hardy (Diptera: Bibionidae) Mango Mealybug, Rastrococcus invadens Williams (Hemiptera: Pseudococcidae) Mediterranean Fruit Fly Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) Melon Aphid, Aphis gossypii Glover (Hemiptera: Aphididae) Melon Fly, Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) Melon Thrips, Thrips palmi Karny (Thysanoptera: Thripidae) Melonworm, Diaphania hyalinata Linnaeus (Lepidoptera: Pyralidae) Mexican Bean Beetle, Epilachna varivestris Mulsant (Coleoptera: Coccinellidae) Migratory Grasshopper, Melanoplus sanguinipes (Fabricius) (Orthoptera: Acrididae) Mole Crickets (Orthoptera: Gryllotalpidae) and Their Biological Control Monarch Butterfly, Danaus plexippus Linnaeus (Lepidoptera: Danaidae) Mormon Cricket, Anabrus simplex Haldeman (Orthoptera: Tettigoniidae) Mountain Pine Beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Curculionidae, Scolytinae) Myndus crudus (Van Duzee) (Hemiptera: Cixiidae) Neotropical Brown Stink Bug, Euschistus heros (Fabricius) (Hemiptera: Pentatomidae) Neotropical Soybean Budborer, Crocidosema aporema (Walsingham) (Lepidoptera: Tortricidae) Northern Corn Rootworm, Diabrotica barberi Smith & Lawrence (Coleoptera: Chrysomelidae) Olive Fruit Curculio, Rhynchites (= Coenorrhinus) cribripennis Desbrochers (Coleoptera: Attelabidae) Olive Fruit Fly, Bactrocera oleae (Rossi) (= Dacus oleae) (Diptera: Tephritidae) Olive Psyllids, Euplyllura spp. (Hemiptera: Psyllidae)

Onion Maggot, Delia antiqua (Meigen) (Diptera: Anthomyiidae) Oriental Fruit Fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) Pea Aphid, Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) Pea Leafminer, Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) Pear Psylla, Cacopsylla pyricola (Foerster) (Hemiptera: Psyllidae) Pepper Weevil, Anthonomus eugenii Cano (Coleoptera: Curculionidae) Phoracantha Longicorn Beetles (Coleoptera: Cerambycidae) Pickleworm, Diaphania nitidalis (Stoll) (Lepidoptera: Pyralidae) Pine Weevil, Hylobius abietis (Coleoptera: Curculionidae) Pink Hibiscus Mealybug, Maconellicoccus hirsutus Green (Hemiptera: Pseudococcidae) Pistachio Seed Wasps, Eurytoma plotnikovi Nikol’skaya (Hymenoptera: Eurytomidae) and Megastigmas pistaciae Walker (Hymenoptera: Torymidae) Potato Aphid, Macrosiphum euphorbiae (Thomas) (Hemiptera: Aphididae) Potato Tuberworm, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae) Plum Curculio, Conotrachelus nenuphar Herbst (Coleoptera: Curculionidae) Pseudo-Curly Top Treehopper, Micrutalis malleifera (Fowler) (Hemiptera: Membracidae) Red Imported Fire Ant, Solenopsis invicta Buren (Hymenoptera: Formicidae) Redlegged Grasshopper, Melanoplus femurrubrum (Degeer) (Orthoptera: Acrididae) Red Palm Weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae) Rhammatocerus schistocercoides Rehn (Orthoptera: Acrididae) Rocky Mountain Wood Tick, Dermacentor andersoni Stiles (Acari: Ixodidae)


Roundheaded Pine Beetle, Dendroctonus adjunctus Blandford (Coleoptera: Curculionidae, Scolytinae) Seedcorn Maggot or Bean Seed Fly, Delia platura (Meigen) (Diptera: Anthomyiidae) Silkworm, Bombyx mori (Linnaeus) (Lepidoptera: Saturniidae) Silverleaf Whitefly, Bemisia argentifolii Bellows and Perring (Hemiptera: Aleyrodidae) Small Green Stink Bug, Piezodorus guildinii (Westwood) (Hemiptera: Heteroptera: Pentatomidae) Small Hive Beetle, Aethina tumida Murray (Nitidulidae: Coleoptera) Small Honey Ant, Prenolepis imparis (Say) (Hymenoptera: Formicidae) Small Rice Stink Bug, Oebalus poecilus (Dallas) (Hemiptera: Heteroptera: Pentatomidae) Southern Green Stink Bug, Nezara viridula (L.) (Hemiptera: Heteroptera: Pentatomidae) Soybean Aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) Spined Soldier Bug, Podisus maculiventris (Say) (Hemiptera: Pentatomidae) Spotted Cucumber Beetle or Southern Corn Rootworm, Diabrotica undecimpunctata Mannerheim (Coleoptera: Chrysomelidae) Spruce Budworms, Choristoneura Lederer (Lepidoptera: Tortricidae) Squash Bug, Anasa tristis (DeGeer) (Hemiptera: Coreidae) Squash Vine Borer, Melittia cucurbitae (Harris) (Lepidoptera: Sesiidaae) Stable Fly, Stomoxys calcitrans (Linnaeus) (Diptera: Muscidae) Sweetpotato and Silverleaf Whiteflies, Bemisia spp. (Hemiptera: Aleyrodidae) Sweetpotato Flea Beetle, Chaetocnema confinis Crotch (Coleoptera: Chrysomelidae Alticinae) Sweetpotato Weevil, Cylas formicarius (Fabricius) (Coleoptera: Brentidae) Taiga Tick, Ixodes persulcatus Schulze (Acari: Ixodida: Ixodidae)

Tarnished Plant Bug, Lygus lineolaris Palisot de Beauvois (Hemiptera: Miridae) Taro Caterpillar or Rice Cutworm, Spodoptera litura (Fabricius) Tent Caterpillars, Malacosoma spp. (Lepidoptera: Lasiocampidae) Termites (Isoptera) in South America Timarcha Latreille (Coleoptera: Chrysomelidae, Chrysomelinae) Tomato Hornworm, Manduca quinquemaculata (Haworth) and Tobacco Hornworm, Manduca sexta (Linnaeus) (Lepidoptera: Sphingidae) Tracheal Mite, Acarapis woodi Rennie (Acarina: Tarsonemidae) Tsetse Flies, Glossina spp. (Diptera: Glossinidae) Turnip Aphid, Lipaphis erysimi (Kaltenbach) (Hemiptera: Aphididae) Turnip Root Maggot, Delia floralis (Fallen) (Diptera: Anthomyiidae) Twospotted Spider Mite, Tetranychus urticae Koch (Acari: Tetranychidae) Two-Spotted Stink Bug, Perillus bioculatus (Fabricius) (Hemiptera: Pentatomidae) Twostriped Grasshopper, Melanoplus bivittatus (Say) (Orthoptera: Acrididae) Varroa Mite, Varroa destructor Anderson & Truemann (Acari: Varroidae) Variegated Cutworm, Peridroma saucia (Hübner) (Lepidoptera: Noctuidae) Vegetable Leafminer, Liriomyza sativae Blanchard (Diptera: Agromyzidae) Viburnum Leaf Beetle, Pyrrhalta viburni (Paykull) (Coleoptera: Chrysomelidae) Vine Mealybug, Planococcus ficus Signoret (Hemiptera: Pseudococcidae) Western Balsam Bark Beetle, Dryocoetes confusus Swain (Coleoptera: Curculionidae, Scolytinae) Western Corn Rootworm, Diabrotica virgifera virgifera Leconte (Coleoptera: Chrysomelidae) Western Grapeleaf Skeletonizer, Harrisina brillians Barnes & McDunnough (Lepidoptera: Zyganeidae)

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Western Harvester Ant, Pogonomyrmex occidentalis (Cresson) (Hymenoptera: Formicidae) Western Thatching Ant, Formica obscuripes (Forel) (Hymenoptera: Formicidae) Wheat Stem Sawflies: Cephus cinctus Norton, Cephus pygmaeus (L.) and Trachelus tabidus (F.) (Hymenoptera: Cephidae) White Grubs, Phyllophaga, and Others (Coleoptera: Scarabaeidae)

Winter Moth, Operophtera brumata (L.) (Lepidoptera: Geometridae) and Its Biological Control Wireworms, Several Genera and Species (Coleoptera: Elateridae) Yellowstriped Armyworm, Spodoptera ornithogalli (Guenée) (Lepidoptera: Noctuidae)

List of Contributors Abivardi, Cyrus Institute of Integrative Biology ETH Zurich Universtät-Str.16 (CHN) CH-8092 Zurich Switzerland Abou-Fakhr, Efat M. Department of Plant Sciences Faculty of Agricultural and Food Sciences American University of Beirut P.O. Box 11-0236 Bliss Street Beirut Lebanon Adams, Byron J. Department of Microbiology and Molecular Biology Brigham Young University Provo, Utah 84602 USA Adler, Peter Department of Entomology Clemson University Box 340365 114 Long Hall Clemson, South Carolina 29634-0365 USA Agnello, Arthur M. Department of Entomology New York State Agricultural Experiment Station Cornell University Geneva, New York 14456-0462 USA Agrios, George Plant Pathology Department University of Florida

Gainesville, Florida 32611-0680 USA Ajjan, Iskandar University of Tishreen P.O. Box 740 Latakia Syria Ajlan, Aziz Department of Plant Protection College of Agricultural and Food Sciences King Faisal University P.O. Box 55009 Hofuf, Al-Hasa 31982 Saudi Arabia Albajes, Ramon Universitat de Lleida Centre UdL-IRTA Rovira Roure 177 25199 Lleida Catalonia Spain Alborn, Hans USDA, Agricultural Research Service Chemistry Research Unit 1600-1700 SW 23rd Drive Gainesville, FL, 32608 USA Aldryhim, Yousif P.O. Box 2460 Riyadh, 1141 Saudi Arabia Alekseev, Andrey N. Russian Parasitological Society P.O. Box 738

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List of Contributors

191186 St. Petersburg, D-186 Russia All, John Department of Entomology University of Georgia 413 Biological Sciences Building Athens, Georgia 30602 USA Alomar, Òscar IRTA Centre de Cabrils Carretera de Cabrils s/n 08348 Cabrils Barcelona, Catalonia Spain Alvarez, Juan M. Aberdeen Research and Education Center University of Idaho P.O. Box 870 Aberdeen, Idaho 83210-0870 USA Amalin, Divina M. USDA-APHIS 13601 Old Cutler Road Miami, Florida 33158 USA

Arif, Basil Great Lakes Forestry Center 1219 Queen Street East Sault Ste. Marie, Ontario P6A 5M7 Canada Armstrong, Earlene Department of Entomology University of Maryland 4122 Plant Sciences Building College Park, Maryland 20742 USA Arthurs, Steven Department of Entomology Biological Control Laboratory Texas A&M University College Station, Texas 77843-2475 USA Asaro, Christopher Department of Entomology University of Georgia 413 Biological Sciences Building Athens, Georgia 30602-2603 USA Attathom, Tipvadee Department of Entomology Kasetsart University Kamphaengsaen Campus Nakhon Pathom, 73140 Thailand

Amerasinghe, Felix P. International Management Institute 127 Sunil Mawatha, Pelawatta Battaramulla, 10120 Sri Lanka

Baldwin, Rebecca W. Entomology and Nematology Department P.O. Box 110620 University of Florida Gainesville, Florida, 32611 USA

Anderson, Robert Canadian Museum of Nature P.O. Box 3443, Station D Ottawa, Ontario K1P 6P4 Canada

Barbara, Kathryn A. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA


Barfield, Carl Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA

Behmer, Spencer T. Department of Entomology Texas A&M University College Station, Texas 77843-2475 USA

Barrera, Juan F. Departamento de Entomología Tropical El Colegio de la Frontera Sur Tapachula, Chiapas, 30700 México

Bellotti, Anthony C. CIAT - Centro Internacional de Agricultura Tropical Apartado Aéreo 6713, Cali Colombia

Barth, Martin Friedrich-Miescher-Laboratorium der Max-Planck-Gesellschaft Spemannstr. 39 720726 Tübingen Germany Baumgärtner, Johann International Centre of Insect Physiology and Ecology (ICIPE) P.O. Box 17319 Addis Ababa Ethiopia Baz, Arturo Universidad de Alcala Department Biologia Animal Alcala de Henares Madrid, E-28801 Spain Becnel, James J. Center for Medical, Agricultural and Veterinary Entomology USDA-ARS Gainesville, Florida 32611-0970 USA Beeman, Richard W. USDA-ARS GMPRC 1515 College Avenue Manhattan, Kansas USA

Beard, Charles E. Box 340315 - 114 Long Hall Entomology, Soils and Plant Sciences Clemson University Clemson, South Carolina 29634-0315 USA Bennett, Gary W. Center for Urban and Industrial Management Department of Entomology Purdue University 1158 Smith Hall West Lafayette, Indiana 47907-1158 USA Bentz, Barbara J. Rocky Mountain Research Station Forestry Sciences Lab 860 N 1200 E Logan, Utah 84321 USA Berisford, C. Wayne Department of Entomology University of Georgia 413 Biological Sciences Building Athens, Georgia 30602 USA Berlinger, Menachem J. Entomology Laboratory Agricultural Research Organization Gilat Regional Experiment Station

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P.O. Box 7710 Be’er-Sheva, 84843 Israel Bernays, Elizabeth A. Department of Entomology University of Arizona P.O. Box 2100 Tucson, Arizona 85721-0036 USA Berry, Colin Cardiff School of Biosciences Cardiff University P.O. Box 911 Museum Avenue Cardiff, Wales CF10 3US UK Bidochka, Michael Department of Biological Sciences Brock University St. Catharine’s, Ontario Canada Blackwell, Alison Center for Tropical Veterinary Medicine University of Edinburgh Easter Bush Veterinary Centre Roslin, Midlothian EH25 9RG UK Blum, Murray S. Department of Entomology University of Georgia 413 Biological Sciences Building Athens, Georgia 30602 USA Boevé, Jean-Luc Département d’Entomologie IRSNB-KBIN Royal Belgian Institute of Natural Sciences Rue Vautier 29

B-1000 Bruxelles Belgium Borgemeister, Christian Institute of Plant Diseases and Plant Protection University of Hannover Herrenheuser Str. 2 30419 Hannover Germany Bostanian, Noubar J. Horiticultural Research and Development Centre Agriculture and Agri-Food Canada 430, Boulevard Gouin St.-Jean-sur-Richelieu, Quebec J3B 3E6 Canada Boucher, Stéphanie Lyman Entomological Museum McGill University, Macdonald Campus Ste-Anne-de-Bellevue, Québec H9X 3V9 Canada Boucias, Drion Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Bowles, David E. Resource Protection Division Freshwater Conservation Branch/River Studies Program Texas Parks and Wildlife Department P.O. Box 1685 San Marcos, Texas 78666 USA Brambila, Julieta Florida Department of Agriculture and Consumer Services Division of Plant Industry


1911 SW 34th Street Gainesville, Florida 32614 USA Brandenburg, Rick Department of Entomology North Carolina State University P.O. Box 7613 Raleigh, North Carolina 27695-7613 USA Brault, Aaron C. Centers for Disease Control and Prevention National Center for Infectious Diseases Division of Vector-Borne Infectious Diseases P.O. Box 2087 Foothills Campus Fort Collins, Colorado 80522 USA Brewer, J. Wayne Department of Entomology Auburn University 301 Funchess Hall Auburn University, Alabama 36849-5413 USA Brown, Harley P. Department of Zoology University of Oklahoma 730 Van Vleet Oval, Room 314 Norman, Oklahoma 73019-6121 USA Brown, Susan J. Division of Biology Kansas State University 9 Anderson Hall Manhattan, Kansas 66506 USA Broza, Meir University of Haifa Oranim, Tivon 36006 Israel

Burden, Beverly Department of Biological Sciences Louisiana State University - Shreveport One University Place Shreveport, Louisiana 71115 USA Buss, Eileen A. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Byers, George W. Snow Entomological Division Natural History Museum University of Kansas 1460 Jayhawk Boulevard Lawrence, Kansas 66045-7523 USA Cabana, Jean AFA Environment Inc. 1100, Rene-Levesque Boulevard West 25th Floor Montreal, Quebec H3B 5C9 Canada Caceres, Carlos FAO/IAEA Agricultural and Biotechnology Laboratory A-2444 Seibersdorf Austria Calabrese, Diane M. 1000 Robin Road Silver Spring, Maryland 20901-1873 USA Cane, James H. USDA-ARS Bee Biology and Systematics Laboratory Utah State University

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5310 Old Main Hill Logan, Utah 84322-5310 USA Capinera, John L. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Cardwell, Kitty F. USDA/CSREES Washington, D.C. USA Cave, Ronald D. Entomology and Nematology Department University of Florida Indian River Research and Education Center Ft. Pierce, Florida 34945-3138 USA Cédola, Claudia V. CEPAVE Universidad Nacional de La Plata Consejo Nacional de Investigaciones Científicas y Técnicas 2 No 584 (1900) La Plata Argentina Chapman, Reg Arizona Research Laboratories Division of Neurobiology University of Arizona P.O. Box 210077 Tuscon, Arizona 85721-0077 USA Cheng, Lanna Scripps Institution of Oceanography University of California, San Diego 9500 Gilman Drive LaJolla, California 92093-0202 USA

Cherry, Ron Everglades Research and Education Center University of Florida 3200 E. Palm Beach Road Belle Glade, Florida 33430 USA Chiappini, Elisabetta Istituto di Entomologia e Patologia Vegetale Facoltà di Agraria Università Cattolica del Sacro Cuore Via Emilia Parmense, 84 Piacenza, 29100 Italy Choate, Paul M. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Chouinard, Gérald Institut de Recherche et de Développement en Agroenvironnement 3300 Sicotte Saint-Hyacinthe, Quebec J2S 7B8 Canada Chow, Yien-Shing National Museum of Natural Science 1, Kuan Chien Road Taichung 404, Taiwan Republic of China Christian, Peter National Institute for Biological Standards and Control Potters Bar, Hertfordshire UK Cilek, James E. Biting Fly and Tick Control Section John A. Mulrennan, Sr. Public Health Entomology Research and Education Center


Florida A&M University 4000 Frankford Avenue Panama City, Florida 32405-1933 USA Clement, Stephen L. USDA-ARS Western Regional Plant Introduction Station Washington State University 59 Johnson Hall P.O. Box 646402 Pullman, Washington 99164-6402 USA Collier, Rosemary H. Horticulture Research International Wellesbourne, Warwick CV35 9EF UK Conlong, Des E. SASA Experiment Station Private Bag X02 Mount Edgecombe Kwa Zulu-Natal, 4300 South Africa Constantino, Reginaldo Depto de Zoologia Universidade de Brasília 70910-900 Brasília, DF Brazil Coons, Lewis B. Integrated Microscopy Center University of Memphis 201 Life Sciences Building Rooms LS 101-113 Memphis, Tennessee 38152-6040 USA Costas, MIguel Facultad de Biología Universidad Complutense de Madrid 28040 Madrid Spain

Cranshaw, Whitney Department of Bioagricultural Sciences and Pest Management Colorado State University Fort Collins, Colorado 80523-0001 USA Cresswell, James School of Biological Sciences University of Exeter Hather Laboratories Prince of Wales Road Exeter, EX4 4PS UK Crist, Thomas O. Department of Zoology Miami University Pearson Hall Room 212 Oxford, Ohio 45056-1400 USA Crooker, Allen Biology Department Hartwick College Oneonta, New York 13820 USA Cuda, James P. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Cumming, Jeffrey M. Canadian National Collection of Insects Arachnids and Nematodes Agriculture and Agri-Food Canada K.W. Neatby Building, C.E.F. Ottawa, Ontario K1A 0C6 Canada Cushing, Paula E. Department of Zoology Denver Museum of Nature and Science

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2001 Colorado Boulevard Denver, Colorado 80205-5798 USA Cusson, Michel Natural Resources Canada Canadian Forest Service 1055 rue du P.E.P.S. P.O. Box 3800 Sainte-Foy, Quebec G1V 4C7 Canada Czél, Gyozo Hungarian Natural History Museum Budapest Hungary Daane, Kent M. Division of Insect Biology ESPM University of California Berkeley, California 94720 USA Dam, Nicole M. van Netherlands Institute of Ecology Centre for Terrestrial Ecology P.O. Box 40 6666 ZG Heteren The Netherlands Dame, David Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Daniels, Jaret C. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA

Danoff-Burg, James A. Department of Ecology, Evolution and Environmental Biology Columbia University 1020 Schermerhorn Extension, MC5557 1200 Amsterdam Avenue New York, New York 10027 USA Davidson, Diane W. Department of Biological Sciences University of Utah 257 South, 1400 East Salt Lake City, Utah 84112-0840 USA DeClercq, Patrick Laboratory of Agrozoology, Department of Crop Protection Faculty of Agricultural and Applied Biological Sciences Ghent University Coupure Links 653 B-9000 Ghent Belgium Denell, Robin E. Division of Biology Kansas State University 9 Anderson Hall Manhattan, Kansas 66506 USA Denmark, Harold A. Florida Department of Agriculture and Consumer Services Division of Plant Industry 1911 SW 34th Street Gainesville, Florida 32614 USA Devorshak, Christina USDA-APHIS-PPQ Center for Plant Health Science and Technology


Plant Epidemiology and Risk Analysis Laboratory Raleigh, North Carolina USA

1200 University Street Spearfish, South Dakota 57799-9003 USA

Dicke, Marcel Laboratory of Entomology Wageningen University P.O. Box 8031 6700EH Wageningen The Netherlands

Dunford, James, C. Department of Entomology and Nematology University of Florida Gainesville, Florida, 32611 USA

Dietrich, C.H. Center for Biodiversity Illinois Natural History Survey 607 East Peabody Drive Champaign, Illinois 61820 USA

Dyby, Susanne D. Res. Le Rambouillet Bat. B 1 Allée des Lucioles Beaulieu-sur-Mer, 06310 France

Dorchin, Netta Museum Koenig Adenauerallee 160 53113 Bonn Germany Downer, R.A. Laboratory for Pest Control Application Technology Ohio Agricultural Research and Development Center Ohio State University 1680 Madison Avenue Wooster, Ohio 44691-4096 USA Downie, D.A. Department of Zoology and Entomology Rhodes University Grahamstown 6140 South Africa Downing, Holly Unit 9003 College of Arts and Sciences Black Hills State University

Easton, Emmett Department of Plant and Environmental Protection Sciences University of Hawaii at Manoa 3050 Maile Way Gilmore Hall 310 Honolulu, Hawaii 96822-2271 USA Ebert, Timothy A. Laboratory for Pest Control Application Technology Ohio Agricultural Research and Development Center Ohio State University 1680 Madison Avenue Wooster, Ohio 44691-4096 USA Edmunds, Malcolm Department of Environmental Management University of Central Lancashire Preston, PR1 2HE UK

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Ellis, Amanda Florida Department of Agriculture and Consumer Services Division of Plant Industry P.O. Box 147100 Gainesville, Florida 32614-7100 USA Ellis, James D. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Emmel, Thomas C. McGuire Center for Lepidoptera Research and Conservation University of Florida Gainesville, Florida 32611-0620 USA Epsky, Nancy D. USDA/ARS Subtropical Horticulture Research Station 13601 Old Cutler Road Miami, Florida 33158 USA Farag, Mohamed A. Department of Chemistry and Biochemistry Texas Tech University Lubbock, Texas 79409-1061 USA Fasulo, Thomas R. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Feir, Dorothy Biology Department St. Louis University St. Louis, Missouri 63103 USA

Felicioli, Antonio Universita’ degli Studi di Pisa Dipartimento di Anatomia, Biochimica e Fisiologia veterinaria Viale delle Piagge n° 2, 56100 Pisa Italy Feng, Qili Great Lakes Forestry Center 1219 Queen Street East Sault Ste. Marie, Ontario P6A 5M7 Canada Finch, Stan Horticulture Research International Wellesbourne, Warwick CV35 9EF UK Finke, Mark D. 6811 Horned Owl Trail Scottsdale, Arizona 85262-8519 USA Fishel, Fred University of Florida, Pesticide Information Office PO Box 110710 Gainesville, Florida 32611-0710 USA Fitzgerald, T.D. Department of Biology State University of New York at Cortland Cortland, New York 13045 USA Floate, Kevin D. Agriculture and Agri-Food Canada Lethbridge Research Centre 5403 1st Avenue P.O. Box 3000 Lethbridge, Alberta T1J 4B1 Canada


Flowers, R. Wills Center for Biological Control/Entomology Division of Agricultural Sciences Florida A&M University Tallahassee, Florida 32307 USA Fornasari, Luca Clas de l’Ermitage 636, ave. E. Jeanbrau 34090 Montpellier France Frank, J. Howard Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Franz, Gerald FAO/IAEA Agricultural and Biotechnology Laboratory A-2444 Seibersdorf Austria Froeba, Jason G. Entomology and Nematology Department University of Florida Gainesville, FL 32611-0620 USA Gabrys, Beata Institute of Biotechnology and Environmental Sciences University of Zielona Gora Monte Cassino 21b 65-561 Zielona Gora Poland Gäde, Gerd Zoology Department University of Cape Town Private Bag

Rondebosch 7700 Cape Town Republic of South Africa Galante, Eduardo CIBIO University of Alicante 03080 San Vicente del Raspeig Alicante Spain Gall, Lawrence F. Peabody Museum of Natural History Yale University P.O. Box 208118 New Haven, Connecticut 06520-8118 USA Gangwere, Stan K. Department of Biological Sciences Wayne State University Detroit, Michigan 48202 USA Garcia, Lloyd North Carolina Department of Agriculture and Consumer Sciences Plant Industry Division P.O. Box 27647 Raleigh, North Carolina 27611 USA Gayubo, Severiano F. Area de Zoología Facultad de Biología Universidad de Salamanca 37071 Salamanca Spain Gerberg, Eugene J. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA

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Gerlach, Günter Botanischer Garten München - Nymphenburg Menzinger Str. 65 80638 München Germany Gerling, Dan Department of Zoology Tel Aviv University Ramat Aviv, 69978 Israel Ghiradella, Helen Department of Biology State University of New York at Albany Albany, New York 12222 USA Giberson, Donna Department of Biology University of Prince Edward Island 550 University Ave. Charlottetown, PEI C1A 4P3 Canada Giblin-Davis, Robin M. Fort Lauderdale Research and Education Center University of Florida 3205 College Avenue Davie, Florida 33314-7719 USA Gibson, G.A.P. Agriculture and Agri-Food Canada 960 Carling Avenue Ottawa, Ontario K1A 0C6 Canada Glenn, D. Michael USDA-ARS, Appalachian Fruit Research Station 2217 Wiltshire Rd. Kearneysville, WV 25430 USA

Goebel, Régis SASEX-CIRAD Entomology Department Private Bag X02 Mount Edgecombe, 4300 South Africa Goettel, Mark Lethbridge Research Centre Agriculture and Agri-Food Canada 5403 1st Avenue South P.O. Box 3000 Lethbridge, Alberta T1J 4B1 Canada Gold, Clifford S. CIAT (International Center for Tropical Agriculture) P.O. Box 6247 Kampala Uganda Goodman, Katie Department of Biological Sciences Western Illinois University Macomb, Illinois 61455 USA Goula, Marta University of Barcelona Barcelona Spain Greco, Nancy M. CEPAVE Universidad Nacional de La Plata Consejo Nacional de Investigaciones Científicas y Técnicas 2 No 584 (1900) La Plata Argentina Grewal, Parwinder S. Department of Entomology The Ohio State University


Columbus, Ohio 43210 USA Gruner, Susan V. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Guertin, Claude INRS Institut Armand-Frappier 531 Boulevard des Prairies Laval, Quebec H7V 1B7 Canada Gupta, Virendra K. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Gwynne, Darryl T. University of Toronto at Mississauga Mississauga, Ontario L5L 1C6 Canada Habeck, Dale Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Hahn, Daniel A. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Halbert, Susan Florida Department of Agriculture and Consumer Services Division of Plant Industry 1911 SW 34th Street Gainesville, Florida 32614 USA

Hall, Donald W. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Hall, Jason P.W. National Museum of Natural History Smithsonian Institution Washington, D.C. 20560-0127 USA Hall, Robert D. Office of Research University of Missouri 205 Jesse Hall Columbia, Missouri 65211 USA Handler, Alfred M. Center for Medical, Agricultural and Veterinary Entomology USDA-ARS P.O. Box 14565 1700 SW 23rd Drive Gainesville, Florida 32608 USA Hangay, George 80 Gondola Road Narrabeen, New South Wales 2101 Australia Hansen, Laurel D. Department of Biology Spokane Falls Community College 3410 W. Fort George Wright Dr. Spokane, WA 99224-5288 USA Harman, Dan M. University of Maryland Center for Environmental Science

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Appalachian Laboratory Frostburg, Maryland 21532-2307 USA Haunerland, Norbert H. Department of Biological Sciences Simon Fraser University Burnaby, British Columbia V5A 1S6 Canada Headings, Mark Agricultural Technical Institute Ohio State University 1328 Dover Road Wooster, Ohio 44691-8905 USA Heath, Allen AgResearch Wallaceville Wallaceville Animal Research Centre PO Box 40063, Upper Hutt, 5140 New Zealand Held, David W. Entomology Department University of Kentucky S-225 Agricultural Science Center Building North Lexington, Kentucky 40546-0091 USA Henneman, M.L. Department of Biological Sciences University of Bristol Bristol, BS8 1TH UK Heppner, John B. Florida State Collection of Arthropods Florida Department of Agriculture and Consumer Services Division of Plant Industry P.O. Box 147100 Gainesville, Florida 32614-7100 USA

Hernandez, Santiago Universities of Cordoba and Extremadura Cáceres, 10071 Spain Hilje, Luko Plant Protection Unit 7170 CATIE Turrialba, Cost Rica Hinkle, Nancy C. Department of Entomology University of Georgia 413 Biological Sciences Building Athens, Georgia 30602 USA Hirsch, Helmut V.B. Department of Biology State University of New York at Albany 1400 Washington Avenue Albany, New York 12222 USA Ho, Chyi-Chen Taiwan Agricultural Research Institute Department of Applied Zoology Wufeng Taichung, Taiwan Republic of China Hodges, Greg S. Florida Department of Agriculture and Consumer Services Division of Plant Industry 1911 SW 34th Street Gainesville, Florida 32614 USA Horton, David R. USDA/ARS 5230 Konnowac Pass Road Wapato, Washington 98951 USA


Hou, Roger F. Department of Entomology National Chung Hsing University Taichung 402, Taiwan Republic of China Howard, Forrest W. Fort Lauderdale Research and Education Center University of Florida Ft. Lauderdale, Florida 33314-7719 USA Hoy, Marjorie A. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Huber, John Canadian Forestry Service 960 Carling Avenue Ottawa, Ontario K1A 0C6 Canada Hunter, Fiona F. Department of Biological Sciences Brock University St. Catharine’s, Ontario L2S 3A1 Canada Hurd, Hilary Keele University School of Life Sciences Keele, Staffordshire ST55BG UK Hurd, Lawrence E. Department of Biology Washington & Lee University Lexington, Virginia 24450 USA Ioffe-Uspensky, Inna Department of Parasitology The Hebrew University of Jerusalem

Hadassah Medical School Jerusalem Israel Isman, Murray B. Faculty of Agricultural Sciences University of British Columbia 248-2357 Main Mall Vancouver, British Columbia V6T 1Z4 Canada James, Rosalind R. USDA/ARS, Bee Biology and Systematics Laboratory Department of Biology, UMC 5310 Utah State University 5310 Old Main Hill Logan, Utah 84321-5310 USA Jaffe, Klaus Universidad Simón Bolívar Apartado 89000, Caracas 1080 Venezuela Jeremías, Xavier Museum of Natural Sciences C./ Catalunya 28 08758 Cervelló (prov. Barcelona) Spain Jolivet, Pierre 67, Bd Soult 75012 Paris France Juárez, M. Patricia Facultad de Ciencias Médicas Universidad Nacional de la Plata Calle 60 y 120 C.C. 455 La Plata, 1900 Argentina

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Kabissa, Joe C.B. Tanzania Cotton Lint and Seed Board Pamba House Garden Avenue P.O. Box 9161 Dar Es Salaam Tanzania Kalkar, Ö. Department of Entomology Clemson University Clemson, South Carolina USA Katsoyannos, Byron Aristotle University of Thessaloniki Department of Agriculture Laboratory of Applied Zoology and Parasitology Thessaloniki, 541 24 Greece Kathirithamby, Jeyaraney Department of Zoology Oxford University South Parks Road Oxford OX1 3PS, UK Keeley, Larry L. Department of Entomology Texas A&M University 2475 TAMU College Station, Texas 77843-2475 USA Kerr, Peter H. California Department of Food and Agriculture Plant Pest Diagnostics Branch 3294 Meadowview Rd. Sacramento, California 95832 USA Kfir, Rami ARC-Plant Protection Research Institute Rietondale Research Station 600 Soutpansberg Road

Private Bag X134 Pretoria, 0001 South Africa Khan, Zeyour R. ICIPE P.O.B. 30772 Nairobi Kenya Kima, Peter E. Microbiology and Cell Science Department University of Florida Building 981, Box 110700 Gainesville, Florida 32611-0700 USA Klassen, Waldemar Tropical Research and Education Center University of Florida 18905 SW 280th Street Homestead, Florida 33031-3314 USA Klotz, John H. Department of Entomology University of California Riverside, California USA Klowden, Marc J. Division of Entomology University of Idaho Moscow, Idaho 83844-2339 USA Koehler, Philip G. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0602 USA Kok, L.T. Department of Entomology College of Agriculture and Life Sciences Virginia Polytechnic Institute and State University


216 Price Hall Blacksburg, Virginia 24061-0319 USA Kondratieff, Boris C. Department of Bioagricultural Sciences and Pest Management Colorado State University Fort Collins, Colorado 80523 USA Kouloussis, Nikos A. Aristotle University of Thessaloniki Laboratory of Applied Zoology and Parasitology Thessaloniki, 541 24 Greece Krafsur, Elliot S. 206 Hidden Valley Circle Shepherdstown, West Virginia 25443 USA Lacey, Lawrence A. USDA-ARS Yakima Agricultural Research Lab 5230 Konnowac Pass Road Wapato, Washington 98951 USA Lambdin, Paris L. Department of Entomology and Plant Pathology University of Tennessee 2431 Center Drive 205 Ellington Plant Sciences Building Knoxville, Tennessee 37996-4560 USA Lapointe, Stephen L. USDA-ARS, U.S. Horticultural Research Lab 2001 South Rock Road Fort Pierce, Florida 34945 USA Landis, Douglas A. Department of Entomology Center for Integrated Plant Systems

Michigan State University 204 Center for Integrated Plant Systems East Lansing, Michigan 48824-1311 USA Lawrence, Pauline O. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Leather, Simon R. Division of Biology Imperial College London Silwood Park Campus Ascot, SL5 7PY UK Lebiush-Mordechi, Sarah Entomology Laboratory Agricultural Research Organization Gilat Regional Experiment Station P.O. Box 7710 Be’er-Sheva, 84843 Israel Lecoq, Michel Centre de Coopération Internationale en Recherche Agronomique pour le Développement Prifas TA 40/D 34398 Montpellier, Cedex 5 France Lee, Clarence M. Department of Biology Howard University 415 College Street N.W. Washington, D.C. 20059 USA Lee, How-Jing Department of Entomology National Taiwan University Taipei 106, Taiwan Republic of China

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Legaspi, Benjamin C., Jr. USDA-ARS, FAMU-Center for Biological Control 6383 Mahan Drive Tallahassee, Florida 32308 USA Legaspi, Jesusa C. USDA-ARS, FAMU-Center for Biological Control 6383 Mahan Drive Tallahassee Florida 32308 USA Legg, David Department of Renewable Resources College of Agriculture University of Wyoming P.O. Box 3354 Laramie, Wyoming 82071 USA Leppla, Norman C. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Leskey, Tracy USDA-ARS Appalachian Fruit Research Station 45 Wiltshire Road Kearneysville, West Virginia 25430 USA Liburd, Oscar Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Liebman, Matt Department of Agronomy Iowa State University Ames, Iowa 50011-1010 USA

Lloyd, James E. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Long, Lewis S. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Lord, Cynthia C. Florida Medical Entomology Laboratory University of Florida 200 9th Street S.E. Vero Beach, Florida 32962-4699 USA Lord, Jeffrey USDA-ARS Northern Plains Area Grain Marketing and Production Research Center Biological Research Unit 1515 College Avenue Manhattan, Kansas 66502-2796 USA Lounibos, L. Philip Florida Medical Entomology Laboratory University of Florida 200 9th Street S.E. Vero Beach, Florida 32962-4699 USA Luna, María G. Department of Ecology and Evolutionary Biology University of California at Irvine 321 Steinhaus Hall Irvine, California 92697-2525 USA Lysyk, Tim Laboratory of Vector Ecology Agriculture and Agri-Food Canada


P.O. Box 3000 5403 1st Avenue South Lethbridge, Alberta T1J 4B1 Canada

1600/1700 SW 23rd Drive P.O. Box 14565 Gainesville, Florida 32604 USA

MacVean, Charles Instituto de Investigaciones Universidad del Valle de Guatemala Aptdo. Postal 82 Guatemala City Guatemala

Manley, Donald G. PeeDee Research and Education Center Clemson University 2200 Pocket Road Florence, South Carolina 29506-9706 USA

Magalhães, Bonifácio EMBRAPA Recursos Genéticos e Biotecnologia Parque Estação Biológica Final WS Norte CEP 70770-900 Brasilia-DF Brazil

Mapes, Carol C. Biology Department Kutztown University Kutztown, Pennsylvania 19530 USA

Maimala, S. Department of Agriculture Ministry of Agriculture and Cooperation Chatuchak, Bangkok Thailand Marshall, David Ecology and Evolutionary Biology University of Connecticut 75 N. Eagleville Rd., U-3043 Storrs, Connecticut 06269 USA Malakar-Kuenen, Raksha Division of Insect Biology ESPM University of California Berkeley, California 94720 USA Mankin, Richard USDA/ARS Center for Medical, Agricultural and Veterinary Entomology

Marcos-Garcia, Maria Angeles CIBIO University of Alicante 03080 San Vicente del Raspeig Alicante Spain Martínez, Javier Universities of Cordoba and Extremadura Cáceres, 10071 Spain Martínez, Maricela Instituto Mexicano de Tecnología del Agua (IMTA) Paseo Cuaunhahuac 8532 Progreso Jiutepec, Morelos Mexico Mason, Peter G. Eastern Cereal and Oilseed Research Centre Agriculture and Agri-Food Canada 960 Carling Avenue Ottawa, Ontario K1A 0C6 Canada

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Matthews, Deborah L. Department of Entomology and Nematology University of Florida Gainesville, Florida 32611 USA Matsumoto, Yoshiharu University of Tokyo Tokyo Japan Matthiessen, John N. CSIRO Entomology Underwood Avenue Floreat, Western Australia 6014 Australia McAuslane, Heather J. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA McCravy, Kenneth W. Department of Biological Sciences Western Illinois University 1 University Circle Macomb, Illinois 61455 USA McFadyen, Rachel CRC Australian Weed Management Natural Resource Sciences Meiers Road Indooroopilly, Queensland Australia McIver, James Forestry and Range Sciences Laboratory Pacific Northwest Research Station USDA Forest Service 1404 Gekeler lane LaGrande, Oregon 97850 USA

McSorley, Robert Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Meagher, Robert USDA-ARS Center for Medical and Veterinary Entomology 1700 SW 23rd Drive Gainesville, Florida 32608-1069 USA Medal, Julio Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Meinke, Lance J. Department of Entomology University of Nebraska Lincoln, Nebraska 68583-0816 USA Meinking, Terri L. Department of Dermatology University of Miami School of Medicine 1600 NW 10 Avenue P.O. Box 016960 (R-117) Miami, Florida 33101 USA Menalled, Fabián D. Department of Agronomy Iowa State University Agronomy Hall Ames, Iowa 50011-1010 USA Merkl, Ottó Hungarian Natural History Museum H-1088 Budapest Baross utca, 13 Hungary


Meyer, Jason Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Meyerdirk, Dale E. USDA APHIS, PPQ National Biological Control Institute 4700 River Road Unit 135 Riverdale, Maryland 20737-1228 USA Miller, Barry R. Centers for Disease Control and Prevention National Center for Infectious Diseases Division of Vector-Borne Infectious Diseases P.O. Box 2087 Foothills Campus Fort Collins, Colorado 80522 USA Miller, Dini M. Department of Entomology Virginia Tech University, 216A Price Hall Blacksburg, Virginia 24061 USA Miller, Laura T. West Virginia Department of Agriculture Plant Industries Division 1900 Kanawha Boulevard, East Charleston, West Virginia 25305-0191 USA Mitcham, Elizabeth Department of Plant Sciences, Mail Stop 2 University of California One Shields Avenue Davis, California 95616 USA Mitsuhashi, Jun Department of Bioscience Tokyo University of Agriculture

Sakuragaoka 1-1-1 Setagaya-ku Tokyo, 156-8502 Japan Mizell, Patricia A. North Florida Research and Education Center University of Florida 155 Research Road Quincy, Florida 32351 USA Mizell, Russell F., III North Florida Research and Education Center University of Florida 155 Research Road Quincy, Florida 32351 USA Moriya, Seiichi Insect Ecology Laboratory National Agricultural Research Center 3-1-1, Kannondai Tsukuba, Ibaraki 305-8666 Japan Morrill, Wendell L. Department of Entomology Montana State University Bozeman, Montana 59717-0001 USA Moya-Raygoza, Gustavo Universidad de Guadalajara Departamento de Botánica y Zoología Apartado Postal 139 Zapopan, Jalisco 45101 Mexico Mutun, Serap Abant Izzet Baysal University Department of Biology Bolu, 14280 Turkey

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Nadel, Hannah USDA-ARS SJVASC San Joaquin Valley Science Center 9611 Riverbend Ave. Parlier, California 93648 USA

Nayar, Jai K. Florida Medical Entomology Laboratory University of Florida 200 9th Street SE Vero Beach, Florida 32962 USA

Nagoshi, Rod USDA-ARS Center for Medical, Agricultural and Veterinary Entomology P.O. Box 14565 Gainesville, Florida 32608 USA

Nealis, Vince Natural Resources Canada-Canadian Forest Service Pacific Forestry Centre 506 W. Burnside Road Victoria, British Columbia V8Z 1M5 Canada

Napper, Emma Rothamsted Harpenden, Hertfordshire AL5 2JQ UK

Negron, Jose F. USDA Forest Service Rocky Mountain Research Station 240 West Prospect Fort Collins, Colorado 80526 USA

Naranjo, Steven E. USDA-ARS Western Cotton Research Laboratory 4135 E. Broadway Road Phoenix, Arizona 85040 USA

Neuenschwander, Peter International Institute of Tropical Agriculture 08 B.P. 0932 Cotonou Bénin

Nation, James L. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA

Neven, Lisa, G. USDA-ARS, Yakima Agricultural Research Laboratory 5230 Konnowac Pass Road Wapato, WA 98951 USA

Navajas, Maria Institut National de la Recherche Agronomique Campus International de Baillarguet CS 30016 Montferrier sur Lez cedex, 34988 France

Nguyen, Khuong Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA

Navarette, Ignacio Universities of Cordoba and Extremadura Cáceres, 10071 Spain

Nicolson, Sue Department of Zoology & Entomology University of Pretoria Pretoria 0002 South Africa


Noling, Joseph W. University of Florida Citrus Research & Education Center 700 Experiment Station Rd. Lake Alfred, Florida 33850 USA

Okuda, Takashi National Institute of Agrobiological Sciences Anhydrobiosis Research Unit, 1-2 Ohwashi Tsukuba, 305-8634 Japan

Norris, Douglas E. Johns Hopkins University Bloomberg School of Public Health W. Harry Feinstone Department of Molecular Microbiology and Immunology 615 North Wolfe Street Rm E5008 Baltimore, Maryland 21205 USA

O’Neill, Kevin M. Department of Land Resources and Environmental Sciences Montana State University Bozeman, MT 59717 USA

Northfield, Tobin University of Florida North Florida Research and Education Center 155 Research Rd. Quincy, Florida 32351 USA O’Brien, Lois B. College of Engineering Sciences, Technology and Agriculture Florida A&M University Tallahassee, Florida 32307-4100 USA O’Hara, James, E. Agriculture and Agri-Food Canada 960 Carling Avenue Ottawa, Ontario K1A 0C6 Canada Oi, David H. USDA-ARS Center for Medical, Agricultural and Veterinary Entomology 1600 SW 23rd Drive Gainesville, Florida 32608-1067 USA

Orphanides, George M. Agricultural Research Institute P.O. Box 22016 Nicosia, 1516 Cyprus Otis, Gard W. Department of Environmental Biology University of Guelph Guelph, Ontario N1G 2W1 Canada Overholt, William Allan Indian River Research and Education Center University of Florida Fort Pierce, Florida USA Panizzi, Antõnio R. Embrapa Soja Caixa Postal 231 Londrina, PR 86001-970 Brazil Papadopoulos, Nikos T. Aristotle University of Thessaloniki Laboratory of Applied Zoology and Parasitology Thessaloniki, 541 24 Greece

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Parra, José Roberto Postali Departamento de Entomologia Fitopatologia e Zoologia Agrícola. Esalq/USP, C.P. 9 - 13418-900 Piracicaba, SP Brazil Paré, Paul W. Department of Chemistry and Biochemistry Texas Tech University Lubbock, Texas 79409-1061 USA Paulson, Gregory S. Shippensburg University Department of Biology Shippensburg, Pennsylvania 17257 USA

P.O. Box 443051 Moscow, Idaho 83844-3051 USA Peña, Jorge E. Tropical Research and Education Center University of Florida 18905 SW 280th Street Homestead, Florida 33031-3314 USA Pendland, J.C. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA

Peairs, Frank B. Department of Bioagricultural Sciences and Pest Management Colorado State University Fort Collins, Colorado 80523-1177 USA

Pereyra, Patricia C. CEPAVE Universidad Nacional de La Plata Consejo Nacional de Investigaciones Científicas y Técnicas 2 No 584 (1900) La Plata Argentina

Peck, Daniel C. Department of Entomology, Barton Laboratory New York State Agricultural Experiment Station Cornell University 630 West North Street Geneva, New York 14456 USA

Philogène, Bernard J.R. Department of Biology University of Ottawa Poste 4166 30 Marie Curie Street Ottawa, Ontario K1N 6N5 Canada

Peck, Stewart B. Department of Biology 4640 CTTC Building Carleton University Ottawa, Ontario K1S 5B6 Canada

Pickett, John A. Rothamsted Harpenden, Hertfordshire AL5 2JQ UK

Pellmyr, Olle Department of Biological Sciences University of Idaho Room 252, Life Sciences Building

Pinzauti, Mauro Universita’ degli Studi di Pisa Dipartimento di Coltivazione e Difesa delle Specie Legnose Via S. Michele degli Scalzi, n°2, 56100 Pisa Italy


Pollet, Marc Research Group Terrestrial Ecology University of Ghent, Ghent, Belgium and Royal Belgian Institute of Natural Sciences Brussels Belgium

Pszczolkowski, Maciej Missouri State University and State Fruit Experiment Station 9740 Red Spring Road Mountain Grove, Missouri 65711 USA

Potter, Daniel A. Department of Entomology University of Kentucky S-225 Agricultural Science Center Building North Lexington, Kentucky 40546-0091 USA

Punzo, Fred Department of Biology University of Tampa Box 5F 401 West Kennedy Boulevard Tampa, Florida 33606 USA

Powers, Ann M. Centers for Disease Control and Prevention National Center for Infectious Diseases Division of Vector-Borne Infectious Diseases P.O. Box 2087 Foothills Campus Fort Collins, Colorado 80522 USA

Purcell, Alexander H. Division of Insect Biology University of California 201 Wellman Berkeley, California 94720-3112 USA

Preston, Catherine A. USDA - ARS Center for Medical, Agricultural and Veterinary Entomology P.O. Box 14565 1700 SW 23rd Drive Gainesville, Florida 32608 USA Prischmann, Deirdre USDA ARS NPA NCARL 2923 Medary Ave. Brookings, South Dakota 57006-9401 USA Prokopy, Ronald J. Department of Entomology University of Massachusetts Fernald Hall Amherst, Massachusetts 01003 USA

Puterka, Gary USDA-ARS, PSRL 1301 N. Western Stillwater, Oklahoma 74074 USA Ragsdale, David W. Department of Entomology University of Minnesota 1980 Folwell Avenue St. Paul, Minnesota 55108 USA Raina, Ashok K. USDA-ARS Southern Regional Research Center Formosa Subterranean Termite Research Unit 1100 Robert E. Lee Boulevard P.O. Box 19687 New Orleans, Louisiana 70179-0687 USA

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Randolph, Sarah Department of Zoology University of Oxford South Parks Road Oxford, 0X1 3PS UK

Rey, Jorge Florida Medical Entomology Laboratory University of Florida 200 9th Street S.E. Vero Beach, Florida 32962 USA

Rashidan, Kia University of Saint Boniface 200 Avenue de la Cathedral Winnipeg, Manitoba R2H 0H7 Canada

Ribes, Eva University of Barcelona Barcelona Spain

Ratcliffe, Brett C. Systematics Research Collections University of Nebraska Lincoln, Nebraska 68588-0514 USA Redborg, Kurt E. Department of Biology Coe College 1220 First Avenue Cedar Rapids, Iowa 52402 USA Reina, David Faculty of Veterinary Sciences Universities of Cordoba and Extremadura Cáceres, 10071 Spain Resh, Vincent H. Environmental Science, Policy and Management University of California 201 Wellman Hall Berkeley, California 94720 USA Retnakaran, Arthur Great Lakes Forestry Center 1219 Queen Street East Sault Ste. Marie, Ontario P6A 5M7 Canada

Richman, David B. The Arthropod Museum Entomology, Plant Pathology and Weed Science Department New Mexico State University MSC 3BE, Box 30003 Las Cruces, New Mexico 88003 USA Riddick, Eric W. USDA-ARS Biological Control and Mass Rearing Research Unit 810 Highway 12 East P.O. Box 5367 Mississippi State, Mississippi 39762-5367 USA Riley, David G. Coastal Plain Region University of Georgia P.O. Box 748 Tifton, Georgia 31793-0748 USA Rinkevich, Frank D.L. Department of Biology Millersville University Millersville, Pennsylvania 17551 USA Rivers, David B. Department of Biological Sciences Butler University


4600 Sunset Avenue Indianapolis, Indiana 42608 USA Roderick, George Environmental Science (ESPM) University of California Berkeley, California 94720-3114 USA Rogers, Michael E. Department of Entomology University of Kentucky S-225 Agricultural Science Center North Lexington, Kentucky 40546-0091 USA Roltsch, William J. California Department of Food and Agriculture Biological Control Program 3288 Meadowview Road Sacramento, California 95832 USA Roe, Kelly Department of Biological Sciences Western Illinois University Macomb, Illinois 61455 USA Rosenberg, David M. Freshwater Institute 501 University Crescent Winnipeg, Manitoba R3T 2N6 Canada Ross, Edward S. California Academy of Sciences Department of Entomology Golden Gate Park San Francisco, California 94118 USA Rossi, Anthony Department of Natural Sciences University of North Florida

Jacksonville, Florida 32224 USA Rothschild, Marjorie Integrated Microscopy Center University of Memphis 201 Life Sciences Building Rooms LS 101-113 Memphis, Tennessee 38152-6040 USA Rust, Michael K. Department of Entomology University of California, Riverside Riverside, California USA Rutledge, C. Roxanne Florida Medical Entomology Laboratory University of Florida 200 9th Street S.E. Vero Beach, Florida 32962-4699 USA Sanborn, Allen F. Barry University School of Natural and Health Sciences 11300 NE Second Avenue Miami Shores, Florida 33161-6695 USA Sánchez, Norma E. CEPAVE Universidad Nacional de La Plata Consejo Nacional de Investigaciones Científicas y Técnicas 2 No 584 (1900) La Plata Argentina Sanford, Malcolm T. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA

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Sarzynski, Erin Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Sastry, Shivashankar National Institute of Mental Health Saint Elizabeth Hospital U.S. Department of Health and Human Services Washington, D.C. USA Schabel, Hans G. College of Natural Resources University of Wisconsin Stevens Point, Wisconsin 54481 USA Scheffrahn, Rudolph H. Fort Lauderdale Research and Education Center University of Florida 3205 College Avenue Fort Lauderdale, Florida 33314 USA Scherer, Clay W. DuPont Professional Products Wilmington, Delaware USA Schmelz, Eric USDA, Agricultural Research Service Chemistry Research Unit 1600-1700 SW 23rd Drive Gainesville, Florida 32608 USA Schmidt, Justin O. Southwestern Biological Institute 1961 W. Brichta Dr. Tucson, Arizona 85745 USA

Schneider, David C. Ocean Sciences Memorial University of Newfoundland St. John’s, Newfoundland A1B 3X7 Canada Schöning, Caspar Department of Population Biology University of Copenhagen Universitetsparken 15 2100 Copenhagen Denmark Schulthess, Fritz IITA Contonou Republic of Benin Schuster, Jack Universidad del Valle Aptd 82 Guatemala City Guatemala Scotti, Paul D. The Horticulture and Food Research Institute of New Zealand Mt. Albert Research Centre Auckland New Zealand Seal, Dakshina R. Tropical Research and Education Center University of Florida 18905 SW 280th Street Homestead, Florida 33031-3314 USA Serrano, David Department of Entomology and Nematology University of Florida Gainesville, Florida32611 USA Setamau, Mamoudou Texas A&M Agricultural Experiment Station Weslaco, Texas 78596-8399 USA


Shaaya, Eli Department of Food Science Agricultural Research Organization The Volcani Center P.O. Box 6 Bet Dagan, 50250 Israel

Shirk, Paul D. USDA-ARS Center for Medical, Agricultural and Veterinary Entomology Box 110970 Gainesville, Florida 32611-0970 USA

Shanower, Thomas G. USDA-ARS Northern Plains Agricultural Research Laboratory Pest Management Research Unit 1500 N. Central Avenue Sidney, Montana 59270 USA

Showler, Allan T. USDA-ARS, SARC 2413 East Highway 83 Building 201 Weslaco, Texas 78596 USA

Shapiro-Ilan, David I. USDA-ARS, SAA Southeastern Fruit and Tree Nut Research Laboratory 21 Dunbar Road Byron, Georgia 31008 USA Shepard, B. Merle Coastal Research and Education Center Clemson University 2865 Savannah Highway Charleston, South Carolina 29414-5333 USA Shields, Vonnie D.C. Biological Sciences Department Towson University 800 York Road Towson, Maryland 21252-3042 USA Shippy, Teresa D. Division of Biology Kansas State University Manhattan, Kansas USA

Shukle, Richard H. USDA-ARS Department of Entomology Purdue University West Lafayette, Indiana 47907 USA Sikes, Derek S. University of Alaska Museum 907 Yukon Drive Fairbanks, AK 99775-6960 USA Sims, Kelly R. Department of Entomology and Nematology University of Florida Gainesville, Florida 32611 USA Sinclair, Bradley J. Entomology, Ontario Plant Laboratories, Canadian Food Inspection Agency K.W. Neatby Building, C.E.F. Ottawa, Ontario, K1A 0C6 Canada Sivinski, John USDA-ARS Center for Medical, Agricultural and Veterinary Entomology

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1700 SW 23rd Drive Gainesville, Florida 32604-2565 USA Skevington, Jeff Agriculture and Agri-Food Canada K.W. Neatby Building, C.E.F. 960 Carling Ave. Ottawa, Ontario K1A 0C6 Canada Slaney, David Ecology and Health Research Center Department of Public Health Wellington School of Medicine and Health Sciences University of Otago P.O. Box 7343 Wellington South New Zealand Smagghe, Guy Laboratory of Agrozoology Faculty of Agricultural and Applied Biological Sciences Ghent University Coupure Links 653 B-9000 Ghent Belgium Smith, Hugh University of California Cooperative Extension 624-A West Foster Road Santa Maria, California 93455 USA Smith, John P. John A. Mulrennan, Sr., Public Health Entomology Research & Education Center Florida A&M University 4000 Frankford Avenue Panama City, Florida 32405-1933 USA

Soler Cruz, M.D. Amparo Department of Parasitology University of Granada 18071 Granada Spain Solter, Leellen F. Illinois Natural History Survey 607 East Peabody Drive Champaign, Illinois 61820 USA Somma, Louis A. Department of Entomology and Nematology University of Florida Gainesville, Florida 32611 USA Soroka, Juliana J. Agriculture and Agri-Food Canada Saskatoon Research Centre 107 Science Place Saskatoon, Saskatchewan S7N 0X2 Canada Sourakov, Andrei Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Spafford, Helen School of Animal Biology (M0895) University of Western Australia 35 Stirling Highway Crawley, W.A. 6009 Australia Stange, Lionel A. Florida Department of Agriculture Division of Plant Industry P.O. Box 110980 Gainesville, Florida 32611-0980 USA


Steck, Gary J. Florida State Collection of Arthropods Division of Plant Industry 1911 SW 34th Street Gainesville, Florida 32608-1201 USA Stocks, Ian 308 Long Hall Department of Entomology, Soils, and Plant Sciences Clemson University Clemson, South Carolina 29634-0315 USA Steinkraus, Donald C. Department of Entomology University of Arkansas Virology Laboratory 319 Agriculture Building Fayetteville, Arkansas 72701 USA Stewart, Kenneth W. Department of Biological Science University of North Texas P.O. Box 305220 Denton, Texas 76203-5220 USA Stonedahl, Gary 106 Briza Court Bellingham, Washington 98226 USA Striganova, Bella R. Laboratory of Soil Zoology and General Entomology A. N. Severtsov Institute of Ecology and Evolution Russian Academy of Sciences Leninsky Prospect, 33 Moscow 119071 Russia

Sullivan, Daniel J. Department of Biological Sciences Fordham University Bronx, New York 10458 USA Swisher, Marilyn E. Department of Family, Youth and Community Sciences University of Florida Gainesville, Florida 32611-0310 USA Sword, Gregory School of Biological Sciences University of Sydney The Macleay Building A12 Sydney, NSW 2006 Australia Tabachnick, Walter J. Florida Medical Entomology Laboratory University of Florida 200 9th Street SE Vero Beach, Florida 32962-4699 USA Tanaka, Seiji Laboratory of Insect Life Cycles and Physiology Division of Insect and Animal Sciences Independent Administrative Institution Ohwashi 1-2, Tsukuba, Ibaraki 305-8634 Japan Tartar, Aurélian Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Taylor, Steven J. Center for Biodiversity Illinois Natural History Survey

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607 East Peabody Drive (MC-652) Champaign, Illinois 61820-6970 USA Teal, Peter E.A. USDA-ARS Center for Medical, Agricultural and Veterinary Entomology 1700 SW 23rd Drive P.O. Box 14565 Gainesville, Florida 32604 USA

Tinsaara, William Bioversity International P.O. Box 24384, Kampala Uganda Tipping, Christopher Delaware Valley College 700 East Butler Ave. Doylestown, Pennsylvania 18901 USA

Tew, James E. Ohio State University 1608 Madison Avenue Wooster, Ohio 44691-1030 USA

Triplehorn, Charles Department of Entomology Museum of Biological Diversity Ohio State University 1315 Kinnear Road Columbus, Ohio 43212-1192 USA

Thomas, Michael C. Florida State Collection of Arthropods Florida Department of Agriculture and Consumer Services P.O. Box 147100 Gainesville, Florida 32614-7100 USA

Trumble, John T. Department of Entomology University of California Riverside, California 92521-0001 USA

Thompson, Sarah Department of Entomology North Carolina State University P.O. Box 7613 Raleigh, North Carolina 27965-7613 USA Thompson, Vinton Roosevelt University Chicago, Illinois 60605 USA Tilgner, Erich Department of Entomology University of Georgia 413 Biological Sciences Building Athens, Georgia 30602 USA

Tsai, James H. Fort Lauderdale Research and Education Center University of Florida 3205 College Avenue Fort Lauderdale, Florida 33314-7799 USA Tzanakakis, Minos E. Aristotle University of Thessaloniki Department of Applied Zoology and Parasitology Thessaloniki, 541 24 Greece Ueshima, Norihiro Matsusaka University Matsusaka, Mie Japan


Uspensky, Igor Department of Chemistry A. Silberman Institute of Life Sciences Hebrew University of Life Sciences Jerusalem 91904 Israel Valles, Steven M. USDA-ARS Center for Medical, Agricultural, and Veterinary Entomology 1600 SW 23rd Drive Gainesville, Florida 32608 USA Vandergast, Amy G. U.S. Geological Survey San Diego, California USA VanderMeer, Robert K. USDA-ARS Center for Medical, Agricultural and Veterinary Entomology P.O. Box 14565 1700 SW 23rd Drive Gainesville, Florida 32608 USA Vázquez, M. Ángeles Departamento de Zoología y Antropología Física C/ José Antonio Novais 2, pl.X Lab. 9 Universidad Complutense de Madrid 28040 Madrid Spain Vega, Fernando E. USDA-ARS Insect Biocontrol Laboratory Beltsville Agricultural Research Center Building 011A, Room 214 Beltsville, Maryland 20705 USA

Verma, K.K. HIG1/327, Housing Board Colony Borsi, DURG - 491001 India Vickerman, Danel B. Department of Entomology University of California Riverside, California 92521-0001 USA Villegas, Baldomero California Department of Food and Agriculture Biological Control Program 3288 Meadowview Road Sacramento, California 95832 USA Vincent, Charles Horticultural Research and Development Center Agriculture and Agri-Food Canada 430 Boulevard Gouin Saint-Jean-sur-Richelieu, Quebec J3B 3E6 Canada Wallace, John R. Department of Biology Millersville University Millersville, Pennsylvania 17551 USA Wang, Ping Entomology Department Cornell University New York State Agricultural Experiment Station Geneva, New York 14456 USA Wang, Qiao Institute of Natural Resources Massey University PB 11122 Palmerston North New Zealand

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Weber, Donald C. USDA, ARS, PSI, Insect Biocontrol Laboratory Bldg. 011A, Rm. 107, BARC-West Beltsville, MD 20705 USA Weber, Richard G. Department of Entomology and Applied Ecology University of Delaware Newark, Delaware 19716 USA Webster, Thomas C. Atwood Research Facillity Kentucky State University Frankfort, Kentucky 40601 USA Weinstein, Philip Ecology and Health Research Center, Department of Public Health Wellington School of Medicine and Health Sciences University of Otago P.O. Box 7343 Wellington South New Zealand Weintraub, Phyllis G. Agricultural Research Organization Gilat Research Station D.N. Negev, 85280 Israel Weissman, David B. Department of Entomology California Academy of Sciences Golden Gate Park San Francisco, CA 94118 USA Weston, Paul A. Department of Entomology Cornell University

Comstock Hall Ithaca, New York 14853-0901 USA Wheeler, Alfred G. Department of Entomology Clemson University 114 Long Hall Box 340365 Clemson, South Carolina 29634-0365 USA Wiener, Linda St. John’s College Santa Fe, New Mexico 87501 USA Wild, Alex Department of Entomology University of Arizona PO Box 2100 Tucson, Arizona 85721-0036 USA Williamson, R. Chris Department of Entomology University of Wisconsin 237 Russell Labs Madison, Wisconsin 53706-1520 USA Willis, John S. Department of Cellular Biology University of Georgia 724 Biological Sciences Building Athens, Georgia 30602-2607 USA Willis, Judith H. Department of Cellular Biology University of Georgia 724 Biological Sciences Building Athens, Georgia 30602-2607 USA


Willmott, Keith R. McGuire Center for Lepidoptera Research and Conservation University of Florida Gainesville, Florida 32611 USA Wing, Steven R. University of Florida P.O. Box 115001 Gainesville, Florida 32611 USA Worner, Sue National Centre for Advanced Bio-Protection Technologies Bio-Protection and Ecology Division Lincoln University P.O. Box 84, Canterbury New Zealand Wysiecki, María L. CEPAVE Universidad Nacional de La Plata Consejo Nacional de Investigaciones Científicas y Técnicas 2 No 584 (1900) La Plata Argentina Yousten, Allan A. Department of Biology Virginia Tech 2119 Derring Hall

Blacksburg, Virginia 24061-0406 USA Yu, Simon J. Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Zachvatkin, Yuri A. Department of Entomology K. A. Timiryazev Agricultural Academy Timiryazeva St., 49, Build. 12 Moscow 127550 Russia Zhu, Kun Yan Department of Entomology Kansas State University 123 Waters Hall Manhattan, Kansas 66506-4004 USA Zaspel, Jennifer Entomology and Nematology Department University of Florida Gainesville, Florida 32611-0620 USA Zuparko, Robert L. Essig Museum of Entomology University of California 201 Wellman Hall Berkeley, California 94720-3112 USA

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Abafi-Aigner, Lajos (Ludwig Aigner) george hangay Narrabeen, New South Wales, Australia Ludwig Aigner was born on the 11 February 1840 at Nagyjécsa, Torontál Shire, Transylvania, Hungary, now Romania. His family moved to Temesvár, a large town in Transylvania, where he received a formal education in commerce and begun his career as a book merchant. His family was of ethnic German stock and young Ludwig only learned Hungarian when, in 1858, they moved to Pozsony (now Bratislava and in the Slovak Republic), a large town with predominantly Hungarian inhabitants. From here he soon moved on to Pest (now Budapest) and in 1863, as it was the custom in those years, he wandered all over Austria and Germany. He completed his studies in Köln and Stuttgart before returning to Pest. He always had an interest in entomology and he became a keen amateur lepidopterologist. However, besides entomology, he had a great variety of other interests too, especially in the field of publishing, writing, historical research as well as aspirations in business. He found success in publishing and in establishing a popular bookshop. In 1870 he was initiated as a Freemason and eventually he rose to the highest positions in the Order. For 12 years he has worked on an extensive monograph of the history of Freemasonry. He used his Hungarian pen name “Abafi” in a hyphenated form with his

original family name: Abafi-Aigner and changed his German Christian name “Ludwig” to the Hungarian equivalent “Lajos.” However, despite his successes in publication and writing his business begun to decline in the 1880s and within a few years he faced financial difficulties, which ultimately led to the closure of his famous bookshop. Disillusioned, he discontinued most of his business activities, and from 1890 he devoted all his time and energy to lepidopterology. In 1895, he published the results of his studies in the Természetrajzi Füzetek (Notebooks of Natural History), the journal of the National Museum’s Natural History Department and he was one of the authors of Fauna Regni Hungariae (Catalogue of Hungary’s Fauna). He resurrected Rovartani Lapok (Entomological Papers), which was established in 1884 but ceased to exist in 1886. His treatment of the butterfly fauna of Hungary won the coveted Bugát Prize. Based on this work he published Butterflies of Hungary in 1907. The book was (and probably still is) one of the most popular entomological publications in Hungary. It has inspired countless young entomologists and made the name of Abafi-Aigner well known to every naturalist in the country. He passed away on the 19 June 1909.

Reference Horváth C (1990) A rovartan tudósa. E’ let és Tudomány 45:290, 312

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Abaxial Surface

Abaxial Surface The lower surface of a leaf (contrast with adaxial surface).

Abbott, John John Abbott was born in London in 1751. In England, he was given drawing lessons and, through his drawing instructor, was introduced to Dru Drury, a collector of insects who had been president of the Linnean Society. These two encounters encouraged him to collect insects and draw them, but his father was training him to be an attorney. Finding legal paperwork not to his liking, he emigrated to Virginia in 1773. After 2 years in Virginia, he relocated to Georgia, where he served as a private in the Third Georgia Continental Battalion during the Revolutionary War. For his military service he received several hundred acres of land, and worked as a planter and schoolmaster. In Virginia he had collected American insects and bird skins, and drew and painted insects and birds. Some of the specimens and paintings were shipped to England for sale. Some of the paintings, after sale, adorned books on birds, insects, and spiders written by various authors, not necessarily with acknowledgment to Abbott. In all, Abbott produced over 3,000

drawings of a quality that was very high for that time. Some of the insect illustrations included not only adults, but also larvae and the plants on which they fed, and even observational notes. He died about 1840.

Reference Mallis A (1971) American entomologists. Rutgers University Press, New Brunswick, NJ, 549 pp

Abbott’ s Formula A mathematical technique commonly used to assess mortality in insecticide trials when there is need to correct for a change (decrease) in the background population density (i.e., in the check or control plots). The formula is: % corrected control = 100 × (% alive in the check % alive in the treatment)/(% alive in the treatment)

Abdomen The posterior of the three main body divisions of an insect (Fig. 1).  Abdomen of Hexapods

Abdomen, Figure 1 Cross section of an insect abdomen, showing components of the insect circulatory system and direction of hemolymph flow (adapted from Evans, Insect biology).

Abdomen of Hexapods

Abdomen of Hexapods severiano f. gayubo Universidad de Salmanca, Salamanca, Spain The abdomen constitutes the caudal tagma in the hexapods and is usually larger than the other two, the head and the thorax. This region is also referred to as a visceral area because it houses the visceral organs. Its form can vary depending on the group, and even on the species. The maximum number of observed segments is 11, although certain authorities consider a twelfth segment that in fact corresponds to a telsonic caudal region. In general, the number of segments decreases from the preimaginal phases to the adult stage, especially in those holometabolous insects in which the last segments of the adults are formed from imaginal discs during pupation. In the groups considered most

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primitive, the number of abdominal segments is usually greater, as occurs in the Protura with 11 segments (Figs. 2–5). An exception is the Collembola, which only possess six. In addition, it is necessary to keep in mind that, in certain cases, the total number of visible segments does not coincide with what a particular individual actually possesses, since some segments remain “invisible” upon being telescoped, particularly those of the posterior region of the abdomen. According to Bitsch, a generalized abdominal segment would be limited anteriorly by a presegmentary domain, separated from the segmentary domain proper (of greater size) by a suture that begins an internal crest named the costa or antecosta. This crest anteriorly delimits an acrotergite or precosta in the tergal part and a presternite in the sternal part. In this idealized model, the muscles would be inserted in successive antecostas. No known structure is homologous to the thoracic furca. The presence of the gonopore (double in Ephemeroptera) in segments VIII and IX (in VII in the case of Ephemeroptera), and fundamentally of the external structures related to reproduction (the genitalia), produce important modifications in those segments. Considering the presence of these genitalia, three regions of the abdomen are recognized: an anterior (pregenital or visceral region that includes the first eight segments), median (genital region, eighth and ninth segments), and caudal regions (postgenital region, tenth and eleventh segments plus the telsonic region).

The Pregenital Region

Abdomen of Hexapods, Figure 2 Diagram of a proturan (Protura) showing abdominal segments and appendages: dorsal view (left), ventral view (right).

In the most generalized condition, the first abdominal segments conserve their basic structure, being easily distinguished from the thoracic segments. Nevertheless, the most frequent condition is that which produces morphological modifications that affect the thoracic-abdominal union. These modifications usually consist of reductions that affect the sternal region and involve a greater or lesser desclerotization of different structures and their

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Abdomen of Hexapods

Abdomen of Hexapods, Figure 3 Diagram of chewing louse (Mallophaga) showing abdominal segments, including numbering of segments: dorsal view (left), ventral view (right).

incorporation to the metathorax. In this sense, the case of the Hymenoptera, Apocrita stands out, in which a narrowing is produced between the second and the third abdominal segments, which incorporate the thorax and is named the propodeum. The rest of the abdominal segments are called the gaster or metasoma. The region formed by the propodeum and the thorax constitutes the mesosoma. The narrowing allows a great amplitude of movements of the metasoma, which permits stinging in the capture of prey in aculeates. In some groups, like Formicidae and Sphecidae (Aculeata), one or two segments of the metasoma form a narrower zone called the petiole. In the pregenital region, several appendicular structures can be found. Thus, three pairs of highly

modified appendages exist in Collembola. In Archaeognatha, very developed coxites are differentiated, above which are inserted styli in a median position and the exsertile vesicles in the most internal position. The styli are elongated pieces, articulated in their base above the external face of the coxite. They are unisegmentary and lack muscles inserted in their base, often presenting an apical spine. Taking into account their position and their embryonic development, the styli are considered by the majority of authorities as vestigial appendages, and more concretely as reduced telepodites. The exsertile vesicles are considered internal coxal formations (internal coxalia of some authorities).

Abdomen of Hexapods

antenna pretarsus tibiotarsus femur trochanter coxa precoxae collophore

eye pronotum mesonotum metanotum

tenaculum (catch)

manubrium dens mucro

furcula (spring)

Abdomen of Hexapods, Figure 4 Diagram of springtail (Collembola) showing furcular appendage at tip of abdomen.

In Pterygota the abdominal appendages remain restricted to the larval forms (Lepidoptera and Hymenoptera, Tenthredinoidea), although rough appendicular pairs already exist in the polypodous type of embryos. These abdominal appendages are named “false legs” or “prolegs” and are retractile, conical and membranous projections, with a circular planta that bears a crown, usually with hooks, to adhere to the substrate.

The Genital Region The transformations that affect the eighth and ninth abdominal segments are a consequence of the development of special external structures that in the case of the male serve in the transfer of sperm, and in the case of the female allow for oviposition. These structures together are known by the name genitalia. The origin of the genitalia is controversial, although the majority of authorities accept that, at

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least in part, it is of appendicular origin. In this sense, it is clear that in the Archaeognatha the eighth and ninth segments are basically similar in males and females and their structures are homologous to those already indicated for the pregenital segments. Taking into account this relationship, the genitalia of Archaeognatha are considered primitive, and therefore fundamental to interpret the genitalia of Pterygota. In the eighth segment of the Archaeognatha, the basal part of the appendicular structure is named first gonocoxa or gonocoxite and bears the first gonostylus; in the ninth is found the second gonocoxa with its corresponding stylus. In both segments (at times in the eighth, always in the ninth) formations homologous to the exsertile vesicles appear, which are called gonapophyses (parameters in the males and gonapophysis proper in the females). The fundamental difference between both sexes lies in the presence in the males of a phallic structure. The female genitalia in the Pterygota constitute the ovipositor. The gonocoxites are incorporated into the lateral wall of the genital segments in a complete manner in the eighth segment, forming the first valvifer. In the ninth segment the basal part is incorporated into the lateral wall, originating the second valvifer, while the rest is extended, forming the third pair of valves (dorsal or lateral valves of some authorities), which are not homologous in Archaeognatha. The other two pairs of valves are the ventral valves, corresponding to the eighth segment, and the internal valves, corresponding to the ninth segment. These two pairs of valves are homologous to the gonapophysis of Archaeognatha. In the case of the generalized type of ovipositor like that of Orthoptera, these three pairs of valves are linked through the length of their course, forming in their interior a canal for oviposition. Among the sclerites that are situated in the base of the valves (in addition to the valvifers already mentioned) are found the intervalves (intervalvulae of the authorities) by way of elongated transverse formations, one in the base of the valves of the eighth segment and another in the base of the valves of the ninth segment. The typical ovipositor

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Abdomen of Hexapods

Abdomen of Hexapods, Figure 5 Comparative development of cerci on earwig (Dermaptera, top left); grasshopper (Orthoptera, top right); scorpion fly (Mecoptera, lower left); silverfish (Zygentoma).

that was just described can experience modifications according to the functions that it carries out; one of the most drastic is found in Hymenoptera, Aculeata, where it is transformed into a sting that serves the females as an attacking organ, either to capture prey or as a defense. On the other hand, the process of oviposition can be carried out through other, different structures, as occurs in the females of certain Diptera. In that case, the last segments are retractile and the intersegmental zones are highly

developed, in such a way that they can become telescoped, forming oviposition tubes; this type of “ovipositor” is named the ovicauda. Not being homologous to the genitalia, many authorities call it terminalia. The masculine genitalia present great morphological variability, which together with their taxonomic importance, have been the object of an infinity of descriptions, many of them without truly anatomical criteria. This has originated the

Abdomen of Hexapods

use of very varied terminologies that have done nothing but complicate its study and impede the establishment of homologies even in the same group, creating in this way a great nomenclatorial chaos. In the males, in addition to the genitalia proper, other structures (processes, lobes, etc). exist that intervene in functions other than those strictly related to the transfer of sperm; among the most common is the grasping of the female during mating. It has already been mentioned that the majority of authorities consider that the interpretation of the genitalia of Pterygota should be made by homology with the basic condition that is found in Archaeognatha. In this group, the phallic complex is formed by a median organ, the phallus or penis, and a pair of segmented pieces named parameres, that in the case of maximum development can exist in the eighth and ninth segments. The parameres correspond to the gonapophysis of the females (although the term gonapophysis is utilized indistinctly for both sexes by some authorities). Many morphological models have been proposed to describe the male genitalia of Pterygota. The most complete, since it gathers and discusses early data, is that proposed by Bitsch. According to this author, what together forms the copulatory organ (phallus or penis) and the structures associated with the parameres (considered in the sense expressed by the Archaeognatha) is named the phallic complex. The aedeagus is a sclerotized tube, situated above a largely membranous phallobase, although in more complex cases the phallobase presents an internal fold that remains membranous (endotheca) while the external part is sclerotized (phallotheca or theca). The aedeagus presents an invagination that forms a more or less developed internal chamber (the endophallus), which communicates with the gonopore at its base and in the other extreme communicates with the exterior through the phallotreme. In counter-proposition to the endophallus, the part formed by the external walls of the phallobase and the aedeagus forms the ectophallus. The phallic complex can present variable development, even being able to cause the aedeagus to disappear,

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or on the contrary, increase in complexity, developing spines and other types of processes named flagellum, virga or pseudovirga over the internal walls of the endophallus. When the endotheca and the endophallus are evaginated, the genitalia are converted into authentic intromittent organs. The primitive position of the male genitalia can be displaced through different types of turns; one of the most showy cases is that which occurs in some Hymenoptera, Symphyta that present the condition called strophandric, which is characterized by a 180° rotation of the genitalia. Rotations have also been observed in males of Diptera. The postgenital region, as was mentioned in the beginning of this section, comprises the tenth and eleventh segments plus the telsonic region. The tenth segment has been detected in Protura, Diplura, Archaoegnatha, Thysanura (Zygentoma), Ephemeroptera, Plecoptera, and some Orthoptera. The morphology of this segment is basically similar to the pregenital segments, although with certain frequency it can form a ring when the tergum and sternum unite, or the sternal region can be membranous. In embryonic forms, a pair of appendicular outlines is seen above this segment. In certain holometabolous insects, structures of uncertain meaning appear, such as the socii of some Hymenoptera. The eleventh segment is recognized in the majority of embryonic phases of hexapods. In Archaeognatha and Thysanura it forms an annular structure from whose dorsal part is differentiated a long and narrow process called filum terminale, while from the lateroventral position are differentiated the cerci that in the adults possess numerous divisions. In the Pterygotes, the eleventh segment is formed by the epiproct (tergal region) and the paraprocts (in the lateroventral position); in the more primitive groups exist cerci (whose length and number of divisions are variable) situated in the membranous zones that exist between the epiproct and the paraprocts. The telsonic, asegmentary region constitutes the perianal membrane or periproct.  Alimentary Canal and Digestion

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Abdominal Pumping

References Bitsch J (1979) Morphologie abdominal des insects. In: Grassé, P-P (ed) Traité de Zologie, VIII (II): 291–600 Bitsch J (1994) The morphological groundplan of Hexapoda: critical review of recent concepts. Annales de la Société Entomologique de France 30:103–129 Deuve T (2001) The epipleural field in hexapods. Annales de la Société Entomologique de France 37:195–231 Matsuda R (1970) Morphology and evolution of the insect abdomen. Pergamon Press, New York, NY Snodgrass RE (1935) Principles of insect morphology. MacGraw Hill, New York, NY

Abdominal Pumping Contraction of the muscles associated with the abdomen can result in collapse and expansion of the air sacs. This forces relatively large volumes of air in and out of the insect through the spiracles, promoting ventilation. This is called active ventilation, in contrast with the more normal gas exchange mechanism of insects, diffusion or passive ventilation. To a small degree, abdominal pumping also promotes gas exchange through the trachea, but the trachea is quite resistant to change in shape. Abdominal pumping is more important for larger insects such as locusts, which display abdominal pumping almost continuously, but especially when active. In these insects air is sucked in through some spiracles and pumped out through others.  Active Ventilation

Abiotic Disease A disease caused by factors other than pathogens (e.g., weather or nutrition).

Abiotic Factors Factors, usually expressed as factors affecting mortality, characterized by the absence of life. Abiotic factors include temperature, humidity, pH, and other physical and chemical influences.

Abnormality In insect pathology, deviation from the normal; a malformation or teratology; a state of disease.

Abrocomophagidae A family of chewing lice (order Phthiraptera).  Chewing and Sucking Lice

Absolute Methods of Sampling Techniques used to sample insect populations that provide an estimate per unit of area (e.g., per square meter, per leaf or per plant). Types of absolute methods include unit of habitat, recapture, and removal trapping. (contrast with relative methods of sampling).  Sampling Arthropods

Acanaloniidae A family of insects in the superfamily Fulgoroidae (order Hemiptera). They sometimes are called planthoppers.  Bugs

Acanthmetropodidae A family of mayflies (order Ephemeroptera).  Mayflies

Acanthopteroctetidae A family of moths (order Lepidoptera). They commonly are known as archaic sun moths.  Archaic Sun Moths  Butterflies and Moths

Acaricides or Miticides

Acanthosomatidae A family of bugs (order Hemiptera).  Bugs

Acaricide A pesticide applied to manage mite populations. An acaricide is also called a miticide.  Acaricides or Miticides

Acaricides or Miticides marjorie a. hoy University of Florida, Gainesville, FL, USA An acaricide or miticide is a pesticide that provides economic control of pest mites and ticks. Mites and ticks are collectively called either acari or acarina. Some products can act as insecticides or fungicides as well as acaricides. An acaricide is a pesticide used to kill mites and ticks (Table 1). Always check with state and federal authorities to be sure products containing these active ingredients are registered for use. Always read labels carefully and follow the directions completely. The toxicity of an acaricide is determined by a dose-response curve or a concentration-response curve. Such curves are obtained by exposing test mites or insects to increasing concentrations or doses of the pesticide and recording the resulting mortality after a given time interval. One estimate of toxicity used is the term LD50 (which is the dose required to kill 50% of the test population). The LC50 is the concentration required to kill 50% of the test population. If the dose is introduced through the insect’s mouth it is an oral LD50, if it is introduced through the skin or integument it is a dermal LD50, and if it is introduced through the respiratory system it is the inhalation LD50. A measured dose is applied to an arthropod by inserting a measured amount of toxicant into the gut or by

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applying a measured amount to the integument. The lower the LD50 or LC50, the more toxic the poison. An LC50 is obtained when a mite is exposed to a particular concentration of toxicant but the actual amount of toxicant the individual experiences is not determined. For example, if the pesticide is applied to foliage and the mite walks about on the foliage, the actual amount of toxicant the mite is exposed to depends on the activity of the mite, the amount taken up through the integument or by feeding. Figure 6 shows a concentration-response curve in parts per million (ppm) for the acaricide Omite (propargite) exhibited by adult females from colonies of the Pacific spider mite Tetranychus pacificus. The concentration required to kill 50% of the individuals is the LC50. The two types of F1 females (produced by crossing Chapla males and Bidart females, and vise versa) respond similarly and their concentration-response curves are about midway between those of the resistant (Bidart) and susceptible (Chapla) colonies, which indicates that resistance may involve a semidominant mode of inheritance. The term mode of inheritance describes how the trait is inherited; for example, the resistance can be determined by a single major dominant (only one copy of the gene is required for the mite to express the resistance) or recessive (two copies of the gene are required) gene. Or, the resistance can be a quantitative trait determined by multiple genes of equal and additive effect. In this example, the propargite resistance may be determined a single semidominant gene with modifying genes, but additional tests are required to resolve whether more than one gene actually contributes to this resistance.

Acaricide Classification Pesticides are classified in several ways, including: (i) their mode of entry into the target pest, (ii) chemical structure, or (iii) source.

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Acaricides or Miticides, Table 1 Acaricides (miticides) currently or recently available for general and

restricted use to control mites and ticks* Name** (chemical type) Some trade names Abamectin (avermectin B1a; produced from the bacterium Streptomyces avermitilis) Affirm, Agri-Mek, Avid, vertimec, Zephyr Amitraz (triazapentadiene) Acarac, Mitac, Ovidrex,Triatox,Topline Azadirachtin (tetranortriterpenoid extracted from the Neem tree) Align, Azatin, Turplex

General Use (GU)*** Restricted Use (RU) GU, Class IV (practically nontoxic)

GU, Class III (slightly toxic)

GU, Class IV

Bifenazate (carbazate) Floramite Class IV

Bifenthrin (pyrethroid) Talstar, Brigade, Capture

RU, Class II (moderately toxic)

Carbaryl (carbamate) Adios, Bugmaser, Crunch, Dicarbam on formulation Hexavin, Karbaspray, Septene Sevin, Tornadao, Thinsec

GU, Class I, II or III, depending

Chlorobenzilate (chlorinated hydrocarbon) Acaraben, Akar, Benzilan, Folbex Chlorfenapyr (pyrrole) Pylon, Pyramite, Pirate

RU, Class III, may cause tumors in mice Class I

Cinnamon oil (cinnamaldehyde) Cinnamite

Exempt from registration under FIFRA

Citronella oil Demeton-S-Methyl (organophosphate) Meta-Systox, Azotox, Duratox, Mifatox

Exempt from FIFRA No longer registered for use in USA; Class I, highly toxic

Potential use Also an insecticide; affects nervous system and paralyzes insects or mites; used in citrus, pears, nut tree crops Used in pears, cotton, and on cattle, and hogs to control insects, ticks and mites Azadirachtin is similar to insect hormones called ecdysones, which control metamorphosis; also may serve as a feeding deterrent; used to control insects and mites on food, greenhouse crops, ornamentals and turf Mites on greenhouse, shadehouse, nursery, field, field, landscape and interiorscape ornamentals, not registered in USA for use on food Insecticide and acaricide that affects the nervous system and causes paralysis; used on greenhouse ornamentals and cotton General use pesticide to control insects on citrus, fruits, cotton, forests, lawns, nuts, ornamentals, shade trees, poultry, livestock and pets. Also works as a mollusccide and acaricide Used for mite control on citrus and in beehives; also kills ticks; use cancelled in USA Used to control spider mites, broad ites, budmites, cyclamen mite, rust mites and some insects. Broad spectrum miticide/ insecticide/fungicide controls or repels pests; could be phytotoxic in some cases; used in ornamentals, shade or nursery trees, vegetables, herbs and spices Repels insects and ticks Systemic and contact insecticide and acaricide, widely used against diverse pests


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Acaricides or Miticides, Table 1 (Continued) Name** (chemical type) Some trade names

General Use (GU)*** Restricted Use (RU)

Potential use

Dicofol (organochlorine) Acarin, Difol, Kelthane, Mitigan

GU, Class II or III, depending on formulation

Miticide used on fruits, vegetables, ornamentals and field crops

Dicrotophos (organophosphate) Bidrin, Carbicron, Dicron, Ektafos

RU

Contact systemic pesticide and acaricide used to control sucking, boring and chewing pests on coffee, cotton, rice, pecans; used to control ticks on cattle

Dienochlor (organochlorine) Pentac, often formulated with other pesticides

GU, Class III

Contact material used for plant-feeding mites on ornamental shrubs and trees outdoors and in greenhouses; disrupts egg laying of female mites; use cancelled in USA

Dinocap (dinitrophenyl) Arathane, Caprane, Dicap, Dikar Karathane, Mildane

GU, Class III

Used as a fungicide and as an acaricide for ticks and mites; use cancelled in USA

Disulfoton (organophosphate) Disyston, Disystox, Dithiodemeton, Dithiosystox, Solvigram, Solvirex

RU, Class I, highly toxic

Systemic insecticide and acaricide used to control sucking insects/ mites on cotton, tobacco, sugar beets, cole crops, corn, peanuts, wheat, grains, ornamentals, potatoes

Endosulfan (chlorinated hydrocarbon) Afidan, Cyclodan, Endocide, Hexasulfan, Phaser, Thiodan, Thionex

RU, Class I

Contact insecticide and acaricide used to control many pests on tea, coffee, fruits, vegetables, grains

Ethion (organophosphate) Acithion, Ethanox, Ethiol, Nialate, Tafethion, Vegfru Foxmite

GU, Class II

Insecticide and acaricide used on wide variety of food, fiber and ornamentals, including greenhouse crops, citrus, lawns and turf

Eucalyptus oil

Exempt from FIFRA

Repels mites; repels fleas and mosquitoes

Fenamiphos (organophosphate) Nemacur, Phenamiphos, Bay 68138

RU, Class I

A nematicide that has some activity against sucking insects and spider mites

Fenbutatin oxide (organotin) Vendex

RU

Miticide used on perennial fruits, eggplant and ornamentals

Fenitrothion (organophosphate) Accothion, Cyfen, Dicofen, Fenstan, Folithion, Mep, Metathion, Micromite Pestroy, Sumithion, Verthion

GU

Acaricide and insecticide effective gainst a wide array of pests

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Acaricides or Miticides, Table 1 (Continued) Name** (chemical type) Some trade names Formothion (organophosphate) Aflix, Anthio, Sandoz S-6900

General Use (GU)*** Restricted Use (RU) RU, Class II

Hexythiazox (ovicide, growth regulator) Savey

Class III

Lambda cyhalothrin (pyrethroid) RU, Class II Charge, Excaliber, Granade, Hallmark, Icon, Karate, Matador, Saber, Sentinel Lindane (organochlorine) Agrocide, Benesan, Benexane, BHC, Gammex, Gexane, HCH, Isotox, Kwell, Lindafor, Lintox, Lorexane, Steward

RU, Class II Most uses cancelled in USA because of potential to cause cancer

Methamidophos (organophosphate) Monitor, Nitofol, Tamaron, Swipe Patrole, Tamanox

RU, Class I

Methidathion (organosphosphate) Somonic, Supracide, Suprathion

RU, Class I

Methomyl (carbamate) Acinate, Agrinate, Lannate, Lanox, Nudrin, NuBait

RU, Class I

Mevinphos (organophosphate) Fosdrin, Gesfid, Meniphos, Menite, Mevinox, Mevinphos, Phosdrin, Phosfene Monocrotophos (organophosphate) Azodrin, Bilobran, Monocil 40, Monocron, Nuvacron, Plantdrin Naled (organophosphate) Bromex, Dibrom, Lucanal

RU, Class I

Oxamyl (carbamate)

RU, registration in USA withdrawn in 1988

GU, Class I

Potential use Systemic and contact insecticide and acaricide, used against spider mites on tree fruits, vines, olives, hops, cereals, sugar cane, rice Ovicide/miticide effective against spider mites on tree fruits, christmas trees, strawberries, hops, peppermint, caneberries Insecticide and acaricide used to control a variety of pests in cotton, cereals, hops, ornamentals, potatoes, vegetables; controls ticks Insecticide and fumigant; used in lotions, creams and shampoos for control of lice and mites (scabies) in humans Systemic, residual insecticide/ acaricide/avicide with contact and stomach action, used to control chewing and sucking insects and mites in many crops outside the USA Insecticide and acaricide with stomach and contact action used to control a variety of insects and mites in many crops Broad spectrum insecticide and an acaricide to control ticks, acts as a contact and systemic pesticide Insecticide and acaricide effective against a broad spectrum of pests, including mites and ticks; use cancelled in greenhouses Systemic and contact insecticide and acaricide

Contact and somach insecticide and acaricide, used against mites in greenhouses RU, Class I granular form is banned Insecticide/acaricide/nematacide in USA that controls a broad spectrum of mites, ticks and roundworms on field crops, vegetables, fruits, ornamentals


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Acaricides or Miticides, Table 1 (Continued) Name** (chemical type) Some trade names Neem oil Trilogy

General Use (GU)*** Restricted Use (RU)

Potential use

Broad spectrum fungicide and acaricide in citrus, deciduous fruits and nuts, vegetables, grains Permethrin (pyrethroid) Ambush, Class II or III, depending on Broad spectrum used on nut, fruit, Cellutec, Dragnet, Ectiban, formulation RU in agriculture vegetable, cotton, ornamentals, Indothrin, Kafil, Kestrel, Pounce, because of adverse effects on mushrooms, potatoes, cereals, in Pramex, Zamlin, Torpedo aquatic organisms greenhouses, home gardens, on domestic animals Petroleum oils (refined petroClass IV Kills by contact a wide range of leum distillate) Sunspray and mite and insects; complete coverage is essential; may act as a others feeding or oviposition deterrent. Phytotoxicity can occur if plants are stressed, especially by lack of water; some plant cultivars are more susceptible than others. Used as dormant and as foliar sprays. Phorate (organophosphate) RU, Class I Insecticide and acaricide used on Agrimet, Geomet, Granutox, pests, including mites, in forests, Phorate Rampart, Thimenox, root and field crops, ornamentals Thimet, Vegfru and bulbs Phosalone (organophosphate) GU, No longer for sale in USA due Broad spectrum insecticide/ to carcinogenic effects acaricide used on deciduous trees, vegetables, cotton. Phosmet (organophosphate) GU, Class II, some tolerances in Broad spectrum insecticide, used foods changed in 1994 by EPA to control insect and mites on apples, ornamentals, vines; is used in some dog collars. Propargite (organosulfide) GU Acaricide used in many crops but Comite, Omite not USA Rosemary oil (rosemary essential Meets requirements of USDA Broad spectrum contact oil) Hexacide National Organic Program Exempt insecticide/miticide used in fruits, from FIFRA nuts, vegetables. Could be phytotoxic on some cultivars. Soybean oil (essential oil) Low acute toxicity to humans, generally recognized as safe Spinosad (macrocyclic lactone) Broad spectrum insecticide and Conserve miticide used on ornamentals and in greenhouses. Sulfur (sulfur) Cosan, Hexasul, GU, Check label for restrictions Fungicide and acaricide; used to Sulflox, Thiolux control plant diseases, gall mites, spider mites, used widely in food and feed crops, ornamentals, turf and residential sites; a fertilizer or soil amendment, mixing with oil can cause phytotoxicity

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Acaricides or Miticides, Table 1 (Continued) Name** (chemical type) Some trade names Triforine (piperazine derivative)

General Use (GU)*** Restricted Use (RU) RU, Class I

Wintergreen oil (contains methyl Exempt from FIFRA salicylate)

Potential use Fungicide used on almonds, apples, asparagus, berries, cheeries, hops, ornamentals, peaches, rose; also controls spider mites Used to control mites (Varroa) in honey bees; causes contact mortality and reduced fecundity when mites feed on syrup

* The list is based on chemicals currently registered in the USA, which can change as new information regarding environmental impact and human health effects become available. Inclusion in this list does not necessarily indicate that the products are effective acaricides; application methods and resistance levels in individual mite populations can affect efficacy. **Most have a variety of trade or other names, as well as different formulations, which can affect their toxicity. ***Restricted Use (RU) means that pesticides may be purchased and used only by certified applicators. Check with specific state regulations for local restrictions.

Mode of Entry 95 90

A pesticide can enter and kill mites as stomach poisons, contact poisons, and or as fumigants. A systemic acaricide is absorbed into a plant or animal and protects that plant or animal from pests after the pesticide is translocated throughout the plant or animal.

Chapla reciprocal F1 females

80 60 40 20

Bidart

10 5

Chemical Structure 101

102

103

ppm propargite

Acaricides or Miticides, Figure 6 This is a concentration-response curve showing the responses of a colony of Tetranychus pacificus resistant (Bidart) and susceptible (Chapla) to propargite (Omite). The mortality of adult females at different concentrations has been transformed into a straight line. The concentration-responses of the reciprocal F1 females in crosses between the susceptible and resistant populations are intermediate and similar.

Pesticides are classified as organic or inorganic. Inorganic pesticides do not contain the element carbon (but include arsenic, mercury, zinc, sulfur, boron, or fluorine). Most inorganic pesticides have been replaced by organic pesticides.

Source Organic pesticides include botanicals (natural organic pesticides) produced by plants (such as natural pyrethrums, nicotine, rotenone, essential oils such as those from the neem tree, soybean


oil). Essential oils are any volatile oil that gives distinctive odor or flavor to a plant, flower or fruit, such as lavender oil, rosemary oil, or citrus oil. Essential oils have been registered as pesticides since 1947 and at least 24 different ones are available in registered products. These are used as repellants, feeding depressants, insecticides, and miticides. Botanicals have relatively high LD50 values to mammals, so usually are considered safe to humans. Some newer pesticides are derived from microbes, such as avermectin or spinosad. Synthetic organic pesticides are commonly used in pest management programs and can be separated into groups based on their chemistry. The main groups are: chlorinated hydrocarbons (such as DDT and chlordane, which are banned from use in most parts of the world), organophosphates (such as malathion, parathion, azinphosmethyl), carbamates (carbaryl, propoxur), pyrethroids (permethrin, fenvalerate),and a variety of newer products with very different chemistries including nicitinoids, pyrroles, carbazates, and pyridazinones.

Insecticides as Acaricides Many insecticides have acaricidal properties. Sometimes an insecticide is more effective as an insecticide than as an acaricide (lower concentrations are required to kill the insect than are required to kill the mite species). Some products are more toxic (often for unknown reasons) to mites than to insects. We think that mites have the same fundamental physiological responses to toxic chemicals as insects, although mite physiology and responses to pesticides have been studied less often. Different mite species appear to respond differently to different products, which could be due to behavioral differences (feeding behavior, location on plant, activity levels), differences in cuticle thickness, differences in detoxification rates, or other biochemical, morphological or behavioral factors. Different

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formulations also can influence toxicity to different species of both insects and mites. Many insecticides are effective acaricides (or at least they were before resistance to them developed). For example, many OPs (such as azinphosmethyl, parathion, ethion, dimethoate) were toxic to spider mites until resistance to these products developed. Likewise, carbamates, formamides, and many pyrethroids have both insecticidal and acaricidal properties. Other products have both fungicidal and acaricidal properties. The reasons as to why these products are effective on particular taxonomic groups are generally unknown.

Acaricide Types Pesticide registrations change frequently so some of the materials listed here may be obsolete. Always check with state and federal authorities to be sure products containing these active ingredients are registered for use. Always read labels carefully and follow the directions completely.

Chlorinated Hydrocarbons Dienochlor (Trade name = Pentac) is a chlorinated hydrocarbon acaricide with long residual activity. It has been used in greenhouses and on outdoor ornamentals. Pentac cannot be used on food crops and has short residual activity when used outdoors. It has a rapid effect on mites, stopping their feeding within hours. Endosulfan and DDT have also been used as acaricides (as well as insecticides).

Essential Oils Soybean oil was first registered in 1959 for use as an insecticide and miticide. Three products currently are registered to control mites on fruit trees, vegetables and a variety of ornamentals. Soybean oil is not phytotoxic under most conditions. Many of these oils are approved for organic farming.

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Inorganics Sulfur is a good acaricide and fungicide, although it can be phytotoxic (cause plant injury), especially if plants are not well watered during hot weather. Sulfur is probably the oldest known acaricide. Sulfur (dusts, wettable p owders and flowable formulations) are usually highly effective acaricides for spider mites and rust mites, with two known exceptions. Spider mites in California vineyards (Tetranychus pacificus and Eotetranychus willamettei) developed resistance to sulfur, probably because sulfur was applied up to 20 times a season over many years to control powdery mildew. After a number of years, these spider mites became pests because they were no longer controlled by the sulfur which had been applied to control powdery mildew. A number of years later, a predatory mite called Metaseiulus occidentalis was demonstrated to have developed a resistance to sulfur. The resistance to sulfur in this natural enemy of spider mites is based on a single major dominant gene; once the predator became resistant to sulfur it became an effective predator of spider mites in San Joaquin Valley vineyards in California. The resistance to sulfur in M. occidentalis is unusual; even very high rates of sulfur are nontoxic to the resistant populations. Interestingly, populations of this predator collected from nearby almond orchards in California are susceptible to sulfur, indicating that populations are subjected to local selection and evolution. No genetic analyses have been conducted on the resistance to sulfur in the spider mites, so their mode of inheritance to sulfur resistance remains unknown. The biochemical mechanism of resistance is unknown for both spider mites and their predators.

Petroleum Oils Petroleum oils are excellent insecticides/acaricides/fungicides for integrated mite management programs and have been used in pest management programs for over 100 years.

Different types of petroleum oils are used with different molecular weights. Most oils used are distillations of petroleum, although some oils derived from plants (sesame, almond, citrus) are used. Crude petroleum oil is a complex mixture of hydrocarbons with both straight chain and ring molecules. Crude oil is separated into a range of products by distillation and refining. The lightest fractions include gasoline, kerosene, diesel and jet fuel. As these lighter fractions distill or boil, they are separated into different fractions. Spray oils are derived from the lighter lubricating oil fraction and distill at a temperature range of 600 to 900°C. Currently used petroleum oils in the USA are narrow-range oils and have had the waxes, sulfur, and nitrogen compounds removed. Labels on sprays usually describe the degree to which the sulfur compounds have been removed and the percentage of active oil. The sulfur compounds are likely to cause phytotoxic effects, so the degree of removal of these compounds (called the UR rating) is an important piece of information on the label and commonly is greater than 92%. The composition of oil should be greater than 60%. Since the mid-1960s, narrow-range horticultural oils have been used both as dormant or summer oil sprays. These highly refined and narrow range petroleum oils rarely cause phytotoxicity and increasingly are used for controlling both insect and mite pests on deciduous trees, citrus, and ornamental trees and shrubs. Oils have a wide range of activity against scales, mites, psyllids, mealybugs, whiteflies, leafhoppers, and eggs of mites, aphids and some Lepidoptera. Heavier dormant sprays are used to control overwintering pests in deciduous trees and vines. Summer oils are used to control pests during the growing season. Oil kills mites and their eggs by contact. The toxicity appears to be due to suffocation of the pest, although it may also be due to chemical effects. Oils block spiracles, reducing the availability of oxygen and suffocation occurs within 24 h. Penetration and corrosion of tracheae, damage to muscles and nerves may also contribute to the toxicity of oils. Oils are sometimes a repellent to pests. Once the oil


dries it is no longer toxic to most natural enemies; thus the very short residual activity of oil makes it a useful material for integrated mite management programs, although it also means that there is no residual toxicity to the pests. No resistance to oils has been reported in pest arthropods, including mites, perhaps because oils have a relatively short residual activity. Oils are easy to apply, relatively inexpensive, and safe to handle. They are relatively harmless to vertebrates, dissipate quickly after spraying, and leave little or no residue on crops. Oils man be used by organic farmers. A disadvantage to petroleum oils is that they have little residual activity and kill only upon contact, so thorough and precise coverage is necessary to achieve effective control. Phytotoxicity can occur even with these narrow-range oils, especially if plants are weakened or under moisture stress. Thus, applications should not be made during droughts, or periods of very high temperatures. Some varieties of plants are more susceptible to phytotoxicity than others, so caution should be taken when using oils for the first time on a particular crop or cultivar. Oils are not compatible with sulfur or some other pesticides, causing serious phytotoxicity problems.

Organosulfurs Tetradifon (Tedion) and propargite (Omite, Komite) are organosulfurs. These products contain sulfur as a central atom with two phenyl rings. Tedion is particularly toxic to mites, but has very low toxicity to insects. Organosulfurs are often ovicidal as well as toxic to active stages. Propargite was used for many years (more than 20) and appeared to some to be immune to the development of resistance in spider mite populations. However, propargite resistance has now developed in many populations of spider mites around the world. Propargite is less toxic to beneficial phytoseiid predators than to pest spider mites, and thus could be used in integrated mite management programs, although at high concentrations it also is toxic to phytoseiid predators.

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Organotins Cyhexatin (Plictran) and fenbutatin-oxide (Vendex) are examples of tin compounds that are primarily acaricides and fungicides. Plictran (cyhexatin) was introduced in 1967 and was widely used for many years before resistance developed in spider mites. Some people had assumed that the organotins were immune to resistance problems. The organotins were useful products because they were more toxic to spider mites than to phytoseiids and thus were very useful in integrated mite management programs. Fenbutatin-oxide (Vendex) is another organotin. These products were taken off the market in the USA due to concerns about safety.

Insecticides with Acaricidal Activity Organophosphorus Pesticides The organophosphates (pesticides that include phosphorus) are derived from phosphoric acid and are the most toxic of all pesticides to vertebrates. They are, in fact, related to nerve gases by structure and mode of action. Organophosphorus pesticides (OPs) are less persistent in the environment than the organochlorines such as DDT. Organophosphorus pesticides (such as azinphosmethyl, parathion, ethion, demeton, dimethoate) function by inhibiting important enzymes (cholinesterases) in the nervous system. Acetylcholine is the chemical signal that is carried across synapses (where the electrical signal is transmitted across a gap to a muscle or another neuron. After the electrical signal (nerve impulse) has been conducted across the gap by acetylcholine, the cholinesterase enzyme removes the acetylcholine so the circuit won’t be kept on. When OPs poison an organism, the OP attaches to the cholinesterase so it cannot remove the acetylcholine. The circuits then remain on because acetylcholine accumulates. This gives rise to rapid twitching of the voluntary muscles and to paralysis, which is can be lethal if it persists in the vertebrate respiratory system.

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Not all OPs are highly toxic to vertebrates; if the phosphorus is modified by esterification (adding oxygen, carbon, sulfur and nitrogen), six different classes of OPs can be produced. Some of these are relatively safe to vertebrates, such as malathion. The use of most OPs is being eliminated in the USA due to the Food Quality Protection Act.

Carbamates Carbamates (aldicarb, carbofuran, methomyl, propoxur) are derivatives of carbamic acid. The mode of action of carbamates is to inhibit cholinesterase. The carbamates were introduced in the 1950s. Carbaryl (Sevin) is one of the most popular products available to home gardeners for controlling a variety of insect pests and has low mammalian oral and dermal toxicity. Methomyl (Lannate) and aldicarb (Temik) are examples of other carbamates. Sevin is well known to induce outbreaks of spider mites after applications are made to control other pests. The outbreaks are due to two factors; (i) Sevin kills phytoseiid predators and other natural enemies of spider mites, and (ii) it stimulates reproduction of spider mites, a process called hormoligosis. Even very low doses of Sevin appears to act like a hormone to stimulate reproduction of the two-spotted spider mite Tetranychus urticae. It is likely that the use of carbamates also will be eliminated or greatly reduced in the USA due to the Food Quality Protection Act.

Formamides Formamides include chlorodimeform (Galecron or Fundal), amitraz, and formetanate (Carzol). These products are effective against the eggs of Lepidoptera and also against most stages of mites and ticks. The mode of action of these products is unclear, but thought to be due to the inhibition of monoamine oxidase, which results in the accumulation of compounds called biogenic amines.

Pyrethroids Many of the pyrethroids have acaricidal activity. Some (such as bioresmethrin, fenpropathrin and bifenthrin) are considered effective acaricides. Unfortunately, pyrethroids usually are very toxic to beneficial arthropods, including phytoseiid predators. These detrimental effects can be very long lasting because the residues persist a long time. Few have been found useful for integrated mite management programs for this reason. Laboratory selection of phytoseiids ( Amblyseius fallacis, Metaseiulus occidentalis, Typhlodromus pyri) for resistance to two pyrethroid insecticides has been successful. The pyrethroid-resistant strains were developed for use in apple pest management programs using both laboratory and field selection methods.

Pyrroles Pyridaben is a novel pyrrole pesticide that works as a mitochondrial electron transport inhibitor to block cellular respiration, causing pests to become uncoordinated and die. Can be used on both insects and mites.

Other Acaricides Azadirachtin This is a triterpenoid extracted from the seeds of the neem tree Azadirachta indica. Extracts include a combination of compounds, the proportion of which vary from tree to tree. Such variability in this natural product makes it difficult to predict the precise effect of the product when extracted by local people. Commercial products may be more consistent in their effect because they have been tested to confirm their quality and are blended to achieve a consistent product. Azadirachtin blocks the action of the molting hormone ecdysone.


Avermectin Avermectin is a natural product containing a macrocyclic lactone glycoside that is a fermentation product of Streptomyces avermitilus, which was isolated from soil.Avermectin is actually a mixture of two homologs, both of which have biological activity. Avermectin has insecticidal and acaricidal properties and is closely related to ivermectin, which kills nematodes. At appropriate rates, abamectin is less toxic to beneficial phytoseiids than to spider mites; it paralyzes active spider mite stages, but is not toxic to eggs. Avermectin has translaminar activity (meaning it is taken up by the plant tissue and subsequently by spider mites feeding on the plant tissues), but has a short residual toxicity to phytoseiids. Resistance to this product has been reported in some populations of spider mites. A resistant strain of M. occidentalis was obtained after laboratory selection, suggesting that resistance mechanisms may be present in field populations. The mode of action of avermectin involves blocking the neurotransmitter gamma-aminobutyric acid (GABA) at the neuromuscular junction. Mites that are exposed to abamectin become paralyzed and, although they do not die immediately, the paralyzed mites do stop feeding.

Clofentezine and Hexythiazox These are very interesting growth regulators of mites; they kill eggs (ovicides) of spider mites, but not the active stages of spider mites. The products have different chemistries, but both are nontoxic to phytoseiid mite eggs or active stages! In fact, the phytoseiid mite Metaseiulus occidentalis can be fed a diet consisting solely of spider mite eggs that have been killed with these products and the predator females reproduce and their progeny develop normally. This selectivity makes the products particularly useful for integrated mite management programs because predators can be maintained while suppressing spider mite populations. Unfortunately, resistance to these products has developed

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in spider mite populations in several locations around the world, including Europe and Australia.

Tebufenpyrad This is a phenoxypyrazole and has been evaluated under the trade name Pyranica in Australia, where it was shown to be useful in integrated mite management programs in apples because it is selective (relatively nontoxic) to phytoseiid predators.

Acaricides and Fungicides Benomyl is a carbamate that has been used primarily as a fungicide, but also has acaricidal properties. Benomyl is interesting because it acts as a sterilant of phytoseiid predators. Adult phytoseiid females treated with benomyl survive, but they do not deposit eggs. This product apparently disrupts spindle fiber formation in cells and interferes in the synthesis of DNA, resulting in females that are unable to reproduce.

Resistance in Mites Resistance to pesticides is an increasingly serious problem around the world. Resistance to one or more pesticides has been documented in more than 440 species of insects and mites. Spider mite and tick species have readily developed resistance to all classes of pesticides. Resistance is a decreased response of a population of animal to a pesticide or control agent as a result of their application. It is an evolutionary or genetic response to selection. Tolerance is an innate ability to survive a given toxicant dose without prior exposure and evolutionary change. Cross resistance is a genetic response to selection with compound A that generates resistance to both compound A and other compounds (B and C). Multiple resistance is resistance to different compounds due to the coexistence of different resistance mechanisms in the same individuals. Multiple resistances usually are

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generated by sequential or simultaneous selection by more than one type of pesticide.

Methods for Evaluating Resistance There are a variety of methods available for assessing resistance to pesticides in mites. The test method chosen will depend upon the goals of the researcher. Each method has strengths and weaknesses. Resistance is a genetically-determined change in the ability to tolerate a pesticide. Therefore, one must have at least two different populations to test – one that is putatively resistant and one that exhibits the normal, wild type response. Unless these two populations can be compared under identical laboratory conditions, it is difficult to document resistance because historical data are of questionable value in assessing whether a population is resistant. This is because it is very difficult to conduct identical bioassays in two different laboratories, even when attempts are made to use the same methods. Small differences in techniques can result in very large differences in toxicity data. For example, spider mites tested on smooth leaves may respond very differently than spider mites tested on the same plant species but on a variety with hairy leaves. Small differences in formulations and temperature also influence responses of mites to pesticides. Small differences in age or feeding status also influence toxicity responses. Most conclusions about resistance should be based on comparative data obtained by the same researcher under identical conditions. The apparent failure of a product to control a mite population under field conditions is NOT adequate evidence for resistance. Field failure is a reason to investigate further, but field failures can occur for a variety of reasons that have nothing to do with resistance. Failures could occur because the pesticide applicator may have mixed the product improperly, coverage may have been inadequate, the pH of the water used to mix the pesticide could have altered the toxicity of the product, and the product could have been old or degraded due to improper storage.

Slide Dip Bioassays Slide dip bioassays of adult female spider mites and phytoseiids have been proposed as a standard method for assessing resistance or tolerance. This method involves placing adult female on their backs on to double-sided sticky tape applied to glass microscope slides and dipping the slides into a specific pesticide concentration. This method has the virtue of being relatively rapid and easy to conduct. However, measuring toxicity to adult females after 24 or 48 h is not an appropriate assay for many pesticide types (for example ovicides, growth regulators). Also, the results probably bear little relation to the field toxicity of the product. It is very likely that many products are much more toxic to the mites using this assay than they would be under field conditions, where mites can feed and move around and coverage is rarely complete, so this method may give no information about whether the resistance level induced is relevant to field concentrations used. Leaf Dip or Leaf Spray Bioassays Leaf dip or leaf spray bioassays involve placing mites on leaf disks, which are then sprayed or dipped into a specific concentration of pesticide. This type of bioassay provides an exposure that is more similar that the mites would experience under field conditions and it is possible to measure survival, fecundity, and ability to successfully develop on pesticide residues. Whole Plant Bioassays This approach, which involves spraying the entire plant, is very realistic, unless the plants (and pesticide residues) are not exposed to sunlight or rain. Field Tests Field trials are the most realistic method for assessing resistance, but it can be difficult to determine why the predators or spider mites died (did other tolerant predators fly in and eliminate the pest?). If adequately replicated over time and space, field trials provide very relevant information. The relevance of application method (high or low volume), coverage,

Accessory Gland

and droplet size can be assessed. Unfortunately, field trials are the most expensive to carry out so the methods described above are often used to save time and funds.  Insecticides  Insecticide Toxicity  Insecticide Formulation  Detoxification Mechanisms in Insects  Pesticide Resistance Management  Pesticide Application

References Cranham JE, Helle W (1985) Pesticide resistance in Tetranychidae. In: Helle W, Sabelis MW (eds) Spider mites: Their biology, natural enemies and control, vol. 1B. Elsevier, Dordrecht, The Netherlands, pp. 405–421 Croft BA (1990) Arthropod biological control agents and pesticides. Wiley-Interscience, New York, NY Davidson NA, Dibble JE, Flint ML, Marer PJ, Guye A (1991) Managing insects and mites with spray oils. IPM Education and Publications, Statewide IPM Project, Publication 3347. University of California, Division of Agricultural Natural Resources, Oakland, California. EXTOXNET: [email protected] This site provides information about pesticides, including concepts in toxicology and environmental chemistry. It is a cooperative effort of

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the University of California-Davis, Oregon State, Michigan State, Cornell and the University of Idaho. Roush RT, Tabashnik BE (1990) Pesticide resistance in arthropods. Chapman and Hall, New York, NY

Accessory Cell A wing cell not normally present in the taxon.

Accessory Circulatory Organ Although the dorsal vessel (heart) is normally considered to be the organ responsible for blood circulation in insects, sometimes small sac-like structures are located at the base of appendages (antennae, legs, wings). These structures are capable of contractions independent of the dorsal vessel, and assist in circulation. This is also called “accessory pulsatile organ.”

Accessory Gland A gland associated with the male or female reproductive system, and producing substances associated with the sperm or eggs, respectively (Fig. 7). Male accessory glands produce such substances to

ovary ovariole calyx lateral oviduct spermatheca accessory gland median oviduct vagina

Accessory Gland, Figure 7 Diagram of the female reproductive system, as found in Rhagoletis (Diptera) (adapted from Chapman, The insects: structure and function).

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Accessory Vein

facilitate sperm transfer, as a barrier to further insemination, as a means of altering female behavior, and as a means of providing nutrition to the female. Females produce substances for packaging their eggs, adhering them to a substrate, and providing a protective coating over the eggs.

Accessory Vein An extra branch of a longitudinal vein. Such veins normally are designated by a subscript of “a.” Wings of Insects

 Sampling Arthropods

Acephalous The condition of lacking an apparent head. This term is usually applied to certain flies and wasps that lack a well-defined head.

Acerentomidae A family of proturans (order Protura).  Proturans

Accessory Hearts Pulsatile, sac-like organs that assist in circulation of the hemolymph into appendages such as the antennae, wings, and legs.

Accidental Host A host in which the pathogenic microorganism (or parasite) is not commonly found.

Accidental Species Species that occur with a low degree of consistency in a community type. Such species are not useful for community definition.

Acclimation The adaptation of an organism’ s physiological responses to existing environmental conditions. A nearly equivalent term is “acclimatization,” though acclimation may be a more rapid or laboratory-based phenomenon, whereas acclimatization is a long term, field-based phenomenon.

Accuracy A measure of the closeness of an estimate to the true mean or variance of a population.

Acetylcholine The synaptic transmitter substance found in the insect central nervous system. When released into the synaptic cleft, it is bound to a receptor, depolarizing the postsynaptic membrane and stimulating nervous excitation.

Acetylcholine Esterase An enzyme that breaks down acetylcholine after it is released into the synaptic cleft of insect neurons. Interference with acetyl choline esterase, as by exposure to some insecticides, results in prolonged stimulation of the nerves.

Achilidae A family of insects in the superfamily Fulgoroidae (order Hemiptera). They sometimes are called planthoppers.  Bugs

Aclerididae A family of insects in the superfamily Coccoidae (order Hemiptera).  Bugs

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera)

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera) marta goula University of Barcelona, Barcelona, Spain Acoustic signaling is found in many hemipteran families. It serves a variety of purposes, particularly defensive behavior such as repelling potential predators and signaling alarm or distress, but also for species spacing within a particular habitat, reproduction, and coordination of group actions. Vibratory signals for reproductive purposes may be produced by males and/or females, leading to aggregation to mate attraction, courtship and copulation. Non-receptive females may sing to reject copulation (male-deterring stridulation), as in the subfamily Triatominae (Reduviidae) and in Pentatomidae (e.g., Nezara viridula). The vibratory signals produced by many insect species cannot be heard by the human ear because the sounds are low frequency and generally transmitted by mechanical vibrations through the substrate, and not by the air. The study of acoustical communication has greatly progressed in accordance with improvement of recording and analyzing equipment, including the necessary computer software.

Production of Vibrational Signals and Songs Vibrational signals and songs are produced by stridulation (stridulatory device, stridulatory organs), by body vibration, or by a simple tymbal mechanism. Stridulation occurs widely in Heteroptera, and is the act of producing sound or vibration by rubbing together certain body parts. The first systematic survey of sound-producing devices in the Heteroptera was that of Handlirsh in 1900. To stridulate, usually both a movable and

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a stationary portion are needed. The movable part is called the plectrum or scraper. The stationary portion may be called the stridulitrum, file, strigil (strigile, strigilis) or lima (pl., limae). The stridulitrum is typically striated or finely tuberculated, and the plectrum is a structure with a well-defined lip or ridge, tubercles, or provided with spines. Different parts of the body may be involved to function as the stridulatory device. The forewing edge is most commonly used as a stridulitrum (file), while the hind femur is the most usual structure used as a plectrum (scraper). Other stridulitrum may be located in the head, associated with the mouth (labium, maxillary plate), the thorax (propleurum, metapleuron, prosternal groove), the wings (metathoracic wing vein, hypocostal lamina or articulatory sclerite, underside of clavus), the legs (forecoxa, mesotrochanter, tibia, femora), and the abdomen (sternum, the connexival margin, posterior margin of the pygophore). There are also a variety of locations for the plectrum or scraper: the rostrum, the legs (forecoxal cavity, coxal peg, hind tibia, and fore-, middle or hind femur) or the abdomen. Some stridulatory devices are present in several families, whereas others are only known from a few genera or even a single species. Examples of stridulation devices are that of the Corixidae (spinose area inside the front femur against the clypeus, genitalia against abdomen segments), Scutelleridae (wart-like, toothed tubercles in the hind tibia against the femur), Reduviidae (tip of the labium against a cross-striated furrow (Fig. 8) in the prosternal groove), some Pentatomoidea and Lygaeiodea (dorsal abdominal files against teeth on the under-sides of the hindwings), some Miridae, Lygaeidae, Largidae and Alydidae (hind femur against forewing edge) and some other Pentatomoidea (tubercles on the hind femora against strigose regions on abdominal sterna). Morphological differences in the stridulatory device may, in some cases, be related to differences in the songs emitted by either males or females, as

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Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 8 The stridulatory apparatus in Reduviidae: the tip of the labium is rubbed against a cross-striated furrow in the prosternal groove.

occurs in the burrower bugs (Fig. 9) Scaptocoris castanea and S. carvalhoi. In S. castanea, males have a longer stridulitrum than females. However, in S. carvalhoi the stridulitrum length does not differ between sexes. Instead, in S. carvalhoi the male stridulitrum has more teeth than in the female stridulitrum. There are no intersexual differences for this latter morphological trait in S. castanea. Differences in the stridulatory apparatus may be related to interspecific differences, with a specific diagnostic value. In the genus Triatoma (Reduviidae), it is possible to distinguish between T. guazy and T. jurbergi at any nymph stage or in the adults by studying the stridulatory sulcus (stridulitrum). As T. jurbergi is naturally infected with Trypanosoma cruzi, the causal protozoan of Chagas disease (American trypanosomiasis), identification of specimens along their whole life cycle is of great medical importance. In other instances, morphological differences in the stridulatory device do not cause differences in their song patterns. For example, in Reduviidae of the subfamily Triatominae, individuals of the same species have stridulatory grooves with different inter-ridge distances, though the frequency spectra and repetition rates are similar.

A tymbal is formed by abdominal tergal plates fused together and which vibrate over a hollow chamber within the abdomen. The tymbal is activated by muscular contractions and produces body vibrations that are low frequency. Tymbals have been found in Piesmatidae, Pentatomidae, Acanthosomatidae, Cydnidae, Lygaeidae, Coreidae and possibly Reduviidae, and similar vibration-producing mechanisms have been found in Plataspidae and Rhopalidae. Differences exist about precise abdominal parts and muscle contraction mechanisms among the tymbals of different families. For example, the des cription of the N. viridula tymbal follows: The first and second abdominal tergites are fused into a forward-backward movable tymbal-like plate that is loosely fixed, anterior and posterior, to the thorax and to the third abdominal tergum, by a chitinous membrane, and more firmly, laterally, to the pleurites. Longitudinal and lateral compressor muscles contract synchronously and in phase with these vibratory waves. All Heteroptera species investigated so far emit low frequency narrow-band signals by body vibration, and/or broadband signals produced by stridulation. For example, in Cydnidae and Pentatomidae, vibratory mechanisms produce a low frequency vibration (around 100 Hz), and the stridulatory vibration extends up to 10 kHz.

Reception of Vibrational Signals and Songs Although sound production is found quite widely in Heteroptera, it is not common to find structures specialized for sound reception. Sound reception in Heteroptera is possible due to the presence of either scolopophorous organs or tympanal organs. Scolopophorous organs are mechanoceptors, and they occur widely in insects. They are composed of sensory sensilla (scolopodia), which may be arranged in groups, and are distally attached to a membrane in the body wall or to the body wall itself. Scolopophorous organs may be located in


antennae (Johnston’s organ), legs (subgenual organ, joint chordotonal organ), thoracic pleura, or abdominal terga. Legs are the site of sensory organs that detect vibratory signals with highest sensitivity. For example, at the dorsal side of each leg of N. viridula there

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are four scolopodial organs: femoral, tibial, tarso pretarsal and subgenual organs. The receptor neurons may be low frequency (most sensitive between 50 and 100 Hz) or high frequency sensitive (there are two types: middle frequency neurons being sensitive around 200 Hz, and higher frequency

a

b

c

d

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 9 Interspecific differences in the stridulatory devices found in females of the burrower bugs Scaptocoris castanea and S. carvalhoi (Hemiptera: Cydnidae). Images a and b are S. castanea; images c and d are S. carvalhoi. Images a and c show the stridulitrum in the postcubital vein of the hind wings (scale bar = 100 µ); images b and d show the central section of the stridulitrum, showing details of the teeth (scale bar = 10 µ) (adapted from Čokl et al (2006) Physiol Entomol 31:371–381).

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neurons sensitive around 700–1000 Hz). Also, the Johnston’s organ of N. viridula has several vibratory sensitive organs which respond in the frequency range between 30 and 100 Hz. When standing on its host plant, the male of N. viridula, by different combinations of legs and antennae, may compare the vibratory signals on two branches of the host plant, and choose the best one in order to locate the singing female. The most probable mechanism underlying resolution of direction by vibratory cues (vibratory directionality) may be time-of-arrival differences (perception of vibratory signals by two different receptors in the insect). For example, when legs of the receptor bug are separated by 2 cm, a time-of-arrival difference between 0.125 and 0.250 ms is created, very close to that found in scorpions, where vibrational directionality is well known. Reduviidae also receive vibratory signals via legs and antennae. Fewer data are available on leg vibratory receptor organs in other land bug species. Among land bugs, no sensory organs for airborne sound have been found. Tympanal organs have been found in the mesothorax of the Corixidae, and are in contact with the physical gill air bubble. They are able to catch airborne sounds, and to respond to stridulation frequencies produced by conspecific bugs.

Transmission of Vibratory Signals and Songs Independent of their mode of production, vibrational signals may be transmitted by the substrate (substrate-borne vibrations) or by the air (airborne vibrations). The signals may travel a short or long distance, or travel at a low or high speed. Low-frequency components are more suitable for longer-range communication through plants. Low frequency signals travel longer distances, but slowly; high frequency signals travel shorter distances, but quickly. Long-range vibratory songs are associated with pre-mating calling and vibrational orientation, and close-range vibratory songs are associated with courting rivalry and repelling.

Substrate-borne vibrations are less costly to the emitter. Also, substrate-borne vibrations are more far-reaching signals for intraspecific communication and not easily perceived by a potential predator or parasitoid. Usual substrates to transmit vibrational signals are plants or soil. The characteristics of plants as transmission media for insect-produced vibrations have been described, and in many respects they determine signal production and the mode of reception. Depending on the physical properties of the host plant, the vibratory signals are transmitted effectively or not. Vibrations can be transmitted all along the stem, but the physical properties of a plant (e.g., elasticity, water content) affect resonance of insect vibrations. For transmission through plants, insects commonly emit broadbanded-mixed stridulatory and vibratory signals. Higher-frequency signals produced by stridulation are less relevant for longdistance communication through plants. However, narrow-band and low frequency songs are efficient in long-distance communication when well tuned to the resonant spectra of their host plants. The vibrational pulse reflects when attaining both the root area and top of the plant, and reflected waves travel up and down the stem several times. Reflections change the patterns of the input signal. Abiotic factors (temperature, rain, wind) may significantly modify plant resonance, masking insect vibratory signals and thus the effectiveness of the signal. Plant-borne vibrations seem to be important in the success of group-living, herbivorous insects for locating and remaining in a group of conspecifics, for locating food resources, and to avoid predation. Also, small insects that are not able to emit airborne sounds efficiently at low frequencies in many cases communicate with vibratory signals transmitted through plants. In the stink bug Nezara viridula (Pentatomidae) (Figs. 10 and 11), a species which has become a model for all Pentatomorpha in relationship to acoustical communication, its vibratory signals were recorded and described first as airborne sound. However, further investigations showed that their most important mode of transmission is as


substrate-borne vibrations. In N. viridula, a male could perceive a female calling in a Cyperus stem 2 m away from him, mechanically coupled only by roots and the surrounding earth. Below the leg of the singing bug, the intensity of signals was about 4 mm s–1. On the bottom of the same stem (a distance of 80 cm) it decreased to around 3 mm s–1, and at the place of the receiving bug, 200 cm away, it was approximately 0.5 mm s–1. When transmitted through the soil, signals travel a shorter distance and are more attenuated than when transmitted through a plant stem. For example, in Scaptocoris species (Cydnidae) the velocity

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 10 Oscillograms of songs emitted by males and females of the southern green stink bug, Nezara viridula (Pentatomidae) (adapted from Čokl, Virant-Doberlet (2003) Annu Rev Entomol 48: 29–50).

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of soil transmitted signals varied between 1.5 and 12.9 ms-1 at a distance of 0.5 cm.

Acoustic Characteristics of Vibrational Signals A vibrational signal may be characterized by its temporal (pulse train duration, repetition times, inter-pulse intervals) (Fig. 12) and spectral characteristics (dominant frequency). All of these characteristics may be measured by the receptor insect, who may modify its behavior in response to the message. The dominant frequency of signals produced by the vibratory mechanism lies between 50 and 200 Hz in most Heteroptera. Between species, songs differ in their time structure and amplitude modulation of their units. On the other hand, spectrally and temporally different pulse trains trigger the same male behavior in N. viridula. In Rhodnius prolixus (Reduviidae), the maledeterring call has a main carrier frequency of about 1500 Hz, and the disturbance stridulation has a main carrier frequency of about 2200 Hz. In Rhinocoris iracundus (Reduviidae), low-frequency components of carrier frequency below 200 Hz are exchanged with frequency-modulated stridulatory components whose dominant frequency lies between 1 and 2 kHz. In Triatoma infestans (Reduviidae), distress songs have a peak of frequency between 700 and 800 Hz, although in other reduviids the carrier frequency may reach about 2000 Hz. In N. viridula, dominant frequencies between 80 and 150 Hz were found in songs either as airborne sounds, or substrate or body vibrations. Body vibrations are around 100 Hz, and lie close to the range of best frequency sensitivity of low frequency receptor cells.

Specificity and Variability of Vibratory Signals Sounds, especially those involved in the reproductive process (attraction, courtship, copulation),

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Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 11 Laser vibrometer recordings taken from a plant fed upon by Nezara viridula showing the pattern of recordings at various distances (in cm) from the point of stimulation (adapted from Miklas et al (2001) J Insect Behav 14: 313–332).

Duration (D)

Inter pulse trains interval (IPI)

Repetition time (RT)

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 12 Temporal parameters of a vibratory signal (adapted from Miklas et al (2003) Behav Process 61: 131–142).

can be very complex and highly species-specific, and may be used as taxonomic characters of land bugs. In contrast, signals are much less specific when they provide information about enemies, rival mates, or serve as distress (disturbance or alarm) signals. Females of N. viridula sing to trigger the male approach, and to evoke emission of the male courtship song. Females coming from populations of different geographic origin emit different calling songs, which can be differentiated by males. Females of N. viridula may emit a song that rejects copulatory attempts of males and stops their courting, and this is also known in the reduviid Rhodnius prolixus. The courtship songs of both males and females in different populations are not markedly different, but the calling songs


may differ in some features and may be the source of reproductive isolation among populations. Nezara viridula produces four different species and sex-specific songs, and two of them play a vital role in mate location. There is song variability within populations (inter-individual variability). To assess those differences, the temporal song (pulse train duration, repetition times, inter-pulse intervals) and spectral song characteristics (dominant frequency) may be measured. Males usually show a preference for the females of their own population, although they may recognize females from other populations as potential partners. In Tritoma infestans, stridulation songs differ in their syllable durations, repetition rate and main carrier frequency, depending on the song function. Differences come from rubbing their rostrum (scraper) at different speeds on the prosternal file. Also in Rhodnius prolixus, the different frequency between deterrent and disturbing signals can be explained on the basis of a different rubbing velocity by the proboscis against the prosternal stridulatory organ (Fig. 13). In Scaptocoris carvalhoi and S. castanea (Cydnidae), two sympatric burrower bugs, high individual variation of the dominant frequency was observed in both male and female emissions (Fig. 14).

Vibratory Signaling in the Families of Heteroptera Vibratory signaling has been reported in several Dipsocoromorpha and Leptodomorpha, but has been better studied in the following families: Veliidae (Gerromorpha), Nepidae, Corixidae, Notonectidae (Nepomorpha), Reduviidae, Miridae, Tingidae, Nabidae (Cimicomorpha), Aradidae, Acanthosomatidae, Cydnidae, Pentatomidae, Scutelleridae, Tessaratomidae, Thaumastellidae, Colobathristidae, Lygaeidae, Piesmatidae, Largidae, Alydidae, Coreidae, Rhopalidae (Pentatomorpha) (Figs. 15 and 16). Selected examples follow:

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Oscilloscope Video camera

Accelerometer

VCR

Amplifier

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 13 Experimental setupused to study substrate-borne signals produced by stridulation in Rhodnius prolixus (Hemiptera: Reduviidae). The accelerometer generated a signal with voltage proportional to the instantaneous acceleration of the moving object, electrical signals were amplified and monitored by an oscilloscope, then this information was stored in the sound track of a videotape. Also, the behavior of the bugs was simultaneously videotaped (adapted from Manrique, Schilman (2000) Acta Trop 77:271–278).

Corixidae In Corixidae, males or both sexes use speciesspecific sound for mate attraction and in courtship. The sounds are produced by stridulation, i.e., rubbing together specially modified parts of the body, or the partner’s body.

Notonectidae In Notonectidae, males produce species-specific courtship sounds by rubbing roughened parts of their front tibiae and femora against a special stridulatory region at the base of the rostrum (Fig. 17). In genus Buenoa, the sound can be heard at a distance of several meters. While next to the female, but before clasping her, the sound pattern can change.

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Acoustical Communication in Heteroptera (Hemiptera: Heteroptera) Scaptocoris carvalhoi Male Female

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Scaptocoris castancea Male Female

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Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 14 Vibratory emissions of male and female burrower bugs Scaptocoris carvalhoi (above) and S. castanea (below) (Hemiptera: Cydnidae). A and B designate the two types of female song found in S. carvalhoi. Time scales are marked below oscillograms (adapted from Čokl et al. (2006) Physiol Entomol 31:371–381).

Reduviidae Distress (disturbance or alarm) signals in Reduviidae may be produced either as nymphs or adults (males and/or females). In Panstrongylus rufotuberculatus (Reduviidae), stridulation occurs only under conditions of extreme provocation. Its sound is audible by the human ear, which is unusual among stridulating Triatominae, and is similar to the sound of sandpaper scraping wood. The tip of the rostrum is rubbed along the transversely ridged prosternal groove with an anterior-posterior movement; the return stroke (posterior-anterior) is silent. Stridulation lasts for about 5 min, although the insect remains immobile when held for a longer time. In a

silent environment, the sound is audible at about 1 m away. A disturbance call has been described in the following triatomine species: Dipetalogaster maxima, Triatoma infestans, T. guasayana, T. sordida, Panstrongylus megistus and Rhodnius prolixus. In the spined assassin bug, Sinea diadema, agonistic interactions between adult females may be resolved by stridulation in 33% of the cases. Stridulating individuals retreated more often than their non-stridulating opponents, indicating that stridulation may be a startle mechanism employed by temporarily disadvantaged individuals to escape from encounters. Together with other signs, stridulations provide information on the identity and relative fitness of the opponent.


Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 15 Artabanus lativentris (Hemiptera: Aradidae): (above) ventral view of abdomen, with file (stridulitrum), (below) hind leg with detail of scraper (plectrum) in the interior surface of the hind tibia (adapted from Schuh and Slater 1995 True bugs of the world (Hemiptera-Heteroptera): classification and natural history. Cornell University Press, Ithaca, NY, 335 pp).

The acoustic repertoire of the ambush bug, Phymata crassipes, is quite large and may be displayed by females, males or nymphs. Its vibrational songs may be emitted in response to, and alternating with, calls from conspecifics, or even human speech or whistle. Sound emission is related to disturbance, interaction with other males and females, or courtship. Signals are produced by locomotory, stridulatory and/or vibratory mechanisms. Airborne signals directly or indirectly stimulate vibrational receptors. Bugs within a group respond to each other only via substrate, even in close proximity.

Miridae Although a stridulatory device has been described in several tribes and subfamilies, the functions of acoustical communication in Miridae are still unknown.

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Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 16 Phyllomorpha laciniata (Hemiptera: Coreidae): (above) dorsal view of pronotum with scraper (plectrum) at its margin, (below) detail of spines of scraper (adapted from Moulet 1995 Faune de France 81).

Tingidae In the tingid Corythuca hewitti, vibrational signaling during group movements may occur as groups of nymphs are attended by a female. It has been reported that a disturbance of the leaf where C. hewitti aggregated caused feeding to stop and dispersal by the bugs, with occasional stopping of the bugs to vibrate the abdomen in a vertical plane, a behavior followed by conspecifics.

Cydnidae In cydnids, the low species and sex specificity of pure stridulatory signals indicates that these vibratory emissions may play a role in disturbance (defensive) behavior, as in Tritomegas bicolor. Stridulatory signals are also related to aggregation or some other unspecific behavioral context. Cydnid bugs engage in rival singing and also distress (disturbance or alarm) signals, either as nymphs or adults (males and/or females). Courtship, acceptance and rivalry songs show higher specificity and in most cases are

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of the emitted signals and the uniformity of songs indicate that calling and courtship may be mediated by signals of other modalities. The lack of low frequency signals may be explained by the direct contact of the bug with soil, which mechanically prevents free vibration of the abdomen.

Pentatomidae

Acoustical Communication in Heteroptera (Hemiptera: Heteroptera), Figure 17 Male Anisops megalops (Hemiptera: Notonectidae): (above) foreleg with detail of scraper (plectrum) in the interior surface of the fore-tibia, (below) lateral view of the head with file (stridulitrum) on the labium (adapted from Schuh and Slater 1995 True bugs of the world (Hemiptera-Heteroptera): classification and natural history. Cornell University Press, Ithaca, NY, 335 pp).

roduced by low frequency body vibration and/or p by stridulation. Tritomegas bicolor produces courtship, mating, and male rivalry calls by stridulation and body vibration. In Sehirus luctuosus, the male’s courtship call is produced by body vibration, giving a drumming song. Two types of speciesspecific male courtship songs, produced by stridulatory and vibratory mechanisms, have been described. The first type triggers female response, a species-specific agreement song. The second type stimulates pair formation. In the group-living species of genus Scaptocoris, the absence of low frequency components

Pentatomid bugs engage in rival singing. For example, Nezara viridula and Rhapigaster nebulosa may alternate rival songs until one or both stop singing, and in P. lituratus, males perform rival singing. Vibrational directionality has been demonstrated in host or prey searching in the predatory stink bug Podisus maculiventris. The general pattern of singing during pre- mating behavior is similar for all Pentatomoidea. Calling starts with the emission of the female calling song, which triggers males to respond with calling and courtship songs, activates them to walk on the plant, and enables directional movement toward the female. Alternation of male and female songs may result in more or less complex duets, as is the case in N. viridula. Nezara viridula vibrates its body as part of intersex communications (courtship, directional cue for locating the mate, mate recognition), which implies that substrate-borne signals are highly species-specific. The female song causes the male to walk, to respond with the calling and courtship songs, and to approach the source of the song with characteristic search behavior. In contrast, females show no reaction to vibratory stimulation and no vibrational directionality.  Insect Acoustics  Cicada Acoustics  Vibrational Communication

References Čokl A, Virant-Doberlet M (2003) Communication with substrate-borne signals in small plant-dwelling insects. Annu Rev Entomol 48:29–50

Acoustic Communication in Insects

Čokl A, Nardi C, Bento JMS, Hirose E, Panizzi AR (2006) Transmission of stridulatory signals of the burrower bugs Scaptocoris castanea and Scaptocoris carvalhoi (Heteroptera: Cydnidae) through the soil and soybean. Physiol Entomol 31:371–381 McGavin GC (1993) Bugs of the world. Blandford, London, UK, 192 pp Miklas N, Čokl A, Renou M, Virant-Doberlet M (2003) Variability of vibratory signals and mate choice selectivity in the southern green stink bug. Behav Process 61:131–142 Reyes-Lugo M, Díaz-Bello Z, Abate T, Avilán A (2006) Stridulatory sound emission of Panstrongylus rufotuberculatus Champion, 1899 (Hemiptera: Reduviidae: Triatominae). Braz J Biol 66(2A):443–446 Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera – Heteroptera): classification and natural history. Cornell University Press, Ithaca, NY, 335 pp Wheeler AG Jr (2001) Biology of the plant bugs. Cornell University Press, Ithaca, NY, 507 pp

Acoustic Aposematism (Clicking) by Caterpillars Adult Lepidoptera are well known to perceive sound, such as the ultrasonic cries of insectivorous bats. Some even produce sounds that are used for social communication. Less well known is the sound production and reception of larvae. Some caterpillars employ vibrational signals with ants (e.g., Lycaenidae and Riodinidae), communicate about space with conspecifics (e.g., Gracillariidae), or detect insect predators or parasitoids (e.g., Noctuoidea and Gracillariidae). However, “clicking” sounds are an audible sound produced by caterpillars of silk moth (Saturniidae) and hawk moth (Sphingidae). This noise has also been described as “squeaking” or “crackling,” and originates with the mandibles. Defensive sounds are usually categorized as startle or warning behaviors; startle sounds warn a potential predator, causing momentary hesitation and escape of the potential prey, whereas warning sounds alert a potential predator that it is inadvisable to attack. Associated with the clicking sound is regurgitation behavior, and both actions follow disturbance of the larva. Regurgitant usually is adverse to predators, and is a widespread defensive behavior among insects. Thus, clicking is thought to warn potential

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predators of an unpleasant experience if predation is attempted, but it is also possible that clicks function as startle sounds, allowing escape. This latter explanation seems unlikely, however, as caterpillars usually move very slowly, so escape is not very likely.  Acoustic Communication in Insects  Vibrational Communication

Reference Brown SG, Beottner GH, Yack JE (2007) Clicking caterpillars: acoustic aposematism in Antheraea polyphemus and other Bombycoidea. J Exp Biol 210:993–1005

Acoustic Communication in Insects allen sanborn Barry University, Miami Shores, FL, USA Sound is used by a wide variety of insects for diverse purposes. It is difficult to evolve an acoustic communication system. There must be modifications to produce sound, transmit the sound in the environment and modify the sound to specific biological purposes, as well as the evolution of structures that will receive and decipher the signals. Arthropods are one of only two major groups of animals (along with the vertebrates) that have evolved acoustic communication and insects are the primary group of arthropods to exhibit acoustic behavior. At least ten orders of insects possess species that produce acoustic signals.

Sound Sound is generated by causing the repeated compression and rarefaction of an elastic medium. The waves of compression produced will then travel through the medium to the receptor or target. The medium can be air, water or a substrate – so sound also encompasses vibrations. As the sound energy travels through the environment, it is modified

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by various interactions with the components of that environment. In addition, sound waves are reflected as they move through any environment. This bending of sound waves can initiate interactions among the waves. The signal begins to deteriorate as a result of these wave interactions and with the variations in the signal initiated due to temperature and humidity. Acoustic energy is also lost as it is absorbed by structures in the environment and as a result of spherical spreading from the sound source. The loss of signal integrity due to these environmental interactions is termed the excess attenuation of the signal. The amount of excess attenuation varies with the habitat and the original signal properties. To complicate matters, the small size of insects requires that they use high frequencies (Fig. 18) to transfer energy efficiently to the signal. This will limit the range of a given signal because higher frequencies attenuate more rapidly in the environment. To use lower frequencies, insects must modify their bodies or behaviors to increase the efficiency of sound production. For example, tree crickets (Gryllidae) create a baffle by inserting their body in a leaf

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to decrease the acoustic short circuiting of a small dipole sound source, mole crickets (Gryllotalpidae) dig burrows which act as loudspeakers that amplify and direct their calls skyward, and the hollow abdomen of male cicadas (Cicadidae) acts as a resonating structure to amplify the acoustic signals produced by the tymbals. The sound producing systems of insects are generally vibrating structures. These structures are necessary because muscles cannot contract rapidly enough to produce high frequency sounds. The sound generating structures vibrate multiple times for each muscle contraction, so the sound producing systems act as frequency multipliers. Once the vibrations are initiated, the sound can be modified by attached resonant structures. There are many different schemes that can be employed to describe insect calls. The variety of sound production mechanisms has led to a variety of terminologies. No one terminology has been successful in describing the different sound production mechanisms or phylogenetic relationships of insects. When sounds are recorded and analyzed in any acoustic work, each analysis of acoustic signals in

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Acoustic Communication in Insects, Figure 18 Acoustic signal produced by the cicada Beameria venosa (Uhler). (a) Sonogram of calling song illustrating energy distribution of the call. Middle trace is an oscillogram illustrating the temporal pattern of the call. (b) Expanded oscillogram to show individual sound pulses within the call.


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insects should provide a detailed description of the terminology used to describe the signals, and illustration of the terminology on any oscillogram or sonogram in the work.

Sound Production There are several different types of sound production mechanisms that have evolved in insects. The relatively low muscle contraction frequency means that additional structures had to evolve in order to produce the high frequency sounds that small body size will require to generate acoustic signals efficiently. The primary mechanism used by insects to produce sound is a stridulatory apparatus. The chitinous exoskeleton and jointed appendages of insects are preadapted for modification into stridulatory apparati. Each stridulatory apparatus is composed of a file and plectrum or scraper. The file is generally a row of small cuticular teeth that is rubbed against a ridge or blade (the plectrum) on some other body part (Fig. 19). The teeth are bent as they catch on the plectrum and pop forward as they release from the plectrum. The release causes the teeth to vibrate alternately compressing and expanding air molecules producing sound. In general, these vibrations will occur in a single plane, resulting in a dipole being formed that produces an asymmetrical sound field at close range. The joints and exoskeleton of insects have permitted stridulatory apparati to evolve in many locations on the body. There are file and scrapers found between antennal segments (Phasmatodea), separate mouthparts (Orthoptera), head and thorax (Coleoptera), abdominal segments (Hymenoptera), wings and thorax (Lepidoptera, Hemiptera), body parts and legs (Hemiptera, Orthoptera), legs and wings (Orthoptera, Lepidoptera, Coleoptera), legs and legs (Thysanoptera, Hemiptera), between wings (Orthoptera), and between segments on the genitalia (Lepidoptera, Hemiptera). A tymbal organ is a specialized sound production organ. It is a ribbed, chitinous membrane attached to a tymbal

Acoustic Communication in Insects, Figure 19 Stridulatory apparatus of the cicada Tettigades undata Torres. The file (illustrated) is located on the mesothorax in this group of cicadas. The plectrum is located on the tegmina. Sound pulses are p roduced as the tegmina is rubbed over the series of m esothoracic ridges.

muscle (Fig. 20). The tymbal buckles as the tymbal muscle contracts. Sound pulses are produced when the tymbal buckles, when individual ribs buckle and potentially when the tymbal returns to its relaxed position. The unbuckling of the tymbal is assisted by the resilin within the tymbal. The resonant frequency of the tymbal determines the frequency of the sound pulses produced. Additional structures such as the opercula, tymbal covers, various muscles and the abdominal air sacs can modify the sound produced. The abdominal air sacs can become rather large as in the bladder cicada Cystosoma saundersii Westwood whose abdomen is so large, to resonate at a low frequency, that the male has difficulty flying. The tymbal is a common organ in the Hemiptera and acts as the ultrasonic pulse generator in the Lepidoptera. Percussion is another mechanism of sound production used by insects. Crepitation, a clicking sound produced by the wings, is another percussion mechanism in insects. The wings are clapped together or banged on the substrate to produce a sound pulse in some Hemiptera. It is relatively rare for airborne signals which are generally produced as a by-product of flight. The wings may strike each other or the legs

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production in insects. This method of sound production has been described in a number of insects, most notably the Madagascan hissing cockroach (Gromphadorhina portentosa [Schaum]), the Death’s Head hawk moth (Acherontia atropos [L.]) and some African Sphingids (Lepidoptera). In addition to the airborne signals produced by acoustic insects, it has now been shown that vibrational signals are also produced by sending information through the substrate. These vibrational signals are primarily produced by tremulation but also can be important in deciphering an airborne signal, particularly at close range to the sound source. Vibrational signals have been identified in members of the Neuroptera, Diptera, Hemiptera, Plecoptera, Coleoptera, Orthoptera, Mecoptera, Raphidioptera, Lepidoptera and Hymenoptera. Acoustic Communication in Insects, Figure 20 Tymbal organ of the cicada Beameria venosa (Uhler). The internally attached tymbal muscle buckles the tymbal to produce a sound pulse.

during flight-producing sound pulses as in the acridid grasshoppers (Orthoptera). However, specialized percussive sound production systems have evolved. A castanet is found on the costal margin of the tegmina in some moths (Lepidoptera) which produces a pure tone when struck. The acridid grasshopper Paratylotropidia brunneri Scudder can snap their mandibles together to generate sound. Percussion has been observed in Hemiptera, Isoptera, Plecoptera, Lepidoptera, and Orthoptera. Tremulation is the vibration of unspecialized body parts to generate sound. The abdomen is often moved dorso-ventrally or laterally to send vibrations through the legs to the substrate. This mechanism has been well studied in the lacewings (Neuroptera). Wing vibrations can also be used to send information over short distances. This type of signal is produced by members of the Diptera (flies and mosquitoes) and Hymenoptera. The expulsion of tracheal air is the final and relatively rare mechanism of insect sound

Sound Reception A receptor for acoustic signals is necessary for a communication channel to exist. Because sound is produced by changing air pressure, a modified mechanoreceptor is needed to sense the acoustic information. The receptors can be classified as either a pressure detector or a particle detector. Pressure detectors are membranes that bend when pressure is unequal on the two sides of the detector. Particle detectors are long structures that move when impacted by many particles moving in the same direction. The movement of the particle detector alternately stretches and compresses sensory cells at the base of the organ. The primary type of pressure receptor organ is a tympanum, which has evolved independently in at least eight orders of insects. Tympana are generally a thin membrane system stretched over a closed cavity. The tympanum bends away from the side of higher pressure setting up oscillations as the sound waves strike the membrane. Each tympanum has a resonant frequency based on its thickness, size and shape. The resonant frequency is generally tuned to the carrier frequencies of the communication channel to increase the efficiency of information transfer.


The tympana are associated with other mechanoreceptor organs to transduce the signal for the nervous system. As the tympana oscillate, vibrations are sent to various types of receptors, generally a specialized chordotonal organ called a scolopidial organ, which act as the input site to the central nervous system. There can be elaborate structures associated with the tympana to transduce energy into the central nervous systems such as the crista acoustica of the crickets and katydids (Orthoptera) and Müller’s organ of locusts (Orthoptera), which provides frequency discriminating abilities. These pressure receptors are generally found in pairs, one on each side of the body. This provides an animal with a means to determine the direction from which the sound originated. The sensory structures for vibrational signals are trichoid sensilla generally found on the feet or cerci or through specialized subgenual and metatarsal organs located in the legs. The subgenual organs are located just distal to the femoral-tibial joint in all six legs to promote detection and directional hearing. They are similar to tympana in that they are chordotonal organs but lack the tympanal membranes and tracheal air sacs of the tympanal system. Particle receptors are generally specialized structures found in specific groups of insects. For example, female fruit flies (Diptera) sense the courtship signals produced by the male with a special antennal segment called an arista. Male mosquitoes and midges (Diptera) have plumose antennae which detect the species-specific wing beat frequencies produced by females. Johnston’s organ is a more complex chordotonal organ found in the antennal pedicel of some Diptera and Hymenoptera which is stimulated by the vibration of the antennal flagella. The long bristles and antennae provide a mechanical advantage to the sensory cells increasing the sensitivity of the receptor.

Functions of Acoustic Signals Sound has many potential benefits in that the signals can be used day or night, can be modified quickly, and can travel a significant distance even if

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conditions are not optimal for other signal pathways. However, sound is energetically costly to produce and advertises your position to potential predators as well as potential mates. Even with these potential problems, insects have evolved diverse functions for acoustic signals. Acoustic signals are used for a variety of purposes in insects including sexual signaling, courtship signals, aggression, social recruitment and defense. A primary function of acoustic signals is as an intraspecific communication channel. Sounds are used to attract mates and to isolate species reproductively. Each species has a characteristic call that can prevent related species from cross mating. The calls produced by individual signalers can be compared by receivers providing the opportunity to select a mate who is producing a call that exhibits specific characteristics. This is particularly true when callers have congregated into localized areas, which is another function of acoustic signaling. Mates may be selected based on the number of calls, the temporal patterns, loudness, etc. The specific characteristics used by a given species are usually chosen based on their ability to demonstrate the viability of the caller. Duets between individuals (either intrasexual or intersexual) can also act as mechanisms to determine mate choice. The signals often change as potential mates approach. These courtship sounds are modified advertisement calls which provide further opportunities for mate assessment. Acoustic signals can also be used intraspecifically to space individuals in the environment, as aggression signals, or as competitive signals to jam the signal of a neighbor. Eusocial insects use acoustic signals as warnings, to recruit a defensive response within the colony, and to recruit foragers to specific food sources. Predator deterrence is another significant function of acoustic signals. The loud sounds produced by many insects (e.g., cicadas [Hemiptera]), can startle a potential predator giving the insect a chance to escape. The percussion sounds produced by acridid grasshoppers (Orthoptera) are thought to be defensive displays. Sound production has evolved specifically for this anti-predator

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function in click beetles (Coleoptera). The acoustic systems that use air movement in the Death’s Head moth (Lepidoptera), cockroaches (Blattodea) and grasshoppers (Orthoptera) also have anti-predator functions. Moths (Lepidoptera) have evolved a sound production system that is used to jam the ultrasonic signals of the bats that prey upon them. The arctiid moths emit ultrasonic pulses as bats approach which act to confuse the bat as to the exact location of its target. This gives the moth a chance to escape while the bat circles around for another attempt at capturing the insect. These pulses may also have an aposomatic function warning bats of a potentially distasteful meal. Insects have also evolved specialized acoustic receptors as a means of avoiding predation. Bat-detectors have evolved independently in geometrid, noctuid and hawk moths (Lepidoptera), lacewings, (Neuroptera), praying mantises (Mantodea), beetles (Coleoptera), crickets, locusts and katydids (Orthoptera). These batdetectors provide an early warning system for the insects that a bat is nearby giving the insect a chance to escape before the bat can sense an insect in the vicinity.  Sound Production in the Cicadoidea  Acoustic Aposematism  Drumming Communication and Intersexual Searching Behavior of Stoneflies (Plecoptera)

References Bailey WJ (1991) Acoustic behavior of insects, an evolutionary perspective. Chapman and Hall, London, UK, 225pp Drosopoulos S, Claridge MF (eds) (2006) Insect sounds and communication: physiology, behavior, ecology and evolution. CRC Press, Boca Raton, FL, 532 pp Elliot L, Hersberger W (2007) The songs of insects. Houghton-Mifflin Company, Boston, MA, 228 pp Ewing AW (1989) Arthropod bioacoustics: neurobiology and behavior. Comstock Publishing Associates, Ithaca, NY, 260 pp Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, Chicago, IL, 531 pp

Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, New York, NY, 414 pp

Acrididae A family of grasshoppers (order Orthoptera). They commonly are known as shorthorned grasshoppers.  Grasshoppers, Katydids and Crickets

Acriology The study of grasshoppers, katydids, crickets and their relatives (Orthoptera). This is sometimes expanded to include the orders of insects related to Orthoptera (the Orthopteroids) such as cockroaches (Blattodea), mantids (Mantodea), stick insects (Phasmatodea), earwigs (Dermaptera), and gladiators (Mantophasmatodea).  Classification  Grasshoppers, Katydids and Crickets

Acrobat Ants (Hymenoptera: Formicidae) A term applied to ants of the genus Crematogaster. Typically they are small, shiny brown or black, and possess a pedicel with two nodes. They elevate the gaster (tip of the abdomen) over the thorax or head when alarmed. Acrobat ants usually are found in association with wood or trees, including the tunnels of termites and wood boring beetles. They are omnivorous and tend aphids. Their bite can be painful.  Ants (Hymenoptera: Formicidae)  Ant-Plant Interactions

Acroceridae A family of flies (order Diptera). They commonly are known as small-headed flies.  Flies

Aculeus

Acrolepiidae A family of moths (order Lepidoptera). They commonly are known as false diamondback moths.  False Diamondback Moths  Butterflies and Moths

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Active Ingredient (A.I.) The toxic component of an formulated pesticide. It also is known as the toxicant.

Active Space Acrolophidae A family of moths (order Lepidoptera). They commonly are known as tube moths.  Tube Moths  Butterflies and Moths

The area or space in which the concentration of pheromone (or other behavioral chemical) is at or above threshold concentration necessary to elicit a response from the receiver.

Active Ventilation Acron A preoral, unsegmented portion of the body, anterior to the first true body segment. This is also known as the prostomium.

Acrosternite The narrow marginal region at the anterior edge of a sternite. It appears to be the posterior edge of the preceding sternite, and includes the intersegmental fold. It is found on the abdominal sterna, but absent from the thoracic sterna.

Action Threshold A level of pest abundance that stimulates action to protect plants from serious damage.  Economic Injury Level (EIL) and Economic Threshold (ET) Concepts in Pest Management

Although most gas exchange in insects occurs through diffusion (passive ventilation), in some cases it is inadequate to meet the oxygen needs of insects, particularly large or flying insects. Thus, muscular contractions acting via hydrostatic pressure (pressure on the hemolymph) compress the trachea and air sacs to force carbon dioxide out and allow more rapid intake of air. The exact mechanism varies among taxa, but usually involves contraction of the abdomen, and synchronization of opening and closing of the spiracles.  Abdominal Pumping

Aculae Small spines on the wing membrane of Lepidoptera.

Aculeus Active Dispersal The redistribution of animals caused by their own actions such as flying or walking. The wings of insects allow active dispersal frequently (contrast with passive dispersal).

This term has several meanings depending on the taxon of insects under consideration. In Hymenoptera, it is synonymous with the sting, an eversible hollow cylindrical structure at the tip of the abdomen used to deliver venom. Though derived from the ovipositor, it is not used

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to deliver eggs. Among Diptera, this term is sometimes used to refer to a pointed, sclerotized structure associated with the reproductive system in males. Among Lepidoptera, this term refers to hair-like structures on the body and wings of primitive moths; these also are known as microtrichia.

Acute Of short duration, characterized by sharpness or severity.

Acute Bee Paralysis A disease of honey bees caused by a picornavirus. Symptoms include trembling, sprawled appendages, and sometimes hairlessness (contrast with chronic bee paralysis).

Aculeate Pertaining to the stinging Hymenoptera (suborder Aculeata), a group including the bees, ants, and many wasps.  Wasps, Ants, Bees and Sawflies (Hymenoptera)

Acute Toxicity The toxicity of a pesticide determined after 24 h. The toxicity resulting from a single dose or exposure.  Insecticide Toxicity  Insecticides

Adaptation This term has at least two meanings: changes in the form or behavior of an organism during its life, and natural selection of organisms in evolutionary time. In entomology, usually the latter definition is intended.

Adaptation of Indigenous Insects to Introduced Crops wendell. l. morrill Montana State University, Bozeman, MT, USA Host range expansion, or adaptation of insects to new crops, is a world-wide phenomenon that has been observed repeatedly and extensively. It is particularly well documented in North America, where forests and prairies consisting of indigenous plants were planted extensively to introduced cultivated crops only after European emigrants arrived in the eighteenth century. Although many new insect pests were also accidentally introduced from Europe into Canada and the United States, many species of native insects adapted to the new crops and became economically important pests (Table 2). Prior to widespread introduction of cultivated crops, some species of native insects fed on a wide range of plants and therefore might be expected to accept the new crops readily. Although polyphagous insects such as grasshoppers (Orthoptera: Acrididae), wireworms (Coleoptera: Elateridae), and cutworms (Lepidoptera: Noctuidae) readily accepted corn, wheat and other crops, not all of the species within these groups became agricultural pests. For example, several hundred species of cutworms and grasshoppers are present, but only about a dozen species in each group have achieved regular pest status. Other native insect species had a narrower host range, and therefore adapted to a more narrow range of crops, or perhaps only a single crop. In the south the boll weevil, Anthonomus grandis grandis Boheman (Coleoptera: Curcullionidae), originally fed on native plants in Mexico related to cultivated cotton, and dispersed northward into the new cotton belt of the southeastern United States as cotton was planted extensively. In the north, the wheat stem sawfly, Cephus cinctus Norton (Hymenoptera: Cephidae), fed on hollowstemmed wild grasses, and within 10 years after tillage began in Alberta, wheat was damaged from

Adaptation of Indigenous Insects to Introduced Crops

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Adaptation of Indegenous Insects to introduced Crops, Table 2 Examples of American insect pests that have adapted to introduced crops Insects with wide host ranges

Old host plant

New host plant

Apple maggot, Rhagoletis pomonella (Walsh) Diptera: Tephritidae

Hawthorne

Apple

Chinch bug, Blissus leucopterus leucopterus Heteroptera: Lygaeidae

Grasses

Corn

Western corn rootworm, Diabrotica virgifera virgifera LeConte Coleoptera: Chrysomelidae

Grasses

Corn

Western bean cutworm, Loxagrotis albicosta (Smith) Coleoptera: Chrysomelidae

Solanaceous weeds

Corn, beans

Colorado potato beetle, Leptinotarsa decemlineata (Say) Coleoptera: Chrysomeliodae

Buffalo burr

Potato

Carrot weevil, Listronotus oregonensis (LeConte) Coleoptera: Curculionidae

Umbelliferous weeds

Carrots, etc.

California red scale, Aonidiella aurantii (Maskell) Hemiptera: Diaspididae

Shrubs and trees

Citrus

Boll weevil, Anthonomus grandis Boheman Coleoptera: Curculionidae

Malvaceous weeds

Cotton

Insects with wide host ranges

Old host plant

New host plant

Sugar beet wireworm, Limonius californicus Coleoptera: Elateridae

Weeds, grasses

Field and vegetable crops

White grubs, Phyllophaga spp. Coleoptera: Scarabidae

Weeds, grasses


False chinch bug, Nysius raphanus Weeds, grasses Howard Hemiptera: Lygaeidae


Tarnished plant bug, Lygus lineolaris (Palisot de Beauvois) Hemiptera: Miridae

Weeds, grasses


Army cutworm, Euxoa auxiliaris (Grote) Lepidoptera: Noctuidae

Weeds, grasses


Yellow striped armyworm, Spodoptera ornithogalli (Guenée) Lepidoptera: Noctuidae

Weeds, grasses


Redlegged grasshopper, Melanoplus femurrubrum (de Geer) Orthoptera: Acrididae

Weeds, grasses


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Adaptation of Indigenous Insects to Introduced Crops

Adaptation of Indegenous Insects to introduced Crops, Table 2 (Continued) Insects with wide host ranges

Old host plant

New host plant

Migratory grasshopper, Melanoplus sanguinipes (Fabricius) Orthoptera: Acrididae

Weeds, grasses


the Canadian prairie provinces south into Montana and North Dakota. In the eastern United States the apple maggot, Rhagoletis pomonella (Walsh) (Diptera: Tep hritidae), expanded its host range to included newly introduced cultivated fruits, especially apples. The Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae) originally fed on solanaceous weeds in Mexico or the southwestern United States, and quickly spread across the United States on potatoes once it gained access to potato acreage. These are just a few examples of insects accepting new hosts, and the same phenomenon is well documented for important tropical crops such as sugarcane and cacao, and other crops, as they were introduced and cultivated in various locations around the world. Some of the native insect populations originally occurred at low levels because their host plants were relatively sparse. Large acreage of new monocrop habitats therefore resulted in an abundant food supply, excellent survival, and eventually in pest population outbreaks. Also, the native environments were relatively stable, and supported a wide range of beneficial insects suppressed herbivorous insects. However, soil tillage within the agricultural environments produced highly disturbed systems, and pests with high fecundity were not effectively suppressed by predators and parasitoids. America’s native insects displayed considerable plasticity in acquiring new hosts. This trend has been noted everywhere agriculture is practiced, and we can expect the number of pests to increase with time, and especially with the area planted to each particular crop, as indigenous species adapt to imported host plants or crops are exposed to additional potential pests in new geographic areas. However, species accrual occurs most rapidly soon after plant introduction, and the number of species

feeding on a plant (species richness) does not increase indefinitely, leveling off after less than 300 years if there is not an increase in crop acreage. We can observe insects with both broad and narrow host selection behavior expanding their host range to include introduced crop plants. This is not surprising for generalist species, which feed broadly on many plants, but it is quite interesting when insects with a narrow host range adopt new hosts. In such cases the species with a narrow host range usually are pre-adapted to accept the foreign crops because they feed on plants in the same family as the introduced crop. North America possesses close relatives to nearly all the introduced crops among its indigenous flora, so it is not surprising that insects associated with the native plants would adapt to the introduced crops. The presence of secondary plant metabolites (allelochemicals) such as alkaloids, terpenoids, and cyanogenic glycosides often serves to keep non-adapted insects from feeding extensively on plants, but may serve as chemical cues or stimulants for insects that are adapted. Thus, insects that specialize on cruciferous weeds and crops are attracted to allylisothiocyanate, and insects that feed on cucurbitaceous weeds and crops are attracted to cucurbitacin. Host selection behavior by insects is not a static situation, nor is it as simple as the singlechemical scenario presented above. It is constantly evolving in response to various biotic characteristics such as herbivory, and even to crop cultural practices. Some natural selection of insect strains may have occurred during the adaptation from native to introduced plants. In the northern Great Plains, wheat matures earlier in the season than wild grasses. Therefore, after a century, adult wheat stem sawflies are now active nearly a month earlier than previously, and now are more effective in utilizing wheat.

Adelidae

Changes in farming practices that have also impacted populations of native insect pests in croplands. Originally, horses were used for farming, and oats were needed for their feed. Later, the horses were replaced by tractors, and the need for oats was reduced. Oats are resistant to wheat stem sawflies, and when oats was eliminated from the cropping system, the vast acreages of wheat resulted in a population explosion of the sawflies. More recently, canola has been included in the Canadian Prairie Provinces, and populations of grass-feeding insects are somewhat disrupted by the presence of a non-host, cruciferous crop. Other water and soil conservation practices such as alternate-year summer fallow, strip cropping, and chemical fallow have affected the prevalence of both pest and beneficial insects. Beneficial insect populations were also impacted by tillage and cultural practices, and changes in the chemical constituency of crop plants. Parasitoids have complex host searching behavior that begins with finding plant environments in which their hosts could occur. Therefore, it was necessary for the parasitoids to learn that the new crops could be sources of hosts. In the case of the wheat stem sawfly, only two of the known parasitoid species have currently adapted from wild grasses to wheat. Parasitoids may be more favored by one plant cultivar than another, or less favored by a crop than a similar weed. The availability of food for the adult parasitoid or predator, either nectar from blossoms or extra floral nectaries or pollen from blossoms, is often implicated in differential survival of beneficial insects among different plants. Overall, adaption by herbivorous insects to new host plants is a dynamic and widespread phenomenon. Though sometimes it is difficult to determine whether it is the change in the constituency of the host plant that accounts for insect acceptance, or it is some other factor such as widespread host plant availability that accounts for insect abundance, it is clear that the relationship between insects and plants is not static, resulting

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in a continuing stream of new pest problems for crop plants.  Host Plant Selection by Insects  Allelochemicals  Plant Resistance to Insects

References Bernays EA, Chapman RF (1994) Host-plant selection by phytophagous insects. Chapman and Hall, New York, NY Connor EF, McCoy ED (1979) The statistics and biology of the species-area relationship. Am Nat 113:791–833 Kim KC (1993) Insect pests and evolution. In: Kim KC, McPheron BA (eds) Evolution of insect pests; patterns of variation. Wiley, New York, NY, pp 3–25 Morrill WL, Kushnak GD (1996) Wheat stem sawfly (Hymenoptera: Cephidae) adaptation to winter wheat. Environ Entomol 25:1128–1132 Strong DR (1979) Biogeographic dynamics of insect-host plant communities. Annu Rev Entomol 24:89–119

Adaxial Surface The upper surface of a leaf (contrast with abaxial surface).

Adeheterothripidae A family of thrips (order Thysanoptera).  Thrips

Adelgidae A family of insects in the order Hemiptera. They sometimes are called pine and spruce aphids.  Aphids  Bugs

Adelidae A family of moths (order Lepidoptera). They commonly are known as long horned fairy moths.

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Adephaga

 Long horned Fairy Moths  Butterflies and Moths

Adephaga One of four suborders of beetles (Coleoptera), and one of two suborders that contain numerous and important beetles (the other is suborder Polyphaga). It is comprised of about nine families, the principal ones being Carabidae, Gyrinidae, and Dytiscidae. Nearly all groups are predatory, and many are aquatic.  Beetles (Coleoptera)

Aderidae A family of beetles (order Coleoptera). They commonly are known as antlike leaf beetles.  Beetles

Adfrontal Areas A pair of narrow oblique sclerites on the head of a caterpillar. The adfrontal areas border the front, which normally is triangular, so the adfrontal areas take on the shape of an inverted “V.”  Head of Hexapods

Adelphoparasitism A type of hyperparasitism occurring in Hymenoptera: Aphelinidae in which the males are parasitoids of females of their own species (the females parasitize Hemiptera).

Adherence The ability of a material such as a pesticide to stick to a surface.

Adipohemocyte A type of hemocyte, ovoid in shape and likely secretory in function.  Hemocytes of Insects: Their Morphology and Function

Adipokinetic Hormone (AKH) A decapeptide hormone synthesized in neurosecretory cells of the corpora cardiaca and important in the regulation of lipid metabolism, and sometimes carbohydrate or proline metabolism and other physiological functions.  Adipokinetic and Hypertrehalosemic Neurohormones

Adipokinetic and Hypertrehalosemic Neurohormones gerd gäde, heather g. marco University of Cape Town, Rondebosch, Republic of South Africa The adipokinetic hormones and hypertrehalosemic hormones of insects comprise a family of peptide hormones that primarily regulate the levels of energy metabolites, such as trehalose, diacylglycerol and proline that circulate in the hemolymph. These peptide hormones are products of neurosecretory neurons located in the corpora cardiaca, neuroendocrine glands attached to the brain. The structural organization of the insect corpora cardiaca is similar to the hypothalamus-neurohypophysis of the vertebrate endocrine system.

Historical Perspective The existence of hypertrehalosemic hormones was discovered with the observation that injections of extracts of corpora cardiaca elevated the

Adipokinetic and Hypertrehalosemic Neurohormones

concentration of trehalose in the hemolymph of cockroaches (hypertrehalosemia). Unlike vertebrates that use glucose as the major blood carbohydrate, the hemolymph of insects generally contains the disaccharide trehalose, an α-1-1gluco-glucoside, as its major circulating carbohydrate. In addition, the enzyme glycogen phosphorylase in the fat body of cockroaches was demonstrated to be activated when these insects were injected with an extract from the corpora cardiaca. Subsequently, studies in locusts showed that injections of corpora cardiaca extracts elevated hemolymph diacylglycerols, instead of trehalose, and this action was referred to as an adipokinetic or hyperlipemic effect. Injections of locust corpora cardiaca extracts into cockroaches produced the hypertrehalosemic response, and vice versa. Hence, it was likely that the adipokinetic hormone (AKH) of locusts and the hypertrehalosemic hormone (HrTH) of cockroaches were related, or identical, peptides. The locust adipokinetic hormone was isolated and characterized first. It was obtained from the migratory locust, Locusta migratoria, and its primary structure consisted of ten amino acids. It was designated Locmi-AKH-I according to the newest nomenclature for naming insect neurohormones. The amino acid composition and sequence of Locmi-AKH-I had a remarkable similarity to a previously reported red pigment-concentrating hormone (Panbo-RPCH) obtained from the shrimp Pandalus borealis and later found in various crustaceans. It was shown that Locmi-AKH-I was also present in the desert locust, Schistocerca gregaria. Subsequently, both L. migratoria and S. gregaria were shown to contain a second adipokinetic hormone (Locmi-AKH-II and Schgr-AKH-II, respectively) that differed from each other by the amino acids in position 6. The two locust AKH-IIs were octapeptides with sequences similar to those of Locmi-AKH-I and Panbo-RPCH. A third octapeptide AKH (Locmi-AKH-III) was also found in L. migratoria and a similar octapeptide (designated Phymo-AKH-III) occurs in pyrgomorphid and pamphagid grasshoppers, but an AKH-III is

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missing in S. gregaria. Subsequently, three research groups ultimately reported, in the same year, the presence of two octapeptides from the corpora cardiaca of the American cockroach, Periplaneta americana, that were structurally related to the locust AKHs and the crustacean RPCH. These two peptides were isolated on the basis of myotropic or heartbeat acceleration bioassays and are referred to as cardio acceleratory hormones (Peram-CAH-I and Peram-CAH-II), but they also produced hypertrehalosemia in the cockroach and represent the hypertrehalosemic hormones. These pioneering studies, along with numerous subsequent studies, demonstrated that there are, so far, about forty structurally related, but distinct, peptides with adipokinetic and hypertrehalosemic effects in the insects and one in crustacean (Table 3). The name adipokinetic hormone/red pigment-concentrating hormone (AKH/RPCH) family was coined for this general family of peptides, which likely encompasses the arthropods.

Chemistry of the AKH/RPCH Family The members of the adipokinetic hormone/red pigment-concentrating hormone family share numerous structural features. They consist either of eight, nine or ten amino acids, depending on the insect species from which they are isolated. They are blocked by pyro-glutamate at the N-terminus and by an amide moiety at the C-terminus. Presumably, blocked termini prevent degradation of the neuropeptides by amino- and carboxypeptidase enzymes while circulating in the hemolymph. Aromatic amino acids, usually phenylalanine and tryptophan, always occupy positions 4 and 8, respectively, but aromatic amino acids can also occupy other positions. The peptides are usually neutral under physiological conditions, but a few have a negatively charged aspartate at position 7. Glycine is always present at position 9 as deduced from cDNA analysis of the precursor. The terminal glycine is converted to the amide moiety on the tryptophan in the octapeptides.

45

Schistocerca, Phymateus

Orthoptera, Ensifera

Leu

pGlu

Locusta

Locmi-AKH-II

=Schgr-AKH-II

Tettigonia, Decticus

pGlu

Leu

Val

pGlu

Gryllus, Acheta, Gryllodes

Grybi-AKH

Ile

pGlu

Phymateus

a

Leu

Phymo-AKH-III

pGlu

Leu

Val

Locusta

pGlu

pGlu

Locmi-AKH-III

a

Schgr-AKH-II

Leu

pGlu

Locusta, Schistocerca

Locmi-AKH-I

Orthoptera, Caelifera

Not known

Leu

Manto-AKH

pGlu

Mantophasmatodea

Carausius, Sipyloidea, Extatosoma

Val

Carmo-HrTH

pGlu

Phasmatodea

Empusa, Sphodromantis

Gromphadorhina

Emppe-AKH

Leucophaea, Blattella

Val

Mantodea

Blaberus, Nauphoeta

Bladi-HrTH

pGlu

Leu

pGlu

Periplaneta, Blatta

Peram-CAH-II

Val

pGlu

Val

Val

Periplaneta, Blatta

pGlu

pGlu

Val

2

a

Pseudagrion, Ischnura

Psein-AKH

pGlu

1

Structure

Peram-CAH-Ia

Anax, Aeshna

Anaim-AKH

Blattodea Blattidae Blaberidae Blattellidae

Libellula, Pantala, Orthetrum

Libau-AKH

Odonata

Genus

Peptide name

Asn

Asn

Asn

Asn

Asn

Asn

Asn

Asn

Thr

Asn

Asn

Thr

Asn

Asn

Asn

Asn

3

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

4

Ser

Ser

Thr

Thr

Ser

Ser

Thr

Ser

Thr

Thr

Ser

Thr

Ser

Thr

Ser

Thr

5

Thr

Thr

Pro

Pro

Thr

Ala

Pro

Pro

Pro

Pro

Pro

Pro

Pro

Pro

Pro

Pro

6

Gly

Gly

Trp

Trp

Gly

Gly

Asn

Gly

Asn

Asn

Gly

Asn

Asn

Gly

Ser

Ser

7

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

8

NH2

NH2

NH2

NH2

NH2

NH2

Gly

NH2

Gly

NH2

Gly

NH2

NH2

NH2

NH2

NH2

9

Thr

Thr

Thr

10

NH2

NH2

NH2

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Order

Adipokinetic and Hypertrehalosemic Neurohormones, Table 3 Representative sequences of adipokinetic/hypertrehalosemic peptides from various insect orders

46 Adipokinetic and Hypertrehalosemic Neurohormones

pGlu pGlu pGlu

Platypleura, Munza, Cacama, Magicicada, Diceroprocta Pyrrhocoris, Disdercus

=Peram-CAH-II Pyrrhocoris, Disdercus Corixa Lethocerus Nepa

Hemiptera/Homoptera Placa-HrTH

Corpu-AKH

Letin-AKH

Nepci-AKH

Hemiptera, Heteroptera

Leu

pGlu

Hymenoptera Tenthredo Xylocopa, Bombus Vespula, Vespa Apis

=Schgr-AKH-II

=Grybi-AKH

=Manse-AKH

Heliothisb

Tenar-HrTH

Helze-HrTH

Manduca, Vanessa, Bombyx, Heliothisb

=Peram-CAH-II Leptinotarsa

Manse-AKH

Leptinotarsa

=Peram-CAH-I

Lepidoptera

Leu

pGlu

Onitis

Oniay-CC

a

pGlu

Scarabaeus, Gareta

pGlu

pGlu

pGlu

pGlu

pGlu

pGlu

pGlu

Leu

Val

Leu

Leu

Leu

Val

Tyr

Phe

Phe

Scade-CC-II

pGlu

Scarabaeus, Gareta, Onitis

Val

Scade-CC-I

pGlu

Coleoptera

Palpares

Leu

Val

Leu

Leu

Leu

Val

Val

Ile

=Grybi-AKH

pGlu

pGlu

pGlu

pGlu

pGlu

2

Neuroptera

Pyrap-AKH

Labidura, Forficula

=Grybi-AKH

Dermaptera

Microhodotermes

Micvi-CC

1

Structure

Isoptera

Genus

Peptide name

Order

Thr

Asn

Asn

Asn

Thr

Thr

Thr

Asn

Asn

Asn

Asn

Asn

Asn

Asn

Asn

Thr

Asn

Asn

Asn

Asn

3

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Tyr

Tyr

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

Phe

4

Thr

Ser

Ser

Ser

Ser

Thr

Thr

Ser

Ser

Ser

Ser

Ser

Ser

Ser

Ser

Thr

Thr

Ser

Ser

Thr

5

Ser

Thr

Thr

Thr

Ser

Ser

Pro

Pro

Thr

Pro

Pro

Thr

Ser

Pro

Pro

Pro

Pro

Pro

Thr

Pro

6

Ser

Gly

Gly

Gly

Gly

Ser

Asn

Asn

Gly

Val

Asp

Gly

Gly

Tyr

Ser

Asn

Asn

Ser

Gly

Asn

7

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

Trp

8

Gly

NH2

NH2

Gly

Gly

Gly

NH2

NH2

NH2

NH2

NH2

NH2

NH2

NH2

NH2

NH2

NH2

Gly

NH2

NH2

9

NH2

Gly

Asn

NH2

NH2

NH2

NH2

Asn

10


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pGlu

pGlu

pGlu

pGlu

1

Leu

Leu

Leu

Leu

2

Structure

Asn

Thr

Thr

Thr

3

Phe

Phe

Phe

Phe

4

Ser

Thr

Thr

Ser

5

Pro

Pro

Pro

Pro

6

Gly

Gly

Ala

Asp

7

Trp

Trp

Trp

Trp

8

NH2

NH2

NH2

NH2

9

10

a

Note that the peptide in certain orders is identical. For example: Peram-CAH-I and -II of the Blattodea, Blattidae is also present in Coleoptera (Leptinotarsa); Schgr-AKH-II of Orthoptera, Caelifera is present in Orthoptera, Ensifera and in Hymenoptera (Xylocopa, Bombus); Grybi-AKH of Orthoptera, Ensifera is also present in Dermaptera, Neuroptera and Hymenoptera, etc. b Heliothis is revised to Helicoverpa.

Pandalus

Tabanus

Tabat-AKH

Panbo-RPCH

Anopheles

Anoga-AKH

Crustacea

Phormia, Drosophila

Phote-HrTH

Diptera

Genus

Peptide name

Order

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Adipokinetic and Hypertrehalosemic Neurohormones, Table 3 Representative sequences of adipokinetic/hypertrehalosemic peptides from various insect orders (Continued)

48 Adipokinetic and Hypertrehalosemic Neurohormones


Some of the members of this peptide family have additional post-translational modifications besides the blocked termini. For example, two HrTH decapeptides are present in the corpora cardiaca of the stick insect, Carausius morosus; one of these decapeptides is glycosylated and has a unique C-glycosylation where the sugar is linked to the C-2 atom of the indole ring of tryptophan. Another unusual modification has been found in an AKH of the protea beetle, Trichostetha fascicularis: the corpora cardiaca contain two AKHs, one of which is an octapeptide with a phosphothreonine at position 6. The relationships between individual AKH and HrTH peptides and insect species are complex. There are no clear rules concerning which peptide occurs in which order of insects. Several species within an order may share the same peptide and have other species-specific sequences, and the same peptide may be present in species of different orders. As described above, the two locust species, S. gregaria and L. migratoria, share an identical decapeptide (Locmi-AKH-I); each species possesses a second, unique octapeptide (LocmiAKH-II; Schgr-AKH-II); and L. migratoria contains a third octapeptide (Locmi-AKH-III) that does not have a complement in S. gregaria. Cockroach species of the families Blattellidae and Blaberidae share a single hypertrehalosemic decapeptide hormone (Bladi-HrTH), whereas cockroaches of the family Blattidae contain two octapeptide hormones (Peram-CAH-I and -II). In addition, there is overlap between orders. Grybi-AKH is present in certain crickets and in species of Neuroptera, Dermaptera and Heteroptera. Peram-CAH-I and -II of the blattid cockroaches are also found in the Colorado potato beetle, Leptinotarsa decemlineata, and Peram-CAH-II is shared with the heteropteran bug, Pyrrhocoris apterus. Whereas Peram-CAH-I and -II mobilize glycogen from the fat body of the cockroach to increase hemolymph trehalose, the same or similar peptides increase hemolymph proline in beetles to serve as the major flight substrate. Unlike the complex situation in insects, the crustaceans apparently possess only the single

A

anbo-RPCH peptide which has a chromatophoroP tropic effect. Panbo-RPCH has also been found in an insect species, the heteropteran stinkbug, Nezara viridula, where it has an adipokinetic effect. Phylogenetic relationships of the HrTHs have been proposed for the cockroaches based on morphological, behavioral and physiological characters congruent with the distribution of the various structures of the HrTHs within the order.

Physiological Actions The general physiological action of the adipokinetic and hypertrehalosemic hormones in insects is to elevate the hemolymph metabolites that are used by the muscles and other tissues as a source of energy, regardless of the nature of the metabolites. This is accomplished by stimulating the fat body, which is the hormone’s target tissue, to convert its stores of triacylglycerides or glycogen to diacylglycerides or trehalose, respectively, or to synthesize proline. The diacylglycerides, trehalose or proline are released from the fat body to increase their respective levels in the hemolymph. The same peptides that elevate diacylglycerides in locusts elevate trehalose when administered to cockroaches, and vice versa, and the hormones of locusts and cockroaches elevate proline in the Colorado potato beetle. The decision as to whether lipid-, carbohydrate-, or proline-mobilizing pathways are activated is a species-related function of the enzyme composition in the fat body. Muscular activity for animal locomotion can involve either long-term or short-term events. Long-term activities might entail sustained, nonemergency actions such as migration or persistent searching for food, mates or shelter. Short-term activities might consist of local searching activities but may also require immediate, brief, emergency responses such as evading attack by a predator or defending a breeding territory. Longterm events require a steady supply of energy metabolites, whereas short-term events may be

49

50

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brief but intense, and, if successful, they can be followed by a period of recovery to replenish exhausted metabolites. The adipokinetic hormones are often involved in prolonged, constant muscular activity such as migration. This is characteristically true for the locusts whose migratory behavior has been described since biblical times. Migration is a sustained flight activity that uses muscular oxidation of fatty acids to produce energy, since fatty acids deliver more energy per mole than carbohydrates. However, carbohydrate serves as the major source of muscular energy during initial flight, and lipid becomes the major source for energy as flight persists and becomes sustained. Based on differing physiological effects, it is speculated that the three AKHs may exert different regulatory actions on metabolite mobilization and use during the different stages of migration. Locmi-AKH-II is likely to be the major carbohydrate-mobilizing hormone that provides trehalose for initial flight; LocmiAKH-I is the major hormone responsible for fat mobilization during sustained flight and LocmiAKH-III may be responsible for regulating energy metabolism during rest. Furthermore, during lipid mobilization, AKH performs several distinct but related actions. In the fat body, AKH activates lipase for triacylglyceride degradation; this is achieved by binding of the AKH to a G-protein coupled receptor at the cell membrane, activation of adenylate cyclase resulting in the second messenger cAMP which, in conjunction with Ca2+, is responsible for lipase activation. In the hemolymph, AKH increases the lipid-carrying capacity of lipophorins (proteins) resulting in increased amounts of low-density lipophorin for shuttling lipids from the fat body to the muscles. At the flight muscle level, AKH increases the rate of lipid oxidation. Recent research on a number of terrestrial and aqueous heteropteran bugs that have various feeding patterns (plant sap sucking, predators, obligatory hematophagous), also established a lipid-based activity (flight and/or swimming) metabolism that is regulated by the respective AKHs of these insects.

By contrast, insects such as cockroaches, bees and flies use only carbohydrate (trehalose) as the primary source of energy for muscular activity and locomotion. These species do not migrate and lack the adipokinetic response, but they are faced with emergency situations of predator evasion, and in such cases, the hypertrehalosemic hormone mobilizes trehalose in response to the emergency. However, injections of hypertrehalosemic hormone show that significant elevation of the hemolymph trehalose may take as long as 10–30 min. This delay in elevating hemolymph carbohydrate is too long to significantly assist the insect in evading capture. Furthermore, the open circulatory system of insects does not efficiently direct circulating metabolites to the muscles in the manner of the closed circulatory system of vertebrate animals. Energy metabolites, such as trehalose, must constantly be maintained at high levels in the hemolymph to meet urgent, immediate demands. Hence, the role of the hypertrehalosemic hormone appears to be to replace depleted hemolymph trehalose and maintain it at high levels. Maintenance of high trehalose levels allows the insect to make quick responses to elude capture that may require only seconds, or at most, several minutes to conclude. If the insect is successful at escape, the hormone stimulates the degradation of fat body glycogen to restore the high trehalose levels by activating specifically the enzyme glycogen phosphorylase after the hormone has bound to a G-protein coupled receptor on the membrane of a fat cell and had activated a phospholipase C, resulting in the production of inositol trisphosphate and the release of Ca2+ from internal stores (influx of external Ca2+ is also activated by HrTH) which sets in motion a cascade of activation of kinases and, finally, glycogen phosphorylase. Removal of the hypertrehalosemic hormone does not affect the ability of such insects to be active for the short term (several minutes), but after exhaustion, lengthens their recovery time. Tsetse flies and various beetle species fuel their flight metabolism by the partial oxidation of

Adjuvants

proline and the production of alanine. For continuous flight or replenishment of proline reserves in the fat body a unique system exists in these insects to synthesis proline: the respective AKHs activate a lipase in the fat body and the fatty acids that are liberated from triacylglyerols undergo β-oxidation, and the resulting acetyl CoA units are used in conjunction with alanine to synthesize proline. Alanine, which is derived from the partial oxidation of proline, is re-used for proline synthesis and can be viewed as a shuttle system for the transport of acetyl units. Although the mobilization of energy for flight and other metabolically intense situations is likely the major function for the adipokinetic and hypertrehalosemic hormones, the hormones exhibit pleiotropic actions. The hypertrehalosemic hormones were isolated originally based on their cardioacceleratory action on the heart. This is a logical action for the hormone since elevated heartbeat rate would facilitate distribution of the energy metabolites throughout the body and assure their ready access to the muscles. In keeping with the stimulatory action of AKH on lipid degradation in locusts, lipid synthesis is inhibited by AKH. Other, less well characterized actions include: inhibition of RNA and protein synthesis related to vitellogenesis in locusts and crickets, and the stimulation in cockroaches of the oxidative capacity of mitochondria during fat body maturation, and of gene expression for a fat body cytochrome P450 related to lipid oxidation. These latter actions by the hormones may be equally important as their effects on mobilization of energy metabolites, but they are poorly elucidated because of insufficient research, and they cannot yet be placed into perspective as to their physiological significance. Other actions in which AKHs seem to be involved are an enhanced activation of the locust immune system and, possibly, in the activation of an antioxidant protection mechanism in potato beetles. In summary, the adipokinetic-hypertrehalosemic-hyperprolinemic hormones constitute a family of peptides that are adapted to the

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individual biology of the insect species in which they are found. They display a unique relationship with their target tissue in that the hormone carries the endocrine message to the target tissue (fat body) to mobilize energy stores, but the target tissue determines which metabolic pathways are activated depending on the biology of the species. It is this biology that determines the nature of the muscular activity (prolonged– migration; brief–predator evasion) and its metabolic need for consuming carbohydrates, lipids or proline as a source of energy.

References Beenakkers AMT (1969) The influence of corpus allatum and cardiacum on lipid metabolism in Locusta. Gen Comp Endocr 13:492 Fernlund P, Josefsson L (1972) Crustacean color-change hormone: amino acid sequence and chemical synthesis. Science 177:173–175 Gäde G (1989) The hypertrehalosaemic peptides of cockroaches: a phylogenetic study. Gen Comp Endocr 75:287–300 Gäde G (2004) Regulation of intermediary metabolism and water balance of insects by neuropeptides. Annu Rev Entomol 49:93–113 Mayer RJ, Candy DJ (1969) Control of haemolymph lipid concentration during locust flight: an adipokinetic hormone from the corpora cardiaca. J Insect Physiol 15:611–620 Steele JE (1961) Occurrence of a hyperglycemic factor in the corpus cardiacum of an insect. Nature 192:680–681 Stone JV, Mordue W, Batley KE, Morris HR (1976) Structure of locust adipokinetic hormone, a neurohormone that regulates lipid utilization during flight. Nature 263:207–221 Vroemen SF, van der Horst DJ, van Marrewijk WJA (1998) New insights into adipokinetic hormone signalling. Mol Cell Endocrinol 141:7–12

Adjuvants Chemicals added to insecticides to improve their effectiveness. Examples of adjuvants include toxicity, stability, and adhesion.  Insecticide Formulations  Insecticides

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Adoption Substance

Adoption Substance A secretion presented by a social parasite that induces the host insects to accept the parasites as members of their colony.  Social Insect Pheromones

Adult The sexually mature stage of an animal. The adult is usually the winged stage in insects. With rare exceptions, the adult does not molt again.  Metamorphosis

Adventive An organism that has arrived in an area from elsewhere. It is not native, and likely arrived as an invader or accidental introduction. It is also known as nonindigenous.  Invasive Species

Aedeagus The intromittent (copulatory) organ of the male; the distal portion of the phallus. Sometimes referred to as the penis.  Abdomen of Hexapods

Adulticide A pesticide used to kill adult insects. This term often is used to describe products used to kill adult mosquitoes. (contrast with larvicide)  Insecticides

Adultoid Reproductive In higher termites, a supplementary reproductive that in indistinguishable morphologically from the reproductive.

Aenictopecheidae A family of bugs (order Hemiptera).  Bugs

Aeolothripidae A family of thrips (order Thysanoptera). They commonly are known as broad-winged thrips or banded thrips.  Thrips

Adult Transport A behavior in which social insects (usually ants) drag or carry their nestmates to a new location. This normally occurs during colony emigration.

Aepophilidae A family of bugs (order Hemiptera). The sometimes are called marine bugs.  Bugs

Adventitious Veins In some insects, additional wing veins are present which are neither secondary nor intercalary veins. They usually are the result of the lining up of cross veins.  Wings of Insects

Aeshnidae A family of dragonflies (order Odonata). They commonly are known as darners.  Dragonflies and Damselflies

African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae)

Aetalionid Treehoppers Members of the family Aetalionidae (order Hemiptera).  Bugs

Aerial Photography In pest management, photographs taken by an airplane or satellite that are used to identify variations within fields/crops to help make management decisions.

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even though it causes no economic loss. The presence of some insects in homes or on ornamental plants are examples of aesthetic pests, though in the latter case if they inhibit the ability to market plants then the same insect can be come an economic pest.  Economic Injury Level (EIL) and Economic Threshold (ET) Concepts in Pest Management

Aestivation A state of inactivity or curtailment of normal activity during the summer months. Diapause

Aeropile The opening in the egg surface (chorion) through which air enters.

Aerosol The air suspension of liquid or solid particles of small diameter. This is a common formulation for flying insects or for household use where no additional formulation or preparation is desired.  Insecticides  Insecticide Formulations

Aesthetic Injury Level The level of pest abundance above which aesthetic, emotional, or sociological considerations require pest control actions. Economic considerations are not relevant.  Economic Injury Level (EIL) and Economic Threshold (ET) Concepts in Pest Management

Aesthetic Pest A pest which, through its presence or actions, is deemed objectionable and in need of elimination

Aetalionidae A family of insects in the order Hemiptera. They sometimes are called aetalionid treehoppers.  Bugs  Treehoppers

African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae) joe c. b. kabissa Tanzania Cotton Lint and Seed Board, Dar Es Salaam, Tanzania The African armyworm (Fig. 21) is a larva of a nocturnal moth, Spodoptera exempta (Walker). This species, although commonly referred to as the African armyworm, occurs rather widely in the grasslands of tropical and subtropical Africa and Asia. In Africa, where S. exempta is of major economic importance, its occurrence is confined to countries south of the Sahara: Tanzania, Kenya, Uganda, Ethiopia, Somalia, Malawi, Zimbabwe, Zambia and South Africa. Outside Africa, S. exempta has been reported from southwest Saudi Arabia in the republic of Yemen, southeast Asia, Australia, New Zealand and Hawaii.

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African Armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae), Figure 21 African armyworm: top left, adult female, top right, adult male; middle left, solitary form of larva; middle right, gregarious form of larva; lower left, pupae in soil; lower right, eggs on foliage.

During an armyworm outbreak, larvae of S. exempta march together in long columns, akin to army columns, in search of susceptible plant material. This is the basis for the name “armyworm.” When susceptible plant material is found, it is often voraciously devoured to ground level. In typical armyworm outbreaks, larval density may

exceed 1,000 per m2 over areas covering tens or even hundreds of square km. In Africa, S. exempta is adapted for survival on seasonal grasslands by combining a high intrinsic rate of increase with “migration” to places of rainfall where grasses are suitable for survival of its caterpillars. Because of its capability to move over long


distances, hundreds and sometimes thousands of km across national boundaries freely, S. exempta is truly an international pest. Often times it appears sporadically and suddenly in dense outbreaks capable of causing extensive and enormous damage to susceptible rangeland grasses, cereal crops and sugarcane. Because of its ability to appear suddenly and then disappear equally suddenly, the African armyworm has sometimes been referred to by farmers as the “mystery worm.” The scale of devastation to crops and pastures by armyworm is comparable only to that caused by locusts. Thus, the armyworm is greatly feared wherever it occurs.

Biology and Ecology Adult moths of S. exempta have a wing span in the range of 20–37 mm. The forewings are characterized by an overall dull gray-brown appearance. The hind wings are whitish with dark veins. The two sexes can be distinguished by examining the number of bristles on the frenulum (the mechanism that couples the fore and hind wings during flight), which are single in the males and multiple in the females. A characteristic feature of the African armyworm is the presence of racquet-shaped scales at the tip of the abdomen of the males and black scales on the tip of the body of the females. Females of S. exempta lay between 100 and 400 eggs per night in a mass covered by black scales from the tip of their abdomen. Eggs are small, 0.5 mm in diameter, whitish in color, but then turn black prior to hatching. Eggs are often laid on the lower side of leaves and hatch in about 2–4 days after oviposition. There are six larval instars extending over a larval period of between 14 and 22 days depending on the temperature and the host plant on which the larvae have been reared. Fully grown sixth instar larvae are often 25–35 mm long. Pupation occurs 2–3 cm below the soil surface. This process is often preceded by a sudden and synchronized disappearance of larvae that quickly burrow into the ground, particularly if soil conditions are moist enough.

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Adults emerge within 7–12 days after pupation and can live up to 14 days if appropriately fed. In their lifetime, females can lay up to 1,000 eggs. Spodoptera exempta is not known to enter into any type of diapause. This probably explains why this species has to migrate soon after emergence. Spodoptera exempta exhibits a phenomenon called polyphenism, or phase polymorphism (i.e., the occurrence in a population of two or more phenotypes due to exposure to different environmental conditions). For example, up until the third molt, all larvae of S. exempta remain green in body color. However, at this stage, depending on whether there are many larvae or just a few, they will turn black or remain in various shades of green or brown. If there are large numbers of larvae present as in a typical outbreak situation, larvae tend to be characteristically velvety black on top with pale lines on each side and greenish-yellow underside; this phenotype is called the gregarious phase. It is during this phase that S. exempta is most devastating to crops. Larvae in the gregarious phase tend to be very active and often march on the soil in one direction only looking for fresh food. They also feed high on the plant during the day. However, if not crowded, the developing larvae remain one of the many shades of green, pink or brown color until they pupate. In contrast to black gregarious larvae, they are sluggish, living mostly at the bases of plants and are not as destructive to crops. Although their appearance is so different, they are the same insect and one may easily be converted into the other. Nevertheless, because moths derived from gregarious and solitary larvae exhibit the same level of readiness to fly, phase change in S. exempta is construed as being merely a stress phenomenon associated with crowding. It is unknown whether this aspect of phase polymorphism is of any evolutionary significance to S. exempta. In the case of locusts, it is thought that the solitary form is the one that enables the populations to persist at a low level during the dry season when there are no

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outbreaks occurring. It is worth speculating, in the case of S. exempta, that at such low densities, its populations continue to breed during the dry season in areas where grasses remain green, such as in the cool highland areas and, more especially, the coastal areas where it is hot and there are periodic showers during the dry season. This form may, therefore, be of some critical survival value for this pest.

Seasonal Movements and Armyworm Outbreaks Upon emergence, adult moths of S. exempta are fully capable of movement from their breeding sites to new areas. Such flights can be very short, or very long, depending on whether they are carried in a downwind direction or not. Nevertheless, because they are one-way journeys, they cannot, therefore, be regarded as migration in its strict ethological sense – where there is invariably a return flight to breeding sites. The question of how armyworm outbreaks start has baffled scientists and farmers alike for a long time. Because moths emerge over a period of up to 12 days, and can also fly off on “migration” at different times, they become widely dispersed and do not form swarms as occurs with locusts. Moreover, the moths are weak fliers and are often carried in a downwind direction. Thus, moths disperse in space and time downwind. For purposes of this narrative, an armyworm outbreak is simply described as the sudden appearance of larval infestations, often simultaneously on many farms in one region. Two hypotheses, the continuity and the concentration hypotheses, have been put forward in order to explain how outbreaks begin during an armyworm season. The continuity hypothesis, which is based on biogeographical analyses of past outbreaks, proposes that much of the armyworm population is always at crowded, outbreak densities, and that the seasonal absence of reports represents not a real absence of outbreaks, but a

temporary loss of contact with the main population in remote and perhaps uninhabited areas. This continuity implies that the first outbreaks to appear in East Africa are due to the migration of parent moths from the north at the end of the season. Although there is ample evidence of adult dispersal on the wind over distances up to several hundred km in a few successive nights, there is little evidence in support of a southward dispersal at the start of an armyworm outbreak in East Africa. The concentration hypothesis, on the other hand, postulates that because of occasional capture of moths in traps during the off-season, as well as the finding of rare caterpillars after concerted searches, S. exempta persists during such times of year as uncrowded populations (the solitary phase, in which caterpillars remain green and unreported), and that the first outbreaks of the season are due to concentration of moths before the synchronized mating and egg laying. Thus, there seem to be two types of armyworm outbreaks: primary and secondary outbreaks. During primary outbreaks, sources of outbreaks are the low density populations that survive and breed during dry seasons in green areas of the coast and the highlands. Secondary outbreaks occur downwind from the coast near the first highlands. During years of serious armyworm outbreaks, the first outbreaks often start in Tanzania, Zimbabwe and Malawi at about the beginning of the wet season in December, and are followed by a progression of outbreaks at about one generation time-intervals from Tanzania through Kenya, Uganda, Ethiopia, Somalia to the Yemen and from Zimbabwe to South Africa. Wind convergence plus localized weather and moth behavior provide the mechanism for transporting and concentrating moths emerging from primary outbreaks. Flight mechanisms of S. exempta prior to outbreaks have been the subject of extensive studies. After drying and hardening their wings, moths first move up into the trees. Then, when they are ready, they fly up several hundreds of meters into the air, where if caught up by prevailing wind, are carried away downwind. When dawn arrives, the moths


descend and hide on the ground in the grass, but at dusk they take off again. They will continue to do this for several days, either until they die, or until they come to an area where rain is falling. Rain causes the moth to descend to the ground. The winds coming out of the rainstorm have the effect of concentrating the moths, rather as though they were being swept together with a brush. This is the reason why armyworms occurring during outbreaks are not evenly distributed. Upon descent to the ground, moths tend to drink water if this is available, mate and then lay their eggs. At this stage dispersal will have come to an end. In Africa, seasonal rains are brought by the meeting of large scale winds from the northeast and the southwest at the Inter-Tropical Convergence Zone (ITCZ). The position of the ITCZ moves with the sun across the tropical zone twice each year, from north to south between July and December and from south to north between January and June. The first outbreaks, designated as primary outbreaks in East Africa, usually occur in central Tanzania in November or December. Occasionally they occur further south, in Mbeya, Mtwara and Lindi regions of Tanzania. More rarely, they occur in southeastern Kenya. Moths produced by these primary outbreaks are then carried by the wind towards the ITCZ, which has meanwhile moved north. The moths are thus concentrated in areas where the rains are just beginning, and so they breed and multiply yet again. If conditions are suitable, they will increase at an enormous rate. Although the first outbreaks are only a few hectares in extent, by February and March there may be outbreaks of hundreds of square km. Thus, as the ITCZ takes the rains northwards, so the moths, carried by the prevailing wind, move with it, bringing new armyworm outbreaks, designated secondary outbreaks, to northern Tanzania, Kenya, Somalia, Ethiopia, Sudan and eventually Yemen. Armyworm outbreak seasons vary greatly in severity, extent and timing in each of these countries. From September to November, there are seldom armyworm outbreaks in any part of eastern Africa. The armyworm seems to disappear during

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the dry season. But since they have no diapause, they must be living and breeding somewhere. It has now been established that they survive in quite low numbers along the coastal area, where some rain falls in every month of the year. When the rains begin again in central Tanzania, small numbers of moths migrate inland from the coast and it is these that cause the first outbreaks.

Economic Importance of Outbreaks of S. exempta During armyworm outbreaks, feeding damage by S. exempta to cultivated and wild host plants is almost entirely restricted to the leaves, although when food is scarce, the young stems or flowers, particularly of wild grasses, may also be eaten up. The young larvae at first eat the upper and lower surface tissue of the leaves, which results in the skeletonization, or windowing, of the leaves. As a rule, armyworm larvae tend to prefer young plants and recently germinated crops, often defoliating them to ground level. It is estimated that two larvae can completely destroy a 10-day-old maize plant with 6–7 leaves and a single larva can consume 200 mg of dry mass of maize leaves in the course of the sixth instar. Destruction of cereal crops such as maize, rice, wheat or sorghum often necessitates replanting of the entire affected crop. S. exempta larvae are most damaging to cultivated and wild host plants during outbreaks when gregarious bands of larvae travel together on the ground. Such armyworm outbreaks are often capable of causing total crop loss within hours at the local level. Thus, crop losses as a result of armyworm outbreaks can be potentially devastating to local and national economies as they occur in some of Africa’s most impoverished economies. Losses are sometimes difficult to assess quantitatively because of hidden costs such as effects of forage destruction, damage to subsistence farms, the expense of additional seed and, most importantly, food aid from international donors.

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Survey and Control Circumstantial evidence from light and pheromone traps shows that long distance migrations occur between moth emergence and the next breeding areas which are in the vicinity of seasonal passages of low-level wind convergence such as Inter-tropical Convergence Zone or African Rift Convergence Zones. Furthermore, increasing levels of moth catches in light and pheromone traps have been found to be followed by increased probability of infestations of larvae occurring 2–4 weeks later at up to 200 km from the trap. Because primary outbreaks of S. exempta originate from moths taken downwind from sources nearest the coasts of eastern Africa, and concentrate where heavy rains are falling, control of this pest involves accurately detecting primary outbreaks and eliminating them before the subsequent moths emerge and move downwind causing secondary outbreaks in another region or country. The major objective is to kill as many armyworms as possible on pasture or crops before subsequent moths emerge and move downwind. Normally, the largest and densest outbreaks are attacked first. This approach is referred to as “strategic control.” However, because primary outbreaks often remain unnoticed until after secondary outbreaks have occurred, direct elimination of the latter becomes the main objective in multiple outbreak situations. Monitoring possible sources of the moths that cause primary outbreaks has involved deployment of a network of light and pheromone traps, as well as ground searches for low-density larvae in the off-season in areas historically known to be sites of primary outbreaks. In addition, for all primary outbreak areas, rainfall stations must report on a weekly or daily basis the amount of rainfall during the first month of the rainy season. Recently, there have been attempts to introduce predictive models that integrate African Real Time Environmental Monitoring and Information System (ARTEMIS) and satellite imagery and synoptic weather data that has been applicable for detection and elimination of gregarious locusts. The major challenge

associated with armyworm monitoring, forecasting and control in countries most ravaged by this pest is the inadequacy of funding for these operations. Because elimination of all primary outbreaks is almost impossible to achieve, management strategies for S. exempta tend to focus more on suppression of secondary outbreaks. This approach has invariably been dependent on the application of pesticide sprays. To date, a series of low toxicity pesticides are often used (e.g., synthetic pyrethroids, carbamates and organophosphates). Previously, highly toxic, persistent and broad spectrum pesticides such as DDT, BHC, dieldrin and a series of others were used due to lack of alternative, safer products. However, due to the need for rapid intervention and coverage of fairly extensive areas during outbreaks, newer oil-based pesticides are being applied as ultra-low volume (ulv) formulations using hand held, battery driven applicators. Nevertheless, suppression tactics are only costeffective when applied in a timely manner on farmland. Outbreaks occurring on uncultivated land often remain unchecked. Unfortunately, control of armyworms by less toxic means has received far less attention than in the case of other international migratory pests such as locusts, which have been the targets for tests involving fungi, protozoa and even viruses. Extensive studies in eastern Africa have confirmed that all life stages of the armyworm are subject to attack by a diversity of natural enemies. For example, up to 90% of armyworm caterpillars in the last instar can be killed by a nuclear polyhedrosis virus (NPV). Similarly, pupal and prepupal stages can be killed by a cytoplasmic virus. The only fungus known to attack armyworms during conditions of high humidity and temperature is Normuraea rileyi. Armyworms infected by this fungi typically climb to the top of grass blades where they die amidst masses of mycelia. Armyworm larvae are also subject to parasitism by some 28 species of tachnid flies (Diptera: Tachinidae). In cases of parasitism from wasps (Hymenoptera), some 25 parasitoids have been

African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae)

isolated from eggs, larvae and pupae of S. exempta. Apart from attack by parasitoids, there are several arthropod predators that prey on armyworms, including ants (Hymenoptera: Formicidae) and beetles (Coleoptera), which often prey on eggs and early larval stages of S. exempta. To date, there has been no effort to study the potential of some of these natural enemies for commercialization. Armyworm outbreaks also attract flocks of avian predators, notably storks such as Marabou storks, white (European) storks and Abdim’s storks. Occasionally, such assemblages of predators help to eliminate small primary or secondary outbreaks of S. exempta. For the more foreseeable future, it is evident that preventive control of armyworms will continue to rely on diligent surveillance during recessions and, as outbreaks occur, intensified scouting will be necessary to locate and then eliminate pockets of solitary morphs before outbreaks.

References Regional Armyworm Programme of Desert Locust Control Organization for Eastern Africa (1992) The African armyworm DLCO-EA, Addis Ababa, Ethiopia, 19 pp Meinzingen WF (ed) (1993) African armyworm. In: A guide to migrant pest management in Africa. FAO AGP, Rome, Italy, pp 71–85 Rose DJW (1979) The significance of low-density populations of the African armyworm, Spodoptera exempta. (Walker). Philos Trans R Entomol Soc London B 287:393–402 Odiyo PO (1979) Forecasting infestation of a migrant pest: the African armyworm, Spodoptera exempta. (Walker). Philos Trans R Entomol Soc London B 287:403–413

African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae) jamie ellis1, amanda ellis2 1 University of Florida, Gainesville, FL, USA

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Florida Department of Agriculture and Consumer Services, DPI, Gainesville, FL, USA 2

The African honey bee (Apis mellifera scutellata Lepeletier) is a subspecies (or race) of western honey bee (A. mellifera L.) that occurs naturally in sub-Saharan Africa but has been introduced into the Americas. More than 10 subspecies of western honey bees exist in Africa and all justifiably are called “African” honey bees. However, the term “African (Africanized) honey bee” refers exclusively to A.m. scutellata in the bee’s introduced range (Fig. 22). Subspecies of western honey bees are native to Europe and Africa but have been spread widely outside their native range due to their economic importance as pollinators and producers of honey. Initially, only European subspecies of honey bees (hereafter referred to as European bees) were introduced into the Americas, where they were found to be productive in temperate North America but less so in Central and South America where tropical/subtropical climates dominate. In response to the poor performance of European bees in Brazil, Warwick Kerr, a Brazilian scientist, traveled to southern Africa to screen African honey bee subspecies for productivity and viability. His visit resulted in the importation of A.m. scutellata into Brazil in the late 1950s. Dr. Kerr hoped that through experimentation and selective breeding, the African bee could be made manageable and available for use by Brazilian beekeepers. As such, he initiated efforts to breed gentleness into the African stock while amplifying its many positive traits. The breeding effort was not carried to completion because the African bees swarmed accidentally, ending their initial quarantine. Following this, the bees began to spread throughout Brazil and into other parts of South America. All subspecies of Apis mellifera can interbreed or hybridize. Consequently, African bee hybridization with European bees became frequent as African bees moved into areas previously occupied by European bees. It is this hybridization with

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African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae), Figure 22 The natural distribution of Apis mellifera scutellata in Africa (modified from Hepburn HR, Radloff SE (1998) Honeybees of Africa. Springer-Verlag, Berlin, 370 pp), and its distribution in the Americas.

European honey bees that earned them the name “Africanized” honey bees. Traditionally, “African” and “Africanized” have been used interchangeably although the former really refers to the pure race and the latter to the hybrid. The spread of African bees throughout South and Central America, fueled by rapid hybridization with European subspecies and the dominance of African alleles over European ones, occurred at a rate of 200–300 miles per year. Because their

ovement through South and Central America m was rapid and largely unassisted by humans, African bees earned the reputation of being the most successful biologically invasive species of all time. In 1990, populations of African honey bees had saturated South and Central America and begun to move into the USA. As of 2006, African honey bees were established in the southernmost USA: Texas, California, New Mexico, Arizona, Oklahoma, Louisiana, Arkansas, Alabama, and Florida.


The spread of African bees in the U.S. continues, albeit at a much slower rate than what occurred throughout South and Central America. This slowed rate of territory expansion appears due to climatic limitations. African bees do not survive in temperate climates as well as European bees do. Therefore, they have failed to establish populations below about 32° latitude in the southern hemisphere. Although they have expanded beyond this parallel in the northern hemisphere, African bee expansion northward also appears limited climatically, being found only below about 34° latitude currently.

Description and Behavior African honey bees cannot be distinguished from European honey bees easily, although they are slightly smaller than the various European races. Laboratory personnel use morphometric analyses to determine the likelihood that a given colony is Africanized or fully African. With honey bees, the measurement of wing venation patterns and the size and coloration of various body parts (morphometry) are important determinants of identification at the subspecific level. Morphometry has been used to differentiate honey bee races since the 1960s and remains the first round of identification when suspect colonies are discovered. Morphometric analyses were first used to differentiate Africanized and European honey bees in South America in 1978. A more rigorous identification is achieved by genetic analysis and often is necessary when the suspect bees are a hybrid between African bees and the European subspecies. Other differences between African and European bees manifest themselves behaviorally. To the casual bystander, the primary identifying behavioral characteristic of Africanized bees is their heightened defensiveness compared to that of European subspecies. Selection pressures induced by man are, in part, responsible for this increased defensiveness.“Beekeeping” (management

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of honey bee colonies by humans) is more common in Europe, where the native honey bees have been bred for gentleness and ease of management. In contrast, “honey hunting” (near-complete destruction of hive to harvest contents) is more common in Africa, resulting in a bee that is more defensive of its nest. Other selection pressures that led to a heightened defensiveness in African bees include climatic stresses, resource availability, and predation by birds, mammals, and various reptiles. These selection pressures resulted in an African race of bee that can be 10 + times more defensive than any of the various European races of bee. All honey bees readily defend their nests, and an attack usually means that the victim is too close to the nest. While European races of bees may attack a nest intruder with >10 bees, African bees may attack the same intruder with >1,000 bees. Further, African bees defend a larger radius around their nest and require lower levels of stimuli to initiate an attack. Because of these characteristics, African bees are capable of killing large mammals, including man. This defensiveness has earned them the nickname “killer” bee. It is important to note that their ability to kill humans has nothing to do with their size or the potency of their venom. African bees are smaller than European bees and probably deliver a comparatively smaller dose of venom to their victim than do European bees. Because both bees use the same type of venom, human deaths are a result of the number of stings they receive rather than an increased potency of African bee venom. Another behavioral difference between African and European bees concerns colony level reproduction and nest abandonment. African honey bees swarm and abscond in greater frequencies than their European counterparts. Swarming, bee reproduction at the colony level, occurs when a single colony splits into two colonies, thus ensuring survival of the species. European colonies commonly swarm 1–3 times per year. African colonies may swarm >10 times per year. African swarms tend to be smaller than European ones, but the

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African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier (Hymenoptera: Apidae), Figure 23 (a) African bees swarm readily and nest in unusual locations, including (b) exposed on tree limbs, (c) within cavities in the soil, (d) within discarded furniture.

swarming bees are docile in both races. Regardless, African colonies reproduce in greater numbers than European colonies, quickly saturating an area with African bees. Further, African bees abscond frequently (completely abandon the nest) during times of dearth or repeated nest disturbance, while this behavior is atypical in European bees. Another common difference between African and European honey bees is their choice of nest locations. African honey bees are less selective when considering a potential nesting site than are European bees. They will nest in a much smaller

volume than European honey bees and have been found in water meter boxes, cement blocks, old tires, house eaves, barbecue grills, cavities in the ground, and hanging exposed from tree limbs, just to name a few places. One rarely finds European colonies in any of these locations because they prefer to nest in larger cavities like those provided by tree hollows, chimneys, etc. As one can imagine, humans inadvertently provide multiple nesting sites for African bees. Therein lies the primary reason African bees are encountered frequently by humans (Fig. 23).


A final behavioral curiosity of African bees concerns nest usurpation (or colony takeover) of European colonies. Small African swarms containing a queen often land on the outside infrastructure of a European colony (a wall, beekeeper-managed hive, etc.). As time passes, the worker bees in the African swarm begin to exchange food/pheromones with the European workers from the colony. This gradually ensures the adoption of the African bees into the European colony. Somewhere during this process, the European queen is lost (perhaps killed by the African bees – her fate remains uncertain at this point) and the African queen is introduced into the colony, thus becoming the reigning matriarch. European bees do not display this behavior but often fall victim to it, thus creating an African colony from a preexisting European one. Other behavioral differences between African and European races exist and are worth discussing briefly. For example, African bees are more “flighty” than European bees, meaning that when a colony is disturbed, more of the bees leave the nest rather than remain in the hive. African bees use more propolis (a derivative of saps and resins collected from various trees/plants) than do European bees. Propolis is used to weather-proof the nest and has various antibiotic properties. African colonies produce proportionally more drones (male bees) than European bees. Their colonies grow faster and tend to be smaller than European colonies. Finally, they tend to store proportionately less food (honey) than European bees, likely a remnant of being native to an environment where food resources are available throughout the year.

Life Cycle and Genetic Dominance Mating biology and developmental time play an important role in the success of African bee colonies in replacing European colonies in an area. For the most part, mating and developmental biology are similar for African and European

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bees, but key differences confer adaptive benefits to the former. Virgin queens of all western honey bees emerge from peanut hull-shaped waxen cells. After a short time of further maturation, a virgin queen will leave the colony to mate with drones. All mating occurs in the air, with the fastest drones being the most successful suitors. Queens will mate multiple times over the course of 7–10 days and during this time they will mate with an average of 12–20 drones. Queen bees store semen in an organ called a spermatheca. African colonies produce more drones/colony so drone populations in an area tend to favor African bees. As such, virgin European queens are more likely to mate with African drones rather than European ones. Further, flight time and distances of mating flight from the colony tend to result in European queens encountering African drones more often than European drones, thus setting the stage for hybridization. All honey bees undergo complete metamorphosis but the time from egg to adult varies by subspecies. The newly-mated queen bee oviposits in wax cells constructed by worker bees. Fertilized eggs result in female offspring, either workers or queens. If fed a diet rich in royal jelly, the female larva will develop into a queen, with the reciprocal true for the development of workers. Drones result from unfertilized eggs and consequently only inherit genetic material from their mother (they have no father). Developmental time varies by caste member (see Table 4) and favor African honey bees because they generally develop faster than European bees. When bee colonies decide to make a new queen, newly emerged female larvae are fed royal jelly constantly. Because Africanized offspring, including queens, develop faster than European offspring, a queen having an African genotype is more likely to emerge earlier than a queen with a European genotype. The first queen to emerge kills all of her queen sisters that have not yet emerged from their cells. The Africanized virgin proceeds to mate in an area having higher densities of African drones. Over time, this results

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in the colony becoming more African with the European phenotype being replaced almost altogether. This process is exacerbated further due to the dominance of African genetic traits over European ones. Finally, African bees are more resistant to many honey bee pests/pathogens than are European bees. Western honey bees face a myriad of pests and diseases, the most severe of which include varroa mites (Varroa destructor), tracheal mites (Acarapis woodi), small hive beetles (Aethina tumida), and American foulbrood (Paenabacilis larvae). These bee pests almost eliminated all wild colonies of European honey bees in North America. Because African bees are resistant to many of these pests/diseases, their survivorship in the wild is favored over that of European bees.

Public Risks Due to their heightened defensive behavior, African honey bees can be a risk to humans. Children, the elderly, and handicapped individuals are at the highest risk of a deadly attack due to their inability or hampered ability to escape an attack. African honey bees are agitated by vibrations like those caused by power equipment, tractors, lawn mowers, etc. Further, their nesting habits often put them in close proximity to humans. Because of this, precautions should be taken in an area where

African Honey Bee, Africanized Honey Bee, or Killer Bee, Apis mellifera scutellata Lepeletier ( Hymenoptera: Apidae), Table 4 The developmental time in days (from egg to adult) of European and African honey bees  

European honey bees

African honey bees

Queen

16

14

Worker

21

19–20

Drone

24

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Africanized honey bees have been established. These precautions are not suggested to make people fearful of honey bees but only to encourage caution and respect of honey bees. The precautions include remaining alert for honey bees flying into or out of an area (suggesting they are nesting nearby), staying away from a swarm or nest, and having wild colonies removed from places that humans frequent. The latter is perhaps the most important advice one can heed when dealing with African bees. In the USA, a large percentage of African bee attacks occur on people who know a nest is present but elect not to have it removed (or try to do it themselves). If an attack occurs, remembering a few simple recommendations will increase one’s chances of minimizing the effects and severity of the attack. If attacked, a victim should run away from the area using his shirt to cover his head and especially airways. Running through tall grass or small trees will help to disrupt the attacking bees. The victim should not stand and swat at the bees. The bees are defending their nest, and the victim needs to get away from that nest as quickly as possible. It is important that the victim get cover in a bee-proof vehicle or structure if either is available. One should not jump into the water or hide in bushes. The bees can remain defensive and in the area for some period of time, thus increasing the risk to the victim. If stung, the victim should remove the stinger quickly by scraping it rather than by pulling it. One should see a doctor immediately if breathing is affected. Many African bee attacks can be prevented by limiting the number of nesting sites that are available to the bees. A homeowner, school worker, etc. can “bee proof ” his or her property by eliminating possible nesting sites. This can be accomplished by removing any unnecessary debris from an area and closing off wall, chimney, electrical and plumbing-related gaps that are >30 mm using a small-mesh hardware cloth or caulking. This will limit bee access to potential nesting sites. Finally, one should check walls and eaves of structures regularly, looking for bee activity.


Managing African Bee Colonies It is important to remember that African honey bees pollinate crops and produce honey just like other races of honey bees. Beekeepers in South Africa use African honey bees as the bee of choice in their operations. So, African bees can be managed efficiently and safely but the skills required to manage African bee colonies differ from those required to manage European bee colonies. In general, the management of African bee colonies has been discouraged in the US while accepted in Central and South America. This may have to do with the public perception of honey bees, particularly African bees, in the USA and the robust legal system in place in the USA. On the other hand, beekeepers in Central and South America routinely use African bees in their operations with slight management modifications. In fact, some South American countries are among the leading honey producers in the world, due largely to the presence of African bees in the country. Beekeepers in South and Central America utilize a number of management practices in order to keep African bees. First, they keep single bee colonies on individual hive stands rather than using one hive stand for multiple colonies. This limits the management activity to one colony at a time rather than aggravating other colonies while working only one. Secondly, beekeepers in South and Central America use ample amounts of smoke when working African bee colonies. It is believed that smoke masks the alarm pheromone of the bees, thus lessening the defensive response of the colony. Most South and Central American beekeepers agree that copious amounts of smoke should be used when working African bee colonies. It is important to smoke the colonies well before any work is done, for once bees from a colony are agitated, smoke may fail to calm them down. Beekeepers managing African bees wear appropriate protective gear. A typical beekeeper working an African colony would wear a full bee

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suit, boots, gloves, and a bee veil. Bee veils (protective headgear) are worn by almost all beekeepers worldwide. Traditionally, the veil mesh protecting the face is colored black to keep down the sun’s glare. African bees (and most honey bees) attack dark colors so black-faced veils often get covered with bees. Consequently, beekeepers can use white-faced veils to keep the bees off of their veils. Beekeepers managing African colonies often tape their bee suits to their boots and gloves to limit the possibility of bee access. Finally, some beekeepers in areas with African bees try to requeen African bee colonies with European queens. This is not a common practice in sub-Saharan Africa. Most African beekeepers in areas having African bees gladly use the bee in their operations, paying little attention to the bees’ defensiveness.

Conclusion The economic impact of African bees in an area can be substantial. Keepers of European bees often notice a decrease in resource availability for their bees because of the density of African bee colonies in an area, and thus the demand on the available resources is high. Furthermore, cities, municipalities, etc., often initiate eradication programs, with much futility. Finally, the loss of animal and human lives is a tragic occurrence, being beyond measurable cost. African bees also may affect the environment negatively. Colony densities as high as 300 African bee colonies per square mile have been suggested. If true, African bees may have a substantial impact on the native flora and fauna in an area. While this impact often is not reported and largely is not understood, it could be significant considering the potential number of colonies and their need for resources. Thus, the world’s most infamous honey bee is among nature’s most enigmatic creatures.  Apiculture (Beekeeping)  Honey Bee

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African Horse Sickness Viruses

References Caron DM (2001) Africanized honey bees in the Americas. The A.I. Root Co., Medina, OH, 228 pp Hepburn HR, Radloff SE (1998) Honeybees of Africa. Springer-Verlag, Berlin, 370 pp Winston ML (1992) Killer bees: the Africanized honey bee in the Americas. Harvard University Press, Cambridge, MA, 176 pp

African Horse Sickness Viruses cynthia c. lord University of Florida, Florida Medical Entomology Laboratory, Vero Beach, FL, USA African horse sickness is a highly fatal, noncontagious disease of equines, particularly horses. The African horse sickness virus group consists of nine serotypes, in the genus Orbivirus, family Reoviridae. It is closely related to the bluetongue viruses, which cause disease in cattle and sheep. Infection with any of the serotypes of African horse sickness virus usually results in severe disease and high mortality in horses. Donkeys and mules generally exhibit less severe disease and lower mortality, while wild equids such as zebra generally show no signs of disease or mortality after infection. The serotypes are differentiated based on the host immune response, and there is some cross reaction between serotypes. All nine serotypes are endemic to sub-Saharan Africa, and have caused serious epidemics when introduced outside this area. African horse sickness has had a significant impact on the history of some parts of Africa, as horses could not be used in exploration and farming. Outbreaks of African horse sickness have a significant economic impact, resulting from the direct loss of animals, the costs of control programs, and trade regulations and quarantines restricting movement of equines from infected areas. The virus is transmitted by biting midges in the genus Culicoides. Culicoides imicola has been implicated in most outbreaks, while in endemic areas there may be several species of Culicoides

midge involved in the transmission cycle. Most species of equines can develop viremias sufficiently high to infect midges. Some tick species have been shown to be able to become infected and transmit the virus in the laboratory, but the importance of this transmission route in nature is unknown. In endemic areas, African horse sickness viruses circulate primarily between midges and zebra, and frequently multiple serotypes are present. Transmission rates can be very high. For example, in the Kruger National Park, South Africa, zebra foals typically are exposed to all nine serotypes by the time they are 1 year old. The first outbreak outside the sub-Saharan zone began in 1959 in Saudi Arabia and Iran, spreading to involve Afghanistan, Pakistan, Syria, Lebanon, Jordan, Iraq, Turkey, Cyprus and parts of India before being controlled by vaccination campaigns and the loss of most susceptible horses by the end of 1961. Another outbreak occurred in North Africa in 1965, crossing into Spain in 1966. An outbreak of African horse sickness serotype 4 virus began in central Spain in 1987 and ultimately encompassed a large part of Spain, along with parts of Portugal and Morocco. This outbreak was the first recorded instance of an African horse sickness virus overwintering outside of Africa. African horse sickness cases occurred for four subsequent years in Spain, and it was not eradicated until 1990. The most likely route of introduction was via zebra imported from Namibia. Control and eradication of the virus was achieved only by extensive vaccination campaigns and slaughter of infected or exposed equines. It is estimated that 2,000 horses died and over 350,000 were vaccinated during this outbreak. In 1989, an outbreak of serotype 9 occurred in Saudi Arabia. Spain was divided into African horse sickness-free and infected regions, in order to allow movement of horses for the 1992 Olympics held in Barcelona. No vaccination was allowed in the African horse sickness-free region, so that any transmission activity would be observed. Equine movement out of the infected region was prohibited.

African Horse Sickness Viruses

A similar strategy is used in South Africa, with an African horse sickness-free zone in the Western Cape Province, based on historically low incidence of African horse sickness, and that C. imicola is rare. Surrounding this zone is a surveillance zone and a protection zone. No vaccination is allowed in the free and surveillance zones, and strict movement controls are in place for equines moving from other areas of the country. The zoning creates an area where animals can be held prior to exportation. In 1999, there was an outbreak of African horse sickness in the surveillance zone, opening debate about the effectiveness of the movement restrictions and the vector species involved. Currently, the zoning is still in place and there have not been further outbreaks in the African horse sickness-free zone. Clinical signs of African horse sickness in horses generally begin with fever. There are three forms of African horse sickness disease in horses: pulmonary, cardiac, and febrile. The febrile form, often referred to as horse sickness fever, does not progress beyond fever and generally resolves. The pulmonary form begins with fever and progresses to respiratory difficulty, coughing and nasal discharge. Death is due to pulmonary edema and cardiac failure. The cardiac form also begins with fever, and subsequently edemas develop around the head, neck and chest. Death results from cardiac insufficiency and progressive pulmonary edema. Mortality rates can be as high as 95% in horses, although donkeys and mules are much less susceptible and mortality rates are much lower. Movement of donkeys may be important in the spread of these viruses outside the endemic area, as they are rarely clinically ill and so infected animals are not noticed. There is variation in virulence between the nine African horse sickness serotypes, along with differences between breeds of horse and individual immune responses to the virus. Vaccines have been developed against these viruses, but due to the immunological differentiation between the serotypes, cross protection is not complete and full protection requires vaccination against each serotype. Routine vaccination of

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horses, against all serotypes, is practiced in endemic areas. Elsewhere, vaccination generally is not used routinely or is not allowed. In outbreak situations, the virus is first typed to determine the serotype involved, then vaccination is targeted against that serotype only. Most countries restrict importation of equids from endemic countries. An extended quarantine period usually is imposed, thus restricting the movement of horses for competition. Because it is difficult to differentiate between vaccinated and infected animals, generally there are restrictions on importing vaccinated animals. Antibodies to African horse sickness viruses have been found in other animals such as elephants, camels, and bovines, but there is no apparent illness and their impact on the transmission cycle is not known. Dogs can become infected and die by eating meat from the carcass of an infected animal. Antibodies to African horse sickness have been found in wild canids and other carnivores, most likely also via feeding on infected carcasses. Humans have been infected only rarely, generally through laboratory accidents with vaccine strains. African horse sickness has never been found in the New World. However, there are species of Culicoides, particularly the C. variipennis complex, present throughout the U.S. Some members of this complex are competent vectors of African horse sickness viruses in the laboratory, and will be competent vectors in the field should an African horse sickness virus be introduced. Vector competence for the C. variipennis complex varies considerably for the closely related bluetongue viruses, but we lack information on similar variation for African horse sickness viruses. The implications of this for an introduction of any of the African horse sickness viruses is unknown, but requires further study.

References Bram RA, George JE, Reichard R, Tabachnick WJ (2002) Threat of foreign arthropod-borne pathogens to livestock in the United States. J Med Entomol 39:405–416

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Africanized Bees

Holbrook FR, Tabachnick WJ, Schmidtmann ET, McKinnon C, Bobian RJ, Grogan WL (2000) Sympatry in the Culicoides variipennis complex (Diptera: Ceratopogonidae): a taxonomic reassessment. J Med Entomol 37:65–76 House JA (1993) Recommendations for African horse sickness vaccines for use in nonendemic areas. Rev élev Méd Vét Pays Trop 46:77–81 Mellor PS, Boorman J (1995) The transmission and geographical spread of African horse sickness and bluetongue viruses. Ann Trop Med Parasitol 89:1–15 Mellor PS, Boorman J, Baylis M (2000) biting midges: their role as arbovirus vectors. Annu Rev Entomol 45:307–340

Africanized Bees Honeybees in the Western Hemisphere that are derived from hybridization of African and European subspecies of Apis mellifera. The degree of hybridization is unresolved.  Bees  Honeybee  African Honey Bee

African Mahogany-Feeding Caterpillar, Heteronygmia dissimilis aurivillius (Lepidoptera: Lymantriidae) hans g. schabel University of Wisconsin, Stevens Point, WI, USA Several genera and species of mahoganies in various parts of the tropics are highly valuable timber species, among them African mahogany (Khaya spp.). Relatively few defoliators are known to target this genus, among them caterpillars of several silkmoths, the nymphalid Charaxes and the lymantriid Heteronygmia. Only the latter, presumably monophagous on Khaya, appears to have pest potential as indicated by small-scale outbreaks observed in Morogoro, Tanzania, in the 1980s. A succession of four generations per year allow Heteronygmia dissimilis to be active most of the year, except for a period of estivation during the hottest season, i.e., from November to February. Eggs are found from early March to late October

with peaks from May to August, i.e., during the cool, dry season. Egg clusters are located mostly on the lower trunks of trees and consist of 24–130 glossy, globular or dimpled spheres, each about 1 mm in diameter. They hatch 6–10 days after oviposition, depending on the season (Fig. 24). Caterpillars of various instars are found anytime between early March to the end of November, with periods of greatest abundance from June to September. All larval instars are hairy and last instars occur in two color phases. One of them is milky-green; the other, more common one, a highly camouflaged, brown to greyish-white mottled bark pattern including up to three, more or less distinct dorsal saddles. Caterpillars feed solitarily, and move with great speed and agility when disturbed, including a hopping and ballooning response during the first four instars. Early instars skeletonize Khaya leaflets at night and spend the day motionless on or underneath leaflets. Older instars are free feeders and rest on the lower trunk during the day. All instars shun the foliage of just-expanding shoots. There are five instars in males and six in females, each of them lasting from 5–6 days. Pupae are found from late February to early December, abundantly so from June to September. They often are cradled in loose leaf shelters tied together by sparse strands of silk or in other hiding places, such as under bark scales. The moths are present from February to mid-November, most abundantly so from May to September. They rest during the day and are attracted to lights at night. Slender male moths are light to dark or reddish brown with substantial plumose antennae, whereas the white to cream-colored females are bigger and more robust with smaller antennae. Males have wingspans of about 40 mm and are able fliers, while females with wingspans of about 50 mm, are reluctant to take to the air and then only as poor fliers. Both sexes have faint to more pronounced grey line markings and a small black dot on each front wing. Before oviposition, the greatly distended abdomen of the female is greenish. Male moths reach adulthood after an average of 41 days (September/October), females after about 45

African Mahogany-Feeding Caterpillar, Heteronygmia dissimilis aurivillius (Lepidoptera: Lymantriidae)

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African Mahogany-Feeding Caterpillar, Heteronygmia Dissimilis aurivillius (Lepidoptera: Lymantriidae), Figure 24 Egg (top left) (2x), last instar larva (top right) (1x), pupa (bottom left) (1.7x) and (mating) adult stages (bottom right) (2x) of Heteronygmia dissimilis, respectively. Both sexes are represented in the bottom figures, the larger females being above in each picture. (Photo: H. Schabel et al. 1988; reprinted with permission from ICIPE, the International Centre of Insect Physiology and Ecology.)

days of development. On the average, each female produces about 200 eggs, laid in several batches. While no field control of Heteronygmia has been undertaken to date, a laboratory study documented full protection of Khaya leaves from defoliation by H. dissimilis, following application of 1% crude, aqueous seed extracts of the neem tree (Azadirachta indica).

Numerous arthropod predators of the caterpillars and pupae are believed to be generalists with little impact. On the other hand, four hymenopterous and two dipterous parasites affecting various stages of H. dissimilis seem more specific. Seasonally, egg parasites in particular had significant impacts on this insect and in conjunction with the fungus Paecilomyces farinosus, which severely

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African Maiden Moths (Lepidoptera: Thyretidae)

ecimated pupae during the rainy season, were d responsible for serious setbacks in the annual buildup of H. dissimilis. As a result, natural controls seem to be quite effective with this insect.

References Ballard E (1914) Two pests of mahogany in Nyasaland. Bull Entomol Res 5:61–62 Rwamputa AK, Schabel HG (1989) Effects of crude aqueous neem extracts on defoliation of Khaya nyasica by Heteronygmia dissimilis (Lepidoptera: Lymantriidae) in East Africa. In: Alfaro RI, Glover SG (eds), Proceedings, IUFRO Working Group on Insects Affecting Afforestation, XVIII International Congress of Entomology. Vancouver, British Columbia, Canada, pp 245–250 Schabel HG, Schabel A, Msanga HP (1988) Bioecological aspects of the mahogany defoliator Heteronygmia dissimilis in Morogoro, Tanzania. Insect Sci Appl 9:179–184

African Maiden Moths (Lepidoptera: Thyretidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA African maiden moths, family Thyretidae, include 212 species, all African. The classification remains controversial and various specialists also place the group within Arctiidae. The family is in the superfamily Noctuoidea, in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults medium-size (23–57 mm wingspan). Haustellum usually reduced or vestigial; antennae pectinate; wings very elongated, with reduced hindwings (some with greatly reduced hindwings). Maculation typically dark with white or hyaline patches, or more colorful. Adults perhaps mostly diurnal; often wasp mimics. Larvae are thought to be leaf feeders, but most species remain unknown biologically. Host plant records include Thymelaeaceae and Ulmaceae, for the few species known biologically.

References Janse AJT (1945) On the South African species of Metarctia, with the description of a new species. J Entomol Soc South Africa 8:91–98 Kiriakoff SG (1949) Over de phylogenie van de Thyretidae fam. nov. (Lepidoptera). Natuurwetenschappen Tijdschrift 30:3–10 Kiriakoff SG (1953) Les Thyretidae du Musée Royal du Congo Belge (Lepidoptera Notodontidae). Annales du Musée Royal du Congo Belge, Sciences Zoologiques (8) 26:1–91 Kiriakoff SG (1957) Notes sur les Thyretidae (Lepidoptera: Notodontidae). Bulletin et Annales de la Société Royale Entomologique de Belgique 93:121–160 Kiriakoff SG (1960) Lepidoptera. Fam. Thyretidae. In: Genera Insectorum. Brussels, 214:1–66

African Pine-Feeding Grasshoppers, Plagiotriptus pinivorus (Descamps) and P. Hippiscus (Gerst.) (Orthoptera: Eumastacidae) hans g. schabel University of Wisconsin, Stevens Point, WI, USA These grasshoppers are excellent examples of indigenous insects that developed a preference for an exotic plantation-grown crop, in this case pines. Plagiotriptus pinivorus attained some prominence after causing persistently severe defoliation of exotic pines, especially Pinus patula, in Malawi in the 1960s, resulting in significant tree mortality. A smaller scale defoliation of P. patula was observed at Morogoro in Tanzania in the mid1980s, which was attributable to another, very closely related species, Plagiotriptus hippiscus. Both of these grasshoppers are highly polyphagous, including herbaceous hosts, shrubs and both angiosperm and gymnosperm trees. The prime requirement for P. pinivorus seems to be access to evergreen or semi-evergreen vegetation in areas of moderate to heavy rainfall, i.e., mostly at altitudes between 1,525–2,135 m, but occasionally as low as 490 m.

African Pine-Feeding Grasshoppers, Plagiotriptus pinivorus (Descamps) and P. Hippiscus (Gerst.) (Orthoptera: Eumastacidae

Plagiotriptus pinivorus in Malawi exhibits three generations every 2 years, and the complete life cycle takes about 1 year. Nymphs and adults have been observed on pines throughout the year, except from December to late January. Copulation occurs anytime, but peaks from October to January and May to June. During copulation, the small male assumes a characteristic dorso-lateral position by clinging to one of the hind femurs of the female. Both males and females are promiscuous. About 7–20 days after the last mating, females seek bare soil and dig a shallow pit to lay a batch of up to six eggs. They then resume voracious feeding in the trees, before laying other batches of eggs at 17–35 day intervals. Eggs incubate from 49–248 days, with an average of 115 days. The winter population hatches from April to May, maturing in November, while the summer population hatches from December to January and matures from May to July. Within the same batch, an average of 34 days and a maximum of 88 days may elapse between first and last hatch. Nymphal peak emergence and rainfall are strongly correlated in February, allowing prediction

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of emergence two weeks in advance. Another smaller peak in emergence in August, however, cannot be explained by rainfall. The first instar nymph is ephemeral (about 12 h), and will molt immediately when reaching the soil surface, before feeding on ground vegetation for the next 2–3 weeks. Advanced instars complete their life cycle on trees, each instar lasting about one and a half to over two months. Young instars are wasteful feeders. There are generally six instars for males and seven for females. Despite the extra instar, females develop more rapidly and reach adulthood at about the same time as do males. Adult males (Fig. 25) are about 1.5–2 cm long, moderately robust grasshoppers. Their abdomen, shield-like pronotum and greatly enlarged hind femora are strongly compressed. A minute set of non-functional wings, not found on nymphs, is hidden under the pronotum. The thread-like antennae are about one third the length of the head. The abdomen is strongly reflexed over the back in the male. The insect is largely leaf-green, but sports inconspicuous, small areas of blue, pink, red and white on various parts of the legs, wings, antennae and the pronotal

African Pine-Feeding Grasshoppers, Plagiotriptus pinivorus (Descamps) and P. hippiscus (Gest.) (Orhthoptera: Eumastacidae), Figure 25 Plagiotriptus hippiscus female (above) and male (below) with size comparison (shaded) (drawing, Paul Schroud).

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African Primitive Ghost Moths (Lepidoptera: Prototheoridae)

ridge. Eyes are golden yellow. Females are about twice the size of males, more robust and generally less compressed. They are uniformly leafgreen, except for the golden yellow eyes and valves of the ovipositor. Their wings are also minute and hidden under the pronotal shield. Numerous invertebrate and vertebrate predators, including skinks, birds and blue monkeys, as well as parasites were documented, but ultimately they were deemed insufficient by themselves to reduce populations of the grasshopper to non- damaging levels. As a result, sticky bands and chemical controls were relied on for monitoring and control purposes, respectively. In the 1960s in Malawi, gamma-BHC at 0.5% proved the most effective insecticide for ground and aerial applications at ultra-low volume formulations. Spraying of road banks was particularly recommended, as insects clustered there for oviposition in the bare ground.

References Lee RF (1972) A preliminary account of the biology and ecology of Plagiotriptus spp. (Orthoptera: Eumastacidae). Malawi Forest Research Institute Research Record 48, Forestry Research Institute of Malawi, Zomba, 100 pp Schabel HG, Hilje L, Nair KSS (1999) Economic entomology in tropical forest plantations: an update. J Trop For Sci Xth Anniversary Issue: 303–315.

African Primitive Ghost Moths (Lepidoptera: Prototheoridae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA African primitive ghost moths, family Prototheoridae, comprise 12 species of small moths from South Africa. The family is in the superfamily Hepialoidea, in the infraorder Exoporia. Adults small (18–mm wingspan), with head rough-scaled; haustellum reduced and vestigial mandibles

present; labial palpi long and porrect, 3-segmented; maxillary palpi short and 3-segmented; antennae short. Maculation is brown or gray, with various darker spots. Biologies and larvae remain unknown.

References Davis DR (1996) A revision of the southern African family Prototheoridae (Lepidoptera: Hepialoidea). Entomol Scand 27:393–439 Davis DR (2001) A new species of Prototheora from Malawi, with additional notes on the distribution and morphology of the genus (Lepidoptera: Prototheoridae). Proc Entomol Soc Wash 103:452–456 Davis DR (2003) Prototheoridae. In: Lepidopterorum Catalogus, (n.s.). Fasc. 11. Assoc Trop Lepid Gainesville, 8 pp Janse AJT (1942) Prototheoridae. In: Janse AJT (ed) The moths of South Africa, Pretoria, 4(1): 65–74

African Red Tick, Rhipicephalus evertsi, (Acarina: Ixodidae) This important tick, known as African red tick, affects ungulates in Africa.  Ticks

African Skipper Moths (Lepidoptera: Apoprogonidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA African skipper moths, family Apoprogonidae, includes only a single species from South Africa. The family is in the superfamily Uranioidea, in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults medium size (46–56 mm wingspan), with head rough scaled and eyes large; haustellum naked; labial palpi porrect; maxillary palpi minute, 1-segmented; antennae clubbed (hooked at tip). Wings triangular and

African Swine Fever

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African Slug Caterpillar Moths (Lepidoptera: Chrysopolomidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA

African Skipper Moths (Lepidoptera: Apoprogonidae), Figure 26 Example of African skipper moths (Apoprogonidae), Apoprogones hesperidis Hampson from South Africa.

short; body robust. Maculation dark gray with some pale markings, plus pale discal spot on fore- and hindwings. Adults presumed diurnal, but nothing is known of the biology or larvae (Fig. 26).

References Janse AJT (1932) Family Sematuridae. In: The moths of South Africa, 1:87–89. Pretoria [Apoprogones] Seitz A (1926) Subfamilie: Apoprogeninae [sic]. In: Seitz A (ed) Die Gross-Schmetterlinge der Erde. Teil 14. Die afrikanischen Spinner und Schwärmer, pl. 1. A. Kernen, Stuttgart, pp 16–17

African Sleeping Sickness A disease of humans caused by protozoans in the genus Trypanosoma. It is also known as human sleeping sickness or human trypanosomiasis. The same disease, when infecting other vertebrate animals, is called nagana. It is transmitted by tsetse flies in Africa.  Sleeping Sickness or African Trypanosomiasis  Trypanosomes  Tsetse Flies  Nagana

African slug caterpillar moths, family Chrysopolomidae, are a small African family of about 30 known species. Two subfamilies are known: Ectropinae and Chrysopolominae. The family is in the superfamily Cossoidea (series Limacodiformes) in the section Cossina, subsection Cossina, of the division Ditrysia. Adults medium size (24–52 mm wingspan), with head scaling smooth; haustellum and maxillary palpi absent; antennae short and bipectinate in males. Body robust. Wings rounded and broad (some with irregular distal margins). Maculation mostly pale brown, often with subapical wing line and light discal spot; hindwing with forewing line and coloration continued (Fig. 27). Adults nocturnal as far as is known. Larvae leaf-feeding and slug-like, with small spines; often colorful. Host plants include Celastraceae. No economic species are known.

References Aurivillius C (1911) Chrysopolomidae. In Lepidopterorum catalogus, 1:1–4. W. Junk, Berlin. Hering EM (1928) Familie: Chrysopolomidae. In: Seitz A. (ed) Die Gross-Schmetterlinge der Erde. Teil 14. Die afrikanischen Spinner und Schwärmer, pl. 76. A. Kernen, Stuttgart, pp. 477–479 Herring EM (1937) Revision der Chrysopolomidae (Lep.). Ann Transvaal Mus 17:233–257, pl. 9

African Swine Fever A viral disease of hogs, this tick-transmitted disease is found on several continents.  Ticks

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Agaonidae (Hymenoptera)

opening. The females of some species actively gather and carry pollen in thoracic pockets or specialized leg structures. The cultivated fig, Ficus carica, has many varieties that no longer rely on pollination to produce edible ripe syconia. However, a few varieties still require the pollination service provided by the agaonid partner, Blastophaga psenes.  Wasps, Ants, Bees and Sawflies  Fig Wasps

African Slug Caterpillar Moths (Lepidoptera: Chrysopolomidae), Figure 27 Example of African slug caterpillar moths (Chrysopolomidae), Chrysopoloma similis Aurivillius from South Africa.

Agaonidae (Hymenoptera) hannah nadel USDA-ARSSan Joaquin Valley Science Center, Parlier, CA, USA A tropical family of about 750 species of miniscule wasps (order Hymenoptera) that are mutualistically associated with fig plants (Ficus spp.). The associations are usually between a unique pair of fig and wasp species and are crucial for the reproduction of both. The winged female wasp enters a young floral receptacle, the flask-like syconium, and lays single eggs in many of the tiny female flowers lining its inner surface. Carrying pollen from her natal fig, she deposits it onto the stigmas during oviposition, ensuring seed production for the fig and food for her own offspring. The syconium will generally not ripen without pollination. The female is trapped inside the syconium and dies there. After the larvae develop and pupate in seed-galls, the wingless adult males emerge first and chew holes into galls to mate with the quiescent females inside, and then cooperatively chew an opening through the syconial wall. The changed atmosphere inside the syconium wakes the females, which chew out of their galls, actively or passively pick up pollen, and leave through the

References Bronstein JL (1988) Mutualism, antagonism, and the fig-pollinator interaction. Ecology 69:1298–1302 Galil J, Eisikowitch D (1968) On the pollination ecology of Ficus sycomorus in East Africa. Ecology 49:259–269 Galil J, Zeroni M, Bar Shalom D (Bogoslavski) (1973) Carbon dioxide and ethylene effects in the co-ordination between the pollinator Blastophaga quadriceps and the syconium in Ficus religiosa. New Phytol 72:1113–1127 Machado CA, Jousselin E, Kjellberg F, Compton SG, Herre EA (2001) Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps. Proc R Soc London B 268:685–694 Ramirez BW (1969) Fig wasps: mechanisms of pollen transfer. Science 163:580–581 Weiblen GD (2002) How to be a fig wasp. Annu Rev Entomol 47:299–330 Wiebes JT (1966). Co-evolution of figs and their insect pollinators. Annu Rev Ecol Syst 10:1–12

Agathiphagidae A family of moths (order Lepidoptera). They commonly are known as Kauri moths.  Kauri Moths  Butterflies and Moths

Agassiz, Jean Louis Rodolphe Louis Agassiz was born at Môtier-en-Vuly, Switzerland, on May 28, 1807. He displayed an early interest in natural history. In 1824 he entered Universität Zürich for medical training, then

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moved to Universität Heidelberg in Germany. In Heidelberg his interest in natural history increased. His next move was to Universität München and, while there in 1829 and still only 21 years old, he published a work on Brazilian fishes, using the collected materials of von Martius and von Spix. His next zoological endeavor was to begin research on fossil fishes. In 1831, he moved to Paris still with the ambition of completing his medical training. However, he spent part of each day studying fossil fishes and he came under the influence of Cuvier and adopted the latter’s views of creation. Thus, according to Agassiz, each species was the result of separate creation, not of evolution. In 1832–1846 he was a professor at Université de Neuchâtel, Switzerland. In 1836, Louis began to study glaciers and their effects, on which he published works in 1840, 1846 and 1847. In Switzerland, he also published a large catalog “Nomenclator zoologici” of the names of animals, of which some fascicles were on insects. In 1846 he moved to the USA, was welcomed as a famous scientist, and in 1848 was appointed professor of zoology and geology at Harvard University. At Harvard, he clashed with Asa Gray, professor of botany, about evolution, because Gray supported Darwin’s theory. However, it was Louis’ efforts and influence that led to the foundation of the Museum of Comparative Zoology at Harvard University, an institution that became very influential in research on insect systematics. He also was a cofounder of the U.S. National Science Foundation. He died in Cambridge, Massachusetts, on December 14, 1873. His son Alexander and two daughters of his first marriage accompanied him to the USA (his first wife having died in Switzerland). Alexander Agassiz (1835–1910) likewise became a zoologist. Louis Agassiz remarried in 1850 in the USA.

Nordenskiöld E (1935) The history of biology: a survey. Tudor, New York, 629 pp.

References

This term is used to refer to insects that lack mandibles, which essentially means that they lack mouth structures.  Mouthparts of Hexapods

Anon (1998) Jean Louis Rodolphe Agassiz. Encyclopedia of world biography, 2nd ed. Gale, Detroit, MI

Age Polythism This refers to the division of labor within a colony of social insects wherein the responsibilities of the individuals change as they mature.

Aggregation A group of individuals consisting of more than just family members; a coming together of individuals to form a group. (contrast with colony)  Cycloalexy  Allelochemicals

Aggregation Pheromone A pheromone that causes insects to aggregate. This type of pheromone is used by insects for mating, feeding, or oviposition.  Pheromones

Aggregative Response The response of predators in which they increase their time spent in areas with more prey, leading to higher predator density, and fewer prey.  Learning in Insects  Predation: The Role of Generalist Predators in Biodiversity and Biological Control

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Aggressive Mimicry

Aggressive Mimicry This is a type of mimicry in which a predator mimics their prey, allowing ready capture and consumption of the victim.  Mimicry  Myrmecomorphy  Myrmecophiles

Agonoxenidae A family of moths (order Lepidoptera). They commonly are known as palm moths.  Palm Moths  Butterflies and Moths

Agricolous This refers to species that dwell in agricultural habitats.

Agricultural Chemicals Pesticides, adjuvants, and other chemicals, other than fertilizers, that are used to enhance crop production.  Insecticides  Acaricides or Miticides

Agricultural Consultant Someone trained in the agricultural and management sciences who provides plant and animal production and protection services for a fee. Independent crop consultants sell the advising service only, deriving no income from sale of products, whereas other crop consultants usually derive some income from product sales such as pesticides or fertilizer.  Careers in Entomology

Agricultural Crop Pests in Southeast Asia Including Southern China emmett r. easton University of Hawaii at Manoa, Honolulu, HI, USA Southeast Asia is often called the Oriental faunal region and includes the provinces of southern China south of the Yangtse river (Anhui, Fujian, Guangdong, Guangxi, Guizhou, Hainan, Hubei, Hunan, Jiangshu, Jiangxi, Sichuan, Yunnan and Zhejiang) as well as the island of Taiwan, islands and peninsular area of Hong Kong, Macao and those countries to the south including Vietnam, Malaysia, Singapore, Myanmar (Burma), Cambodia and Laos, as well as portions of Pakistan and India. The northern provinces of India share similar faunal elements as southern China as both are at a similar latitude. The insect fauna of northern China is more Palearctic in nature and many of the northern species will differ from those in the southern provinces or elsewhere in Southeast Asia.

Insects of Rice What are believed to be key pests, or those of major importance as opposed to minor can vary from country to country. In Vietnam and southern China, the rice stemborer complex of lepidopterous insects includes the yellow or small rice borer, Scirpophaga incertulas (Wlk), the striped rice-stalk borer, Chilo suppressalis (Wlk), the darkheaded rice borer, C. polychrysus (Meyr) (all Pyralidae) and the noctuid pink borer, Sesamia inferens (Wlk). Although they are considered minor pests in some regions, because the rice plants are able to tolerate some damage and can compensate for light infestations, these insects have been ranked as major pests in the countries of Malaysia and Thailand. The yellow or small rice borer, Sc. incertulas, has a wide distribution in Southeast Asia and is found in India, Pakistan,

Agricultural Crop Pests in Southeast Asia Including Southern China

Sri Lanka, Bangladesh, Myanmar (Burma), Vietnam, Singapore, Taiwan and Hong Kong. The common names of these insects generally refer to the color of the larval stage such as the pink borer, S. inferens, with pinkish-colored larvae, or the yellow larvae of the small rice borer. The head capsule in larvae of C. suppressalis is brown in color while larvae of Sc. incertulas are yellow with brown heads and the pink borer caterpillar, Sc. inferens, is pink in color and larger when mature than the other species. The larvae tunnel as caterpillars into the stems of the rice plants. There they feed on the plant tissues and destroy the growing points of the plant causing wilting of new shoots, eventually producing a condition known as “dead heart.”’ In mature plants, empty panicles appear white in color, and the condition is known as “white-head.” Masses of eggs are generally laid on the leaves in the case of the female dark-headed borer or striped rice borer. Pupation generally occurs in the stem with these species. The female pyralid moths in the genus Scirpophaga have a scale tuft at the tip of their abdomens, while female moths in the genus Chilo have no scale tuft at the end of the abdomen. The female Sc. incertulas has a yellow forewing, which is whitish in Sc. nivella. The eggs of stemborers are often attacked by the parasitoid wasps Trichogramma sp. (Trichogrammatidae) and Telenomus rowani (Scelionidae). In Malaysia, granular insecticides have been used to control rice stem borers when the incidence in stems (tillers) exceeds l0%, but this practice is not recommended in southern China or in northern Vietnam where the plants are able to tolerate some damage and compensate for injury.

Rice Leafhopper and Planthopper Complex The rice leafhopper and planthopper complex includes Nephotettix virescens (Dist) and N. nigropictus (Stål), the green rice leafhoppers (Hemiptera:

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Cicadellidae) and Nilaparvata lugens (Stål) and the brown plant-hopper (Hemiptera: Delphacidae). These leafhoppers are important in Thailand and Malaysia as well as in India and Pakistan, while the planthopper is more widely distributed and is found in southern China, India, Taiwan, Japan and some of the Pacific Islands. The planthopper is unusual in that it is able to migrate between land masses and migrates from East China to Japan annually. This insect also has migrated to Macao (where rice is no longer grown due to urbanization) from mainland China. Nephotettix virescens is an important vector of two viral diseases in Malaysia. The first disease is similar to yellow dwarf disease and the second is called Tungro disease. Both cause a stunting of plant growth, the first disease a general yellowing and profusion of tillers, while the second causes a reddening of the leaves. Both diseases decrease crop yield. The eggs of the rice leafhoppers are laid in rows within leaf-sheaths. The five nymphal stages are completed in l7 days in Malaysia. Leafhoppers generally feed on the upper parts of the plant, while the planthopper, Nilaparvata, feeds at the base of the plants near the water line. The brown planthopper is sometimes considered the most serious pest of rice in Asia. They cause a “scorching” of the plants, or a condition known locally as “hopperburn,” when the number of nymphs and adults per clump of rice exceeds 900 or more. The eggs are generally laid in plant tissue. The young resemble the parents except for their smaller size and absence of wings. Five nymphal stages generally require two weeks to develop. Predators can include the staphylinid beetle Paederus fuscipes and the coccinellid beetle Harmonia octomaculata. In Thailand and Malaysia, another important pest of rice is the rice gall midge, Orseolia oryzae (W.-M.) (Diptera: Cecidomyiidae), which is also found in Pakistan, India, Bangladesh, Sri Lanka and parts of Indonesia as well as in southern China, where it is considered of minor importance. The larvae of the fly feed between the leaf sheaths and, when reaching the apical buds, can

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lacerate tissue and can cause the formation of a gall known locally as a “silver” or onion shoot. The adults are delicate looking midges, long and brown in color with long legs. Upon hatching, the pale, 1 mm long larva grows to 3 mm and becomes reddish in color. The pupa, when formed, is pinkish and turns red with age. Grassy vegetation near the rice fields is often associated with the presence of the midge. The rice leaf folder, Cnaphalocrocis medinalis (Gn), (Lepidoptera: Pyralidae), is considered one of the more important pests of rice in southern China as well as in Malaysia and Thailand. It is also found in India, Pakistan, Sri Lanka and Bangladesh. The larvae fold the leaf while feeding and transparent patches form so that the rice plant appears ragged. The adult moths lay eggs on young, 4 to 6-week-old plants or in nursery stock in Malaysia. Early instar caterpillars feed by scraping the epidermis from rice leaves, while later instar caterpillars fold them. The opposite edges of the leaf, or one edge of the leaf, is attached to the midrib by silken threads produced by the larvae. Pupation occurs inside a silken cocoon within the folded leaf. Parasitoid wasps, such as Apanteles opacus (Braconidae) or Temelucha philippinensis (Ichneumonidae), often keep populations in check in Malaysia. The lepidopterous armyworm and cutworm complex, including the rice armyworm, Mythimna loreyi (Duponchel), and the rice ear-cutting caterpillar or paddy armyworm, Mythimna separata (Wlk), are important pests in Thailand and southern China. The paddy armyworm affects rice in Pakistan, Sri Lanka, India and Bangladesh. The larvae feed on leaves and stems and can defoliate the plants. The rice skipper, Parnara guttata (Bremer & Grey) (Lepidoptera: Hesperiidae), was formerly considered a major pest in southern China, but recent mass production and release of parasitic wasps has probably lowered its status to a minor pest. The larvae roll the apical portion of the leaves, web the sides and cut off the apex, forming long, conspicuous tubes.

Sugar Cane Insects The lepidopterous sugar cane borer complex in Thailand includes several pyralids including the yellow top or early shoot borer, Chilo infuscatellus (Snellen), the sugar cane stem borer, Chilo sacchariphagus (Bojer), the white top borer, Scirpophaga excerptalis (Walker) and the noctuid sugar cane stalk borer, Sesamia inferens (Wlk). The larvae of these insects bore into the shoots of sugarcane. As the common name suggests, the larvae of the yellow top or early shoot borer tunnel into the growing shoots of the plant, while the larvae of C. sacchariphagus bore into the stems. The noctuid moth larvae of purple stalk borer, Sesamia inferens, previously discussed as a pest of rice, also affects sugar cane, but sugar cane is not preferred for oviposition as are rice and grasses. The larvae are colored purple to pink dorsally and white ventrally and have a reddishorange head capsule. The adult moth is fawn- colored with dark brown streaks on its forewings and whitish hindwings. In Malaysia, the white sugar cane aphid, Ceratovacuna lanigera Zehntner, a mealybug-like insect (Hemiptera), causes injury. The non-winged females and nymphs are covered by a waxy layer, while the winged adults are bluish-green in color and are not covered with a layer of wax.

Fruit Tree Insects: Mango-Citrus-Banana-Litchi One of the most important fruit tree insects is considered to be the Oriental fruit fly, Batrocera dorsalis Hendel (Tephritidae). It is found in Hawaii as well as in other Pacific islands and the southeast Asian countries of Thailand and Malaysia where it is a serious mango pest. In southern China, where there are fewer mangoes grown, it is considered a minor pest. In addition to mangoes, the guava and carambola are affected in Malaysia. The larvae or fly maggots feeding inside the skin of the fruit cause it to decay. Female flies puncture the skin of the fruit


with their ovipositors, laying several eggs inside. The larvae can hatch in one day and develop through three instars in about a week. When mature, they are able to leave the fruit by “flipping” themselves in the air and dispersing to enter the ground to pupate. Fruits can be protected from these flies by bagging them using paper bags. The use of traps treated with methyl eugenol as an attractant has met with some success, but as only the males are attracted, it is not totally effective as a control. In Malaysia, a longhorn beetle known as the mango shoot borer, Rhytidodera stimulans (White), tunnels into the young growing shoots of the tree. Eventually it kills the outer branches, which often break off during subsequent wind storms. In southern China, the citrus long-horn beetle, Anoplophora chinensis (Forst.) (Cerambycidae), is considered one of the most important pests of citrus trees. The larvae of these beetles tunnel under the bark of young trees and sometimes into the heartwood, which can cause the death of the plants. The adult beetles have striking black and white body coloration. Parasitoid wasps have difficulty reaching the larvae that bore into young healthy trees. Butterflies (Lepidoptera) are not considered to be serious pests of agricultural crops in the northern hemisphere with the exception of the small white, Pieris rapae. However, in the semi and tropical regions of the world, cold climatic conditions are not as severe and the insects often do not have to enter diapause (hibernation), so there can be continuous generations in some regions almost throughout the year. Papilionid butterflies, as well as several species of skippers (Hesperiidae), cause injury to plants because they are able to oviposit in both the spring and the fall. In Southeast Asia, the lemon or lime butterfly, Papilio demoleus (L.), and another species known by the common names of the common Mormon swallowtail or the white-banded swallowtail, Papilio polytes L., lay their eggs on the undersides of leaves of citrus plants and are considered important in southern China as pests of citrus. Another species, Papilio xuthus L., is also becoming

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i ncreasingly important, particularly in the Pacific island area. The first instar in these Papilionid butterflies are colored differently than older larvae, which may be an adaptation that protects them from predators such as birds or lizards. The early stage larva resembles a bird or lizard dropping as it is dark brown in color with white markings that may appear to be unappetizing to the predator. When the caterpillar is older, its color changes to green with grey and white markings. Hand picking the larvae is probably an adequate control in young plants. The orange spiny whitefly, Aleurocanthus spinifera (Quaintance) (Hemiptera: Aleyrodidae), is an important insect in southern China as well as India, Sri Lanka, Bangladesh, Malaysia and Thailand. The adults are l mm in length and lay eggs on the undersides of leaves. There are three nymphal stages and the third-stage nymph appears blackish in color with waxy secretions on the outer edge of the body so it looks superficially like an insect pupa. Both the nymphs and the adults remove plant nutrients when feeding, and the honeydew produced by the nymphs encourages a sooty mold to grow on the upper surfaces of the leaves and the fruits. Heavy infestations of this insect cause fruit production to fall off. A parasitic wasp, Eretmocerus serius (Aphelinidae), has been effective in regulating the orange spiny whitefly in Malaysia. Aphids, such as the black citrus aphid, Toxoptera aurantii (Bayer de Fonscolombe), and the brown citrus aphid, Toxoptera citricida (Kirkaldy), are important in southern China and also range into India, Sri Lanka and Bangladesh. Fruit-piercing moths, such as Othreis fullonia (Cl.) (Noctuidae), pierce the ripening fruits of citrus, mango, papaya and guava or banana in order to obtain sap. A short, stout proboscis with a barbed tip enables the moth to puncture the skin of the fruit and can permit the entry of plant pathogens such as viruses or secondary rots that can cause premature fruit drop. Fruit-piercing moths are considered of major importance today in southern China. Management of their

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populations is difficult as the immature of O. fullonia do not feed on citrus trees. Instead, the caterpillars feed on the foliage of the Erythrina species of shade trees. On the Pacific island of Guam, the eggs can be laid on the foliage all year round and the insects are considered to be major pests as they feed on ripe banana, mango, papaya, pomegranate and guava as well as tough-skinned citrus fruits. On banana plants, there are two species of leaf rollers or banana skippers in Southeast Asia, one of which is Erionota thrax (Hesperiidae), which rolls the banana leaves in Malaysia, Thailand and in southern China. The caterpillars cut and roll strips of banana leaf, then hide in the roll that is held together by silken threads. They emerge at night to feed and are often covered with a white powdery secretion.

Litchi and Longan Fruit Insects The litchie stink bug, Tessaratoma papillosa (Drury) (Hemiptera: Tessaratomidae), has been considered the most important pest of litchi (Litchi chinensis) and longan (Euphoria longan) fruit trees in the Guangdong region of southern China, including Hong Kong and Macao as well as Vietnam and Thailand. The adults are mostly brown dorsally and whitish underneath. Immature bugs, more brightly colored than the adults, have red markings dorsally often with a white waxy secretion underneath. Plant sap is taken from the stems of fruit trees. The saliva of the bug can stain the clothing of fruit tree workers. Also, the fluid is extremely irritable if it gets in the eyes. An effective biological control of the litchie stink bug has been developed in southern China by the Guangdong Entomological Institute in which the egg parasitic wasp, Anastatus japonicus (Eupelmidae), has been mass-reared and released to achieve control in the Fujian, Guangdong and Guangzi provinces. Biological control of the litchie stink bug has also been reported from the northern highlands of Thailand.

Vegetable Insects The diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is currently considered among the top 25 most important arthropod pests in southern China. It was the first agricultural pest in Malaysia to be reported resistant to pesticides, and it is also an important pest in Thailand as well as in India. Its distribution has been considered cosmopolitan. Cruciferous plants, such as the cabbages, are affected. The caterpillars penetrate the epidermis of leaves, mining the tissue and making windows or holes in it. The adult is recognized by the pale triangular or diamond-shaped marks seen on the midline of the back when the wings are closed. The caterpillar is pale green in color, and it wriggles violently when disturbed, sometimes falling off the edge of the leaf. A microbial insecticide, Bacillus thuringiensis, is effective in the control of the diamondback moth, but farmers in some areas of Malaysia have not accepted it because this method takes longer to kill the caterpillars than other insecticides. The green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae), is a cosmopolitan insect in Southeast Asia that damages developing vegetables, such as potato, sweet potato, tomato and cotton, by their feeding punctures. Three color varieties or subspecies of this insect are recognized in southern China. An all-green form, known as N. viridula smaragdula, is the most common, accounting for 75–80% of vegetable bugs observed in Macao in l996. A second form with yellow on the head and pronotum, N. viridula torquata, makes up about 10% of the stink bug population, while the least common form is mostly all yellow with green spotting on the hemelytra and abdomen, and is called N. viridula aurantiaca (1.0%). The small white butterfly, Pieris rapae (L.) (Lepidoptera: Pieridae), along with two other species, is still considered important in southern China and Southeast Asia. The small cabbage butterfly, Pieris canidia (Sparrman), also damages nasturtium. In both species, larvae feed singly in the cabbage heart, make holes in the leaves and cause frass accumulation. The insects are also found in India, Taiwan and the

Agroecology

Philippines, and breeding can be continuous with up to eight generations annually, which is not the case in northerly regions, where overwintering occurs in the pupal stage. The Asian corn borer, Ostrinia furnacalis (Guenee) (Lepidoptera: Pyralidae, Pyraustinae), is more important in the northern countries of Southeast Asia including southern China where corn is grown. The Guangdong Entomological Institute rates it as a highly important pest there. The larvae bore into the stalks and the ears of corn, and can also survive on foxtail millet, Setaria italica, and on Panicum grasses. The eggs are laid in clusters of 10–40 underneath leaves about a week before the plant forms its inflorescence. The young larvae can scarify the leaves and later, bore into the stem. Pupation generally occurs within the stalk, but can occur within the ear. The Asian corn borer’s range includes India, Sri Lanka, Korea, China, Hong Kong, Taiwan, Vietnam, Japan, Malaysia, Thailand, Singapore and Indonesia.  Tropical Fruit Pests and Their Management  Sugarcane Pests and Their Management  Vegetable Pests and Their Management

References Denton GWR, Muniappan R, Austin L, Diambra OH (1999) Fruit-piercing moths of Micronesia. Agricultural Experiment Station, University of Guam. Tech Report #217, 26 pp Hirose Y (ed) (1992) Biological control in South and East Asia. Kyushu University Press, Fukuoka, Japan, 68 pp Ooi PAC (1999) Insects in Malaysian agriculture. Tropical Press, Kuala Lumpur, Malaysia, 106 pp Robinson GS, Tuck KR, Shaffer M (1994) Field guide to smaller moths of Southeast Asia. Malaysian Nature Society, Kuala Lumpur & Natural History Museum, London, 308 pp Waterhouse DF (1998) Prospects for the classical biological control of major insect pests and weeds in Southern China. Entomologia Sinica 5:320–341

Agroecology robert mcsorley University of Florida, Gainesville, FL, USA

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Agroecology is the application of ecological principles to agricultural production systems and the resources needed to sustain them. A convenient unit of study is the agroecosystem, often a single agricultural field. A major difference between an agroecosystem and a natural ecosystem is in the level of human intervention and management involved. Like natural ecosystems, agroecosystems consist of living (biological) and nonliving (chemical, physical) portions. The science of agroecology examines the living organisms (collectively called the community) in the system, their interactions with one another, and the environmental factors that influence them.

Nutrient Cycling The organisms within an ecological community depend on one another for energy and materials. Green plants are referred to as producers since they are at the base of the food chain in ecosystems. Initially, carbon and energy are stored in plant tissues through the process of photosynthesis. Consumers must obtain their carbon and energy by eating plants or other organisms. Therefore carbon and other materials move from green plants to herbivores to carnivores, including predators and parasites. The different levels of energy production and consumption (producers, herbivores, predators) are called trophic levels, although in reality many organisms do not restrict their feeding to one level. For instance, some Hymenoptera that are parasitoids as larvae may feed on pollen or nectar as adults. As a result, the paths along which materials move through the organisms in the community can be quite complicated, and collectively they make up the food web within the community. Many nutrients, including nitrogen, phosphorus, potassium, and other elements, are essential components of plant and animal tissues. These nutrients have distinct cycles in ecosystems, and they cycle in food webs along with carbon and other materials. Nutrients are released into the soil during decomposition of organic molecules, where they

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Agroecology

are converted into forms that can be taken up by plant roots, completing the nutrient cycle. Microarthropods such as mites and springtails are particularly important in the decomposition process.

Cropping Systems Crop performance depends on a range of key resources including nutrients, water, soils, and other environmental factors, and many agricultural management practices are aimed at optimizing and conserving these resources. Various types of cropping systems may be selected to address specific goals or conservation issues. Conservation tillage and other reduced tillage practices are important for soil conservation and reduction of erosion. The crop residues that remain on the soil surface in uncultivated sites can also aid in conservation of water and organic matter, and may provide some nutrients when they decompose (Fig. 28). Monoculture allows a grower to specialize by growing only one crop, while polyculture permits a grower to diversify by growing multiple crops on the same land. Multiple cropping on the same site may occur at the same time or over time. In the United States, the most common form of multiple cropping is crop rotation, in which different crops are grown on the same site in different seasons or years. Cover crops are crops with limited market value that are grown on the site during seasons that are unfavorable for growing the main economic crops for the region. In the southeastern United States for example, a winter cover crop of rye (Secale cereale) or crimson clover (Trifolium incarnatum) may be grown in a field reserved for cotton or peanut production during the summer. Cover crops can provide various advantages, including erosion reduction, increased supply of nitrogen, competition with weeds, or hay for animals. Green manures, which are usually legume cover crops, are grown specifically for their nitrogen-rich residues and soil fertility benefits. Intercropping, or mixed cropping (Fig. 29), refers to the growing of two or more crops at the same time on the same land. The practice is quite common in

some regions, and many variations exist. Some tropical subsistence intercropping systems are especially diverse and complicated.

Pest Management The cropping system used has a direct effect on pest management, which is an important aspect of agroecology. For example, monoculture may encourage buildup of some pests, such as corn rootworms (Diabrotica spp.) or wireworms (Elateridae), that can be managed by appropriate crop rotation. In many cases, the use of intercropping has resulted in less severe pest outbreaks and increased diversity of natural enemies compared to monocultured systems. Tritrophic (plant-herbivore-predator) interactions and the structure of the food web may be affected by changes in the cropping system, such as use of an intercrop, or changes in crop variety or fertility level. The development and use of biologically based pest management tactics such as use of natural enemies or resistant varieties require a detailed knowledge of pest biology and ecology, including life cycle, population dynamics, and interactions with the physical and biological environment, including potential competitors, predators, and parasites. Such tactics may be directed toward preventing pest buildup rather than reacting to high pest numbers already present in crisis situations. However, the design of a system in which pest numbers are less likely to reach crisis levels, due to the presence of effective natural enemies for example, requires advanced planning based on sound ecological data.

Landscape Ecology An individual agroecosystem does not stand alone, since organisms, materials, and energy move freely in and out of the system. Landscape ecology examines the agroecosystem in the context of the surrounding region or landscape, an essential

Agroecology

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Agroecology, Figure 28 Residues from a previous rye crop cover the soil surface between plant rows in this conservation tillage system.

approach in dealing with migrating insects or regulated pests. The condition of field borders, hedgerows, and adjacent fields critically affects pest management within a specific field. Movement of pesticides, fertilizers, and other potential pollutants from the agroecosystem to natural ecosystems is a major environmental concern.

Many natural ecosystems are highly dependent on recycling, since cycles of nutrients, water, and other materials tend to be relatively closed. In contrast, an agroecosystem is not a closed system, because its purpose is to produce harvest for export to other ecosystems. This process depletes essential resources from the agroecosystem

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Agromyzidae

Agroecology, Figure 29 One of the simplest forms of intercropping is to use one crop as a windbreak, like the sugarcane planted along with the eggplant crop shown here.

which must be restored if the system is to remain productive. The movement of essential resources into the agroecosystem and the recycling of existing resources are therefore critical concerns, to anticipate and ensure that supplies of critical resources for agricultural production will be conserved over time to sustain future agricultural production.  Organic Agriculture  Integrated Pest Management (IPM)  Conservation Biological Control  Flower Strips as Conservation Areas for Pest Management  Plant Resistance to Insects  Cultural Control of Insect Pests

Gliessman SR (1998) Agroecology: ecological processes in sustainable agriculture. Sleeping Bear Press, Chelsea, MI Jackson LE (ed) (1997) Ecology in agriculture. Academic Press, San Diego, CA Powers LE, McSorley R (2000) Ecological principles of agriculture. Delmar Thomson Learning, Albany, NY

References

A family of beetles (order Coleoptera). They commonly are known as primitive carrion beetles.  Beetles

Altieri MA (1994) Biodiversity and pest management in agroecosystems. Food Products Press, New York, NY Cavigelli MA, Deming SR, Probyn KL, Harwood RR (eds) (1998) Michigan field crop ecology. Extension Bulletin E-2646. Michigan State University, East Lansing, MI Coleman DC, Crossley DA Jr (1996) Fundamentals of soil ecology. Academic Press, San Diego, CA Collins WW, Qualset CO (eds) (1991) Biodiversity in agroecosystems. CRC Press, Boca Raton, FL

Agromyzidae A family of flies (order Diptera). They commonly are known as leaf-miner flies.  Flies  Leaf-miner Flies (Agromyzidae)

Agyrtidae

A.I. An abbreviation for “active ingredient,” the active component of an insecticide, or the toxicant.

Alarm Pheromones of Insects

 Insecticides  Insecticide Formulation  Insecticide Toxicity

Alarm-Defense System Defensive behavior that also serves as an alarm signaling mechanism.

Air Sacs The trachea of insects are sometimes dilated or expanded to form pouch-like structures called air sacs. Their occurrence varies among taxa, but their presence lowers specific gravity and enhances air exchange, thus enhancing flight.  Active Ventilation  Abdominal Pumping

Alarm Pheromone A pheromone released to trigger alertness, dispersion or group defense by insects.  Alarm Pheromones of Insects  Chemical Ecology

Alarm Pheromones of Insects emma napper, John. a. pickett Rothamsted, Harpenden, Hertfordshire, UK Alarm pheromones are defined as chemical substances, produced and released by an organism, that warn or alert another of the same species of impending danger. This is exemplified by many species of aphids (Hemiptera: Aphididae) in which the pheromone is caused to be released by attack, for example, by predators, with ensuing dispersal by which individual aphids may avoid a subsequent attack. However, the term alarm

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heromone also is employed when the respondp ing individuals are stimulated to show aggression towards the attacking agent. This is common in the social Hymenoptera; for example, the honeybee, Apis mellifera (Hymenoptera: Apidae), and many ant species respond aggressively to their alarm pheromones. As alarm pheromones can benefit the survival of members of the species involved, it is common for insects that employ alarm pheromones to live in congregations for some or all of their life cycle. In the case of social Hymenoptera, the colony is genetically related, and in asexually reproducing aphids, the colony is clonal. Although the survival of siblings or clones by alarm pheromone response at the cost of the attacked individual appears altruistic, in genetically related colonies, genes from the individual will predominate in the survivors and be passed on to their kin.

Hemipteran Alarm Pheromones Alarm Pheromones of Aphids (Hemiptera: Aphididae) When disturbed or attacked, many aphid species release alarm pheromone from droplets secreted from tube-like structures called cornicles on their dorsal posterior. This phenomenon has been studied exclusively in the asexual forms and most often in asexually reproducing wingless females. Aphids nearby exhibit a variety of behaviors ranging from stopping feeding and moving away, to running or dropping off the plant and even attacking the predator. However, not all aphids in a group respond. The relative risks of predation and costs of escape, for example, cessation of feeding and risk of desiccation, affect the likelihood of any particular response. In studies of the peach-potato aphid, Myzus persicae, the pea aphid, Acyrthosiphon pisum, and the rose-grain aphid, Metopolophium dirhodum, early stages were found to be less sensitive to alarm pheromone than later ones.

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However, older wingless M. persicae require the greatest stimulation of alarm pheromone before responding, while winged M. persicae, particularly those not feeding, are extremely sensitive to alarm pheromone. The lack of response from the early stages suggests that the risk of predation to these nymphs is lower than the risk involved in ceasing to feed and dropping from the plant. When young M. dirhodum respond to alarm pheromone, they do so by moving to another part of the plant rather than by dropping. Winged adults, on the other hand, are more responsive to alarm pheromone, perhaps because they can more readily move off the host. The sugarcane woolly aphid, Ceratovacuna lanigera, also shows different reactions to alarm pheromones at different life stages; it shows attack behavior until adult, when the normal aphid dispersal response takes over. Considerable variation is seen between aphid species in their sensitivity to alarm pheromones and in both the speed and the form of the response. This variation often can be explained by differences in the ecology of the species. Some aphids, particularly those tended by ants, stay on the plant and respond by walking or “waggling” their abdomens rather than falling off the plant. These aphids appear to depend more on the protection afforded by their ant attendants than their own defensive mechanisms. Aphids that walk away from a source of alarm pheromone tend to form new clusters a short distance from the original site, thus ensuring continued ant attendance. Susceptibility to insecticide also has been found to correlate with responses to alarm pheromone. Susceptible strains produce more pheromone and respond more quickly and in higher numbers than insecticide-resistant strains. In addition, clones collected from around the world showing knockdown resistance to pyrethroid insecticides, and esterasebased insecticide resistance, showed lower levels of disturbance to the synthetic alarm pheromone. These aphids may therefore suffer increased predation or parasitism in the absence of insecticides, affecting the evolutionary fitness of insecticide resistant clones. This may be due to physiological effects associated

with resistance, which could affect mobility or sensitivity of the nervous system to stimuli. Aphids that have dropped from a plant may re-colonize or may move to another host plant further away. The turnip aphid, Lipaphis erysimi, and M. persicae dislodged by alarm pheromone are less likely to return to the original host plant than when mechanically dislodged. Similar patterns of behavior are found in A. pisum. Aphids dislodged by a predator or experimentally with synthetic alarm pheromone spend longer “running” before the “search” for a host plant began, whereas aphids dislodged mechanically are more likely to begin to search for a host plant immediately. Droplets secreted from the cornicles comprise two types of material: a volatile, rapidly vaporizing fraction which is the alarm pheromone, and a waxy fraction, consisting mainly of triglycerides, that crystallizes on contact with foreign particles outside of the aphid’s body. The waxy component appears to function as a sticky or quick-setting irritant to predators and parasitoids and a releasing substrate for the alarm pheromone component. The main component of the alarm pheromone (Fig. 30) of many aphids is the sesquiterpene hydrocarbon (E)-β -farnesene (1). Other components may also be present as found in the alarm pheromone blend of the vetch aphid, Megoura viciae, which contains the monoterpenes (-)-α pinene, (-)-β -pinene, (Z,E)-α -farnesene and (E,E)-α -farnesene, in addition to (E)-β -farnesene. There is a high degree of cross-activity of both natural alarm pheromone and (E)-β -farnesene among species within the aphid subfamilies, Aphidinae and Chaitophorinae. This is typical of insect alarm pheromones in general, since such cross-activity does not reduce their evolutionary value. However, the main component of the alarm pheromone of the spotted alfalfa aphid, Therioaphis maculata, and the sweet clover aphid, T. riehmi, in the Drepanosiphinae, is the cyclic sesquiterpene (-)-germacrene-A (2). In the turnip aphid, L. erysimi, it has been demonstrated that isothiocyanates, acquired from chemicals in the host plants, synergize the effect of


the alarm pheromone. These isothiocyanates are likely to be released from aphid honeydew so that, when there is a high number of other aphids in the immediate vicinity, the percentage of aphids responding to alarm pheromone increases.

Alarm Pheromones of True Bugs (Hemiptera, Heteroptera) The Pentatomidae is the dominant family of stinkbugs, or shield bugs. The family comprises many species that are pests of economic importance, especially in warmer climates. These insects secrete a complex mixture of chemicals when strongly molested. The energetic cost of the defense response, especially production of defense chemicals, is significant and considerable provocation usually is required to cause release. In adults, the source of the defense compounds is the

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metathoracic gland, while in nymphs it is the dorsal abdominal glands. These are precursors to the metathoracic gland in adults and perform the same defense function. The chemical content of these secretions is similar throughout the order; for example, the components of the secretion of the stinkbug Cosmopepla bimaculata are a complex mixture of hydrocarbons, aldehydes and esters. The secretion, which can be ejected from either or both metathoracic glands in controlled amounts or even resorbed, displays a defensive function as a predator repellent. In one case, researchers have shown uncommon dedication in describing the repellency by squeezing adults in their mouths and chewing nymphs. The effects were a burning sensation and numbness of the tongue for up to two hours. In addition to repelling predators, the secretions possess alarm pheromone activity and cause adults to drop off plants. In the field, C. bimaculata are found highly clumped and the occurrence of large

Alarm Pheromones of Insects , Figure 30 Defense secretion of Cosmopepla bimaculata showing a typical range of compounds produced by stinkbugs. Chemical structures of alarm pheromones are referenced in the text by bold numbers.

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Alarm Pheromones of Insects, Figure 30 (Continued)

numbers living together gives an evolutionary advantage to possessing an alarm pheromone. Six-carbon-long aldehydes, in particular (E)- 2-hexenal, are common components of defensive secretions and are found in many families of heteropterous insects, including the Pentatomidae, Coreidae, Pyrrhocoridae, Cimicidae, Cynidae and Alydidae. it is thought that the general irritant properties of aldehydes provide a repellent effect to predators with hydrocarbons such as n-tridecane, another ubiquitous component, acting to

spread the oily secretion so that the aldehydic components can exert full irritant effect. (E)-2Hexenal has been reported to have the added dual functions of both alarm and aggregation pheromone, depending on the stimulus concentration, as well as use as a defense chemical. In the case of the bed bug, Cimex lectularius, and Eurydema rugosa, low concentration of (E)-2-hexenal acts as an aggregation pheromone while high concentration produces an alarm response. Alternatively, it has been reported that n-tridecane, the other


Alarm Pheromones of Insects, Figure 30 (Continued)

biquitous component of defense secretions, is a u bifunctional pheromone for the southern green stinkbug, Nezara viridula (Heteroptera: Pentatomidae), which causes dispersal at high concentration (one individual equivalent) and aggregation at low concentrations. The multifunctional aspect of these compounds has important repercussions for their practical use as dispersal agents for pest species in the field, as the low concentration response of aggregation may dominate once the applied high concentration of compounds has diminished.

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The pentatomid bug Erthesina fullo is a major pest of pine and hardwood trees. Both sexes produce a secretion from the metathoracic gland causing conspecific adults to drop from plants, fly or move away. The secretion comprises nine identified compounds, esters and aldehydes (about 35%) including (E)-2-hexenal and (E)-4oxo-2-hexenal (3) and long chain alkanes, including 50% n-tridecane. Likewise, adult and nymph secretions from Dysdercus cingulatus (Heteroptera: Pyrrhocoridae) revealed 55 identified compounds, although the major components are again aldehydes and n-tridecane, features common with several more species of pentatomids from the genus Chlorochroa and Piezodorus guildinii. The leaf-footed bug, Leptoglossus zonatus (Heteroptera: Coreidae), is an economically important pest of Brazilian corn. An extract obtained from the metathoracic gland by immersion in hexane showed that the major compounds were all of six-carbon length: hexanal, hexanol, hexyl acetate, hexanoic acid, and (E)-4oxo-2-hexenal (3). (E)-2-Hexenal was found in the nymph extracts but not in the adult, an example of the general rule that exocrine chemistry of heteropterous nymphs is distinct from that of the adult. In this case, different life-stages possess different alarm pheromone systems. When tested individually, all components produced varying degrees of alarm response in adults and nymphs and even mating insects would stop and disperse, over-riding the sex pheromone response. These compounds are not species specific and are, for instance, found in L. oppositus and L. clypealis, a situation that mirrors the cross-activity of (E)-β-farnesene in many aphid species (see above), providing more evidence that this non-specific activity does not reduce alarm pheromone value in evolutionary terms. Adults of the bean bug, Riptortus clavatus (Heteroptera: Alydidae), a pest of Japanese soybean, secrete (E)-2-hexenyl acetate in its defensive response. This causes an alarm response in adults

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and nymphs. Interestingly, adults also produce (E)-2-hexenal, and although some response was found when tested at high concentration, there was no response at physiological concentration, suggesting that this compound is not an alarm pheromone. The examples shown above demonstrate that alarm pheromones of heteropteran families are based on a chemical selection general to insects of a wide taxonomy and show little species specificity. The alarm behavior caused by high concentrations of n-tridecane or (E)-2hexenal is rationalized easily but the aggregation due to low concentrations is more difficult to explain. Perhaps these substances are constantly emitted in very small quantities due to their volatility and act so as to direct individuals to a region where conspecifics can be found and therefore where food most probably is located, as well as the defensive advantage in being part of a large group. Triatomine bugs (Heteroptera: Reduviidae) are blood-sucking insects that live throughout the Americas and cause public health problems by transmitting the protozoa Trypanosoma cruzi, the causative agent of Chagas disease, to humans. Secretions from Brindley’s gland (a simple sac, metathoracic in origin) of several species all revealed isobutyric acid as the major component. Subsequently, other short-chain and branchedchain fatty acids have been identified, and together with isobutyric acid, they act as a powerful defensive secretion. Pure isobutyric acid vapor, however, also caused an alarm response in Rhodnius prolixus while another report revealed that low concentrations of isobutyric acid attracted R. prolixus adults. This defense compound therefore shows the same multifunctional alarm and aggregation properties as described for components of the stinkbug secretions (see above). Triatomine bugs are inactive and hide during the day, congregating in protective sites. This aspect of group living can help explain the evolutionary advantage in possessing aggregation and alarm responses.

Alarm Pheromones of Social Insects (Hymenoptera) The Honeybee (Hymenoptera: Apidae) When the honeybee (Apis mellifera) is attacked, alarm pheromones released serve to muster help and to direct the attack. Specialized guard bees present at the nest entrance carry out attacks. Although these guards are relatively few compared to the colony population, release of alarm pheromone can result in synchronized attacks by more than 100 workers against an intruder. Guard bees initiate attacks by raising their abdomens, protruding their stings and releasing alarm pheromone from the sting chamber. The workers then alert the rest of the hive by wing beating, aiding dispersal of the pheromone, and by running into the hive. After a few seconds, many excited bees may rush out of the hive entrance and search, or stop and assume a characteristic tense and aggressive posture with a slightly raised body, wings extended, mandibles agape and antennae waving. In this highly activated state, they will fly to attack at the slightest further provocation. These two stages of alarm response are called alerting and activation and are characteristic of alarm pheromones. Alerted workers need to search for and discover the enemy to prevent any further threat. To do this, they rely on other cues to direct the attack such as odor, jerky movement and hairy body covering. Once the threat is located, it is stung, injecting a dose of venom. However, the shaft of a sting is barbed and a bee is unable to withdraw it from the skin of vertebrates, so the sting, together with associated motor apparatus and glands, are severed from the bee as it attempts to fly away and are left attached to the enemy. The severed sting apparatus continues to pump venom into the victim and alarm pheromone is dispersed from the exposed under-surface of the sting shaft membrane to mark an enemy and make it a more obvious target. The main alarm pheromone component of the sting gland was identified in 1962 as isopentyl


acetate (4). Although a number of other compounds are known to be present, isopentyl acetate and (Z)-11-eicosen-1-ol (5) account fully for the activity of the sting pheromone. The roles of the two compounds in the pheromone appear to differ, with (Z)-11-eicosen-1-ol responsible for prolonging the activity of isopentyl acetate. Other compounds such as 1-hexanol and 1-butanol increase the number of bees responding. Stinging bees often grip an enemy with their mandibles and deposit an alarm substance. At the hive entrance, more bees examine mandibular gland extracts of worker honeybees applied to filter paper than examined unscented filter paper. 2-Heptanone (6) has been identified from the mandibular gland secretion, and when filter papers or small corks carrying 2-heptanone were placed at the hive entrance, the guard bees were alerted and attacked them. As the mandibles are used for grasping an intruder, it seems likely that the main function of 2-heptanone is to label the intruder to be attacked. Under certain circumstances, honeybee alarm pheromones are repellent. The presence of alarm pheromone deters honeybees from foraging at dishes of sugar syrup and from exposing their Nasonov glands and fanning which normally attracts other bees. Furthermore, a high concentration of alarm pheromone repelled foraging bees from crops including oilseed rape, normally highly attractive to bees, in an area that had many honeybee colonies.

Alarm Pheromones of Ants (Hymenoptera: Formicidae) The Formicidae is a huge family comprising thousands of ant species, all of which are social insects, living in colonies that vary hugely in size. Members of an ant colony may be differentiated into castes that specialize in carrying out particular tasks and vary in their response to alarm pheromone. Soldiers show a more aggressive response, are more likely to respond when the

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threat is closer to the nest and may be specialized to deal with vertebrate predators. Also, workers of the Texas leaf-cutting ant, Atta texana (Formicidae: Myrmicinae), have a lower threshold for alarm pheromone response than the queen and males. Other factors governing the type and intensity of alarm response are the age and size of ant colony. When alarm pheromone is present in sufficient concentration to excite the workers, other stimuli are needed to direct an attack. Workers often will touch everything they encounter and the full-scale alarm response may rely on additional cues, such as the presence of an alien object. Alarm pheromones also may function with acoustic alarm signals. Ant species in the sub-family Dolichoderinae produce vibration signals using their mandibles to scratch the ground or the abdomen to hit the ground, increasing alarm behavior in other workers. Vibrations are produced also by leaf-cutting ants which act as warning signals. Alarm pheromones also are used by ants to attract attention if they are trapped, and may be released by reproductive ants just before mating flights to ensure that aggressive workers protect them from potential predators. The context in which a worker encounters an alarm pheromone also influences the response. Workers of the grass-cutting ant Atta capiguara (Formicidae: Myrmicinae) are less likely to show alarm behavior if already engaged in a task. Foragers carrying leaves do not respond to alarm pheromone, whereas minor workers and foragers that are not carrying leaves do respond. Ant alarm pheromones may be produced from one or several sources. The army ants or Eciton ants (Formicidae: Ecitoninae) and the rare Leptanilla sp. (Formicidae: Leptanillinae) of Indonesia have large mandibular glands, which are believed to be the sole source of the alarm pheromone. However, other species rely on a combination of secretions from several glands. Formica and Myrmica species use products from the poison and Dufour’s gland (both opening near the base of the sting), as well as the

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andibular gland. Ponerine ants (Formicidae: m Ponerinae) use secretions from the pygidial gland as alarm components, whereas the poison gland is the most important gland of several other species, including the harvester ant, Messor barbarus (Formicidae: Myrmicinae). Ants are able to detect and respond to specific isomers of their alarm pheromone. Myrmica rubra and M. scabrinodis use 3-octanol (7) as the alarm pheromone produced from mandibular glands. Experiments carried out using the two optical isomers (8a, b) of this compound showed that M. rubra workers only responded to one of the isomers, (R)-3-octanol (8a), while M. scabrinodis workers reacted more strongly to the natural 9:1 mixture of R and S isomers. This work suggests that there may not only be specific chemicals but also species-specific mixtures of isomers. Many other Myrmica species have 3-octanol and 3-octanone as alarm pheromones but may have species-specific ratios of the two, which allow ant species to only show a full alarm reaction to their specific alarm pheromone blend. Myrmica species of grass-cutting ants share the main component of alarm pheromone, 4-methyl-3-heptanone (9), but they have speciesspecific modifying components. The response to 4-methyl-3- heptanone was compared to that elicited by the bodies of workers that had their heads crushed to release the natural alarm pheromone. 4-Methyl-3-heptanone and bodies caused the same level of attraction but the full range of alarm beha vior was seen only with the bodies. In contrast, workers of the giant tropical ant, Paraponara clavata (Formicidae: Paraponera), produce two components, 4-methyl-3-heptanone and 4-methyl3-heptanol. Atta capiguara is a grass-cutting ant species that lives in colonies with hundreds of thousands of workers. Workers are polymorphic, varying in size from small minors and medias to the larger foragers and soldiers. Minors and medias do most of the nest tasks whereas foragers collect the grass; however, minors often are found on foraging trails despite the fact they do not carry grass. They are

believed to be patrollers as they have a stronger response to alarm pheromone than foragers and soldiers. Minors of other Atta species are also more efficient at recognizing intruding ants than other castes. As is the case with honeybees described above, the complete alarm response can be described by a number of behaviors. These behaviors and their elicitors have been dissected in an elegant piece of research on the African weaver ant, Oecophylla longinoda. The major workers produce a secretion from the mandibular gland comprising four active components: hexanal, hexanol, (E)-2-butyl-2octenal (10), a dimer of hexanal produced chemically by self-condensation, and 3-undecanone (11). Hexanal, a highly volatile component with an active space of 5–10 cm (the area around an emission where the concentration is at or above that required for a behavioral response), causes the ants to be alerted, making quick runs in random and changing direction with mandibles open and antennae waving. Hexanol attracts directly to the source at a range of 1–5 cm; it is repellent at very close range and also causes further excitement. As the hexanol disperses, 3-undecanone is attractive over this close range and, along with (E)-2-butyl2-octenal, acts as a marker for attack and biting to hold the source occurs. This process is called a local attack. In addition, O. longinoda also has a mass attack alarm response. The poison gland of the major and minor workers contains venom that is ejected by raising the gasters above vertical when an attacked object is held in the jaws. The venom contains a blend of straight chain hydrocarbons and formic acid. Formic acid initiates approach and attack while n-undecane causes mandible opening, gaster raising and also short-range approach to the source. The combination of these behaviors allows location and initial attack of still and moving objects followed by recruitment of workers to continue attack. The properties that make alarm pheromone cues for conspecifics also enable them to act as cues for parasites and predators of ants to find their prey. Apocephalus paraponerae is a parasitic fly that


attacks the ant Paraponera clavata. Females and males of A. paraponerae are attracted to injured, fighting or freshly killed workers. After finding a worker, the female lays a few eggs, which will hatch and then feed on the victim for 3–7 days. Both male and female A. paraponerae also feed on the wounds of the injured workers and gather near their victims to mate. The heads of P. clavata workers contain two chemicals, 4-methyl-3-heptanone and 4-methyl-3-heptanol, which are particularly attractive to A. paraponerae. These compounds are common alarm pheromone components of ants and are released when the workers are stressed. However, it has been suggested that because these parasites use alarm pheromone for finding their host, P. clavata may be under pressure to reduce the amount of alarm pheromone released and that this ant may even have lost alarm behavior response as a result of this pressure. Similarly, the zodariid spider, Habronestes bradleyi (Zodariidae), a predator of the meat ant, Iridomyrmex purpureus, detects the alarm pheromone, in this case 6-methyl-5- hepten-2-one (12), given out by fighting workers and uses it to locate its prey.

Alarm Pheromones of Thrips (Thysanoptera: Thripidae) Thrips are small, economically important pest insects, often known as thunderflies. The defensive behavior of thrips includes raising and lowering the abdomen and secretion of a droplet of anal fluid highly repellent to predatory ants. Western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae), are not social but tend to be found in clumped distributions. Adults and nymphs of western flower thrips produce an anal droplet containing decyl acetate and dodecyl acetate (13) in a molar ratio of 1.5:1. Each component, at levels of 1 ng, produces the alarm response of walking away from the source or dropping from leaves. The response, however, is only over short distances and limits the potential for pheromone use in pest management.

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Cockroach Alarm Pheromones (Blattodea: Blattidae) Defensive secretions are well known in cockroaches. They are produced from ventral inter-segmental glands and comprise an organic and an aqueous phase. In the case of the Florida woods cockroach, Eurycotis floridana (Dictyoptera: Blattidae), 90% of the organic phase (which comprises 85% of the total secretion) is (E)-2-hexenal, a compound found in many heteropteran bugs and discussed above. The rest of the organic secretion comprises approximately 40 other components, including mainly aldehydes, alcohols and carboxylic acids, while the aqueous phase contains gluconic acid, glucose and gluconolactone. The secretion acts as a conspecific alarm pheromone in these gregarious insects with nymphs responding at lower concentrations than adults do. Ethanolic extracts of the American cockroach, Periplaneta americana, also repel conspecifics from aggregations in daytime shelters. However, there was no evidence that this repellent is released by living insects as an alarm pheromone but is instead endogenously produced from dead insects and is effective against other cockroaches with diverse phylogenetic relationships. The effect, therefore, is not pheromonal, as the authors explain the activity in terms of unsaturated fatty acids (oleic, linoleic and linolenic acids) which emerge as signals of death and injury among organisms from a wide phylogenetic background. Both of the reports described above provide evidence that the use of alarm pheromones to increase dispersal for pest management purposes will be of limited value. Due to the aggregation effect at low concentration, treated areas could become attractive. Also, if low concentrations were used as attractants in a lure and kill approach, dead insects would repel others before they become ensnared.

Alarm Pheromones of Beetles (Coleoptera) Despite the vast numbers of species in the order Coleoptera, inhabiting a wide range of ecological

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niches, little is known of the existence of behavioral responses to alarm pheromones they may possess. Species of beetles that are group-living are most likely to demonstrate alarm responses. Gyrinid beetles (Coleoptera: Gyrinidae), known as whirligig beetles, live in open habitats on fresh water surfaces and typically aggregate in groups containing hundreds of individuals, dispersing in the evening to forage. Although easy to detect by fish, they are seldom preyed upon due to a repellent secretion released as a last resort to physical attack. The secretion also acts as an alarm pheromone over short distances, increasing locomotory activity and defensive movement, such as diving and active underwater swimming. Although alarm dispersal after attack can occur, the aggregations of beetles themselves indicate to experienced predators to avoid the group and confer an aposematic effect acting at the group level rather than the individual level.

Lacewing Alarm Pheromones (Neuroptera: Chrysopidae) The green lacewing, Chrysoperla carnea (Neuroptera: Chrysopidae), is an important predator of pest aphids and, as such, is a beneficial insect. It discharges a malodorous secretion from glands at the anterior of the prothorax. The major component of this secretion has been identified by gas chromatography, mass spectroscopy and chemical synthesis as (Z)-4-tridecene (14) and gas chromatography coupled electroantennagrams revealed that it is detected by the lacewing antennae. Predatory ants displayed avoidance behavior in response to it, suggesting a defensive function, and in laboratory experiments, adult lacewings avoid entering areas where it is present. In the field, it acts as an antagonist to trap catches using known attractants and, as such, could be described as an alarm pheromone. Another species of lacewing, Peyerimhoffina gracilis, also produces the identical compound. As lacewings are not known to be gregarious, the exact ecological purpose of this compound is being investigated.

Conclusions It can be seen that alarm pheromones are used widely by a broad taxonomic diversity of insects and elicit equally varied behavioral responses, including escape or aggressive behavior. Alarm pheromones are generally low molecular weight, organic compounds and so are volatile, dispersing quickly, and do not persist in the environment. In addition, the chemical nature of the alarm pheromone often is unstable, increasing the lack of persistence. This allows conspecifics to be alerted very quickly over a fairly large area and yet not cause false alarm after the danger has passed. Alarm pheromones are often produced in glands responsible for biosynthesis, storage or release of defense secretions. This association between alarm pheromones and defense glands, including those near the sting or mandibles, has led to the hypothesis that alarm pheromones have evolved from chemicals that originally had a defensive role, or are themselves defense compounds that have taken on an additional alarm pheromonal role. The fact that known defense components have additional multifunctional pheromonal roles of alarm (high concentration) and aggregation (low concentration) also points to the possibility that these pheromonal roles have evolved from compounds originally used for defense. Of particular interest is the common lack of species specificity found in alarm pheromones, which is in contrast to that of other pheromones. Sex pheromones, for example, are so specific that they can be the sole identifiable trait in defining morphologically identical populations, such as within the species complex of the sandfly, Lutzomyia longipalpis (Diptera: Psychodidae). However, the alarm pheromone of different aphid species is (E)-β-farnesene and different species of Atta grass- cutting ant use 4-methyl-3-heptanone. In addition, production of (E)-2-hexenal and n-tridecane is ubiquitous as multifunctional pheromone components in terrestrial true bugs, and it is possible that (E)-4-tridecene may reveal itself to be common in green lacewings. Discrimination between these behavioral signal compounds, therefore, is not

Alderflies and Dobsonflies (Megaloptera)

essential to their function as alarm pheromones, and there may even be evolutionary benefits in being able to respond to alarm pheromones of related species of insects.

References Aldrich JR, Blum MS, Lloyd HA, Fales HM (1978) Pentatomid natural products. Chemistry and morphology of the III-IV dorsal abdominal glands of adults. J Chem Ecol 4:161–172 Bowers WS, Nault LR, Webb RE, Dutky SR (1972) Aphid alarm pheromone: isolation, identification, synthesis. Science 177:1121–1122 Bradshaw JWS, Baker R, Howse PE (1979) Multicomponent alarm pheromones in the mandibular glands of major workers of the African weaver ant. Physiol Entomol 4:15–25 Dawson GW, Griffiths DC, Pickett JA, Woodcock CM (1983) Decreased response to alarm pheromone by insectresistant aphids. Naturwissenschaften 70:254–255 Free JB, Pickett JA, Ferguson AW, Simpkins JR, Smith MC (1985) Repelling foraging honeybees with alarm pheromones. J Agric Sci 105:255–260 Hölldobler B, Wilson EO (1990) The ants, 1st ed. The Belknap Press of Harvard University Press, Cambridge, MA Nault LR, Phelan PL (1984) Alarm pheromones and sociality in pre-social insects. In: Chemical ecology of insects. Chapman and Hall, London, UK, pp 237–256 Pickett JA, Griffiths DC (1980) Composition of aphid alarm pheromones. J Chem Ecol 6:349–360

Alarm-Recruitment System Recruitment of nest members to a particular location to aid in colony defense.  Sociality of Insects

Alary Muscles james l. nation University of Florida, Gainesville, FL, USA The alary muscles, so named because of their general wing or delta shape in many insects, lie immediately on top of the dorsal diaphragm. The muscles

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robably aid the dorsal diaphragm in providing supp port for the heart, the part of the dorsal vessel in the abdomen. The muscle fibers fan out from a small point of origin on the lateral wall of the dorsum to a broad insertion on the heart in many insects, presenting the typical delta appearance. In some insects, however, the delta shape is not so evident. Some alary muscle fibers pass beneath the heart and extend laterally from side to side, and thus help to support the heart. In places, the fibers may also run parallel to the long axis of the heart for a short distance. The pairs of alary muscles tend to agree with the number of pairs of ostia, the (usually) lateral openings in the dorsal vessel that allow hemolymph to flow into the heart in the abdomen. Alary muscles generally do not occur in the thorax, but in some insects, a few ostia open outward in the thorax, allowing hemolymph to flow outward. In addition to support, the alary muscle may assist in the expansion (diastole) of the heart after each contractile wave passes a given point, and thus aid in pulling hemolymph into the incurrent ostia. They are not necessary for diastole, however, as evidenced by severing them with little or no apparent effect on the heart beat.

Alate (pl., Alatae or Alates) The winged forms of insects, particularly aphids.

Alderflies Members of the family Sialidae (order Megaloptera).  Alderflies and Dobsonflies

Alderflies and Dobsonflies (Megaloptera) lionel stange Florida Department of Consumer and Agricultural Services, Division of Plant Industry, Gainesville, FL, USA

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Alderflies and Dobsonflies (Megaloptera)

The order Megaloptera comprises about 190 species in 60 genera in two families. All the larvae are aquatic. The larvae, especially of Corydalinae, are among the most primitive of the Holometabola. The metamorphosis from larva to adult is relatively simple. The family Sialidae, commonly called alderflies, is a small group of about 70 species in about eight genera. They are worldwide. Most of the adults have a similar appearance and are usually dark brown to black in coloration. They lack ocelli and have the fourth tarsomere bilobed. They are an ancient group known from the Permian, about 200 million years ago, and evidently have not evolved much since then. In fact, the wing venation has many features in common with the Protoperlaria, a fossil order considered by some as ancestral to the Plecoptera. The adult life span is probably short since the reduced mouthparts do not seem adapted for extensive feeding. The eggs are laid in rows, forming large masses situated on branches, bridges, and other objects overhanging the water. The larvae hatch and fall into the water where they are predacious on other aquatic insects, especially caddisflies. There are as many as 10 larval instars which may last up to two or more years until pupation. The larva crawls out of the water and digs into the bank to form an earthen cell several feet from the edge of the water. The genera are restricted geographically. The genus Sialis Latreille is Holarctic, Protosialis Van der Weele is South American, Austrosialis Tillyard and Stenostialis are Australian, Haplosialis Navas is from Madagascar, Leptosialis is African, Indosialis Lestage is Oriental and Nipponsialis Kuwayama is Japanese. The larva has seven lateral processes and the abdomen terminates in an elongate process. The only world compilation is by Van der Weele (1910) but is greatly out of date. The family Corydalidae, or dobsonflies, is characterized by having three ocelli and the anal region of the hindwing is very wide, folded fanlike at rest (Fig. 31). The fourth tarsomere is not modified. There are several hundred species in about 20 genera and two subfamilies.

Alderflies and Dobsonflies (Megaloptera), Figure 31 Adult dobsonfly (Corydalidae).

The Corydalinae with about 60 species, is distributed in the New World (three genera), South Africa (one genus) and Asia (f ive genera). This subfamily does not have pectinate antennae and the head is usually quadrate, often with a postocular spine. Often there are more than four crossveins between the radius and radial sector. The male terminalia are distinctive with a well developed ninth gonostylus. Many of the species are very large. Corydalis Latreille is the largest genus in the New World with about 30 species. The males of this genus often have the mandibles greatly extended which is similar to Acanthacorydalis Van der Weele from Asia. Platyneuromus christil (Navás) from Central America, has a tremendously expanded postocular flange. The larva has eight lateral processes and the abdomen ends in a pair of claw-like structures. In America, the larvae are called hellgrammites and are used for fishing. In one case, a larva was found inside a fish stomach many hours after ingestion. Glorioso (1982) has provided a good reference.

Alexander, Charles Paul

The Chauliodini was reviewed by Kimmins (1954) who recognized 12 genera. The genera are restricted in distribution similar to the Corydalinae and are found in the Cape region of South Africa (two genera), North America (four genera), Chile (three genera), Australia (one genus), Madagascar (one genus), and Asia (four genera). Males and rarely females have pectinate antennae in some genera.

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References Beier M (1973) The early naturalists and anatomists during the renaissance and seventeenth century. In: Smith RF, Mittler TE, Smith CN (eds) History of entomology. Annual Reviews, Inc., Palo Alto, CA, pp 81–94 Nordenskiöld E (1935) The history of biology: a survey. Tudor, New York, NY, 629 pp

Aldyidae References Glorioso MJ (1981) Systematics of the dobsonfly subfamily Corydalinae (Megaloptera: Corydalidae). Sys Entomol 6:253–290 Kimmins DE (1954) A new genus and some new species of the Chauliodini (Megaloptera), with notes on certain previously described species. Bull Br Mus Nat Hist Entomol 3:417–444 Van der Weele (1910) Megaloptera. Collections Zoologiques du Baron Edm. de Selys Longchamps, fasc 5, 93 pp

Aldrovandi, Ulisse (Ulysse, Ulysses) Ulisse Aldrovandi was born in Bologna, Italy, in 1522. He studied law in Bologna, and then philosophy and medicine in Padua and Rome, earning a doctorate in medicine in 1552. In 1560, he was appointed professor in Bologna, a position that he held for 40 years. He lectured mainly on pharmacology, but he collected natural history objects and employed artists to draw them. He published four large volumes during his lifetime, but his friends and pupils used his voluminous manuscripts to publish 10 more volumes after his death. His (1602) “De animalibus insectis libri VII” was the first book to be published on insects, although the “insects” included various other kinds of invertebrates. A chapter was devoted to the structure of the insect body. Insect reproduction and metamorphosis were described; respiration and the senses of touch, taste, and smell are discussed, and the life of honey bees is described. He died in 1605.

A family of bugs (order Hemiptera). They sometimes are called broad-headed bugs.  Bugs

Aleyrodidae A family of insects in the order Hemiptera. They sometimes are called whiteflies.  Whiteflies  Bugs

Alexander, Charles Paul Charles Alexander was born in New York state on September 25, 1889. He entered Cornell University in 1909, receiving B.Sc. and Ph.D. degrees in 1913 and 1918, respectively. He was employed as systematic entomologist in the Snow Entomological Museum at the University of Kansas in 1917– 1919 and then by Illinois Natural History Survey in 1919–1922. Next he moved to Massachusetts Agricultural College and was placed in charge of teaching entomology. He served as chairman of the Department of Entomology and Zoology for 10 years, for the last three of which he was dean of the School of Science (of what had by then become the University of Massachusetts). He was president of the Entomological Society of America in 1941–1943 (two terms). His almost exclusive subject of research was the family Tipulidae (crane flies) about which he published over 1,000 papers

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Alfalfa Leafcutting Bee, Megachile Rotundata (Hymenoptera: Megachilidae)

and described over 10,000 species, an enormous production. After retirement from teaching, he moved his insect collection to his house and continued working on it until the death of his wife, Mabel, in 1979. Two years later he transferred his collection to the National Museum of Natural History in Washington, DC. He died at home in Massachusetts on December 12, 1981.

commercial scale. M. rotundata is of eastern Mediterranean origin and was first found in North America in the 1940s near seaports. It probably gained entry as diapausing pre-pupae within tunnels in the wood used to make shipping crates or pallets.

Reference

Once a suitable tunnel has been found, the female uses her mandibles to neatly cut oblong pieces of leaves or flower petals which she uses to build cells end to end in the tunnel, starting at the far end and finishing near the entrance (Fig. 32). About 15 leaf pieces are arranged in overlapping layers and cemented together to form a thimbleshaped cell with a concave bottom. The cell is then provisioned with nectar and pollen. During this process, the female enters the tunnel head first, regurgitates the nectar, then turns around to remove the pollen from the scopa (the pollencollecting hairs on the underside of her abdomen) and tamps the pollen into the nectar with the tip of her abdomen. The provisions for each cell consist of about two-thirds nectar and one-third pollen, requiring 15–25 provisioning trips. It is while collecting the nectar and pollen that the bees pollinate the flowers that they visit. When the cell has been adequately provisioned, the female lays a single egg directly on the surface of the provisions and then caps the cell with several circular leaf pieces. She then proceeds to construct the next cell, repeating this process until the tunnel is filled. She then plugs the end of the tunnel with 10–15 leaf pieces cemented together to form a plug. Females continue filling tunnels with cells until pollen and nectar sources are no longer available. Upon hatching, the larva immediately begins feeding on the provisions within its cell, undergoing four instars before reaching maturity. It then deposits a ring of fecal pellets within the cell and spins a tough silken cocoon within which it overwinters as a diapausing pre-pupa. During the feeding period, the waste

Byers GW (1982) In memoriam Charles P. Alexander 1889– 1981. Journal of the Kansas Entomological Society 55:409–417

Alfalfa Leafcutting Bee, Megachile rotundata (Hymenoptera: Megachilidae) mark s. goettel Agriculture and Agri-Food Canada, Lethbridge, AB, Canada The alfalfa leafcutting bee, Megachile rotundata Fabricius (Hymenoptera: Megachilidae), has been successfully semi-domesticated within the last 50 years to pollinate alfalfa for seed production in North America. Honey bees are inefficient pollinators of alfalfa and, although bumbles bees and some other wild bees are efficient pollinators, they have proved difficult to manage. The use of the alfalfa leafcutting bee has succeeded in greatly increasing the seed yield of alfalfa. In western Canada, the average alfalfa seed yield using this bee exceeds 300 kg/ha, whereas without it is usually less than 50 kg/ha. The genus Megachile contains many species that nest in tunnels in dead trees or fallen logs. Most are solitary, but M. rotundata is gregarious and, although each female constructs and provisions her own tunnel, she will tolerate close neighbors. This behavioral characteristic is one of the main reasons why this species has been amenable to management on a

Life History


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Alfalfa Leafcutting Bee, Megachile Rotundata (Hymenoptera: Megachilidae), Figure 32 Alfalfa leafcutting bee, Megachile rotundata. (1) Adult on alfalfa flower. Flowers are pollinated while the bees visit the flowers to collect nectar and pollen for provisioning their cells. (2) A single egg is deposited on the surface of pollen/ nectar provisions within a cell which the female constructs within tunnels using oblong pieces of leaves or flower petals. (3) The egg placed into the cell hatches within 2 to 3 days and the larva immediately begins to consume the provisions. The larva pupates after undergoing 4 instars. (a) single egg, (b) 3rd instar, and (c) 4th instar larvae within the cell. Cell caps have been removed. (4) X-ray of leafcutting bee cells used to determine quality of c ommercial bees. (a) empty cell, (b) chalkbrood cadavers, (c) Pteromalus venustus parasitoid cocoons. (5) Nesting boards separated to show arrangement of bee cells constructed within the tunnels. In the fall, the boards are removed from the field and the cells are stripped from the boards using specialized automated equipment. (6) Chalkbrood cadaver within the cell. Note the ring of frass deposited on the outside edge of the cell. Normally, the larva would spin a tough silken cocoon within which it overwinters as a diapausing pre-pupa. Larvae infected with chalkbrood usually succumb just after defecating and just prior to cocoon spinning.

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products of digestion are accumulated internally until the larva defecates just before forming the cocoon. In the spring, the pre-pupa pupates. After a pupal period of 3–4 weeks, the adult emerges and chews its way out of the cocoon. Mating takes place soon after emergence of the adults. Females store enough sperm from a single mating to fertilize all of their eggs. Soon after mating, the females seek out suitable sites in which to excavate tunnels or select suitable preexisting ones, either natural or man-made.

Domestication The gregarious nature of M. rotundata and its willingness to accept artificial domiciles has permitted the commercial scale management of this species for crop pollination. Initially, observant alfalfa seed producers in the northwestern U.S.A. noticed that this species, which had undergone a population increase following natural establishment, would nest in man-made structures such as shingled roofs and they started to provide artificial tunnels by drilling holes in logs positioned around the edges of the seed fields. The next step was to provide nests consisting of wooden blocks drilled with closely spaced tunnels. Although reasonably successful on a small scale, this method was not suitable for the management of the large numbers of bees (50,000–75,000/ha) required for commercial alfalfa seed production. Consequently a “loosecell” system was developed. This system uses 10 mm thick boards of wood or polystyrene which are grooved on both sides and stacked together to form hives of closely packed tunnels about 7 mm in diameter and 150 mm in length. At the end of the season, the boards are separated and the cells removed using specialized automated equipment. After being stripped from the boards the cells are tumbled and screened to remove loose leaf pieces, molds and some parasites and predators. The clean cells are then placed in containers for overwintering storage at about 50% R.H. and 5°C. In the spring, the cells are placed in trays for incubation at 70%

R.H. and 30°C. A few days before the bees are due to emerge, the trays are moved to especially designed shelters spaced throughout the alfalfa seed fields. By selecting the date when incubation begins, and if necessary manipulating the incubation temperature, the emergence of the bees can be adjusted to coincide with the start of alfalfa bloom. An advantage of the loose cell system of management is that it facilitates the control of parasitoids, predators and disease, and assessment of the quality of the progeny. Leafcutting beekeepers routinely send samples of cells to specialized leafcutting bee “cocoon” testing centers, where they are x-rayed and incubated to provide estimates of numbers of intact cells, incidence of parasites and pathogens, and sex ratio. These data are used to determine stocking rates and to set a price if bees are to be marketed. The proportion of females, which is usually only about a third, is of particular interest because they are the primary pollinators.

Natural Enemies About 20 species of insects are known to parasitize or prey on the immature stages of the alfalfa leafcutting bee. The most important of these are several species of chalcid wasps, including Pteromalus venustus Walker, Monodontomerus obscurus Westwood, Melittobia chalbii Ashmead and Diachys confusus (Girault). The most widespread and damaging is P. venustus, which probably arrived in North America with its host. The female parasitoid pierces the host cocoon with her ovipositor, stings the larva or pupa to paralyze it, and then lays some eggs on its surface. The parasitoid larvae then feed upon the bee larva eventually killing it. Normally 15–20 adult P. venustus emerge from each host cocoon. Two other enemies, which are more of biological interest than economic significance, are several species of cuckoo bees, Coelioxys (Megachilidae) and the brown blister beetle, Nemognatha lutea LeConte. Cuckoo bees are very similar to

Alfalfa (Lucerne) Pests and their Management

leafcutting bees, but lack the structures required for collecting pollen. The female cuckoo bee lays her egg in the partially provisioned cell of the leafcutting bee while the rightful owner is out foraging. When partly grown, the cuckoo bee larva kills the leafcutting bee larva and usurps the provisions. Brown blister beetle females lay their eggs on flowers and the first instar larvae (triungulins) attach themselves to any bee that visits the flower. When the bee returns to its nest, the triungulin detaches and begins feeding on the cell contents, destroying 2 or 3 cells before reaching maturity. Several stored-product insects including the driedfruit moth, Vitula edmandsae serratilinnella Ragonot, and stored-product beetles such as the sawtoothed grain beetle, Oryzaephilus surinamensis (Linnaeus), the red flour beetle, Tribolium castaneum (Herbst) and the confused flour beetle, Tribolium confusum (Jacquelin du Val) can cause serious damage during overwintering storage, especially if sanitation practices are lax. Most of the parasitoids and predators can be largely controlled by proper construction of hives and nesting materials, physical removal during the loose-cell processing and strict hygiene during storage. However, successful control of the major pest, the chalcid P. venustus, often requires carefully controlled fumigation using dichlorvos (2, 2-dichloro-vinyl dimethyl phosphate) resin strips. The only disease causing significant losses to the leafcutting bee industry is chalkbrood, caused by the fungus Ascosphaera aggregata Skou. The disease was first reported in leafcutting bees in 1973, and remains most severe in the western U.S. states, where losses of more than 65% of bees are not uncommon. Bee larvae become infected after consuming pollen provisions contaminated with the fungal spores which germinate within the midgut and penetrate into the hemocoel. Larvae soon die and turn a chalk white color as the mycelium fills the body. Sporogenesis occurs beneath the host cuticle resulting in the formation of ascospores which are bound in “spore balls” within ascomata. At this stage, the cadaver turns black. Spores are spread by adults that must chew their

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way through infected cadavers in order to exit their nesting tunnels. Chalkbrood can be adequately managed through strict hygiene and decontamination of the bee cells, nest materials and shelters. Initially, decontamination was performed by dipping in household bleach. However, fumigation with paraformaldehyde has become the method of choice, and is highly effective for the control of both A. aggregata and foliar molds, which can sometimes pose a health risk to the beekeeper.  Bees

References Goerzen DW, Watts TC (1991) Efficacy of the fumigant paraformaldehyde for control of microflora associated with the alfalfa leafcutting bee, Megachile rotundata (Fabricius) (Hymenoptera: Megachilidae). BeeScience 1:212–218 Goettel MS, Richards KW, Goerzen DW (1993) Decontamination of Ascosphaera aggregata spores from alfalfa leafcutting bee (Megachile rotundata) nesting materials by fumigation with paraformaldehyde. BeeScience 3:22–25 Hill BD, Richards KW, Schaaljie GB (1984) Use of dichlorvos resin strips to reduce parasitism of alfalfa leafcutter bee (Hymenoptera: Megachilidae) cocoons during incubation. J Econ Entomol 77:1307–1312 Richards KW (1984) Alfalfa leafcutter bee management in Western Canada. Publication #1495E. Agriculture Canada, Ottawa, Canada, 53 pp Richards KW (1987) Alfalfa leafcutter bee management in Canada. Bee World 68:168–178 Vandenberg, JD, Stephen WP (1982) Etiology and symptomatology of chalkbrood in the alfalfa leafcutting bee, Megachile rotundata. J Invertebr Pathol 39:133–137

Alfalfa (Lucerne) Pests and their Management john l. capinera University of Florida, Gainesville, FL, USA Alfalfa (lucerne), Medicago sativae, is one of the most important legumes used in agriculture. It is the principal roughage for ruminants, as well as

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being an important source of protein in animal diets. It is surpassed only by grass, corn, and soybean as an animal feed, and is especially important to the dairy industry. The USA is the world’s largest producer of alfalfa, but it also is an important crop in Australia, Europe, Argentina, China, South Africa, and the Middle East. There are other uses for alfalfa, though they are minor. Alfalfa sprouts are a salad ingredient, alfalfa shoots are sometimes consumed as a leafy vegetable, and dehydrated alfalfa is sometimes formulated as a tablet to be consumed as a dietary supplement. Alfalfa is a cross-pollinated species. It relies on insects, often domesticated leafcutting bees, honey bees, alkali bees, and various wild bees, for pollination. Wind pollination does not occur because the blossom is structured in a way that physical “tripping” to expose the stigma to the anthers is required. Bees manipulate the blossom when foraging for nectar and pollen and thereby “trip” the blossom, an action that results in the bee being struck in the head. An interesting aspect of pollination is that some bees learn to avoid the tripping process to avoid being struck, thereby robbing the flower without pollination occurring. Older honey bees are good at avoiding tripping, but naïve young honey bees trip the blossom and provide pollination. Alfalfa is normally harvested before, or at, the initiation of flowering, which maximizes protein content of the harvested hay. Because pollinators are often present in alfalfa fields during the bloom period, care must be taken when using insecticides for pest suppression to avoid products that are highly toxic to pollinators, at least if seed production is a concern. However, most alfalfa is grown only for forage, and without regard for seed production. Thus, insecticide use may include the bloom period, though if pollinator populations are reduced, other crops that require pollination may be inadvertently affected. Alfalfa is unusual as a field crop in that it is a short-lived perennial, living 3–12 years. It may be harvested from once to 12 times per year, depending on climate and growing conditions. It has deep roots, and is resistant to drought, though in arid

climates it is irrigated. It is tolerant of cold, growing well in cool and cold climates. It does not tolerate hot, humid climates, however. Alfalfa often is cut and dried before it is baled and stored. To speed up the process of drying, alfalfa is commonly flailed or passed through a set of rollers to break or crush the stems, facilitating the drying process. The crushing process is called crimping and sometimes can cause problems for horses because blister beetles (Coleoptera: Meloidae) are incorporated into the hay (see below, blister beetles). Dried alfalfa is tied into bales of various sizes, including large cylindrical bales, and stored under shelter, or packaged in plastic, to avoid moisture. If the alfalfa is to be fed to cattle, however, it is not dried, and instead it is finely chopped and stored in trenches, silos, or bags where it can ferment and maintain high nutrient levels. Cattle are not very susceptible to poisoning by blister beetles. Alfalfa has undergone considerable breeding to produce strains that have not only suitable agronomic conditions, but also are disease and pest resistant. Nevertheless, insects can damage alfalfa nearly everywhere it is grown. Some of the important pests are listed in the table, and the most important are discussed below.

Alfalfa Weevil, Hypera postica (Gyllenhal) (Coleoptera: Curculionidae) In many regions, this is the most important pest of alfalfa. It is found in Europe, the Middle East, Central Asia, and North America. Alfalfa weevils overwinter as adults in the soil of weedy, brushy areas near alfalfa fields. They disperse to alfalfa in the spring and oviposit within the stems. The eggs are oval and yellow. Early instars developing from these eggs are slate colored, but develop a bright green color and a white stripe down the middle of the back as they mature. Larvae have a black head capsule. They display four instars and will grow to about 8–10 mm in length. After feeding for 3–4 weeks, larvae spin loosely constructed cocoons on


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Alfalfa (Lucerne) Pests and their Management, Table 5 Some pests of alfalfa (lucerne), and locations where they are considered to be damaging Feeding behavior

Primary taxon

Common name

Scientific name

Location

Above-ground, chewing

Coleoptera

Sitona weevil

Sitona discoides

Australia

Small lucerne weevil

Atrichonotus taeniatulus

Australia

Vegetable weevil

Listroderes obliquus

Australia

Alfalfa weevil

Hypera postica

Europe, Asia, N. America

Clover leaf weevil

Hypera punctata


Clover head weevil

Hypera meles

Europe, N. America

Blister beetles

Epicauta spp.

N. America

Flea beetles

Epitrix, Systena, Disonycha spp.

N. America

Orthoptera

Grasshoppers

Melanoplus spp.

N. America

Wingless grasshopper

Phaulacridium spp.

Australia

Lepidoptera

Armyworm

Mythimna spp.,

Australia

Armyworm

Persectania spp.

Australia

Armyworm

Pseudaletia unipuncta

N. America

Variegated cutworm

Peridroma saucia

Europe, Asia, Africa, N. America

Army cutworm

Euxoa auxiliaris

N. America

Granulate cutworm

Agrotis subterranean

N. America, S. America

Black cutworm

Agrotis ipsilon

N. America, Europe, Africa

Beet armyworm

Spodoptera exigua

Asia, N. America

Fall armyworm

Spodoptera frugiperda


Budworm

Helicoverpa punctigera

Australia

Corn earworm

Helicoverpa zea


Alfalfa looper

Autographa californica

N. America

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Alfalfa (Lucerne) Pests and their Management, Table 5 Some pests of alfalfa (lucerne), and locations where they are considered to be damaging (Continued) Feeding behavior Primary taxon Common name Scientific name Location

Lucerne leafroller

Merophyas divulsana

Australia

Alfalfa caterpillar

Colias eurytheme

N. America

Webworms

Loxostege spp.

N. America, Europe, Asia

Collembola

Lucerne flea

Sminthurus viridis

Australia, Europe, Africa

Diptera

Alfalfa blotch leafminer

Agromyza frontella

Europe, N. America

Above-ground, sucking

Acari

Redlegged earth mite

Halotydeus destructor

Australia

Clover mite

Bryobia spp.

Australia

Twospotted spider mite

Tetranychus urticae

No. America

Collembola

Lucerne flea

Sminthurus viridis

Europe, N. Africa, Australia

Hemiptera

Pea aphid

Acythosiphum pisum

Europe, Asia, Australia, N. & S. America

Blue alfalfa aphid

Acythosiphum kondoi

Mediterranean, Australia, N. & S. America

Spotted alfalfa aphid

Therioaphis maculata

Mediterranean, Australia, N. America, Asia

Potato leafhopper

Empoasca fabae

N. America

Lucerne leafhopper

Austroasca alfalfae

Australia

3-cornered alfalfa hopper

Spissistilus festinus

N. America

Meadow spittlebug

Philaneus spumarius

N. America

Tarnished plant bugs

Lygus spp.

Europe, N. America

Alfalfa plant bug

Adelphocoris spp.

Europe, N. America

Thysanoptera

Flower thrips

Frankliniella spp.


Below-ground

Coleoptera

Clover root curculio

Sitona hispidula

Europe, N. & C. America


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Alfalfa (Lucerne) Pests and their Management, Table 5 Some pests of alfalfa (lucerne), and locations where they are considered to be damaging (Continued) Feeding behavior Primary taxon Common name Scientific name Location

Alfalfa snout beetle

Otiorhynchus ligustici

N. America

African black beetle

Heteronychus arator

Africa, Australia

Whitefringed beetle

Naupactus leucoloma

Australia, S. America

Small lucerne weevil

Atrichonotus taeniatulus

Australia

plants or in litter on the soil, pupate, and emerge as adults in 1–2 weeks. Adults are 5–6 mm long, have a long snout, and have a dark stripe down the back. They are light brown at emergence and darken in several days. The number of generations varies according to climate, but eventually they leave fields for grassy, brushy, weedy areas where they become inactive until the onset of winter. Damage is caused by the larval stage which feeds on leaves; damage ranges from pinholes to skeletonization of leaves. Adults generally cause minor damage. Peak damage is usually just prior to the first cutting or after the first cutting, as both larvae and adults feed on new growth; this can seriously affect regrowth of the stand. Also, cool, cloudy weather exacerbates damage done by the alfalfa weevil. Cool and cloudy weather conditions slow the regrowth rate of alfalfa, and also increase the daily feeding period of the weevil because both larvae and adults tend to hide under crop residue during bright sunlight and will not actively feed during such periods. Weevil larvae can be found early in the Spring. It is important to scout for live larvae and injured terminals on the first crop, but also subsequent crops. Sweep net sampling can be used to detect weevil presence. Several species of wasps can be effective in maintaining weevil populations below economic threshold levels. Among the effective parasitoids are Bathyplectes curculionis (Thomson), B. anurus (Thomson) and B. stenostigma (Thomson) (Hymenoptera: Ichneumonidae); Microctonus

aethiopoides Loan and M. colesi Drea (Hymenoptera: Braconidae) Oomyzus incertus (Ratzenberg) (Hymenoptera: Eulophidae); Dibrachoides dynastes (Forester) and Peridesmia discus (Walker) (Hymenoptera: Pteromalidae); and Anaphes luna (Girault) (Hymenoptera: Mymaridae). A fungal pathogen, Zoophthora phytonomi Arthur (Phycomycetes: Entomophthoraceae), attacks weevil larvae and can control populations in several days, though it is most effective under moist conditions. These biological control agents are extremely effective control measures in all but major outbreak periods. However, when fields show damage on 35–40% of plant tips more than 7–10 days prior to harvest, chemical suppression is often initiated. Early harvest (first crop) is very effective in killing larvae, and is preferred to chemical control if the planned harvest is less than 7–10 days away. If harvesting is used to control alfalfa weevil, the stubble and debris should be examined closely for adults and larvae, and stems should be examined for feeding signs. It may be necessary to spray stubble, though in many areas producers can avoid insecticide use consistently through timing of harvest.

Root Weevils, Sitona spp., Atrichonotus taeniatulus (Berg), Others (Coleoptera: Curculionidae) Root weevils such as clover root curculio, Sitona hispidula (Fabricius), in North America; and sitona

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weevil, Sitona discoideus Gyllenhal, small lucerne weevil, Atrichonotus taeniatulus (Berg), in Australia, and whitefringed beetle, Naupactus leucoloma Boheman in Australia and South America, can be significant pests of alfalfa. Although the adults commonly feed on the foliage, the principal damage is due to larval feeding on the roots of the alfalfa plant. Eggs are laid in fall or spring, on the soil surface or lower parts of plants. Eggs hatch in the winter or spring. White, legless larvae move into the soil and feed on roots until they pupate. Pupae are found just below the soil surface. Adults emerge in the summer months and live up to a year. The adults are brown or black, blunt-snouted weevils up to about 10 mm long. There is one generation per year. Adults migrate by crawling, and thus infest new areas rather slowly. The adults feed on alfalfa leaf margins, leaving crescent-shaped notches, and chew on stems and leaf buds of seedlings, but this tends to cause minor loss. Most damage is caused by the larvae. First larval instars feed on root nodules and lateral roots; later instars feed on the taproot. Feeding on the taproot can girdle the plant, resulting in plant death. Such damage also weakens the overall vigor of a stand, perhaps contributing to winter-kill and increased susceptibility to disease. It is difficult to control larvae because they are in the soil and largely protected from insecticide. Suppression aimed at adults usually requires multiple applications. It is inadvisable to plant alfalfa into a field which has previous ly been infested, to plant into fields previously supporting legume crops, or to seed alfalfa next to established stands.

Blister Beetles (Epicauta spp.) (Coleoptera: Meloidae) There are several species of North American blister beetles that can be of concern in alfalfa. They are a problem not because of their food habits (they tend to feed mostly on blossoms) but because they contain the toxin cantharidin within their bodies. When alfalfa is harvested, if the hay is crimped it may

c ontain crushed blister beetles that may prove toxic to horses that ingest the hay. The most abundant blister beetle in alfalfa fields generally is the black blister beetle, E. pensylvanica (De Geer). However, the species that is most toxic is E. vittata (Fabricius). Most blister beetles are recognized by the shape of their body. They are narrow, cylindrical, and soft. The region between the head and wings is distinctly narrower than the wings, and is usually narrower than the head. Most species have one generation per year, although some have two. Blister beetles overwinter as larvae. The adults begin to emerge in the Spring and adults deposit their eggs where grasshopper egg pods may occur, as larvae feed on the grasshopper eggs. If grasshoppers are not abundant, then blister beetles are unlikely to be abundant. When both are numerous, it is advisable to harvest alfalfa early, before bloom, as this is the only time that beetles are attracted to the crop. There is some yield loss associated with this approach, of course, and an alternative it to treat the crop with insecticides. If insecticide is used, alfalfa should be harvested as soon as possible after the pre-harvest interval expires, to get hay out of the field before it is re-infested. A principal problem with blister beetle management is that the beetles tend to aggregate. Thus, there may be relatively few beetles in field, but a large number in one location, and these may be crushed together and concentrated into one or a few bales of hay. Thus, they are hard to detect by standard sampling methods. When alfalfa hay is purchased for horses, it is advisable to acquire early-crop hay, or hay from areas free of high grasshopper populations. Alternatively, inspection of the hay as it is fed to horses can reveal the presence or absence of beetles.

Potato Leafhopper, Empoasca fabae (Harris) (Hemiptera: Cicadellidae) Potato leafhopper is indigenous to eastern North America. Adults are about 3.5 mm long,


wedge-shaped, winged, and green. Nymphs are similar in appearance, but are smaller, yellowishgreen to fluorescent green, and wingless. Each Spring, potato leafhoppers migrate north from southern states where they overwinter. Timing of the first and subsequent arrivals in the north is heavily dependent on weather patterns. Adults lay eggs in stems and leaf veins; eggs hatch in 6–9 days in mid-summer. Each generation takes approximately 30–35 days to mature, resulting in several generations. Adults and nymphs both feed on alfalfa with piercing-sucking mouthparts, sucking plant sap and injecting a toxin into the plant. Damage is called “hopperburn,” and is a yellow wedge-shape area beginning at the tips of leaves. The leaves may eventually turn entirely yellow or reddish. Plants may become stunted. Leaf hoppers cause yield loss, reduced nutritional quality of alfalfa, and reduced plant vigor that results in increased winter-kill and slower regrowth of the crop the next spring. In some regions of the USA, the potato leaf hopper is the worst insect pest of alfalfa, and can cause losses of 80% or more if not controlled. Leaf hoppers are not generally a problem in the first crop in an established stand, but as the population increases, all subsequent crops will need to be monitored for infestation. The characteristic hopperburn will not appear until some yield and quality loss has occurred, so it is important to scout for leaf hoppers weekly on the second and subsequent crops. Scouting may be concluded 7–10 days prior to harvest. Potato leaf hopper economic thresholds are based on plant height. Scouting is accomplished by sweep net sampling. As an example, following are treatment thresholds recommended for Minnesota, USA. Average plant height

# adult leafhoppers/ sweep

< 3 inches

0.3

3–7 inches

0.5

8–12 inches

1.0

> 12 inches

2.0

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Although the potato leaf hopper has natural enemies, they often get left behind when the adults disperse. Thus, a combination of crop monitoring and insecticide suppression is often the principal management strategy. Chemical control of potato leafhopper is effective, but should not be used if harvest is within seven days of harvest. Cutting will kill a large percentage of nymphs, and will force adults out of the field. Cutting is the control of choice if thresholds are reached within seven days of harvest. Additionally, early harvest may be an alternative to insecticides when thresholds are reached late in the year.

Aphids (Hemiptera: Aphididae) Several aphids are pests of alfalfa, including pea aphid, Acyrthosiphon pisum (Harris); blue alfalfa aphid or bluegreen aphid, Acyrthosiphon kondoi Shinji, cowpea aphid, Aphis craccivora Koch; green peach aphid, Myzus persicae Sulzer; and spotted alfalfa aphid, Therioaphis maculata Buckton. All these aphids are small, measuring 3 mm or less. Their color varies, depending on species. They may or may not be winged. In most climates, in early Spring nymphs hatch from eggs that were laid in the fall; these aphids are all female. Females can reproduce without mating when conditions are favorable, and they do so in Spring and Summer. In the Summer, the entire life cycle takes only a few days. Males appear in late Summer, and mate with females to produce eggs capable of overwintering. Aphids use piercing-sucking mouthparts to remove plant sap, and prefer to feed on young growth. Aphid feeding can result in stunted or wilted plants. The plants may also turn yellow. Aphids commonly attain high densities in alfalfa, but in most years natural enemies keep aphid populations at levels that are not economically important. Many natural enemies of pea aphids exist, including green lacewing larvae (Neuroptera: Chrysopidae), damsel bugs (Hemiptera: Nabidae), and parasitic wasps

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(Hymenoptera, various families), lady beetles (Coleoptera: Coccinellidae), and disease (fungi).

Plant Bugs (Hemiptera: Miridae) Several species of plant bugs affect alfalfa, but the most common are tarnished plant bug, Lygus lineolaris (Palisot de Beauvois), and alfalfa plant bug, Adelphocoris lineolatus (Goeze). Adult tarnished plant bugs are brown, winged, and 4–6 mm long; nymphs are green, wingless, and the third and subsequent instars have black spots. Adult alfalfa plant bugs are light green, winged, and 7.5–10 mm long; nymphs are green, wingless, and have red eyes. Tarnished plant bugs overwinter as adults; alfalfa plant bugs overwinter as eggs in plant tissue. During the growing season, the entire life cycle takes 20–50 days, depending on temperature. There are two to five generations per year. Plant bugs suck sap from plants and inject toxic saliva into the plant. They cause leaves to crinkle, plants to be stunted, and flower buds to abort. They are abundant in all but the earliest portions of the season. Although traditionally considered mostly a seed pest, plant bugs also contribute to forage yield reductions. If bugs are abundant more than seven days prior harvest, chemical control may be warranted.

Grasshoppers (Melanoplus spp. and Phaulacridium spp.) (Orthoptera: Acrididae) Everywhere alfalfa is grown, grasshoppers and locusts will feed on the crop. However, they are only casually associated with alfalfa, attacking the crop only when abundant. None feed preferentially on alfalfa. In North America, the principal pests are Melanoplus spp., and in Australia Phaulacridium spp. is the major grasshopper pest. These economically important grasshoppers overwinter as eggs. Populations disperse into cultivated fields or pastures as their populations build through the season.

Most egg laying occurs in late summer and fall in production areas; most species prefer uncultivated, grassy or weedy areas, and lay eggs 1–3 cm below the soil surface. Grasshoppers are generally considered a minor pest except during periods of great abundance, and then they can do great damage. An exception is Australia, where wingless grasshopper has become an increasingly severe pest of alfalfa. Damage has increased in Australia due to widespread cultivation of alfalfa, which is more suitable than grasses for nymphal growth and survival. Grasshopper nymphs and adults damage alfalfa by chewing on leaves from the margin inward in an irregular pattern. Attacks are often on new growth, but will occur on any stage. The margins of fields are most likely to be damaged. In North America, grasshopper infestations are more severe in warm and dry years. Warm, dry weather immediately following egg hatch favors survival of nymphs, because nymphal growth rates and survival are lower in cool, wet weather. Long, warm autumns prolong the egglaying season, and result in larger populations in the next growing season. It can take 3–5 years for populations to build to economically important levels. In Australia, drought also is implicated, but mermithid nematodes are a critical element in grasshopper biology. Absence of rainfall, and clearing of drier, higher elevation pasture impedes the ability of the nematodes to parasitize the grasshoppers. Grasshoppers are naturally suppressed by numerous natural enemies, but when weather conditions favor the grasshoppers their populations increase quickly. The natural enemy population increases as their food supply becomes more available, but the lag in natural enemy abundance can result in crop damage by the grasshoppers. Weedy fence rows, irrigation ditches, and fallow fields are important sources of grasshoppers. Weed populations should be managed, which may require tillage or burning to make these habitats less productive for grasshoppers.


Cutworms, Armyworms and Budworms (Lepidoptera: Noctuidae) The caterpillars of several moths can become abundant enough to cause significant loss to alfalfa.Among these are the armyworms Mythimna spp., Persectania spp., and Pseudaletia unipuncta Haworth; variegated cutworm, Peridroma saucia (Hübner); army cutworm, Euxoa auxiliaris (Grote); granulate cutworm, Agrotis subterranea (Fabricius); beet armyworm, Spodoptera exigua (Hübner); budworm, Helicoverpa punctigera (Wallengren), and many others. The important species vary among regions, though they are similar ecologically. The larvae of cutworms, armyworms, and budworms range in color from greenish-yellow to brownish-black. Larvae are 2–5 cm long at maturity. The wings of the adults vary from tan to dark brown with mottling or stripes. Pupae are 1–3 cm long and are reddish-brown to black in color. There are one to six generations per year. Larvae overwinter in the larval or pupal stage, depending on species. Larvae feed on stems and leaves of plants, and can limit regrowth after harvest. Larvae will also cut the stems of seedlings. Their occurrence as economic pests is sporadic. Although these insects have many natural enemies, when they are abundant insecticides are the preferred approach to population reduction.

Lucerne Flea, Sminthurus viridis (Collembola) Sminthurus viridis, the lucerne flea or clover springtail, is an insect relative (hexapod) belonging to the order Collembola (the springtails). It is bright green with a roughly spherical body and may swarms in large numbers on living plants, including alfalfa or lucerne, thus the first part of the common name. The second part of the common name was given for its jumping

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ability and its minute size, not because it is a flea or related to fleas. This species has a patchy distribution in Europe and North Africa, and has been accidentally introduced to Australia, where it is most injurious. It also affects lupine flowers, lentils, beans, and field peas. Immature lucerne fleas consume small patches of foliage, whereas adults consume the entire leaf except for the veins. Early season spraying of insecticide is the most common recommendation to curb their damage.

Mites (Acari) Mites generally are not major pests of alfalfa, but under arid conditions or along the margins of f ields they can be quite damaging. The most important are clover mites, Bryobia spp. (Acari: Tetranychidae), and redlegged earth mite, Halotydeus destructor Tucker (Acari: Penthaleidae), in Australia, and twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) in North America. They rupture the cells of leaf tissue, imparting a silver or yellow appearance, and reducing yield.

Pest Management in Alfalfa Alfalfa is an excellent crop for the practice of modern pest management tactics because (i) it is quite tolerant of damage; cosmetic injury is not important; (ii) it is a perennial crop, providing harborage throughout the year for an immense assemblage of insects, including predators and parasitoids; (iii) it is an important crop, so extensive research on the pests have been conducted; (iv) it is amenable to various cultural manipulations, and produces multiple crops over a large portion of the year; and (v) it is a favorite crop for rotations, so there is ample opportunity to integrate its culture with the culture of other crops. The principal tactics used for alfalfa production include scouting and use of an economic threshold for decision making, natural and classical

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Alfalfa Weevil, Hypera Postica (Gyllenhal) (Coleoptera: Curculionidae)

biological control, cultural control, and chemical control. The economic threshold varies among insect species, geographic locations, crop management practices and economic conditions, but most locations have established such benchmarks for initiating chemical control. A large number of insecticides are registered for this crop, so growers have ample opportunity to select products according to their need and budget. A modest level of host plant resistance apparently exists in alfalfa, and although resistance is effective mostly against aphids, there is also some success with alfalfa weevil and leaf hoppers. A large number of beneficial arthropods have been moved around the world in an effort to attain biological suppression of invading alfalfa-feeding insects. In some cases this has met with success. For example, alfalfa blotch leafminer, Agromyza frontella (Diptera: Agromyzidae), was considered a serious pest when it first invaded the eastern USA, but following release of wasp parasitoids it fell to minor pest status. Similarly, the status of spotted alfalfa aphid, pea aphid and blue alfalfa aphid was affected by importation of beneficial insects. A native entomopathogenic fungus, Zoophthora phytonomi, has adapted to the invasive alfalfa weevil and sometimes provides good suppression. Pea aphid is affected by the fungus Erynia neoaphidis under favorable weather conditions. Generalist predators such as lacewings, lady bird beetles, nabids, soft-winged flower beetles, big-eyed bugs, and minute pirate bugs are often active in alfalfa, and provide good suppression of aphids, thrips, and also consume eggs and young larvae of caterpillars. Cultural manipulations are the most important tactics for management of alfalfa pests. In particular, early harvesting can provide acceptable or even nearly complete control of alfalfa weevil, alfalfa blotch leafminer, several caterpillars, aphids, and leaf hoppers because when the crop is cut the insects are exposed to lethal levels of heat and dryness, or the environment becomes so unsuitable that the insects move elsewhere. Crop rotation is most important for root feeding pests, many of which take several years to develop damaging

populations. Strip cropping is commonly recommended because the uncut areas retain populations of natural enemies, allowing the beneficial insect to move into newly harvested alfalfa as it regrows and becomes infested with pests. Farmers rarely embrace this approach, however, opting for operational efficiency over economic pest control.

References University of California (1981) Integrated pest management for alfalfa hay. Publication #3312, 98 pages Summers CG (1998) Integrated pest management in forage alfalfa. Integr Pest Manage Rev 3:127–154

Alfalfa Weevil, Hypera postica (Gyllenhal) (Coleoptera: Curculionidae) An important defoliator of alfalfa (lucerne).  Alfalfa (Lucerne) Pests and their Management

Alga (pl., Algae) An aquatic non vascular plant, often very small in size. Algae can reach pest status when weather and nutrient levels favor its growth, and pesticides may be needed to suppress it.

Alien An organism that is native elsewhere. These are also referred to as exotic or foreign.  Invasive Species

Alienicolae In heteroecious aphids, viviparous parthenogenetic females developing on herbaceous (secondary) host plants.  Aphids

Alimentary Canal and Digestion

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Alimentary Canal and Digestion james l. nation University of Florida, Gainesville, FL, USA Insects feed upon many different kinds of food, including paper, wood, plant phloem and xylem sap, plant leaves, roots and stems, animal tissues, hair, wool, and vertebrate blood. The alimentary canal (often simply called the gut in much of the literature) evolved to accommodate such diverse foods in a variety of morphological and physiological ways. Thus, there is no “typical” insect alimentary canal just as there is no typical insect. Nevertheless, there are similarities in the structure of the alimentary canal in all insects and nearly all must digest some of the same complex molecules, such as proteins, lipids, and carbohydrates. In every insect alimentary canal three regions can be identified morphologically and physiologically: the foregut or stomadeum, the midgut or mesenteron, and the hindgut or proctodeum (Fig. 33). One or more of these regions may be greatly reduced in size, or expanded in size, depending upon the feeding behavior of the insect. A cuticular layer, the intima, attached to the epithelial cells, lines the fore- and hindgut regions. The old intima is partially digested and the residue sloughed off into the gut and excreted at each molt, and a new intima is secreted. The midgut does not have an attached cuticular lining, but may have a non-attached peritrophic membrane that separates the food enclosed within from the delicate surface of the midgut cells. If a peritrophic membrane is present, it is often secreted several times each day.

The Foregut The buccal cavity (mouth), pharynx, esophagus, crop, proventriculus and attached salivary glands comprise the foregut. Secretions from the salivary glands attached near the mouth are swallowed

Alimentary Canal and Digestion, Figure 33 A generalized drawing of the alimentary canal in a cockroach to show the major divisions of the c anal. Many variations occur in the overall structure of the alimentary canal in insects, and this is not i ntended to suggest that the cockroach alimentary canal is typical of insects.

with the food, lubricate the food, and may begin some carbohydrate digestion. In some insects the crop is not a noticeably modified part of the foregut, but often the crop comes off the foregut as a diverticulum. In other insects it is an enlarged portion of the foregut. In opportunistic and possibly irregular feeders such as praying mantids, the crop composes more than half of the alimentary canal, apparently an evolutionary development to store a large amount of food when available and tide the mantid over periods when prey is scarce. Some insects (for example, many orthopterans) regurgitate enzymes from the midgut into the crop, and these enzymes, along with salivary secretions, digest food in the crop. The digested food components still enter the midgut to be absorbed, and there is no evidence that the crop ever secretes

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enzymes itself. The cuticular intima creates a barrier even against the absorption of water from the crop. The proventriculus controls the entry of food into the midgut in liquid feeders, but in many insects it is modified into a grinding apparatus with hard, sclerotized ridges and spines, and heavy musculature for breaking and tearing the food into smaller particles.

The Midgut The midgut in most, but not all, insects is the main site for digestion, absorption, and secretion of digestive enzymes. The epithelium is a single layer of cells, but several types of cells occur in some insects. The most common cells are tall, relatively narrow ones called columnar or primary cells by various authors. They have extensive microscopic microvilli on the apical or lumen surface (Fig. 34) and extensive invaginations of the basal cell membrane, features that greatly increase the surface area on both sides of the cell over which secretion and absorption occur. The columnar cells are the primary cells that secrete digestive enzymes and absorb digested products. In all insects that feed as adults and live for days or weeks, there are small regenerative cells distributed at the base of the columnar cells, or sometimes clustered together

in nidi (nests). The regenerative cells grow into mature epithelial cells to replace cells worn out or those that disintegrate to release digestive enzymes. Midgut cells may be completely replaced every few days in insects that live longer lives. Gastric caeca, small finger or sac-like diverticula from the midgut, often arise at or near the origin of the midgut, but may be located at various points along the midgut. The caeca appear to secrete digestive enzymes and may be important in absorption of digested products. The midgut does not have an attached cuticular lining on the surface of the cells, but midgut cells in the majority of insects secrete a thin membrane composed of chitin and protein, the peritrophic membrane, that surrounds the food and shields the delicate microvilli of the midgut cells from contact with potentially rough and abrasive food particles. Although the peritrophic membrane is thin, varying from 0.13 μm to about 0.4 μm thick, it also is thought to make it more difficult for viruses, fungi, bacteria, and protozoans to get to the surface of the midgut cells where they might be able to enter the cells and create an infection. Some insects produce several peritrophic membranes per day, each encasing the one before it, perhaps increasing protection from random breaks or punctures by larger food particles, and thus affording more protection for the midgut

Alimentary Canal and Digestion, Figure 34 A brush border of microvilli on the lumen surface of midgut cells in a mole cricket.


cells from possible fungi, parasites, viruses, and bacteria ingested with the food. A peritrophic membrane occurs in living representatives of some of the earliest insects to evolve, and it is believed to have evolved very early in a generalist scavenger feeder in which protection of midgut microvillar surfaces from food particles, sand, or other hard substances coincidentally ingested was likely to be important. A peritrophic membrane is present in many insects that do not feed upon rough or solid food, such as some blood feeders (but not all blood feeders), and in adult lepidopterans that take flower and plant nectars. Although the peritrophic membrane is not present in all groups of insects, like other gut features, it has been conserved over long evolutionary time, lending support to views that it has multiple functions, especially protection from disease invaders and may even have properties that could bind toxicants and limit their access to cells. Absorption of digested food substances has not been studied in most insects, but one mechanism has been partially elucidated for absorption of amino acids derived from protein digestion in larvae of Lepidoptera. Interspersed among the tall columnar cells lining the midgut in larvae of Lepidoptera (and some other groups of insects as well) are cells shaped much like a goblet and called, appropriately enough, goblet cells. The apical cell membrane of the goblet cavity has metabolic machinery that uses energy derived from splitting ATP to push or pump protons (H+) into the goblet cavity. A different set of machinery in the goblet cell membrane, an antiporter mechanism, reabsorbs the protons and simultaneously secretes potassium ions into the goblet cavity. The net result of the secretion of potassium ions is that a strongly alkaline midgut (a midgut pH as high as pH 8 to about 11) is produced, and a high voltage (up to 240 mV in some reports) is created between the gut lumen (positive) and the interior of cells lining the gut. The voltage created by the pump enables an absorptive mechanism in membranes of columnar cells to reabsorb K+ and amino acids from protein digestion. Thus, potassium ions are recycled between

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the epithelium cells and the gut lumen and seem to play a major role in amino acid absorption. The high midgut pH may provide plant feeding insects some protection against tannins that are common in the food plants of phytophagous insects. Tannins can complex with an insect’s own enzymes and proteins in the food, and may result in reduced digestion and absorption. Many details and the precise metabolic components in the cell membrane that support and enable these secretory and absorptive mechanisms remain to be elucidated, but what is already known emphasizes the complexity of insect digestive functions.

The Hindgut The hindgut is not only a posterior extension of the alimentary canal, but it also plays a major role in excretion through secretion of some substance into the lumen, and reabsorption of useful substances such as ions, water and some nutrients from the Malpighian tubule effluent. The Malpighian tubules typically arise at the origin of the hindgut (but exceptions do occur) and pass relatively large volumes of an ultrafiltrate of hemolymph components minus proteins into the beginning of the hindgut. The cuticular lining on hindgut cells is thinner and has larger pores than the lining in the foregut, permitting reabsorption of water, some ions, and useful metabolites that are returned to the hemolymph. In most terrestrial insects, water conservation is vital to life, and the hindgut must conserve the water that the Malpighian tubules flush into the hindgut. Waste products such as undigested food material (cellulose, for example, which most plant-feeding insects cannot digest and use), uric acid, and other allelochemicals picked up from the food are concentrated in the rectum and eventually excreted. The hindgut secretes some molecules into the lumen for excretion. Experimental evidence indicates that secretion and selective reabsorption helps regulate pH of the hemolymph in some insects. Specialized cells, the rectal papillae and

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rectal pad cells, in the rectum of many insects have characteristic ultrastructure and physiological mechanisms typical of highly reabsorptive cells. Water conservation by the rectum results in the relatively dry frass or fecal pellets characteristic of many terrestrial insects. The highest degree of specialization in the hindgut occurs in those insects that digest cellulose, such as termites. In termites, the hindgut is usually divided into several chambers harboring either bacteria or protozoa that secrete all or part of the cocktail of enzymes needed to digest cellulose. Glucose, liberated from cellulose digestion, may be fermented by the resident microorganisms, with the end products being short chain fatty acids (principally acetic acid) that can be absorbed by the termite and used as an energy source. Some termites release methane, a greenhouse gas, from the metabolic activities of their microorganisms, but whether this is a significant natural source of methane is a topic of debate by various scientists.

Digestive Enzyme Secretion Midgut cells secrete and release digestive enzymes in several ways. They may enclose digestive enzymes in small vesicles surrounded by a membrane and then release the enzymes into the alimentary canal by fusing the vesicle membrane with the cell membrane. In some insects, parts of the cell (some of the microvilli) or the entire midgut cell may disintegrate and release enzymes into the gut lumen. Of course, when the entire cell breaks down, the cell must be repaired or replaced. Replacement occurs through the growth of the regenerative cells. Extraoral digestion (digestion outside the insect body) occurs in some insects, including seed feeders and some predatory insects. By injecting enzymes from the salivary glands and midgut into the food source (animal or plant material) and then sucking back the liquef ied digestion products, insects can utilize very high percentages

of the nutrient value of the food source. Some insects reflux enzyme secretions and partially digested products by repeatedly sucking up and reinjecting the liquef ied juices into the food. Ref luxing mixes the secretions and fluids and extends the effective life of the digestive enzymes, and is particularly effective when the food contains a limiting boundary, such as the shell of a seed or the cuticle of an insect that acts as a container for the liquefying body contents.

Carbohydrate Digestion Starch and sucrose are the typical carbohydrates that insects digest from plant food, and glycogen and various sugars are present in animal tissue eaten by carnivorous insects. Cellulose, the major complex polysaccharide present in plant tissue, cannot be digested by most insects. Carbohydrate digestion begins with the action of α-amylase, an enzyme present in the salivary gland secretions of many insects. Amylase works best at slightly acid pH, and hydrolyzes interior glucosidic linkages of starch and glycogen, resulting in a mixture of shorter dextrins. In the midgut α -glucosidase and oligo-1, 6-glucosidase (isomaltase) digest smaller dextrins, releasing glucose. Many insects also have one or more α- or β-glycosidases that digest a broad range of small carbohydrates, such as maltose, sucrose, trehalose, melezitose, raffinose, stachyose, melibiose, raffinose, and stachyose. Some insects can secrete trehalase in the gut to digest trehalose, the principal blood sugar typically in high concentration in insects. β-glucosidase, β-galactosidase, and β-fructofuranosidase act upon various substrates to release simple sugars in the gut. An insect usually has only a few of these carbohydrate digesting enzymes, depending upon the food it eats. For example, Apis mellifera honeybees have several α -glucosidases or sucrases that act rapidly upon sucrose, usually the principal carbohydrate in the nectar taken by honeybees. They utilize the resulting glucose and fructose for an immediate energy source and for


making honey. Termites, some beetles, a few cockroaches, and woodwasps in the family Siricidae digest cellulose with aid (usually) from fungi, bacteria, or protozoa, which produce some or all of the complement of three enzymes necessary for cellulose digestion.

Lipid Digestion The major storage forms of lipids (fats) in both plants and insects are triacylglycerols, esters of fatty acids with glycerol. Midgut cells, and in some cases symbionts, secrete lipases, which are enzymes that hydrolyze triacylglycerols and release fatty acids and glycerol. Amino acids, proteins, and fatty acylamino complexes act as emulsifiers in the midgut of some insects facilitating the digestion of fats. The glycocalyx layer, a viscous protein and carbohydrate complex that often lies on the surface of the microvilli, probably aid in emulsifying fats and in promoting contact between lipases and triacylglycerols. Fatty acids released from triacylglycerols are resynthesized into the insect’s own triacylglycerols and stored in fat body cells. Immature insects typically store relatively large amounts of triacylglycerols, and use some of the released fatty acids during pupation and for egg development. Some insects, for example Orthoptera, Lepidoptera, and some aphids, mobilized fatty acids rapidly enough to use fatty acid metabolism to support flight, but other groups such as Diptera and Hymenoptera cannot release fatty acids from the fat body and transport them to the flight muscles rapidly, and so they only use carbohydrates for flight energy. They still can use lipids during pupation, and for other metabolic processes that occur more slowly.

Protein Digestion All animals must have a pool of amino acids available for synthesis into proteins, and for repair of tissues and organs. Most animals,

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including insects, get their amino acids from digestion of dietary proteins. Within insects as a group, there are several different types of protein digesting enzymes, some of which act at acid pH, others at slightly alkaline pH, and some at highly alkaline pH. Usually a particular species will have several different proteinases, but no insect is known to have both an acid-effective proteinase and an alkaline-effective proteinase. The pH of the alimentary canal is important to the action of any digestive enzyme, and no insect is known to have an alimentary canal that is strongly acid in one part and strongly alkaline in another part. Proteinases are classified broadly as serine, cysteine, aspartic acid, and metallo-proteinases depending upon the amino acid or metal at the active site of the enzyme. Trypsin and chymotrypsin are two endoproteinases with alkaline pH optima (about pH 8) that are common in many insects and which attack large proteins internally at the linkage between certain amino acid, thus breaking the protein into smaller polypeptides. Most insects appear to have several types of exopeptidases that remove the terminal amino acid from a protein or peptide chain. Thus, through the concerted action of both types of digestive enzymes, a protein can be completely digested with release of its component amino acids. Cysteine- and aspartic acid-proteinases have mildly acid pH optima, and are called cathepsins by some authors. All members of a taxonomic group may not have the same type of proteinases. Many beetles have cysteine proteinases most active at slightly acid pH, while some scarabeid beetles secrete serine-proteinases that act at the high midgut pH typical of these insects, and they have no detectable cysteine-proteinases. Lepidoptera typically secrete trypsin-like enzymes active at alkaline pH. One defense mechanism that has evolved against herbivory in many plants is the presence of proteinase inhibitors, some of which inhibit serine proteinases while others act upon cysteine proteinases. Experimentally, it has been shown that some insects secrete multiple trypsin enzymes

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(isozymes of trypsin) and others just secrete larger amounts of the same few isozymes after consuming a trypsin inhibitor. This counter action by the insect probably allows some protein digestion to escape ingested inhibitors, but transgenic plants designed to have proteinase inhibitors have been tested and proven to have adverse effects upon the growth of some insects.

Absorption of Digested Products Few details are known about the absorption of digested products by insects. In many vertebrates, glucose absorption from the alimentary canal requires an active mechanism involving ATP to supply the energy. In those insect that have been studied, glucose from digestion of carbohydrates is rapidly absorbed passively by a process known as facilitated diffusion, and involvement of ATP is not necessary. Fat body cells on the hemolymph side of the gut rapidly synthesize absorbed glucose into the disaccharide trehalose, keeping the hemolymph concentration of glucose low in most insects. Consequently, even low concentrations of glucose in the gut have a favorable diffusion pathway to the hemolymph and continue to be absorbed passively. In larvae of a few lepidopterans that have been carefully studied (Manduca sexta, Philosamia cynthia, Bombyx mori), amino acids are actively absorbed by transport proteins in the apical membranes of midgut columnar cells. Energy for absorption comes from the high K+ concentration in the gut lumen and high transepithelial potential created by the proton-ATPase pump active in midgut goblet cells. The transport proteins in these membranes show strong specificity for particular amino acids, and transport systems for at least six different amino acids are known, and transport systems for other amino acids probably will be discovered. In the Colorado potato beetle, Leptinotarsa decemlineata, transport proteins for leucine and tyrosine have been demonstrated in midgut tissue.

Gut pH The pH of the alimentary canal is highly variable in different species of insects. The pH of a gut segment influences the action of enzymes secreted into or carried with the food into the gut, influences solubility and toxicity of toxins and plant allelochemicals, and may alter the population of gut microorganisms. In most insects, the crop has little or no presence of buffering agents and tends to be slightly acidic, a factor favoring carbohydrate digesting enzymes. Larvae of Lepidoptera and Trichoptera tend to have a very high midgut pH, varying from about 8 to 10, promoted by goblet cells that secrete potassium and bicarbonate into the lumen of the midgut. They have protein digesting enzymes that are favored by the high pH, and the high pH may afford some protection from tannins and other allelochemicals that they ingest with their plant food.

Illustrative Examples of Diversity in Food, Form and Function of the Alimentary Canal The following examples are not intended to be a comprehensive review of foods, and alimentary canal structure and physiology, but will merely highlight interesting diversity. Opportunistic feeders may have evolved modifications to capture and store food when available, and thus survive lean periods when food is not available. For example, the foregut of the praying mantis, Tenodora sinensis, is long and wide, and occupies nearly the entire length of the body, apparently an adaptation for storage of prey when it can be captured. The midgut, eight gastric caeca, and hindgut are compressed into the last three abdominal segments. Probably much of the digestion occurs in the posterior part of the crop with enzymes passed forward from the small midgut. Considering the universal presence of cellulose in plant tissues, relatively few insects evolved the ability to use cellulose as a source of nutrients.


Termites, some beetles, a few hymenopterans, and a few cockroaches do use cellulose as a carbohydrate source. The hindgut of termites is highly specialized for housing gut microbiota that provide the cellulase enzymes needed to digest cellulose, although there is some evidence that certain termites may be able to produce some or all of the several enzymes necessary to completely digest cellulose. Gut variation exists among the castes in a colony; for example, soldiers in the family Rhinotermitidae are fed liquid food by the worker caste, and do not have to digest cellulose so they have reduced gut structure. The workers are responsible for colony construction and nutrition, and they have highly evolved hindgut chambers to hold various types of microbiota. Termites hatch without their gut microbiota, and lose most of their gut symbionts at each molt, but they become reinfested by feeding upon fluid and excreta from older nymphs. Termites in the family Termitidae have symbiotic bacteria in the hindgut, while termites in some other families have flagellate protozoans as well as bacteria in a multi-compartmented hindgut, and they get some or all of their cellulase(s) from their symbionts. Some termites, the Macrotermitinae, cultivate fungus gardens in their underground nests and get their cellulases from the conidiophores of the fungus. Symbionts in the hindgut of some termites can capture atmospheric nitrogen in an organic form, which is probably quite important to many termites because their diet of wood is relatively low in proteins. Some fungus-growing termites convert some of the protons (H+) and carbon dioxide from the initial fermentation of glucose into methane (CH4), and some investigators have suggested that termites are a significant environmental source of methane, a greenhouse gas. Larvae of the woodwasp (Hymenoptera, Symphyta, Siricidae, genus Sirex) acquire cellulase and xylanase from fungi ingested with the wood on which they feed. Larvae of cerambycid beetles and of some other beetles feed upon wood in down or dying trees; they generally have long life cycles because wood is so nutrient poor, especially

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protein poor. Fungi growing in the dead wood and ingested by the larvae may provide additional nutrients and/or enzymes for digesting the wood. Hemiptera take xylem or phloem sap, both of which are poor in amino acids and protein, but usually rich in sucrose (150 to more than 700 mM). They typically excrete a copious, dilute fluid, and in some, such as aphids, the fluid contains so much sugar that it is called honeydew. They have to ingest large volumes of fluid to get the amino acids, and then they have to get rid of the excess water and sucrose. A characteristic evolutionary feature of the gut in Hemiptera is the filter chamber in which a loop of the hindgut is in direct contact with part of the foregut and a great deal of the ingested fluid diffuses directly into the hindgut from the foregut without passing through the midgut. This, of course, causes loss of some amino acids and other components that may be needed, but water and sucrose, both of which are in excess of needs, are the major components lost. The filter chamber is able to concentrate gut fluid up to 10-fold in some xylem feeders (Cicadoidea and Cercopoidea), but only about 2.5-fold in members of the Cicadelloidea, which are phloem feeders. Xylem feeders probably need to concentrate xylem fluids more because of the lower amino acid content (3–10 mM amino acids per liter in xylem fluid) than do phloem feeders (15–65 mM amino acids per liter in phloem fluid). Pre-oral digestion with enzymes secreted into the prey occurs in many of the predacious beetles. Seed feeders also employ pre-oral digestion by injecting salivary secretions and possibly regurgitated midgut enzymes into the seed, allowing these to liquefy part of the seed, and then sucking the nutrients and enzymes back. Pre-oral digesters often reflux the liquefied contents by repeatedly imbibing and then reinjecting the mixture of enzymes and digested nutrients into the seed. Refluxing likely conserves enzymes longer, gives them more opportunity to function, and allows the insects to use more of their potential food. In honeybees and some other related hymenopterans, the midgut is closed off from the

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Alimentary System

hindgut by a plug of cellular tissue during larval development, and any food that cannot be digested and absorbed into the body must remain in the midgut. Just before pupation the connection between midgut and hindgut is opened, and accumulated undigested residue, such as the shells of pollen grains, is excreted into the cell. Adult honeybees clean the cell and the larva pupates inside the cell. Nectar taken by male and female mosquitoes is stored in a large, sac-like crop that is a diverticulum from the foregut, but blood meals taken by the females are passed directly into the midgut for the beginning of digestion. The midgut is differentiated functionally into an anterior and a posterior region. The anterior part secretes carbohydrate digesting enzymes, and nectar components are digested as fluid from the crop and is passed into the anterior midgut. This arrangement keeps possible trypsin inhibitors that may be present in nectar away from the site of protein digestion, which occurs in the posterior midgut. Simple sugars resulting from digestion, or those already in the nectar, are absorbed in the anterior midgut. The posterior midgut cells secrete trypsinlike enzymes and protein (blood) digestion and absorption occur in the posterior midgut. The posterior midgut cells, more so than anterior midgut cells, have extensive microvilli and basal infoldings characteristic of secretion and absorptive processes. The midgut cells in this region get stretched by the large volume of blood that a mosquito takes if it is allowed to feed to repletion. Consequently, the cells have several types of connecting structures (desmosomes) between cells to help hold them together and prevent excessive leaking of materials in or out between cells while they are stretched. Larvae of Lepidoptera have a very short foregut, a large, long, relatively straight midgut, and a short hindgut. There is no storage or digestion in the short, nearly vestigial foregut. Nearly all lepidopterous larvae are phytophagous feeders, and the gut modifications appear to be an adaptation to pass food quickly into the long

midgut so that digestion can begin. Feeding is nearly continuous when plenty of food is available, and larvae may ingest more than their body weight in food daily. Food moves rapidly through the relatively straight gut and frass droppings are frequent in phytophagous caterpillars. Because the larval and adult forms of Lepidoptera have very different life histories and food habits, the adult gut is quite different from that of the larva. Many adult Lepidoptera feed only upon nectar, which is stored in the crop and slowly released into the midgut for digestion to simple sugars. Some adult Lepidoptera have vestigial mouthparts and do not feed at all; they survive and (females) produce eggs at the expense of body substance, and they generally live only a few days. An unusual food utilized by Tineola bisselliella larvae (clothes moth) is wool, and larvae have a very strong reducing action in the midgut that breaks disulfide bonds between adjacent loops of the proteins, causing the wool proteins to lose their three-dimensional shape and unfold. This allows more access for protein digesting enzymes.

References Chapman RF (1998) The insects: structure and function. Cambridge University Press, Cambridge, UK, 770 pp Klowden MJ (2002) Physiological systems in insects. Academic Press, New York, NY, 415 pp Nation JL (2002) Insect physiology and biochemistry. CRC Press, Boca Raton, FL, 485 pp

Alimentary System The alimentary system (canal) is a system of tubular structures that takes in food at the mouth, stores the food, fosters digestion and absorption of nutrients, and allows excretion of waste materials from the rectum. It is conveniently divided into the foregut, midgut, and hindgut (Fig. 35).  Alimentary Canal and Digestion  Foregut

Allegheny Mound Ant, Formica exsectoides (Hymenoptera: Formicidae) foregut esophagus crop

gastric caecum

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hindgut

midgut ventriculus

pylorus

ileum

rectum

pharynx

buccal cavity

anus proventriculus

mouth

Malpighian tubule

Alimentary System , Figure 35 Generalized insect alimentary system (adapted from Chapman, The insects: structure and function).

 Midgut  Hindgut

likely have other effects as well, but they are still relatively unknown (contrast with allatostatins).  Juvenile Hormone

Alinotum The notal plate of the meso- or metathorax in a pterygote insect.  Thorax of Hexapods

Alleculidae A family of beetles (order Coleoptera). They commonly are known as comb-clawed beetles.  Beetles

Alitrunk The portion of the thorax to which the wings are attached.  Thorax of Hexapods

Allatostatins These are neuropeptides from neural and nonneural tissues that affect the corpora allata, inhibiting production of juvenile hormone. They likely have other effects as well, but they are still relatively unknown (contrast with allatotropins).  Juvenile Hormone

Allatotropins These are neuropeptides from neural and nonneural tissues that stimulate the corpora allata, resulting in synthesis of juvenile hormone. They

Allegheny Mound Ant, Formica exsectoides (Hymenoptera: Formicidae) gregory s. paulson Shippensburg University, Shippensburg, PA, USA The Allegheny mound ant, Formica exsectoides Forel, is a common mound-building ant of the northeastern and central United States. Workers are approximately 3/8 inch long (1 cm) with a reddish-tan head and thorax, and a dark brown abdomen. In suitable habitat, F. exsectoides will form dense populations, their presence easily discernible due to conspicuous mound-type nests which can be as large as 15 feet (4.6 m) in diameter and 4 feet (1.2 m) high. At one site near Altoona, Pennsylvania, researchers counted more than 30 large mounds per acre. Despite the conspicuous nature of F. exsectoides nests and its wide

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Allegheny Mound Ant, Formica exsectoides (Hymenoptera: Formicidae)

geographic range, relatively few papers concerning this species have been published since H.C. McCook’s first paper in 1877. Nests tend to be clustered in the habitat (Fig. 36). Nests in each cluster often will share foraging trails and resources. Although there is little aggression between workers from different nests or nest clusters, the workers still show fidelity to a home nest. Nests of F. exsectoides have multiple queens (polygynous) although there is tremendous variation in the number of queens per mound. Over 1,400 queens were reported in one mound, but that is probably an anomaly. Most mounds probably contain fewer than 20 queens. Due to the large number of queens, the reproductive output of a nest can be prodigious resulting in large numbers of workers in a colony. More than 250,000 workers have been found in some nests. Reproductive forms (alates) are present in the nests from mid-summer until early fall. Activity of the ants is related to ambient conditions but, in general, workers are active from late March until November. Formica exsectoides are generalist predators, scavengers and collect honeydew from symbiotic hemipterans.

Habitat has a significant effect on physical characteristics of F. exsectoides nests. Forest nests tend to be significantly larger in height, width, length, nest footprint and volume than nests in meadows. In general, the nests are round, but it is not uncommon to find elongated nests that are orientated to the sun. The shape of a nest and its orientation may help the ants to maintain a relatively constant internal temperature and relative humidity.

References Andrews EA (1925) Growth of ant mounds. Psyche 32:75–87 Andrews EA (1927) Ant mounds as to temperature and sunshine. J Morphol Physiol 44:1–20 Bristow CM, Cappaert D, Campbell NJ, Heise A (1992) Nest structure and colony cycle of the Allegheny mound ant, Formica exsectoides. Forel (Hymenoptera: Formicidae) Insectes Sociaux 39:385–402 Bristow CM, Yanity E (1999) Seasonal response of workers of the Allegheny mound ant, Formica exsectoides. (Hymenoptera: Formicidae) to artificial honeydews of varying nutritional content. Great Lakes Entomol 32:15–27

Allegheny Mound Ant, Formica Exsectoides (Hymenoptera: Formicidae), Figure 36 Three large nest mounds of Formica exsectoides in a Pennsylvania forest clearing.

Allelochemicals

McCook HC (1877) Mound-making ants of the Alleghenies, their architecture and habits. Trans Entomol Soc Am 6:253–296 Rowe HC, Bristow CM (1999) Sex ratio and sexual dimorphism in Formica exsectoides, the Allegheny mound ant (Hymenoptera: Formicidae). Great Lakes Entomol 32:207–218

Allele One of two or more alternative forms of a gene at a particular locus. If more than two alleles exist, the locus is said to exhibit multiple allelism.

Allelochemic A non-nutritional chemical produced by one species (often a plant) that affects the growth, health, or behavior of another species (often an herbivore).  Allelochemicals

Allelochemicals murray s. blum University of Georgia, Athens, GA, USA For thousands of years insects and plants have been locked in a battle for which survival is the ultimate prize. For insects, plants constitute food sources for growth and development, and in some cases, sites for reproduction. On the other hand, plants attempt to counter insects feeding on their tissues (herbivory) so that their own vigorous growth and development will occur and lead to reproductive success. The consequences of this warfare are great and for humankind the outcomes of these battles may be of major economic significance in terms of the production of various foods. The welfare of various human populations can be threatened if hordes of ravenous insects consume specific crops that are the mainstays of these populations. But plants do not take this “lying down.” Over thousands

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of years, plants have done everything possible to make life miserable for insects. On the other hand, insects have returned the favor many times over. In recent geological time, plants and insects have changed their “spots” (plant-feeding strategies), resulting in an incredible point-counterpoint relationship of these organisms that is characterized by some remarkable developments. As far as nutrients are concerned, different kinds of plants (species) are fairly similar and can provide an insect herbivore with the basic nutrients required for growth and development. These compounds (chemicals) are called primary compounds because they are required for the insect’s growth, development, and reproduction. All insects require these compounds and in theory they should be readily available from a wide variety of plant species. But most species of insects, rather than feeding on many different kinds of plants, limit their plant menu to a relatively small number of plant species (monophagy), most of which are related. Significantly, the limited preferences that insects have for their food plant species are due to non-nutritive compounds that usually vary from one plant group to another. These compounds are not related to the primary compounds identified with growth and development, and it is apparent that these plant-derived compounds (allelochemicals) generally have functions related to other species of organisms. These compounds are obviously not primary compounds but rather secondary compounds (non-nutritive) whose manufacture has been described as secondary metabolism. Indeed, these allelochemicals appear to be responsible for both the associations and non-associations that insects have with specific groups of plant species. In essence, it would be no exaggeration to state that the host-plant preferences of insects really reflect the ability of an insect species to either tolerate, or be repelled by, an allelochemical. Allelochemicals are not mysterious compounds but rather are a very important part of the everyday world, especially in terms of human food preferences. In a sense, the strong food preferences exhibited by insects are not so different from those

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of humans, with one striking exception. Many insect species are “locked in” to specific food plants, and these insects will reject a foreign plant species and die in the absence of their normal food plant. On the other hand, there is little evidence that human beings will subject themselves to starvation if their favorite foods are not readily available.

A World of Allelochemicals Fruits and vegetables possess characteristic odors and tastes that create desire (preference) for these foods. Significantly, these tastes and smells are not identified with the primary compounds responsible for plant growth and development, such as sugars, fats, and proteins. Therefore, the plant has invested in producing a variety of chemicals that will not help it grow or reproduce. While an onion may possess a distinctive odor and taste for both insects and humans (not necessarily the same odor and taste for both), this fact hardly justifies the onion spending its energy and resources to produce an onion fragrance. On the other hand, if the taste and odor of onions combine to make this vegetable distasteful and repellent to most plant-feeding insects, then these allelochemicals perform a very vital function. In essence, it is generally believed that these secondary compounds are responsible for protecting plants from herbivores and possibly pathogens as well. A brief examination of some well-characterized allelochemicals offers a means of examining these compounds as agents of defense both as toxins and as repellents. Oleander, which has a very limited number of herbivores, is extremely toxic because of the presence of allelochemicals that are somewhat related to cholesterol. The odor of the plant probably constitutes an early-warning system that makes potential herbivores aware of the danger of feeding on this plant. The same can be said for the tobacco plant which, like oleander, does not have too many insect herbivores. Leaves of the tobacco plant are quite toxic, but in some South American populations young children become addicted to the

icotine in the leaves before they are ten years old. n Nitrogen-containing compounds (alkaloids) produced by opium poppies are powerful repellents for a wide range of insect species, and there is no doubt that compounds such as morphine and heroin, which are powerful human narcotics, were evolved to deter herbivores rather than to function as narcotics for humans. Alkaloids such as nicotine have been adapted to function as insecticides, and a variety of plant products such as derris, rotenone, ryania, and sabadilla are also used as insecticides in different cultures. In some cases, allelochemicals such as prunasin in cherry leaves cause poisoning in livestock. Not to be outdone, humans have frequently utilized the alkaloid strychnine to murder people. However, it would be a mistake to lose track of the fact that, human abuses notwithstanding, these allelochemicals were evolved as plant protectants long before humans appeared. Obviously, allelochemicals do not provide plants with absolute protection against herbivores. Indeed, probably all plants containing allelochemicals are fed upon by insects, and in many cases these herbivores are only found on a limited number of host plant species. For example, monarch butterf ly caterpillars are limited to the milkweed species. Bark beetles limit their attacks to pines and related conifers, developing in environments that are rich in toxic turpentines. These insects have breached the chemical defenses of their hosts, and in so doing, they have “captured” specific kinds of food plants that are either repellent or highly toxic to most other species of insects. Guaranteed these “forbidden fruits,” these herbivores should have to share their food resources with very limited numbers of competitors. Barring an ecological disaster does not devastate the populations of their host plant species, this specialization should have much to recommend it. On the other hand, many insect species choose a lifestyle which is characterized by feeding on a variety of unrelated plant species. Insects like the monarch butterfly and bark beetles that are restricted to a limited number of related plant species are referred to as specialists.

Allelochemicals

These herbivores have become resistant to the toxic effects of their host plant allelochemicals, and in many cases they appear to be completely immune to the plant toxins they ingest. In the case of monarch caterpillars feeding on milkweeds, it has been demonstrated that these larvae actually grow more rapidly on milkweed plants containing the highest concentration of toxins. Indeed, allelochemical concentrations may be generally quite high, often averaging 5–10% of the dry weight of the plant. By contrast, plantfeeding generalists feed on a wide range of plant species, often unrelated. However, in general, these herbivores select plant species in which the concentrations of allelochemicals are not too high, enabling them to process low levels of a wide variety of plant toxins. The immunity of specialists to the toxic effects of the allelochemicals in their diets demonstrates that for these insects these compounds can no longer be considered poisons. Surprisingly, the basis for this important allelochemical resistance, which has great economic significance, was only understood about thirty years ago.

Sequestration and its Consequences Insects such as the monarch butterfly store compounds in their tissues that render them unpalatable to predators. These compounds, the cardenolides, were ingested by the larvae from their milkweed food plants, and retained in their bodies into the adult stage. The storage of these milkweed compounds is called sequestration, and constitutes a widespread phenomenon among specialists feeding on allelochemical-rich plants. In a sense, sequestration represents the insect’s success in utilizing the plant’s chemical defenses for its own purposes. Indeed, sequestration can be regarded as a form of detoxication since potentially toxic compounds are removed from the circulation and stored in the tissues. Sequestration has been detected in at least seven orders of insects including species of toxic

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grasshoppers, aphids, lacewings, beetles, wasps, butterflies and moths. In general, these insects are brightly (= warningly) colored, a characteristic described as aposematic. Armed with the toxins from their food plants, large insects such as brilliantly colored grasshoppers move very slowly, as if to advertise their poisonous qualities to the world. Obviously the term toxic is relative, since these insects routinely sequester these allelochemicals during normal feeding. However, since these specialists are physiologically adapted for ingesting these compounds, their ability to tolerate these allelochemicals is really not surprising. On the other hand, non-adapted species (e.g., predators) would certainly encounter toxic reactions if they ingested these toxic plant products. The fates of allelochemicals, which are usually present in mixtures, are not at all predictable after ingestion by an adapted herbivore. Although many compounds are sequestered immediately after ingestion, others may be metabolized before being stored, or even eliminated after being metabolized. In other cases selected allelochemicals in a mixture may be absorbed and sequestered whereas other compounds in the mixture may be eliminated immediately. An examination of the options for initially processing ingested allelochemicals emphasizes the versatility of specialists in treating the toxic compounds produced by their food plants.

Sequestration of Insect Toxins by Vertebrates: A Significant “Allelochemical” Phenomenon It has become evident that the allelochemical relationship of insects and plants is paralleled by a similar relationship of amphibians and insects. It is now recognized that the sequestration of ingested toxic insect compounds by vertebrates differs little from this phenomenon in insect herbivores and plants. In essence, a variety of insect toxins is sequestered by amphibians and these compounds have similar protective functions for frogs and

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insects (see Allelochemicals as phagostimulants). Frogs exploit insect allomones (defensive compounds) as if they were animal “allelochemicals,” and it seems worthwhile to emphasize this congruency in examining the scope of allelochemistry. Frogs in the genus Dendrobates contain mono-, di-, and tricyclic alkaloids which are clearly of ant origin. The alkaloids, termed pumiliotoxins, appear to be products of ant species in the genera Brachymyrmex and Paretrechina and constitute the only known dietary source of alkaloids of these frogs, not unlike the specialist insects feeding on narrow plant diets enriched with allelochemicals. The same phenomenon has been described for the myrmicine ant Myrmicaria melanogaster which synthesizes ten alkaloids. Some of these alkaloids have previously been identified in a dendrobatid frog and a toad. Neurotoxic steroidal alkaloids, the batrachotoxins, have been isolated from New Guinea birds in the genera Pitohui and Ifrita. These compounds are among the most toxic natural substances known, and they are not produced by captive birds, suggesting a dietary source. Recently, the batrachotoxins were identified in beetles in the genus Chloresine (Melyridae) which are normally fed on by the bird species. Since the genus Chloresine is cosmopolitan, it is the possible source of some of the avian alkaloids found in birds in different areas. Vertebrate sequestration of alkaloids from insects has only recently been explored. Clearly this chemical storage has a common denominator with sequestration of alkaloids by insects (see Allelochemicals as pheromonal precursors) and should be examined as a paradigm of comparative physiology. Clearly, insects are pivotal to both systems, either as food for vertebrates or food for insects, with sequestration the major common feature.

Initial Processing of Allelochemicals by Specialists Once an adapted insect has ingested an allelochemical, a menu of options is available for

rocessing it. An insect species may utilize a varip ety of adaptive strategies for processing a single compound that is characteristic of the host plant defense.

Immediate Allelochemical Excretion Some insects essentially fail to absorb ingested allelochemicals from the gut. These compounds are excreted directly and are concentrated in the feces. A lymantriid moth larva that is a specialist on the coca plant, which is the source of the alkaloid cocaine, rapidly excretes this compound with only traces being found in the blood. However, cocaine may still have defensive value for the larva as part of an oral regurgitate that is externalized when the larva is disturbed. Three different species of moth larvae that feed on tobacco plants rapidly excrete nicotine, a very toxic and reactive alkaloid. There is no evidence that nicotine is absorbed from the gut of any tobacco feeder, but as is the case for the moth larva excreting cocaine, nicotine in oral or anal exudates constitutes an excellent defensive compound.

Allelochemical Metabolism Many insect specialists rapidly metabolize ingested allelochemicals which are then sequestered, or in some cases excreted. Nicotine, which is both highly reactive and very toxic, is converted to a non-toxic metabolite called cotinine by both tobacco-feeding insects and those that are not tobacco feeders. Since cotinine has virtually no toxicity to insects, it is probable that its production from nicotine constitutes true detoxication. Cabbage-feeding insects feed on plants that are rich in sinigrin, a compound that yields a highly toxic mustard oil when metabolized.

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Although sinigrin can be sequestered without generating the reactive mustard oil in a variety of cabbage-feeding species, cabbage butterflies (whites) actually break down sinigrin and sequester the highly reactive mustard oil. For these butterflies, the mustard oil is more suitable for storage than sinigrin. Larvae of the tiger moth Seirarctia have evolved a novel strategy for coping with the toxic effects of MAM, a compound derived from cycasin which is a constituent in the cycad leaves upon which they feed. When larvae encounter MAM, they convert it to cycasin which is absorbed through the gut wall before being sequestered. Since the enzyme that produces cycasin or MAM is only found in the gut, once cycasin crosses the gut wall into the blood prior to sequestration there is no chance of MAM being generated from cycasin. Many species of moths, butterflies, and grasshoppers feed on plant species that produce extremely toxic compounds known as pyrrolizidine alkaloids. These alkaloids, present as mixtures, are frequently sequestered by these specialist insects and, in some cases, metabolized plant compounds are the preferred storage forms. For example, larvae of the tiger moth (Tyria species) feed on ragwort and primarily sequester the alkaloid seneciphylline, although this compound is present in the plant as the N-oxide. Conversely, the grasshoppers of the Zonocerus species convert the ingested alkaloid monocrotaline to its N-oxide before sequestering the compound. Insects feeding on milkweed metabolize the toxic cardenolides (steroids) produced by these plants, converting them into compounds that can be readily sequestered. The milkweed bug (Oncopeltus species) oxidizes cardenolides as a mechanism for converting these steroids into compounds that can be efficiently sequestered. Similarly, larvae of the monarch butterfly store metabolized cardenolides in tissues after oxidizing these compounds into suitable chemical forms for sequestration.

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Selective Biomagnification of Allelochemicals in Tissues There is little indication that the profiles of insectstored allelochemicals in any way mirror those of their host plant. In a sense, each insect species treats ingested allelochemicals distinctively, so that a compound totally excreted by one species may constitute the main sequestration product of another. The very toxic grasshopper Poekilocerus bufonius sequesters only two of the cardenolides that it ingests from its milkweed food plant. Similar selectivity is shown by moth larvae (Syntomeida species) which sequester oleandrin, the main steroid found in the leaves of oleander. On the other hand, a variety of other insects feeding on oleander leaves do not sequester oleandrin. Similar unpredictability characterizes the sequestration of pyrrolizidine alkaloids by moth larvae. Tiger moths (Amphicallia species) sequester the alkaloids crispatine and trichodesmine, whereas the main alkaloid present is crosemperine. Another tiger moth (Tyria species) concentrates senecionine in its tissues in spite of the fact that this compound is a trace constituent in the leaves. Tyria is no less curious as a sequestrator because it stores jacobine, jacozine, and jacoline as minor constituents in adults, yet these three compounds are major alkaloids in the leaves.

The Diverse Functions of “Captured” Allelochemicals While highly concentrated allelochemicals may constitute a major deterrent to non-adapted insects, these compounds can represent a real treasure trove for species for which these plant products are non-toxic. Indeed, in the course of exploiting for their own protection compounds that are repellent or toxic to most insect species, specialists have gone beyond the point of simply being resistant to allelochemicals. In many cases, a variety of specialist species have utilized the rich

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allelochemical pool that is available in order to develop a menu of remarkable functions.

Insect Sequestration of Bacterial Compounds and their Glandular Secretion Prokaryotes (bacterial types) are almost everywhere and their widespread association with insects is certainly well established. But the bases for these diverse bacteria-insect relationships are, for the most part, terra incognita. However, very recent research suggests one very surprising function for bacteria in insect glands. All major types of metabolism evolved in prokaryotes and the success of these organisms was both cause and effect of changing environments on earth. If these bacteria are sequestered in insect secretory glands, their great metabolic abilities could be utilized to biosynthesize bacterial allelochemicals which could be used as potent defensive compounds. This possibility appears to have been realized as a product of the virtual ubiquity of both insects and their biosynthetically versatile prokaryotes. Predaceous diving beetles (Dytiscus species) are distinguished by their ability to produce defensive steroids, some of which are novel animal products that are limited to species of diving beetles. Furthermore, insects do not synthesize cholesterol which in insects must be obtained from exogenous sterols. However, it now appears that the surprising steroidal versatility of dytiscids may reflect the biosynthetic elegance of bacteria rather than insects. Adult diving beetles may contain concentrations of at least 10 bacterial species, mostly detected in a variety of organs. Culturing individual bacterial species resulted in the identification of diverse steroids that had previously been characterized in the prothoracic defensive glands of the adults. The steroid-rich secretions of these glands function as vertebrate deterrents that can cause emesis of fish that swallow these beetles. If the dytiscid-bacterial

association is typical of a variety of insect species and their bacterial symbiotes, then a multitude of insect-bacterial relationships may require reevaluation of possible examples of insect sequestration of bacterial allelochemists. Non-pathogenic bacteria are commonly housed in insects and, in a sense, these prokaryotes are sequestered by their insect hosts. Furthermore, if the bacteria synthesize toxic compounds which may be externalized from a defensive gland (prothoracic glands of dytiscids), then the bacterial products may be regarded as bacterial allelochemicals that have been sequestered. Indeed, bacterial compounds of symbiotic bacteria of insects clearly constitute an unrecognized group of allelochemicals.

Additives in Defensive Glands Milkweed bugs (Oncopeltus species) add cardenolides, derived from their milkweed host plants, to their thoracic defensive gland secretion which considerably enhances the deterrency of their secretion. Similarly, a warningly colored generalist, the lubber grasshopper (Romalea guttata) incorporates a large number of allelochemicals derived from a variety of plant species into its thoracic gland secretion. This grasshopper generally feeds on plants with low concentrations of allelochemicals, but if it is fed high concentrations of plants with known repellents (e.g., onion), the odorous secretion can be highly deterrent. Another toxic grasshopper, Poekilocerus bufonius, utilizes allelochemicals as the mainstay of its defensive secretion. This aposematic (very warningly colored) insect sequesters two of six cardenolides from its milkweed diet which are the major irritants in the secretion when it is sprayed at adversaries. Utilization of allelochemicals as defensive gland constituents is particularly pronounced in the swallowtail larvae of Atrophaneura alcinous, which feed on leaves that are rich in toxic aristolochic acids. Seven aristolochic acids are sequestered by the larvae and all are transferred to the defensive gland in the head. The acids are

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concentrated in the gland and are the major deterrents for birds.

Regurgitation and Defecation of Allelochemicals The intestines of stimulated grasshoppers can discharge ingested plant products which may serve as repellents for predators. Regurgitated allelochemicals can effectively repel ants, as is the case for anal discharges from the hind gut. When tactually stimulated, the milkweed bug, Oncopeltus fasciatus, also defecates a solution containing repellent allelochemicals. In this case, they are cardenolides ingested from their milkweed food plant.

Allelochemicals as Tissue Colorants The cuticular (skin) coloration of many insects is diet-dependent and is highly adaptive since it enables the insect to respond in a positive way to its background color. Diet-induced changes may result in the insect being cryptic (background matching), whereas aposematic species can be background contrasting. Background quality, which is of great survival value, appears to be controlled by allelochemicals that are widespread in the diets of moths, butterflies and true bugs. These insects are particularly sensitive to the carotenoids (e.g., tomato red) that fortify their host plants. If the large white butterfly, Pieris brassicae, is reared on its normal diet of cabbage leaves, the pupae are green and contrast with their background. This toxic insect contains high concentrations of carotenoids, and the carotenoid lutein is concentrated in the cuticle. On the other hand, if these insects are reared on an artificial diet lacking carotenoids, they possess a turquoise-blue coloration and exhibit no response to background. In the absence of carotenoids, these insects are quite conspicuous on their background and could be readily detected by predators.

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Allelochemicals as Inhibitors of Toxin Production Some plant toxins are present in plants in an inactive form only to be converted to toxic compounds after ingestion by herbivores. This is particularly true for many cyanogens (cyanidecontaining toxins) that generate cyanide when the leaf surface is broken as would occur with a plant feeder. It now appears that cyanogenesis (producing cyanide) in damaged leaves may be inhibited by allelochemicals that are compartmentally isolated from the cyanogens in the intact leaves. Leaves of papaya, Carica papaya, contain two cyanogens that yield hydrogen cyanide after enzymatic attack. However, tannins, which are widely distributed in plants, inhibit the release of cyanide caused by the action of enzymes that attack the cyanogens. Insects attacking plants containing cyanogens may have adapted tannins to prevent cyanide release, a strategy that may be suitable for other plant groups that yield toxic products after leaf damage.

Allelochemicals as Pheromonal Precursors Bark beetles (Scolytidae) in the genera Dendroctonus and Ips convert the hydrocarbons produced by their pine hosts into alcohols that are utilized as either aggregation or sex pheromones (communication compounds) by the attacking beetles. Similarly, butterflies in the family Nymphalidae and moths in the family Arctiidae convert pyrrolizidine alkaloids (PAs) into sex pheromones that are especially critical during courtship. The PAs may be collected from damaged plants by males to be transformed into sexual pheromones that constitute the key to reproductive success. For these males, the allelochemicals (PAs) are identified with reproductive fitness.

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Allelochemicals as Structural Paint Some insects actually “paint” structures with ingested compounds possessing considerable biological activity. Larvae of the parsnip webworm, Depressaria pastinacella, apply ingested allelochemicals to silk-webbed flowers that serve as housing units. The applied compounds are derived from wild parsnip, a food plant that is rich in highly toxic furanocoumarins. These compounds are sequestered in the silk glands before being applied to the flowers in which the larvae reside. Since the larvae are quite sensitive to ultraviolet light, the presence of UV-absorbing furanocoumarins on their silken housing is highly adaptive. In addition, because these allelochemicals possess pronounced antimicrobial activity against bacteria and fungi, their presence on the silk can act as a major barrier to pathogens.

Allelochemicals as Metabolites in Primary Metabolic Pathways Some specialist herbivores metabolize the characteristic allelochemicals in their host plants into compounds that are of major significance in growth and development. In essence, these specialists exploit their food plants by utilizing not only their primary nutrients for growth and development, but their allelochemicals as well. Larvae of the bruchid beetle, Carydes brasiliensis, develop exclusively on seeds of a legume (pea family) that contains canavanine, a foreign amino acid related to arginine. Canavanine is highly toxic when incorporated into proteins by non-adapted herbivores. On the other hand, larvae of C. brasiliensis metabolize canavanine into products of great metabolic significance. Large amounts of ammonia are generated for fixation into organic compounds, and an amino acid is produced from canavanine for ready metabolism. Thus, the very toxic allelochemical of the legume has been thoroughly exploited by the beetle larvae as a source for key nutrients.

Beetle larvae in the genus Chrysomela also convert a toxic allelochemical into a metabolite with considerable importance in growth and development. These larvae feed on leaves of willow (Salix), a rich source of salicin, a toxic metabolite. Metabolism of salicin yields a very effective defensive compound that is sequestered by the larvae in defensive glands. In addition, this metabolism generates enough glucose to account for about one-third of the daily caloric requirements of the larvae. Salicin should be regarded as an allelochemical nutrient.

Allelochemicals as Agents of Sexual Development Tiger moths in the genus Creatonotus feed on plant species that produce high concentrations of pyrrolizidine alkaloids (PAs). These compounds are converted to sex pheromones by the males. Additionally, these allelochemicals control the development of important secondary sexual characters called coremata. The coremata are eversible andraconial (male) organs that are the source of the volatile sex pheromones of the males, and their degree of development is controlled by the amount of PAs ingested by the developing larvae. In effect, PAs are functioning as male hormones that regulate both sex pheromone production and development of the coremata.

Allelochemical Discharge from Nonglandular Reservoirs Some insects sequester ingested allelochemicals in non-glandular reservoirs that can be evacuated upon demand. Gregarious larvae of the European pine sawfly, Neodiprion sertifer, sequester toxic turpentine terpenes in foregut pouches. These pinederived compounds can be discharged upon demand to function as highly effective predator deterrents. Similarly, lygaeids such as the milkweed bug, Oncopeltus fasciatus, sequester cardenolides

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from their milkweed hosts in dorsolateral spaces on the thorax and abdomen. Significantly, high concentrations of cardenolides are stored in these spaces, resulting in a concentrated deterrent discharge which repels potential predators.

Allelochemicals as Defensive Agents of Eggs Insects ingesting allelochemicals often utilize these compounds as protectants for the next generation of insects. These plant compounds may be sequestered in the eggs in order to provide a formidable defense against predators and pathogens. The insect embryo must be resistant to the toxic effects of the allelochemicals that have been sequestered in the reproductive system. For example, chrysomelid beetle adults feeding on willow and poplar sequester the toxic allelochemical salicin which is used to fortify the eggs. Salicin has different functions in the embryo and the larvae. For the embryo, salicin is a deterrent toxin which can kill ants. For the young larvae, salicin is converted to salicylaldehyde, a powerful repellent that is not frequently encountered in insects. A wide variety of allelochemicals are sequestered in insect eggs which includes pyrrolizidine alkaloids, aristolochic acids, cannabinoids, quinones, cardenolides and mustard oils. It is evident that the females of a large number of species have appropriated their host-plant defenses (allelochemicals) for protection of their eggs.

Allelochemicals as a Copulatory Bonus Females may obtain allelochemicals suitable for their own protection and that of their eggs from the seminal ejaculate. For example, males of ithomiine butterflies gather pyrrolizidine alkaloids (PAs) from flowers and decomposing foliage and about half of the PAs are channeled to the spermatophore (sperm packet) that is transferred to the female during copulation. Since the females are rarely found feeding on

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alkaloid sources, the copulatory bonus ensures that these toxic allelochemicals will be available to protect both the female and her eggs. It is also very significant that the resistance of the spermatozoa to the known toxic effects of the pyrrolizine alkaloids enables the copulatory bonus strategy to be highly adaptive.

Allelochemicals as Synergists for Pheromones The intimate relationship of specialist insects and their food plants is exemplified by the turnip aphid, Lipaphis erysimi, and its alarm pheromone. This aphid is typical of many aphid species. Paired glands near the tip of the abdomen secrete an alarm pheromone that causes both adults and larvae to disperse and drop off of the food plant. The alarm pheromones synthesized by the aphids are key communications chemicals that enable these insects to “abandon ship” when threatened by a predator. Surprisingly, (E)-B-farnesene, the major alarm agent for a large variety of aphid species, is only weakly active when secreted by the turnip aphid. However, the activity of this pheromonal secretion is increased appreciably by allelochemicals that act as powerful synergists for the major alarm pheromone. These synergists are derived from typical food plant compounds that have been modified by the aphids.

Allelochemicals as Phagostimulants The close relationship of insect specialists and their allelochemicals is further demonstrated by some species of sawflies and chrysomelid beetles which feed on very bitter food plants. Adults of the turnip sawfly, Athalia rosae, feed on the surface of a plant that is not a larval food plant. Compounds in the leaf surface that are responsible for their bitter taste are powerful phagostimulants for A. rosae. In addition, these bitter compounds are incorporated into the cuticle, thus providing these sawflies with a cuticular set of “armor” to protect against aggressive predators.

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Similarly, species in three genera of chrysomelid beetles utilize cucurbitacins, compounds found in their squash and pumpkin hosts, as phagostimulants that are biomagnified in their bodies. The beetles are rendered distasteful and, as is the case for the sawflies, the allelochemicals possess dual roles that both induce ingestion and promote sequestration of highly distasteful compounds.

eridania, from a host of allelochemicals. Unrelated plant compounds rapidly induce enzymatic in creases of 2 to 3-fold in larvae. Significantly, the rise in P-450 activity is immediate and proceeds rapidly over much of its course during the first few hours. These results strongly suggest that P-450 induction is critical to allelochemical tolerance.

Allelochemicals as Inducers of Detoxifying Enzymes

In some cases, insects have produced powerful repellents from allelochemicals in their food plants and have thus exploited the plant’s defensive chemistry in a very efficient way. Such a strategy is particularly adaptive because the insect has benefited both nutritionally and defensively from feeding on its host. Host plant exploitation is particularly pronounced in some chrysomelid beetle larvae in the genera Chrysomela and Phratora. The larvae feed on willow and poplar leaves, both of which contain salicin, a well known feeding deterrent for non-adapted species. The beetle larvae convert salicin to salicylaldehyde and glucose, utilizing the former for defense and the latter for growth. For these chrysomelid larvae, the conversion of salicin to salicylaldehyde is doubly beneficial. Very little energy is used to synthesize salicylaldehyde, compared to what is required to produce other defensive compounds that must be totally synthesized. Because salicylaldehyde is a far more effective repellent than salicin, the beetle larvae receive a very important double bonus by converting the allelochemical into a compound that can be readily stored and secreted from the defensive glands.

Both generalist and specialist insects can encounter a diversity of allelochemicals with varying degrees of toxicity. For generalists this is particularly true since a generalist diet can sample a wide variety of plant species containing a large diversity of allelochemicals. On the other hand, specialists may encounter fewer allelochemicals but it is likely that these compounds will be at high concentrations. In the case of both feeding modes, it is obviously necessary to possess mechanisms for blunting the toxic properties of the ingested allelochemicals. Detoxication would appear to constitute the key process for neutralizing the toxicities of ingested allelochemicals. The enzymes chiefly identified with converting allelochemicals into less toxic compounds are the mixed-function oxidases, particularly cytochrome P-450. Mixed-function oxidases metabolize fat-soluble toxins into water-soluble ones that can be excreted. The level of these enzymes may determine the tolerance of an insect for a particular allelochemical. For a generalist ingesting a large diversity of allelochemicals derived from many plant species, the induction of a variety of these oxidases would promote the possibility of detoxifying many kinds of plant compounds. For a specialist, fewer oxidases at very high levels would enable the herbivore to detoxify the very high concentrations of allelochemicals in its restricted food plants. Mixed-function oxidases play a key role in protecting the southern armyworm, Spodoptera

Allelochemicals as Allomonal Precursors

Allelochemicals as Communicative “Jamming” Agents In theory, plant species could reduce or eliminate herbivory if the plants generated volatile compounds identical to or similar to the pheromones utilized by herbivores as signals. If these signals

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were behaviorally disruptive, feeding could be appreciably diminished, to say the least. The wild potato, Solanum berthaultii, has effectively “jammed” the pheromonal alarm signal of its potential aphid herbivore. (E)-B-farnesene, an alarm pheromone of the aphid Myzus persicae, is also produced by wild potatoes, resulting in repellency and dispersion of the aphids. In effect, the potato has exploited the aphid’s herbivory by utilizing a highly disruptive compound that has been evolved by aphids as a warning signal.

Quenchers of Phototoxic Allelochemicals Diverse plant species produce photo-activated compounds that are highly toxic to insects after digestion. In essence, these compounds generate highly toxic species of oxygen that attack key biochemicals such as nucleic acids. On the other hand, if the herbivore simultaneously ingests allelochemicals that are effective quenchers of toxic oxygen species along with the phototoxins, then survival and prosperity are possible. The availability of these allelochemical antioxidants has enabled some insect species to utilize food plants that are “forbidden fruits” for most herbivores. Larvae of the tobacco hornworm feed on a variety of plant species that contain the phototoxin α-terthienyl, a constituent of many species of asters (Asteraceae). However, the additional ingestion of β-carotene reduces mortality from 55% (controls) to 3% (+carotene) during 48 h. β-carotene, an effective quencher of toxic oxygen species, is concentrated in the tissues of the larvae where it can serve as a potent antioxidant for photoactivated toxins found in its food plant.

Antibiotic Functions of Allelochemicals The demonstrated range of allelochemicals against insect-associated viruses, fungi and bacteria makes it probable that these arthropods have

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commonly exploited plant compounds as key elements in their phytochemical defenses. A compound commonly produced by conifers is a-pinene, which inhibits diverse microorganisms including the insect pathogen Bacillus thuringiensis. Along with several related compounds, α-pinene reduces the infectivity of B. thuringiensis for larvae of the Douglas fir tussock moth, Orgyia pseudotsugata. At concentrations approximating those found in fir needles, a-pinene increases the 50% lethal dose for B. thuringiensis by 700-fold. A pathogenic fungus, Nomuraea rileyi, frequently attacks lepidopterous (moth) larvae such as the corn earworm, Helicoverpa zea. However, the pathogenicity to this larva can be reduced if the moth ingests a tomato alkaloid, α-tomatine. If the larvae ingest α-tomatine prior to exposure to fungal conidia, it increases larval survivorship considerably. The alkaloid is a further asset to H. zea because it is quite toxic to larval parasites of the corn earworm. The pathogenicity of viral pathogens of H. zea can also be compromised by host plant allelochemicals. Chlorogenic acid, a common plant compound, is oxidized to chlorogenoquinone by plant enzymes, and this oxidation product binds to a nuclear polyhedrosis virus. Binding to this baculovirus results in a reduction in digestibility and a decrease in infectivity. Furthermore, it appears that the liberation of infective virons in the midgut, which is a requirement for successful infection, is impaired by the binding of chlorogenoquinone to the baculovirus.

Specialists and Generalists: Two Selected Case Studies Although specialists and generalists may be highly efficient sequestrators, the storage characteristics of both groups differ considerably. Some insights into how these insects manipulate the allelochemicals in their diets have been provided by recent studies of the fates of a variety of ingested plant chemicals. An analysis of these studies demonstrates that the particulars of sequestration are, if nothing else, very unpredictable.

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The Monarch Butterfly, Danaus plexippus The monarch is a specialist that feeds exclusively on different species of milkweeds. Milkweeds contain steroids called cardenolides, which are somewhat related to vertebrate hormones such as testosterone. These compounds are toxic and highly emetic, vomiting often following their ingestion by non-adapted species. Polar (water soluble) cardenolides are sequestered in the large volume of gut fluid possessed by the larvae. Sequestration is much more efficient from plants with low level cardenolide concentrations than with high concentrations. Significantly for the monarch, and not necessarily for other milkweed feeders, it is the large volume of gut fluid that makes it possible to feed and develop on these plants. The cardenolide-rich gut fluid, which may exceed one-third of the larva’s total liquid volume, is withdrawn at pupation to become part of the hemolymph (blood) pool, stored primarily under the wings. Subsequently, the wing scales (bird predators beware), along with the hemolymph, become the richest sources of cardenolides in the body after being withdrawn from the gut fluid. The volume of gut fluid decreases before pupation only to increase again before pupal molting. Again, gut fluid diminishes during pupal development only to increase again in the new adult. The cardenoliderich gut fluid is again converted to hemolymph during adult development so that very little remains to be lost when the newly developed adult evacuates accumulated waste products from its gut. The polar cardenolides in the gut fluid clearly are the source of the defensive compounds manipulated by the monarch at all stages. The larval and pupal exuviate (cast skins) eliminated after molting are an excretory form for the cardenolides, as is the case for these compounds in the wing scales. Excretion notwithstanding, the ability of all life stages to manipulate the cardenolide pool is quite pronounced. This is evident in 2-day-old pupae that contain low concentrations of cardenolides

in the gut fluid but high concentrations in the hemolymph. However, before wing expansion in the newly developed adult, the cardenolide level in the hemolymph is at its lowest, only to increase to the highest level in any life stage. The presence of high levels of cardenolides in the blood of the adult demonstrates that these compounds are not locked in tissues but rather are circulating freely, possibly to be utilized upon demand. The warningly colored (aposematic) adult monarch utilizes a defensive system based on compounds that it did not ingest as an adult. Although the complexities of cardenolide sequestration in this species are evident, it is highly significant to understand these ingested steroids are an extraordinarily dynamic state.

The Lubber Grasshopper, Romalea microptera (also known as R. guttata) This large grasshopper found in the southeastern United States is quite conspicuous because of it red, black and yellow coloration. It is one of the most aposematic (warningly colored) species in its habitat. This brightly colored grasshopper is especially distinctive because it is a generalist that feeds on a very wide range of plants belonging to a variety of species. Lubber grasshopper is known to feed on 104 plant species belonging to 38 families, many of which produce toxic allelochemicals. Both immature and mature grasshoppers are capable of causing emesis in predators such as lizards,demonstrating that all stages of these insects are protected from at least some predatory vertebrates. Immature individuals of R. microptera produce defensive compounds that cause emesis in both lizard and bird predators. Additionally, mature and adult grasshoppers secrete defensive compounds from paired tracheal (respiratory) glands in the metathorax. These glands only become active near the adult period and their secretion can be extremely repellent to small predatory insects such as ants. At least 50 compounds are produced by the defensive glands, the secretions varying intraspecifically, so

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that components of females of the same age and population sometimes differ by 70-fold, with some compounds being absent in certain individuals. However, in addition to the compounds synthesized in the metathoracic glands, a number of allelochemicals are sequestered in these glands as a reflection of an individual grasshopper’s diet. Indeed, the composition of the metathoracic gland secretion of each grasshopper appears to be unlike that of any other grasshopper, since no two of these generalist grasshoppers have identical diets from which to sequester allelochemicals. For a predator, each lubber secretion may be sufficiently distinctive to make it impossible to learn an olfactory pattern that clearly identifies the prey as lubber grasshopper. Lubber grasshopper is unusual in being a polyphagous (eating many plant species) insect species that sequesters allelochemicals. In general, monophagous (feeding on one group of plant species) and stenophagous (feeding on a limited range of plant species) insect herbivores characteristically sequester plant compounds, but not generalist feeders. Furthermore, if R. microptera is presented with a restricted diet (specialist feeding mode), the number of compounds in the secretions and their concentrations are reduced, and the relative composition of the secretion is markedly different from that of field-collected grasshoppers. Significantly, if grasshoppers are presented with only a single-host plant as a food source, they frequently feed readily, sequestering host-plant volatiles, and exhibit no immediate ill effects. Lubbers feeding only on wild onion sequester a large number of onion volatiles which impart a strong onion odor to the secretion. The secretion is a powerful repellent to hungry ants and is considerably more active than the secretions of field- collected grasshoppers. Compounds in other single-plant diets (e.g., catnip) produce secretions that are similarly active. The secretion of lubber grasshopper clearly has both a dietary and an individual origin that correlates with great variations in secretory components. The possibility that these grasshoppers can temporarily switch to a monophagous feeding

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mode in the presence of a preferred host plant is not unreasonable, and can result in a secretion with a high a concentration of sequestered allelochemicals as is characteristic of some specialist insects. Lubber grasshopper is quite unpalatable and emetic to a variety of vertebrates, especially birds. Diverse bird species have been demonstrated to vomit after ingestion of these grasshoppers, presumably as a consequence of Romalea-synthesized toxins that fortify their bodies. While Romalea would appear to be completely defended against birds, as is often the case, the best defense has been overcome by a better offense. Shrikes, predatory birds that impale their insect prey on spines or even barbed wire, capture lubber grasshoppers and impale them. However, the birds wait for about 48 h before they remove and eat the grasshoppers. Though shrikes “store” all their food in this manner, in all likelihood the emetic toxin(s) produced by Romalea decomposes during the time the grasshopper is impaled.

References Blum MS (1981) Chemical defenses of arthropods. Academic Press, New York, NY Blum MS (1983) Detoxication, deactivation, and utilization of plant compounds by insects. In: Hedin P (ed), Plant resistance to insects. American Chemical Society, Washington, DC, pp 265–275 Bowers MD (1990) Recycling plant natural products for insect defense. In: Evans DL, Schmidt JO (eds), Insect defenses. Adaptive mechanisms and strategies of prey and predators. State University of New York, Albany, NY, pp 353–386 Evans DL, Schmidt JO (eds) Insect defenses. Adaptive mechanisms and strategies of prey and predators. State University of New York, Albany, NY, 482 pp Gibson RW, Pickett JA (1983) Wild potato repels aphids by release of aphid alarm pheromone. Nature 302:608–609 Pasteels JM, Gregoire JC, Rowell-Rahier M (1983) The chemical ecology of defense in arthropods. Annu Rev Entomol 28:263–289 Whitman DW (1988) Allelochemical interactions among plants, herbivores, and their predators. In: Barbosa P, Letourneau D (eds), Novel aspects of insect-plant interactions. Wiley, New York, NY, pp 11–64

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Allelopathy

Allelopathy The ability of a plant species to produce substances that are toxic to certain other plants. Allelopathic chemicals may affect germination, growth or reproduction of plants.

Allen’s Rule Among mammals and birds, individuals of a species occurring in colder climates tend to have shorter appendages, and a correspondingly lower surface to volume ratio, than members of the same species living in warmer climates. This trend results from the need to conserve heat in cold climates but to eliminate excess heat in hot climates. A variant of this is Bergmann’s rule. These rules do not apply to ectothermic animals such as insects.  Bergmann’s Rule  Thermoregulation

Allochronic Speciation A mechanism of speciation wherein new species develop in the same place but are separated due to their tendency to occur at different times.  Speciation Processes Among Insects

Allomone A chemical that is released by one species that influences the behavior or physiology of a different species. The organism releasing the substance usually benefits. Allomones are a type of semiochemical used in warning.  Chemical Ecology

Allopatric Having separate and mutually exclusive areas of distribution (contrast with sympatric).

Allopatric Speciation A mechanism of speciation resulting from geographic separation of populations, particularly physical barriers such as mountains and oceans.  Speciation Processes Among Insects

Allophagic Speciation A mechanism of speciation wherein new species develop in the same place, but are separated by their preference for different food.  Speciation Processes Among Insects

Allogenic Succession A temporal succession of species that is driven by processes from outside the community (contrast with autogenic succession).

Allometric Growth A growth pattern in which different parts of an organism grow at defined rates. In some cases, the body parts remain proportional (isometric growth), in other cases they do not. Departure from isometric growth is used to explain castes of social insects, which may have disproportionately large heads, mandibles, etc.

Allozyme Allozymes are a subset of isozymes. Allozymes are variants of enzymes representing different allelic alternatives of the same locus.

Almond Seed Wasp, Eurytoma amygdali Enderlein (Hymenoptera: Eurytomidae) nikos a. kouloussis Aristotle University of Thessaloniki, Thessaloniki, Greece

Almond Seed Wasp, Eurytoma Amygdali Enderlein (Hymenoptera: Eurytomidae)

The almond seed wasp is a serious pest of almonds, Prunus amygdalus Batch, in several countries of southeastern Europe and the Middle East, and also in Armenia, Azerbaijan, and Georgia. The adult female is 6–8 mm long and has a black head with dark brown eyes. The thorax and the spindleshaped abdomen are shiny black. The tibiae and tarsi are light brown while the remaining parts of the leg are black. The male is usually smaller than the female (4–6 mm long). The larva is whitish, legless, tapering in both ends, curved and clearly segmented. Its head is light brown and very small. Its length when fully grown is about 6 mm. Almond seed wasp is a univoltine species, with a small part of the population completing its life cycle in two or more years because of prolonged diapause. The diapause terminates during the winter. Pupation takes place inside the fruit in late winter to early spring. Adults emerge after boring a circular exit hole through the hard pericarp with their mandibles. Shortly after adult emergence, virgin females release a volatile sex pheromone to attract males for mating. Within a few days they mate and the females start ovipositing (Fig. 37) into unripe, green almonds. Using her long ovipositor, the female drills through the pericarp of unripe, green almonds and the integument of the seed, and deposits a stalked egg within

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the translucent nucellar tissue. After oviposition, the female deposits onto the fruit surface a host-marking pheromone. This pheromone enables females to discriminate between the infested and uninfested fruit, and to select the latter for oviposition. Thus, a uniform distribution of eggs among available fruits is achieved, and an optimal use of the available fruit for larval development. The newly hatched larva bores through the nucellus and the embryo sac to feed on the developing seed embryo. The larva attains full size in midsummer, and enters diapause within the seed integument of the destroyed almond, which usually remains on the tree in a mummified condition. Owing to oviposition by the wasp certain varieties suffer a heavy premature drop. In most varieties though, the main damage consists in the consumption of the seed by the larvae. This damage varies depending on the variety. Certain soft-shelled varieties may lose up to 90% of their crop. Others are nearly immune because by the time females emerge in spring their pericarp has become too thick and endocarp too hard for the ovipositor to penetrate. Though not a common practice, planting of resistant varieties might be an effective strategy against this pest. The pest can be controlled by collection and destruction of mummified fruits before adult

Almond Seed Wasp, Eurytoma Amygdali Enderlein (Hymenoptera: Eurytomidae), Figure 37 Female Eurytoma amygdali ovipositing into an almond.

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emergence in spring, which is an effective measure if applied in large areas by multiple growers. However, the method most commonly used is the application of systemic insecticides against the neonate larvae within the oviposited almonds. This strategy is meant for varieties that do not suffer fruit drop because of oviposition. Recent studies have indicated that a single spraying can be effective if applied when 10–50% of the eggs have hatched. This percentage can be determined by dissecting sampled almonds under a binocular microscope. Estimates of egg hatch can be obtained by knowing the time the first adults emerge from infested almonds in spring. This can be determined by following the exit of adult wasps from infested almonds kept in cages in the orchard, or by following the population of males with the use of sex pheromone traps containing live virgin females as lures.

References Katsoyannos BI, Kouloussis NA, Bassiliou A (1992) Monitoring populations of the almond seed wasp, Eurytoma amygdali, with sex pheromone traps and other means, and optimal time of chemical control. Entomologia Experimentalis et Applicata 62:9–16 Kouloussis NA, Katsoyannos BI (1991) Host discrimination and evidence for a host marking pheromone in Eurytoma amygdali. Entomologia Experimentalis et Applicata 58:165–174 Plaut HN (1971) On the biology of the adult of the almond seed wasp, Eurytoma amygdali End. (Hym., Eurytomidae) in Israel. Bull Entomol Res 61:275–281 Plaut HN (1972) On the biology of the immature stages of the almond wasp, Eurytoma amygdali End. (Hym., Eurytomidae) in Israel. Bull Entomol Res 61:681–687 Tzanakakis ME, Papadopoulos NT, Katsoyannos BI, Drakos GN, Manolakis E. Premature fruit drop caused by Eurytoma amygdali (Hymenoptera: Eurytomidae) on three almond varieties. J Econ Entomol 90:1635–1640

Alpha Taxonomy The identification of organisms, and particularly the description and naming of organisms (species) new to science.

 Beta Taxonomy  Gamma Taxonomy

Alternate Host One of the hosts of a pathogen or insect where a portion of the life cycle occurs. Often this term is used to refer to a weed host of a crop pest or disease.

Alternation of Generations Some insects undergo reproduction that involves alternation of sexual and asexual generations. Typically, females produce both males and females but at some point females cease producing males and produce only females parthenogenetically. Later generations then commence production of males again, allowing sexual reproduction to occur before the parthenogenetic cycle begins again. This occurs most often in Hymenoptera and Hemiptera.  Aphids (Hemiptera: Aphididae)  Gall Wasps (Hymenoptera: Cynipidae)

Altruism Self destructive behavior that is performed for the benefit of others; sacrifice.

Alucitidae A family of moths (order Lepidoptera). They commonly are known as many-plumed moths.  Many-Plumed Moths  Butterflies and Moths

Alula The expanded membrane at the base of the trailing edge of the front wing.  Wings Of Insects

Amber Insects: DNA Preserved?

Amazonian Primitive Ghost Moths (Lepidoptera: Neotheoridae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Amazonian primitive ghost moths, family Neotheoridae, are defined on the basis of a single species from the Amazonian area of southern Brazil, although two additional species have been discovered for the family recently. The family is part of the superfamily Hepialoidea, in the infraorder Exoporia. Adults medium size (38 mm wingspan), with head roughened; haustellum short and vestigial mandibles present; labial palpi long, porrect and 3-segmented; maxillary palpi very small and 2-segmented. Wing maculation is dark and unicolorous. Biologies and larvae remain unknown.

References Kristensen NP (1978) A new familia of Hepialoidea from South America, with remarks on the phylogeny of the subordo Exoporia (Lepidoptera). Entomologia Germanica 4:272–294 Kristensen NP (1999) The homoneurons Glossata. In: Kristensen NP (ed), Lepidoptera, moths and butterflies, vol 1: evolution, systematics, and biogeography. Handbuch der Zoologie. Band IV. Arthropoda: Insecta. Teilband 35:51–63. W. de Gruyten, Berlin

Amber Insects: DNA Preserved? marjorie a. hoy University of Florida, Gainesville, FL, USA Amber is a polymerized form of tree resin that was produced by trees as a protection against disease agents and insect pests. The resin hardened and, sometimes, captured insects, seeds, feathers, microorganisms, plants, spiders, and even small

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vertebrates that got stuck in the sticky exudate. The hardened resin was preserved in the earth for millions of years, especially in regions where it was deposited in dense, wet sediments such as clay or sand that formed in the bottom of an ancient lagoon or river delta. For thousands of years, people have collected amber. Many people use amber as a gem, but scientists find amber a magnificent way to identify ancient organisms. Amber can be found in a variety of sites around the world. The composition, color, clarity, and other properties of amber vary according to age, conditions of burial and type of tree that produced the resin. The oldest amber is from the Carboniferous (360–285 million years ago, mya) and can be found in the United Kingdom and in Montana in the USA. Permian amber is 185–145 million years old and found most often in Russia. Triassic amber (245–215 mya) can be found in Austria, and Jurassic amber (215–145 mya) is found in Denmark. Cretaceous amber (65–140 mya) is found in many locations around the world and represents the time when dinosaurs reigned and flowering plants evolved along with a variety of insects. For example, the rich amber deposits in central New Jersey in the USA are from the Turonion period of the Upper Cretaceous, about 92 mya. Other Cretaceous-period amber is found in North Russia and Japan. Baltic amber is found in the Baltic sea where amber has been collected and made into decorative objects for at least 13,000 years. In the Dominican Republic, amber deposits 23–30 million years old are found in rock layers. Dominican amber is particularly rich in insect inclusions. This amber was formed from the resin of an extinct tree in the legume family. Tertiary amber deposits are found in several locations around the world and are from 1.6 to 65 million years old. Tertiary deposits in the USA are found in Arkansas. Some websites with photographs showing amber inclusions can be viewed at: – Amber Inclusions at: http://www-user.uni-bremen. de/~18m/amber.html;

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– Amber on-line at: www.ambericawest.com/amberpics. html; – American Museum of Natural History at: www.amnh. org/exhibitions/amber/; or – The Amber Room at: http://home.earthlink.net/-skurth/ AMBER.HTM.

Insect DNA in Amber? The ability to amplify dinosaur DNA from insects preserved in amber in the film Jurassic Park captured the imagination of the public. Subsequently, the PCR was used to amplify DNA fragments from insects preserved in ancient amber, but these results have been controversial, as have been the results from amplifying dinosaur DNA. Why the controversy? Is amber a special form of preservative that allows DNA to persist for unusually long periods of time (millions of years)? Amber entombs insect specimens completely, after which they completely dehydrate so the tissue is effectively mummified. Terpenoids, which are major constituents of amber, could inhibit microbial decay. Certainly, preservation of amberembedded insects seems to be exceptional and insect tissues in amber appear comparable in quality to the tissues of the frozen wooly mammoth (which is “only” 50,000 years old). But is the DNA in these tissues preserved? DNA has been extracted from a variety of insects in amber, including a fossil termite Mastotermes electrodominicus estimated to be 25–30 million years old, a 120- to 130-million year old conifer-feeding weevil (Coleoptera: Nemonychidae) and a 25- to 40-million year old bee. These are extraordinary ages for DNA! The DNA sequences obtained from all amberpreserved insects meet several, but not all, criteria of authenticity; the fossil DNA sequences “make phylogenetic sense” and DNA has been isolated from a number of specimens in several cases (although the weevil example was derived from a single specimen). However, the extraction and amplification of fossil DNA sequences from

amber-preserved insects has yet to be reproduced in independent laboratories, despite multiple attempts to do so, which has cast doubt on the authenticity of the reports. One of the most controversial claims involved the isolation of a “living” bacterium from the abdomen of amber-entombed bee. Bacterial DNA from a 25-million-year-old bee was obtained and sequenced and a bacterial spore was reported to be revived, cultured, and identified. The classification of the bacterium is controversial because the bacterium could have come from a currently undescribed species of the Bacillus sphaericus complex. The modern B. sphaericus complex is incompletely known, so the “new” sequence obtained could be that of a modern, but previously unidentified, bacterium because this group of bacteria often is isolated from the soil. Other claims of amplifying ancient DNA have been disproved. For example, the mitochondrial cytochrome b sequence of an 80-million-year-old dinosaur from the Upper Cretaceous in Utah was later discovered to be, most probably, of human origin. Likewise, a 20-million-year-old magnolia leaf produced sequences that were similar to those of modern magnolias. The authenticity of the magnolia sequences were cast into doubt because they were exposed to water and oxygen during preservation and DNA is especially vulnerable to degradation under such conditions. The most common ancient DNA analyzed is usually mitochondrial DNA because it is so abundant; however, this abundance makes it easy to contaminate the ancient sample with modern mtDNA. The amplification of ancient DNA remains highly controversial because the technical difficulties are great. DNA is a chemically unstable molecule that decays spontaneously, mainly through hydrolysis and oxidation. Hydrolysis causes deamination of the nucleotide bases and cleavage of base-sugar bonds, creating baseless sites. Deamination of cytosine to uracil and depurination (loss of purines adenine and guanine) are two types of hydrolytic damage. Baseless sites weaken

Ambrosia Beetles

the DNA, causing breaks that fragment the DNA into smaller and smaller pieces. Oxidation leads to chemical modification of bases and destruction of the ring structure of base and sugar residues. As a result, it is almost always impossible to obtain long amplification products from ancient DNA. PCR products from ancient DNA often are “scrambled.” This is due to the phenomenon called “jumping PCR,” which occurs when the DNA polymerase reaches a template position which carries either a lesion or a strand break that stops the polymerase. The partially extended primer can anneal to another template fragment in the next cycle and be extended up to another damaged site. Thus, in vitro recombination can take place until the whole stretch encompassed by the two primers is synthesized and the amplification enters the exponential part of the PCR. This phenomenon makes it essential that cloning and sequencing of multiple clones be carried out to eliminate this form of error in interpretation. Most archeological and paleontological specimens contain DNA from exogenous sources such as bacteria and fungi, as well as contaminating DNA from contemporary humans. Aspects of burial conditions seem to be important in DNA preservation, especially low temperature during burial. The oldest DNA sequences reported, and confirmed in other laboratories, come from the remains of a wooly mammoth found in the Siberian permafrost; these sequences are “only” 50,000 years old rather than millions of years old. Theoretical calculations and empirical observations suggest DNA should only be able to survive, in a highly fragmented and chemically modified form, for 50,000–100,000 years. Because only tiny amounts of DNA usually can be extracted from an archeological specimen, stringent precautions and multiple controls are required to avoid accidental contamination with modern DNA. A methodology to deal with ancient specimens has been proposed that includes careful

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selection of well-preserved specimens, choice of tissue samples that are likely to have best DNA preservation, and surface sterilization to eliminate surface contamination. The operations should be carried out in a laboratory dedicated to work on ancient specimens and work on ancient DNA should be separated from that on modern DNA. Most importantly, multiple negative controls should be performed during DNA extraction and PCR set up, although a lack of positives in the negative controls is not definitive proof of authentic ancient DNA. Another crucial step is the authentication of the results. Putatively ancient DNA sequences should be obtained from different extractions of the same sample and from different tissue samples from different specimens. The ultimate test of authenticity should be independent replication in two separate laboratories. So far, this type of replication has not been achieved for DNA from amber-preserved arthropod specimens.

References Austin JJ, Ross AJ, Smith AB, Fortey RA, Thomas RH (1997) Problems of reproducibility— does geologically ancient DNA survive in amber-preserved insects? Proc R Entomol Soc London B 264:467–474 Hofreiter M, Serre D, Poinar HN, Kuch M, Paabo S (2001) Ancient DNA. Nat Rev Genet 2:353–359 Poinar G Jr, Poinar R (2001) The amber forest: a reconstruction of a vanished world. Princeton University Press, Princeton, NJ Poinar HN, Stankiewicz BA (1999) Protein preservation and DNA retrieval from ancient tissues. Proc Natl Acad Sci USA 96:8426–8431 Yousten AA, Rippere KE (1997) DNA similarity analysis of a putative ancient bacterial isolate obtained from amber. FEMS Microbiol Lett 152:345–347

Ambrosia Beetles Some members of the subfamily Scolytinae (order Coleoptera, family Curculionidae).  Beetles

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Ambush Bugs

Ambush Bugs Members of the family Reduviidae (order Hemiptera).  Bugs

Ameletopsidae A family of mayflies (order Ephemeroptera).  Mayflies

Amelitidae A family of mayflies (order Ephemeroptera).  Mayflies

Amerasinghe, Felix P Felix Amerasinghe was a noted Sri Lankan medical entomologist. He was known for his work on the taxonomy and ecology of disease-transmitting arthropods. Amerasinghe graduated from the University of Peradeniya, Sri Lanka, and received his Ph.D. from the University of Bristol, United Kingdom, in 1977. He made important long-term studies in the effects of irrigation on mosquito populations and malaria transmission, and became an authority on Japanese encephalitis. The development of keys for the identification of South Asian mosquitoes was one of his important contributions, greatly enhancing disease surveillance programs. Amerasinghe worked principally at the University of Peradeniya, but also at the University of Sri Lanka, and in later years joined the International Water Management Institute as research leader, initiating studies on the socioeconomic impact of malaria, malaria parasitology, and molecular biology. He died in Colombo, Sri Lanka, on June 7, 2005.

Reference Konradsen F, de Silva A, van der Hoek W (2005) Felix P. Amerasinghe. American Entomologist 51:191

American Butterfly Moths (Lepidoptera: Hedylidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA American butterfly moths, family Hedylidae, total only 40 known species, all Neotropical. The family is in the superfamily Geometroidea, in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults medium size (35–65 mm wingspan), with head scaling normal; haustellum naked; labial palpi upcurved; maxillary palpi 1 to 2-segmented; antennae filiform. Wings triangular, with forewings somewhat elongated and often with apex emarginated (Fig. 38); hindwings usually more rounded. Body usually narrow. Maculation somber hues of brown and gray, often with apical dark patch and some speckling, plus pale or hyaline patches (rarely mostly pale or hyaline). Adults nocturnal. Larvae are leaf feeders. Host plants are recorded in Euphorbiaceae, Malvaceae, Sterculiaceae, and Tiliaceae.

American Butterfly Moths (Lepidoptera: Hedylidae), Figure 38 Example of American butterfly moths (Hedylidae), Macrosoma lucivittata (Walker), from Ecuador.

American Grasshopper, Schistocerca Americana (Drury) (Orthoptera: Acrididae)

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References Aiello A (1992) Nocturnal butterflies in Panama, Hedylidea (Lepidoptera: Rhopalocere). Quintero D, Aiello A (eds), Insects of Panama and Mesoamerica. Oxford University Press, Oxford, pp 549–553 Scoble MJ (1986) The structures and affinitxies of the Hedyloidea: a new concept of the butterflies. Bull Br Mus Nat Hist Entomol 53:251–286 Scoble MJ (1990) An identification guide to the Hedylidae (Lepidoptera: Hedyloidea). Entomologica Scandinavica 21:121–158 Scoble MJ (1998) Hedylidae. In Lepidopterorum Catalogus, (n.s.). Fasc. 93. Association for Tropical Lepidoptera, Gainesville, FL, 9 pp Scoble MJ, Aiello A (1990) Moth-like butterflies (Hedylidae: Lepidoptera): a summary, with comments on the egg. J Nat Hist 24:159–164

American Dog Tick  Ticks

American False Tiger Moths (Lepidoptera: Dioptidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FLa, USA American false tiger moths, family Dioptidae, total 507 species, primarily Neotropical (505 sp.); actual fauna likely exceeds 800 species. Two subfamilies are known: Dioptinae and Doinae. Some specialists place the family within the Notodontidae. The family is in the superfamily Noctuoidea, in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults medium size (22–58 mm wingspan) (Fig. 39). Maculation mostly very colorful, with various patterns of large spotting, and some lustrous. Larvae and pupae often also colorful Adults are mostly nocturnal, but some are diurnal or crepuscular. Larvae are leaf feeders, particularly toxic plants in families like Aristolochiaceae, Euphorbiaceae, Passifloraceae, and Violaceae, but also on various others like Fagaceae. Very few are economic.

American False Tiger Moths (Lepidoptera: Dioptidae), Figure 39 Example of American false tiger moths (Dioptidae), Josia gigantea Druce, from Mexico.

References Bryk F (1930) Dioptidae. Lepidopterorum catalogus, 42:1–65. W. Junk, Berlin, Germany Miller JS (1987) A revision of the genus Phryganidia Packard, with description of a new species (Lepidoptera: Dioptidae). Proc Entomol Soc Wash 89:303–321 Prout LB (1918) A provisional arrangement of the Dioptidae. Novitates Zoologicae 25:395–429 Seitz A (ed) (1925–1927) Familie: Dioptidae. In: Die GrossSchmetterlinge der Erde. 6. Die amerikanischen Spinner und Schwärmer, pl. 67–71. A. Kernen, Stuttgart, Germany, pp 499–534 Todd EL (1981) The noctuoid moths of the Antilles – Part I (Lepidoptera: Dioptidae). Proc Entomol Soc Wash 83:324–325

American Grasshopper, Schistocerca americana (Drury) (Orthoptera: Acrididae) john l. capinera University of Florida, Gainesville, FL, USA This grasshopper is found widely in eastern North America, from southern Canada (where it is an occasional invader) south through Mexico to northern South America. In the midwestern states, where it is common, the resident population receives a regular infusion of dispersants from southern locations. In the southeast it is quite common, and one of the few species to reach epidemic densities. It is native to North America.

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Life History In warm climates, American grasshopper has two generations per year and overwinters in the adult stage. In Florida, eggs produced by overwintered adults begin to hatch in April-May, producing spring generation adults by May-June. This spring generation produces eggs that hatch in AugustSeptember. The adults from this autumn generation survive the winter. The eggs of S. americana initially are light orange in color, turning tan with maturity. They are elongate-spherical in shape, widest near the middle, and measure about 7.5 mm in length and 2.0 mm in width. The eggs are clustered together in a whorled arrangement, and number 75–100 eggs per pod, averaging 85 eggs. The eggs are inserted into the soil to a depth of about 4 cm and the upper portion of the oviposition hole is filled by the female with a frothy plug. Duration of the egg stage is about 14 days. The nymphs, upon hatching, dig through the froth to attain the soil surface. Normally there are six instars in this grasshopper though sometimes only five. The young grasshoppers are light green in color. They are extremely gregarious during the early instars. At low densities the nymphs remain green throughout their development, but normally gain increasing amounts of black, yellow, and orange coloration commencing with the third instar. Instars can be distinguished by their antennal, pronotal, and wing development. The first and second instars display little wing development but have 13 and 17 antennal segments, respectively. In the third instar, the number of antennal segments increases to 20–22, the wings begin to display weak evidence of veins, and the dorsal length of the ventral lobe of the pronotum is about 1.5 times the length of the ventral surface. Instar four is quite similar to instar three, with 22–25 antennal segments, though the ratio of the length of the dorsal to ventral surfaces of the pronotal lateral lobe is 2:1. In instar five there are 24–25 antennal segments, and the wing tips assume a dorsal rather

than ventral orientation but the wing tip does not exceed the first abdominal segment. In the sixth instar (Fig. 41) there are 24–26 antennal segments and the wing tips extend beyond the second abdominal segment. The overall body length is about 6–7, 12–13, 16–18, 22–25, 27–30, and 35–45 mm for instars 1–6, respectively. Development time is about 4–6, 4–6, 4–6, 4–8, 6–8, and 9–13 days for the corresponding instars when reared at about 32°C. The adult (Fig. 40) is rather large, but slender bodied, measuring 39–52 and 48–68 mm in length in the male and female, respectively. A creamy white stripe normally occurs dorsally from the front of the head to the tips of the forewings. The forewings bear dark brown spots, the pronotum

American Grasshopper, Schistocerca Americana (Drury) (Orthoptera: Acrididae), Figure 40 Adult of American grasshopper, Schistocerca americana (Drury).

American Grasshopper, Schistocerca Americana (Drury) (Orthoptera: Acrididae), Figure 41 Sixth instar of American grasshopper, Schistocerca americana (Drury).


dark stripes. The hind wings are nearly colorless. The hind tibiae normally are reddish. Overall, the body color is yellowish brown or brownish with irregular lighter and darker areas, though for a week or so after assuming the adult stage a pinkish or reddish tint is evident. Adults are active, flying freely and sometimes in swarms. They normally are found in sunny areas, but during the warmest portions of the day will move to shade. Adults are long lived, persisting for months in the laboratory and apparently in the field as well. This can lead to early-season situations where overwintered adults, all instars of nymphs, and new adults are present simultaneously. Mild winters favor survival of overwintering adults and apparently lead to population increase if summer weather and food supplies also are favorable. Adults of American grasshopper tend to be arboreal in habit, and a great deal of the feeding by adults occurs on forest, shade, and fruit trees. The nymphs, however, feed on a large number of grasses and broadleaf plants, both wild and cultivated. During periods of abundance, almost no plants are immune to attack, and vegetables, grain crops, and ornamental plants are injured. American grasshopper consumes bean, corn, okra, and yellow squash over some other vegetables when provided with choices, but free-flying adults normally avoid low-growing crops such as vegetables, corn (maize) being a notable exception. The natural enemies of S. americana are not well known. Birds such as mockingbirds, Mimus polyglottos polyglottos (Linnaeus), and crows, Corvus brachyrhynchos brachyrhynchos Brehm have been observed to feed on these grasshoppers. Fly larvae, Sarcophaga sp. (Diptera: Sarcophagidae) are sometimes parasitic on overwintering adults. Fungi have also been investigated for grasshopper suppression and Metarhizium anisopliae var. acridum kills American grasshopper quickly under laboratory conditions. This fungus is effective under adverse field conditions in Africa, so it may prove to be a useful suppression tool.

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Damage Grasshoppers are defoliators, eating irregular holes in leaf tissue. Under high density conditions they can strip vegetation of leaves, but more commonly leave plants with a ragged appearance. American grasshopper displays a tendency to swarm, and the high densities of grasshoppers can cause severe defoliation. Because American grasshopper is a strong flier, it also sometimes becomes a contaminant of crops. When the late-season crop of collards in the Southeast is harvested mechanically, for example, American grasshopper may become incorporated into the processed vegetables. Although most grasshoppers can be kept from dispersing into crops near harvest by treating the periphery of the crop field, it is much more difficult to prevent invasion by American grasshopper because it may fly over any such barrier treatments. Populations normally originate in weedy areas such as fence rows and abandoned fields. Thus, margins of fields are first affected and this is where monitoring should be concentrated. It is highly advisable to survey weedy areas in addition to crop margins if grasshoppers are found, as this gives an estimate of the potential impact if the grasshoppers disperse into the crop. Also, it is important to recognize that this species is highly dispersive in the adult stage, and will fly hundreds of meters or more to feed.

Management Foliar applications of insecticides will suppress grasshoppers, but they are difficult to kill, particularly as they mature. Bait formulations are not usually recommended because these grasshoppers spend little time on the soil surface, preferring to climb high in vegetation. Land management is an important element of S. americana population regulation. Grasshopper densities tend to increase in large patches

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of weedy vegetation that follow the cessation of agriculture or the initiation of pine tree plantations. In both cases, the mixture of annual and perennial forbs and grasses growing in fields that are untilled seems to favor grasshopper survival, with the grasshoppers then dispersing to adjacent fields as the most suitable plants are depleted. However, as abandoned fields convert to dense woods or the canopy of pine plantations shades the ground and suppresses weeds, the suitability of the habitat declines for grasshoppers. Disturbance or maturation of crops may cause American grasshopper to disperse, sometimes over long distances, into crop fields. Therefore, care should be taken not to cut vegetation or till the soil of fields harboring grasshoppers if a susceptible crop is nearby. Planting crops in large blocks reduces the relative amount of crop edge, and the probability that a crop plant within the field will be attacked.  Grasshopper Pests in North America  Grasshoppers and Locusts as Agricultural Pests  Grasshoppers, Katydids and Crickets (Orthoptera)

References Capinera JL (1993) Differentiation of nymphal instars in Schistocerca americana (Orthoptera: Acrididae). Fla Entomol 76:175–179 Capinera JL (1993) Host-plant selection by Schistocerca americana (Orthoptera: Acrididae). Environ Entomol 22:127–133 Capinera JL, Scott RD, Walker TJ (2004) Field guide to the grasshoppers, katydids, and crickets of the United States. Cornell University Press, Ithaca, NY, 249 pp Kuitert LC, Connin RV (1952) Biology of the American grasshopper in the southeastern United States. Fla Entomol 35:22–33

American Foulbrood Historically, this is the most virulent disease of honey bees throughout the world. The bacterium responsible for the disease, Paenibacillus

(= Bacillus) larvae, form heat- and drought- resistant spores that persist for years and germinate under favorable conditions. It is expressed in older larvae and young pupae, though infection occurs earlier, and young larvae are more susceptible than older larvae. Infected individuals turn darker in color, then black, and eventually collapse into a hardened mass in the cell. Signs of infection include a sour odor, perforated or sunken caps on the cells, and the presence of black deposits in the cells. If foulbrood is present, insertion of a twig or probe into a suspect cell will result in a gummy, stretchy substance being drawn out of the cell, often forming a thread or rope and called “ropy.” Field diagnosis is possible by experienced inspectors, but is best confirmed microscopically or by molecular techniques. There are several subspecies of P. larvae, and P. larvae ssp. larvae is considered responsible for American foulbrood, with other subspecies also affecting honey bees. Transmission occurs by feeding infected honey or pollen, by using infected equipment, and sometimes by installing infected package bees or queens. Feeding bees sugar syrup therefore is preferable to feeding them honey, and disinfection of hive tools is always recommended. Natural transmission from hive to hive can occur through robbing behavior. Queens and workers can carry the disease. Bee colonies that are infected normally are eliminated by burning them. Antibiotics can be fed to colonies to prevent infection.  Honey Bees  Apiculture  Paenibacillus

References Alippi AM, López AC, Aguilar OM (2002) Differentiation of Paenibacillus larvae subsp. larvae, the cause of American foulbrood of honeybees, by using PCR and restriction fragment analysis of genes encoding 16S rRNA. Appl Environ Microbiol 68:3655–3660 Morse RA, Nowogrodzki R (1990) Honey bee pests, predators and diseases, 2nd ed. Cornell University Press, Ithaca, NY, 474 pp

American Serpentine Leafminer, Liriomyza Trifolii (Burgess) (Diptera: Agromyzidae)

American Serpentine Leafminer, Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) This leafminer has long been found in eastern North America, northern South America, and the Caribbean. However, in recent years it has been introduced into California, Europe, and elsewhere. Expanded traffic in flower crops appears to be the basis for the expanding range of this species. Liriomyza trifolii (Burgess), sometimes known as the American serpentine leafminer, readily infests greenhouses. As a vegetable pest, however, its occurrence is limited principally to tropical and subtropical regions.

Life Cycle and Description Leafminers have a relatively short life cycle. The time required for a complete life cycle in warm environments is often 21–28 days, so numerous generations can occur annually in tropical climates. Growth at a constant 25°C requires about 19 days from egg deposition to emergence of the adult. Development rates increase with temperature up to about 30°C; temperatures above 30°C are usually unfavorable and larvae experience high mortality. At 25°C, the egg stage requires 2.7 days for development; the three active larval instars require an average of 1.4, 1.4, and 1.8 days, respectively; and the time spent in the puparium is 9.3 days. Also, there is an adult preovipostion period that averages 1.3 days. The temperature threshold for development of the various stages is 6–10°C, except that egg laying requires about 12 C.

Egg Eggs tend to be deposited in the middle of the plant; the adult seems to avoid immature leaves. The female deposits the eggs on the lower surface of the leaf, but they are inserted just below the epidermis. Eggs are oval in shape and small in size,

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measuring about 1.0 mm long and 0.2 mm wide. Initially they are clear, but soon become creamy white in color.

Larva Body and mouth part size can be used to differentiate instars; the latter is particularly useful. For the first instar, the mean and range of body and mouth parts (cephalopharyngeal skeleton) lengths are 0.39 (0.33–0.53) mm and 0.10 (0.08–0.11) mm, respectively. For the second instar, the body and mouth parts measurements are 1.00 (0.55–1.21) mm and 0.17 (0.15–0.18) mm, respectively. For the third instar, the body and mouth parts measurements are 1.99 (1.26–2.62) mm and 0.25 (0.22– 0.31) mm, respectively. A fourth instar occurs between puparium formation and pupation, but this is a nonfeeding stage and is usually ignored by authors. The puparium is initially golden brown in color, but turns darker brown with time.

Adult Adults (Fig. 42) are small, measuring less than 2 mm in length, with a wing length of 1.25–1.9 mm. The head is yellow with red eyes. The thorax and abdomen are mostly gray and black although the ventral surface and legs are yellow. The wings are transparent. Key characters that serve to differentiate this species from the vegetable leafminer, Liriomyza sativae Blanchard, are the matte, grayish black mesonotum and the yellow hind margins of the eyes. In vegetable leafminer the mesonotum is shining black and the hind margin of the eyes is black. The small size of this species serves to distinguish it from pea leafminer, Liriomyza huidobrensis (Blanchard), which has a wing length of 1.7–2.25 mm. Also, the yellow femora of American serpentine leafminer help to separate it from pea leafminer, which has darker femora. Oviposition occurs at a rate of 35–39 eggs per day, for a total fecundity of 200–400 eggs. The female makes

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American Serpentine Leafminer, Liriomyza Trifolii (Burgess) (Diptera: Agromyzidae), Figure 42 Adult of American serpentine leafminer, Liriomyza trifolii.

numerous punctures of the leaf mesophyll with her ovipositor, and uses these punctures for feeding and egg laying. The proportion of punctures receiving an egg is about 25% in chrysanthemum and celery, both favored hosts, but only about 10% in tomato, which is less suitable for larval survival and adult longevity. Although the female apparently feeds on the exuding sap at all wounds, she spends less time feeding on unfavorable hosts. The males live only two to three days, possibly because they cannot puncture foliage and therefore feed less than females, whereas females usually survive for about a week. Typically they feed and oviposit during much of the daylight hours, but especially near mid-day.

Host Plants Liriomyza trifolii is perhaps best known as a pest of chrysanthemums and celery, but it has a wide host range. For example, at least 55 hosts are known from Florida, including bean, beet, carrot, celery, cucumber, eggplant, lettuce, melon, onion, pea, pepper, potato, squash, and tomato. Flower

crops that are readily infested and which are known to facilitate spread of this pest include chrysanthemum, gerbera, gypsophila, and marigold, but there are likely many other hosts, especially among the Compositae. Numerous broad-leaved weed species support larval growth. The nightshade Solanum americanum, Spanish needles, Bidens alba, and pilewort, Erechtites hieracifolia, were suitable weed hosts in Florida.

Damage Punctures caused by females during the feeding and oviposition processes can result in a stippled appearance on foliage, especially at the leaf tip and along the leaf margins. However, the major form of damage is the mining of leaves by larvae, which results in destruction of leaf mesophyll. The mine becomes noticeable about three to four days after oviposition, and becomes larger in size as the larva matures. The pattern of mining is irregular. Both leaf mining and stippling can greatly depress the level of photosynthesis in the plant. Extensive mining also causes premature


leaf drop, which can result in lack of shading and sun scalding of fruit. Wounding of the foliage also allows entry of bacterial and fungal diseases. Although leaf mining can reduce plant growth, crops such as tomato are quite resilient, and capable of withstanding considerable leaf damage. It is often necessary to have an average of one to three mines per tomato leaf before yield reductions occur. Leafminers are most damaging when they affect floricultural crops due to the low tolerance of such crops for any insect damage.

Natural Enemies Parasitic wasps (parasitoids) of the families Braconidae, Eulophidae, and Pteromalidae are important in natural control, and in the absence of insecticides usually keep this insect at low levels of abundance. At least 14 parasitoid species are known from Florida alone. Species of Eulophidae such as Diglyphus begina (Ashmead), D. intermedius (Girault), D. pulchripes, and Chrysocharis parksi Crawford are generally found to be most important in studies conducted in North America, although their relative importance varies geographically and temporally. Predators and diseases are not considered to be important, relative to parasitoids. However, both larvae and adults are susceptible to predation by a wide variety of general predators, particularly ants.

Management Sampling There are many methods to assess leafminer abundance. Counting mines in leaves is a good index of past activity, but many mines may be vacant. Counting live larvae in mines is time consuming, but more indicative of future damage. Puparia can be collected by placing trays beneath foliage to capture larvae as they evacuate mines, and the captures are highly correlated with the number of

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active miners. Adults can be captured by using adhesive applied to yellow cards or stakes.

Insecticides Chemical insecticides are commonly used to protect foliage from injury, but insecticide resistance is a major problem. Insecticide susceptibility varies widely among populations, and level of susceptibility is directly related to frequency of insecticide application. In Florida, longevity of insecticide ef fectiveness is often only two to four years, and then is usually followed by severe resistance among the treated populations. Rotation among classes of insecticides is recommended to delay development of resistance. Reduction in dose level and frequency of insecticide application, as well as preservation of susceptible populations through nontreatment of some areas, are suggested as means to preserve insecticide susceptibility among leafminer populations. Insect growth regulators have been more stable, but are not immune from the resistance problem. Insecticides also are highly disruptive to naturally occurring biological control agents, particularly parasitoids. Use of many chemical insecticides exacerbates leafminer problems by killing parasitoids of leafminers. This usually results when insecticides are applied for lepidopterous insects, and use of more selective pest control materials such as Bacillus thuringiensis is recommended as it allows survival of the leafminer parasitoids. Because parasitoids often provide effective suppression of leafminers in the field when disruptive insecticides are not used, there has been interest in release of parasitoids into crops. This occurs principally in greenhouse-grown crops, but is also applicable to field conditions. Steinernema nematodes have also been evaluated for suppression of leaf mining activity. High levels of relative humidity (at least 92%) are needed to attain even moderately high (greater than 65%) levels of parasitism. Adjuvants that enhance nematode survival increase levels of leafminer mortality, but thus far nematodes are not considered to be a practical solution to leafminer infestations.

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American Silkworm Moths (Lepidoptera: Apatelodidae)

Cultural Practices Because broadleaf weeds and senescent crops may serve as sources of inoculum, destruction of weeds and deep plowing of crop residues are recommended. Adults experience difficulty in emerging if they are buried deeply in soil.  Vegetable Pests and Their Management  Flies

References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, CA, 729 pp Leibee GL (1984) Influence of temperature on development and fecundity of Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) on celery. Environ Entomol 13:497–501 Minkenberg OPJM (1988) Life history of the agromyzid fly Liriomyza trifolii on tomato at different temperatures. Entomologia Expimentalis et Applicata 48:73–84 Minkenberg OPJM, van Lenteren JC (1986) The leafminers Liriomyza bryoniae and L. trifolii (Diptera: Agromyzidae), their parasites and host plants: a review. Wageningen Agric Univ Pap 86–2. 50 pp Parrella MP, Robb KL, Bethke J (1983) Influence of selected host plants on the biology of Liriomyza trifolii (Diptera: Agromyzidae). Ann Entomol Soc Am 76:112–115 Schuster DJ, Gilreath JP, Wharton RA, Seymour PR (1991) Agromyzidae (Diptera) leafminers and their parasitoids in weeds associated with tomato in Florida. Environ Entomol 20:720–723 Zehnder GW, Trumble JT (1984) Spatial and diel activity of Liriomyza species (Diptera: Agromyzidae) in fresh market tomatoes. Environ Entomol 13:1411–1416

American Silkworm Moths (Lepidoptera: Apatelodidae) john b heppner Florida State Collection of Arthropods, Gainesville, FL, USA American silkworm moths, family Apatelodidae, are exclusively New World, and total 252 species, mostly Neotropical (247 sp.). Three subfamilies are known: Apatelodinae, Epiinae, and Phiditiinae.

American Silkworm Moths (Lepidoptera: Apatelodidae), Figure 43 Example of American silkworm moths (Apatelodidae), Apatelodes palma Druce, from Ecuador.

Some researchers consider the family part of Bombycidae. The family is in the superfamily Bombycoidea (series Bombyciformes), in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults (Fig. 43) small to medium size (20–74 mm wingspan), with head scaling roughened; haustellum absent (rarely vestigial); labial palpi small; maxillary palpi absent; antennae bipectinate; body robust. Wings broadly triangular; hindwings rounded. Maculation varied but mostly shades of brown or gray, rarely more colorful, with various markings. Adults are nocturnal. Larvae are leaf feeders. Host plants include various records in Aquifoliaceae, Betulaceae, Bignoniaceae, Lauraceae, Oleaceae, Rosaceae, among others.

References Franclemont JG (1973) Apatelodidae. In: Dominick RB, et al (eds), The moths of America north of Mexico including Greenland. Fasc. 20.1, Bombycoidea, 16–23. Classey EW, London Seitz A (ed) (1929) Familie: Bombycidae. Die Gross-Schmetterlinge der Erde, 6:675–711, pl. 89, 140–142. A. Kernen. [Apatelodidae], Stuttgart, Germany

American Tropical Silkworm Moths (Lepidoptera: Oxytenidae)

American Swallowtail Moths (Lepidoptera: Sematuridae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA American swallowtail moths (Fig. 44), family Sematuridae, total 36 Neotropical species, one of which just reaches into the United States, in southern Arizona. The family is in the superfamily Uranioidea, in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults medium to large (42–100 mm wingspan), with head roughened and eyes large; haustellum naked; labial palpi upcurved, with long second segment and correctly angled short, smooth apical segment; maxillary palpi minute, 1-segmented; antennae thickened, with elongated club (slightly hooked at tip). Wings triangular, with hindwings tailed (usually hindwings with some emarginations); body sometimes robust. Maculation various shades of darker brown, with vertical lines and bands, often brightly colored in the hindwings; often with eyespots on the tails. Adults are nocturnal but some may be crepuscular.

American Swallowtail Moths (Lepidoptera: Sematuridae), Figure 44 Example of American swallowtail moths Sematuridae), Sematura lunus (Linnaeus), from Costa Rica.

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Larvae are leaf feeders, but few known biologically. Host plants are unrecorded.

References Seitz A (ed) (1930) Familie: Uraniidae [part]. Die GrossSchmetterlinge der Erde, 6:829–837, pl. 139. A. Kernen, Stuttgart, Germany Fassl AH (1910) Die Raupe einer Uranide. Zeitschrift für Wissenschaftliches Insektenbiologie 6:355 Strand E (1911) Zur Kenntnis der Uraniidengattung Coronidia Westw. and Homidia Strand n. g. (=Coronidia auct. p.p.) (Lep.). Deutsche Entomologische Zeitschrift 1911:635–649 Westwood JO (1879) Observations on the Uraniidae, a family of lepidopterous insects, with a synopsis of the family and a monograph of Coronidia, one of the genera of which it is composed. Trans Zool Soc London 10:507–542, 4 pl

American Tropical Silkworm Moths (Lepidoptera: Oxytenidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA American tropical silkworm moths, family Oxytenidae, include 60 species, all Neotropical. Some specialists consider this family a subfamily of Saturniidae. The family is in the superfamily Bombycoidea (series Saturniiformes), in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults medium size to large (45–98 mm wingspan), with head vertex somewhat roughened; haustellum developed; labial palpi very large; maxillary palpi absent; antennae bipectinate; body somewhat slender or robust but with hair-like scales. Wings triangular with with falcate apex but sometimes rounded; hindwings somewhat angled and with short tails or sometimes rounded. Maculation mostly white with paired dark gray vertical striae and hindwings similar, but some species are dark brown with indistinct markings. Adults nocturnal. Larvae are leaf feeders; some mimic snakes. Host plants recorded in Rubiaceae.

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Ametabolous

References Heppner JB (2003) Oxytenidae. Lepidopterorum catalogus, (n.s.). Fasc. 115. Association for Tropical Lepidoptera, Gainesville, FL, 12 pp Jordan K (1924) On the Saturnoidean families Oxytenidae and Cercophanidae. Novitates Zoologicae 31:135–193 Schüssler H (1936) Oxytenidae. Lepidopterorum catalogus, W. Junk, The Hague, 75:1–20

Ametabolous Organisms that do not display the process of metamorphosis. In ametabolous organisms there is little change in body form during growth and molting.  Metamorphosis

Ametropodidae A family of mayflies (order Ephemeroptera).  Mayflies

Amino Acid Chemical compounds that may occur free, or linked by peptide bonds into proteins.

Ammophilous Sand loving. Organisms inhabiting or preferring sandy habitats are called ammophilous (adjective) or ammophiles (noun).

Amoebae The two best-studied insect amoebae are Malpighamoeba mellificae and Malamoeba locustae, which are associated with the honeybee, Apis mellifera, and the Melanoplus grasshoppers,

respectively. The cysts of the honeybee amoeba are ingested and excyst, releasing slender primary trophozoites that penetrate and multiply in the midgut epithelium. Secondary trophozoites emerge from these cells and migrate to the lumen of the Malpighian tubules. These trophozoites, having pseudopodia, feed in the lumen and cause a flattening of the epithelial layer and a distension of the tubules. The brush border in contact with the amoeba swells in size and loses the associated secretory transport vesicles. Infected tubules contain a mix of secondary trophozoites, precysts, and cysts. The primary damage to the host bee is the malfunction of the Malpighian tubules. Both numbers of amoeba and the presence of other disease agents determine the severity of the amoebiasis in the bee. In general, this disease either induces stress or under appropriate conditions in the springtime can be debilitative, resulting in hive dwindling. Malamoeba locustae, also known as Malamoeba locusta, has been detected in a wide range of grasshopper species and in a single Thysanuran species. Its life cycle is very similar to that observed with M. mellificae. The host grasshoppers ingest the resistant uninucleate cysts, and excysted primary trophozoites invade the midgut and caecal tissues. Within these tissues the trophozoites grow and divide, and within about 10 days release progeny secondary trophozoites into the lumen. These cells migrate to the lumen of the Malpighian tubules and undergo additional cell divisions (Fig. 45). The vegetative development of this amoeba damages the serosal membrane of the tubules, inhibiting their response to insect diuretic hormone. The infected tubules become packed with trophozoites and cysts. At high levels, M. locustae may inhibit the excretory function of the tubules and cause the grasshoppers to become lethargic prior to death. The distended, amoebainfected tubules may rupture, releasing both trophozoites and cysts into the hemocoel. These amoebas are quickly recognized as non-self and are encapsulated by circulating phagocytic

Amphitheridae

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Amoebae, Figure 45 Light micrograph of the cysts of Malamoeba locusta released from infected Malpighian tubules.

hemocytes. This disease, although a problem in laboratory cultured grasshoppers, is rarely detected in natural populations.

References Brooks WM (1988) Entomogenous Protozoa. In: Ignoffo C (ed), Handbook of natural pesticides, vol 5. Microbial insecticides. Part A. Entomogenous protozoa and fungi. CRC Press, Boca Raton, FL, pp 1–149 Liu TP (1985) Scanning electron microscopy of developmental stages of Malpighamoeba mellificae Prell in the honeybee. J Protozool 32:139–144

Amoebiasis Infection of an insect by amoebae.

Amorphoscelididae A family of praying mantids (Mantodea).  Praying Mantids

Amphienotomidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice, or Psocids

Amphiposocidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice, or Psocids

Amphipterygidae A family of damselflies (order Odonata).  Dragonflies and Damselflies

Amphitheridae A family of moths (order Lepidoptera) also known as double-eye moths.  Double-Eye Moths  Butterflies and Moths

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Amphitoky

Amphitoky A type of parthenogenesis in which both females and males are produced.

Amphizoidae A family of beetles (order Coleoptera). They commonly are known as trout stream beetles.  Beetles  Wasps, Ants, Bees and Sawflies

Amplification In molecular biology, the production of additional copies of a chromosomal sequence, found as either intrachromosomal or extrachromosomal DNA. In medical entomology, the production of increased numbers of virus in a host. This is often a prerequisite to acquisition and transmission of the virus by a blood-feeding insect.

Amplification Hosts Hosts of viruses that allow amplification of the virus, usually used in the context of arboviruses. Some hosts do not allow amplification, and so serve as an end-point in the virus cycle.  Dead-end Hosts

Ampulicidae A family of wasps (order Hymenoptera).

Anagrus Fairyflies (Hymenoptera: Mymaridae) elisabetta chiappini Università Cattolica del Sacro Cuore, Piacenza, Italy

Anagrus species (Mymaridae), among the smallest insects known, are endoparasitoids of eggs of Odonata and Hemiptera. The genus is worldwide and about 60 species is now recognized.

Taxonomy and Adult Morphology The metasoma of Anagrus is not constricted basally, so it appears broadly sessile, the hypochaeta in front of the marginal vein is basal to the first macrochaeta, the tarsi are 4-segmented, the posterior scutellum is longitudinally divided, and the foretibia has a comb-like spur. Adult males and females are similar, differing mainly in their antennae, with nine segments and clubbed in females (Fig. 46) and 13 segments and filiform in males. Body color is often darker in males. The genitalia, both in males (the aedeagus) and in females (the ovipositor), have features of taxonomic importance. The genus is subdivided into three subgenera – Anagrella, Anagrus, and Paranagrus.

Biology Like all holometabolous insects, Anagrus species have three distinct immature stages, egg, larva and pupa. The egg is stalked, with an ovoid body that swells during embryogenesis. There are two, apodous, larval instars (Fig. 47), which appear completely different from one another. The first instar is sacciform and usually attached to the egg chorion. It does not show any cuticular structure that could serve to feed, breathe or feel. It is completely immobile and probably obtains nourishment and breathes through its cuticle. The second instar is divided weakly into six body segments, has a mouth and a salivary gland opening, two mandibles and an anus, and various other, probably sensory, structures. No spiracle is present. Second instar larvae are very active and fight each other when in the same host egg. The mature larva (prepupa) develops inside the egg into an exarate pupa and does not spin a cocoon. When development is complete, adults are

Anagrus Fairyflies (Hymenoptera: Mymaridae)

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Anagrus Fairyflies (Hymenoptera: Mymaridae), Figure 46 Adult female of Anagrus sp.

Anagrus Fairyflies (Hymenoptera: Mymaridae), Figure 47 Larva of Anagrus sp.

r ecognizable through the host egg chorion, through which they chew a hole to exit. After emergence the adults shed their waste products (meconium). Males are usually protandrous.

Behavior and Ecology Reproduction is bisexual or parthenogenetic. The latter reproduction is usually arrhenotokous but, rarely, thelytokous parthenogenesis has been recorded. Females are ready to oviposit as soon as they emerge. Copulation, if it occurs, is usually very quick (some tens of seconds) and inseminated females generally do not copulate again. When fed with sugar water, honey or nectar, adults may live for up to 10 days. It is thought that adult host feeding may occur as in other parasitoids. Anagrus species mainly parasitize leafhoppers (Cicadellidae), planthoppers, (Delphacidae) and damsel- or dragonfly (Odonata) eggs, all of which are embedded in plant tissue. To reach the eggs,

females insert their ovipositor into the slit made by the host or through the plant tissue itself, depending on the species. Adults occur in various habitats, both natural and cultivated, depending on where their hosts occur. This includes dry habitats such as vineyards and beet fields to damp or aquatic ones (ponds) where host eggs are found in plants such as Cyperus or Nuphar. Certain Anagrus species can develop both as solitary or gregarious parasitoids in eggs of different size, whereas others appear to be much more specialized on eggs of the same size, in which they always develop as solitary parasitoids. Many Anagrus are extremely important because they provide control of potentially serious pests on many agricultural crops. The most important examples are against leafhoppers such as Empoasca vitis Goethe and Zygina rhamni (Ferrari) in vineyards in Europe and Erythroneura spp. in North America, against leaf- and planthoppers such as Nilaparvata spp. and Sogatella spp. on rice in eastern Asia, and against Perkinsiella sacharicida Kirkaldy on sugarcane in Hawaii. Some biological supply companies mass produce and sell Anagrus atomus L. for biological control. Care must be taken to ensure the sanitary conditions of the product as the parasitoid is bred on the natural host eggs inserted into plant tissue, which could be a potential vehicle for other pests or diseases.

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Anajapygidae

References Chiappini E, Lin NQ (1998) Anagrus (Hymenoptera: Mymaridae) of China, with descriptions of nine new species. Ann Entomol Soc Am 91:549–571 Chiappini E, Triapitsyn SV, Donev A (1996) Key to the Holarctic species of Anagrus Haliday (Hymenoptera: Mymaridae) with a review of the Nearctic and Palaearctic (other than European) species and descriptions of new taxa. J Nat Hist 30:551–595 Moratorio MS (1990) Host finding and oviposition behavior of Anagrus mutans and Anagrus silwoodensis Walker (Hymenoptera: Mymaridae). Environ Entomol 19:142–147 Moratorio MS, Chiappini E (1995) Biology of Anagrus incarnatosimilis and Anagrus breviphragma. Bollettino di Zoologia Agraria e di Bachicoltura, Serie II, 27:143–162 Triapitsyn SV (1997) The genus Anagrus (Hymenoptera: Mymaridae) in America south of the United States: a review. Ceiba 38:1–12 Triapitsyn SV (1998) Anagrus (Hymenoptera: Mymaridae) egg parasitoids of Erythroneura spp. and other leafhoppers (Hemiptera: Cicadellidae) in North America vineyards and orchards: a taxonomic review. Trans Am Entomol Soc 124:77–112

Anajapygidae A family of diplurans (order Diplura).  Diplurans

abdominal segment; in caterpillars (Lepidoptera) it refers to a ventral projection at the tip of the abdomen that is used to eject frass; in some beetle (Coleoptera) larvae it refers to cerci-like projections near the tip of the abdomen.

Anal Gills Gills found at the tip of the abdomen and usually consisting of three to five small clusters.  Abdomen of Hexapods

Anal Hooks In Lepidoptera, small hook or club-shaped structures at the tip of the abdomen that serve to anchor the pupa to the cocoon or silk pad.

Anal Furrow The suture-like groove in the membrane of the wing.  Wings of Insects

Anal Legs (Prolegs) Anal Angle The hind angle of the forewings.  Wings of Insects

Anal Cell A cell in the anal area (anal lobe) of a wing.  Wings of Insects

Anal Comb This term is applied to a variety of structures that differ depending on the taxon. In flea (Siphonaptera) larvae, it refers to several rows of setae on the tenth

In holometabolous larvae, especially Lepidoptera larvae, the appendages of the tenth abdominal segment (the terminal prolegs).

Anal Lobe The posterior region of the wing, occupied by the anal veins.  Wings of Insects

Anal Loop A cluster of cells between the anal wing veins, or between the cubitus and anal vein, in Odonata.  Wings of Insects

Andean Moon Moths (Lepidoptera: Cercophanidae)

Anal Plate The shield-like plate or dorsal covering on the terminal segment in caterpillars, and some other larvae. It usually is dark in color, and is also called the anal shield.

Anal Tube Eversible, tubular organs in the anal region of larval Coleoptera. These organs are armed with microspines and assist in attachment to the substrate.

Anal Vein Longitudinal unbranched vein, or veins, extending from the base of the wing to the outer margin of the wing, below the cubitus vein.  Wings of Insects

Anamorphosis

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Andean Moon Moths (Lepidoptera: Cercophanidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Andean moon moths, family Cercophanidae, include 30 species of mostly austral South American moths. There are two subfamilies: Cercophaninae (four sp.) and Janiodinae (26 sp.). Some specialists consider this family a subfamily of Saturniidae. The family is in the superfamily Bombycoidea (series Saturniiformes), in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults (Fig. 48) medium size to large (24–105 mm wingspan), with head vertex roughened; haustellum absent; labial palpi very large; maxillary palpi absent; antennae bipectinate; body robust, with long hair-like scales. Wings broadly triangular, often with apex falcate, or more rounded; hindwings rounded or emarginated but sometimes with tails. Maculation various, but mostly shades of brown with diagonal line and fainter markings, but some with long tails and lighter tan, and with eyespots. Adults are nocturnal. Larvae are leaf feeders.

Postembryonic development in which additional abdominal body segments are added at the time of molting (the opposite of epimorphosis).

Anaxyelidae A family of wood wasps (order Hymenoptera, suborder Symphyta). They commonly are known as incense-cedar wood wasps.  Wasps, Ants, Bees and Sawflies

Ancistrosyllidae A family of fleas (order Siphonaptera).  Fleas

Andean Moon Moths (Lepidoptera: Cercophanidae), Figure 48 Example of Andean moon moths (Cercophanidae), Cercophana venusta (Walker) from Chile.

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Andesianidae

Host plants recorded in Celastraceae, Lauraceae, Saxifragaceae, and Tiliaceae.

References Angulo AO, Heppner JB (2004) Cercophanidae. Lepidopterorum catalogus, (n.s.). Fasc. 116. Association for Tropical Lepidoptera, Gainesville, FL, 8 pp Jordan K (1924) On the Saturnoidean families Oxytenidae and Cercophanidae. Novitates Zoologicae 31:135–193, pl. 6–21 Schüssler H (1936) Cercophanidae. Lepidopterorum catalogus, W. Junk, The Hague, 76:1–12 Ureta RE (1943) Revisión del género Polythysana Wlk. (Saturniidae). Boletin del Museo Nacional de Historia Natural de Chile 21:55–70, 4 pl Wolfe KL, Balcázar LMA (1994). Chile’s Cercophana venusta and its immature stages (Lepidoptera: Cercophanidae) Trop Lepidoptera 5:35–42

Andesianidae A family of moths (order Lepidoptera) also known as valdivian forest moths.  Butterflies and Moths  Valdivian Forest Moths

Andrenidae A family of bees (order Hymenoptera, superfamily Apoidae).  Bees  Wasps, Ants, Bees and Sawflies

Australia Department of Agriculture. He began a study of a weevil pest of fruit trees, Otiorhynchus cribricollis, that required detailed autecological studies. In 1933, he moved to Melbourne, appointed by the CSIR as assistant research officer, to work on the autecology of Thrips imaginis, a pest of apple trees. He worked in the School of Agriculture and Forestry at the University of Melbourne. While working, he was able to complete a thesis for which he was awarded the degree of Master of Agricultural Sciences. He married, and in 1935 moved to the Waite Agricultural Research Institute in Adelaide. His main duties now turned to a study of Austroicetes cruciata, a plague grasshopper, and diapause of its eggs. However, his supervisor, who had been working on Thrips imaginis, died suddenly, leaving copious unanalyzed data, whose completion and publication fell to Herbert. The published work was criticized because it concluded that climatic factors were all-important in the population dynamics of the pest, without room for action of biotic factors. But it led to collaboration with L.C. Birch on a book (1954) “The distribution and abundance of animals.” Then, after Herbert moved to the Zoology Department of the University of Adelaide, it led to a book designed as a textbook for students: (1961) “Introduction to the study of animal populations.” In 1962, Herbert was appointed chairman of the Zoology Department. In the 1960s, with collaborators, he developed a program for control of Dacus tryoni, Queensland fruit fly, by release of sterile males. His next book, also co-authored with L.C. Birch was (1984) “The ecological web.” He died on January 27, 1992, following his wife by some years, but survived by his son and daughter.

Andrewartha, Herbert George Herbert Andrewartha was born in Perth, Australia, on December 21, 1907. In 1924, he entered the University of Western Australia from which he obtained a bachelor’s degree in agriculture. He was then appointed as assistant entomologist by the Western

Reference Birch LC, Browning TO (1993) Herbert George Andrewartha 1907–1992. Historical Records of Australian Science 9(3), Available at www.asap.unimelb. edu.au/bsparcs/ aasmemoirs/andrewar.htm Accessed August 2002

Angel Insects (Zoraptera)

Androconia In Lepidoptera, glandular wing and body scales. Scent scales.

Androparae In aphids, viviparous females that are produced on the secondary host in the autumn, and then fly to the primary host to produce males.  Aphids

Anemometer An instrument used for measuring wind speed, an important tool when considering use of pesticides because high wind speeds can result in pesticide drift.

Anemotaxis A movement in response to air movement or air currents.

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Angel Insects (Zoraptera) This is a small group of minute insects. They are infrequently encountered, and poorly known. The order name is based on the Greek words zoros (pure), a (without), and pteron (wing). There are only about 30 species described, all in the family Zorotypidae.

Characteristics Angel insects are only about 3 mm long, with a wing span of 7 mm. They are dimorphic: a wingless form that lacks eyes, ocelli, and is only slightly pigmented, and a winged form (Fig. 49) that bears eyes, ocelli, and is darker in color. They have chewing mouthparts. The antennae are filiform, and consist of nine segments. The legs are unspecialized, the tarsi 2-segmented. The wings have simplified venation, and the wings can be shed, as is the case with termites. The abdomen is cylindrical and consists of 11 segments. Very short, 1-segmented cerci occur near the tip of the abdomen. Metamorphosis is not pronounced.

Angel Insects (Zoraptera), Figure 49 A diagram of an angel insect showing a dorsal view. The wings are removed from the left side of the body.

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Angoumois Grain Moth, Sitotroga cerealella (Lepidoptera: Gelechiidae)

Biology Angel insects are found beneath bark, in humus, decaying wood, and sometimes in association with termites. They are believed to feed on fungi. Apparently they swarm, and drop wings after swarming. They are gregarious, but there is no evidence of social organization.

References Arnett RH Jr (2000) American insects, 2nd edn. CRC Press, Boca Raton, FL, 1003 pp Riegel GT (1987) Order Zoraptera. In: Stehr FW (ed) Immature insects, vol 1. Kendall/Hunt Publishing, Dubuque, Iowa, pp 184–185 Gurney AB (1938) A synopsis of the order Zoraptera with notes on the biology of Zorotypus hubbardi Caudell. Proc Entomol Soc Wash 40:57–87

Angoumois Grain Moth, Sitotroga cerealella (Lepidoptera: Gelechiidae) This is an important primary pest of stored grain.  Stored Grain and Flour Insects

In humans the same disease is known as African sleeping sickness or human trypanosomiasis. It is transmitted by tsetse flies in Africa.  Trypanosomes  Tsetse Flies  Sleeping Sickness or African Trypanosomiasis

Anisembiidae A family of web-spinners (order Embiidina).  Web-spinners

Anisopodidae A family of flies (order Diptera). They commonly are known as wood gnats.  Flies

Anneal The process by which the complementary base pairs in the strands of DNA combine.

Annual Angulate Forming an angle.

Anholocyclic Life Cycle A life cycle in which there is a complete lack of male insects (generally aphids). In this type of life cycle only viviparous parthenogenetic females are present throughout the year. (contrast with holocyclic life cycle)  Aphids

Animal Sleeping Sickness Also known as nagana, this is a disease of animals caused by protozoans in the genus Trypanosoma.

A plant that normally completes its life cycle of seed germination, vegetative growth, reproduction, and death in a single growing season or year.

Anobiidae A family of beetles (order Coleoptera). They commonly are known as death-watch beetles.  Beetles

Anomosetidae A family of moths (order Lepidoptera). They also are known as Australian primitive ghost moths.  Australian Primitive Ghost Moths  Butterflies and Moths

Antennae of Hexapods

Anoplura A suborder of wingless ectoparasitic insects commonly known as sucking lice (order Phthiraptera). It is sometimes treated as an order.  Chewing and Sucking Lice

Anostostomatidae A family of crickets (order Orthoptera). They commonly are known as wetas and king crickets.  Grasshoppers, Katydids and Crickets

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Antennae of Hexapods severiano f. gayubo Universidad de Salamanca, Salamanca, Spain According to the known data on anatomy and embryology, the antennae are postoral structures of an appendicular nature that have been displaced, and now situated secondarily above the anterolateral regions of the cranium, in front of the mouth. Taking into account their intrinsic musculature, two fundamental types of antennae can be distinguished:

Anteclypeus The lower of the two divisions of the clypeus.  Mouthparts of Hexapods

Antagonist An antagonist usually is an organism (usually a pathogen) that does no significant damage to the host, but its colonization of the host protects the host from significant subsequent damage by a pest.

Antecosta (pl., antecostae) An internal ridge on the anterior portion of a tergum or sternum. It serves as a point of attachment for the longitudinal muscles.

Antenna (pl., antennae) The paired segmented sensory organs, borne one on each side of the head. The antennae commonly protrude forward. Each antenna (Figs. 50 and 51) consists of three segments: the basal scape, a small pedicel, and an elongate flagellum. The flagellum is usually subdivided into many sections.  Antennae of Hexapods

Segmented Type Each antennal division (antennomere) possesses intrinsic musculature (although the last segment generally lacks it). This type is found in Diplura and Collembola.

Annulated Type Three segments are recognized that, from the basal to the apical zone of the antenna, are called scape, pedicel and antennal flagellum (Fig. 50). The scape is a robust segment that unites the head capsule with a cuticular reinforcement (Fig. 51), the antennal socket (also called the torulus). In the antennal socket one or two condyles are distinguished, which serve to articulate the scape. The second segment is called the pedicel, and it usually varies in form and development, although it is generally small. Lastly, the flagellum is usually divided into several divisions called flagellomeres. The movement of the antennae is carried out through extrinsic or motor muscles of the scape, generally forming three or four functional groups. Depending on the insect group, these muscles are inserted in the head capsule or in the tentorium.

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lateral ocellus scape

compound eye postocular area

pedicel

cervix

flagellum

gena cervical sclerites tentorial suture

clypeus labrum

basimandibular sclerite maxilla labium labial palpus

mandible maxillary palpus

Antennae of Hexapods, Figure 50 Side view of the head of an adult grasshopper, showing some major elements.

The antennae usually have bristles and s ensilla of different types that act as chemoreceptor-, thermoreceptor- or hygroreceptor-type sensory organs. In addition, the antennae of males display modifications tending to increase their surface area, which permits harboring a great number of sensilla and acting as “detectors” that detect pheromones emitted by the females, and enable (usually) the males to locate the females for reproductive functions. Certain modifications in the antennae of the males can also be related to particular courtship behavior prior to mating. In relation to the functions carried out by the antennae, it is necessary to highlight the presence, in the pedicel, of Johnston’s organ, which is formed by cordotonal sensilla. It is fundamentally a proprioreceptor organ that provides information about the position of the

antennae with respect to the head, the direction and force of the wind, or of the water currents in aquatic insects. In addition, it can act as an auditory organ in male mosquitoes and chirinomids, which perceive the sound produced by the females in flight. The number of flagellomeres is a character that, in certain cases, is related to the sex, as occurs in some Aculeate Hymenoptera in which the males display 11 flagellomeres and the females 10. In others, it represents an important taxonomic character, emphasized in this sense the family Argidae (Hymenoptera: Symphyta) whose individuals display the flagellomere undivided. Various types of antennae exist (Fig. 52), the appearance of which is owed fundamentally to the variation in form and development of the flagellomeres. The most important are:


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flagellum

vertex

antenna frons

pedicel scape

median ocellus

face anterior tentorior pit basimandibular sclerite frontoclypeal suture

mandible clypeus

clypeolabral suture

labrum maxillary palpus maxilla labial palpus

Antennae of Hexapods, Figure 51 Front view of the head of an adult grasshopper, showing some major elements.

Filiform

Aristate

The flagellomeres, normally numerous, are narrow, cylindrical, and of similar size. It is the most common type in the insects.

The last flagellomere is normally very wide and bears a conspicuous bristle named the arista. Examples are found in Diptera (Syrphidae and Muscidae).

Moniliform There exists a narrowing in the union of each flagellomere, which are more or less spherical, with the antenna acquiring a “rosaried” appearance (like the beads of a rosary). There are examples in various families of beetles.

Stylate The last flagellomere is prolonged apically in a fine and elongated process named the style. Examples are found in Diptera (Rhagionidae and Asilidae).

Setaceous The flagellomeres are extremely fine and diminish in diameter gradually toward the tip; the antenna thus acquires an appearance of seta or hair. The antennae of Odonata constitute a typical example.

Clavate The flagellomeres increase in diameter gradually toward the apex. Examples are found in Coleoptera (Coccinellidae and Tenebrionidae).

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Antennae of Hexapods, Figure 52 Some common types of antennal forms: A, filiform; B, moniliform; C, capitate; D, clavate; E, setaceous; F, serrate; G, pectinate; H, bipectinate; I, plumose; J, aristate; K, stylate; L, lamellate; M, flabellate; N, geniculate.

Capitate

Pectinate

In this case the last flagellomeres are of greater diameter, in contrast with the preceding, forming a“club” or“mace.” Examples are found in Coleoptera (Nitidulidae and Silphidae).

The flagellomeres project laterally, forming a fine and more or less elongated projection. When it is produced over two sides of each flagellum, the antennae are called bipectinate. Examples are found in Coleoptera (Pyrochroidae).

Serrate

Flabellate

The flagellomeres display pointed, lateral prolongations, on one side or on both. Examples are found in Coleoptera (Elateridae).

The flagellum displays long, flattened or more or less cylindrical expansions. Examples are found in some species of Coleoptera (Scarabeidae).

Anther Smut of Carnations

Lamellate Only the last flagellomeres display long, lateral expansions. Examples are found in Coleoptera (Scarabeidae, subfamily Melolonthinae).

Plumose Flagellomeres with numerous long hairs are arranged in a feather-like or whorled form. Examples are found in male mosquitoes (Diptera).

Geniculate The scape is relatively long, forming a clear angle with the rest of the antenna (pedicel plus flagellum). Examples are found in Hymenoptera (Formicidae and Chalcidoidea), and in Coleoptera (Lucanidae). Within this type of antenna, particular variations can exist, as in the case of the Ormyridae (Hymenoptera: Chalcidoidea), in which the first divisions of the flagellum are of a lenticular type (lens shaped, or double convex).

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Antennal Fossa A groove or cavity in which the antennae are located or concealed. This is also called the antennal insertion.  Antennae of Hexapods

Antennal Sclerite A ring into which the basal joint of each antenna is inserted.  Antennae of Hexapods

Antennation Sensory or tactile movements with the antennae that result in contact of the antennae with an object.

Antennule A small antennal or feeler-like process.

Anterior References Denis JR, Bitsch J (1973) Morphologie de la tête des insects. In: Grassé PP (Dir) Traité de Zoologie, VIII (I):1–593 Gillot C (1995) Entomology, 2nd edn. Plenum Press, New York, NY Manton SM (1977) The Arthropoda. Habits, functional morphology and evolution. Clarendon Press, Oxford, UK Quéinnec E (2001) Insights into arthropod head evolution. Two heads in one: the end of the “endless dispute”? Annales de la Société Entomologique de France 37:51–70 Snodgrass RE (1951) Comparative studies on the head of mandibulate Arthropods. Comstock, Ithaca, NY

Antennal Club On a clubbed antenna, the enlarged distal segments.  Antennae of Hexapods

This term usually is used to refer to the end of the body containing the head, or the direction of the head, or the front of the insect.

Anthelidae A family of moths (order Lepidoptera) also known as Australian lappet moths.  Australian Lappet Moths  Butterflies and Moths

Anther Smut of Carnations This is a fungal disease of carnations that is transmitted by insects.  Transmission of Plant Diseases by Insects

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Anthicidae

Anthicidae A family of beetles (order Coleoptera). They commonly are known as antlike flower beetles.  Beetles

Anthocoridae A family of bugs (order Hemiptera). They sometimes are called minute pirate bugs.  Bugs

Anthomyiid Flies Members of the family Anthomyiidae (order Diptera).  Flies

Anthomyiidae A family of flies (order Diptera). They commonly are known as anthomyiid flies or root maggots.  Flies

Anthomyzid Flies Members of the family Anthomyzidae (order Diptera).  Flies

Anthomyzidae A family of flies (order Diptera). They commonly are known as anthomyzid flies.  Flies

Anthophilous Flower loving. Most insects that feed on nectar or pollen are anthophilous, including many

utterflies and moths (Lepidoptera), wasps, ants b and bees (Hymenoptera), but also numerous flies (Diptera), beetles (Coleoptera) and thrips (Thysanoptera).  Pollination and Flower Visitation  Butterfly Gardening  Night Blooming Plants and their Insect Pollinators  Pollination by Yucca Moths  Apiculture  Plant Extrafloral Nectaries

Anthribidae A family of beetles (order Coleoptera). They commonly are known as fungus beetles.  Beetles

Anthrophagy Feeding on humans by other organisms. The most common anthrophagous organisms are insects, particularly biting flies, followed by lice, fleas, and ticks.  Mosquitoes  Lice  Fleas  Ticks  Pathogen Transmission by Arthropods

Anthrophoridae A family of bees (order Hymenoptera, superfamily Apoidae). They commonly are called cuckoo bees, digger bees, and carpenter bees.  Bees, Wasps, Ants and Sawflies

Anthropocentric An interpretation based on the belief that humans are the central fact or element of the universe,

Antlions

and interpreting everything in relation to human values of interests.

Anthropomorphism The attribution of human qualities or forms to animals or their behaviors.

Anthropophilic An insect that prefers humans as a source of food. A blood-sucking insect that feeds on humans.

Antibiosis A characteristic, often a chemical within a plant, that inhibits survival or reproduction when an insect feeds upon it.  Plant Resistance to Insects

Antibiotic A chemical produced by a microorganism that affects the ability of another microorganism to survive or grow.

Anticodon The triplet of nucleotides in a transfer RNA molecule that is complementary to and base pairs with a codon in a messenger RNA.

Antidote A treatment used to treat the effects of chemical (e.g., insecticidal) poisoning.

Antidiuretic Hormones Hormones acting on the hindgut to promote water reabsorption and conservation.

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Anti-Drift Agent A compound that is added to pesticides to reduce the number of droplets produced at the spray nozzle, and therefore to reduce the possibility of the product drifting away from the target.

Antixenosis An effect due to a characteristic, often a physical or chemical attribute of a plant, that deters feeding or oviposition. This is also called nonpreference.  Plant Resistance to Insects

Antlike Flower Beetles Members of the family Anthicidae (order Coleoptera).  Beetles

Antlike Leaf Beetles Members of Coleoptera).  Beetles

the

family

Aderidae

(order

Antlike Stone Beetles Members of the family Scydmaenidae (order Coleoptera).  Beetles

Antlions Members of the family Myrmeleontidae (order Neuroptera).  Lacewings, Antlions and Mantidflies

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Ant-plant Interactions

Ant-plant Interactions diane w. davidson University of Utah, Salt Lake City, UT, USA Drop a spoon at a picnic and the ubiquity of ants (family Formicidae) is soon apparent. Ants are everywhere, lurking in leaf litter or brazenly scouring terrestrial and arboreal habitats for food in any form. Except in extreme climates that are inhospitable to insects, most terrestrial organisms have necessarily evolved ways to reduce the damage ants can cause, and many have managed even to extract benefits from them. Relationships between ants and humans provide examples: not only have we devised means of protecting our food stores from ants, but we have utilized ants to protect our food. Centuries ago, nests of Old World weaver ants (Oecophylla smaragdina) were cultivated in Asian orchards to control plant pests. Workers of this highly predatory species captured and devoured both the juvenile and adult stages of herbivorous (plant-eating) insects. In some ways, early ants were better suited to serve plants than to injure them. Descended from predatory wasps, they were poorly adapted for herbivory (consumption of plant tissues), and no ant is truly folivorous (leaf-eating). Unable to digest cellulose themselves, ants also differ from termites in lacking gut microbes that can do this for them. Although much of the plant world is therefore not available to ants, plant sap, seeds, and fruit pulp are relatively easy to digest, and many (mostly arboreal) taxa feed on those resources. Such foods tend to be rich in carbohydrate (CHO) but poor in nitrogen (N) (amino acids, peptides and proteins), and dietary excesses of energy-rich CHOs may have subsidized colonization of the arboreal zone, where foragers must commute around a three-dimensional and poorly connected environment. Most ants also scavenge N-rich arthropod carrion, and many are active predators that can potentially benefit plants by attacking their herbivores. In some taxa, associations with intracellular and extracellular gut

microbes contribute to the colony’s N economy through N-recycling and possibly upgrading (conversion of non-essential to essential amino acids). When disturbed by ants, many active insects and other animals can simply fly or walk to safety, but for plants and their seeds, as well as for comparatively immobile nesting animals and juvenile insects, there are no ready escape routes. It is in these organisms that we find some of the most unique or unusual adaptations for both defending against ants and exploiting their behaviors to advantage. Here, several categories of interactions between ants and plants are explored, together with some of the myriad ways in which plants have evolved to reduce or promote association with these ubiquitous insects. Included also are the influence of plant resources on ant ecology and evolution, and the effects of ants on the evolution of plant defenses.

Ants as Seed Predators In warm deserts and other arid regions, ants are often both abundant and diverse, and annual and perennial plants are present more often as seeds than as adults. Here, seed-eating ants abound and may exert strong selection pressures on plant. Selection is mediated mainly by seed consumption, but also by ant effects on soil disturbance and nutrient availability. Seed-eating “harvester ants” typically return seeds individually to a central nest site where they husk and then cache them in underground granaries, often for long time periods. By storing foods that degrade slowly over time, ant colonies can persist in habitats where the production of seeds and other resources is sporadic and unpredictable. During periods of low food availability, many of these ants simply remain underground and forego the risks and poor rewards of external activity. The small individual sizes and ectothermy of ants are correlated with low foraging costs, enabling these insects to forage economically even for tiny seeds with dispersed distributions. Ants can


Ant-plant Interactions, Figure 53 An extensive nest of leaf-cutter ants in the genus Atta (above) and high rates of leaf removal from an unlucky tree (below).

therefore reduce soil seed banks to lower levels than can large, endothermic (“warm-blooded”)

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vertebrate seed-eaters like rodents and birds. Those taxa have higher foraging costs and tend to specialize in feeding on seeds in high density “hotspots,” either in soils or on the plants themselves. Though reduced seed densities can potentially affect both plant densities and community composition, ants may commonly have less impact on plant communities than do vertebrate seed predators. This is so because seed predation by ants tends to fall most heavily on offspring of small-seeded plant species, whereas that by vertebrates often targets large seeds. Seedlings germinating from large seeds begin life with more resources than do those from small seeds and are therefore superior competitors within plant communities. Consequently, the removal of small seeds by ants has comparatively little effect on the densities of large-seeded species, while the removal of large seeds by rodents may lead to increases in the densities of small-seeded species. In at least some localities, differences in seed size specialization by ants and rodents account for disparities in the short-term and long-term effects of these granivores on one another’s populations. When seed-eating rodents were removed experimentally in one study, densities of harvester ants first increased and then declined. The short-term increase was likely due to competition between the two types of granivores, as there was some overlap in the sizes and species of seeds used by the two groups. However, rodent removal eventually led to increases in the densities of large-seeded plants, which subsequently out-competed smallseeded species, to the long-term detriment of ants. Coexisting species of harvester ants often differ in worker body sizes, and small ants cannot carry the largest seeds. To a degree, therefore, worker size differences may remove small and large ants from resource competition with one another, and also determine disparate effects on plant communities. When ant communities are disturbed, either directly or by the introduction of non-native ants, there can be consequences for plant communities. Pathways of interaction can be

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indirect and complex. For example, if an introduced ant species produces a decline in populations of a native harvester ant, plant species on which the native ants specialize may increase at the expense of other components of the plant community. Such changes in community composition are hard to predict, and often become apparent only over long time periods, especially in arid lands with variable climates. On an evolutionary time scale, some plants have acquired adaptation that reduce depredation of their progeny by ants. An example of such an adaptation is the use of hygroscopic awns (e.g., that of Erodium cicutarium) that alternately extend and coil when wet and dry, respectively, pushing the attached seeds beneath the soil surface. Unlike seed-eating rodents, harvester ants have little access to individually buried seeds, so such awns do appear to proffer a refuge from predation by granivorous ants. Whether mechanical, chemical, or phenological (e.g., timing of seed production), mechanisms of seed escape from granivorous ants remain poorly explored.

Early “Farmers” (Attines) To the uninitiated, the cutting and transport of leaf, flower and fruit fragments by New World ants in the tribe Attini looks a great deal like herbivory (Fig. 53). However, as was originally proposed by Thomas Belt, a nineteenth century British mining engineer and amateur naturalist, the ants themselves do not digest cut leaves. Rather, they cultivate fungi that degrade cellulose and other plant products otherwise inaccessible to the ants. In more recent members of this group (species of Atta and Acromyrmex), the workers themselves feed on plant sap released from cut leaves, whereas larvae are fed gonglydia, or swollen tips of fungal hyphae (arms). Together, fungal mycelia and gongylidia supply CHOs (simple sugars, as well as glycogen in Acromyrmex), lipids and N (amino acids and protein). On her nuptial flight, the queen carries fragments of fungal gardens in her infrabuccal chamber,

adjacent to the anterior digestive tract in the head. After mating, she removes her wings, excavates a terrestrial nest, begins to cultivate her fungal garden, and feeds her first worker brood on trophic eggs composed of resources from her degraded wing muscles. Workers eventually take over cultivation and maintenance of the fungal gardens. Larger castes cut, drop, and carry the leaf fragments, while their smaller nestmates “hitch-hike” rides on leaf fragments to defend larger workers against parasitic phorid flies, and care for brood inside the nest. There, they lick and shred leaf fragments into finer pieces, and then chew their edges, depositing fecal droppings with digestive enzymes to aid in decomposition. Protein-degrading enzymes are recycled from the fungi themselves through the ant’s digestive system, which lacks enzymes to degrade them. New leaf fragments are then inoculated with mycelia of older parts of the garden and fertilized with plant material (recent attines) and/or feces and animal matter (early attines). Through application of growth hormones, enzymes, nutrients, and antibiotics, higher attines maintain their fungi almost in monocultures. Nevertheless, recent studies by M. Poulsen, C.R. Currie, and colleagues have identified a virulent fungal pathogen of the gardens, as well as a bacterium living in fovea (small depressions) in worker exoskeleton. These filamentous bacteria, or actinomycetes, produce antibiotics directed mainly toward the common pathogen. Although most folivorous insects are limited to eating a narrow spectrum of plant species, use of fungi as agents of digestion may explain leafcutter tolerance of more varied diets. Nevertheless, different taxa of higher attines specialize on grasses or dicots, and specialization exists even within those categories. Like other herbivores, leafcutters are especially likely to harvest tender young leaves, which lack the fiber and lignin to make them tough. For Atta cephalotes, J.J. Howard and colleagues showed that, the diet is apparently not chosen in response to energy, nitrogen, or moisture content,


but rather to avoid various terpenoids that could poison fungi. According to U.G. Mueller and colleagues, all attines appear to have descended from a common ancestor that forged relationships with fungi either growing on walls of leaf-litter nests or using ants to disperse their spores. Together, with gene sequence data, the fossil record, and confinement of this group to the New World, suggests that this ant-fungal partnership first formed between 45 and 65 million years ago. Direct transmission of fungi from queens to reproductive daughters provided opportunities for greater specialization and dependency to evolve in both partners. Nevertheless, new fungal species have also been domesticated by older, less specialized ant taxa in recent times. The success of the attine-fungal partnership is measurable in its impact on the forest. Mature Atta nests can range over several hundreds of square meters, and worker columns can reach trees more than 100 m from the colony along trails cleared of vegetation. In tropical areas not regularly flooded, attines can be very abundant and exact a considerable toll on plants. Some accounts in the literature judge them to be responsible for 12–17% of all herbivory, but these figures may be too high because they fail to include the mostly invisible losses of plant resources to sap-feeding insects. Throughout much of the Neotropics, higher attines also thrive in disturbed areas dominated by poorly defended pioneer (weedy) plant species. They are similarly destructive to agriculture, and cause millions of dollars in losses annually to crop plants that have been selected by humans for low toxicity.

Pastoralists Ants may also affect plants indirectly through the farming (or “tending”) of insects in the order Hemiptera. With mouthparts highly modified as stylets, or “soda straws,” these insects are phloem- or xylem-sucking consumers of plant sap (Fig. 54) and

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Ant-plant Interactions, Figure 54 Ants tending Hemiptera outside and inside plant stems: (above) Azteca tending mealy bugs ( Pseudococcidae) in the New World tropics, and (below) Podomyrma sp. tending scale insects (Coccidae, arrows) inside branches of Chisocheton (Meliaceae) near Madang, Papua New Guinea.

include aphids, leafhoppers, treehoppers, scale insects, and the like. Because plant sap is N-poor, sapfeeding hemipterans must process large quantities of these liquids to concentrate sufficient nitrogen for

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growth and reproduction. Moreover, while they feed, their relatively immobile immature or nymphal stages are exposed for long time periods to the risks of predation and parasitism. As a by-product of processing large quantities of sap for N, many Hemiptera release excess sugars as “honeydew” from their abdomens. When compensated by this attractive resource, ants forego predation of these insects and even protect them from other natural enemies. Relatively N-rich tissues like young leaves, and the pedicels of flowers and fruits, are particularly good sites for sapfeeders and the ants which herd them there. In Asian rain forests, where plant reproduction is highly sporadic, ants in the genus Dolichoderus have evolved as “migratory herdsmen,” carrying their sap-feeding mealy bugs over long distances in search of optimal feeding sites. Hemipteran tending, often compared to human tending of domestic livestock, is a mainstay for many arboreal ants. Still, to balance their diets, ants occasionally harvest some of the tender hemipteran nymphs and consume N-containing hemolymph of these and other arthropods. The relative strengths of positive and negative effects of the ants (herbivore reduction vs. hemipteran tending) determine the net effect of ants on a plant’s well-being and reproduction (i.e., its fitness).

This net outcome can be positive if herbivores are abundant and tending ants are effective in driving them away. However, as hemipteran populations thrive and grow under ant protection, removal of large quantities of sap can threaten the host plant’s health. Living in intimate contact with hosts, Hemiptera also transmit viral and other plant pathogens. Not surprisingly then, plants appear to have fought back over evolutionary time. For example, hairs (trichomes) on leaves or stems prevent hemipteran stylets from reaching the plant surface. Other evolved responses are best understood in the context of the old adage that “the enemy of my enemy is my friend.” Thus, many plants may have short-circuited the Hemiptera out of these tripartite interactions by paying the ants directly, i.e., by provisioning them with carbohydrate rewards in the form of sugar-rich extrafloral nectars (EFNs, Fig. 55) or lipid-rich pearl bodies (PBs). J.X. Beccera and D.L. Venable hypothesize that by increasing the CHO:protein ratio in the ants’ own diets, plants induce ants to consume more of their Hemiptera. Arguing against this hypothesis for the origin of EFNs are observations of ants tending both sap-feeders and EFNs. Despite such observations, D.W. Davidson and colleagues have proposed that the hypothesis might help to

Ant-plant Interactions,Figure 55 Myrmecophyte-produced food rewards for ants: (left) Extrafloral nectaries (EFNs) at the junction of leaf blade and petiole of Endospermum medullosum (Euphorbiaceae) near Madang, Papua New Guinea; (right) pearl bodies (PBs) on lower leaf surface of Cecropia engleriana (Cecropiaceae) at Cocha Cashu, Peru. Both EFNs and PBs also occur in myrmecophilic plants.


explain early divergence in foraging habits of major ant taxa that differ in their propensity to tend hemiptera versus EFNs.

Biotic Defenses of Plants Even in relationships not (or no longer) involving Hemiptera, production of ant attractant foods should increase the presence of ants on vegetative and reproductive plant tissues and help to deter a variety of insect and other herbivores. Plant adaptations for defense by ants, wasps and other potential predators of insect herbivores are referred to as “biotic defenses,” since they require the collaboration of other living things.

Some Definitions and Constructs Whether the anti-herbivore protection of plants by ants is afforded through consumption of Hemiptera or deterrence of other herbivores, such protection completes the requirement for what are termed “mutualistic” interactions. Both parties in these relationships benefit, the ants directly from plant

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provisioning of resources, and the plants indirectly, usually through deterrence of damaging herbivores. Mostly, these interactions are opportunistic and unspecialized, depending on which ants, herbivores, and plants co-occur within a community. Plants with opportunistic ant associations based on production of food rewards alone are said to be “myrmecophilic” or “ant-loving.” In contrast, at tropical latitudes, many ant-plant relationships have become more highly specialized and obligatory. That is, in the context of their natural communities, partners cannot survive and reproduce in the absence of their associates. In this case, resident “phytoecious” ants protect their host plants, (Fig. 56) and “myrmecophytes” (true “ant-plants”) provide not only food but housing in stem or leaf structures termed “domatia.” Individual ant colonies and myrmecophytes may live together over substantial portions of their life histories in relationships therefore termed “symbiotic mutualisms.” (Although often used incorrectly in place of “mutualism,” the term “symbiosis” - literally “living together” - is value neutral, including negative interactions like parasitism, as well as mutually beneficial interactions.) “Cheater” ants, which benefit plants less than the evolved partner, or otherwise negatively

Ant-plant Interactions, Figure 56 Caulinary (left) and foliar (right) domatia of ant-plants. Forming the domatia of many myrmecophytes are swollen stems or support structures, either naturally hollow or with weak pith, removed by ants. Shown here (left) is a branch of Duroia hirsuta (Rubiaceae, vic. Iquitos, Peru), swollen at attachment of large opposite leaves. Tiny ants in genus Myrmelachista inhabit these n aturally hollow caulinary domatia. Foliar domatia, like that shown here for Tococa sp. (Melastomataceae, from Cocha Cashu, Peru) (right) are highly modified and more obviously evolved to accommodate ants.

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impact hosts, may occasionally prevail in sym bioses because they are better colonists or competitors. In symbiotic ant-plant relationships, partners are more likely to have undergone coevolution, i.e., reciprocal genetic (evolutionary) responses to selection pressures exerted by each partner on the other. Coevolution has two aspects: coadaptation and cospeciation, and only the former occurs frequently in symbiotic ant-plant partnerships. Illustrating coadaptation (reciprocal adaptation), many plants have evolved restrictive (Fig. 57) entrances to their domatia as a means of favoring colonization by certain ant taxa over others, while queens of phytoecious ants have responded by evolving traits enabling them to recognize and colonize such entrances expeditiously. Similarly, plants and ants may have coadapted with respect to the types or sizes of food rewards offered (Fig. 58) and their utilization or accessibility. In contrast, cospeciation (the co-radiation of ant and plant lineages to give congruent phylogenies) appears to be quite rare even in tropical symbiotic ant-plant relationships. Rarity likely results from the fact that ant and plant propagules (i.e., new queens and seeds) disperse independently, leaving much opportunity for new partnerships to form over evolutionary time. Seeds must germinate and produce seedlings of a threshold size before the next generation of hosts can support ant colonies. Environmental variation or randomness in the abundances of, and proximities

Ant-plant Interactions, Figure 57 The prostomata (stem entrances) of Cecropia species come in various sizes and forms correlated with host use by different ant taxa: Cecropia engleriana (above) produces a narrow inverted prostoma, recognized and colonized by comparatively small queens of Azteca australis (Dolichoderinae) (center); in c ontrast (below), those of Cecropia sp. nov (“pungara”) are convex and covered in u rticating hairs; this host species attracts much larger queens of a ponerine ant, P achycondyla luteola. Both photos are from Cocha Cashu, Peru.


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Ant-plant Interactions, Figure 59 A hypothetical case of cospeciation, illustrated by the congruent or mirror-image phylogenies (= genealogies, solid dark lines) of associated (dotted lines) ant and plant taxa. On each occasion when a plant species splits into two distinct taxa, the associated ant lineage also undergoes a speciation event. For cospeciation to have occurred, splits in plant and ant lineages must have occurred contemporaneously and be attributable to selection imposed by the partner. Otherwise, an ant lineage may have just radiated secondarily over a pre-existing plant lineage. The dotted and grey lines depict two kinds of evolutionary colonization events: respectively, host switching and de novo colonization by a previously unassociated ant lineage.

Ant-plant Interactions, Figure 58 Food bodies of myrmecophytic Cecropia also come in different sizes, as shown here for Cecropia membranacea (above), usually associated with tiny Azteca ants, and closely related Cecropia sp. nov. (“pungara”) (below), housing the much larger Pachycondyla luteola. Both are from at Cocha Cashu, Peru.

to, sources of colonizing queens, provide ample opportunity for host-switching or de novo colonization by previously uninvolved ant taxa. This

icture contrasts sharply with that for, e.g., higher p attines and their fungi; there, I.H. Chapela and colleagues have shown that queens transmit fungi between generations of colonies, and phylogenies of the two lineages are largely congruent (Fig. 59). Despite little evidence for cospeciation in symbiotic ant-plant associations, contemporaneous diversification within partner lineages may occur through diffuse coevolution, defined by D.H. Janzen as reciprocal evolutionary responses to a suite of potential partners. Additionally, if host availability were often limiting, phytoecious ants may frequently have colonized non-myrmecophytic relatives of those plants, exerting new selection on these species to evolve ant-attractive traits. Based on multiple independent origins of myrmecophytism in older and more recent Asian Macaranga, S.-P. Quek and colleagues have proposed just such a scenario. A parallel argument is that, lacking their typical associates, habitat-switching hosts could

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have provided evolutionary opportunity for the origin of new phytoecious ant taxa. These examples are relevant in the context of the different selection pressures driving diversification in myrmecophytes versus phytoecious ants. As noted by D.W. Davidson and D. McKey, proliferation of plant species has been driven principally by colonization of new habitats, accompanied by evolution of new defensive strategies and (correlated) growth rates, etc. In contrast, ants have diversified mainly in response to biogeographic factors and (especially) plant traits favoring certain associates over others (below). Why this asymmetry? Plants grow through seedling stages without their ants, and their success during this most vulnerable period depends on factors such as light and nutrient regimes, i.e., on habitat. Additionally, any of several ant taxa may provide acceptable protection against herbivores. In contrast, phytoecious ants are typically restricted to their hosts throughout the life history, and disparities in host characteristics (e.g., habitat-correlated growth rates and investment in biotic defense) should be highly consequential. This asymmetry in selection pressures is reflected in both the specificity of partnerships and evidence for coadaptation. Individual Cecropia species can house ants in different genera or even sub-families, while associated ants do not inhabit plants outside this genus. Similarly, phytoecious ants of bamboos have adapted to these hosts by evolving means of water evacuation from nest culms (active bailing or passive engineering), and they do not live elsewhere. In contrast, no bamboo has been determined to have evolved ant attractants.

Factors Driving Evolutionary Specialization Factors driving evolutionary specialization in phytoecious ants are apparent from assessing both the taxonomic affiliations of these ants and traits of coadapted partners. Despite the frequent impression that such ants are ferociously aggressive

against vertebrates (including many an unfortunate investigator), they appear often to include comparatively weakly competitive ant taxa that persist only in association with myrmecophytes. Several plant traits, separately or in combination, contribute to the capacity of these plants to serve as refugia from natural enemies. First, many myrmecophytes produce nutritionally complete food rewards that eliminate the need for resident ants to forage in more competitive environments off their hosts. Acacia and Macaranga are examples. Second, derived from taxa in which stem hairs are common, a number of myrmecophytes possess stems and domatia covered with long, dense hairs (trichomes, Fig. 55) that exclude larger-bodied enemy ants, competitors and perhaps predatory army ants, while permitting tiny resident taxa to commute among them. Such hosts include Cordia nodosa, Duroia hirsuta, and Hirtella spp., with tiny Allomerus and Azteca ants, as well as a variety of myrmecophytic Melastomataceae. Third, many myrmecophytes, e.g., Macaranga and Cecropia, grow as little-branched, pole-like plants with few points of contact over which enemy ants might invade from neighboring vegetation. Fourth, the mutualism between ants and Macaranga has been shown by S.-P. Quek, S.J. Davies, and colleagues to have originated on hosts with irregular “wax blooms” on stems. Many insects, including most ants, have difficulty walking on epicuticular waxes, but as W. Federle and colleagues have demonstrated, “wax-running” ants in at least two genera (Crematogaster and Camponotus) evolved to utilize the slippery hosts. During the co-radiation of plant and Crematogaster lineages, stem types (waxy or smooth) continued to constrain host shifts. All of the previously described traits are attributes that likely preadapted plants to associate with competitively inferior ants searching for sanctuary. In addition, phytoecious ants themselves have often evolved to reduce interaction with enemies by pruning vines and other vegetation contacting their hosts. (This behavior may coincidentally enhance the host’s light environment.) At least one such ant species (Pseudomyrmex dendroicus on


Triplaris americana) even prunes leaves of its own host when they bear invasions of enemy ants. In the Neotropics, a majority of pruning ants defend themselves using proteinaceous stings, which tend to be very effective against vertebrate enemies, but less effective than chemical sprays against social insect enemies, including many other arboreal ant taxa. Also suggesting that pruning evolved to limit invasions of competitors, Federle and colleagues find that ant taxa living on waxy-stemmed Macaranga hosts do not prune as intensively as do those inhabiting more recent non-waxy species. The latter ants are also more recent, and the evolution of pruning in ants may have benefited host plants by reducing the cost of epicuticular waxes. The advent of pruning coincides with a switch to more generalized host associations, as ant taxa from waxy stem hosts expanded their host ranges to non-waxy hosts. Finally, M. Frederickson has shown that phytoecious ants best at pruning are not always those that are best at protecting plants from herbivores. Therefore, a myrmecophyte’s failure to filter out supposed “cheaters” that didn’t prune may be due to alternative benefits provided by the ant species in question.

Conflicts of Interest between Partners As for partners in virtually all interspecific interactions, the evolutionary interests of paired ants and plants are often in conflict. For example, although selection may favor ant colonies that extract the maximum resource possible from their hosts (e.g., by tending sap-feeders, as well as consuming plant-produced ant rewards), selection on plants should magnify cost-efficiency by producing the greatest protection for the least investment in resources devoted to housing and feeding of ants. The most striking examples of evolutionary conflicts of interest come from cases where ants modify plant architecture in ways that are beneficial to them but harmful to their hosts. Working in African savannahs, M.L. Stanton and colleagues have shown that Crematogaster nigriceps attacks

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the axillary buds of its host (Acacia drepanolobium), killing apical meristems (growing tips) and greatly curtailing host reproduction in the process. However, by reducing lateral spread, destruction of meristems may also diminish potential contacts between branches of hosts and those of neighboring acacias, some with competitively superior ants that threaten resident colonies. Tetraponera penzigi, a second, competitively subordinate occupant destroys EFNs of its host, perhaps making it less attractive to more dominant ants on neighboring hosts. Similar conflicts of interest are apparent in neotropical ant-plant relationships. The most common inhabitant of Cordia nodosa in southeastern Peru is an Allomerus that destroys flowers and fruits of its host. D.W. Yu and N.E. Pierce have shown that ant fecundity is greater on plants with curtailed reproduction, because hosts produce more domatia and associated leaves, sites of food body production. Cordia populations might be expected to decline to local extinction under such “cheating” by Allomerus, but Yu and colleagues have also demonstrated that alternative and beneficial Azteca ants are better long-distance colonists, and that the frequency of association with these ants increases as plant density declines. Finally, T.J. Izzo and H.L. Vasconcelos report that selection on plants to fight back under similar circumstances is apparent in relationships between Allomerus and another Amazonian ant plant, Hirtella myrmecophila. Reproductive structures of this understory treelet are produced only on older branches from which leaf domatia have been aborted, and where worker ants are therefore few or absent.

Long-Term Evolutionary Histories of Ant-Plant Associations Over long-term evolutionary history, one can expect “ownership” of host taxa to have changed hands in concert with changes in the fortunes of one-time ant partners and their competitors for the benefits of mutualistic association. Are there regularities in the

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trajectories that these relationships take over time? One might speculate that competition among ants for plants, together with filtering of ants by plants, could produce even greater specialization by the associated taxa, and that this might be a one-way and largely irreversible process. For ants, possible examples involve several closely related genera of tropical arboreal, stem-nesting ants in the formicine tribe Plagiolepidini. (Together, these genera are set apart from others in the tribe by workers possessing just 9 or 10 antennal segments.) Two Old World tropical genera, Petalomyrmex and Aphomomyrmex, are each represented by just a single West African species and are specialized to one and two host plant species, respectively. Because the probable closest relatives of these taxa (Myrmelachista and Brachymyrmex) occur as free-living species in the New World, it seems likely that ancestors of the African species were once free-living and more widely distributed, and that competition could have driven Petalomyrmex and Aphomomyrmex to extreme specialization. The genus Myrmelachista includes both free-living and plant-associated species. On average, the former (mainly with 10-segmented worker antennae) have generalized foraging and stem-nesting habits and reside mainly in high elevation cloud forests along the Andean and Central American mountain chains, normally above the elevational ranges of dominant free-living competitors in ant genera Crematogaster and Azteca. At intermediate and low elevations, and within the ranges of these dominants, J.T. Longino has found that congeneric species are mostly phytoecious ants, principally inhabiting hosts in plant families Lauraceae and Meliaceae. Myrmelachista hosts generally lack domatia and food rewards (i.e., are not true myrmecophytes), and associated ants tend sap- feeders inside stem nests. At least some phytoecious Myrmelachista occurring at intermediate elevations apparently do not attack encircling vines, though a congeneric species at lower elevations (likely M. flavocotea in a more competitive environment) does prune vegetation contacting its host. Finally, in Central Amazonia, at least two different Myrmelachista species occupy and maintain

“supay chacras,” or “devil gardens.” These are orchard-like stands where all but one or two myrmecophytes (and sometimes small, herbaceous resource plants) are killed by the tiny workers that cut major leaf veins and deposit formic acid in the wounds. Leaves necrose and die, and none but favored host and resource plants are able to recruit new individuals inside these bizarre areas. In summary, it is possible that basal Myrmelachista species persist only in the absence of strong competitors, or where competitively dominant ant taxa have driven lowland lineages toward increasing specialization that permits coexistence with strong competitors. However, this hypothesis will remain conjecture until tested rigorously after reconstructing phylogenetic histories of associated lineages. Natural selection to magnify the colonizing and competitive abilities of particular ant associates, coupled with that to filter cheaters, may eventually reduce partnerships to relationships between single, highly specialized ant and plant species, whose persistence is balanced precariously on the premise that each partner will thrive despite changes in the abiotic (physical) and biotic environment. However, natural selection is shortsighted, capable only of enhancing short-term fitness. Over the long term, it can neither anticipate nor respond to the threat of loss of the sole partner. Therefore, it is reasonable to speculate that fewer than all of the ant-plant associations that have ever existed still exist today. Nevertheless, the most thoroughly studied evolutionary trajectories of phytoecious ants are those described by S.-P. Quek and colleagues for Crematogaster of Macaranga, and show wax runners breaking away from hosts with waxy stems to occupy plants that should constitute a more competitive environment.

Implications of Exudate-Feeding for the Evolutionary Ecology of Ants The most conspicuous effects of plants on ant ecology and evolution involve phytoecious ants whose


colonies are specialized to live their entire life histories on myrmecophytic plants. However, more generally, plants appear to have markedly influenced the biology of ant taxa feeding substantially as “herbivores,” either directly on plant wound secretions and EFN, and/or indirectly, on insect honeydew. Such foods, collectively termed “exudates,” consist principally of sugars (EFN) and water and are notoriously poor sources of essential amino acids and proteins. Though a certain amount of carbohydrate might be paired with available nitrogen sources as the “nutritionally complete food” needed to subsidize growth and reproduction, exudate-feeders should be left with an “excess” of CHOs. Natural selection may then favor colonies that are able to deploy excess CHO for acquisition of more limiting nutrient, N. Across the spectrum of exudate-feeding ants, species appear to accomplish this in one or more of several ways. First, they may use excess CHOs to subsidize rapid locomotion, leading to what have been termed higher “dynamic densities.” Faster locomotion enables workers to cover more area per unit time, and potentially, to encounter protein resources at a faster rate. Second, defense of true spatial territories is rare among ants generally, but appears to be commonest in species most apt to have excess CHOs to fund this costly behavior. Third, N-starved ants may also reduce percent body weight N, though there are competing explanations for this pattern. Thus, evolutionary transitions from predation and scavenging to substantial dependence on plant and insect exudates correlate with transitions in chemical weaponry. N-rich proteinaceous compounds, or N-containing alkaloidal compounds (both mediated by stings) are replaced by N-free compounds released as volatile sprays or sticky glues from the same or different glands. Whether such transitions are due to N-limitation, or the ineffective nature of C-based weaponry in killing or paralyzing prey, is currently unsettled. By “paying” ants mainly in CHO-rich food rewards, myrmecophilic and myrmecophytic plants may encourage predatory behavior by attending ants seeking to balance their diets

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(above). Recently, D.W. Davidson and S.C. Cook found that rainforest plants supply EFN at sugar concentrations far exceeding those acceptable to most arboreal ants. They therefore suggest that high sugar concentrations may serve to manipulate communities of attending ants by favoring the most protein-limited taxa that would not forage for sugar at lower concentration. Finally, widespread availability of CHO-rich plant foods in the arboreal zone undoubtedly selected for domination of these foods by placing nests near the food source. For ants already nesting in leaf-litter twigs, this transition may not have been difficult, but appropriate cavity space would not always have been available. Many arboreal ant taxa have therefore evolved the capacity to construct their own nests from carton, silk, or leaves cemented to one another to create cavity space.

Some Parallels Between Ants and Plants A central theme running through this article has been that the balance of resources accessible to animals (Hemiptera and ants) affects the evolutionary ecology of these organisms by determining the types of resources available for various organismal functions. This argument is no less true for myrmecophytic plants and, in fact, was adopted by ant biologists based on its explanatory power in plants. In rainforest plants, for example, E.W. Schupp and D.H. Feener have shown that Nfree but carbon-rich food rewards for ants (EFNs and PBs) are more typical of taxa growing in disturbed habitats under high light, than of groups typical of the dark forest understory. Apparently, high rates of carbon-gain in open habitats enable plants to divert some of that carbon to defense. A second reason why biotic defenses may occur at high frequency in fast-growing, “pioneer” species of disturbed sites may relate to the shorter average leaf life spans of those species. D. McKey has argued persuasively that shorter leaf life spans should favor foliar defenses that are “reclaimable,”

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i.e., can be diverted from aging leaves to more valuable young leaves as time passes. In contrast, much higher, but one-time, investment in nonreclaimable defenses (e.g., the lignin and fiber contributing to leaf toughness) are warranted only when the life expectancy of leaves is relatively long. One can speculate that the pattern in plants might also be applied to predict aspects of ant biology. For example, a substantial, one-time investment in producing thicker (N-rich) exoskeleton might only be warranted in ant species with long-lived workers. This interesting hypothesis has yet to be tested. Two final patterns in defensive investment are apparent in at least some myrmecophytic plants, and may extend as well to ants and other social insects. Comparing closely-related pairs of Cecropia species from different microhabitats at the same rainforest site, it appears that relatively slowgrowing taxa from shaded habitats invest in biotic defenses both earlier and more heavily than do their faster-growing relatives from sunny habitats. The latter pattern is understandable in the context of a cost-benefit analysis of defense. For species growing regularly at low light, leaf replacement is very slow due to resource limitation, so plants ought to defend existing leaves well. Moreover, any opportunity cost of defense (calculated in lost growth, survivorship, and reproduction) would be low in comparison to that for species capable of growing rapidly in high light. The combination of high replacement costs and low opportunity costs is thought to select for high defensive investment. (Applied to ants, this pattern suggests the currently untested hypothesis that mean colony growth rates are inversely related to defensive investment in individual workers.) C. Brouat and D. McKey have argued that, in myrmecophyte lineages with interspecific variation in developmental onset of biotic defense, precocious (early) onset should be the derived state; however, few data are available to test this prediction. Others have suggested that costly chemical defenses produced early in development should be abandoned after onset of biotic defense, but recent tests in genera

Acacia and Inga contradict this theory, and suggest that chemical and biotic defenses may be targeted at different types of herbivores. With respect to ants and other social insects, parallel reasoning might predict an inverse relationship between colony growth rate and investment in defense of incipient (young) colonies. One form of protection for young colonies is production of “nanitic” workers, scaled-down in size. This strategy enables young colonies to make more workers from a given resource base, and to spread the risks of foraging over more individuals. Are young workers smaller relative to normal workers in otherwise comparable species with intrinsically slow growth rates? Again, relevant data are lacking. In summary, ant colonies and plants share some intriguing features that make models developed in one taxon potentially useful to investigators of the other taxon. Both types of organisms live anchored to a central place (not perfectly true for ants), grow to indeterminate size set by local resource availability, and add vegetative and reproductive parts in a modular way. These commonalities suggest that we might eventually discover additional models that are useful in explaining life history traits and other characters shared by the two groups.

Nutritional Benefits to Plants (Myrmecotrophy) Among plants evolving associations with benevolent ants are certain epiphytic higher plants. Depending on trunks and branches of other plant species for structural support, epiphytes grow without directly parasitizing their hosts and obtain water and nutrients from rainfall and aerial deposition. Because high humidity and warm temperatures are conducive to this lifestyle, epiphytic higher plants are exceptionally diverse and abundant in tropical lowland wet forests, and (especially) in misty montane forests. (Tropical Africa is exceptional in this regard, due to frequent and


severe droughts during the evolutionary histories of its plant life, and small expanses of montane forests in contemporary times.) By virtue of small size, these unrooted plants stand to benefit significantly from even small quantities of nutrients amassed as workers retrieve prey, discard refuse, and defecate within a confined area. From a mix of vegetable fiber, glandular secretions, refuse, and feces, many ants build “carton” shelters (for themselves and tended Hemiptera), and carton can potentially contribute to plant nutrition. Two categories of plants, New World “ant- garden” epiphytes and Australasian “ant-house” epiphytes, have evolved a variety of traits that increase frequency and intimacy of relationships with beneficial ants. To encourage seed dispersal to nutrient hotspots in ant nests and carton, both sets of species produce seeds with attractive chemicals and/or food bodies. The common occurrence of methyl-6-methyl-salicylate on seeds of 11 unrelated ant-garden epiphytes, combined with the use of these same compounds as pheromones (withinspecies communication chemicals), suggests that this chemical could function as an ant attractant. Generations of seed dispersal by ants appears to have allowed ants to “capture” the evolution of their epiphytes, just as humans have captured and diverted the evolutionary histories of their crop species. (Alternatively, in both of these systems, plants may have captured and diverted the evolutionary histories of their gardeners!) The successes of ant-epiphyte partnerships are evident from their often remarkable abundances. Ant gardens can account for the majority of epiphytic higher plants in forests with a distinct dry season, and ant-house plants dominate the epiphytic floras of open kerangas forests in Asia. Whereas other epiphytes cannot survive extended periods of drought, ant-garden taxa benefit from moisture absorbed from the air and stored in the rich, organic ant cartons. Ant-house epiphytes have evolved even more elaborate adaptations to procure benefits from their ant inhabitants. Those in the sub-family Hydnophytinae (Family, Rubiaceae) are descended from tuberous ancestors whose storage tissues

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were devoted principally to water storage. Ant- associated species in several different genera have reduced their investments in storage and allocated space within their tubers to two types of cavities used by the ants. Colonies of Anonychomyrma and Philidris nest in smooth- and dry-walled cavities, while placing feces and refuse in wet-walled cavities with “warts,” actually modified roots. The epiphytes satisfy a significant fraction of their nitrogen requirements by tapping into these wastes. Epiphytic Dischidia species (Asclepiadaceae) frequently grow adjacent to the Hydnophytinae on the same hosts and are inhabited by the same ant colonies. In addition to their “normal” leaves, which grow appressed to tree trunks, these species produce highly modified leaves, involuted to form the cavities in which ants live. Stomata are concentrated on internal cavity walls formed by abaxial (lower) leaf surfaces. Through their stomata, plants take up the carbon dioxide (CO2) needed for photosynthesis. When stomata (Fig. 60) open to perform this chore, they lose precious water, an especially limiting commodity for unrooted epiphytes of the hot, dry canopy. However, stomata of ant-house Dischidia open into a relatively moist, enclosed space where the partial pressure of CO2 is enhanced by ant respiration, and this alleviates transpirational water losses. Using stable isotope technologies, K.K. Treseder and colleagues showed that Dischidia major from Bako National Park in Sabah, Malaysia, obtains about 39% of its carbon from ant-respired CO2. Isotopic studies of N revealed that about 29% of the plant’s N comes from ant feces, refuse and carton, into which plants insert adventitious roots from the bases of both normal leaves and leaf domatia. Often growing with the Hydnophytinae and Dischidia are ant-occupied ferns in the genus Lecanopteris, and any of several ant taxa can occupy each of these epiphytes. Although associations between ants and epiphytes are not obligate for either party, it is rare to find one partner in the absence of the other. This is likely due to the combination of frequent nest site limitation in ants, and water and nutrient limitation in epiphytes.

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Ant-plant Interactions, Figure 60 Myrmecotrophic epiphytes: (upper left) At Cocha Cashu, Peru, 11 different epiphyte species from seven plant families can occur in carton “ant-gardens.” This garden contains mainly seedling Peperomia macrostachya; (upper right) Myrmecodia tuberosa (Rubiaceae, Hydnophytinae) growing on a stunted tree in open “kerangas” forest at Bako National Park, Sarawak; (lower left) cross section of Anthocephalus sp., vic. Wau, Papua New Guinea, showing dry-walled cavities inhabited by ants, and wet-walled cavities with warts (modified roots) that extract nutrients deposited as ant refuse and feces; (lower right) Bornean Dischidia major (Asclepiadaceae, also from Bako): small, circular, flat leaves are typical of non-myrmecotrophic members of the genus, whereas much larger, involuted leaves have evolved in myrmecotrophic species and house associated ants.


Myrmecotrophy is commonest in epiphytes, but as P. J. Solano and A. Dejean have shown, it can also occur where ants leave waste in abandoned domatia as colonies move to new growth. Thus, in Maieta guianensis, protrubances on domatia walls appear to take up N from waste of Pheidole minutula. By an as yet poorly defined mechanism, some rattan palms also benefit nutritionally from ants that build carton nests among spines on external stems. Another monocot (Guadua bamboo), apparently cannot take advantage of ant waste inside stems and actually loses N to scale insects tending by resident carpenter ants.

Ants as Seed Dispersers, Pollinators and Partners of Insectivorous Plants Seed Dispersal Tropical epiphytes are not the only group of plants to take advantage of the willingness of ants to transport seeds. In general, plants are thought to be selected for both “distance dispersal” and “directional dispersal,” and the balance of selection for the two objectives almost certainly varies from species to species. Distance dispersal, or seed dispersal away from the maternal parent, is important for avoiding both asymmetrically strong competition from the mature plant against its seedlings, and transfer of pathogens and seed predators to these offspring. Because ants generally forage over relatively short distances from a central place, they are probably more important in directional dispersal, i.e., directing seeds to “safe sites” or favorable microhabitats. The importance of both forms of dispersal may explain why some “diplochorous” species accomplish both objectives, e.g., by first explosively propelling seeds away from the parent and then using ants to target seeds to a preferred location. The majority of ant-dispersed seeds are taken to or near the nest site, if not into the nest itself, and evolutionary advantages of “myrmecochory” (dispersal by ants) are usually discussed in relation to these sites.

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Ant-plant Interactions, Figure 61 Seeds of Acacia cana (northwestern New South Wales, Australia) have white arils contrasting with black seeds and are “displayed” at the soil surface, where ants are most likely to find them.

Ant-dispersed plants, bearing small food rewards for ants, are common in habitats ranging from rain forests (e.g., herbs in the Marantaceae) to temperate deciduous forests (e.g., violets) and arid lands (North American jimson weed and some Australian acacias and saltbushes, Fig. 61), but the greatest diversity of myrmecochores may occur in areas with infertile soils, Mediterranean climates, and high fire frequency, e.g., especially African fynbos and Australian heath. Depending upon habitat characteristics, hypotheses for the adaptive value of myrmecochory have included giving seeds refuge from fire (chaparral), from competing plants (temperate deciduous forests, where ant nests may be the only vacant sites), or from seed predators (diverse habitats), as well as dispersal to nutrient hotspots on ant mounds (e.g., the nutrient-poor soils of arid Australia). While controversies continue about particular plants and sites, it is likely that each of these hypotheses holds for a subset of plant species. The rewards that plants offer for seed dispersal fall mainly into the category of “elaiosomes,” a kind of aril (= dry fruit) that is rich in oils. Both birds and mammals also feed on arillate fruits. When ant-dispersed species were compared with bird-dispersed (ornithochorous) species in the same sub-genus of Australian Acacia, fruits and

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seeds of the two types of species differed in size, aril composition, color, and presentation. Myrmecochorous seeds were somewhat smaller on average, with arils poorer in lipids (an energy source) and water, but marginally richer in N (amino acids or proteins). In contrast to the colorful arils that ornithochores display prominently on the host, arils targeting ants were white (contrasting readily with black seeds) and presented on the ground after dehiscing. A study by L. Hughes and colleagues compared the elemental composition of myrmecochore arils with that of fleshy fruits from diverse vertebrate-dispersed plant plants. A difference in potassium (K) levels suggested that vertebrate frugivores may require comparatively high levels of K in their fruits. Species growing in poor soils may simply have too little K to produce K-rich fruits, and so may be relegated to myrmecochory. Hughes and colleagues have also identified fatty acids (especially 1,2-diolein) as important components of elaiosomes, which may mimic the composition of insect prey (especially haemolymph) and therefore induce a variety of carnivorous and omnivorous ant species to transport seeds to the nest. Given the ubiquity of ants in most habitats, plants may have evolved to attract ant species that consume only the appendage and not the seed itself. Together, these studies point to syndromes of traits characterizing species with different dispersal agents. Inconstancy in availability of elaiosomes probably prevents ants from specializing on fruits of a particular plant species. Moreover, aside from making a dispersal unit smaller or larger, it is difficult logistically to direct seeds to particular ant species. Not surprisingly then, relationships between ants and myrmecochorous plants tend to be diffuse rather than species-specific, with a variety of ants carrying seeds of a given plant, and often more than one type of elaiosome in an ant diet. Nevertheless, all ant species are not equal in their effects on plant reproductive success. Interspecific differences among carriers affect transport distances, frequency of dropping without retrieval, and rates of seed burial and escape from seed predators. Despite the opportunistic nature of interactions

between myrmecochorous plants and ants, one or more ant species may often have a disproportionate effect on plant reproductive success. For example, at increasing frequency, disruption of ant communities by non-native species (e.g., Argentine ants, Linepithema humile) threatens populations of native plants, including rare and endemic (geographically restricted) species.

Ants as Pollinators While we think most often of bees, flies and hummingbirds as agents of plant pollination, ants can also be effective pollinators under a restrictive set of circumstances. This is apparent despite observations by A.J. Beattie and colleagues that antibiotic compounds produced by the ants’ metapleural and poison glands can suppress pollen germination and pollen-tube growth. (Unlike their wasp ancestors, ants often inhabit nests for multiple generations, and metapleural glands with hygienic function appeared early in ant evolution.) Nevertheless, M. Ramsey suggests that if ubiquitous ants were otherwise effective pollinators, some or even many plant species might be expected to have evolved pollen insensitive to metapleural secretions. The apparent rarity of such immunity suggests that ants may be inadequate as pollinators for some other reason(s). A signal attribute of ants is their tendency to revist food sources such as extrafloral nectaries and Hemiptera. Very likely, conservatism in ant movements detracts from their ability to transmit pollen effectively among individual plants, a requisite for reproduction by self-sterile taxa. Nonetheless, ants may play a role in pollination where smaller plants (e.g., epiphytes or annual herbs) occur at high densities, or by enhancing rates of self pollination when more effective pollinators are scarce. Among the few plant taxa pollinated by ants, a suite of traits, or an “ant-pollination syndrome” (a term coined by J.C. Hickman) points to the circumstances under which ants can be induced to move among individual plants. Ant-pollinated plants (Fig. 62) tend to be small in stature and mostly


prostrate in growth form, so as to preclude the need to compensate ants energetically for walking vertically rather than horizontally. As a consequence of paying little reward, plants encourage workers to keep moving in search of additional nectar or fuel. Other aspects of the ant-pollination syndrome are white color, and open structure, granting ants access to floral nectars, but just small amounts of pollen, and thereby diminishing the need for ants to groom pollen from their bodies. Ant-pollinated flowers also have relatively few ovules, which may all be pollinated even by small pollen deliveries. Given their general ineffectiveness as pollinators, and their almost universal taste for sweet solutions, ants mostly interact with flowers as parasites of the relationships between plants and their real pollinators. Almost certainly for this reason, numerous plants have evolved barriers to exclude ants from floral rewards, e.g., with dense fields of hairs or sticky bands inside the corolla. It has even been suggested that nectars are made toxic or disagreeable to ants, though the taxonomic and geographic

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distributions of such nectars remain poorly known. J. Ghazoul presents some of the strongest evidence for floral ant repellents, demonstrating that a diversity of ants are repelled by something in floral tissues themselves. Still unresolved is the extent to which protection of nectar versus pollen has been the p rincipal stimulus for the evolution of ant repellents. At least some pseudomyrmecine and myrmicine (Cephalotes) ants feed on pollen, but nectar feeding is more widespread in ants, probably because less specialization of the digestive system was required to use that resource. Nevertheless, early in their evolution, flowering plants must have found ways of protecting nutritious pollen from the ubiquitous and often protein-limited ants.

Relationships Between Ants and Insectivorous Plants Carnivorous plants of diverse forms occur on infertile soils in various locations throughout the

Ant-plant Interactions, Figure 62 Mymecocystus species pollinate flowers of at least two desert annuals: Eriogonum abertianum (Polygonaceae) (left) at Portal, AZ, and Euphorbia sp. (Euphorbiaceae) (right) from southern California. The latter is more typical of ant-pollinated plants because of its prostrate growth form. Individual flowers of both species produce minute quantities of nectar, so ants must walk back and forth among individual plants to fill their crops. However, on both species, workers can commute among individuals without energetically costly vertical movement. E. abertianum is rare except in years when winter rains continue through the spring; then it grows in almost monospecific stands with branches of adjacent individuals overlapping at the same level.

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world, and are united by their use of trapped insects as N sources. Pitcher plants are a particularly fascinating life form. They lure insects to the slippery edges of steep-walled pitchers into which fluids with digestive enzymes are secreted and protected from dilution by rainfall by a sort of “roof.” Ants are among the most abundant prey of pitcher plants, being attracted to the pitcher edges by a form of extrafloral nectar. However, C.M. Clarke and R.L. Kitching show that one Camponotus species has evolved a more complicated relationship, perhaps a mutualism, with a carnivorous pitcher plant in Borneo. Thus, the hollow tendrils of Nepenthes bicalcarata house ants that feed on both large insects trapped by its pitchers and mosquito larvae therein. Unlike smaller prey, large insects apparently overwhelm the plant’s digestive capacity and lead to accumulation of ammonia in the pitcher fluids. Removal of excess prey by Camponotus prevents putrefaction of the fluids. Therefore, although the ants do rob some prey from their host plants, the net effect of their presence may be positive.

Effects of Ant-Plant Interactions on the Diversification of Ants Given the extraordinary diversity and widespread abundance of interactions between plants and ants, the two groups would be expected to have influenced one another’s evolutionary histories. This conjecture is supported by recent molecular phylogenetic studies by C. Moreau and colleagues, who show that the diversification of ant “crown groups” (contemporary major taxa) occurred coincidentally with that of flowering plants (angiosperms) in the Late Cretaceous and early Eocene, and involved major taxa of litter ants, as well as the arboreal ants reviewed in the present article. With respect to plants, relationships with ants likely contributed to recent and rapid diversification of species in the genus Inga (Fabaceae), defined in part by EFNs on leaf rhachis, and containing an estimated 300–450 species. Major radiations of ant inhabited plant taxa have also occurred in

genera Cecropia (Cecropiaceae), Macaranga (Euphorbiaceae), Ocotea (Lauraceae), Tachigali (Fabaceae), Triplaris (Polygonaceae) Tococa and Clidemia (Melastomataceae), as well as in various genera of ant-house epiphytes in sub-family Hydnophytinae (Rubiacae).  Ants  Leaf-Cutting Ants  Pollination  Insectivorous Plants  Carnivorous Plants

References Davidson DW (1997) The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biol J Linn Soc 61:153–181 Davidson DW, Epstein WW (1989) Epiphytic associations with ants. In: Lüttge U (ed), Vascular plants as epiphytes. Springer-Verlag, New York, NY, pp 200–233 Davidson DW, Inouye RS, Brown JH (1984) Granivory in a desert ecosystem: experimental evidence for indirect facilitation of ants by rodents. Ecology 65:1780–1786 Davidson DW, McKey D (1993) Ant-plant symbioses: stalking the Chuyachaqui. Trends Ecol Evol 8:326–332 Federle W, Maschwitz U, Bert Hölldobler (2002) Pruning of host plant neighbours as defense against enemy ant invasions: Crematogaster ant partners of Macaranga protected by “wax barriers” prune less than their congeners. Oecologia 132:264–270 Ghazoul J (2001) Can floral repellents pre-empt potential ant-plant conflicts? Ecol Lett 4:1–5 Hickman JC (1974) Pollination by ants: a low-energy system. Science 184:1290–1292 Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University, Cambridge, MA Izzo TJ, Vasconcelos HL (2002) Cheating the cheater: stability of a mutualism between an ant-plant and its associated ants. Oecologia 133:200–205 Mueller UG, Schultz TR, Currie CR, Adams RM, Malloch D (2001) The origin of the attine ant-fungus mutualism. Q Rev Biol 76:169–197 Palmer TM, Stanton ML, Young TP (2003) Competition and coexistence: exploring mechanisms that restrict and maintain diversity within mutualist guilds. Am Nat 162:S63–S79 Quek SP, Davies SJ, Itino T, Pierce NE (2004) Codiversification in an ant-plant mutualism: stem texture and the evolution of host use in Crematogaster (Formicidae: Myrmicinae) inhabitants of Macaranga (Euphorbiaceae). Evolution 58:554–570 Yu DW, Pierce NE (1998) A castration parasite of an ant-plant mutualism. Proc R Entomol Soc London 265:375–382

Ants (Hymenoptera: Formicidae)

Ants Certain members of an order of insects (order Hymenoptera)  Ants (Hymenoptera: Formicidae)  Wasps, Ants, Bees and Sawflies

Ants (Hymenoptera: Formicidae) david h. oi U.S. Department of Agriculture, Agricultural Research Service, Gainesville, FL, USA Ants are one of the most highly evolved and dominant insect groups. They are the largest family of insects in terms of the diversity of species and certainly sheer numbers of individuals. Currently there are well over 12,000 described species of ants, and some suggest that a similar number is yet to be discovered. Individual colonies of some species can contain over 20 million members. Ants belong to the family Formicidae, which consists of 23 subfamilies and 287 genera that are not extinct. Order Hymeoptera Suborder Apocrita Superfamily Vespoidea Family Formicidae

They are found in all terrestrial regions of the world, including the cold subarctic tundra and dry deserts. About half of the world’s precinctive genera are from the Neotropics and a third from the Afrotropical [sub-Saharan Africa] region. The subfamily with the greatest number of species is the Myrmicinae, and is followed by the Formicinae. Ants are true social (eusocial) insects, which is defined by the following characteristics: (i) cooperative brood care, where immature ants are tended by groups of adults that are not their parents; (ii) overlapping generations, where at least two different generations of adults occur simultaneously in the same colony; and (iii) reproductive and non-reproductive castes, where only the

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reproductives are capable of producing fertile offspring. The non-reproductives, or workers, perform tasks necessary for colony survival, such as foraging for food, caring for immature ants and reproductives, and nest building. Eusocial insects have a competitive advantage over nonsocial insects because there is a better probability that groups of sterile workers will be able to complete a task necessary for the survival of the reproductive queen, and also complete a series of tasks simultaneously. If a task is not completed by one worker, another worker can finish the job. This is opposed to a solitary insect where the entire burden of completing tasks from start to finish rests with the individual. Caste determination, or what causes an ant to develop into a reproductive or a worker, is thought to be due to differential genetic expression stimulated by environmental factors. Based on a limited number of species, at least six factors have been identified as being influential in reproductive and worker caste determination: (i) Egg size, where eggs with more yolk and hence larger in size will more likely become queens. (ii) Chilling, eggs and larvae that have been exposed to sufficiently cold winter temperatures tend develop into reproductives in the spring. (iii) Larval nutrition, where food quality and quantity affect larval size. Larvae that reach a threshold size by a critical developmental time become the reproductives. (iv) Temperature, larvae that grow in optimal developmental temperatures tend to become queens. (v) Caste inhibition, production of new queens is inhibited by the presence of a mother queen. (vi) Queen age, where younger queens generally produce more workers. Regulating the occurrence of some of these factors are titers of juvenile hormone. Depending on species and colony conditions, all or just some of these factors may be involved and the degree of the factors’ influence also varies. A sequence of criteria may need to be met for an egg to more likely develop into a queen, otherwise it will be a worker. To illustrate, for an egg to develop into a queen the following

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criteria may need to be met more or less sequentially: (i) is the egg of sufficient size, (ii) did it receive enough winter chilling, (iii) was food sufficient and (iv) temperatures optimal for the larva to reach a critical size by the right time, (v) are mother queens young and preventing new queen development? Meeting criteria will bias or increase the probability of the development of a queen. Determination of major (soldiers) and minor workers in some species is under both environmental and genetic regulation, thus maintaining a characteristic major: minor ratio within a colony. Recently, genetic regulation of workers and queens was found to be absolute in a hybridization zone between two species, where workers were heterozygous and reproductives were homozygous at marker loci for caste determination. Communication needed to coordinate the activities within a colony is mediated by chemical signals called pheromones. Some of the pheromones that have been isolated include a queen pheromone that allows worker ants to recognize a queen, trail-following pheromone which workers use to mark paths between the nest and food, and alarm pheromones which cause ants to disperse and/or attack. Chemical cues also are used in the recognition of colony nest mates, and play a role in aggression and establishing territorial boundaries between colonies. Ants are omnivorous and mobile, allowing them to exploit a wide range of habitats. This is in contrast to termites, another abundant eusocial insect, which are restricted to feeding on wood or other vegetation. Moist environments are conducive to microbial contamination. Secretions from the ant’s metapleural gland contain antibiotics that disinfect moist environs. Having a portable means of sanitation allows ants to exploit areas that other organisms may not be able to live in. These attributes permitted ants to become a dominant terrestrial organism, especially in the tropics. With their large populations and adaptation to a plethora of ecological niches, ants play an important role in natural ecosystems. They are

tremendous earth-movers because of their underground nest building, and thus contribute greatly to the cycling of nutrients. They disperse seeds, scavenge dead organisms, and are a major predator of other arthropods and small invertebrates. In some instances they are directly beneficial to man by being major predators of pests such as crop feeding caterpillars, and ticks of livestock.

Morphology Ants are easy to distinguish from other insects mainly because of the combination of a thin-waist and the presence of elbowed antennae. The waist refers to a segmented constriction called the petiole, located between the thorax and the gaster. The gaster is composed of the broad 4 or 5 posterior segments of the abdomen. Morphologically ants are distinguishable by having a one or two-segmented waist (Fig. 63); always consisting of a petiole if one-segmented, and both a petiole and a postpetiole if two-segmented. The petiole and postpetiole are actually the second and third segments of the abdomen that are reduced or constricted in size. They often have a distinctive node-like form, however in some species it is scale-like or just a small cylindrical segment. Following (Table 6) is a list of four terms that describe sections of the ant abdomen and the corresponding abdominal segments for ants with one- and two-segmented waists. The adult workers and queens have antennae that are geniculate, meaning bent or elbowed. The elbowed appearance arises from having a long first, or basal, antennal segment called the scape, followed by 3–11 short segments (collectively called the funiculus). The basal segments in male antennae are usually not long, and thus, the antennae will not appear to be elbowed. Another unique feature of ants is the small opening or orifice of the metapleural gland. This is located just above the basal segment of the third leg, but often requires magnification to be visible.

Ants (Hymenoptera: Formicidae) Head

Thorax

scape

Abdomen 2-segmented waist petiole & postpetiole gaster

funiculus

a 1-segmented petiole

b

Ants (Hymenoptera: Formicidae) , Figure 63 Distinguishing morphological structures of ants: (a) two-segmented petiole or (b) one-segmented petiole. Elbowed antenna consisting of a long basal segment (scape) and 3–11 short segments (funiculus); posterior portion of abdomen beyond petiole (gaster) [drawings modified from M.R. Smith 1965, (a) Monomorium minimum, (b) Dorymyrmex pyramicus].

Ants (Hymenoptera: Formicidae), Table 6 Abdominal segments that compose sections of the abdomen for ants with one- and two-segmented waists Abdominal Sections

One-segmented Two-segmented waist waist

Propodeum

abdominal segment 1 fused to posterior of thorax

Petiole

abdominal segment 2

abdominal segment 2

Postpetiole

None

abdominal segment 3

Gaster

abdominal segments 3–7

abdominal segments 4–7

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Life/Colony Cycle Ants are holometabolous, having a complete life cycle consisting of eggs, larvae, pupae, and adults. Thus, little adult ants do not grow into big adult ants. The eggs, larvae, and pupae are collectively called brood. In general, colony development is as follows: ant colonies originate after a mating flight when winged virgin queens mate with winged males. After mating, the males die, while the newly mated queen sheds her wings and finds a protected location or excavates a chamber in soil. Within this chamber she will lay a batch of eggs and care for the subsequent larvae and pupae until they become adults. These adults are usually sterile females, which are the worker caste, and they will assist the queen by caring for additional brood, foraging for food, and expanding the nest. An important aspect to the survivorship and growth of ant colonies is trophallaxis, or the exchange of regurgitated food among nestmates. Trophallaxis ensures that food is distributed to all members of the colony including the queen and brood. Once the colony is well established, winged virgin females and males (reproductives) will be produced and will proceed to have a mating flight when environmental conditions are suitable. The original colony will continue to be maintained and produce new reproductives as long as the queen is able to produce viable eggs. Depending on the species, queens have been reported to live from less than a year to as long as 29 years. A major variation to this cycle is the absence of a mating flight by the virgin queens in some species. Mating takes place within the nest with either their brothers or males that fly in from other colonies. New colonies are formed by budding, where a portion of the colony, containing adults, brood, and either or both mated or virgin queen(s), separate from the original colony and move to a new location. In addition to the tremendous number of ant species, there is a broad range of interesting behaviors or life styles among species. Many species have mutualistic relationships with honeydewproducing insects such as aphids and mealybugs

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(Hemipteran). Ants will transport and protect these insects in order to harvest the honeydew they produce. In essence, these ants tend and herd the honeydew producers as if they were cows. Some hemipterans carry plant pathogens, and disease spread is facilitated by ants moving the infected hemipterans to other plants. Another agrarian life-style is that of the leafcutting ants that raise their food in fungal gardens within their nest. These ants use leaves and other fresh vegetation to provide a substrate on which to grow the fungus, and these ants can defoliate trees overnight. Leaf-cutting ants cut pieces of leaves or flowers with their jaws and then carry them back to their nest. Once in their nest, they further chew the vegetation and add feces to form a suitable medium for fungal growth. Finally, they plant and maintain a specific fungus species on the substrate. In Central and South America, leaf-cutting species in the genus Atta and Acromyrmex (subfamily Myrmicinae) can have colonies with an estimated 1–8 million individuals. They build nests consisting of an extensive network of subterranean galleries, and are the most significant pests of agriculture in South America, feeding on citrus, forage grasses, and other crops. Symbiotic relationships with plants been reported for several ant species. One well-studied mutualistic relationship is that between Acacia cornigera trees and the ant Pseudomyrmex ferruginea (subfamily Pseudomyrmecinae). The acacia tree produces thorns, which serve as nesting sites for the ants and it produces structures, called Beltian bodies, that are eaten by the ants. The ants protect the plant from herbivorous arthropods and vertebrates, and destroy competing plants that sprout nearby. Besides their symbiotic interactions with plants and other insects, ant species also have parasitic relationships among each other of which slavery, or dulosis, is one of the more interesting forms. The genus Polyergus (subfamily Formicinae) consists entirely of slave-making species. Workers of Polyergus colonies dash into the nests of ants in the genus Formica (subfamily Formicinae) and steal their larvae and pupae. The stolen

immatures are allowed to develop into adult workers and carry out colony maintenance tasks for their abductors. In fact, the Polyergus workers are so specialized for raiding and killing other ants that their jaws are like sharp curved sabers, morphologically ill-suited for nest building, tending immatures, and food gathering. More extreme extensions of this parasitism are species without a worker caste. These species contain only males and queens that are cared for by the workers of a host colony, which they have infiltrated. They are either fed by the workers or steal food from the host queen, which they often mount and hold onto. The eggs of the parasite are reared to adulthood by the host workers. Parasitized host colonies can be smaller in size, presumably because of the partial diversion of resources to the parasites. Examples of these parasitic ants include Solenopsis daguerrei, a parasite of imported fire ants (Solenopsis invicta, S. richteri), and Teleutomyrmex schneideri, a parasite of Tetramorium caespitum and T. impurum (all in the subfamily Myrmicinae). In contrast to the symbiotic life-styles, many species of ants are extremely predatory and have gained the reputation of being an unrelenting scourge of the jungle. The subfamily Dorylinae consists of a single genus, Dorylus, which contains the African driver ants, also referred to as army ants or legionary ants. Most species are found in the Afrotropical region (sub-Saharan Africa), but a few species are also found in the southern Palearctic, Oriental, and Indo-Australian regions. The various species of African driver ants have colonies with millions of individuals, which regularly move nesting sites and forage for food in large swarming columns or groups. The columns can fan out to produce a large moving front that preys on anything that remains in its path, especially arthropods. At night the colony forms a bivouac, protecting their queens and brood within a mass of worker ants. Thus, there is no permanent nest structure for these nomadic ants. Besides the army ants in the Dorylinae, the subfamily Ecitoninae contain many species of army ants found in the Neotropics, and a


few species in the Nearctic. These armies are smaller than the African species, with colonies of hundreds of thousands rather than millions. The pillaging, nomadic life of the army ants requires a high level of organization and cooperation. Extraordinary cooperative behavior is further exhibited during nest construction by the weaver ants in the genus Oecophylla (subfamily Formicinae). These ants are dominant arboreal ants of the Afrotropical region. They link their bodies together to form chains by grasping the petiole of an adjacent worker with their jaws. The living chains are used to pull the edges of leaves together. Once leaves are held in a desired position, other workers bring forth silk-producing larvae and individually press larval heads to one leaf surface then another, resulting in thousands of sticky silk threads being drawn between the leaves to hold them together. Eventually leaves and stems are bound together to form a tent within which a nest of silken galleries is constructed. This communal nest construction is unique in that it involves the use of immature stages that secrete silk on command. It has allowed these ants to build expansive networks of nests across several trees, which can house a colony of over 500,000 individuals. The adaptability and high reproductive output of many species of ants allow them to thrive in many environments, including that of humans. As such, ants that live in buildings or have high populations in areas used by man are often considered pests. Many pest ants have characteristics that typify the “tramp species”. These ants generally (i) spread around the world via human commerce; (ii) can thrive in man-made environments; (iii) have colonies that are not territorial and thus can result in interconnected nest sites; (iv) have many queens per colony; and (v) have limited or no mating flights resulting in colony reproduction by budding. Ants that sting, such as red imported fire ants (Solenopsis invicta, subfamily: Myrmicinae), are of veterinary and medical importance. Newborn livestock can be blinded or killed by stings at birth. People who are stung usually develop itching pustules that last for several

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days, but some can have hypersensitive reactions, resulting in anaphylaxis and even death in rare instances. Non-stinging ants, such as the Pharoah ant (Monomorium pharaonis, subfamily: Myrmicinae) may be a nuisance to building occupants and are also known to contaminate sterile surgical units, supplies, and food items in hospitals. Invasive ant species, such as the red imported fire ant and the Argentine ant (Linepithema humile subfamily: Dolichoderinae), establish and thrive in non-native locations, invade surrounding areas, and eventually become the dominant faunal species. Invasive ants are a major concern in many areas, ranging from nature preserves to suburbia, because they displace native ants as well as other native organisms.

Control Controlling pest ants can be a difficult task given their broad habitat range, large populations, and a social organization that protects the queen(s) from external influences such as insecticides. Because traditional control approaches of excluding ants from buildings by sealing cracks and crevices or applying insecticides directly to ants or nests generally do not target the queen, significant population reductions, if any, are temporary. Ant baits, however, were developed to use the foraging and nest mate feeding behaviors of ants to distribute a toxicant throughout a colony, including the queen(s). Ant baits typically contain a toxicant dissolved into a liquid food preferred by the pest ant species. This poisoned food can be mixed with an absorbent carrier such as corn grit or formulated into a gel to facilitate handling and application. Some baits are left in liquid form and must be dispensed in a container that serves as a feeding station. Key to effective ant bait is a toxicant with the following three characteristics. First, the concentration of toxicant used should not deter feeding on the bait, because ideally enough bait should be readily foraged upon to be shared with adults and

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immature stages of all castes within a colony. Second, the toxicant should not immediately kill the ants foraging upon the bait. In general, a delay in death or sickness of a minimum of 8 hours from the time of ingestion is required to allow sufficient toxicant to be collected and fed to a significant portion of the colony. If the toxicant causes sickness or death too quickly, distribution of the bait to the rest of the colony stops before enough of the colony is affected, and control will not be obtained. Third, the toxicant should provide a delay in mortality over a wide range of concentrations (typically at least a 10 fold range) because the toxicant is diluted as it is shared among nest mates. Depending on the type of toxicant and colony size, ant baits may take from three days to several months to eliminate a colony. Some bait toxicants do not kill adults but instead disrupt reproduction by the queen, whereby worker caste ants are no longer produced. As the original adult worker population dies naturally, the lack of replacement workers dooms the colony to a slow death as functions that sustain a colony such as food gathering, defense, nest repair, and queen care cannot be carried out. While ant bait development has been a major focus for ant control, other strategies have been developed for specific species. For example, planting forage grasses that are a non-conducive substrate for the growth of fungus needed by leafcutting ants can significantly reduce their populations. Natural enemies of ants are also used to suppress ant populations. In particular, tiny parasitic flies, in the genus Pseudacteon, that develop in the heads of ants, and a pathogen, Thelohania solenopsae, that debilitates queens are being used to suppress populations of imported fire ants. These natural enemies require development within fire ants and unlike chemical control measures, are self-sustaining and can spread naturally among fire ant populations. Effective control of pest ants, as with most insect pests, generally requires the use of several control tactics adapted for a particular species and circumstance.  Myrmecophiles  Myrmecomorphy

 Ant-plant Interactions  Driver Ants  Leaf-cutting Ants  Carpenter Ants  Castes

References Agosti D, Johnson NF (eds) (2005) Antbase World Wide Web electronic publication. antbase.org version (05/2005). Accessed September 2007 Bolton B (1994) Identification guide to the ant genera of the world. Harvard University Press, Cambridge, MA, 222 pp Bolton B, Alpert G, Ward PS, Naskrecki P (2006) Bolton’s catalogue of ants of the world: 1758–2005. Harvard University Press, Cambridge, MA Julian GE, Fewell JH, Gadau J, Johnson RA, Larrabee D (2002) Genetic determination of the queen caste in an ant hybrid zone. Proc Natl Acad Sci USA 99:8157–8160 Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, MA, 732 pp Smith MR (1965) House-infesting ants of the eastern United States: their recognition, biology and economic importance. United States Department of Agriculture, Agricultural Research Service Technical Bulletin No. 1326. 105 pp Williams DF (Ed) (1994) Exotic ants: biology, impact, and control of introduced species. Westview Press, Boulder, CO, 332 pp Williams DF, Oi DH, Porter SD, Pereira RM, Briano JA (2003) Biological control of imported fire ants (Hymenoptera: Formicidae). Am Entomol 49:150–163

Anus The external opening of the digestive tract, through which the food remnants and metabolic waste products are passed.  Alimentary Canal and Digestion  Internal Anatomy of Insects

Aorta A tube located dorsally in the insect’s body that conducts blood from the heart forward to the head region.

Aphids (Hemiptera: Aphididae)

Apatelodidae A family of moths (order Lepidoptera). They commonly are known as American silkworm moths.  American Silkworm Moths  Butterflies and Moths

Aphelinidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

Aphelocheiridae A family of bugs (order Hemiptera).  Bugs

Aphicide An insecticide that is especially effective against aphids.

Aphididae A family of insects in the order Hemiptera. They sometimes are called aphids, green flies, and plant lice.  Aphids  Bugs

Aphidivorous Aphid loving. Many insects are associated with aphids because the feed on the honeydew produced by the aphids (e.g., many ants, some flies including mosquitoes) or on the aphids (e.g., many lady beetles and flower flies). Those that feed on the aphids are said to be “aphidophagous.”

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 Aphids  Sugar Feeding in Blood-Sucking Flies  Aphidophagous

Aphidophagous Aphid feeding.  Aphidivorous  Predation: The Role of Generalist Predatory in Biodiversity and Biological Control  Natural Enemies Important in Biological Control

Aphids (Hemiptera: Aphididae) daniel j. sullivan Fordham University, Bronx, NY, USA Aphids are among the most interesting, unusual, and thoroughly studied of all insect groups. They are worldwide in distribution, and are also called plant lice, antcows, green flies, die Blattläuse, les aphides, los áfidos, etc. They have economic importance because many aphid species are pests of agricultural crops, forest and shade trees. Although small in size (1–10 mm) compared to many other insects, professional as well as amateur entomologists have always been intrigued by their specialized life cycles that are influenced by their host plant relationships. This results in both sexual and asexual reproduction, with a highly dependent, almost parasitic mode of sessile existence that can be parthenogenetic during lengthy periods with a telescoping of generations. Yet, when the photoperiod shortens and the temperature cools, offspring are produced that reproduce sexually. In addition, aphids have life cycles with a polymorphism in adults that have wingless (apterous) and winged (alate) forms or morphs, as well as polyphenism or different morphs even within clones. As alates, migration is enhanced, and this can be involved with overwintering behaviors because of host plant alternation. Hence, aphids are excellent animals for the study of multitrophic ecology, behavior, physiology, genetics,

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evolution, biological control, molecular biology, etc. Besides using field studies of aphids for population sampling and damage assessment, many species can be reared rather easily in the laboratory and greenhouse, thus making them ideal subjects for precise observation and experimentation.

small number compared to many other insect taxa. However, adult polymorphism as winged (alate) and wingless (apterous) morphs, as well as polyphenism within clones increases their overall diversity.

Classification

Although aphids are found worldwide, their species are most abundant in the temperate latitudes, and less so in the tropics. This preferential distribution may have evolved in response to the selective pressures of the temperate regions having constantly changing, yet rather predictable, environmental conditions. As a result, unlike most other phytophagous (herbivorous) insects, aphids show an inverse relationship between the number of aphid species and the number of plant species in different parts of the world. Hence, there are many more aphid species in the temperate latitudes than in the tropics, although there are more plant species in the tropics than in the temperate regions, but with fewer species of aphids. Most aphids (70%) are in the subfamilies Aphidinae and Calaphidinae (=Drepanosiphinae), and many are pests of crops in these temperate zones. However, when some of these species are introduced (accidentally) into tropical and subtropical regions, they are still able to adapt and become pests in these new environments. In addition, although the tropics and subtropics are fairly constant in temperature and photoperiod, it is surprising that there are some endemic species in these regions that are holocyclic in their life cycles (female cyclical parthenogenesis, alternating with sexual reproduction by males and females) which is more common in the temperate zones. This is in addition to the expected anholocyclic life cycle (absence of males, only parthenogenesis by females) which would be normal in the tropics and subtropics. Aphids find their host plants by random search, and ecologists emphasize the importance of the concept of “plant apparency.” Of the more numerous species of aphids in the temperate regions, many are monophagous (feed on one or only a few species of related host plants). However, in the tropics where

Aphids are usually classified in the order Hemiptera, series Sternorryncha or sometimes suborder Homoptera along with the psyllids, whiteflies, scale insects, and mealybugs. Another approach is to put aphids in the order Homoptera and suborder Sternorryncha. Some taxonomists have increased the number of aphid families to as many as 20 with a corresponding realignment of the subfamilies. Further phylogenetic studies with molecular techniques are in progress, but in this overview summary the following composite scheme of the major taxa in aphid classification is given below such that there are 8 subfamilies in the family Aphididae: Order Hemiptera Series Stemorrhyncha (= Suborder Homoptera) Superfamily Aphidoidea Family Aphididae (aphids) Subfamily Aphidinae Tribe Aphidini Tribe Macrosiphini Subfamily Calaphidinae (= Drepanosiphinae) Subfamily Lachninae Subfamily Chaitophorinae Subfamily Greenideinae Subfamily Eriosomatinae Subfamily Hormaphidinae Subfamily Anoeciinae Family Adelgidae (adelgids) Family Phylloxeridae (phylloxerans)

Although the number and organization of the subfamilies can vary, there is general agreement that within the family aphididae, the largest subfamily is the aphidinae, followed by the calaphidinae (=Drepanosiphinae), and the Lachninae. There are over 4,000 species of aphids which is a relatively

Distribution


there are more species of plants and relatively fewer aphid species, these aphids are more polyphagous (feeding on a variety of host plants). Hence, some suggest that aphids originated in the northern hemisphere, and that the tropics presented a barrier to a similar multiplication of species in the southern hemisphere.

Origin and Evolution Based on the classification given above, in the hemipteran superfamily Aphidoidea are the families Aphididae (aphids), Adelgidae (adelgids), and Phylloxeridae (phylloxerans). Paleontology and phylogeny are two sources of information used by systematists to study the evolutionary history of this group. According to these experts, although paleontology should provide a time scale for their ages, unfortunately the fossil evidence is very limited. Only about 125 fossil species have been described, while the number of extant aphid species is over 4,000. Two kinds of fossils exist: (i) imprints from carbonized remnants in clay, limestone or other sediments, which provide only minimal information because aphids are soft-bodied and are not well preserved; and (ii) amber inclusions which have entire specimens that are often caught in a natural position, and so are much more important as fossils. Probably aphids, along with the closely related adelgids and phylloxerans, evolved from a common ancestor about 280 million years ago in the late Carboniferous or early Permian Periods when there were seasonal climatic changes associated with the glacial period. They are now classified together in the superfamily Aphidoidea, and their host plants were primitive gymnosperms (Cordaitales, Cycadophyta). By utilizing their specialized piercing – sucking stylets on the phloem and parenchyma tissues of the gymnosperms, polyphagy was most likely the primitive feeding behavior of the superfamily Aphidoidea. As a result of their parasitic mode of life, individual size in these three families (Aphididae, Adelgidae, Phylloxeridae) was similar and rather small. Although their wings were delicate, their light

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body weight could take advantage of air currents for dispersal. Some consider monophagy as a recent development in aphid evolution, although others speculate that like parthenogenesis, it could have evolved early in the evolutionary history of the Aphidoidea. Another characteristic which aphids share with the adelgids and phylloxerids is the simple nymphal eye of three lenses (triommatidium). From the Triassic Period (240–205 million years ago), only the front wing of one species of aphid (Triassoaphis cubitus) from Australia is known, and it is not easily placed in any superfamily of later periods. Cytogenetic evidence indicates that parthenogenetic reproduction by means of unfertilized eggs may have evolved over 200 million years ago, before these three families (Aphididae, Adelgidae, Phylloxeridae) became independent. This view is supported because a holocyclic life cycle (cyclical parthenogenesis by females, alternating with sexual reproduction by males and females) is now common to all three groups. However, viviparity (live birth) is a special characteristic of aphids, and must have evolved later because the modern adelgids and phylloxerans are only oviparous (lay eggs). By the Jurassic Period (205–138 million years ago), there had developed the recognizable shape of the body, wing venation, proboscis, and legs, while the siphunculi or cornicles and cauda evolved in the Cretaceous Period (138–65 million years ago). A major botanical event also occurred during the Cretaceous with the evolution of angiosperms (flowering plants), which coincided with the radiation and species diversification of aphids. Within the family Aphididae, the Aphidinae (the largest subfamily of modern aphids) is not represented in the fossil record until the late Tertiary Period (65–1.65 million years ago). Tribes of the second largest subfamily, the Calaphidinae (=Drepanosiphinae), developed much earlier in the Upper Cretaceous and early Tertiary Periods. Concerning the third largest subfamily, the Lachninae, there is limited palaeontological evidence of its evolution. Hence, there is some debate as to the relative age of the lachnids. Because 80% of them live on conifers (which are older than the angiosperms), the lachnids

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have generally been regarded as ancient, although some genera may have a recent origin.

Metamorphosis Regardless of whether aphids are born from an egg of oviparous sexual females or live from viviparous parthenogenetic females, their type of metamorphosis is called simple or incomplete: the developmental sequence is egg, to nymph(s), to adult. A nymph resembles the adult, and usually develops in four molts (four nymphal instars or stages) growing larger each time until the adult stage of sexual maturity is reached. This type of metamorphosis is to be distinguished from complex or complete metamorphosis wherein the developmental sequence is from egg, to larva (several molts and instars), to pupa, to adult.

External Morphology Aphids are mostly soft-bodied insects and relatively small (only 1–10 mm in length), usually being plump and ovoid in shape. Because they are plant-sucking insects, they feed by inserting their slender mouthparts into the plant. These needle-like stylets consist of an outer pair of mandibles and an inner pair of maxillae. The inner faces of the maxillary stylets lock together to form two canals: a large central foodcanal for the uptake of plant sap, and a fine duct down which saliva is injected into the plant. The tips of these mouthparts also have a chemosensory function. When the stylets penetrate the plant, they often go between the cells instead of passing through the cells, and in this way they reach the phloem sieve tubes within the veins of the host plant. Most aphids have well-developed compound eyes (larger in the alates than in the apterous morphs) with a great many individual round lenses called facets or ommatidia. In addition, at the posterior margin of the eye protrudes an ocular tubercle or triommatidium composed of three lenses. Aphids without wings are called apterous, while alate aphids have wings with the hind wings

being much smaller than the front wings. Alate aphids (but not apterous) bear three ocelli on the front of the head. The antennae are usually long and thin with five or six segments, and bear placoid sensilla called rhinaria which are the olfactory organs. Legs of aphids do not show much interspecific variation, although more active species tend to have longer legs. Both sets of wings are membranous with the fore wing having two longitudinal veins, one being prominent and the other a weak vein. Both veins run apically into the pterostigma which is a dark, thickened area near the leading edge of the fore wing. When flying, the two pairs of wings work as one, being held together by small hooklets or hamuli on the leading edge of the hind wings that fit into a groove on the trailing edge of the fore wings. On the dorsal surface of both the thorax and the abdomen, many species have cuticular glands that secrete copious quantities of waxy exudates that are powdery or filamentous or rod-like. As a result, when these species are gregarious, the entire colony appears as a white, powdery or cottony mass. At the end and dorsal surface of the abdomen, there are usually a pair of tubular structures called siphunculi or cornicles. By contraction of a muscle, a droplet of a waxy exudate is discharged through the cornicles which rapidly solidifies in the air. When an aphid is touched or attacked by a predator, one or both cornicles may be raised and the sticky fluid released in a defensive role to gum-up the mouth parts and/or antennae of an attacking predator. This may also function as a pheromone either as an alarm to warn other aphids of a predator or for maintaining distance between aphids on a leaf. Above the anal opening, adult aphids usually have a distinct tail or cauda which varies in shape among species from being short and stubby or long and tapering. In the latter case, aphids can flick off a droplet of honeydew that emerges from the anus. Concerning the external genital organs in the adults, the female genital opening or vulva is only a small slit because there is no ovipositor. On the other hand, the male genitalia have prominent sclerotized claspers and an aedeagus or penis that can be retracted.


Internal Anatomy Digestive System Aphids have the usual regions: pharynx, fore gut, midgut, hindgut, etc. with subdivisions and associated parts. However, some species have a filter chamber which is a special structure. With some variations, it consists of a concentric filter system in which the tubular anterior region of the midgut is enveloped by the anterior region of the ectodermal hindgut forming a filter chamber. Perhaps this permits selective filtering of the required nitrogen compounds while rejecting the sugars and conveying excessive amounts of water to the hindgut. The precise function is not clear, and since most aphids do not have a filter chamber, it is probably not essential to their method of feeding.

Bacteriocytes Most aphids have specialized groups of cells called bacteriocytes (or mycetocytes) that usually contain the bacterium Buchnera aphidicola. This symbiotic association seems to be mutualistic, and it is not surprising because many insects that live on specialized and often unbalanced diets such as plant sap do indeed possess symbionts. Although their role in aphid biology is still not completely known, they may help the aphid with its nitrogen utilization, synthesis of vitamins, sterols, etc. Although numerous at birth, the bacteriocytes decrease in number during growth. By the end of the aphid’s reproductive period, practically none remain, suggesting a contribution to embryonic development. These bacterial symbionts are transmitted transovarially to the embryos so that nymphs are born with them.

Nervous System The nervous system comprises four structural parts: brain or supraoesophageal ganglion in the head, suboesophageal ganglion under the brain,

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thoracic ganglionic mass terminating in the ventral nerve cord, and ganglia plus nerves of the stomatogastric system.

Reproductive System Female aphids have two ovaries composed of 4–6 ovarioles. They are remarkable because different female morphs can reproduce parthenogenetically (Fig. 64) and be virginopara/vivipara (give birth to live young by larviposition) without mating because males do not exist at this time. At other times, females can reproduce sexually and be ovipara (deposition of eggs that have been fertilized by males). Development of the female embryo depends on whether it is destined to become a vivipara (live birth) or an ovipara (lays eggs). Influences on the adult female can be genetic as well as environmental. Realizing exceptions depending on the aphid species and geographical location, in general when the environment is favorable (long photoperiod, moderate temperature), the viviparous mother will reproduce parthenogenetically. The embryonic female within her will be born alive as a female nymph, and in turn will give live birth to other viviparae also being all females (see below about anholocyclic life cycle). On the other hand, with less favorable conditions (shorter photoperiod, cooler temperature), the oviparous mother will reproduce sexually after mating with a male, and she will lay fertilized eggs (see holocyclic life cycle). The viviparous parthenogenetic female does not require fertilization, and eggs begin development as soon as they are ovulated from the ovary. Even ovarioles of newly born parthenogenetic females contain developing embryos rather than just eggs. Hence, “telescoping of generations” refers to the fact that a mother can have in her ovarioles developing embryos which in turn also contain embryos or future granddaughters. In the modern family Aphididae, therefore, development may commence even before the mother is born, resulting in a consequent “telescoping of generations.” As a result,

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Aphids (Hemiptera: Aphididae), Figure 64 Aphid diversity. Top left, aphid giving birth to a nymph (photo J.L. Capinera); top right, winged brown citrus aphid, Toxoptera citricida (photo Paul Choate); second row left, green peach aphid, Myzus persicae (photo Jim Castner); second row right, corn leaf aphid, Rhopalosiphum maidis (photo Paul Choate); third row left, turnip aphid, Lipaphis erysimi (photo Jim Castner); third row right, oleander aphid, Aphis nereii (photo Jim Castner); bottom row left, Asian woolly hackberry aphid, Shivaphis celti (photo Lyle Buss); bottom row right, cabbage aphid, B revicoryne brassicae (photo Paul Choate). Note copious and moderate amounts of waxy exudate on woolly hackberry and cabbage aphids, respectively.


postnatal development periods and generation times are short, and reproductive rates are potentially very high. Because aphids are born on the very host plant where they can feed, in many species it requires only 7–14 days for an immature aphid or nymph to metamorphose by several molts into a sexually mature adult when it can begin reproducing. When this is combined with a high fecundity (30 or more nymphs born to each aphid) in a short period of time, the rate of increase is very rapid not only for the individual, but even more so for the entire colony. The offspring of viviparous parthenogenetic females are born rear first, and are fully active. A nymph is similar in shape to the adult, only much smaller. If destined to be a winged (alate) adult it is either born with wing buds or in some species during the early postnatal period the nymph itself will develop them. This can be triggered by unfavorable conditions due to aphid crowding and/or plant deterioration as well as by seasonal changes such as shorter photoperiod and cooler temperatures. However, colonies founded by alates usually produce only apterous offspring, and only later on might alates develop. Hence, there seems to be a “biological clock” mechanism so that there is a gradual switch to alates that depends on an interval of time. In the superfamily Aphidoidea, this viviparity (live birth) characterizes the entire family Aphididae. But only females in this family do this, and not females in the families Adelgidae and Phylloxeridae. However, in all three of these families there are sexual females (oviparae) that mate and deposit eggs (see Life Cycles). Male aphids usually have two to four follicles per testis, although the number, size, and shape varies between species. The vasa deferentia lead to the ejaculatory duct, and in some species there are paired accessory glands.

Excretion Unlike most insects, aphids have no Malpighian tubules, and excrete nitrogenous waste in the form of ammonia instead of uric acid. The large amounts of water in the diet may dilute the ammonia, and

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in addition, symbionts in the mycetomes may detoxify it as well.

Ingestion and Digestion Both as nymphs and as adults, aphids feed by sucking up the sap from the host plant. When the stylets penetrate the plant between the cells, they reach the phloem sieve tubes. In a healthy plant, the sap is under turgor pressure which forces the sap up the food canal between the stylets which reduces the energy needed by the aphid to suck the sap. Nevertheless, there is also a muscular cibarial food pump at the entrance to the pharynx which can be used when the plant wilts and the sap ceases to be under pressure. Although this plant sap is rich in sugars, it is poor in amino acids that are essential for the growth of the aphid. Hence, aphids ingest large amounts of sap in order to acquire sufficient protein. Although there are less nitrogenous compounds in plant sap compared to leaf tissue (such as would be eaten by other phytophagous insects such as the larvae or caterpillars of lepidopterans), aphids make up for this deficiency by imbibing sap at a very fast rate. The unneeded portion of the sap is mainly sugars which can be stored temporarily in a dilated rectum. This sugary material can be eliminated by ejection from the anus in the form of a sugary droplet called honeydew (see section on Ant-Aphid Mutualism). When aphids are numerous, the leaves of their host plant can become coated with sticky honeydew on which sooty mold fungus can develop causing an economic problem on fruit, vegetables, and even cars parked under a tree.

Sex Determination As expected, the number of chromosomes varies with aphid species, but all aphids have sex chromosomes for females designated as XX and males as XO. This system of sex determination is called the XX:XO type wherein females have the full diploid complement of autosomes plus one pair of sex chromosomes: XX.

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Males also have a diploid set of autosomes, but they have only one sex chromosome (XO) rather than two (not the XY as in some other insects and even humans). As discussed below, in holocyclic life cycles (female cyclical parthenogenesis, alternating with sexual reproduction), sexual females and males are produced in response to cues/stimuli that could be external or internal. On the other hand, anholocyclic life cycles (absence of males, only parthenogenesis by unfertilized females) usually exists when the environment (photoperiod and temperature) is relatively constant.

Parthenogenesis This is reproduction without mating, and therefore without a female’s egg being fertilized. As mentioned above, all aphids have the normal diploid autosomes, but the sex chromosomes for females are XX and males are XO (lacking an X). Among insects in general (not just aphids), when a female’s egg is not fertilized, there can be two types of parthenogenetic reproduction: Arrhenotokous parthenogenesis by females produces only male offspring that are all haploid (n) from her unfertilized eggs (common in the order Hymenoptera – ants, bees, wasps). In aphids, some authors hold that the male’s XO sex chromosome determination is only a “type of arrhenotoky” probably resulting from a mini-meiosis in the unfertilized female by which her two X-chromosomes pair and then separate. Males are then XO with the result that they could produce two types of sperm (X and O). However, during meiosis in the male, those sperm without an X-chromosome (designated O) degenerate. This leaves the X-chromosome as the only viable sperm which can fertilize an adult female’s haploid egg (X) resulting in all of her offspring being female (XX). Hence, males are produced by the loss of an X chromosome during a meiotic division resulting in the sex determination of XO. Adult male aphids then produce haploid sperm all of which contain one X chromosome. However, this is not really “arrhenotoky” as traditionally used with other insects because although male aphids have the sex determination

of XO, they do have two sets of autosomes, but only one X chromosome. Thelytokous parthenogenesis by females produces only adult diploid (2n) females from unfertilized eggs, but no males. Female aphids seem to have “diploid parthenogenesis” because there is no reduction division, and development starts from a cell with a complete set of chromosomes including the XX sex chromosomes. Both the adult parthenogenetic females and the sexual females are diploid (2n) with XX sex chromosomes. In anholocyclic life cycles (absence of males, only parthenogenesis by unfertilized females), this reproductive method could continue almost indefinitely, if the environmental conditions permitted. However, in holocyclic life cycles (female cyclical parthenogenesis, alternating with sexual reproduction), sexual females and males are produced. The sexual female produces only haploid eggs (X), and requires mating and fertilization by a male (X) resulting in a diploid zygote with two XX sex chromosomes, such that all aphids hatching from these fertilized eggs are females.

Life Cycles Life cycles in aphids are varied and complicated, but the essential terms are given below: Holocyclic life cycle: A viviparous parthenogenetic female produces live nymphs without mating. But, this is cyclical because it is interrupted during the year with the production of males and females that mate, and this oviparous sexual female deposits eggs. Anholocyclic life cycle: This is the complete absence of males, so that only viviparous parthenogenetic females exist with parthenogenetic reproduction continuing throughout the entire year with all the progeny being female.

Host Plant Alternation Host plant alternation in aphids involves the two types of life cycles:


Autoecious (monoecious) in which aphids are host plant specific, and live on one or only a few species of closely related plants even within a particular genus during the entire year. Most aphid species (over 90%) are of this type, and as a result, there is usually no need for an annual alternation between primary and secondary hosts, so that the anholocyclic life cycle is common. Heteroecious or host plant alternation life cycle (Fig. 65) by which about 10% of aphid species

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spend autumn, winter, and spring on a primary woody host, and the summer usually on secondary herbaceous plants. The primary and secondary host plants usually are unrelated and belong to different families of plants. Although such aphids may be classified as polyphagous, many species are really sequentially monophagous if they live on only one host plant species at a time. This alternation of host plants during the year is accomplished by the holocyclic life cycle described above. These aphids

Aphids (Hemiptera: Aphididae), Figure 65 Life cycle of the heteroecious holocyclic black bean aphid, Aphis fabae. (a) Fundatrix or apterous stem mother, (b) her apterous viviparous parthenogenetic f emale progeny or fundatri-genia, (c) alate emigrant or spring migrant, (d) apterous virginopara, (e) alate virginopara or summer migrant, (f) alate autumn remigrant or gynopara, (g) alate male, (h) apterous ovipara or mating female, (i) egg (after Dixon 1998; Kluwer Academic Publishers).

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use a specialized reproductive strategy by which the sexual generation produces eggs on the primary (woody) host plant on which they overwinter. This is done because eggs are better able to survive the rigors of a cold winter, snow, etc. The cold period of winter is required before the embryo in the egg can complete its development, and this suspended physiological state is called diapause. The embryo will not hatch until the warmth of spring arrives, and when it does, all of the offspring will be female. This female fundatrix or stem mother on the primary (woody) plant is the first individual to begin the new parthenogenetic line which results in only female offspring all of which are genetic clones of herself. Spring not only provides nutrient availability, but also at this time natural enemies probably have not arrived in dangerous numbers. Again there is a trade-off such that all fundatrices are apterous, thus avoiding unnecessary expenditure of energy on developing wings that are not needed because they do not migrate. Instead, energy can be concentrated on embryological development resulting in very high fecundity of more and more females by viviparous parthenogenesis. When the colonies of female progeny on the primary (woody) plant become crowded, morphs appear and become alate spring migrants that fly (often with the help of wind currents) to the secondary host plant. The summer secondary host plant is usually herbaceous, and since these alate migrants are all viviparous females, they will produce only females parthenogenetically for as long as this favorable summer weather continues. By dispensing with mating and egg-laying, their numbers can increase at an astonishing rate. These aphids are usually apterous and sessile, remaining on the host plant for long periods in a parasitic “plant lice” mode. But if there is crowding and/or the plant deteriorates, alates will develop in the next generation, thus permitting movement to a new location and even to a new herbaceous host plant. However, such relocation need not be far away if the agroecosystem consists of many acres planted to monoculture. In the autumn, environmental cues (shorter photoperiod and cooler temperature) will trigger

the seasonal alternation back to a primary (woody) host plant, and a behavioral change into an alate autumn migrant or gynopara. This parthenogenetic female produces sexual females that will mate with males. Overwintering fertilized eggs are deposited, and the cycle is repeated.

Polymorphism and Polyphenism Polymorphism means that there are two or more phenotypes or morphs in a population of the same species. Polyphenism means that there are two or more phenotypes or morphs in the same clone. In other words, genetically identical individuals derived from the same mother by parthenogenesis can differ even though they are all clones. This phenomenon is more common in aphids than in any other insect group, especially in aphids that have host plant alternation. In such a parthenogenetic system of genetic clones, females may have as many as eight different phenotypes that differ in such characteristics as morphology, color, physiology, timing of reproduction, developmental time, numbers and sizes of offspring, longevity, host plant preferences, and alternative host plant species. It is probable that some of this variation is not caused only by genetic differences, but also by variations in the host plant and/or the environment. When environments are regularly cyclical, then seasonal changes and predictable weather patterns can influence the availability and quality of phloem sap that is the basis of aphid feeding. Because of this predictability and reliability, the evolution of aphid species occurred mainly in temperate zone habitats. With this in mind, it is understandable that there has been an environmentally induced morphological and behavioral trade-off so that because alate morphs have energy-costly wings, their developmental time should be slower/longer with a reduced lifetime fecundity compared to the apterous morphs that do not have to expend their energy on wings but rather on offspring production. Hence, there has evolved in aphids both polymorphism and


olyphenism that is adapted to changing yet prep dictable environmental conditions, and resulting in the types of sexual and migrant morphs already mentioned above in earlier sections. No other group of insects can match this diversity.

Soldiers In addition to the sexual and migrant morphs, there is still another of interest: soldiers. These are female nymphs in only a few (1%) of the more than 4,000 species of aphids, and are found in some but not all gall-forming aphids (see section on Galling). They exhibit a behavior of defending the colony against predators, but they do not molt into reproductive adult females and will never produce offspring. These soldiers aggressively attack invaders, sometimes being suicidal. In some, the fore legs and middle legs are thickened which they use to hold and even crush the intruder. If they have frontal horns, they will use these as well as their stylets as weapons in combat. Both soldiers and normal nymphs can be produced by the same mother aphid. In some species, soldiers (like males) do not have symbionts. Animal behaviorists note the evolutionary convergence of “altruism” in these aphid soldiers with the sterile soldier castes of ants, termites, and thrips.

Color Morphs Coloration in aphids may be caused by: (i) brown or black pigmentation of the integument (mainly the tergum) or by sclerotization of the cuticle which can give a metallic shine; (ii) body contents show through the cuticle revealing pigments in internal organs, tissues, hemolymph (types of glycosides not found in any other group of animals or plants), bacteriocytes, etc. Colors can vary between and even within species, but the color is usually green, yellow, reddish, creamy, or almost black; (iii) waxy exudates that form a pattern from glands on the body and appear powdery white or grey.

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Intraclonal color variation is usually induced by environmental factors, especially temperature, crowding, and poor nutrition. Therefore, it is reversible if these factors revert to the previous state. On the other hand, interclonal color variation is genetically fixed between different color morphs of males and females in some species or between the green and red-pink morphs in the pea aphid (Acyrthosiphon pisum), green peach aphid (Myzus persicae), and potato aphid (Macrosiphum euphorbiae). In the first two aphid species, the red-pink allele is dominant to the green allele, so there may be some biological differences influencing fecundity, reproductive rate, host plant preferences, selection of feeding sites, activity, high or low temperature tolerance, etc. For instance, it seems that thermal conditions may influence the pea aphid when the red-pink morph appears in the summer with the green morph doing better in cooler weather. Also crowding and/or reduced plant nutritional value may cause the red-pink morph of the pea aphid to become green. Any ecological significance such as defensive behavior using camouflage or cryptic coloration has not been demonstrated. However, colonies of some species may use color as aposematic warning behavior against birds or other predators as with the oleander or milkweed aphid, Aphis nerii, with its bright yellow color contrasted with black cornicles and cauda, and dark antennae and legs. In other species, some color or pigmented bands may absorb solar radiation that would be advantageous in cool weather.

Aphid Influence on Host Plants Negative Effect Aphids like many sucking insects can have a negative effect on the host plant in one or more of the following ways as will be discussed below: nutrient drain, pathogen transmission, salivary toxins, and honeydew excretion.

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Nutrient Drain When aphids are in sufficient numbers, they can drain the plant of its nutrient sap and cause a breakdown in its tissues. Ironically, it could be this less-healthy situation for the plant that satisfies the nutrient needs of this “parasite.” As a result, the plant may have its leaf area reduced, growth slowed, early leaf fall, become stunted and/or die before its time.

Pathogen Transmission The major danger to plants is probably the damage done only indirectly by aphids sucking sap. The greater harm is done when they are inadvertently the vectors of plant pathogens that cause disease. Most important of such plant pathogens are the viruses. There is a parallel here between aphids transmitting viruses to plants, and mosquitoes transmitting such pathogens as protozoa and viruses to humans resulting in malaria, yellow fever, etc. Like the mosquito, the aphid’s mouthparts are ideally suited for such transmission because the stylets act like a hypodermic needle injecting the virus into the plant as it probes and then sucks the sap. Also, even if the aphid did not have the virus, it would pick it up when it feeds on an already virusinfected plant. A winged aphid (alate) is especially like the mosquito because by flying it can disperse the pathogen to many other host plants. There are two ways in which an aphid vector can transmit a virus from one plant to another: (i) stylet-borne transmission, where the virus contaminates the mouthparts just by the aphid’s probing the host plant. However, this virus is non-persistent on the stylets, lasting only an hour or so, and therefore will eventually disappear on the aphid vector. (ii) circulative transmission, when the aphid actually feeds on an infective plant already having the virus. As a result, the virus invades the body of the aphid. After a latent period, the virus multiplies in the aphid’s tissues and enters the salivary glands, from where it can be injected

into the next plant when it goes to feed. What is especially dangerous about this mode of transmission is that once infected, the aphid maintains the virus for life, and so continues as a vector being able to infect many other plants in succession. In either case, more plant viruses are transmitted by aphids than by any other group of animals, and they probably do more damage this way than by merely sucking the sap from plants. Vegetatively propagated plants such as potatoes are especially susceptible because the disease is transferred with the seed tubers to the progeny causing further yield losses. Weeds sometimes act as host reservoirs for such viruses.

Salivary Toxins Some aphids have toxins in their saliva that cause plant tissues to yellow around the feeding site, and sometimes develop deformities such as leaf-curl, galls, etc. This can negatively influence plant growth and reduce a productive yield of the crop.

Honeydew Excretion This very natural aspect of aphid biology and behavior is discussed later in the section on “Ant– Aphid Mutualism.” In the present context, however, the honeydew that is deposited not only becomes sticky to the touch, but can attract saprophytic sooty-mold fungi to the plant. This may cover the leaf surface and accelerate aging of the plant. It is economically damaging if the fruit or vegetable is blemished and rendered unattractive for sale in a market. Also, car owners are unhappy with this sticky goo on their automobiles if they unknowingly parked under a tree infested with aphids.

Beneficial Effect Some researchers suggest that aphids may be beneficial to plants in a kind of symbiotic mutualism.


In this unproven scenario, plants benefit by having the aphids remove surplus sugars (especially trisaccharide melezitose) which can be utilized by nitrogen fixing bacteria in the soil. As a result, these bacteria increase in the soil beneath aphidinfested plants and make more nitrogen available for the plant’s growth, and hence are beneficial to the plant.

Galling Some species are called gall aphids because they cause the plant to develop swollen tissues called “galls” that are usually on the leaf or petiole. This involves a combination of both inhibition and stimulation of the plant tissue at the feeding site that results from stylet probing and injection of saliva. Galls are hollow outgrowths on the plant and can appear as abnormalities or deformities. This cecidogenesis or gall-forming behavior is not limited to aphids, but is also produced by hymenopteran gall wasps and dipteran gall flies or midges. Although relatively few species of aphids induce galls, the shape of the galls is often characteristic for each species of aphid, so that the aphid seems to have the major role in forming the shape of the gall. Galls not only give protection to the aphid, but may also provide a better food source in the following way. A gall provides sheltered protection for the aphid from insect predators and parasitoids, and the aphid’s feeding may influence the metabolism of the plant and cause physiological changes that could improve the aphid’s food supply. Often, there can be intense competition and aggressive behavior among gall aphids for the best feeding sites on a leaf or petiole where a gall can be formed. The formation of a gall by the plant probably is due to the plant tissue’s reaction to aphid feeding when it probes with its stylets and injects large amounts of saliva into the host plant. It is known that a plant growth hormone called indole acetic acid (IAA) is present in aphid saliva, and so it may be that this chemical induces gall formation.

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owever, this growth hormone normally is found H in the plant itself which may account for its presence in the sap-feeding aphid. Gall aphids synchronize their development with their host plant, and may even modify the development of the host plant itself. Finally, some galling aphids are unusual in having soldiers (see section above on Soldiers), and these species tend to produce completely closed galls on their primary hosts. However, not all aphid galls are completely closed, but in those that are, a monoclonal colony of aphids can exist within the gall that was started by a fundatrix. Hence, there is probably a long evolutionary history between the plant as host and the aphid as parasite in this galling behavior. As is often true in similar hostparasite relationships among animals, the host plant may not suffer unduly in this parasitic type of symbiosis when both organisms have been in contact with each other over millions of years.

Ant-Aphid Mutualism There is a symbiotic mutualism between these two major groups of insects by which the ants obtain a sugar-rich food (honeydew) from the aphids, while the ants protect aphids from predators and parasitoids (see section on Natural Enemies). This is the result of a long-term evolutionary history. An ant that imbibes this sugary honeydew can transport it to nestmates in its crop, and then transfer it to another ant by means called trophallaxis. However, not all species of aphids are antattended, nor do all species of ants attend aphids, and even myrmecophilous (ant-loving) aphids differ in their dependence on ants. Most myrmecophilous aphids live above-ground and are gregarious, rather large in size, and often conspicuously colored. But as a result of this mutualism with ants, these aphids do not have well-developed defensive structures on their bodies, and do not display escape behavior to avoid an approaching ant nor even a predator or parasitoid, perhaps because they feel “safe” in the company of their ant protectors.

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This mutualistic behavior is all the more amazing when it is realized that most ant species are aggressive predators that would normally attack any available prey, especially rather helpless aphids. Yet, the ants that associate with aphids do so in an almost tender way, and “milk” them for their sugary honeydew which comes from the anus. The ant may antennate or stroke the rear of the aphid’s abdomen to stimulate this release of honeydew droplets which the aphid does in an accommodating way without any interruption in its normal feeding behavior. Aphids that are not attended by ants behave differently by raising and contracting the abdomen/rectum, thus ejecting the droplet of honeydew some distance from themselves. Some species even use their hind legs to flick the honeydew away, perhaps to avoid contaminating the colony with this sugary material that might develop sooty-mold fungus. As a general rule, aphids that are not ant attended have a long cauda and long siphunculi or cornicles, perhaps used for defensive purposes against predators and parasitoids, since there are no ants to protect them. Studies have shown that ants can have a positive effect on the number of aphids, and even on the efficiency of feeding by increasing the ingestion of phloem sap with a resulting increase in the production of honeydew as a reward for the ants. Ant attended aphid colonies are usually larger, feed more heavily, and produce fewer winged (alate) offspring. There can also be a stabilizing effect on aphids, so that the size of the aphid colony may be dependent on the presence of ants. However, when an aphid colony becomes too large, the host plant will deteriorate more quickly and the aphids may move off it leaving the ants behind. To avoid this loss of honeydew source, it may be that ants control the aphid population size and keep it stable so that the host plant will not be excessively harmed. On the other hand, if the aphids become too few to produce an adequate supply of nutritious honeydew, the ants may switch to another and larger myrmecophilous aphid

c olony or even to a different aphid species that might be nearby. Ants search plants for aphids, and when they are discovered, the ant returns to the nest laying down a recruitment chemical pheromone trail which worker ants from the nest follow to the aphids. Since many species of ants tend a variety of species of aphids, it has been suggested that at least some elements of the ants’behavior are learned rather than innate. Both ants and aphids make great use of intra-specific and perhaps even interspecific pheromonal communication. Most ant colonies tend a number of aphid species simultaneously, and it seems likely that there is competition between the aphids for the ants’attention. Seasonal changes in ant availability and their demand for honeydew might be factors in this competition. In temperate regions, host plant availability for aphids and therefore honeydew production vary seasonally, as does the ants’ability to collect these sugars. It is unclear to what extent there may be predation of aphids by their ant “protectors,” but it seems that a significant amount of predation does indeed occur. Perhaps the ants need some protein as well as carbohydrates from honeydew, and in a coevolutionary way the aphids may find limited predation (especially in large colonies) a necessary price to pay for protection from natural enemies, and even for the removal of potentially contaminating sugary honeydew.

Natural Enemies of Aphids This discussion will be limited to the natural enemies of aphids that are themselves insects, and not other animals such as birds, nor even pathogenic fungi, etc., that also can kill aphids. In entomology, insects that attack, feed on, and kill other insects are called entomophagous insects. However, in the present context, insects that kill aphids are more precisely called aphidophagous insects. As a general introduction, some definitions must be given. Insects that attack, feed on,


and kill other insects (not just aphids) are divided into two major categories:

Predators Predators are insects that attack, feed on, and kill the prey directly. Depending on the species of predator, both males and females as well as the immature stage and/or the adult can do this. Usually, more than one prey is required for the predator to reach adult sexual maturity. Predators of aphids expend energy and time searching for prey, and so maximum efficiency is achieved when the predator finds an entire colony of aphids and not just an individual. Once in a colony, many predators proceed slowly and stealthily so as not to raise an alarm. An extreme example of such a predator would be the blind, legless larva of a syrphid hoverfly (mentioned below). Examples of major predators of aphids are given next:

Ladybird Beetles (Order Coleoptera, Family Coccinellidae) These are the best known of aphid predators, and they feed both as immature larvae and also as adults. These are very familiar beneficial insects, but often incorrectly called “ladybugs” because “bug” should be limited to the true bugs in the order Hemiptera that have piercing-sucking mouthparts. They have a convex shape and usually colorful markings. Because they are very common wherever aphids are found around the world, they have been intensely studied for their use in biological control programs. The coccinellids that are brightly colored are demonstrating warning or aposematic behavior, i.e., they are distasteful to their own predators, such as birds. Even their eggs are often orange or yellow. The larvae that hatch from these eggs are notorious for their cannibalism on coccinellid eggs and other smaller sibling larvae because they have to feed almost immediately on some prey or die. As the larva molts and

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increases in size, it can sometimes consume more than 100 aphids per day. The larva has pointed jaws which it uses to pierce the aphid cuticle. Saliva is then injected into the aphid which digests the body contents into a semi-liquid which can be sucked up. Solid remains of the aphid may be eaten later if the larva is large enough. However, coccinellids have their own natural enemies especially in the orders Diptera and Hymenoptera.

Lacewings (Order Neuroptera, Families Chrysopidae, Hemerobiidae) These are delicate “nerve-winged” insects with large transparent wings that are often colored light green or brown as is the body. Depending on the species, they feed both as larvae and adults, and are considered important predators of aphids (perhaps second only to coccinellids) and have therefore been used in biological control programs. The larvae have hook-like piercing jaws that are used to suck up the body contents. The aphid prey is held up in the air while it is being eaten. In some species, the adult lacewing lays eggs with each one attached to the end of a vertical stalk which is quite visible when many eggs are laid together on a leaf.

Hoverflies (Order Diptera, Family Syrphidae) As the name indicates, the adult flies hover in the air over one spot, and then dart to another location. The adults can be seen visiting flowers where they feed on nectar and pollen, and so are also called flower flies. The abdomen is often brightly colored with bands of white or yellow contrasting with a black background, perhaps as mimicry of wasps. It is not the adults that eat aphids, but rather the female lays her eggs close to or within an aphid colony. From each egg hatches a dipteran larva or maggot that is blind and legless, dorso-ventrally flattened and tapered at the anterior end. Like

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lacewings, the syrphid larva feeds on the aphid by piercing and sucking out the body contents, while holding the prey aloft.

Cecid Flies (Order Diptera, Family Cecidomyiidae) These tiny flies are often called gall midges although the species that attacks aphids do not form galls on plants. Hence, these cecid flies are also called aphid midges, but the adult does not feed on aphids. Each female can lay about 100 eggs on leaves and stems of plants infested with aphids. It is the maggot-like larva that feeds by piercing the aphid with its long serrated mandibles, sucking out the body contents.

Anthocorid Bugs (Order Hemiptera, Family Anthocoridae) These are called minute pirate bugs or flower bugs because they are often found on flowers where they may feed on plant juices. Most species are general predators on thrips, mites, and other small arthropods besides aphids. However, the two genera Anthocoris and Orius are predominantly aphid predators. Being hemipterans, they have simple or incomplete metamorphosis, and the adults as well as the nymphs feed on aphids by sucking out the insides through their styliform mouthparts.

Parasitoids Parasitoids are insects (orders Hymenoptera and Diptera) in which the adult female attacks what is called the host, but she only indirectly kills the host because the female merely lays her egg in, on or near it. It is the larval offspring from the egg that actually feeds on and kills the host. In older literature, these parasitoids were called parasites, but this terminology was misleading because a

true parasite (flea on a dog) usually does not kill the host (dog). Parasitoids of aphids are micro-wasps (4 to 5 mm in length or smaller) in the order Hy menoptera, and are usually classified both taxonomically and behaviorally in only two families, Aphelinidae (superfamily Chalcidoidea) and Aphidiidae (or Family Braconidae and Subfamily Aphidiinae) (superfamily Ichneumonoidea). These parasitoids are quite host specific in using only aphids as hosts (and no other group of insects). But, even among the thousands of aphid species as possible hosts, different parasitoid species display a feeding behavior that ranges from a continuum of polyphagy to a certain host specificity of oligophagy to monophagy, so that many species of parasitoids limit their attacks to only one or a few species of aphids. Using as an example a typical species in the genus Aphidius in the family Aphidiidae, the female micro-wasp is quite host-specific, and is called endophagous because she lays an egg inside the live aphid. Her ovipositional behavior is to attack the aphid with a quick thrust of her ovipositor which is usually brought forward between her legs, and is positioned in front of and beneath her head. After the egg has been successfully deposited inside the live aphid, the female departs to attack another aphid, and her involvement with the first aphid is ended. Her offspring, however, is the parasitoid larva that hatches from the egg inside the live aphid that will ultimately kill the aphid. Oddly enough, the aphid host usually continues to feed on the host plant as if nothing had happened and without changing its normal behavior. Over a period of approximately 8–10 days that varies with the species of aphid and parasitoid, the larva molts several times while gradually devouring the aphid internally, finally killing it. Then the fourth and last larval instar spins a cocoon inside the dead aphid, whose exoskeleton becomes hard and changes from its original color to brown (which is now referred to as a “mummy”). The parasitoid larva may fasten the ventral side of the mummy to the leaf. It pupates inside the mummy,


and approximately 4–5 days later (or about 12–15 days after the original oviposition) the new adult wasp parasitoid cuts a circular emergence or exit hole in the mummy (usually in the dorsum of the abdomen) and pulls itself out. The adult wasp will find a mate within a short time after emerging from the dead aphid mummy. When fertilized, this new generation of adult female will start the cycle again by attacking and depositing her egg inside another aphid. Note that it is the parasitoid larva that feeds on and kills the host aphid, not the adult female that only oviposits inside the aphid and then departs. Remember that during the moderate summer months, there are long periods in the life cycle of an aphid colony when it is sessile and does not move very far away as long as the host plant provides sufficient nourishment. Perhaps for this reason, micro-wasp parasitoids of aphids have been used quite successfully in biological control programs around the world.

Hyperparasitoids The micro-wasp parasitoid described above is technically called a primary parasitoid, and it is considered beneficial because it kills the aphid which may be a pest insect. However, there are other species of micro-wasps also in the order Hymenoptera, but not in the same families as the primary parasitoids of aphids just discussed. These micro-wasps have evolved to a higher trophic level so that we have an example of multitrophic ecology and behavior. At the 1st trophic level is the host plant, then at the second trophic level is the herbivorous or phytophagous aphid, and at the third trophic level is the carnivorous or entomophagous primary parasitoid. Finally, at the fourth trophic level is a different species of microwasp called a secondary parasitoid or hyperparasitoid that attacks the primary parasitoid while it is still inside the aphid. This food web involving four trophic levels of plant, to aphid, to primary parasitoid, to hyperparasitoid has been used as a model system in community ecology.

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Since many aphid species are such worldwide pests, hyperparasitoids of aphids have been especially well-studied, and can be categorized as follows depending on their adult ovipositional and larval feeding behaviors: (i) The female wasp of endophagous hyperparasitoid species deposits her egg inside the primary parasitoid larva while it is still developing inside the live aphid, before the aphid is mummified. But, the egg does not hatch until after the mummy is formed, and then the hyperparasitoid larva feeds internally on the primary larval host still inside the mummy. (ii) The female wasp of ectophagous hyperparasitoid species waits until the primary parasitoid larva has killed the aphid and formed the mummy. Then she drills a hole through the mummy, and deposits her egg externally on the surface of the primary parasitoid larva inside. After hatching, the hyperparasitoid larva feeds externally on the primary larval host while both are still inside the mummy. In both cases, the hyperparasitoid larva then pupates inside the mummy, and as with the primary parasitoid described above, the new adult wasp hyperparasitoid cuts an emergence or exit hole in the mummy (usually in the dorsum of the abdomen) and pulls itself out. The adult wasp hyperparasitoid will find a mate within a short time after emerging from the dead aphid mummy. When fertilized, this new generation of adult female hyperparasitoid will start the cycle again by attacking and depositing her egg in or on a primary parasitoid larva inside another aphid. There is an economic interest in hyperparasitism because if primary parasitoids are considered beneficial insects (especially when used in biological control programs) then it would seem that hyperparasitoids that attack primary parasitoids might be detrimental. On the other hand, some ecologists suggest that perhaps hyperparasitoids play a positive role in the ecosystem by preventing an excessive increase in the numbers of the primary parasitoids that might so reduce the p hytophagous host as to result in the local elimination not only of the insect pest, but also the beneficial primary species as well. If more phytophagous insects of

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the same species (such as aphids for example) were to move into this local area without sufficient primary parasitoids to attack them, then there might be a resurgence of the insect pest.

(biological control), host plant resistance (HPR), modifying aphid behavior, and finally integration of these methods (IPM).

Aphid Defenses

Chemical Control and Resistance

As mentioned earlier in the section on polymorphism, there are aphid soldiers in a few species that perform an altruistic role. These are female nymphs that have morphological adaptations to defend a colony against predators. Even if they are not killed in this action, they do not reproduce. Usually, species that have soldiers tend to form closed galls on their primary hosts (see section on Galling). However, the majority of aphid species do not have soldiers, yet many species are still capable of defending themselves by various means such as the following: aggressive kicking, thick defensive cuticles and/or spines, waxing predators and parasitoids, using stylets to attack and kill eggs of predators and even other species of aphids, or suddenly falling off the leaf onto the substrate as a tactic that permits their escape from an impending attack by an aphidophagous natural enemy. Some aphids also emit chemical alarm pheromones that warn other aphids nearby of imminent danger. In this regard, it is interesting that some aphid alarm pheromones may also act as kairomones (communication chemicals between different species) so that predator coccinellid beetles are actually attracted to the aphids.

Prior to World War II, chemical control of aphids was limited to nicotine and arsenical products. These aphicides were sprayed on the crop, and at the time seemed to have little negative residual or systemic effects. After the war, however, DDT and other chlorinated hydrocarbons were developed and widely used as broad-spectrum insecticides that were considered to be a panacea not only for control of aphids, but for many other insect pests as well. Although not systemic, they did have residual effects that in the beginning seemed to be a benefit because they were long-lasting. But eventually, evidence from field studies demonstrated that these residues persisted in the ecosystem, and accumulated in the food chain causing unexpected dangers to non-target organisms, especially to fish, birds, and even mammals. In addition, the unintended killing of beneficial insects that were the natural enemies of the insect pest resulted in pest resurgence, traded-pests, etc. The excessive use of these chemicals with these dangerous side-effects was eventually banned in many countries around the world. New generations of chemical insecticides were developed such as the organophosphates, carbamates, and pyrethroids. To control aphids, special aphicidal properties were emphasized:

Control of Aphids

1. Selective toxicity: predators and parasitoids not killed, nor any other non-target organisms. 2. Systemic activity: chemical is applied not only to foliage and seeds, but especially to the soil where the roots take it up via the vascular system where aphids feed on the phloem sieve tubes. 3. Residues: Some residual activity may be needed to prevent aphids from reinfesting the crop. In the case of food and fodder crops, however, chemical persistence can be dangerous. Aphicides on such

Prevention of damage to plants is especially important when a major agricultural crop could be destroyed by aphids at great financial loss to the farmer. Even forest and shade trees have economic as well as esthetic significance when they are used for logging or as parks. Control involves using methods to protect the crop from aphid attack by various means such as chemicals, natural enemies


plants should decompose into harmless compounds before harvest. 4. Rapid action: to prevent transmission of non-persistent viruses, quick mortality of aphids is necessary. Some synthetic pyrethroids show repellent action that deters aphids from settling. 5. Low phytotoxicity: the aphicide should not harm the crop itself because the purpose of the chemical is to protect the plant from aphids without having a toxic effect on the plant.

Application of Aphicides No general rule can be given because so much depends on local conditions, type of chemical, length of growing season, aphid population size, time of day, weather, etc. Sometimes soil or seed application is sufficient instead of dusting or spraying, and of these two, if the crop is dense, then perhaps dusting is better than spraying. Farm advisors should be contacted because they know the local situation for making recommendations.

Resistance It is well-documented that chemical insecticides are powerful agents of natural selection so that over time some mutated insects such as aphids develop resistance. This renders the chemical inefficient, resulting in attempts to restore success by repeating applications, then increasing the dosage, etc. In addition, as mentioned above, the beneficial natural enemies are also negatively affected. There are reports of 20 or more aphid species that have developed resistance to various chemical insecticides. The green peach aphid, Myzus persicae (Sulzer), is an excellent example. It is a notorious aphid pest that not only has secondary hosts in over 40 different plant families, but it is one of the most important vectors of over 100 plant viruses. Although M. persicae is probably of Asian origin, it is now found worldwide.

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As a result of many years of subjection to chemical insecticides, natural selection has developed resistance in large populations of many aphid species not only in the field, but especially in greenhouses. The biochemical cause of resistance in aphids is still being studied, and there seems to be a positive correlation between resistance and the activity of enzymes (esterases). It has also been suggested that symbionts are involved in resistance. In any case, although some chemical aphicides may still need to be used, they should be applied judiciously to avoid the typical insecticide treadmill cycle of excessive dependence on chemicals with unintended results such as pest resurgence, traded-pests, etc.

Biological Control Biological control is the intentional use by humans of an insect pest’s natural enemies such as beneficial insect predators and parasitoids as well as pathogens (bacteria, viruses, protozoa, fungi, nematodes, etc.) in order to lower the population level of the insect pest below the economic threshold so that crop loss is reduced and the farmer can have a successful harvest. In the field, the aphids’sessile feeding behavior for long periods of the year makes them especially attractive to natural enemies. In addition, aphids are amenable to studies in the laboratory where many species can be rather easily reared along with their natural enemies for research and experimentation in insect cages, growth chambers, and environmentally controlled walk-in rooms. As a result, and because of their worldwide pest status (especially in the temperate zones), aphids have been the target of many successful biological control programs. There is an aspect of this method called classical biological control wherein the natural enemy is introduced as an exotic parasitoid or predator from another country or even more frequently from another continent. Also, the insect pest is often an exotic invader into a new habitat or the insect pest could be indigenous. In either case,

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it seems that the indigenous natural enemies are incapable of keeping the new or old insect under control so that it has now reached pest status. To obtain the exotic natural enemy involves foreign exploration and importation, mass rearing, colonization, establishment, etc. Three examples of this type of classical biological control of aphid pests are given here because they are so well documented, and can be easily referenced in the entomological literature: 1. The first case of successful aphid biological control was against the wooly apple aphid, Eriosoma lanigerum (Hausmann), a serious pest of apple in North America and now worldwide in distribution. Beginning in 1920, an aphelinid wasp parasitoid, Aphelinus mali, was imported from the United States and became established in 42 countries with generally satisfactory results. 2. Another success was with the spotted alfalfa aphid, Therioaphis trifolii (=maculata) (Buckton), which invaded the southwestern United States in 1953. Two aphidiid wasp parasitoids, Trioxys complanatus and Praon exsoletum, as well as the aphelinid Aphelinus exsoletum were imported from the Middle East, and resulted in excellent control of this exotic aphid. This case was also important historically because the concept of integrated pest management (IPM) was pioneered during this period by entomologists at the University of California. 3. Finally, although the pea aphid, Acyrthosiphon pisum (Harris), was a Palearctic species, it had existed as an exotic invader in North America since the end of the 1800s where it was a pest on alfalfa and peas. Indigenous predators and parasitoids seemed ineffective, so in 1958 the specialized aphidiid parasitoid, Aphidius smithi, was imported from India into the western United States. Later in 1963, the polyphagous aphidiid parasitoid, Aphidius ervi, was introduced from Europe into the eastern U.S. Both parasitoids have been successfully established resulting in good control. Of ecological interest here is that over time, it seems that A. smithi is being replaced in the west

by A. ervi that was first introduced in the east. However, good control of the pea aphid continues across the continent.

Unlike these three examples of classical biological control involving exotic aphids, it can happen that for various ecological and behavioral reasons the aphid pest is indigenous and the native natural enemies do not control it. In this case, at least the conservation of the existing, indigenous natural enemies is of primary importance. This can even be assisted by augmentation and inundative releases of these indigenous natural enemies from mass-rearing insectaries. Sometimes, exotic but taxonomically closely related species to the indigenous species of natural enemy might be imported from abroad and used to complement the native species, thus improving the possibility of controlling an indigenous pest. In comparison with chemical control, biological control is non-polluting, non-toxic, and selfperpetuating, and makes no claim about completely eradicating the insect pest. Instead, the population level of the pest is lowered to an economic threshold acceptable to the farmer. Since this involves a living ecosystem, biological control tends to be permanent, and therefore less expensive. Needless to say, whether the pest is an aphid or some other insect, proper scientific procedures demand that extensive research be done on the biological aspects of both the insect pest as well as the natural enemies (indigenous and exotic) in relation to the ecosystem. Finally, pathogens such as bacteria, viruses, protozoa, fungi, nematodes, etc., can be used as microbial insecticides against insect pests. Aphid diseases have been recognized for over 150 years, but only entomogenic fungi in the order Entomophthorales have been considered as the main pathogen against aphids. Usually warm and humid weather can spread the fungus very quickly into an epizootic, especially when the aphid colony is crowded. The infected aphid becomes brown and inflated with liquid when it dies of mycosis. This can happen in the tropics and greenhouse, but in


field conditions in temperate regions humidity is not that predictable. Much can still be done to use the potential of fungi in biological control programs against aphids. The other pathogens such as bacteria and protozoa do not seem to have been demonstrated to cause infections in aphids. Although baculoviruses and picornaviruses can be transmitted transovarially and reduce the longevity of an aphid, no viral epizootics of aphids have been reported.

Host Plant Resistance (HPR) Many plant species have defenses against herbivores including insects that is genetically heritable, and hence controlled by one or more genes. Resistance of plants to insect attack is related to the heritable qualities of the plant that may reduce the damage. The main task of agronomists is to increase the yield and quality of a crop by standard breeding methods. However, this can also include trying to breed genotypes into crops that make them resistant to insect attack by using one or more of the following mechanisms: 1. Antibiosis: physico-chemical characteristics of the plant that kill the insect; 2. Antixenosis: pest insect is repelled by the plant or at least has no preference for it; 3. Tolerance: the plant can recover even after some feeding damage by the insect.

Plant characteristics vary depending on the species, but host plant resistance can be morphological (leaf size, shape, color, pubescence, thickness, texture), biochemical (lack of nutrients, allomones [feeding repellents, ovipositional and feeding deterrents, toxins], kairomones [attractants for natural enemies]). Entomologists work closely with the agronomists to test or screen the supposedly resistant crops (but still as high-yielding as possible) to see if indeed these genotypes are also resistant to a particular insect pest that is being studied. To do this, hundreds of insect pests are

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constantly being mass-reared in the insectary. These are used not only for laboratory studies of insect-plant interactions, but especially for the pur pose of bringing them into the field for artificial infestation. In the field, these insect pests are placed on the cultivar to be infested and eventually evaluated as to the amount of damage caused to the plant as it grows. It must be stated, however, that HPR to one insect pest does not mean that a cultivar is resistant to other taxa or even to related species. Furthermore, the genotype may not be resistant to other biotypes or races of the same insect pest species that initially showed host plant resistance. Concerning HPR for aphids, the same general principles and procedures are used as just mentioned above. Hundreds of cultivars have been developed for resistance to aphids for more than fifty important crop plants in the families Leguminosae, Gramineae, Compositae, Cruciferae, Cucurbitaceae, Rosaceae, Solanaceae, etc. The problem of biotypes or races also occurs among aphids because of their parthenogenesis, telescoping of generations, host plant alternation, etc.

Modifying Aphid Behavior Aphid behavior can be modified by both prevention of landing by aphids in flight, and by repelling aphids that have already landed. Flying aphids are attracted or repelled from plants by light of a particular wavelength. When winged aphids first fly, they are attracted to the blue-ultraviolet light from the sky. However, after a period of flight this is reversed, and instead of flying upwards, the sky may repel them and they are attracted to the orange-yellow-green light reflected from the leaves below. This behavior might be exploited by using yellow traps to lure them away from crops in a field (though as yet this has not been demonstrated). The yellow trap can be filled with some liquid that kills the aphids that have landed in them. Yellow traps are used extensively to monitor flights of aphids.

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Plant odors are volatile substances produced by plants that attract aphids in their host selection. Aphids on agricultural crops tend to be polyphagous, so perhaps specific volatile cues are not too important. However, aphids on perennial crops and wild plants are more oligophagous and even monophagous for which plant odors are needed. Hence, attractant baits have been tried as well as repellent chemicals that may also have a role in aphid control. Alarm pheromones are released by some species of aphids when they are attacked by natural enemies. It would be advantageous for flying aphids to avoid landing on a plant where aphid colonies are being attacked and have released an alarm pheromone. Synthetic alarm pheromones have been used successfully, but because some are highly volatile, a formulation with a slow release would enhance this control method. Synthetic chemical repellents would be a nontoxic alternative to insecticides, and are safer to the applicator and to the environment. However, there is a problem with aphids that are vectors of a non-persistently transmitted virus. It would have to have its repellent effect act very quickly before the aphid makes its first probe. Even chemical aphicides have this difficulty in not acting fast enough to prevent that first probe by which an uninfected aphid picks up the virus, or if already infected, then before the aphid probes into a healthy plant. There is a continuing need to study the chemoreception of aphids and their resulting behavioral responses.

Cultural Control This method involves the use of normal agricultural practices to reduce pest damage not only by aphids but also by other insects. Such cultural techniques can include the following: timing of planting and/or harvesting to disrupt the normal cycle of aphid landing and feeding; crop rotation varies the crop during the season or annually with another plant that would be unattractive to the aphid

and/ or less important to the farmer; intercropping uses the same principle but alternates field rows or sections of the crop with another plant; tillage (mechanical manipulation of soil to reduce weeds, improve drainage by plowing, hoeing, etc.); sanitation is the removal of weeds or crop residues that might provide the aphid an alternate host; water management depends on the needs of the host plant and the biology of the aphid species.

Integrated Pest Management (IPM) In their evolution, aphids have taken advantage of favorable agricultural habitats especially through monoculture, thus making the agroecosystem an attractive food source. Although different species of aphids vary in their host range from polyphagy to monophagy, they are often able to survive on herbs in the vicinity of the crop or simply to fly to another area where a more suitable host plant is more available. Realistically therefore, eradication is all but impossible. Because of various side effects mentioned earlier, reliance only on chemical insecticides should not be the main option. Instead, it is sensible to integrate as many of these control methods just discussed. This concept of integrated pest management (IPM) was first developed at the University of California during the late 1950s. An acceptable definition of integrated pest management (IPM) should include the following entomological and ecological aspects: a pest management system that utilizes all suitable control methods to reduce and maintain the pest population level below that causing economic injury, with special concern for the environment including the insect’s natural enemies. This sound ecological philosophy should be applied to aphids and to other insect pests whenever possible.

Important Aphid Species Although there are over 4,000 aphid species, only a small percentage of these are pests. Nevertheless, it


is not surprising that general interest and most of the funded research at universities and institutes should be concentrated on aphid species that indeed are pests of agricultural crops, forest and shade trees because of their commercial and economic importance. With this bias in mind, listed in alphabetical order (English names) is a sampling of some important aphid species: black bean aphid, Aphis fabae Scopoli; black citrus aphid, Toxoptera aurantii (Fonscolombe); blue alfalfa aphid, Acyrthosiphon kondoi Shinji; brown citrus aphid, Toxoptera citricidus (Kirkaldy); cabbage aphid, Brevicoryne brassicae (Linnaeus); corn leaf aphid, Rhopalosiphum maidis (Fitch); corn root aphid, Aphis (Protaphis) maidiradicis Forbes; cotton or melon aphid, Aphis gossypii Glover; cowpea or black legume aphid, Aphis craccivora Koch; grain aphid, Sitobion avenae (Fabricius); green apple aphid, Aphis pomi De Geer; green peach aphid, Myzus persicae (Sulzer); greenbug, Schizaphis graminum (Rondani); oleander or milkweed aphid, Aphis nerii Fonscolombe; poplar petiole gall aphid, Pemphigus populitransversus Riley; pea aphid, Acyrthosiphon pisum (Harris); potato aphid, Macrosiphum euphorbiae (Thomas); rose aphid, Macrosiphum rosae (Linnaeus); spotted alfalfa aphid, Therioaphis trifolii forma maculata (Buckton); tulip-tree aphid, Illinoia liriodendri (Monell); walnut aphid, Chromaphis juglandicola (Kaltenbach); woolly apple aphid, Eriosoma lanigerum (Hausmann). Several of these important aphid species are worth special mention:

Green Peach Aphid Myzus persicae (Sulzer) is probably the most polyphagous of all aphids. As a result, it is the most important insect vector of plant diseases including transmission of over 100 plant viruses such as curly top of sugar beets, peach yellows, cranberry false blossom, aster yellows, and various potato viruses, etc. It is pr obably of Asian origin on its principal primary host Prunus persica (peach), and then followed this host

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wherever it was planted which is now worldwide in distribution. Its secondary hosts are in over 40 different plant families, including many that are also economically important. In temperate regions it is usually heteroecious holocyclic, but can be anholocyclic where peach is absent and the climate permits winter survival. Because it is relatively easy to rear in laboratories and greenhouses, this aphid’s biology, anatomy, physiology, etc., has been intensely researched. In addition, because of its economic importance, the ecology of M. persicae has been studied, especially for use with biological control.

Black Bean Aphid Aphis fabae Scopoli is also heteroecious holocyclic, and in Europe it alternates between Euronymus (strawberry bush) and various secondary hosts where it feeds on many agricultural crops including Vicia faba (broad bean) and other legumes. Besides this polyphagous behavior, it is a vector of more than 30 plant viruses. It is widespread in temperate regions of the Northern Hemisphere, as well as South America and Africa, except for the hotter parts of the tropics and the Middle East. A. fabae may be a complex of species, and outside of Europe where it seems to have originated, its taxonomic status is unclear. However, because of its importance, it too has been intensely studied in both field and laboratory research projects.

Cotton or Melon Aphid Aphis gossypii Glover is very polyphagous not just on cotton and cucurbits, but also on such diverse crops as citrus, eggplant, okra, peppers, coffee, potato, cocoa, and many ornamentals such as Hibiscus. In addition, it can transmit over 50 plant viruses to important crops such as beans, peas, soybeans, crucifers, celery, cowpea, sweet potato, tobacco, tulips, strawberry. Its distribution is now

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worldwide including the tropics and many Pacific islands. In the temperate latitudes with cold temperatures where crops are raised in greenhouses, A. gossypii is a major pest. Perhaps it is of palaearctic origin because it is anholocyclic in Europe. However, it seems to be holocyclic in North America, China, and Japan.

Oleander or Milkweed Aphid Aphis nerii Fonscolombe is an especially interesting aphid because of its attractive bright yellow color contrasted with black cornicles and cauda, and dark antennae and legs. Such aposematic behavior advertises and warns potential predators that it is unpalatable and even harmful. This is because while feeding, it has sequestered poisonous chemicals (cardiac glycosides) from its host plants mainly in the families Apocynaceae and Asclepiadaceae such as oleander and milkweed. It has thus coevolved by transferring for its own protection the “poisonous” defense of these host plants. Instead of using cryptic or camouflage defense as many other insects do, A. nerii demonstrates behavioral convergent evolution with the similarly bright warning coloration (orange and black) of the monarch butterfly that also feeds on milkweed. A. nerii then reinforces this aposematic behavior by forming dense colonies that are frequently concentrated on young stems. Also unusual is its life cycle that seems to be only anholocyclic with no sexual morphs. It is widely distributed in the warmer regions of the Old and New World, plus the tropics and subtropics.

races and subspecies on different host plants, but mostly important legumes such as alfalfa, clover, peas, broad beans, etc. A. pisum is a vector of more than 30 virus diseases, and although probably palaearctic in its origin, it is now worldwide in its distribution where it is holocyclic in the temperate regions, and perhaps anholocyclic in warmer climates. Because it can be reared easily in the laboratory with its micro-wasp parasitoids, as mentioned earlier, it was an example of a classical biological control program that was successful.

Summary Aphids fascinate the non-entomologist as well as amateur and professional entomologists because of their sometimes unique and always unusual biologies. Although small in size, their external morphology and internal anatomy as well as their polymorphism and polyphenism make aphids interesting. One marvels at their reproductive behavior (parthenogenesis, telescoping of generations, sex determination), life cycles (host plant alternation), ant–aphid mutualism, etc. Finally, of course, aphids have had an enormous economic impact as pests on the world’s agricultural crops, forest and shade trees, not only by their feeding, but as vectors of plant viruses. This is a great challenge to humankind to control them by using ecologically safe as well as effective methods. Hence, aphids are a rewarding subject for observation and research.  Bugs  Transmission of Plant Diseases by Insects  Plant Viruses and Insects

Pea Aphid Acyrthosiphon pisum (Harris) is a large aphid with slender appendages and long cornicles. There are both green and red-pink morphs, similar to the potato aphid, Macrosiphum euphorbiae (Thomas), that also has green and red-pink morphs with both aphid species being in the same aphidine tribe Macrosiphini. The pea aphid seems to be a complex of

References Blackman RL (1974) Aphids. Ginn and Company, London, UK, 175 pp Blackman RL, Eastop VF (2000) Aphids on the world’s crops: an identification and information guide, 2nd edn. Wiley, Chichester, UK, 466 pp Dixon AFG (1998) Aphid ecology - an optimization approach, 2nd edn. Chapman and Hall, London, UK, 300 pp

Apiculture (Beekeeping)

Minks AK, Harrewijn P (eds) (1989) Aphids: their biology, natural enemies and control, vol 2A (450 pp), vol 2B (364 pp), vol 2C (312 pp). Elsevier, Amsterdam, The Netherlands van Emden HF (ed) (1972) Aphid technology: special reference to aphids in the field. Academic Press, New York, NY, 344 pp

Aphid Flies Members of the family Chamaemyiidae (order Diptera).  Flies

Aphodius Grubs (Coleoptera: Scarabaeidae) At least two species of Aphodius are important pests of turfgrass.  Turfgrass Insects and their Management

Aphrophoridae A family of bugs (order Hemiptera, suborder Cicadomorpha).  Bugs

Aphylidae A family of bugs (order Hemiptera, suborder Pentamorpha).  Bugs

Apiary A location where honey bees and bee hives are kept.  Apiculture (Beekeeping)

Apical A term pertaining to the apex (tip) or outer end.

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Apiculture (Beekeeping) malcolm t. sanford1, james e. tew2 1

University of Florida, Gainesville, FL, USA The Ohio State University, Columbus, OH, USA

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The science and art of managing honey bees called apiculture or beekeeping is a centuries-old tradition. The first beekeepers were hunters, seeking out wild nests of honey bees, which often were destroyed to obtain the sweet reward, called honey, for which these insects are named. As interest in honey bees grew, so too did the entomological and biological knowledge needed to better manage colonies of Apis mellifera. The innovations that allowed modern beekeeping to arise were primarily developed in the 19th century. The most important include the moveable-frame hive, smoker and centrifugal extractor. It is remarkable that these continue to be the hallmark of the beekeeper a century and a half later. Honey bees are native to the Old World, but were quickly introduced into the Americas and Australia as part of European settlement. This social, perennial insect is now found on all continents and in most environments. Although honey continues to be an important product of honey bees, their most valuable service is pollination. A large commercial pollination effort exists in many countries to ensure maximum quality and quantity of crops pollinated by honey bees. The major crops involved are nuts, berries, fruits and vegetables. Although the technology employed in beekeeping is traditional, the problems facing present day apiculture are modern and formidable. This is due primarily to worldwide distribution of exotic diseases and pests that have devastated beekeeping industries and honey bees alike. The major problems affecting U.S. beekeeping over the last thirty years come from introduction of the tracheal mite (Acarapis woodi), Varroa mite (Varroa destructor) and small hive beetle (Aethina tumida). These have produced a new kind of beekeeping that is much

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more aligned with production agriculture because it has become associated with and/or reliant on chemicals. It is an irony that honey bees, heretofore considered wild animals needing minimal human intervention, have become more domesticated, requiring human help to survive human-induced introduction of exotic species. In spite of the increase in time and effort needed to keep bees in the modern setting, the fascination presented by the honey bee and its products continues. Thus, a small but enthusiastic cadre of novice beekeepers appears each season to take up the challenge of managing one of nature’s most complex creatures. This infectious “joy of beekeeping” continues to proliferate across the generations, afflicting both beginners and commercial beekeepers generations removed from the first person in their family to be smitten by the beekeeping bug. The purpose of this article is to describe aspects of beekeeping that will be important for a basic understanding of the craft by both novice beekeepers and the general public. It includes information on the honey bee colony and its management, as well as that with reference to nectar and floral resources and the use of these important insects in commercial pollination.

Products of the Hive Many people keep bees because they are fascinated by these social insects. The vast majority, however, are also interested in collecting the useful products of the hive, which include: Honey: Modified nectar collected by honey bees that is mostly carbohydrate. Pollen: The male floral part collected by honey bees that is mostly protein. Propolis: A mixture of resins and oils collected by bees from plants used to “glue” hive parts together and patch holes. Beeswax: The material that makes up the bee nest. Royal Jelly: A high-protein food that is used to feed developing queens.

Venom: A mixture of compounds injected by bees for defensive purposes.

The Honey Bee Colony Honey bee biology is described elsewhere in this document. The colony of Apis mellifera is composed of one queen (fertilized female), up to several thousand males (drones) and tens of thousands of workers (unfertilized females). For the purposes of the beekeeper, worker bees are the most important; they are often divided into two classes, young nurse bees (feed the young) and older forager bees (collect pollen and nectar).

Major Developments in Beekeeping Most new ideas in beekeeping are not novel. A scan of the literature usually will show that they have been developed, sometimes on several separate occasions, by enterprising apiculturists in the past. Three eras have been identified in the development of the craft. Beekeeping prior to 1500 was primitive (rustic), and consisted of little more than honey hunting, robbing the sweet from established nests. A famous rock painting at Cueva de las Arañas, Spain, depicts this activity as early as 5000 b.c. The Philistines dabbled in beekeeping as did the ancient Egyptians, Greeks, Sumerians, and others. Even before the honey bee was introduced to the Americas, other kinds of bees were kept for honey and wax. The Inca and Maya of the New World cultured the stingless bees (meliponidae). There is a renaissance in this activity in the American tropics, but the term “beekeeping” has always been reserved for those managing the Old World western honey bee (Apis mellifera). From 1500 to 1851 (pre-modern beekeeping), great strides occurred in knowledge about honey bees. The queen was discovered to be female in 1586. Drones were first identified to be males in


1609. Pollen was determined to be the male part of plants in 1750. Drones were shown to mate with the queen in 1792 and recognized as parthenogenic in 1845. Concurrently with biological knowledge, management technique evolved. For example, the concept of supering (adding boxes on top of colonies for honey storage) was developed in 1665. A wide variety of so-called “patent” hives were marketed in the 1800s, an era known for huge controversy over size and style of box, none of which were really suitable to launch a new kind of beekeeping. The modern beekeeping era began in 1851 when the Reverend L.L. Langstroth discovered the significance of the “bee space,” which led to the invention of the movable-frame hive. Other advances followed: Johannes Mehring developed the first foundation in 1857. Major Hruschka produced an extractor in 1865. Moses Quinby invented the smoker in 1875 and published his first bee book in 1853. Comb honey production began with W.C. Harbison of California in 1857. The years 1859 to 1890 encompassed the era of comb honey, known as the “golden age of beekeeping.” Samuel Wagner published the first issue of American Bee Journal in 1861. Gleanings in Bee Culture was first published in 1873; it became simply Bee Culture in the 1990s. Migratory beekeeping up and down the Mississippi River began in 1878 (it occurred much earlier in ancient Egypt on the Nile). Package bees were first used in 1879. J. George Doolittle developed the concept of commercial queen rearing in 1888, using the grafting (larval transfer) technique. Lloyd Watson first used instrumental insemination of the queen bee in 1926. This technology spawned studies in controlled genetics, which led to selection of commercial lines such as “Starline” and “Midnite” honey bees. This continues to be of importance and increasingly is responsible for advances in selecting for hygienic behavior (disease resistance) and tolerance to pests. With recognition that apiculture was a legitimate vocation, the honey bee has been spread worldwide by beekeepers. This continues even

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today. The Irish and Norwegians may have brought honey bees to the Americas as early as 900 a.d. They came to the colony of Massachusetts in 1665, where the aborigines called them “white man’s flies”. These insects may have been introduced sooner into the New World by the Spanish conquistadors via Mexico, Florida, or Cuba. Italian bees (Apis mellifera ligustica) were first introduced into the United States in the 1860s, and Frank Benton imported Cyprian and Tunisic stock in the 1870s. Many more introductions succeeded these first attempts. African honey bees (Apis mellifera scutellata) were brought to Brazil in 1957. Semen from these so-called “killer bees” was introduced into the United States in the 1960s, but natural migration through Latin America allowed a population to become established in the United States only when it crossed the Texas border in 1990. Varroa jacobsoni (now known as Varroa destructor) was introduced to Apis mellifera in the 1950s via its original Asiatic host Apis cerana. This parasitic mite had spread to all continents except Australia by the 1990s. New bee foods, including high fructose corn syrup and the Beltsville Bee Diet® were introduced in the 1970s. Honey became a world commodity in the 1980s. The small hive beetle (Aethina tumida) was introduced from South Africa into the United States in 1998.

Sources of Information Beekeeping information can be found many places. Traditional print resources include: Bee Culture, A.I. Root Co., P.O. Box 706, Medina, Ohio 44258, phone 1-800-289-7668 extension 3220, fax 330-725-5624 American Bee Journal, 51 South 2nd Street, Hamilton, Illinois 62341, phone 217-847-3324, fax 217-8473660 The Speedy Bee, P.O. Box 998, Jesup, Georgia 315980998, phone 912-427-4018, fax 912-427-8447

The Internet is now a prime source on information. However, it is suggested beginners find the bee inspector and state university extension

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educator in their state and address questions directly to them. Each year, the magazine Bee Culture publishes a comprehensive list in the April edition.

Equipment Of all things in beekeeping that are affected by the modern world, perhaps beekeeping equipment is the best candidate to look at within the context of newly evolving technology. Plans for standard, traditional wooden beehives can be found in many publications. Some parts of a beehive are easily made at home, especially brood chambers, supers, tops and bottoms. However, others may not be; frame construction, for example, is best left to commercial manufacturers. A major equipment consideration is use of beeswax, recycled from the bees themselves. Traditionally bees have been guided to make their nest (comb) through use of embossed beeswax “foundation.” This material not only guides the bees in making worker cells, but also saves much time and energy in the bargain. Plastic (waxcoated or not) is being increasingly used for foundation. Beekeeping equipment is available from many places across the nation. Several concepts are important when considering equipment. These are: (i) standardization, usually based on conserving the bee space; (ii) changes in nominal lumber size, contributing to availability and wastage problems in cutting wooden ware; and (iii) constant development and evaluation of new materials. Although plastics come to mind, there have even been hives made from concrete to withstand tropical conditions. Nevertheless, wood continues to be the material of choice by most beekeepers. Because individual suppliers or equipment and prices are constantly changing, only an overview of beekeeping implements and paraphernalia is possible here. For up-to-date prices, it’s best to consult the bee journals, which actively cater to the trade and bee supply outlets.

Protective equipment for the beekeeper has also followed the same route. New materials such as plastic netting, Velcro® and others have meant that beekeepers can work with more peace of mind during manipulation of colonies. As already noted, traditional beekeeping equipment is made from wood. However, plastic equipment also is in use for the traditional bee box. Plastic is also widely used as a wax foundation base and in single component plastic frames. Plastic frames resist damage, do not require painting, and do not require assembly. However, it often takes more resources by the bees to “draw out” plastic or beeswax-coated plastic foundation. Some disadvantages of plastic are its tendency to warp and become brittle when exposed to sunlight and difficulty in being sterilized by heat. Various companies use plastic to make containers for bee products. Such containers eliminate the extracting phase of beekeeping and provide a container for honey in its natural comb. There are all manner of gadgets used in the art and business of keeping bees that do not generally get mentioned in standard references. The following are some of these gems: 1. The slatted (or slotted) rack was used initially to take up the space of a deep bottom board. It assists in ventilation and reduces brace and ladder comb. Some beekeepers swear by it, some at it. 2. A division board feeder is a hollow insert filled with syrup that takes the place of a frame in a super when a population is small. Easily homemade from a board and nails, they quickly feed a small colony. 3. A robber screen can be used to protect small colonies from being foraged by larger colonies, especially during nectar dearth. 4. Top feeders come in various styles. These avert the necessity to open the colony and/or to fill a frame-style division board feeder. Top feeders hold more and are more accessible. 5. A screened ventilated bottom board provides air circulation during both summer and winter. Newer information also suggests these are useful in controlling exotic mite populations.


6. Various painted patterns on the front of colonies can help bees identify their own home, thus reducing drifting (bees losing their way and entering foreign colonies). 7. Drip boards serve several purposes. They collect errant honey leaks from supers stored on them, provide air space between the floor and honey stored in frames, and a space for two-wheeled hand trucks to grip the stack. 8. A screened division board placed between two alien colonies enables them to access each other’s odors, while keeping them physically separate. The end result is two queens working together to produce a large population. Eventually they can be joined after this close but separate association, however, one of the queens is eliminated in the bargain.

Building Equipment Although it can rarely be built more cheaply than it can be purchased, only basic woodworking skills and tools are needed to build wooden beekeeping equipment. Box joints are currently the most common, and according to some, the strongest kind to use in beekeeping applications. Producing them requires a jig, usually home made, to neatly and precisely cut the slots to line up with the fingers. Butt joints are more forgiving; two boards are butted together and simply nailed. The TIM joint is fast but weak. If a colony is not going to be moved, it will probably work okay. The dado joint, used by some manufacturers, is becoming more popular, and is strong enough to withstand the rigors of moving and manipulation. When building equipment, in all instances, respect bee space requirements and be sure to build your equipment to fit standard measurements.

Protecting Wooden Equipment Some wood may last longer while some may last much less time, depending on the climate, but hives are definitely helped by some type of

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protective coating. The average life of a bee box is about seven years. Scraped and routinely painted, equipment can go much longer. Since the inside surfaces of bee hives should not be painted, the paint film on the outer surface is often stressed by water migrating to the film from the inside of the hive rather than from the outside. Oil-based paints will readily peel within just a couple of years. Due to ease of application and lower cost, latex paints are better. The rubber-based latex paints will flex and resist chalking and peeling much more than oil paints, but they, too, will finally succumb to mildew and peeling. Some commercial beekeepers and beekeepers in other countries routinely dip equipment in paraffin or beeswax. This is a good finish that protects the wood from all sides and ends, but requires working around hot, flammable paraffin. Once the equipment has begun to show signs of wear, simply dip it again in hot paraffin to recoat the finish and to remove wax and propolis residue. In recent years, polyurethane exterior stains have become popular and have been consistently improved. As with paraffin impregnation, many of these stains are water repellent, resist mildew and fading, and clean up with water and soap. A final warning concerns pressure-treated wood. The materials used to preserve the wood are usually toxic to honey bees. Thus, treated wood is not recommended for bee colonies. Even the sawdust is considered a health hazard and dust masks are recommended when working so-called Wolmanized® treated wood.

Wearing Protective Equipment The most important protective equipment is the veil, which protects the face, the most sought-after target for guard bees. Veils can be used without a helmet, or attached to a pith-type helmet, made of plastic or other material. Almost any hat that keeps the veil material off the face and neck will work. Veils usually have a mesh bottom that is snugged down over the collar onto the shoulders with a

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variety of ties and/or strings. Veils that attach to the bee suit with a zipper are popular, mostly because they are convenient, easily maintained, and virtually bee proof. They are also more expensive. Bee suits usually are light in color, but many wear what’s available, simply to keep their clothes clean. The white coverall suit is most popular, with a variety of pockets, cuffs and attachments. White is also the most difficult to keep clean. They are made from a variety of materials – cotton, cotton blends and synthetics – each with its own peculiar attributes. Suits should be “roomy,” to allow bending and stretching and lifting room, and for other clothes underneath. This also keeps the suit from stretching tautly over the skin underneath, which bees can then easily sting through. Seasoned beekeepers seldom wear gloves because they feel they lose that “delicate” touch when manipulating colonies. However, many beginners start with them. Most gloves have cloth gauntlets of some type to seal the sleeves of the bee suit. Glove materials range from full leather to plastic to split leather to rubber. Some are ventilated, while others have no fingers. Wearing gloves can help build confidence in manipulating bees. As one gains experience, the finger tips can be cut off, which still protects most of the hand, while ensuring a more sensitive manipulation. Boots and pants-cuff clasps range from high top rubber boots to baling twine. The goal is to keep bees on the ground from crawling up pants legs – an unnerving experience. Comfort, durability, safety and cost are all important. All equipment should fit the job. A hobbyist with a few colonies will use, and need, different equipment than a commercial pollinator.

Management The “meat and potatoes” of beekeeping is management. It is often the best manager who makes the most honey from his/her bee colonies. Experience is extremely important if one is to manage bees

successfully. There is no better piece of advice for the novice beekeeper than to begin small and only expand as experience is gained. A vital ingredient of this experience is permanent, detailed record keeping and knowing intimately the characteristics of the honey bee ecotype one is working with. One must also master the basics of opening and inspecting a colony with the aid of smoke, yet not destroying its cohesiveness. Beekeeping knowledge comes about slowly and being able to implement it effectively often takes far longer than expected. In order to appreciate the techniques of beekeeping, one must first gain an understanding of the dynamics of the colony during the year. A recommended exercise for the beginning beekeeper is to construct a beekeeping calendar. Regional characteristics of beekeeping are easily identified through the use of the calendar, which shows average dates of bloom, colony population characteristics and bee manipulations. Such a timetable also can be broken down into a number of beekeeping activities, each requiring certain decisions. These include inspecting a colony in spring, feeding pollen and sugar, monitoring population buildup, controlling swarming, supering, monitoring and removing the honey crop, requeening, preparing for winter and migrating in search of better nectar resources or to move bees into commercial plantings for pollination. No year is ever the same, so the beekeeper must learn to “think like a bee colony,” closely watching environmental changes and anticipating the potential effects on colonies. Major management problems in beekeeping are controlling swarming (the reproductive process of a colony), requeening and managing diseases and pests. Swarming has befuddled even experienced beekeepers. Requeening and queen introduction techniques have been written about for many years, but still confound beekeepers on occasion. Several options often need to be considered for successful introduction of new queens, the life blood of any beekeeping operation. Finally, the challenges of diseases (American and European


foulbrood) and exotic pests (mites, beetles) are complex, requiring an understanding of many possible treatment regimes under the rubric of Integrated Pest Management (IPM). Although controversial, most beginners are advised to begin by managing two colonies. The reasons for this are several. If a hive begins to fail, there are resources in the other the beekeeper can use to help the weaker one along. If one colony is lost entirely, the novice beekeeper may easily lose interest if another colony is not present to take its place.

A Model Bee Yard Somewhere the perfect bee yard exists, but if so, it is not the general rule. Most are the result of a beekeeper’s style that fits both location and management philosophy. Bee yards should be right-up-next-to-the-hives easy to get to all year long. Newly plowed fields, suddenly erected fences, rising creeks, muddy roads, locked gates and the like should be anticipated, and avoided. The most accessible location is worthless without something for the bees to forage on. There should be enough blooms to produce surplus honey for every colony in the apiary. Field crops, hay crops, tree canopies, weed species, horticultural or oil crops all can work. But there needs to be large areas of blossoms blooming a relatively long time. Water is required all season long, too. A lake, stream or pond is best. Swimming pools, cattle troughs or leaky faucets cause potential neighbor problems and should be avoided as bee watering possibilities. A wind break, especially during the colder months in temperate latitudes, is recommended. A tree line, fence or hill works best. Air drainage is important. Cold air drains downhill; colonies at the bottom of a hill get “dumped on” in cold weather. Hill tops, too, suffer winds and wind chill problems. Avoid both. Exposure seems important to some. Colonies receiving morning sun start to forage earlier than those in the shade (at least

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with some races of bees). Southeast is the most common, and probably works best. Bee colonies must be protected from all manner of pests and predators, including humans. Bear (electric fencing), skunks and possum (fencing), cattle and horses (regular fences, though stout), and neighbor prying eyes (screening, hedges) must all be considered. For large bee yards, an out-building that works as a storage shed, work area, extracting room (sometimes) and lunch room is needed. Most of all, a bee yard should be a pleasant place to visit. Scenic, quiet, distant and, most importantly, not a challenge to use.

Inspecting Honey Bees The productivity of honey bee colonies should be actively monitored by the beekeeper, whose job it is to recognize certain conditions and help a colony overcome those causing adversity. Generally, inspection will determine the state of the colony in terms of reproductive ability (queen condition; population of worker bees), nutritional resources (honey and pollen stored in the comb) and whether diseases or pests are present. The latter is increasingly important as exotic organisms continue to proliferate around the globe. Of special significance at the present are two introduced mites, the internal Acarapis woodi and external Varroa destructor. These mites have caused beekeepers to take a closer look at and often use chemical controls inside the living beehive with the concomitant risks that these substances may harm the colony and/or contaminate its products. As a consequence, honey bees have become much more domesticated, as they are increasingly reliant on beekeepers in many areas of the world to help control exotic bee mites. Other diseases that affect colonies are caused by bacteria, fungi, viruses and protozoans. Of particular significance are two bacterial conditions, American foulbrood (Paenibacillus larvae subspecies larvae) and European foulbrood (Melissococcus pluton).

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American foulbrood, in particular, is caused by a spore-forming organism that can resist harsh ecological conditions. Epidemics of this disease are the reason state bee inspection services exist, although many of these have been discontinued recently due to budgetary constraints and lack of support. Discovery of sulfa drugs and later antibiotics has caused a shift in beekeepers’ perceptions concerning the disease, which they have actively kept at bay for decades. Unfortunately, the recent appearance of antibiotic-resistant strains of Paenibacillus larvae subspecies larvae is causing second thoughts by many beekeepers concerning official inspection backed up by apiary legislation. An important adult disease is known as nosema and is caused by the protozoan Nosem apis. This is probably present in every colony of honey bees, but only becomes epidemic when bees are put under stress. It may be far more important in determining bee colony health than is generally given credit. There continue to be numerous so-called “exotic” organisms that impact colonies of honey bees around the world. Ironically, two of these are ecotypes of honey bees themselves: the Africanized honey bee (Apis mellifera scutellata) and the thelytokus Cape of Good Hope bee (Apis mellifera capensis). In addition, various mites are found on Asian honey bees (Apis cerana, Apis dorsata, Apis laboriosa) that conceivably could transfer to Apis mellifera as Varroa destructor did previously. No better example of this constant threat is the surprise introduction of the South African small hive beetle (Aethina tumida) into the United States in the late 1990s.

Honey Bee Ecotypes All honey bees are not the same. This statement, it seems, cannot be said too often around beekeepers and/or the general public. There are those who manage bees exactly the same whether or not their stocks have been selected for overwintering, swarming, rapid brood rearing, pollen collecting

and/or stinging. The belief that all honey bees must behave or act similarly no matter the conditions is the root of many beekeeping controversies over the last two centuries, and the reason many lay persons fail to understand the complexities of these stinging insects. Usually, beekeeping “arguments” pertain to whether or not a certain management technique or a special kind of beekeeping apparatus is practical or efficient. The kind of bee a beekeeper has in his apiaries often will determine whether some concept or idea works or doesn’t work. All too often, however, the bees’ genetics are ignored when contemplating solutions to many of the mysteries of beekeeping. Unfortunately, most beekeepers really do not know what kind of bee they are using. That’s because present bee stock is literally a melting pot of honey bee genes. The predominant races (subspecies or ecotypes) of bees which make up the honey bee genetic mix found in the United States are: Italian (Apis mellifera ligustica), Caucasian (Apis mellifera caucasica), Carniolan (Apis mellifera carnica) and German (Apis mellifera mellifera), the dark bee. Each population evolved under certain ecological conditions and natural selection over a long period of time that have provided them with their own particular survival techniques. These ecotypes are thoroughly intermixed and are extremely difficult to separate in novel environments. In addition, other genes of other ecotypes also are present in small quantities. Because there is such great variability, however, the possibility of quantum leaps in honey bee selection programs is possible. With the coming of the mite Varroa destructor, however, the honey bees’ genetic base has narrowed in many parts of the world. But fortunately there remain pockets of bees that appear to be resistant (tolerant) and these may provide the foundation for rebuilding a honey bee stock devastated by this parasite.

Africanized Bees One of the biggest biological stories of the Americas concerns honey bees. Introduction of the African


honey bee ecotype (Apis mellifera scutellata) has been responsible for raising the public consciousness about these insects. This bee is nothing more than an ecotype adapted to tropical conditions, generally characterized by higher rates of defensive behavior and reproduction. Unfortunately, its fearsome reputation is an outgrowth of sensationalized press coverage of stinging incidents by these so-called “killer bees,” which caused deaths of animals and people in Latin America. As a result many people now view honey bees as aggressive rather than defensive, and think them responsible for a good many human fatalities. The reality is that the number of verified deaths by honey bees is much smaller than reported (almost all stinging insects are routinely called bees). This over-sensationalized topic has affected beekeepers in several ways, most notably by loss of access to beekeeping locations. North America is the last frontier for the Africanized (or African) honey bee and its final distribution is still unknown. Nevertheless, the challenge for many beekeepers in the future will be to strike a balance in their communication with the public about the risks/benefits of their bees. Beekeepers also will have to adapt to this ecotype’s different behavior, which often can be a radical departure from the European ecotypes previously present. A special ecotype inhabits Africa known as Apis mellifera capensis. This bee is characterized by a high degree of thelytoky, which means workers can become laying queens, producing diploid females, in spite of laying unfertilized eggs. This ecotype has created a crisis of sorts in African beekeeping. It is hoped that this honey bee will not be moved out of its homeland by beekeepers and introduced to the rest of the world. The history of honey bee introductions around the world over the last two centuries, however, is not a good omen in this regard.

Smoking Bees Within and outside the dark hive, bees communicate extensively by smell. Nectar, pollen, diseases,

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other insects, brood, the queen, drones – everything in the hive has an odor cue. As complicated as the bees’ odor communication system appears to be, the manner that beekeepers have developed to overcome the bees’ ability to perceive odors, both inside and outside the hive, is relatively simple, and that is to puff cool, white smoke in and around the hive. For reasons not clearly understood, smoke stimulates bees to move to honey stores and engorge, which reduces their propensity to sting. Early smokers were little more than a smoldering fire beneath or near a hive. Later, tobacco pipes were modified to direct smoke into hives as were other devices. After evolving through many different designs and styles, beekeepers in North America have a small, but adequate range of smoker designs from which to choose. Smoker fuels are as numerous as are the beekeepers who use them. Common types include grass clippings, pine straw, sumac pods, cloth rags, rotted wood, wood shavings, and burlap. Essentially, anything can be used that produces cool, white billowing smoke and has not been treated with pesticides, fire retardants or other noxious chemicals. Under normal conditions, smoke is effective for about 2 to 4 minutes before needing to be reapplied.

Moving Bees Bees can be moved almost any way imaginable. Some, of course, are easier and safer than others. Commercial operations need the economy of size and efficiency. A large, flatbed truck serves that purpose. Some come with a flatbed trailer that attaches to the truck to increase efficiency. These trucks usually have customized tie-downs, tool boxes and equipment storage areas. Getting the bees on and off the truck can be done by hand (muscle) or machine. Regular two-wheeled carts, sized to hold hives, often are used for moving. Motorized carts are common, as are booms and Tommy-lifts. Fastest

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are fork-lifts. There are several models available, from the standard, to large, specially designed models for specific bee pallets. Some have cabs, most have protective cages and large tires to navigate easily in muddy conditions. Some can swivel or pivot in the center. Once loaded on the truck bed (many are built to hold an exact number of pallets), tie-downs can be regular rope, self-tightening straps, or wide canvas belts affixed to wooden frames that are used for extra security. A secure net is required at all times to avoid escaped bees on the road. Anytime bees are moved, the boxes should be fastened, entrances closed, the load netted and tied down to prevent shifting. An important consideration in moving bees is temperature. Traditionally this has been managed by periodically spraying the load of bees with fresh water when signs of overheating are evident.

Package Bees The most common way to start a colony, or start beekeeping, is to install a package of bees into an empty home-to-be by removing them from the shipping cage. Packages generally come in threeto five-pound sizes (3,500 bees equal a pound). And there are nearly as many ways to get bees from the shipping cage to the functioning unit as there are people doing the task. But basic biology dictates certain principles be obeyed. A starter box with some or all drawn comb is better than just frames with foundation, as it gives the bees some place to be, and store food immediately, and reduces the amount of gathered food required for wax production, freeing it for brood food. Bees can be “moved in” by dumping them (they are often sprayed with water first to inhibit flying) inside the box (with three frames removed, then replaced, to accommodate the resultant mass); they also can be dumped directly in front, to march right in; or a combination of the above two techniques, where some are placed inside, the remainder outside. The empty package is removed

in a day or so. Once installed, several precautions are recommended. The first rule is: feed, feed, feed. Then feed more, until they don’t take any more. Feeding well into the summer may be required if adequate forage is not available. Checking for queen acceptance, and then queen production is a must, but there is a fine line between too-often and too-seldom observations. It is safer to edge toward the too-often, but just barely. Once established, remove feeders, add supers and prepare for the honey flow and harvest.

Dividing Colonies Splitting a colony is the easiest and least expensive way to increase the number of hives managed. But there are other reasons to split a colony, and there are nearly as many ways to split one as there are colonies to split. The overall principle in making a split is to start with a large, healthy, populous colony (or colonies). The goal is to remove some uncapped brood, some honey and pollen resources to a new box, or two, to start a new colony. A new queen may, or may not be, added. Usually the parent colony should not be reduced to less than half its resources so it can continue to keep pace with the season. Bees, brood or food may be taken from more than one parent to successfully build a new split. Splits must have enough nurse bees to care for the brood, some foragers to gather resources, sealed brood for immediate colony expansion, younger brood for continued expansion and some resources for immediate consumption. Splits are used to “make increase,” or for other reasons. Popular swarm control/prevention measures include splitting a large colony to allow room for expansion, and to relieve brood-nest congestion. Often the “new” colony is rejoined to the parent when the swarming urge is over so the actual number of colonies does not increase. One technique used to reduce mite infestation is to divide a colony later in the season, eliminating the older, infested bees, and overwintering the younger, less infested bees.


Feeding Colonies Providing food to colonies is one of the most timeconsuming and tedious tasks facing any beekeeper. Two types of food are required: carbohydrate and protein. Generally, carbohydrates are provided by nectar in nature and the best analogy to this is sugar syrup, made up by dissolving cane sugar in water. This is then provided through various hive modifications or feeders, some of which are mentioned elsewhere in this article. A relatively new bee food is high fructose corn syrup (HFCS) that is manufactured in huge amounts to service the soft drink and candy trade. Two types exist: 42 and 55. The 55 is generally considered more acceptable to bees because it has more sugar solids. Many beekeepers consider feeding both sugar syrup and HFCS, depending on hive condition. Sugar syrup high in sucrose is considered superior for colony population build up, while HFCS is used strictly to maintain populations. Most suggested feeding regimens concentrate on providing carbohydrate. However, it must be complemented with protein for a balanced diet. This is provided by pollen to the honey bee in nature. The beekeeper, too, can trap and give back pollen or combine it with soy flour and/or yeast (supplement). Protein supplement often is sold ready-made in patties by beekeeping supply outlets.

Producing the Honey Crop The beekeeper seeks to have as large a population of worker honey bees as possible coincidentally when the most nectar-producing flowers are blooming. This nectar is stored above a bee colony in the wild. Thus, beekeepers emulate this by adding extra boxes on top of hives (supers) into which bees place the nectar. Nectar is modified by the bees into honey. The insects add enzymes, changing the material chemically, and reducing the moisture content from 80% (nectar) to about 18.6% (honey). The bees determine when the moisture is correct and then cap over the honey

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with wax. When the supers are filled, they are removed and the honey is extracted from the comb using centrifugal force in special machinery (extractors). Sometimes honey is sold in the comb (known as section or comb and cut-comb).

Extracting the Honey Crop A large honey crop is clearly a mixed blessing. The more supers that go on, the more honey to be processed. More honey means more work, but it also means more money. For years, clever people have tried to develop equipment to make the uncapping, extracting, pumping, filtering, and bottling procedure more convenient, even easy. Though “easy” extracting has not yet been achieved, the process has become much more streamlined. Old processing equipment was made from galvanized tin with lead solder joints. It was solid equipment that was built to stand years of heavy use. The clutch-drive mechanism was simple, heavy-duty, and a bit dangerous. Belts, drives, shafts, and pulleys were all exposed. In fact, a few early extractors were powered by low compression gasoline engines. Extracting was done outside on occasion, a practice that generally has been abandoned. Stainless steel with welded joints is now used on extractors. Other metals may impart an objectionable odor. Smaller hobby-type extractors may use plastic barrels. In many instances, variablespeed direct-current (DC) drive motors are used that allow for the gentle extraction of full combs of honey. The equipment is mechanically simpler, but technologically more complicated. It’s lighter and more maintenance free. Most commercial honey processing lines would be ordered as follows: 1. uncapper 2. extractor(s) 3. heated sump 4. honey pump 5. filter 6. settling tank 7. bottler

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Other equipment in honey processing can include a barrel melter, a flash heater, wax spinner and other equipment-moving devices. A second line would drain honey from wax cappings to the sump. Dried cappings would be melted into beeswax, which could be returned to the bees as foundation.

Managing Swarming Swarms can be both reproductive and migratory. Little can be done about swarming once the “impulse” is generated in a colony. The best ways to control swarming are providing room in the colony and/or regularly requeening with younger individuals. This is a “preventive” strategy that is much more effective. As stated earlier, once the impulse to swarm gets going, it is almost impossible to stop. Generally swarms are reproductive in nature, especially with European honey bees, and can be both a blessing and a curse. The blessing part is that one can be harvested and put to work in an apiary. A secondary blessing, obviously, is that a swarm happens. That means a colony is healthy enough to swarm, something all too rare in these days of increasing stress on managed honey bees. The first thing to do with a swarm is collect it. At times this is easy, sometimes impossible. Swarms high in the air can be collected with vacuum devices, long ladders, or heroic gymnastics. Most can be collected into bags, boxes, supers or whatever and transported to permanent housing. The key is to provide ventilation; putting a strong swarm into an air-tight container is a recipe for disaster! Swarms are generally the gentlest of bees, but if left exposed for several days, they can become hungry and much more defensive. Always have a lighted smoker at the ready when working swarms. The public relations aspect of swarm gathering should not be overlooked. But the macho image many beekeepers display while on the job communicate a mixed message. Once collected

and transported, a beekeeper can do many things with this bunch of bees. The deciding factor is often the size of a swarm. Large swarms, about four or five pounds of bees (3,500 bees equal one pound), can easily survive by themselves. Smaller swarms of one to three pounds can be combined with other swarms to start a large colony; or added to another colony to boost its nectar- and pollengathering capability during a major flow. To be safe, all swarms should be considered infested with mites and treated accordingly. As the queen heading the swarm is from essentially unknown heritage, replacing her with a young one of known parentage should be considered. With the advent of the tropically adapted Africanized (Apis mellifera scutellata) honey bee, another kind of swarming is increasingly seen. This is the migratory swarm, thought to be brought on by stress such as lack of forage or water. This kind of swarm often behaves differently than the reproductive one and may be much more defensive, though not always so.

Managing and Rearing Queens The queen is the key to managing the genetic component of a colony. She contributes one half of all the genes found in a colony, whereas a single drone provides for less than half (queens mate with 17 to 20 drones during a short period in their life just after emerging from the cell). The colony’s characteristics, therefore, have a good chance of being perpetuated in the queen and research has shown that queen selection followed by open mating will ensure a good deal of progress in breeding bees with specific traits. Queen rearing is one of the most demanding beekeeping activities, and more often than not is a true art form. Anybody can produce a queen, but rearing a quality queen with the correct genetic complement for a beekeeping operation is far more difficult. Queen rearing also is directly tied to a timetable, which must be rigidly followed. Often the question is raised whether or not one


should produce queens him/herself, let the bees do it, or purchase a queen. There is no easy answer. The only reply may be to ask the question, “Whose quality control is the best under the circumstances, that of nature or of human beings?” Again, the queen honey bee usually mates with many drones. This ensures large genetic variability, but also means a lack of controlled breeding. It is possible to instrumentally inseminate queen honey bees in an attempt to control genetics in a population. This is not easy, however, and can only be accomplished by trained workers. Most queen rearing facilities produce daughter queens from selected stock that are open mated (uncontrolled) in a natural setting.

Managing Wintering The honey bee can live in almost any climatic environment, but is most stressed by winter in continental climates. Honey bees can produce a warm brood nest even in the coldest winters if supplied with the proper nutrition and number of workers. This leads to the adage that “honey bees never freeze to death, they starve to death.” Beekeepers in cold climates, therefore, have a significant challenge to help their colonies overcome severe conditions of wind and cold. Many pack their hives wintered outdoors in various kinds of materials to conserve warmth. Others move their colonies indoors to protect them. The latter activity was employed by old timers who put their colonies into cellars. This was risky as too much warmth would stimulate a colony to begin to build population, a prescription for disaster. With development of refrigeration, however, it now is routine in some areas to bring smaller-than-normal hives (nuclei) into climate-controlled buildings and keep them in a kind of human-induced diapause, which reduces nutritional requirements to a minimum and conserves worker bee energy and vitality so they can begin to rear brood quickly and efficiently in spring.

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An alternative to wintering is to simply c ollect all the stores and kill colonies off in winter, establishing new hives the following spring with package bees from more tropical areas. This was routinely practiced by Canadian beekeepers who simply purchased bees from the southern US until the border was closed in the early 1980s due to introduction of tracheal and then Varroa mites. To many beekeepers this was a repugnant practice and they were not sorry to see it abandoned. Effective wintering continues to be an important part of bee management as more colonies are lost during this trying time than other seasons of the year.

Nectar and Pollen Sources Nectar and pollen are the only natural foods of honey bees, strictly vegetarian insects, and each geographic area has different sources of these important foods. Every good beekeeper, therefore, must be somewhat of a botanist in order to make sure the bees are located so they have an adequate food supply. Bee plants may also differ from each other in several ways, such as the kinds of nectaries (nectar glands) each supports and/or the time of day they may secrete nectar and/or produce pollen. Nectar and pollen production by flowers is dependent on a great variety of environmental conditions such as soil moisture, pH, profile and fertility, as well as rainfall distribution, temperature and humidity. Over the last four decades, there has been an overall decrease in honey bee forage in the United States due to many factors, especially changing agricultural patterns and increasing urban development. Improving nectar production by genetically selecting for varieties of certain crops that produce large amounts of nectar, or purposely planting nectar-producing varieties in so-called “waste” land, along roadways or on lands reclaimed for mining, are some ways suggested to reverse this systematic reduction of bee forage.

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Few plants produce the vast quantities of nectar the honey bee needs to make a large honey crop. In the state of Florida, for example, less than ten plants are responsible for sizeable honey crops on a consistent basis. Fortunately, in most areas a number of minor nectar crops usually are found which help support honey bees throughout the year, although they often contribute little to the beekeeper’s honey crop. It is of more than passing interest to know that many introduced plants assist honey bees in a number of ways, and the insects may contribute to their proliferation. Though not as readily available as honey, another type of sweet is collected and processed by honey bees. Aphids and other sucking insects often take more than they need from the plants. The excess is extruded and may be collected by ants or honey bees. The resultant product is honeydew. Some think this might have been the “manna” that descended from heaven as noted in the Bible (Exodus 16:1–36).

Commercial Pollination Honey bees are cosmopolitan pollinators, transferring pollen both within and between flowers. Although important to many crops (fruits and vegetables), honey bees are not the most effective pollinators in many situations. This has led to some proclaiming that other bees should be used in preference, such as bumblebees (Bombus sp.) and/or blue orchard bees (Osmia sp.). However, honey bees have significant advantages including very large populations that are easily moved, and a well-known rearing technology. There is no stable pollination service in the United States of the kind described by S.E. MacGregor in his classic volume on insect pollination. This means that pollination is carried out by a number of independent contractors. More recently, pollination brokers in the western United States have become more common. The vast majority of commercial pollination takes place in California on the almond crop. Literally hundreds of thousands of colonies are needed.

Commercial pollination is a service, a much different business than producing a product like honey or pollen. As such, it is not suited to all beekeepers and each should look carefully at the characteristics of this enterprise before dedicating many resources to it. Recently, pollination has received more respect from the general public due to a scarcity of feral or wild honey bees caused by devastating effects of exotic bee mites. This represents a teachable moment for beekeepers, who can now describe with pride the value of their insect charges to the public at large.

Honey Contrasted to Pollination Honey is a world commodity, and is labor intensive to produce. As such, the price of the product can always be expected to be influenced by societies with low labor costs. Indeed, beekeeping is being promoted aggressively as a development tool in many countries because it is relatively environmentally friendly and not capital intensive. Although honey can be imported cheaply in many instances, a process exacerbated by globalization of world commerce, pollination services cannot. In addition, because no food product is involved, chemical treatment for exotic pests (mites) can be applied in a more forgiving way to colonies used strictly for pollination. This means that in the future there will always be a demand for pollination no matter the price of honey. Because commercial pollination seems more assured in the future, beekeepers should continually carefully consider this activity in their enterprise mix.

Conclusion The future of beekeeping or apiculture continues to be mixed. On one hand, the honey bee will be more and more important as growers and the general public continue to realize how necessary this insect is for

Apivorous

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producing a quality food supply through pollination. Because honey is a world commodity, it also is continually under price pressures in developed countries, as it represents a good source of income for countries with a labor-intensive work force. Its reputation is also at risk, however, given the chemicals needed to keep (treated) bee colonies alive and the potential they have to damage the sweet’s reputation through contamination. Whether or not honey and/or pollination are primary, there also are other reasons to keep bees, including using their products, both manufactured (royal jelly, honey, beeswax, venom) and collected (pollen, propolis), for the benefit of humanity, as well as for the general joy of communing with nature and one of its fascinating social organisms. The history of beekeeping activities is long, and it takes time and experience to become a proficient manager of honey bee colonies. This article can provide only some of the basic information on the craft. The authors hope that it will serve as a catalyst for those thinking of taking up the activity, and also a source of basic information for anyone interested in one of humankind’s most fascinating activities.  Honey Bee  Bees  African Bee  Cape Honey Bee  Varroa Mite  Small Hive Beetle  Bee Louse  Pollination by Osmia Bees  Polination and FlowerVisitation

Agricultural Research Service. Online version accessed June 17, 2002; http://bee.airoot.com/beeculture/book/ index.html Caron D (1999) Honey bee biology and beekeeping. Wicwas Press, Cheshire, CT 363 pp Caron D (2001) The Africanized honey bee in the Americas. A.I. Root Co., Medina, OH Graham JM (ed) (1992) The hive and the honey bee. Dadant and Sons, Hamilton, IL Hooper T (ed) (1976) Guide to bees and honey. Rodale Press, Emmaus, Pennsylvania Morse, Roger A (1972) The complete guide to beekeeping. E.P. Dutton, Inc., New York, NY Morse, Roger A, Flottum K (eds) (1990) ABC and XYZ of bee culture. A.I. Root Co., Medina, OH Morse, Roger A, Nowogrodzki R (1990) Honey bee pests, predators, and diseases. Cornell University Press, Ithaca, NY Sammataro D, Avitable A (1998) The beekeeper’s handbook. Cornell University Press, Ithaca, NY Taylor R (1984) The how-to-do-it book of beekeeping. Linden Books, Interlaken, NY Webster TC, Delaplane K (2001) Mites of the honey bee. Dadant and Sons, Hamilton, Illinois

References

A family of flies (order Diptera). They commonly are known as flower-loving flies.  Flies

Bee Culture, A. I. Root Co., Medina, Ohio, accessed June 7, 2002; http://bee.airoot.com/beeculture/Electronic American Bee Journal, Dadant and Sons, Hamilton, Illinois, accessed June 7, 2002; http://www.dadant.com/. Sanford MT. Beekeeping in the Digital Age, Bee Culture, accessed June 7, 2002; http://bee.airoot.com/beeculture/digital/ Who’s Who in Apiculture, Bee Culture, accessed June 7, 2002; http://bee.airoot.com/beeculture/who/who_2002.htm Online Source Book for Beekeeping, accessed June 7, 2002: http://www.beesource.com/suppliers/index.htm McGregor SE (1976) Insect pollination of cultivated crop plants. Agriculture Handbook 496, published by the

Apidae A family of bees (order Hymenoptera, superfamily Apoidae). They commonly are called bumble bees, honey bees, and orchid bees.  Bees  Honey Bee  Wasps, Ants, Bees and Sawflies

Apioceridae

Apivorous Bee eating. Birds, and some predatory insects such as robber flies (Diptera: Asilidae) kill and consume honey bees or, in the case of blister beetles (Coleoptera: Meloidae), ground nesting bees.

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Apneumone

Apneumone A chemical released by a nonliving substance that is beneficial to the receiver. An apneumone is a type of semiochemical.  Chemical Ecology  Semiochemicals

Apodal The condition of lacking “feet” (tarsi). Fly larvae and some beetle larvae, for example, have simple tubercles that aid in movement, but lack legs, including tarsi.

Apodeme A thickened section of the exoskeleton that serves as a point for muscle attachment. On the external surface, it usually is marked as a suture or fold, but internally there may be a significant invagination.

Apodous Larva A larval body form that is legless, robust, and C-shaped or spindle-shaped. The head may be well developed, or not. Apodous larval types include curculionoid, muscoid, and apoid.

Apoidae A superfamily in the order Hymenoptera known as bees. It consists of several families.  Bees  Wasps, Ants, Bees and Sawflies

Apoid Larva A larval body form that is robust, with a welldeveloped head, and cared for by nestmates or

provisioned by the parent. It occurs in ants, bees, and wasps (Hymenoptera).

Apoid Wasps (Hymenoptera: Apoidea: Spheciformes) kevin m. o’neill Montana State University, Bozeman, MT, USA Apoid wasps are a morphologically, behaviorally, and ecologically diverse group of insects that are common in many habitats. Apoid wasps are most closely related to bees, and are placed with them in the superfamily Apoidea, one of three superfamilies of the so-called “stinging Hymenoptera” or Aculeata; the other two subfamilies are Chrysidoidea and Vespoidea (Table 7). The subfamily Apoidea is subdivided into the series Apiformes and Spheciformes, the latter of which are the apoid wasps. Thus, the term “apoid wasps” refers to all members of the superfamily Apoidea that are not bees. Of the four families making up the Spheciformes (Heterogynaeidae, Ampulicidae, Sphecidae, Crabronidae), all but the Heterogynaeidae were formerly placed in the single family Sphecidae (sensu lato) in the superfamily Sphecoidea. But recent consensus splits the old Sphecidae into the Ampulicidae, Sphecidae (sensu stricto), and Crabronidae. The correspondence in taxonomic names between this recent family-level classification and what we might call the “classical” system represented in Sphecid Wasps of the World by Richard Bohart and Arnold Menke is given in the following table. The reason for the recent taxonomic reworking is sound. The “old” Sphecidae and Sphecoidea were artificial groupings evolutionarily, because the wasps in what we now call the Crabronidae are actually more closely related to bees than they are to the Ampulicidae or the “new” Sphecidae. The Apoidea, as a whole, likely has its origins in the early Cretaceous, and it is the wasps that predate the bees. Species of over two dozen extinct apoid wasp genera, including members of the

Apoid Wasps (Hymenoptera: Apoidea: Spheciformes)

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Apoid Wasps (Hymenoptera: Apoidea: Spheciformes), Table 7 Superfamilies of aculeate wasps (classification of the Apoidea is after The bees of the world by Charles Michener) Superfamily

Series

Families

Included groups

Chrysidoidea

 

multiple families

cuckoo wasps, bethylid wasps, and others

Vespoidea

 

multiple families

ants, social wasps, spider wasps, velvet ants, and others

Apoidea

Apiformes

seven families

bees

 

Spheciformes

Heterogynaeidae

apoid wasps

 

 

Ampulicidae

 

 

 

Sphecidae

 

 

 

Crabronidae

 

Ampulicidae, Sphecidae, Crabronidae, and the extinct family Angarosphecidae, have been found in Cretaceous deposits. Over 9,500 described extant species of apoid wasps are unequally distributed among the four families and over 250 genera. Bees, in contrast, are divided among seven families, 425 genera, over 16,000 described species, and perhaps 30,000 species overall (Table 8). As a group, apoid wasps share a number of traits that unite them with bees in a discrete evolutionary lineage: (i) a gap present between tegula (at the base of the wings) and the apex of the posterior edge of the pronotum; (ii) a broadly U-shaped pronotum when viewed dorsally; and (iii) the “propodeal triangle” on the dorsal posterior of the abdomen. A dozen or so shared traits link bees in a single clade within the Apoidea. For example, bees feed pollen and nectar to their young, and continue to eat both pollen and nectar as adults. In contrast, with perhaps one exception, all apoid wasps either feed their young arthropod prey or are brood parasites in the nests of other carnivorous wasps; the single exception is the genus Krombeinictus (Crabronidae) from India whose females provision with pollen and nectar. Adult wasps feed on nectar, sap, or honeydew, and some consume body fluids of prey. Another marked difference between apoid wasps and many bees is that body hairs are simple in the former, but often branched or even plumose in the latter, where they function to trap and carry pollen

(though this may not have been their original function). As a group, apoid wasps vary widely in habits and body size, form, and color. Most species are sexually dimorphic to a greater or lesser extent, females having almost universally larger body sizes and stouter mandibles. Also, only females have stings. Females of ground-nesting species also commonly bear two features not found in either males or in females of species that nest in other locations. The first feature is conspicuous rows of “rake spines” on their foretibia that aid in digging in soil. The second feature is flattened pygidial plates that aid in tamping soil in place during nest construction. Males of some species exhibit peculiar anatomical structures used in courtship and mate competition. Examples include the clypeal and abdominal hair brushes that male beewolves (Philanthus) use to disseminate sex pheromones, and the expanded translucent foretarsal plates of male Crabro that sport species- specific color patterns and which are apparently placed over female’s eyes during courtship.

Heterogynaeidae While the Heterogynaeidae are clearly apoid wasps, their exact relationship to the other three families is somewhat controversial. Heterogynaeids are small wasps, 1.5–5.0 mm in length, that are restricted in

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Apoid Wasps (Hymenoptera: Apoidea: Spheciformes), Table 8 Correspondence of taxa names under the “classical” (Bohart and Menke 1976) and revised (Pulawski 2007) systems of classification of the apoid wasps. Note a few minor taxa have been left out of the table “Classical” taxonomy

Revised taxonomy

Number of Some important Nest extant gen- genera (number of typeb era/speciesa described speciesa)

Host/prey ordersc

not included

Heterogynaeidae

1/8

Heterogyna (8)

–

Unknown

Sphecidae: Ampulicinae

Ampulicidae

6/198

Ampulex (131)

C

Bla

Dolichurus (48)

C

Bla

Sphecidae: Sphecinae

Sphecidae

Ammophila (201)

S

Lep

Chalybion (45)

C

Ara

Chlorion (20)

S, Pa

Ort

Isodontia (61)

C

Ort

Palmodes (20)

S

Ort

Podalonia (66)

S

Lep

Podium (23)

C

Blat

Prionyx (59)

S

Ort

Sceliphron (35)

M

Ara

Sphex (118)

S

Ort

Arpactophilus (43)

C

Hom

Diodontus (73)

C

Hom

Microstigmus (29)

Ps

Clm, Thy

Mimesa (71)

S

Hom

Passaloecus (35)

C, P

Hom

Pemphredon (43)

C, P

Hom

Pluto (58)

S

Hom

Polemistus (36)

C

Hom

Psen (92)

R

Hom

Psenulus (159)

C

Hom

Spilomena (86)

C, P, R

Hom, Thy

Astata (80)

S

Hem

Diplopectron (20)

S

Hem

Dryudella (52)

S

Hem

1/12

Dinetus (12)

S

Hem

38/2686

Gastrosericeus (61)

S

Ort

Larra (63)

Pa

Ort

Sphecidae: Pemphredoninae

Sphecidae: Astatinae (part)

Sphecidae: Astatinae (part)

Crabronidae: Pemphredoninae

Crabronidae: Astatinae

Crabronidae: Dinetinae

Sphecidae: Larrinae Crabronidae: Larrinae

19/731

37/1021

4/151


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Apoid Wasps (Hymenoptera: Apoidea: Spheciformes), Table 8 Correspondence of taxa names under the “classical” (Bohart and Menke 1976) and revised (Pulawski 2007) systems of classification of the apoid wasps. Note a few minor taxa have been left out of the table (Continued) “Classical” taxonomy

Sphecidae: Crabroninae

Sphecidae: Nyssoninae

Revised taxonomy

Crabronidae: Crabroninae

Crabronidae: Bembicinaeb

Number of Some important Nest extant gen- genera (number of typeb era/speciesa described speciesa)

56/1886

84/1708

Host/prey ordersc

Liris (350)

C, S

Ort

Miscophus (183)

S

Ara

Nitela (60)

C

Pso, Hom

Palarus (34)

S

Hym

Pison (196)

C, M

Ara

Plenoculus (20)

S

Hem, Lep

Sericophorus (69)

S

Dip

Solierella (111)

C

Ort, Pso, Hem

Tachysphex (391)

S

Ort

Tachytes (294)

S

Ort, Lep

Trypoxylon (629)

M

Ara

Belomicrus (109)

S

Hem

Crabro (88)

S

Dip

Crossocerus (236)

C, P, S

Eph, Pso, Hom, Mec, Tri, Lep, Dip

Ectemnius (184)

P, R, S

Dip

Entomognathus (63)

S

Col

Lindenius (60)

S

Dip

Oxybelus (262)

S

Dip

Podagritus (116)

S

Col

Rhopalum (277)

P, S

Hom

Alysson (42)

S

Hom

Argogorytes (31)

S

Hom

Bembecinus (187)

S

Hom

Bembix (346)

S

Odo, Neu, Lep, Dip, Hym

Bicyrtes (27)

S

Hem

Clitemnestra (67)

S

Hom

Gorytes (46)

S

Hom

Harpactus (73)

S

Hom

Hoplisoides (79)

S

Hom

Microbembex (34)

S

Artd

Nysson (102)

Bp

Apoe

Stictia (28)

S

Dip

Stizus (120)

S

Ort, Man

Stizoides (29)

Bp

Apoe

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Apoid Wasps (Hymenoptera: Apoidea: Spheciformes), Table 8 Correspondence of taxa names under the “classical” (Bohart and Menke 1976) and revised (Pulawski 2007) systems of classification of the apoid wasps. Note a few minor taxa have been left out of the table (Continued) “Classical” Revised taxonomy Number of Some important Nest Host/prey taxonomy extant gen- genera (number of typeb ordersc a era/species described speciesa) Sphecidae: Philanthinae

Crabronidae: Philanthinae

8/1141

Aphilanthops (4)

S

Hym

Cerceris (868)

S

Col, Hym

Clypeadon (9)

S

Hym

Eucerceris (41)

S

Col

Philanthus (137)

S

Hym

Trachypus (31)

S

Hym

number described species worldwide (see Pulawski 2007); genera included based on genus size and b iological interest (but certain larger genera for which no biological data are available are left off the list). b Bp = brood parasite in nests of other wasps; C = cavity nests; M = mud nests; P = nest excavated in plant stems; Ps = free-standing nest made of plant material bound with silk; R = nest excavated in rotten wood; S = nest excavated in soil. c Apo = apoid wasps; Art = Arthropoda; Ara = Araneae; Bla = Blattodea; Col = Coleoptera; Clm = Collembola; Dip = Diptera; Eph = Ephemeroptera; Hem = Hemiptera; Hom = Homoptera; Hym = Hymenoptera; Lep = Lepidoptera; Man = Mantodea; Mec = Mecoptera; Neu = Neuroptera; Odo = Odonata; Ort = Orthoptera; Pso = Psocoptera; Thy = Thysanoptera; note that each species may prey upon a narrow range of families within each order. d females are scavengers of dead arthropods. e Nysson and Stizoides are brood parasites whose larvae feed on prey provisioned by other wasp species. a

distribution to the eastern Mediterranean region, southern Africa, and Madagascar. Nothing is known about their biology, but there are hints that it may be unique among apoid wasps: females have such short wings as to make them flightless and they have been observed active at night; based on morphological evidence, it has been inferred that heterogynaeids are parasitoids, though they probably do not dig in soil.

prey. Venoms of certain species are known to have specific pharmacological effects on cockroaches, which are somewhat subdued following stinging, but remain active enough that the female wasp can lead them to the nest cavity, as if walking a tethered cow to pasture. Nests of ampulicids may have multiple cells separated by partitions made of plant debris, but are relatively simple compared to nests constructed by many Sphecidae and Crabronidae.

Ampulicidae

Sphecidae

The Ampulicidae have rather elongate bodies and legs that make them proficient runners; they range up to 3 cm or so in body size, and may be metallic blue or green in color. Though geographically widespread, ampulicids appear to be relatively consistent in their habits. Females of all species prey on cockroaches that are stung into temporary paralysis, placed singly in existing cavities, and quickly covered with debris after a single egg is laid on each

The wasps in what is now called the Sphecidae are sometimes referred to as “thread-wasted wasps” in reference to their narrow cylindrical petioles. Sphecids often have quite striking body colors, including the metallic blue (Chlorion aerarium), black and yellow (Sceliphron caementarium), and black and orange with either silver (some Ammophila) or golden hairs (Sphex ichneumoneus). The family includes some of the largest apoid wasps, including


members of the genera Dynatus, Parasammophila, and Sphex that can reach as long as 4–5 cm; sphecids are rarely less than 1 cm long, though this is the case for some Ammophila and Prionyx. Sphecids are more diverse in their nesting habits than are ampulicids. Some dig nest burrows in soil, others nest in existing cavities in wood or construct mud nests de novo. Certain species of Chlorion, on the other hand, are parasitoids that construct no nests at all, but simply sting their cricket prey and then place it back in its own burrow. Prey of sphecids include three orders of insects, along with spiders; some take prey that are large relative to their own body size. Palmodes laeviventris (which preys upon Mormon crickets, Anabrus simplex), Sphex ichneumoneus (which takes crickets and katydids), and certain Ammophila (that take large caterpillars) may provision with prey that approach or even exceed the adult female in body mass.

Crabronidae The Crabronidae, the largest and most diverse of apoid wasp families, contains 90% of the apoid wasps. Crabronids range in size from 1.5 mm long Spilomena that prey on psyllids and thrips, to 35 mm long Sphecius speciosus that prey on cicadas, and 45 mm long Editha magnifica that take butterflies. Even individual genera can exhibit wide size variation; Philanthus in North America, for example, range from the 5 mm long Philanthus parkeri, predators of tiny andrenid bees, to 25 mm long Philanthus bicinctus, predators of worker bumble bees. As a group, crabronids prey on insects of at least 17 orders, along with spiders. The reproductive biology of the Ampulicidae, Sphecidae, and Crabronidae are covered in more detail below.

Reproductive Biology of Females The reproductive strategies of female apoid wasps fall into three broad categories: parasitoidism, brood parasitism, and nest-provisioning. The nest

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provisioners include solitary, communal, and eusocial species, the latter two of which will be discussed in the following section. Unlike some apoid wasps, no vespid wasps or bees are parasitoids, and only the bees include brood parasites. However, apoid wasps have just barely crossed the threshold into eusociality, whereas bees and vespid wasps contain some of the most highly eusocial Hymenoptera. Among apoid wasps, parasitoids lay their eggs singly on a host insect that has been stung by the adult female wasp; no nest is constructed by the female parasitoid, though she may return the host to its own burrow and cover it with debris. Parasitoids are found in the Ampulicidae, a few genera of Crabronidae (Chlorion, Larra), and perhaps the family Heterogynaeidae, though this has yet to be confirmed. Brood parasitic apoid wasps occur in the crabronid tribe Nyssonini (226 species) and genus Stizoides of the Gorytini (29 species). Brood parasites enter provisioned nest cells of other apoid wasps and deposit their own eggs (one per nest cell); the brood parasite larva then feeds on the host’s stored prey, the host egg having been already killed either by the adult female parasite at the time of oviposition (Stizoides) or the parasite larva itself (Nyssonini). The vast majority of female apoid wasps are solitary nest-provisioners that work without assistance from conspecifics to construct a nest and provision each of its brood cells with one or more paralyzed prey. The prey placed in a cell must provide all of the nourishment required by the maggot-like larva (one per nest cell in almost all species) that remains restricted to its own nest cell throughout development. Apoid wasp nest types can be grouped in five categories: cavity nests; nests excavated in plant material; nests excavated in soil; free-standing mud nests; and free-standing nests made of various materials bound with silk. In some genera, different species may construct nests in different categories. Cavity nests, those built within existing cavities, are often constructed in old beetle tunnels in wood, but have also been found in such locations

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as empty snail shells, old plant galls, pitcher plants, rolled leaves, and gaps between stones or between boards on the siding of houses. Such nests usually contain multiple cells separated by a species-specific choice of materials; for example, Chalybion uses mud; Isodontia, chopped grass fragments and plant fibers; Passaloecus, conifer resins; Nitela, wood chips; and Podium, an eclectic mix of detritus, mud, and resin. Wasps that excavate their own nest tunnels in plant materials may tunnel through the pith of plant stems (e.g., in raspberry or sumac) or rotten wood in logs. Cells may be arranged in a linear sequence, and tunnels in the same nest may diverge into separate branches. Nests excavated in soil are, by far, the most common type of nest among apoid wasps. They may be simple, unbranched shallow tunnels terminating in the single brood cell, as is the case for some or all species of Ammophila, Bembecinus, Bembix, Podalonia, and Prionyx. Other species dig branched nests with side tunnels leading to as many as 1–2 two dozen brood cells provisioned in succession over a period of several weeks. Single and multi-celled nests can be found not only among different species of the same genus, but among different females in one species. Free-standing nests constructed de novo by females may be built of mud sculpted into species-specific shapes, as is the case for species of Pison, Sceliphron, and Trypoxylon. Mud nests may be attached to vines, trees, cliff faces, or nowadays, buildings; they may also have multiple cells. In most cases, each nest cell is completely provisioned and closed off by the adult before the next cell is begun, but there is some variation in the duration and timing of provisioning relative to the developmental schedule of offspring. Most species are mass provisioners that completely provision cells with one or more prey before the egg hatches. More rarely, females are progressive provisioners that continue to bring in prey after the egg hatches, sometimes until the larva is ready, or nearly so, to spin its cocoon. Among solitary apoid wasps, only certain Ammophila provision two cells simultaneously. During provisioning, females of those species that hunt relatively small prey carry the prey

in flight from hunting grounds to the nest. Prey are usually carried in the wasp’s legs, sometimes with the aid of the mandibles, but some Oxybelus tote prey impaled on their stings, whereas Clypeadon females carry their ant prey grasped by the thorax using structures on the terminal abdominal segments aptly referred to as “ant clamps.” When they leave nests to forage, females of nest-provisioning apoid wasps face two problems in particular, other than the obvious need to find, sting, and transport their prey: the necessity to protect the unguarded nest from natural enemies and the need to find their way home again. Before departing to hunt, wasps often plug the entrance temporarily as a means of excluding intruders. And when a nest is completed, the female may construct an even more elaborate closure and take steps to conceal the entrance; in ground nesting species, this involves often elaborate and prolonged leveling of the mound of excavated soil adjacent to the nest entrance. Nevertheless, although these actions are likely successful in many cases, apoid wasp larvae are plagued by a variety of natural enemies that commence their attacks at varying times in the life cycle of the wasp. Brood parasites, which include not only other apoid wasps, but mites, flies (Phoridae, Sarcophagidae), and non-apoid wasps (Chrysididae) that feed on the wasps’ own prey, may kill the wasps’ young either directly or indirectly (through starvation). Parasitoids that feed directly on wasp larvae or pre-pupae include, among other insects, flies (Bombyliidae), beetles (Rhipiphoridae), and other aculeate wasps (Chrysididae and Mutillidae). Several detailed studies attest to the fact that female wasps often have excellent homing abilities that lead them back to their nest, even when that nest is one of many hundreds or thousands densely packed into the apparently featureless soil surface of a nesting area. As far back as 1930, Niko Tinbergen’s research showed that a Philanthus triangulum female can relocate her nest by learning the image of the landscape surrounding the nest and matching the memorized image to the configuration of local landmarks when she later returns


with prey. The initial task of learning the image is apparently accomplished during an orientation flight, which in the case of P. triangulum, begins when the female circles the nest in flight, then gradually expands the diameter and height of her loops before departing for her hunting grounds. The form of the orientation flights varies among species, but females of all species share an uncanny ability to find their way home, even after being transported several hundred meters away by researchers. When we examine the ovaries of female apoid wasps, we find several features that vary among species and correlate with overall reproductive strategies. First, although the paired ovaries of nest provisioning species each have three ovarioles (except for Oxybelus which have two), each ovary of brood parasitic species is comprised of four ovarioles (and sometimes five in Stizoides renicinctus). Second, although it is common for females of nest provisioners (especially progressive provisioners) to carry a maximum just one or two mature oocytes in their ovaries at a any time, brood parasites commonly carry 4–6 mature oocytes; and the parasitoid species Larra amplipennis can carry as many as 21. Third, the eggs produced by nest provisioners tend to be larger (relative to overall body size) than those of brood parasites or of Larra. All in all, this meshes with the fact that nest provisioning apoid wasps, because they invest so highly in individual offspring, have relatively low lifetime fecundities compared to parasitoids and brood parasites in their same families. Thus, it is likely common that even the most successful females of some nest provisioners can expect to have fewer than ten offspring during their lives. This contrasts markedly with the high potential fecundities of nonaculeate parasitoid Hymenoptera (e.g., Braconidae, Ichneumonidae).

Communal and Social Species The vast majority of apoid wasps are solitary species, each of whose females occupies a nest alone

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and provisions it without assistance from conspecifics. Nests of both ground- and mud-nesters do sometimes occur in dense aggregations, but true communal and eusocial behavior is relatively rare among apoid wasps. Communal nests, in which small groups of females share a main nest burrow, but in which each provisions her own brood cells, have been reported in several genera (e.g., Cerceris, Moniaecera, Spilomena). In the Neotropics, Microstigmus comes is eusocial, inhabiting nests in which (i) two generations of adult females are present (likely a mother and her daughters), (ii) each nest cell is provisioned cooperatively, and (iii) one female is the primary egg layer. The nests, which are founded by one or more females, have as many as 18 brood cells and 10 adult females (as well as a smaller number of adult males). The nests of Microstigmus are unique among apoid wasps, that of M. comes consisting of a 1–3 cm deep bag of plant fibers embedded in a matrix of silk and suspended from the underside of a leaf by a short, coiled petiole. Other Microstigmus create similar nests, but embedding small pieces of bark, wood, leaf hairs, lichens, sand, or stone in the silk mesh. The use of silk produced by adults in nest construction is limited among apoid wasps to Microstigmus and other Pemphredoninae (e.g., Arpactophilus, Psenulus); however, larval apoid wasps commonly incorporate silk into their cocoons. Finally, whereas other social insects build nests gradually, expanding their size over time, Microstigmus construct their silken abodes all at once and so are limited to their confines until all cells in the nest are completed.

Mating Strategies In 1960, a comprehensive review of the diversity of male apoid wasp behavior would have occupied a brief paragraph, but we now have a much better understanding of male behavior. Perhaps the bestknown male behaviors are the so-called “sun dances” of sand wasps (Bembicinae) in which hundreds or thousands of males swarm over the

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surface of nesting areas seeking newly emerged virgin females (as in many species of Bembix). A variation on this theme sees males attempting to rendezvous with females at the point at which they emerge from the ground when they leave their natal nests (e.g., Bembecinus quinquespinosus, Bembix rostrata, and Glenostictia satan). In other species, males defend discrete territories that are often plots of ground in emergence or nesting areas, as is the case for Sphecius (cicada-killers) and many Philanthus (beewolves). Or males may defend individual nests that are in the process of being provisioned by females (as in some Trypoxylon and Oxybelus, for example). Less commonly, males establish territories at hunting sites frequented by females (e.g., Aphilanthops subfrigidus which defend territories in mating swarms of prey, and Mellinus rufinodus which defend feces that attract flies hunted by females). In yet other species, territories are situated in locations that have no other apparent attractiveness to females other than the presence of the males themselves (e.g., Eucerceris flavocincta, Philanthus basilaris). While defending their territories, male wasps may engage in rowdy battles that involve, depending on the species, wrestling, biting, head butting, abdomen slapping, or mutual flights in which the contestants swirl about one another at dizzying speeds. One should not be left with the impression, however, that males of any given species have just one way to find a mate, as alternative mating tactics are common. Male Stictia heros, for example, may patrol the nesting area in the morning, but shift to defending territories later in the day. And some males of Philanthus zebratus patrol the air space above the nesting area, while others simultaneously defend scent-marked territories nearby. Ultimately, it appears that in most cases it is the females that control which males are successful. Females, after all, are usually the larger sex, so are physically dominant to males (and in the case of Philanthus basilaris, may even prey upon them). So mating is sometimes, though not always, preceded by obvious courtship activities during

which the male induces the female to copulate. This, however, is one of the least-studied aspects of apoid wasp reproductive biology.

Economic Significance of Apoid Wasps A least one genus of apoid wasps, Larra, whose females prey on mole crickets, includes species that have found some success as biological control agents. Other genera contain species that may provide some natural control of pests such as aphids (Passaloecus), biting flies (Bembix, Stictia), cutworms (Podalonia), grasshoppers (Prionyx, Tachysphex), Mormon crickets (Palmodes), and leafhoppers (many genera). On the negative side of the ledger, apoid wasps can be a nuisance to those people that cannot abide the presence of a wasp, no matter what its activities. In North America, large territorial males of the cicadakiller wasp, Sphecius speciosus, sometimes bother homeowners and park visitors who mistake male investigatory flights for something more hostile. The large nest mounds of female cicada-killers that appear in otherwise immaculate lawns are considered unsightly by some. In Africa, Palarus latifrons and Philanthus triangulum can be outright pests when large numbers of females invade apiaries and decimate worker honey bee populations. And we know very little about the potential effect of apoid wasp predators on the biology of other beneficial insects such as native pollinators and biological control agents.  Wasps, Ants, Bees and Sawflies  Bees

References Bohart RM, Menke AS (1976) Sphecid wasps of the world: a generic revision. University of California Press, Berkeley, CA, pp 695 Evans HE (1966) The comparative ethology and evolution of the sand wasps. Harvard University Press, Cambridge, MA, pp 526

Aposematism

Evans HE, O’Neill KM (1988) The natural history and behavior of North American beewolves. Cornell University Press, Ithaca, NY, pp 278 Evans HE, O’Neill KM (2007) The sand wasps: behavior and natural history. Harvard University Press, Cambridge, MA, pp 340 Goulet H, Huber JT (1993) Hymenoptera of the world: an identification guide to families. Research Branch, Agriculture Canada, Publication 1894/E. Centre for Land and Biological Resources Research, Ottawa, Canada, pp 668 Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, New York, NY, pp 772 Krombein KV (1967) Trap-nesting wasps and bees: life histories, nests, and associates. Smithsonian Press, Washington, DC, pp 570. Matthews RW (1991) Evolution of social behavior in the sphecid wasp. In Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, NY, pp 570–602 Michener CD (2000) The bees of the world. The Johns Hopkins University Press, Baltimore, MD, 913 pp Melo GAR (1999) Phylogenetic relationships and classification of the major lineages of Apoidea (Hymenoptera), with emphasis on the crabronid wasps. Natural History Museum, University of Kansas, Scientific Papers 12:1–55 Melo GAR, Gonçalves RB (2005) Higher-level bee classifications (Hymenoptera, Apoidea, Apidae sensu lato). Revista Brasileira de Zoologia 22:153–159 Ohl M, Bleidorn C (2006) The phylogenetic position of the enigmatic family Heterogynaidae based on molecular data, with description of a new, nocturnal species (Hymenoptera: Apoidea). Syst Entomol 31:321–337. O’Neill KM (2001) Solitary wasps: natural history and behavior. Cornell University Press, Ithaca, NY, pp 406 Pulawski WJ (2007) Catalog of the Sphecidae sensu lato (=Apoidea excluding Apidae). California Academy of Sciences. Available at http://www.calacademy.org/ research/entomolog y/Entomolog y_Resources/ Hymenoptera/sphecidae/Genera_and_species_PDF/ introduction.htm Tree of Life Web Project (1995) Apoidea. Bees, digger wasps. Version 01 January 1995 (temporary). http:// tolweb.org/Apoidea/11190/1995.01.01 in The Tree of Life Web Project. Available at http://tolweb.org/

Apolysal Space During molting, a very small space is created by the separation of the epidermis from the old cuticle. This space, called the apolysal space, contains molting fluid during the process of cuticle digestion.

A

Apolysis Separation of the epidermal cells from the inner surface of the endocuticle. This is the first step in the process of molting.

Apomorphic A character that is derived and not ancestral.

Apomorphy When considering classification and phylogeny, a derived character state.

Apophysis An internal or external elongate projection of the body wall.

Apoprogonidae A family of moths (order Lepidoptera). They also are known as African skipper moths.  African Skipper Moths  Butterflies and Moths

Aposematism heather j. mcauslane University of Florida, Gainesville, FL, USA Aposematism is a strategy used by many organisms that increases their conspicuousness, and alerts or warns potential predators of their toxicity, their ability to inflict pain or, more simply, their unpredictibility. Insects have evolved this strategy to a high degree, although it is found occasionally in other terrestrial

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organisms such as snakes, lizards, and frogs, and in aquatic organisms such as nudibranches. Aposematic signals usually are visual in nature and involve bright and contrasting coloration, usually black and red, yellow or orange or black and white. Visual signals may be enhanced by certain odors, sounds or behaviors, presenting a multimodal signal that predators may recognize and learn more easily. Visual aposematism as an antipredator strategy only works well against predators with color vision and good learning ability. Birds, and to a lesser extent lizards and amphibians, are the most common predators for which aposematic coloration (Figs. 66 and 67) is an effective deterrent. The naïve predator associates the particular color pattern of an aposematic organism with the unpleasant after effects of eating or attempting to eat it. Aposematic insects usually back up their warning signal with chemical defenses (unless they are harmless mimics of another toxic organism). These chemical defenses may be toxins that are stored inside the insect’s body that could cause death if ingested and absorbed by the predator. H owever,

the toxins themselves often are emetic (for example, cardiac glycosides in the Monarch butterfly, Danaus plexippus, and lucibufagins in Photinus fireflies), meaning that they cause the predator to regurgitate the prey item before a lethal dose of the toxin has been absorbed. The toxins also are often bitter so that the predator is less likely to pursue the attack once the bitter compounds have been contacted. In other insects, toxins are not stored within the body but are injected into predators through sharp urticating hairs or spines (for example, larvae of the saddleback moth, (Fig. 68) Sibine stimulea). In these insects, the predator is warned of the prey item’s distastefulness without having to breach the cuticle of the aposematic organism. The naïve predator may need only one trial to associate the color pattern of the aposematic insect with emesis or a bitter taste but more often, learning takes several trials. The speed of learning can be enhanced in several ways. If the predator encounters several toxic insects with the same aposematic pattern within a short period of time, it appears to learn the warning

Aposematism, Figure 66 Aposematic insects are often aggregated, perhaps increasing the rate at which predators associate aposematic coloration with toxicity. The orange and black larvae of the o leander caterpillar, Syntomeida epilais (Ctenuchidae), aggregate in the early instars on oleander, Nerium o leander, a plant containing heart poisons (cardiac glycosides) (photo by James Castner).

Aposematism

A

Aposematism, Figure 67 The black and white larvae of the Giant African Skipper (Hesperiidae) also aggregate on their host plant (photo by Andrei Sourakov).

coloration faster. This may explain why aposematic insects are often gregarious, living in small, usually related, groups. For example, oleander caterpillars, Syntomeida epilais and oleander aphids, Aphis nerii live gregariously on oleander which contains heart poisons. Other factors that can increase the rate of learning are the pairing of

the visual pattern with acoustic signals or olfactory signals. Many aposematic insects hiss, stridulate or make some other noise when predators attack them. Arctiic moths and lubber grasshoppers, Romalea guttata, commonly do this. The association of sound with the color pattern and bitter chemical toxins in the aposematic

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Aposematism, Figure 68 Larvae of the saddleback moth, Sibine stimulea (Limacodidae), advertise their urticating hairs with a pronounced brown and white “saddle” on the lime-green bodies (photo by James Castner).

insects help the predator better remember the color pattern. We are becoming increasingly aware that many insects release volatile pyrazine compounds when under attack. These nitrogen-containing compounds are extremely odorous at low c oncentrations and are thought to produce a universal warning odor in plants and animals. Insects that are aposematic often exhibit what we might call bold behavior, at least for an insect. They are usually active during the day and are not cryptic, rather feeding in an exposed position. Aposematic adults may have an exaggerated slow flight, as do Heliconius butterflies and many arctiid moths. Larvae may wave tentacles and other long protuberances from their body to warn predators. Larvae of the Monarch butterfly (Fig. 69) integrate aposematic behaviors into their multimodal signal to warn of their toxicity. In addition to being conspicuously striped white, yellow and black, they release pyrazine from the head collar region when roughly handled and nod their heads up and down every 2 s while simultaneously twitching their anterior filiform tentacles.

 Allelochemicals  Mimicry  Chemical Ecology

References Guilford T, Nicol C, Rothschild M, Moore BP (1987) The biological roles of pyrazines: evidence for a warning odour function. Biol J Linn Soc 31:113–128 Guildford T (1990) The evolution of aposematism. In: Evans DL, Schmidt JO (eds) Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New York Press, New York, NY, pp 23–61 Huheey JE Bell WJ, Cardé RT (eds) (1984) Chemical ecology of insects. Sinauer Associates, Inc., Sunderland, MA, pp 257–297 Rothschild M, Bergström G (1997) The monarch butterfly caterpillar (Danaus plexippus) waves at passing Hymenoptera and jet aircraft-are repellent volatiles released simultaneously? Phytochemistry 45:1139–1144 Rowe C (2002) Sound improves visual discrimination learning in avian predators. Proc R Soc Biol Sci B 269:1353–1357

Aposymbiotic Separated from its symbiotes, or symbiote-free; this usually refers to mutualistic symbiotes.

Apparent Resources

A

Aposematism, Figure 69 Larvae of the Monarch butterfly, Danaus plexippus (Danaidae), use a multimodal signal to warn potential predators. Their aposematic coloration of black, white, and yellow stripes is enhanced with the release of pungent pyrazine and the behavioral display involving rhythmic nodding of the head and twitching of the filiform tentacles (photo by Lyle Buss).

Apotome A narrow anterior portion of each abdominal sternum, separated by a fold from the rest of the plate. They are present in Apterygota, but indistinct in Pterygota.  Abdomen of Hexapods

Apparent Resources Food resources (either insect or plant) that are “easy to locate” or apparent to potential predators or herbivores. Apparent resources often are protected against consumption by generalist and specialist predators, and generalist or specialist herbivores, by

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Appeasement Substance

possessing broadly effective (though metabolically expensive) chemical defenses such as digestibility reducing substance (contrast with unapparent resources).

Appeasement Substance A secretion presented by a social parasite that reduces aggression by the host insects, and aids parasites in being accepted as members of the colony.

Apple Maggot  Apple Pests and their Management

Apple Pests and their Management arthur m. agnello New York State Agricultural Experiment Station, Geneva, NY, USA Insects with chewing mouthparts inflict great damage on foliage, causing leaves to be skeletonized, riddled with holes, eaten around the edges, or entirely consumed (e.g., larvae of moths, sawflies, and beetles). Other insects suck sap from leaves, stems, or other plant parts, producing a characteristic spotting or browning, curling, or wilting. Feeding on stems or twigs results in dwarfing or wilting. Damage is caused both by removal of the sap and by injury to the plant tissue (e.g., scale insects, aphids, and true bugs). Also included in this category (Fig. 70) are mites, such as the European red mite and the two-spotted spider mite, which damage the leaves by piercing the cell walls with bristle-like mouthparts and ingesting their contents, including the chlorophyll. The injury results in off-color foliage that, in severe cases, becomes bronzed. Scale insects are usually minute, but if they are abundant enough to encrust bark, twigs, or stems they can kill orchard and shade trees. Aphids

produce a curling of the leaves and, when feeding on fruit, may cause it to be stunted or misshapen and may change the sugar content, greatly impairing the flavor. Many insects feed as miners in leaves or as borers in stems, roots, or fruits. Feeding between the upper and lower surfaces of the leaf may cause as much defoliation as external feeding. There are about 500 leafmining species in the United States (e.g., spotted tentiform and apple blotch leafminers). Tunneling causes serious damage. Insects that tunnel into fruit include codling moth, oriental fruit moth, apple maggot, and plum curculio. Damage with more serious consequences can be done by insects that tunnel into the tree trunk, bark, or foliar shoots, such as apple-boring beetles (roundheaded, flatheaded), dogwood borer, American plum borer, European corn borer, and oriental fruit moth. Injection of a chemical into plant tissues while the insect feeds causes abnormal growth (e.g., rosy apple aphid) or produces a gall (woolly apple aphid). Each species of gall insect produces a characteristic gall on a certain part of a particular plant. Insects at the larval and nymphal stages (e.g., woolly apple aphid) that live in the soil and attack the underground plant parts cause extensive damage. Shelters in plants are built by leafrollers and leaf folders, which roll or fold the leaves and tie them with silk, feeding in the shelter so formed. Leaf tiers and webworms tie several leaves or even entire branches together, producing large silken webs or tents. A few insects injure plants when they lay their eggs, particularly in stems or fruits (e.g., plum curculio, apple maggot, periodical cicadas, tree crickets, leafhoppers).

Major Economic Pests Early researchers in New York estimated nearly 500 species of insects known to feed on apple. Fortunately, only a relatively small number of these ever reach economic pest status. A survey conducted in the northeastern U.S. identified a

Apple Pests and their Management

Apple Pests and their Management, Figure 70 Some North American apple pests: (a) codling moth; (b) obliquebanded leafroller; (c) rosy apple aphid; (d) plum curculio; (e) spotted tentiform leafminer; (f) European red mite attacked by predatory mite; within circle, apple maggot adult, larva and pupa.

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total of 191 phytophagous (plant-feeding) insect species in managed and abandoned apple orchards. Most numerous were species of Lepidoptera (mostly moths and their caterpillars, 43%) and Hemiptera (leafhoppers, plant bugs, aphids and scale insects, 32%). Current tabulations of actual economic pests list just over 60 species in New York, approximately half of which are considered important enough to warrant specific control recommendations. This compares with 17 pest species for pear, 12 for peach, and seven for tart cherry and plum. A similar accounting in other production regions reveals certain species with a worldwide distribution, and others, largely representing the above major orders, that are prevalent only in specific areas (Table 9). The following are some of the key pests in the northeastern U.S. growing regions.

Rosy Apple Aphid, Dysaphis plantaginea (Passerini) Biology and Impact The rosy apple aphid is the most damaging of the aphids that attack apple. Its saliva, injected while feeding, is translocated to nearby fruit, causing leaf curling and small, deformed apples. The rosy apple aphid can be distinguished from other aphids by its long cornicles and purple-rose color. It overwinters as an egg on twigs, in bud axils, and in bark crevices. The overwintering eggs of the rosy apple aphid are oblong and pale green at first, then turn shiny black. Rosy apple aphid nymphs are visible beginning around the tight cluster bud stage but are most easily observed at the pink bud stage. The first adults appear around bloom. Second-generation adults appear two to three weeks after petal fall. Some of these move to alternate hosts (such as narrowleaf plantain) and the rest remain in the orchard. The third generation develops by mid-July and moves to alternate hosts. In later summer, adult rosy apple aphids return to the trees to lay eggs.

Decision Making Because rosy apple aphid populations are highly variable, it is important to assess their densities before making a treatment. Sampling can begin at the tight cluster bud stage but is better done at the pink stage when rosy apple aphid nymphs are more easily seen. Rosy apple aphid densities are estimated by sampling 10 fruit clusters from the interior canopy area of 10 trees. Treatment is generally recommended if one infested cluster is found, but for experienced samplers of rosy apple aphids, this is probably too conservative and a threshold of three to five infested clusters would be more appropriate.

Control It is not known how important natural enemies (such as larvae of the fungus gnats, Cecidomyiidae) are in regulating rosy apple aphid populations. Several pesticides can effectively control this pest when applied at the pink bud stage. A material should be used that will conserve natural enemy populations, such as Typhlodromus pyri, an important mite predator.

Spotted Tentiform Leafminer, Phyllonorycter blancardella (Fabricius) Biology and Impact The spotted tentiform leafminer was introduced from Europe in the 1880s. Its host plants include apple, wild cherry, hawthorn, quince, plum, and crabapple. Spotted tentiform leafminer overwinters as a pupa in leaf litter on the ground. Adults emerge at the green tip apple bud stage and lay small, flattened eggs that are deposited singly on leaf undersides. Egg laying begins when leaves unfold after the half-inch green bud stage, and deposition is nearly complete by the end of the pink bud stage. Its f ive larval stages are divided


Apple Pests and their Management, Table 9 Major insect and mite pests of apple Taxon scientific and common name

Geographical distribution

Plant parts affected

Acari: Eriophyidae

 

 

Aculus schlechtendali (Nalepa), apple rust mite

North America, South America, Europe, Australia/New Zealand

Foliage

Eriophyes pyri (Pagenstecher), pearleaf blister mite

North America, South Africa

Foliage

Acari: Tetranychidae

 

 

Bryobia praetiosa Koch, clover mite

North America

Foliage

Bryobia rubrioculus (Scheuten), brown mite

Worldwide

Foliage

Panonychus ulmi (Koch), European red mite

Worldwide

Foliage

Tetranychus canadensis (McGregor), fourspotted spider mite

North America

Foliage

Tetranychus kanzawai Kishida, kanzawa mite

Asia

Foliage

Tetranychus mcdanieli McGregor, McDaniel spider mite

North America

Foliage

Tetranychus urticae Koch, two spotted spider mite

Worldwide

Foliage

Tetranychus viennensis Zacher, hawthorn spider mite

Asia

Foliage

Coleoptera: Bostrichidae

 

 

Amphicerus bicaudatus (Say), apple twig borer

North America

Twigs, Wood

Coleoptera: Buprestidae

 

 

Chrysobothris femorata (Olivier), flatheaded appletree borer

North America

Cambium, Wood

Coleoptera: Cerambycidae

 

 

Prionus imbricornis (Linnaeus), tilehorned prionus

North America

Cambium, Roots

Prionus laticollis (Drury), broad necked root borer

North America

Cambium, Roots

Saperda candida Fabricius, roundheaded appletree borer

North America

Cambium, Wood

Coleoptera: Chrysomelidae

 

 

Nodonota puncticollis (Say), rose leaf beetle

North America

Fruit

Coleoptera: Curculionidae

 

 

Anthonomus pomorum (Linnaeus), apple blossom weevil

Europe, Asia

Buds

Anthonomus quadrigibbus Say, apple curculio

North America

Foliage, Fruit

Conotrachelus nenuphar (Herbst), plum curculio

North America

Fruit

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Apple Pests and their Management, Table 9 Major insect and mite pests of apple (Continued) Taxon scientific and common name



Naupactus xanthographus (Germar), grape snout beetle

South America

Buds, Foliage

Phlyctinus callosus Boheman, banded fruit weevil

South Africa

Fruit

Scolytus rugulosus (Müller), shothole borer

North America

Cambium, Wood

Coleoptera: Scarabaeidae

 

 

Macrodactylus subspinosus (Fabricius), rose chafer

North America

Foliage, Fruit

Popillia japonica Newman, Japanese beetle

North America

Foliage, Fruit

Dermaptera: Forficulidae

 

 

Forficula auricularia Linnaeus, European earwig

Europe

Fruit

Diptera: Agromyzida

 

 

Liriomyza brassicae (Riley), serpentine leafminer

North America

Foliage

Diptera: Cecidomyiidae

 

 

Dasineura mali (Kieffer), apple leafcurling midge

North America, Europe, Australia/New Zealand

Foliage

Diptera: Tephritidae

 

 

Anastrepha fraterculus (Weidemann), S. American fruit fly

South America

Fruit

Bactrocera tryoni (Froggatt), Queensland fruit fly

South America, Australia/ New Zealand

Fruit

Ceratitis capitata (Wiedemann), Mediterranean fruit fly

South Africa

Fruit

Ceratitis rosa Karsch

South Africa

Fruit

Rhagoletis pomonella (Walsh), apple maggot

North America

Fruit

Hemiptera: Miridae

 

 

Atractotomus mali (Meyer), apple brown bug

North America

Fruit

Campylomma liebknechti (Girault), apple dimpling bug

Australia/New Zealand

Fruit

Campylomma verbasci (Meyer), mullein plant bug

North America, Europe

Fruit

Lygidea mendax Reuter, apple red bug

North America

Foliage, Fruit

Lygocoris pabulinus (Linnaeus)

Europe

Fruit

Lygus lineolaris Palisot de Beauvois, tarnished plant bug

North America

Fruit

Plesiocoris rugicollis Fallén

Europe

Fruit

Hemiptera: Pentatomidae

 

 





Antestiopsis orbitalis Ghesquierei Car., antestia bug

South Africa

Fruit

Heteroptera: Tingidae

 

 

Stephanitis pyri Fabricius

Europe

Foliage

Hemiptera: Aphididae

 

 

Aphis pomi DeGeer, apple aphid

North America, South America, Europe

Foliage, Fruit

Aphis spiraecola Patch, spirea aphid

North America, South America, South Africa, Asia

Foliage

Dysaphis plantaginea (Passerini), rosy apple aphid


Foliage, Fruit

Eriosoma lanigerum (Hausmann), woolly apple aphid

Worldwide

Roots, Twigs

Myzus malisuctus Matsumura, apple leafcurling aphid

Asia

Foliage

Rhopalosiphum fitchii (Sanderson), apple grain aphid

North America, South America

Buds, Foliage

Schizaphis piricola Matsumura

Asia

Foliage

Hemiptera: Cicadellidae

 

 

Edwardsiana crataegi (Dg.), apple leafhopper

South America

Foliage

Edwardsiana frogatti Baker

Europe

Foliage

Edwardsiana rosae (Linnaeus), rose leafhopper

North America

Foliage

Empoasca fabae (Harris), potato leafhopper

North America

Foliage

Empoasca maligna (Walsh), apple leafhopper

North America

Foliage

Typhlocyba pomaria McAtee, white apple leafhopper

North America

Foliage, Fruit

Hemiptera: Cicadidae

 

 

Magicicada septendecim (Linnaeus), periodical cicada

North America

Twigs, Wood

Hemiptera: Coccidae

 

 

Parthenolecanium corni (Bouché), European fruit lecanium

North America

Wood, Fruit

Hemiptera: Diaspididae

 

 

Aonidiella aurantii (Maskell), California red scale

North America, South Africa

Twigs, Wood

Chionaspis furfura (Fitch), scurfy scale

North America

Cambium, Fruit

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Epidiaspis leperii (Signoret), Italian pear scale

South America, Europe

Cambium

Hemiberlesia lataniae (Signoret), latania scale

South America

Cambium

Lepidosaphes ulmi (Linnaeus), oystershell scale


Cambium

Quadraspidiotus forbesi (Johnson), Forbes scale

North America

Cambium

Quadraspidiotus perniciosus (Comstock), San Worldwide Jose scale

Cambium, Fruit

Hemiptera: Flatidae

 

 

Metcalfa pruinosa (Say)

Europe

Fruit

Hemiptera: Margarodidae

 

 

Icerya purchasi Maskell, cottony cushion scale

South Africa

Wood, Twigs, Fruit

Hemiptera: Membracidae

 

 

Stictocephala bisonia Kopp & Yonke, b uffalo treehopper


Twigs, Wood

Hemiptera: Pseudococcidae

 

 

Pseudococcus calceolariae (Maskell), citrophilus mealybug

Europe, Australia/New Zealand, South Africa

Fruit

Pseudococcus comstocki (Kuwana), Comstock mealybug

North America

Foliage, Fruit

Hemiptera: Psyllidae

 

 

Cacopsylla mali (Schmidberger), apple sucker


Foliage

Hymenoptera: Tenthredinidae

 

 

Hoplocampa testudinea (Klug), European apple sawfly


Fruit

Lepidoptera: Arctiidae

 

 

Hyphantria cunea (Drury), fall webworm

North America, Europe, Asia

Foliage

Lophocampa caryae Harris, hickory tussock moth

North America

Foliage

Lepidoptera: Carposinidae

 

 

Carposina niponensis Walshingham, peach fruit moth

Asia

Fruit

Carposina sasakii Matsumura, peach fruit moth

Asia

Fruit

Lepidoptera: Choreutidae

 

 

Choreutis pariana (Clerck), apple-and-thorn skeletonizer


Foliage





Lepidoptera: Coleophoridae

 

 

Coleophora multipulvella (Chambers), pistol casebearer

North America, Asia

Foliage, Fruit

Coleophora serratella (Linnaeus), cigar/birch casebearer


Foliage

Lepidoptera: Cossidae

 

 

Cossus cossus Linnaeus, European goat moth


Cambium, Wood

Zeuzera pyrina Linnaeus, leopard moth


Wood, Twigs

Lepidoptera: Geometridae

 

 

Alsophila pometaria (Harris), fall cankerworm

North America

Foliage

Operophtera brumata Linnaeus, winter moth North America, Europe, Asia

Buds, Foliage, Fruit

Paleacrita vernata (Peck), spring cankerworm

North America

Foliage

Lepidoptera: Gracillariidae

 

 

Marmara elotella (Busck), apple barkminer

North America

Cambium

Marmara pomonella Busck, apple fruitminer

North America

Fruit

Phyllonorycter blancardella (Fabricius), spotted tentiform leafminer


Foliage

Phyllonorycter crataegella (Clemens), apple blotch leafminer

North America

Foliage

Phyllonorycter elmaella Doganlar & Mutuura, North America western tentiform leafminer

Foliage

Phyllonorycter ringoniella (Matsumura), apple leafminer

Asia

Foliage

Lepidoptera: Lasiocampidae

 

 

Malacosoma americanum (Fabricius), eastern tent caterpillar

North America

Foliage

Lepidoptera: Lymantriidae

 

 

Euproctis chrysorrhoea (Linnaeus), b rowntail moth


Foliage

Lymantria dispar (Linnaeus), gypsy moth


Foliage

Orgyia antiqua (Linnaeus), rusty tussock moth

North America, South America, Europe, Asia

Buds, Foliage

Orgyia leucostigma (J.E. Smith), whitemarked tussock moth

North America

Foliage, Fruit

Lepidoptera: Lyonetiidae

 

 

Bucculatrix pomifoliella (Clemens), apple bucculatrix

North America

Foliage

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Leucoptera malifoliella (Costa), pearleaf blister moth

Europe, Asia

Foliage

Lyonetia prunifoliella (Hübner), apple lyonetid


Foliage

Lyonetia speculella Clemens, apple leafminer

North America

Foliage

Lepidoptera: Noctuidae

 

 

Amphipyra pyramidoides Guenée, humped green fruitworm

North America

Foliage, Fruit

Helicoverpa armigera (Hübner), cotton bollworm

Europe, Asia, South Africa

Fruit

Lacanobia subjuncta (Grote & Robinson), Lacanobia fruitworm

North America

Foliage, Fruit

Lithophane antennata (Walker), green fruitworm

North America

Fruit

Orthosia hibisci (Guenée), speckled green fruitworm

North America

Foliage, Fruit

Xestia c-nigrum (Linnaeus), spotted cutworm


Foliage

Lepidoptera: Notodontidae

 

 

Datana ministra (Drury), yellownecked caterpillar

North America

Foliage

Schizura concinna (J. E. Smith), redhumped caterpillar

North America

Foliage

Lepidoptera: Pyralidae

 

 

Conogethes punctiferalis (Guenée), yellow peach moth

Asia, Australia/New Zealand

Fruit

Euzophera semifuneralis (Walker), American plum borer

North America

Cambium, Wood

Ostrinia nubilalis (Hübner), European corn borer

North America, South America, Europe, Asia

Foliage, Fruit

Lepidoptera: Sesiidae

 

 

Podosesia syringae (Harris), lilac/ash borer

North America

Cambium, Wood

Synanthedon myopaeformis Borkhausen, apple clearwing moth

Europe, Asia

Cambium, Wood

Synanthedon pyri (Harris), apple bark borer

North America

Cambium, Wood

Synanthedon scitula (Harris), dogwood borer

North America

Cambium, Wood

Lepidoptera: Tisheriidae

 

 

Tischeria malifoliella Clemens, apple trumpet leafminer

North America

Foliage

Lepidoptera: Tortricidae

 

 





Adoxophyes orana Fischer Von R öslerstamm, South America, Europe, Asia summer fruit tortrix

Fruit

Archips argyrospila (Walker), fruittree leafroller

North America

Foliage, Fruit

Archips podana Scopoli, fruittree tortrix


Foliage, Fruit

Archips rosana (Linnaeus), rose tortrix


Fruit

Argyrotaenia citrana (Fernald), orange tortrix

North America

Fruit

Argyrotaenia pulchellana Haworth

Europe

Foliage, Fruit

Argyrotaenia velutinana (Walker), redbanded leafroller

North America

Foliage, Fruit

Choristoneura rosaceana (Harris), obliquebanded leafroller

North America, South America

Foliage, Fruit

Cydia lobarzewskii Nowicki

Europe

Fruit

Cydia pomonella (Linnaeus), codling moth

Worldwide

Fruit

Epiphyas postvittana (Walker), light brown apple moth

Europe, Australia/New Zealand

Foliage, Fruit

Grapholita molesta (Busck), oriental fruit moth

Worldwide

Fruit, Foliage, Twigs

Grapholita prunivora (Walsh), lesser appleworm

North America

Fruit

Hedya dimidioalba (Retzius), marbled orchard tortrix


Buds, Foliage

Pandemis heparana Denis & Schiffermüller, fruittree tortrix


Foliage, Fruit

Pandemis limitata (Robinson), threelined leafroller

North America

Foliage, Fruit

Platynota flavedana Clemens, variegated leafroller

North America

Foliage, Fruit

Platynota idaeusalis (Walker), tufted apple budmoth

North America

Foliage, Fruit

Proeulia auraria (Clarke), fruit leaf folder

South America

Foliage, Fruit

Pseudexentera mali Freeman, pale apple leafroller

North America

Foliage, Fruit

Sparganothis sulfureana Clemens, Sparganothis fruitworm

North America

Foliage, Fruit

Spilonota ocellana (Denis & Schiffermüller), eyespotted bud moth


Foliage, Fruit

Tortrix capensana (Walker)

South Africa

Foliage, Fruit

Orthoptera: Gryllidae

 

 

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Oecanthus fultoni Walker, snowy tree cricket

North America

Cambium, Wood, Twigs

Thysanoptera: Thripidae

 

 

Frankliniella occidentalis (Pergande), western flower thrips


Foliage, Fruit

Taeniothrips inconsequens (Uzel), pear thrips


Buds

into sap-feeders (instars 1–3) and tissue-feeders (instars 4–5). The second-generation adults begin emerging in early June in the northeastern states (average date is June 13 ± 8 days), and larvae are usually present in early July. Third-generation l arvae are usually present in late August. The spotted tentiform leafminer damages only foliage, which the larvae eat and mine. This causes reduced photosynthesis and possibly sequestered nutrients. Foliar damage can cause smaller fruit size, premature drop, and poor color. Damage caused by the second generation is usually of the greatest concern. Third-generation leafminers usually are not a problem if the second generation was controlled properly.

Decision Making A sequential sampling plan can be used to classify spotted tentiform leafminer egg density at the pink stage or the density of sap-feeding mines immediately after petal fall. Treatment is recommended if eggs average 2 or more per leaf on leaves 2, 3, and 4 of a fruit cluster at the pink stage, or if sap-feeding mines average 1 or more per leaf on these leaves at petal fall. Sampling can be completed in approximately 10 min. Proper timing is essential for both the assessment of second-generation leafminer densities and control, if required. If done too early, sampling will underestimate the population. If control is applied too late, it will not be effective. Sampling

for “sap-feeding mines” should be done at approximately 690 degree-days (base 43°F) after the start of the flight of the second generation. On average, second-generation spotted tentiform leafminer moths begin flying in early to mid-June. A decision regarding the third generation is generally not required unless the density of the second brood exceeds two mines per leaf.

Control Many parasitoids effectively limit spotted tentiform leafminer populations in some orchards. Most important are the wasps Apanteles ornigis, Sympiesis marylandensis, and Pnigalio maculipes. Insecticide sprays applied in July and August probably do the most harm to these natural enemies. Some leafminer pesticides are effective without being toxic to natural enemies such as mite predators. Depending on the product chosen, application can be made any time from initial egg deposition until the larvae enter the tissue-feeding stages.

Obliquebanded Leafroller, Choristoneura Rosaceana (Harris) Biology and Impact The oblique banded leafroller prefers plants in the Rosaceae family but will feed on many unrelated deciduous trees. This leafroller overwinters as a


second-or third-instar larva on the tree within closely spun cocoons or hibernacula. Larvae become active in the spring when buds begin to open. As foliage pushes from the buds, larvae often tie leaves together and conceal themselves in the resulting chamber. Spring-generation moths emerge in early June in the northeast, with peak activity in mid-June. First-generation larvae complete their development in late July or early August. Summer-generation moths begin flying in early August. Second-generation larvae feed primarily on foliage, but may cause surface injury to fruit if they are very abundant. After feeding briefly, second-generation larvae enter their winter hibernacula. Spring-generation larvae may eat away large portions of developing fruit. If the fruit survive, they are misshapen with large, deep cavities of healed-over injuries. Fruit damaged by first-brood larvae generally falls off the tree. If not controlled, this spring generation of obliquebanded leafroller may cause only small fruit losses (2–4%). The principal impact of summer-generation obliquebanded leafroller is its feeding damage to the fruit. This generally occurs if a leaf is webbed to an apple or clustered apples touch each other. Feeding areas on the fruit are shallow, irregular, and may range from small punctures to large excavations. This injury is more serious than that caused by the overwintering generation because most injured fruits remain on the tree.

Decision Making During bloom or immediately after petal fall, spring-generation larval densities can be classified as above or below a treatment threshold using a sequential sampling procedure. Treatment is recommended if more than 3% of fruit spurs contain live obliquebanded leafroller larvae. Sampling can usually be completed in approximately 10–15 min. Sampling for the summer-generation larvae should take place approximately 600 DD (base 43°F) after the start of the first summer flight. On

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average, summer-generation obliquebanded leafroller moths start flying the first or second week of June. The value of knowing the precise date of this event on a local basis cannot be overemphasized. If information on adult moth flight is not available, July 5 to 10 is a rough approximation of the appropriate sampling period in the northeast. At 600 DD after the start of the adult flight, populations can be classified according to whether the average percentage of terminals infested with live larvae is greater than 3%.

Control Several parasitoids attack the obliquebanded leafroller, but their effectiveness in regulating leafroller populations in commercial orchards is largely unknown. Most growers favor chemical sprays to reduce damage caused by this insect. A contact insecticide is sometimes applied at bloom to petal fall. Most orchards with a history of leafroller infestation require 1–2 pesticide applications against the second-generation larvae. Selective pesticides, including insect growth regulators and those that are based on the bacterium Bacillus thuringiensis are compatible with IPM because they are not toxic to natural enemies (especially mite predators).

European Red Mite, Panonychus ulmi (Koch) Biology and Impact The European red mite overwinters as an egg on the tree. Egg hatch is usually closely correlated with tree phenology, ordinarily beginning at the early pink bud stage and continuing into bloom. If egg hatch does not coincide with the pink stage, it is usually delayed and starts during early bloom. European red mite adults normally appear by petal fall, but few eggs are laid by the first generation of adults on leaves until the first week after

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petal fall. Early hatching European red mite nymphs feed on older fruit cluster leaves and may cause bronzing by petal fall if populations are high. Early season damage before petal fall is usually insignificant, but some studies have shown that heavy damage in early to mid-June can reduce yields during the next season. In the summer months, the European red mite damages apple leaves by inserting its mouthparts to feed on plant juices. This injury reduces the capacity of the leaf to use sunlight as an energy source (photosynthesis), which may lead to reduced yield and fruit quality. Recent studies of European red mite impact have found that the only effect of moderate European red mite injury during the mid- to late season was a reduction in the color of some red varieties of apples. These results have identified the densities of mites that can be tolerated at various times of the growing season.

Decision Making The natural mortality of overwintering eggs can be substantial but is highly variable (10–to 60%). Therefore, sampling or rating schemes are generally not used for predicting the potential early season severity of the European red mite in commercial orchards by assessing the density of overwintering eggs. During late bloom and petal fall, the European red mite is concentrated on older fruit cluster leaves, and therefore the overall density of the first generation will be overestimated by counting mites on the oldest leaves at that time. Early control of the European red mite is essential to prevent early season damage during the postbloom period. One method used to quantify mite presence is the “mite-day” concept, which measures the number of mites and the period of time they are present on the leaves. One mite-day is equivalent to an average of one mite feeding on a leaf for one day. Thus 10 mite-days can be accrued by one mite feeding on a leaf

for 10 days or 10 mites feeding for one day. The current economic threshold of approximately 550 total mite-days (for the growing season) assumes that no significant accumulations of mite-days occur before mid- to late June. Therefore, a protective prebloom oil treatment is currently recommended for control of early season European red mites. During the summer, the need for a miticide to control the European red mite can be determined from a sample of the mite population in an orchard. A sampling procedure is available that determines mite presence based on examination of leaves of intermediate age. This procedure divides mite populations into three categories: greater than threshold, below threshold, and much below threshold. The last two categories provide an indication of when the population must be sampled again. If the density is much below threshold, the population should be sampled in 11–16 days. If it is minimally below threshold, it should be sampled again in 6–10 days. If mite predators are present, these intervals can be lengthened by approximately 50%. Sampling involves recording on a chart the presence or absence of mites in distinct samples of leaves and continues until a decision on whether to treat them can be reached. From petal fall until June 30, a threshold of 2.5 mites per leaf is used. From July 1 to 31, the threshold is 5 mites per leaf. From August 1 to 15, a threshold of 7.5 mites per leaf is used. Treatment for mites is not currently recommended after mid-August. Adherence to these thresholds will prevent serious injury.

Control The European red mite is an induced pest in commercial apple orchards. This means that pesticides used against other arthropods usually destroy naturally occurring mite predators, allowing European red mite numbers to increase to damaging levels. Several major predators of the


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European red mite may be found in commercial orchards, depending on the part of the country where they are located:

conserve it. Because A. fallacis remains in the tree year-round, even early season applications of pyrethroids are damaging to it.

Typhlodromus pyri (Scheuten)

Metaseiulus occidentalis (Nesbitt)

Adults of T. pyri, a major predacious mite species, are present in the tree at about the time of the European red mite hatch. These predators control low to moderate densities of European red mites but do not regulate high populations. This mite predator is very effective against the European red mite and when present in substantial numbers it will eliminate the need for chemical mite control. T. pyri spends its entire life in the tree, overwinters as an adult female, and is active by bloom. It prefers to feed on the European red mite but will sustain itself on other food sources. Once established in an orchard, if it is not disrupted by pesticides, T. pyri will keep European red mite populations to densities of less than one mite per leaf year after year. It may take two to three years for T. pyri to become abundant in an orchard once a selective pesticide regimen is adopted.

Predominantly found in drier climates such as the northwestern states, this predator can also provide biological control of the European red mite in commercial apple orchards. It has high reproductive and prey consumption rates, and disperses readily into orchards. However, it requires the presence of an alternative prey population in the orchard, such as apple rust mites, to preserve its population numbers when red mites are at low levels.

Amblyseius fallacis (Garman) A. fallacis is also an effective predator of the European red mite, but its continued presence in the tree from year to year is not reliable. It overwinters both in apple trees and in the ground cover beneath them. Ground cover, however, appears to have little influence on number and movement of A. fallacis in the tree. A. fallacis was previously believed to a poor biological control agent because it did not move into the trees until late in the growing season after the European red mite had reached problem levels. More likely, A. fallacis numbers often remain low until late in the season because pesticides toxic to them are used early in the season. If a site has a history of A. fallacis, pesticides should be managed to

Zetzellia mali (Ewing) This minute yellow mite is present in nearly all orchards, overwintering as a gravid female in concealed parts of the tree. Although it prefers older rust mites and the eggs and immature stages of European red mites and two spotted spider mites, it feeds on all stages of these species. It undoubtedly helps to control European red mites but is of little benefit if it is the sole predator species present.

Stethorus punctum (Leconte) This small, black ladybird beetle feeds on several small arthropods, including European red mites. It is more common in orchards in the middle Atlantic states. Success in controlling European red mites depends on keeping a relatively high population of European red mites in the tree (3–5 mites per leaf). For chemical control during the early season, petroleum oil is often recommended (a 2% solution at the half-inch green bud stage or 1% at the tight cluster stage) as an early season IPM program. Oil is relatively safe to predators, relatively economical, and European red mite populations have never

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shown resistance to it. Furthermore, a thorough application of oil applied before foliage is fully developed can kill nearly all the eggs present. Other early season treatment options include contact miticides or ovicides applied at the pink bud stage or at petal fall. Miticides will likely cover less of the foliage present by this time, and most are able to be overcome by the development of resistance in local mite populations, so this is a less desirable alternative. Relatively few miticides can control European red mite during the summer. The available contact miticides must be chosen by their individual performance traits, including their activity against specific mite stages and beneficial arthropods, rate of action and length of residual effectiveness, optimal application conditions for each, and any possible resistance that may be exhibited by local mite populations. Because of the limitations of all contact miticides, good spray coverage is essential. Some research has been done on the use of highly refined petroleum oils to control summer mite populations. Acceptable season-long control has been achieved by using a multiple-spray program starting at petal fall, followed by periodic monitoring throughout the summer. Potential difficulties with this approach include leaf damage and incompatibility with some of the fungicides used to control summer diseases.

Plum Curculio, Conotrachelus nenuphar (Herbst) Biology and Impact Plum curculio adults move into orchards from overwintering sites in hedgerows or the edges of woods and are present in the trees from the late pink stage to early bloom before the fruit is susceptible to damage. Adults are active in the spring when temperatures exceed 60°F. Adult females oviposit in fruit during both day and night but feed mostly at night. Depending on temperature,

overwintering adults remain active for two to six weeks after petal fall. Although adults may feed on blossoms, apples are not susceptible to damage until petal fall, at which time adults damage fruit by both feeding and ovipositing. Unlike fruit injured by other pests, many apples damaged by plum curculio will remain on the tree until harvest. Because adults are not highly mobile, orchards near overwintering sites, woodlands, and hedgerows are most susceptible to attack. Fruit damage is usually most common in border rows next to sites where adults overwinter.

Decision Making Monitoring for the plum curculio is not often recommended because of the amount of time and labor involved and because it is generally assumed to be present in every orchard where populations are endemic. Nonetheless, various techniques have been used to monitor plum curculio damage and the presence of adults: – Clubs or shakers can be used to jar adults from limbs into catching frames or cloths for counting. – Polyethylene funnels hung under branches can be used to capture adult PC. – Immature “scout apples” hung in trees near the edges of orchards serve to measure oviposition scars before petal fall so potential damage can be estimated before control sprays are applied. – Oviposition scars on immature fruit can be counted in orchards starting at petal fall to estimate damage. Because substantial oviposition and damage can occur even after a single warm day and night, frequent scouting for damaged fruit is necessary after petal fall.

Control Several species of wasps parasitize the eggs and larvae of the plum curculio. Ants, lacewings, and ground beetles prey on larvae in the soil, and some


fungi kill larvae. These organisms are not usually sufficient to regulate populations of plum curculio in commercial orchards. The plum curculio is difficult to control completely with insecticides. Relatively high rates and persistent applications are important because adults may be active for two to six weeks after petal fall depending on temperatures. Several commercial products are available to control this insect. In normal orchards that are not near woodlots or hedgerows and have not suffered previous damage, a single application at petal fall will provide seasonal control. In problem orchards, a petal fall application followed by a second spray 10–14 days later will provide adequate control. In orchards with chronic problems, or in seasons when adult activity is prolonged by unusually cool and wet weather, two cover sprays applied 10–14 days apart after petal fall may be necessary to prevent late damage. Research on heat unit accumulation and plum curculio oviposition has proposed that control sprays are no longer necessary whenever the last spray has been applied within 10–14 days after the accumulation of 340 DD (base 50°F) from petal fall.

Codling Moth, Cydia pomonella (Linnaeus) Biology and Impact The codling moth overwinters as a larva in a cocoon under loose bark on the tree trunk. Adults emerge during bloom, and the first flight continues until about 30 days past petal fall. Eggs, laid singly on the upper surface of leaves or fruit, start to hatch at petal fall and continue for two to three weeks. Larvae feed only on fruit. Surface bites, referred to as stings, cause blemishes, and deeper injuries are caused by feeding inside the fruit. Fruits injured by extensive internal feeding usually drop in the middle of June at which time early season damage becomes noticeable.

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Adults from the second or summer generation of codling moth start to fly about mid-July, and the peak flight occurs around the first week in August. Larvae from this generation are active in fruit throughout August. Fruit damage by second generation larvae is generally more serious than that of the first.

Decision Making Adult males can be captured in pheromone traps, but numbers of males captured in these traps cannot be related to potential fruit damage. Thus, pheromone traps are used only to monitor the seasonal activity patterns of adults within an area. It is not practical to monitor commercial apple orchards for CM eggs or larval fruit entries because of the theoretical zero tolerance for internal fruit damage. Developmental models, based on temperature accumulations after the first catch of males, can be used to predict the first egg hatch of codling moths. This approach is used to time initial control sprays for the codling moth at 250–360 DD (base 50°F) after first adult catch for the first generation, and 1260–1370 DD after this same biofix date for the second generation.

Control The codling moth is attacked by both parasites and predators, but these natural enemies cannot effectively control this pest in commercial orchards. To kill the larvae before they enter the fruit, chemical sprays for the codling moth must be initiated before the eggs hatch. The codling moth is most effectively controlled by the same conventional insecticides used against the plum curculio, but it can also be controlled by more selective pesticides such as bacteria (Bacillus thuringiensis), insect growth regulators, viruses, and botanicals, although many of these products are less effective than standard insecticides.

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Apple Maggot, Rhagoletis pomonella (Walsh) Biology and Impact The apple maggot overwinters as a pupa in the soil. Adults from the single annual generation of flies emerge in late June to early July. Females cannot lay eggs until they become reproductively mature, 7–10 days after emergence. Females lay eggs in fruit and the larvae develop there, emerging in the autumn after the fruit has fallen and entering the soil to pupate. Flies are active from July to mid-September, but commercial orchards require protection only from about mid-July through August. Flies do not reach orchards in large numbers until mid-July, and before this date, fruit remaining on the tree is unfavorable for larval development so early infestations do not cause sustainable populations in the orchard. In addition, for unknown reasons, fly activity between late August and mid-September generally does not result in serious damage in most commercial orchards. Larval tunneling inside fruit causes it to become rotten and unmarketable. Early stings caused by punctures from female ovipositors may severely deform the fruit of some varieties, even though no larvae survive.

Decision Making Monitoring to determine whether control sprays are necessary is recommended only in orchards that are not near large sources of outside infestation, such as abandoned orchards or those with no indigenous infestations of flies. In early to mid-July, red sphere traps baited with apple volatile lures are hung in trees along the edge of the block closest to an abandoned orchard or a stand of woods. These traps are checked one to two times per week. A spray of a suitable insecticide is applied if a cumulative average of 3–5 apple maggot flies per trap is captured. After spraying, trap catches are not checked again until after a 10 to 14-day period, during which spray residues would kill any immigrating flies.

Theoretically, there is absolutely no tolerance for apple maggot damage in fruit. In practice, apple maggot damage is not usually detected in normal fruit inspections unless there is approximately 3% fruit damage.

Control Small wasps parasitize apple maggot larvae in fruit, and predators such as birds and crickets may eat larvae or pupae in or near the soil. In natural, unsprayed apple and hawthorn trees, apple maggot populations are not regulated by natural enemies. Parasites and predators are also ineffective at controlling apple maggot in commercial orchards. Apple maggot flies have a limited migratory capability, so all apple and hawthorn trees within 1/4 to 1/2 mile of commercial orchards should be removed if possible. Dropped fruit should not be allowed to remain beneath the tree for more than one or two days. Eliminating fruit drops will break the life cycle of flies in an orchard by preventing larvae from exiting the fruit and entering the soil. Apple maggot flies can be trapped in small, well-pruned trees that are not near large sources of outside infestations. A relatively high density of sticky red spheres (plain or volatile-baited) is required, approximately 1 trap per 100 apples. Mass trapping is usually less effective than chemical control, and apple maggot may still damage 1–5% of fruit from mass-trapped orchards. Most commercial orchards have no indigenous populations of flies. Therefore, chemical control sprays are usually directed against flies immigrating into orchards from outside, unsprayed hosts, including both apples and hawthorns. Most broad-spectrum insecticides are remarkably effective in controlling adults. Insecticides must kill females before they oviposit in the fruit. Residual effectiveness of insecticides is particularly important in controlling apple maggot in commercial orchards when flies are continuously immigrating.

Aquatic Entomology and Flyfishing

References Helle W, Sabelis MW (1985) World crop pests, vol 1: spider mites: their biology, natural enemies and control. Elsevier, Amsterdam, The Netherlands Metcalf RL, Metcalf RA (1993) Destructive and useful insects: their habits and control, 5th edn. McGraw-Hill, New York, NY, pp 1073 Minks AK, Harrewijn P (1987) World crop pests, vol 2: aphids: their biology, natural enemies and control. Elsevier, Amsterdam, The Netherlands Pimentel D (1991) CRC handbook of pest management in agriculture, vol 3. CRC Press, Boca Raton, FL Robinson AS, Hooper G (1989) World crop pests, vol 3: fruit flies: their biology, natural enemies and control. Elsevier, Amsterdam, The Netherlands Van der Geest LPS, Evenhuis HH (1991) World crop pests, vol 5: Tortricid pests: their biology, natural enemies and control. Elsevier, Amsterdam, The Netherlands

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Apterae Wingless forms, usually used in reference to wingless parthenogenetic female aphids.  Aphids

Apteropanorpidae A family of insects in the order Mecoptera.  Scorpionflies

Apterous A term used to denote that the insect is lacking wings.

Apple Proliferation This is an important insect-transmitted mollicute (bacterial) disease of apples in Europe.  Transmission of Plant Diseases by Insects

Apple Rust Mite, Aculus Schlechtendali (Acarnia: Eriophyidae) This is an important apple pest in some areas.  Four-Legged Mites  Mites  Apple Pests and their Management

Apposition Eye A type of compound eye found in diurnal insects in which the ommatidium is shielded by pigment. This type of eye is also called a p hototopic eye.

Appressorium The swollen tip of a fungal hypha that facilitates attachment to the host, and penetration by the fungus.

Apterygote Insect taxa that do not possess and never possessed (in evolutionary time) wings. A member of the class Insecta, subclass Apterygota.

Apystomyiidae A family of flies (order Diptera).  Flies

Aquatic Entomology and Flyfishing john r. wallace, frank d. l. rinkevich Millersville University, Millersville, PA, USA The use of aquatic insects as lures for fish dates back to the second century a.d. In the seventeen volume treatise, De Animalum Natura, the Roman Aelianus discussed his observations of fish consuming insects at the water surface and how Macedonian fishermen used dry flies or spinners to catch what were thought to be trout from the Astraeus River. Not until fifteen

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centuries later did Charles Cotton propose the utility of aquatic insects in fishing. In 1836, Alfred Ronald’s Fly Fisher’s Entomology was published. This publication elaborated on fly tying methods and fishing techniques from an entomological perspective. Most recently, fly anglers are attempting to increase their knowledge about insects, specifically aquatic insects, in terms of imitating fish food items or “matching the hatch.” This quest for entomological knowledge by anglers, in addition to aquatic scientists and fish managers, has prompted the need for better taxonomic and ecological treatments friendly to both the scientist and the angler. In order to create a functional artificial imitation of an insect to improve one’s chances of catching a trophy fish, the angler requires basic identification, ecological and behavioral information of both insects (prey) and fish (quarry).

Terminology: Entomology Versus Flyfishing As with many fields of scientific study, understanding the complexities of both entomology and fly fishing requires an understanding of both languages. While the term “fly fishing” technically refers to only one insect order, Diptera, in reality it encompasses all insect and non-insect invertebrates used as food by fish. Representatives from several orders of terrestrial insects (e.g., Hymenoptera, Orthoptera, Diptera, and Lepidoptera) are common food items of fish and are mimicked with artificial flies. However, aquatic insects are the primary interest of anglers and are the majority of fly patterns mimicked. For example, there are thirteen orders of insects that are classified as aquatic. Only 3% of all insects have a life stage in an aqueous environment. Some of these orders are entirely aquatic whereas others have a few semi-aquatic representatives. Truly aquatic orders are those in which all of their members exhibit some portion of their life cycle in an aquatic habitat. The orders, Ephemeroptera (mayflies), Plecoptera (stoneflies), and Trichoptera (caddisflies) are examples of truly aquatic orders.

Semi-aquatic orders are largely terrestrial with a number of families exhibiting life stages in or near water. Coleoptera (beetles), Diptera (flies), and Lepidoptera (butterflies) represent semi-aquatic orders. Typically, anglers refer to an emergence of insects (but more specifically to those with aquatic larval stages) as a “hatch.” What the angler will call a nymph, the entomologist would refer to as the larval stage of an insect. Mayflies are the only group of insects that have a non-reproductive adult stage (the subimago); anglers refer to this stage as “duns.” Post-ovipositing mayflies typically die with their wings spread on the water surface, and anglers term these “spinners,” referring to the spinning action they exhibit while floating on the water surface. In addition, anglers refer to reproductively mature insects that end their life cycle on the water surface either by nature or that accidentally hop, fly or are blown onto the water surface as “dry flies.” Fly patterns will mimic the larval and adult stages of both terrestrial and aquatic insects. The sports angler often refers to insects by a number of colloquialisms. Educated fishermen often use the term caddis or caddisfly in reference to the order Trichoptera, fishflies for Megaloptera, and sandflies for some Diptera. Mayflies are known by a variety of names such as drakes or upwings.

Morphological Importance Although the standard “mantra” of the dedicated fly angler is that the three most important aspects to catch fish are presentation, size and pattern, anglers must be familiar with many aspects of insect morphology. Most often, hand-tied flies incorporate the obvious features of the insect they are imitating. For many mayfly presentations, large characteristics such as wing size, caudal filaments, and body color are considered when tying flies. Small traits such as specific setation, paraglossae, and tarsal segments are often


ignored largely due to their size relative to the insect and the investment of time that would be spent including these features in a fly. A fish will not recognize these small features because, at times, they may see the lure for only a few seconds. Flies fit into two general classes based on their presentation. Dry flies are presented on the surface and signify the adult stage. Wet flies are fished below the surface and represent larvae. Success of the presentation is largely dependent on the time of the year. Presentation should mimic

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the natural life cycle of the native insects. A sample taken with a kick seine or observation of emergences will indicate what type of fly to use. An emergence of mayflies in the summer is the reason why an adult mayfly mimic presented on the surface may outfish a wetfly of a caddisfly. Several aquatic insect orders are often used as models for fly tying and as live bait. There are many fly imitations of caddisflies, mayflies and stonefly larvae (Fig. 71), as well as aquatic Diptera larvae and adults, due to their ecological importance of providing food for fish.

Insect

Fly Imitation

May Fly Dun (Subimago)

Sidewinder No Hackle Dun

Stone Fly Larva

Rubber-Legged Stone Fly Nymph

Adult Midge

Adult Midge

Emerging Dun

Emerging Dun Imitation

Adult Caddis Fly

Hen Caddis

A.

B.

C.

D.

E.

Aquatic Entomology and Flyfishing, Figure 71 A collection of common aquatic insects used as mimics for wet and dry artificial fly patterns. (A, C, D, and E = represent dry flies; B represents a wet fly or nymph). Illustrations by Mike Gouse (published in Swisher D, Richards C (1991) Emergers. Lyons & Burford Publishers, New York, NY).

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Aquifer

Ecological and Behavioral Importance Though fly fishing strategists argue over imitation vs. presentation, fly fishing tactics that employ ecological and behavioral aspects are as important as using a fly pattern based on the appearance of natural insects. Although insect abundance is important, fish will not eat the most abundant insect if it is not available to them. Three ecological aspects important in the availability of a particular insect include: stage of development, habitat use and activity (either associated with drift or foraging for food). Although aquatic insect larvae are most abundant after hatching, they are not as available as fish food due to their small size and ability to avoid predators. In terms of energetics, a small insect is equivalent to small energetic payoffs. However, as aquatic insects grow and develop from one stage to the next they become more obvious to fish predators through their feeding activities. Thus, availability increases as insects grow and develop. Emergence for aquatic insects is a risky task. It is these emergers that are most available as they struggle to reach the water surface, plant stem or emergent rock from which they attempt to emerge as adults. Fish will concentrate feeding efforts on emerging insects if the adult stage escapes quickly. Those adult insects, both terrestrial and aquatic, that expire on the water surface are readily fed upon by fish. Aquatic insects inhabit a wide variety of microhabitats within a given stream or pond, including rock or log surfaces, on plant stems or other submerged vegetation, as well as swimming openly in the water column. Habitat use by aquatic insects is relative to their needs. For example, foraging for food may put an insect in a different microhabitat other than used during non-feeding periods. Some mayflies may exhibit this behavior switch. Diel feeding activities among Phantom midges (Chaoboridae) also is an example of this type of behavior. Finally, phenological aspects of aquatic insect activity related to emergence, drift and oviposition increase insect availability. Some of these ecological/behavioral phenomena are tied to weather changes, lunar activity, water temperature and current regime.

References Hafele R, Roederer S (1995) An angler’s guide to aquatic insects and their imitations for all North America. Johnson Books Publisher, Boulder, Colorado, 182 pp McCafferty PW (1983) Aquatic entomology. Jones and Bartlett Publishers, Boston, MA, 448 pp Merritt RW, Cummins KW (1996) An introduction to the aquatic insects of North America. Kendall/Hunt Publishing, Dubuque, IA, 862 pp Swisher D, Richards C (1991) Emergers. Lyons & Burford Publishers, New York, NY, 120 pp

Aquifer An underground formation of sand gravel or porous rock that contains water. Aquifers are an important source of water is some areas, and must be protected from pesticide contamination, affecting the type of pesticides and pesticide application technologies that are used.

Aradidae A family of bugs (order Hemiptera). They sometimes are called flat bugs.  Bugs

Arbovirus Viruses transmitted by arthropods. This is an acronym for ARthropod-BOrne VIRUSes.

Archaic Bell Moths (Lepidoptera: Neopseustidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Archaic bell moths, family Neopseustidae, include nine known species (six from Southeast Asia and three from Chile). The family forms a

Arctics

monobasic superfamily, Neopseustoidea, and the only member of the infraorder Neopseustina, of the suborder Glossata and subcohort Myoglossata. Adults small (14–27 mm wingspan), with head roughened; haustellum short, with vestigial mandibles; labial palpi 3-segmented and somewhat upcurved; maxillary palpi 5-s egmented; antennae are mostly rather long and somewhat thickened. Maculation is pale, usually translucent with gray spots, and wing shapes rather broad and quadrate. When resting the wings are held in a rounded shape that resembles a bell. Adults are crepuscular or diurnal. Biologies and larvae remain unknown, but species in Chile are thought to possibly feed on native bamboos.

References Davis DR (1975) Systematics and zoogeography of the family Neopseustidae with a proposal of a new superfamily (Lepidoptera: Neopseustoidea). Smithsonian Contributions to Zoology 210:1–45 Davis DR (1997) Neopseustidae. In Lepidopterorum Catalogus, (n.s.). Fasc. 7. Association for Tropical Lepidoptera, Gainesville, p 8 Davis DR, Nielsen ES (1980) Description of a new genus and two new species of Neopseustidae from South America, with discussion of phylogeny and biological observations (Lepidoptera: Neopseustoidea). Steenstrupia 6:253–289

Archaic Sun Moths (Lepidoptera: Acanthopteroctetidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Archaic sun moths, family Acanthopteroctetidae, are very similar to Eriocraniidae, and include only four species, all North American except for one in the Palearctic (originally described in a separate family Catapterigidae). The family, plus the related Eriocraniiidae, are

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the only members of the superfamily Eriocranioidea, which form the infraorder Dacnonypha of the suborder Glossata. There are two subfamilies: Acanthopteroctetinae and Catapteriginae. Adults small (11–16 mm wingspan, with roughened head scaling and only short 2-segmented labial palpi; maxillary palpi are 5-segmented and folded; haustellum is reduced and vestigial mandibles are present. Maculation is more somber than in Eriocraniidae and adults are thought to all be diurnal. Larvae are blotch leafminers on Ceanothus (Rhamnaceae) in the single known biology.

References Davis DR (1969) A review of the genus Acanthopteroctetes with description of a new species (Eriocraniidae). J Lepid Soc 23:137–147 Davis DR, Frack DC (1987) Acanthopteroctetidae (Eriocranioidea). In: Stehr FW Jr (ed) Immature insects, vol 1. Kendall/Hunt Publishing, Dubuque, IA, pp 345–347 Zagulajev AK, Sinev SY (1988) Catapterigidae, a new family of lower Lepidoptera (Dacnonypha). Entomol Obozrenie 68:593–601 [in Russian] (English translation 1989: Entomol Rev 68:35–43)

Archeognatha An apterygote order of insects, also called Microcoryphia. They commonly are known as bristletails.  Bristletails

Archipsocidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids

Arctics Some members of the family Nymphalidae, subfamily Satyrinae (order Lepidoptera).  Butterflies and Moths

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Arctiidae

Arctiidae A family of moths (order Lepidoptera). They commonly are known as tiger moths, footman moths, or wasp moths.  Tiger Moths  Butterflies and Moths

Arculus A small cross vein of the wing. The position of the cross vein (Fig. 72) varies among orders, but is associated with the cubitus vein.  Wings of Insects

Area-Wide Insect Pest Management waldemar klassen University of Florida, Homestead, FL, USA Area-wide pest management is one of several major plans or strategies for coping with pest problems. Management of localized populations is the conventional or most widely used strategy, wherein individual producers, other operators and households practice independent pest control. However, since individual producers or households are not capable of adequately meeting the challenge of certain very mobile and dangerous pests, the area-wide pest management strategy was developed.

The area-wide pest management strategy includes several substrategies including (i) management of the total pest population in all of an ecosystem, (ii) management of the total pest population in a significant part of an ecosystem, (iii) prevention, which includes containment of an invading population and quarantine, and (iv) eradication of an entire pest population from an area surrounded by naturally occurring or man-made barriers sufficiently effective to prevent reinvasion of the area except through the intervention of man.

Characteristics of Area-Wide Pest Management Immigration of pests into a managed ecosystem prevents their eradication. However, it is easy to underestimate the tremendous impact of the immigration of pests from small untreated foci into a managed area. For example, very few codling moths, Cydia pomonella (L.) develop in the well managed commercial apple orchards, but researchers found that the number of codling moths that overwintered in the in Wenas Valley of Washington State dropped by 96% when a few abandoned orchards and neglected noncommercial apple trees were either removed or sprayed with insecticide. This study indicated that most of the codling moths in commercial orchards originated on untreated host trees that in aggregate were 49°C (120°F) for more than 10 min with laundry detergent. Bed bugs, like all insects, are very susceptible to drowning when exposed to soap, so the addition of laundry detergent will ensure a quick kill. Placing bed clothes in a dryer at 60°C (140°F) for 20 min or longer is also recommended to make sure that no bed bug eggs survive.

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Because bed bugs are susceptible to high temperatures, heat fumigation is being used to eradicate bed bugs from large commercial facilities. Using the heat fumigation technology developed for the treatment of grain silos, fans are used to blow air in from the outside to raise the atmospheric pressure inside the facility. The air is then heated and monitored to make sure that all locations inside the building reach the appropriate temperature (bed bug thermal death point) and pressure. The heat treatment is then maintained for a period of hours to ensure that all bed bugs and bed bug eggs are killed. Although heat fumigation is an effective bed bug treatment, the cost, like that of chemical fumigation, is often prohibitively expensive for the average consumer. Exposing bed bugs to cold temperatures will kill bed bugs but the duration of exposure is often too long to be practical. For example, the thermal death point for adult bed bugs exposed to cold temperatures for 1 h is −18°C (−1°F). Yet, most conventional freezers have a minimum temperature of 0°C (32°F), thus requiring that the bed bugs be frozen long enough to achieve 100% kill. Attempting to kill bed bugs at 0°C will take several days at least, and if the bed bugs are insulated in clothes or bedding it may take several weeks of exposure to ensure that all bed bugs are killed and bed bug eggs are no longer viable. Although increased sanitation and exclusion techniques are necessary to remove bed bug harborages, these techniques alone will not control an established infestation. Therefore, chemical methods must also be employed as part of a comprehensive bed bug management program. As stated earlier, most modern pesticides will not control bed bug infestations when used individually. However, combinations of products with different formulations and modes of action have been evaluated in the field and have been found to produce satisfactory control. These products must be applied according to the product label and the treatment area must be regularly monitored to make sure that the products are working. Field evaluations

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Bed Bugs (Hemiptera: Cimicidae: Cimex spp.)

have determined that microencapsulated products containing pyrethroids are an effective residual spray because the micro capsules stick to the bed bug body allowing for enough exposure time to kill resistant bed bugs. These products can be used for application into cracks and crevices where bed bugs hide and also along baseboards or ceiling/ wall junctions where bed bugs will often harbor when the infestation levels are high. In addition to the crack and crevice applications, products labeled for upholstery treatment can be applied to infested furniture as well as to the mattress and box springs. Some mattress products have residual activity (pyrethroids) while other “non-toxic” products do not. The non-toxic products that contain isopropyl alcohol or sodium laurel sulfate as the primary killing agent will kill bed bugs on contact. Yet, these products evaporate almost immediately after application and bed bugs that survive the treatment will continue to bite and reproduce. Residual dusts are particularly useful in the frame of the box springs and wood components of the other furniture because they stay within the application site and have a very long residual. Residual dusts containing pyrethroids also adhere to the bed bug’s body allowing for the long exposure period (possibly days) necessary to kill resistant bed bugs. “Non-toxic” desiccant dusts will also kill bed bugs but they too may take several days to work. Baseboard, and crack and crevice treatments with insect growth regulators are useful in that they will kill many immature bed bugs during the final molt. However, there is no evidence that insect growth regulators will kill or sterilize adult bed bugs. Although aerosols and foggers are frequently used for bed bug elimination, they are not effective control products because they do not penetrate into bed bug harborages. Overall, a complete bed bug treatment should include the removal of infested items for either treatment or disposal, the laundering of infested clothes and bedding, the elimination of clutter, the sealing of all small cracks and holes that might provide bed bug harborage, a

complete vacuuming of all carpeting and furniture, steam cleaning of upholstered furniture and mattresses to kill bed bugs and their eggs, and treatment of the mattresses and box springs with a non-toxic mattress treatment (preferred) or a labeled residual insecticide. After treating the mattress, both the mattress and box springs should be encased in bite proof, escape proof mattress covers. The infested room should be treated with a combination of residual insecticide spray and an insect growth regulator. These products should be applied according to the label to cracks and crevices, baseboards, and any other bed bug harborage locations. The infested room and all adjoining rooms should then be inspected (and/or treated) weekly to determine the efficacy of the treatment products and to make sure that the bed bug population is being eliminated.

Summary Most entomologists and pest management professionals believe that the resurgence of human bed bugs (both Cimex lectularius and Cimex hemipterus) presents the single greatest indoor pest management challenge in decades. Since the bed bugs’ widespread reappearance in the 1990s, the common bed bug has become a full blown epidemic with new infestations reported in most European countries and in all 50 states in the United States. Likewise, the tropical bed bug has spread throughout the tropics in the last 10 years increasing its range to infest Australia and reestablishing populations in Singapore and other tropical nations where they had been previously eradicated. Because these insects have never completely disappeared from developing nations they have been continuously treated with many insecticide products over the last 50 years. This continuous pesticide pressure has selected for bed bug resistance, particularly to pyrethroids. These pyrethroid resistant populations present a unique problem in developed nations where

Bee Louse, Bee Fly, or Braulid, Braula coeca Nitzsch (Diptera: Braulidae)

public opinion and federal legislation has eliminated entire classes of insecticides from indoor use due to their perceived toxicity. Pyrethroids have been one of the few chemical classes that remain available for indoor use due to their low mammalian toxicity. As a result, pyrethroids are the most frequently used class of chemistry for bed bug control in the United States today. However, with increasing bed bug resistance these products will gradually become less effective at controlling new infestations. Because of the prevalence of bed bug resistance many researchers believe that the bed bug e pidemic will become much more severe in the future. The key to bed bug control in developed nations will ultimately be education. People will have to accept that bed bugs exist and learn how to avoid transporting bed bugs to their homes (from hotels, taxis, air planes, camp cabins, movie theaters, laundromats, day care centers, multiple unit housing, etc.) during the course of their daily activities. The ability of the average citizen to identify bed bugs and bed bug evidence will be critical for them to successfully protect themselves and their home from bed bug infestations.

References Cooper R, Harlan H (2004) Bed bugs and kissing bugs. In: Hedges S (ed) Mallis handbook of pest control, 9th edn. GIE Publications, Cleveland, OH, pp 494–529 Doggett S, Geary M, Russell R (2004) The resurgence of bed bugs in Australia: with notes on their ecology and control. Environ Health 4:30–38 Harlan H (2006) Bed bugs – importance, biology, and control strategies. Armed Forces Management Board Technical Guide No. 44. http//:www.afpmb.org/pubs/tims/TG44/ TG44.htm Johnson CG (1942) The ecology of the bed-bug, Cimex lectularius L in Britain. J Hyg 41:345–361 Moore DJ (2006) Evaluation of multiple insecticidal products for control of the common bed bug (Cimex lectularius, (L.)). Unpublished M.S. thesis, Virginia Tech University, Blacksburg, VA, 118 pp

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Newberry K (1989) The effects on domestic infestations of Cimex lectularius bed bugs of interspecific mating with Cimex hemipterus. Med Vet Entomol 3:407–414 Potter M (2006) The perfect storm: an extension view on bed bugs. Am Entomol 2:102–104 Usinger S (1966) Monograph of Cimicidae. Thomas Say Foundation Vol. VII. Entomological Society of America, Lanham, MD, 585 pp Vall Meyers M, Hall A, Inskip H, Lindsay S, Chotard J (1994) Do bed bugs transmit hepatitis B? Lancet 343:761–763 Webb P, Happ C, Maupin G, Johnson B, Ou C (1989) Potential for insect transmission of HIV: experimental exposure of Cimex hemipterus and Toxorhynchites amboinensis to Human Immunodeficiency Virus. J Infect Dis 160:970–977

Bee Bread A pollen and honey mixture fed to bee larvae by worker bees

Bee Flies Members of the family Bombyliidae (order Diptera).  Flies

Bee Lice Members of the family Braulidae (order Diptera).  Flies  Bee louse

Bee Louse, Bee Fly, or Braulid, Braula coeca Nitzsch (Diptera: Braulidae) jamie ellis University of Florida, Gainesville, FL, USA The bee louse, Braula coeca Nitzsch (Diptera: Braulidae), is a wingless fly that lives as a

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Bee Louse, Bee Fly, or Braulid, Braula coeca Nitzsch (Diptera: Braulidae)

c ommensalist in western honey bee (Apis mellifera L.) colonies. Not much is known about the bee louse as its biology has been studied only irregularly since the 1920s. The fly is presumed to be harmless to its host, although this point is debatable. It is found in many countries, and because no true e conomic damage can be attributed to the fly, it probably poses a minimal threat to bees.

Bee Louse Life Cycle and Behavior Adult bee lice (Fig. 24) are small (30 days.

Eggs Eggs are laid in masses of approximately 100 between leaf surfaces apposed and cemented in place by the female. Eggs complete development in approximately 7 days at 26°C with a lower developmental threshold of 12°C and an upper thermal limit between 30 and 32°C. The niche created by the female apparently provides conditions of temperature and humidity required for egg development.

Larva Neonate larvae fall to the ground where they disperse and burrow into the soil. The lower threshold for development of neonates was estimated to be 15°C. Larval development to pupation occurs in approximately 125 days at 26°C. At the onset of pupation, larvae reared on artificial diet can weigh as much as 600 mg, depending on conditions of temperature and humidity experienced during larval development.

Pupa The pupa creates a chamber in the soil by means of a writhing motion. Pupation is completed in

approximately 3 weeks at 26°C. Initially, the exarate pupa is callow, becoming darker as pupation proceeds.

Adults Adults vary in size between approximately 1 and 2.5 cm in length. Mean male length and mass are less than mean female size. Adults produced on artificial diet vary in weight from about 250 –350 mg. Males engage in prolonged bouts of guarding behavior and can remain mounted and intromitted for hours. There is anecdotal evidence for adult aggregation, presumably mediated by an as yet undiscovered pheromone. Diaprepes adults are largely black but covered with colored scales that range from ashy white to dull orange and bright yellow. Distinct phenotypes occur within defined geographic regions, marked by varying colors and patterns of elytral stripes. The length and number of raised ridges on the elytra devoid of scales varies between populations. On St. Lucia and Puerto Rico, there is subspecific variation in color and elytral ridges linked by intergrades. On Puerto Rico, western lowland populations of D. abbreviatus tend to have whitish elytra. They are brownish in southern and eastern lowlands including Culebra and Vieques. In the western central mountains, there is a larger phenotype often with yellow elytra and an additional strip per elytron; in the eastern mountains, a smaller, grayish, sometimes greenish variety prevails. On Barbados, the weevil was described in 1912 as pale-green with dark, bronze stripes. Emergent adults require 24–48h to fully sclerotize within the pupal chamber in the soil. Initially, adults possess a deciduous mandibular spur that likely facilitates adult emergence from the soil and is subsequently lost. Females have been estimated to produce on the order of 5,000 eggs over the adult lifespan that may be as long as 3–4 months in the field. Females cease oviposition at temperatures below 15°C.

Diaprepes Root Weevil, Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae)

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Damage

Insecticides

Diaprepes abbreviatus was described in 1987 as the single most serious insect pest of agriculture, horticulture, and silviculture on Puerto Rico. In the 1930s, D. abbreviatus rivaled the sugarcane borer, Diatraea saccharalis, as the most serious pest of sugarcane in Barbados. The weevil, an apparently indigenous insect, did not infest sugarcane for centuries despite its extensive cultivation on Barbados. Infestations on sugarcane and sweet potatoes were not observed prior to 1901. By 1904 it had become fairly abundant, but not serious until 1909, and since that date it has increased in virulence every year. In 1922, loss was estimated at 3.5 tons and in 1929 at 5–6 tons of cane/acre on Barbados. Adult feeding damage consists of notching of leaf margins. Adult damage to citrus is considered minor. Larval damage to citrus is a function of direct damage to roots and secondary infection of wounds by pathogenic fungi, particularly Phytophthora spp. For this reason, damage is more severe in poorly drained soils conducive to fungal pathogens. While larvae remain external to citrus roots, they bore into and inhabit subterranean parts of sugarcane, sweet potato, potato, cassava, and other plants with tuberous roots or tubers.

Chlorinated hydrocarbon and other highly persistent insecticides were used as barriers to neonate weevils, for control of larvae in the soil, and as adulticides until the removal of such materials from the market. The waning of the era of persistent insecticides coincided with the introduction of D. abbreviatus into the United States. Several modern insecticides are effective against adults. However, because of the short residual effectiveness of foliar sprays and the prolonged period of adult emergence, adulticides may only be effective when used frequently over large areas. Porous soils and a vulnerable water table in Florida limit the use of soil insecticides on citrus. At least two species of entomopathogenic nematodes are marketed as bioinsecticides for this species.

Management Sampling A modified Tedders trap, consisting of a base of two interlocking vanes topped by a mesh receptacle has been used to estimate relative adult density. Since no pheromone or attractant is known for this species, such traps are inefficient and yield only very small numbers of weevils. The trap is based on the tendency for newly emerged adults to walk over the soil surface to dark vertical shapes. A more productive, active sampling method uses a beat sheet to sample individual trees.

Cultural Practices Publications from the Caribbean in the early 1900s recommended pulling cane stumps after harvest to expose larvae and suggested “a few head of poultry” be kept on hand during the operation. It was suggested that fully developed larvae disperse from the cane stools in search of moist soil to pupate, sometimes moving a considerable distance in the soil. Large numbers of adults emerged after the first heavy rains of May/June. In 1939, a system of cash payments was advocated for collection and destruction of adult weevils. It was noted that continuous cropping of cane increased damage from Diaprepes. In 1911, school children on Barbados, St. Kitts and Antigua were enlisted to collect and destroy adults – 30,000 were captured and destroyed on one estate during 1 month. Adult weevils were reported from pigeon pea, corn, bean, and sweet potato (considered an especially good host for the weevil). Cooperative campaigns over a decade to reduce populations on Barbados were deemed successful due to the fact that the island is small, densely populated, and had a minimal amount of uncultivated land.

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Diaprepes Weevil, Diaprepes abbreviatus (Linnaeus) (Coleoptera: Curculionidae)

Manual collection of newly emerged adults, especially from cane fields, was facilitated by planting attractive host plants such as pigeon pea (Cajanus cajan) or other fast-growing shrubs or trees on field borders. A “bare-root method” has been suggested wherein soil is removed from the roots at the base of citrus stems thereby limiting access by larvae to the crown and thereby reducing the possibility of girdling. Kaolin-based particle films have shown some promise in reducing oviposition in field trials in Florida.

Host Plant Resistance Only low levels of plant resistance to D. abbreviatus have been reported from sexually compatible citrus genotypes. Higher levels of resistance occur in related citroid fruit trees and some nonhost legumes. Recently, active isolates of Bacillus thuringiensis (Bt) have been discovered, raising the possibility of a genetically engineered rootstock transformed to express a Diaprepes-active toxin gene.

Biological Control The toad Bufo marinus was imported to Puerto Rico from Barbados in 1920 and again from Jamaica in 1924 to control white grubs (Phyllophaga spp.) and D. abbreviatus. Two species of egg parasitoids have been established and two other species have recently been released in southern Florida but are constrained by prey availability during the winter months at more northern latitudes. They are not expected to establish in central Florida, Texas, or California unless periodic releases are made. Entomopathogenic nematodes are the only other biological control methods currently used.

References Hall DG, Peña J, Franqui R, Nguyen R, Stansly P, McCoy C, Lapointe SL, Adair RC, Bullock B (2001) Status of

biological control by egg parasitoids of Diaprepes abbreviatus (Coleoptera: Curculionidae) in citrus in Florida and Puerto Rico. BioControl 46:61–70 Lapointe SL (2000) Thermal requirements for development of Diaprepes abbreviatus (Coleoptera: Curculionidae). Environ Entomol 29:150–156 Lapointe SL, Bowman KD (2002) Is there meaningful plant resistance to Diaprepes abbreviatus (Coleoptera: Curculionidae) in citrus rootstock germplasm? J Econ Entomol 95:1059–1065 Lapointe SL, McKenzie CL, Hall DG (2006) Reduced oviposition by Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae) and growth enhancement of citrus by Surround particle film. J Econ Entomol 99:109–116 Shapiro DI, McCoy CW (2000) Virulence of entomopathogenic nematodes to Diaprepes abbreviatus (Coleoptera: Curculionidae) in the laboratory. J Econ Entomol 93:1090–1095 Weathersbee AA, III Lapointe SL, Shatters RG, Hall DG (2006) Activity of Bacillus thuringiensis isolates producing novel endotoxins as measured by an innovative bioassay against neonate Diaprepes abbreviatus (Coleoptera: Curculionidae). Fla Entomol 89:441–448

Diaprepes Weevil, Diaprepes abbreviatus (Linnaeus) (Coleoptera: Curculionidae) Best know as a citrus pest, this weevil has a wide host range.  Citrus Pests and their Management  Diaprepes Root Weevil

Diapriidae A family of wasps (order Hymenoptera). See also. Wasps, Ants, Bees and Sawflies

Diaspididae A family of insects in the superfamily Coccoidae (order Hemiptera). They sometimes are called armored scales. See also,  Bugs

Diatomaceous Earth

Diastatidae A family of flies (order Diptera). They commonly are known as diastatid flies.  Flies

Diastatid Flies Members of the family Diastatidae (order Diptera). See also, Flies

Diatomaceous Earth John L. Capinera University of Florida, Gainesville, FL, USA Diatoms are microscopic algae that live in both fresh and saltwater environments. They become impregnated with silicon from their environment as they grow, leaving a “skeleton” consisting of sili iatoms con dioxide (SiO2) when they die. These d are small. Many elongate forms are only 10–15 microns in length and 5 microns in diameter; others are spherical. They usually are free-floating, and a major component of oceanic plankton. They can be extremely numerous, and comprise the most important primary producers for small animal life in oceans. It is estimated that 25% of all organic carbon fixation (conversion of carbon dioxide and water into sugars by photosynthesis) on earth occurs in oceans due to diatoms. They also are a major source of oxygen. Most are not consumed, of course, and when the algae perish, their bodies accumulate, leaving silica deposits of up to 300 m thick in some areas. These compressed silicaceous deposits, consisting of 85–95% silicon dioxide, are mined for various industrial purposes such as abrasives for polishing, brightening agents in paint, and as filtering or insulating agents.

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Why is Diatomaceous Earth Insecticidal? Diatomaceous earth (also called diatomite), dust, and other small particulate matter have been used for thousands of years to protect stored grain from insects. Diatomaceous earth and dust kill insects by absorbing the waxy fats and oils from the epicuticle of insects. If sufficient waxy material has been absorbed, the insect cannot maintain proper water balance, and perishes due to dehydration. To a lesser degree, diatomaceous earth affects insects through abrasion, though this attribute is very compatible with the effects of oil sorption. Lastly, some repellency effects have been documented, though this is the least important attribute.

Environmental Interactions Diatomaceous earth and dust are more insecticidal in arid environments. Moist grain (greater than about 15%) or humid storage conditions (> about 70%) can negate much of the benefit due to wax loss by insects. High temperatures enhance effectiveness of diatomaceous earth by increasing the rate of water loss. Insects also differ in their innate susceptibility; diatomaceous earth particles (Fig. 47) are more likely to adhere to hairy or rough-bodied species. Insects with these characteristics, and smaller species (with a large surfaceto-volume ratio), or species with a thin epicuticle or thin wax coating, are more susceptible to death from diatomaceous earth. Insects that imbibe food in a liquid form (e.g., sucking insects or mites) are less likely to suffer the effects of diatomaceous earth than those that metabolize water from their food. Efficacy of diatomaceous earth interacts with high temperature (e.g., 50–60°C), but some insect species exposed to a combination of diatomaceous earth and high temperatures perish more rapidly than those exposed to diatomaceous earth and lower temperatures, whereas in other species exactly the opposite response is observed.

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magnesium, iron, phosphorus, sulfur, salt, moisture, volcanic ash, clay, chert, and limestone. Diatomaceous earth products usually contain at least 90% silicon dioxide, however. Diatomaceous earth may be heated to high temperatures (called calcined diatomaceous earth) or left unheated (uncalcined); only uncalcined material is used as an insecticide. Aqueous solutions of sodium silicate can be dried and formulated into very light powders that are more effective (require less material); this is called silica aerogel. Silica aerogel, with its low density, is difficult to apply because it tends to float in the air, so is not often used. Diatomaceous earth is not flammable, is odorless, and is insoluble. Its color varies. Most deposits consist principally of amorphous silica, but a small proportion of crystalline silica occurs, and at a higher proportion in marine deposits.

What is Affected by Diatomaceous Earth?

Diatomaceous Earth, Figure 47 Diatomaceous earth particles viewed with a scanning electron microscope; in the upper image, the bar at the lower right represents 30 microns; in the lower image, the bar represents 7.5 microns.

Variability Among Diatomaceous Earths The size and shape of diatomaceous earth varies according to the dominant species living in the ocean or lake, and so the wax-absorption properties vary as well. Diatomaceous earth often possesses oil absorption values of about two to three times its own mass. The properties that define oil holding capacities are not well known, but particles of 45 microns or greater seem to be inferior. In addition to silicon dioxide, diatomaceous earth deposits may contain any of several contaminants, including aluminum,

Diatomaceous earth has been shown to kill ants, bedbugs, silverfish, caterpillars, crickets, termites, fleas, earwigs, beetles, ticks, mites and many other arthropods. However, the usual target is stored grain insects. Cryptolestes spp. are the most susceptible, followed by Sitophilus, and then by Oryzaephilus, Rhyzopertha, and Tribolium spp. Efficacy seems to be related to physical properties of the dust, rather than its chemical composition. As noted previously, high moisture levels reduce its effectiveness. Some diatomaceous earth formulations contain a low percentage of some other insecticide, commonly pyrethrum and piperonyl butoxide. Diatomaceous earth is usually applied as a dust, but sometimes as a water-based slurry. In addition to functioning as a grain protectant, diatomaceous earth is sometimes used to protect fabric and wood structures.

Safety Diatomaceous earth is considered to lack acute or chronic health effects when consumed by mammals.

Dictyoptera

Sometimes diatomaceous earth is fed to livestock to control worms and other internal parasites. Thus, residues on food are not considered hazardous to humans. The known deleterious effects of diatomaceous earth derive from chronic inhalation of dust, as might occur among miners and processors. Amorphous silica is classified as not carcinogenic, but crystalline silica can cause lung problems. Applicators should be provided with protection of eyes, lungs, and skin. Slurry formulations also reduce the risk of inhalation.

References Fields P, Korunic Z (2000) The effect of grain moisture content and temperature on the efficacy of diatomaceous earths from different geographical locations against stored-product beetles. J Stored Prod Res 36:1–13 Golub P (1997) Current status and future perspectives for inert dusts for control of stored product insects. J Stored Prod Res 33:69–79 Korunic Z (1998) Diatomaceous earths, a group of natural insecticides. J Stored Prod Res 34:87–97 Quarles W, Winn PS (2006) Diatomaceous earth alternative to stored product fumigants. IPM Practitioner 28(1/2):1–10

Dichotomous Keys A system of using a series of statements about specimen-related characters to identify an unknown. The user is presented a series of two choices, and asked to choose the correct one (best fit), which leads to other paired choices, and eventually leads to the correct identification.  Identification of Insects

Dicondylic Articulation or Joint A joint with two points of articulation between the adjacent segments. Having two condyles.  Condyle  Legs

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Dicot A plant with seedlings having two cotyledons. Dicots (dicotyledenous plants) are broadleaf plants.

Dicteriadidae A family of damselflies (order Odonata).  Dragonflies and Damselflies

Dictyopharidae A family of insects in the superfamily Fulgoroidae (order Hemiptera). They sometimes are called planthoppers.  Bugs

Dictyoptera The orthopteroid insects (crickets, katydids, grasshoppers, grylloblatids, stick insects, cockroaches, mantids, termites, and earwigs) have been divided into numerous groups, and one of these is called Dictyoptera. Dictyoptera is usually considered to be an order comprised of the mantids, cockroaches, and sometimes the termites. They seem to share a common origin, and have filiform antennae, are mandibulate, often are winged and have thickened forewings, possess concealed genitalia, and possess pronounced cerci. In one scenario, the Blattodea or Blattaria (cockroaches), Mantodea (mantids), and Isoptera (termites) are considered to be suborders. Some consider mantids and termites to be families of cockroaches, however. In another scenario, Dictyoptera is considered to be a superorder, with these same groups as orders rather than suborders. Though acknowledging the relatedness of these taxa, we treat the roaches, mantids, and termites as orders, and ignore the term Dictyoptera.

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Differential Grasshopper, Melanoplus differentialis (Thomas) (Orthoptera: Acrididae)

Differential Grasshopper, Melanoplus differentialis (Thomas) (Orthoptera: Acrididae) John L. Capinera University of Florida, Gainesville, FL, USA In North America, this grasshopper occurs widely in the central and western regions of the United States, and in northern Mexico; in Canada it occurs in southern Saskatchewan and British Columbia. Within the United States it is absent from the Atlantic and Gulf Coast region, except that it occurs in Pennsylvania, New Jersey, and Maryland. It is infrequent in the Pacific Northwest area. Also, within the large geographic area generally inhabited by differential grasshopper, it is rare in arid environments.

Life History Melanoplus differentialis has a single generation annually, with the egg stage overwintering. This is a late-season species, with eggs hatching about 3 weeks after those of twostriped grasshopper, Melanoplus bivittatus (Say), and 2 weeks after Melanoplus sanguinipes (Fabricius). In Colorado, eggs hatch in June, usually within a 2-week period. Nymphs complete their development in July- August; adults are present from August-October. The eggs are creamy white, yellowish, or light brown in color. They are elongate-cylindrical in shape, tapering to a blunt point at each end. The eggs are about 4–5 mm long and 0.85 mm in diameter. Eggs are clustered within an elongate, cylindrical pod consisting of 40–200 eggs arranged in four columns and held together by frothy material. The eggs are deposited in the soil, and the upper portion of the pod is plugged with additional froth. Eggs are normally deposited among the roots of grasses and weeds, especially along edges of fields, and in moist soil. Embryonic development occurs in the autumn after eggs are deposited, but the embryo enters diapause at about the point of 50%

development, and must endure a period of cold before commencing growth. The nymphs normally develop during the warmest period of the summer, and complete their development in about 30 days, though development times are extended if weather is cool. There are six instars, and the nymphs are not distinctive in appearance. First instars are greenish, yellowish or brownish with an indication of a black stripe on the outer face of the hind femora. Instars two through six are similar but possess a curved dark stripe extending from the back of the eye across the pronotum, and bordered below by a narrower white stripe. The black stripes on the femora are pronounced. The hind tibiae are light green or gray. The nymphs increase in body length from 5.3–6 mm in the first instar, to 5.2–6.8, 9.4–12.6, 12–14, 18–21.5, and 22–32 mm in instars 2–6, respectively. The number of antennal segments is 12, 14–17, 19–20, 21–22, 25–26, and 26 in instars 1–6, respectively. The adults are fairly large grasshoppers, the males measuring 28–34 mm in length, the females 32–44 mm. They display more color variability than most grasshoppers. They may be principally brownish green, or yellow, or almost entirely black, though the yellow form is most abundant. The most distinctive feature of these grasshoppers is the row of black marks, arranged in herring-bone fashion (Fig. 48) on the outer face of the hind femora. These markings are not so evident in the infrequent black form, which instead bears four white blotches on its otherwise black hind femora.

Differential Grasshopper, Melanoplus differentialis (Thomas) (Orthoptera: Acrididae), Figure 48 Adult of differential grasshopper, Melanoplus differentialis (Thomas).


The forewings in all except the black form are uniform grayish or brownish; the hind wings in all forms are colorless. The males bear large, bootshaped cerci. Like many other grasshoppers, differential grasshopper tends to roost on elevated locations at night. This allows them to bask in the morning sun, and to assume activity early in the day. Bushes and other tall vegetation are favorite perches. The host plants preferred by differential grasshopper are tall broadleaf plants such as those typically associated with fence rows, irrigation ditches, and fallow fields. It prefers plants in the family Compositae such as ragweed, Ambrosia spp.; sowthistle, Sonchus asper; sunflower, Helianthus annuus; and prickly lettuce, Lactuca scariola; though it will feed on other broadleaf plants such as kochia, Kochia scoparia; and smartweed, Poly gonum sp.; and on such grasses as bermudagrass, Cynodon dactylon; slender oat, Avena barbata; barley, Hordeum sp.; and Johnsongrass, Sorghum halepense. In North Dakota alfalfa fields, differential grasshopper reportedly ate kochia, Kochia scoparia; quackgrass, Agropyron repens; squirreltail grass, Hordeum jubatum; bristly foxtail, Setaria spp.; and field bindweed, Convolvulus repens, in addition to alfalfa. On prairie, they ate mostly stickseed, Lappula echinata; wavyleaf thistle, Cirsium undulatum; quackgrass, Agropyron repens; and pepperweed, Lepidium densiflorum. Crops sometimes injured include alfalfa, clover, corn, cotton, soybean, sugarbeet, timothy, and small grains such as barley and wheat. However, during periods of great abundance all crops are at risk because under such conditions virtually all green vegetation may be consumed. Weather affects the distribution of differential grasshopper, but in a manner somewhat different from some other grasshopper species. Differential grasshopper is associated with dense vegetation, so it follows that it would thrive in areas with adequate moisture to support lush growth of plants. It is a common, and damaging, species on the eastern edge of the Great Plains, where rainfall is plentiful, and relatively infrequent along the drier

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western edge of this region. Sometimes, during periods of higher than normal precipitation, its abundance expands into areas of the Great Plains normally dominated by species better adapted to dry conditions, such as migratory grasshopper, Melanoplus sanguinipes (Fabricius). When weather returns to normal, however, migratory grasshopper resumes its status as the dominant species. High levels of precipitation are not entirely advantageous for differential grasshopper. Precipitation during the warm months leads to outbreak of disease in differential grasshopper populations. This is a short-term response, and disease outbreaks occur only when grasshoppers are abundant. Differential grasshopper seems to be more susceptible to disease than some other species, including migratory grasshopper. Precipitation accompanied by cool weather during the hatching period is detrimental to differential grasshopper, as is the case for all grasshoppers, largely because it disrupts feeding during the critical early life of the grasshopper. The late onset of winter can favor grasshopper population increase because it allows adults additional time to produce eggs.

Damage This species seemingly has benefited from agricultural practices more than most grasshoppers, with grasshopper survival increased by the abundance of weeds associated with crops, and the irrigation practices of western farms. It also readily exploits disturbed sites in cities and towns. Unlike some of the arid environment-loving species, its numbers and damage may increase following long-term increases in precipitation. The damage caused by differential grasshopper principally takes the form of leaf removal. Plants may be completely defoliated, or left ragged. Because this grasshopper tends to roost in elevated locations at night, where they may nibble while resting, trees and shrubs outside the normal dietary range are sometimes severely injured.

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Management Liquid formulations of insecticides are commonly applied to foliage to protect against damage. Because grasshoppers rarely develop in crops, but instead invade from weedy areas, it is often the edges of crop fields that are most injured. Therefore, application of insecticide to the borders of crop fields is often adequate to protect an entire field. It is even better to apply insecticides to the developing grasshopper populations in weedy areas before they move to crops. This not only minimizes damage to crop plants, but often results in younger grasshoppers being targeted for elimination. Younger grasshoppers are more susceptible to insecticides, with large nymphs and adults sometimes difficult to kill. Application of insecticide-treated bait is an effective alternative to foliar treatments for Melanoplus spp. because these grasshoppers spend considerable time on the soil where they come into contact with baits. Bait formulations are bulky and more difficult to apply than liquid products, so they are less often used, but have the advantage of limiting exposure of crops to insecticide residue and of minimizing mortality of beneficial insects such as predators and parasitoids due to insecticide exposure. Also, the total amount of insecticide active ingredient necessary to obtain control is usually considerably less when applied by bait because the grasshoppers actively seek out and ingest the toxin. Finally, for relatively expensive products that must be ingested to be effective, such as microbial insecticides, baits are the most effective delivery system. The attractant used most commonly for grasshopper bait is flaky wheat bran, though other products such as rolled oats are sometimes suggested. No additives, other than insecticide (usually 5% active ingredient), are necessary because the wheat bran alone is quite attractive to Melanoplus grasshoppers. Other additives such as sawdust, water, vegetable or mineral oil, molasses, amyl acetate, salt, or sugar have been suggested, but provide little or no additional benefit over dry bran. The bait should be broadcast widely to maximize the likelihood of grasshopper contact, and

should be applied while grasshoppers are in the late instars because adults ingest less bait. Elimination of weeds within, and adjacent to, crops is the most important cultural practice, and can have material benefit in preventing damage to crop borders. However, during periods of weather when grasshoppers become numerous they may move long distances and invade crops. Tillage is an effective practice for destruction of eggs. Deep tillage and burial are required, shallow tillage having little effect. All the crop-feeding Melanoplus species deposit some eggs in crop fields, especially during periods of abundance, but it is fence row, irrigation ditch, field edge, and roadside areas that tend to be the favorite oviposition sites, so tillage is not entirely satisfactory unless other steps are taken to eliminate grasshopper egg pods from these areas that cannot be tilled. Though providing suppressive effects, deep tillage is not consistent with the soil and water management practices in many areas, so may not be a good option. Row covers, netting, and similar physical barriers can provide protection against grasshoppers. This approach obviously is limited to small plantings, and can interfere with pollination. Also, grasshoppers are capable of chewing through all except metal screening, so this approach does not guarantee complete protection. The natural enemies of differential grass hopper don’t seem to offer much promise for effective suppression. The microsporidian pathogen Nosema locustae is well studied as a microbial control agent of Melanoplus spp. and is available commercially. It is fairly stable, and easily disseminated to grasshoppers on bait. However, its usefulness is severely limited by the long period of time that is required to induce mortality and reduction in feeding and fecundity. Also, the level of mortality induced by consumption of Nosema is quite low, often imperceptible. It is best used over very large areas, not just on individual farms, and should be applied at least 1 year in advance of the development of potentially damaging populations. Fungi have also been investigated for grasshopper suppression. A grasshopper strain of Beauveria

Dioptidae

bassiana has been effective in some trials, and Metarhizium anisopliae var. acridum has worked well for grasshopper and locust suppression in Africa and Australia, so it may prove useful for Melanoplus spp. Behavioral thermoregulation by grasshoppers, wherein they bask in the sun and raise their body temperatures, is potentially a limiting factor for use of fungi. Basking grasshoppers easily attain temperatures in excess of 35°C; such high temperatures decrease or even prevent disease development in infected grasshoppers. Inconsistent quality control in production of fungi also limits use of these organisms for grasshopper control.  Grasshopper Pests in North America  Grasshoppers and Locusts as Agricultural Pests  Grasshoppers, Katydids and Crickets (Orthoptera)

References Capinera JL, Scott RD, Walker TJ (2004) Field guide to the grasshoppers, katydids, and crickets of the United States. Cornell University Press, Ithaca, New York, 249 pp Parker JR (1939) Grasshoppers and their control. USDA Farmers’ Bulletin 1828, 37 pp Parker JR, Shotwell RL (1932) Devastation of a large area by the differential and the two-striped grasshoppers. J Econ Entomol 25:174–187 Pfadt RE (2002) Field guide to common western grasshoppers. Wyoming Agricultural Experiment Station Bulletin 912, 288 pp Shotwell RL (1941) Life histories and habits of some grasshoppers of economic importance on the Great Plains. USDA Technical Bulletin 774, 48 pp

Digger Bees Members of the family Anthrophoridae (order Hymenoptera, superfamily Apoidae).  Bees  Wasps, Ants, Bees and Sawflies

Digitate Pertaining to structures with finger-like processes.

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Dilaridae A family of insects in the order Neuroptera. They commonly are known as pleasing lacewings.  Lacewings, Antlions and Mantidflies

Dimboa An acronym for 2,4-dihydroxy-7-methoxy-1,4,benzoxazin-3-one, a naturally occurring compound in corn (maize) that provides some resistance against caterpillars.

Dimorphic Having two distinct forms. Among insects, winged and wingless forms are a common example of dimorphism.

Dinidoridae A family of bugs (order Hemiptera, suborder Pentamorpha).  Bugs

Diopsidae A family of flies (order Diptera). They commonly are known as stalk-eyed flies.  Flies

Dioptidae A family of moths (order Lepidoptera). They commonly are known as American false tiger moths and oakworms.  American False Tiger Moths  Butterflies and Moths

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Diphyllostomatid Beetles

Diphyllostomatid Beetles Members of the family Diphyllostomatidae (order Coleoptera).  Beetles

Diphyllostomatidae A family of beetles (order Coleoptera). They commonly are known as diphyllostomatid beetles.  Beetles

Diploid Having two copies of each chromosome.

Diplurans (Diplura) This is an order of hexapods in the class Entognatha. These hexapods are sometimes considered to be insects (class Insecta). This order is also known as Entotrophi.

Classification About 660 species are known from throughout the world, though this groups is not well known. The Campodeidae is well represented in the Holarctic region, with the other families more common in the subtropics and tropics. The taxonomy of Diplura is confused, but six families in two suborders are sometimes recognized: Class: Entognatha Order: Diplura Suborder: Rhabdura Superfamily: Projapygoidea Family: Anajapygidae Family: Projapygidae Superfamily: Campodeoidea Family: Procampodeidae Family: Campodeidae

Suborder: Dicellurata Superfamily: Japygoidae Family: Japygidae Family: Parajapygidae

Characteristics Diplurans resemble symphylans (class Symphyla), or perhaps silverfish (order Thysanura), bristletails (order Archeognatha), or proturans (order Protura). However, they have only three pairs of legs, so they are easily distinguished from the (Fig. 49) many-legged Symphyla. Also, the presence of only two cerci rather than three caudal filaments distinguishes diplurans from silverfish and bristletails. They are distinguished from proturans (order Protura) by the presence of antennae. Diplurans are usually less than 10 mm in length, though their size range is 2–50 mm. They are elongate, soft-bodied, and brownish. The integument is thin, and few scales are found on these animals. The body regions, including the three thoracic segments, are distinct. The head is distinct, and the antennae long, manysegmented, and slender. Compound eyes and ocelli are absent. The biting and chewing mouthparts are entognathous (recessed in the head). The mandibles are elongate. They are wingless, and the three pairs of legs are similar in appearance and moderately short. The tarsi are onesegmented. The abdomen consists of ten well-developed segments and a small 11th segment. The tip of the abdomen bears a pair of cerci. The cerci vary greatly among the taxa, from long, many-segmented antenna-like appendages to stout, strongly sclerotized forceps used for prey c apture. Most of the abdominal segments also bear small appendages. Trachea are present, but Malpighian tubules are vestigial or absent. The immatures greatly resemble the adult stage, differing principally in the number of antennal segments. They are considered to have incomplete metamorphosis.

Dipteromimidae

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number of molts is considerable; up to 20 molts per year are known.

References Antenna Labrum Mandible Maxilla Labium

Coxa Trochanter Femur Tibia Tarsus Abdominal appendage Eversible sac

Arnett RH Jr (2000) American insects, 2nd edn. CRC Press Boca Raton, FL, 1003 pp Allen RT (1994) An annotated checklist and distribution records of the subfamily Campodeiinae in North America (Insecta: Diplura: Rhabdirura: Campodeidae) Trans Am Entomol Soc 120:181–208 Paclt J (1956) Biologie der primär flügenllosen Insekten, Fischer, Jena, 258 pp Paclt J (1957) Diplura, Genera Insectorum, Fascicle 212, 123 pp Wygodzinsky P (1987) Class and order Diplura. In: Stehr FW (ed) Immature insects, vol 1. Kendall/Hunt Publishing, Dubuque, IA, pp 65–67

Pretarsus

Diprionidae

Cercus

Diplurans (Diplura), Figure 49 A diagram of a dipluran showing a dorsal view (left) and a ventral view (right). Note that the cerci are abbreviated.

Biology These small animals are found among fallen leaves and in decaying vegetation, under logs and stones, and in soil and caves. They vary in dietary habits; some feed on vegetation whereas others eat other small soil-inhabiting arthropods. Sperm transfer is indirect, with males producing stalked spermatophores which the female takes up without courtship. Eggs are deposited in the soil. They can be long-lived, with the life span requiring 2–3 years in some species. The

A family of sawflies (order Hymenoptera, suborder Symphyta). They commonly are known as conifer sawflies.  Wasps, Ants, Bees and Sawflies  Sawflies (Symphyta)

Dipsocoridae A family of bugs (order Hemiptera).  Bugs

Diptera An order of insects. They commonly are known as flies.  Flies

Dipteromimidae A family of mayflies (order Ephemeroptera).  Mayflies

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Direct Flight Muscles

Direct Flight Muscles Muscles that connect directly to the wing bases and power the wings directly.

Directive Coloration Colors or marks on potential prey organisms that divert the predator from the more vital regions of an organism. Thus, for example, a bird might be induced to grasp a butterfly in the wing region rather than the abdomen.

Direct Pests Pests that inflict injury directly on the portion of the commodity that is harvested for sale.

Dirofilariasis Jai K. Nayar University of Florida, Vero Beach, FL, USA Dirofilariasis is a complex of veterinary diseases caused by nematodes (round worms) belonging to the phylum Nematoda, order Filarioidea, family Onchocercidae and genus Dirofilaria. The genus Dirofilaria is divided into two subgenera: Dirofilaria and Nochtiella. The subgenus Dirofilaria contains Dirofilaria immitis that causes canine cardiovascular disease (dog or canine heartworm disease) in dogs and dog like carnivores, cats, domestic ferrets, and rarely in humans causing pulmonary dirofilariasis. The subgenus Nichtiella contains Dirofilaria repens that occurs in dogs and cats, D. tenuis in raccoons, D. ursi in bears, and D. striata in bobcats and panthers. The first three species of Dirofilaria in the subgenus Nochtiella cause subcutaneous nodules in their vertebrate hosts and in humans. All parasites belonging to this family complete their development in two hosts. The vertebrate is the final host

and the mosquito is the intermediate host/vector, except in D. ursi where the hosts/vectors are blackflies. The distribution of Dirofilaria immitis is worldwide, thus canine or dog heartworm disease occurs all over the world, especially in tropical and temperate zones. In the United States, it was once limited to the south and southeast regions. However, the disease has spread and is now found in most regions of the United States and Canada, particularly where mosquitoes are prevalent. The distribution is influenced by a reservoir population of animals (usually dogs) that have adult worms in their hearts and microfilariae circulating in the blood, and a mosquito vector in which the early larval stages can develop to the infective larval stage. The distribution of parasites belonging to subgenus Nochtiella is more restricted, for example, D. repens occurs in Europe, Asia, Africa, and Mediterranean countries, D. tenus and D. striata occur in southeast U.S.A. and D. ursi occurs at the U.S.-Canadian border. Dog heartworm disease (dirofilariasis) is a serious and potentially fatal disease in dogs and cats. In dogs and other carnivores, the adult worms normally reside in the heart and large adjacent vessels. Adult worms are long, slender and white. Males are 12–16 cm long and have a corkscrew tail, and females are 25–30 cm long. Adult worms cause disease by clogging the heart and major blood vessels leading from the heart. They interfere with the valve action in the heart. By clogging the main blood vessels, the parasite reduces the blood supply to other organs of the body, particularly the lungs, liver, and kidneys, leading to malfunction of these organs. Most dogs infected with heartworms do not show any signs of disease for as long as 2 years. Unfortunately, by the time signs are seen, the disease is well advanced. The signs of heartworm disease depend on the number of adult worms present, the location of the worms, the length of time the worms have been present, and the degree of damage to the heart, lungs, liver, and kidneys from the adult worms and the microfilariae. The most

Dirofilariasis

obvious signs are: a soft, dry, chronic cough, shortness of breath, weakness, nervousness, listlessness, and loss of stamina. All of these signs are most noticeable following exercise, when some dogs may even faint and die. Once infected, a dog is infected for life. The sexually mature nematodes mate in the right ventricle of the heart and discharge unsheathed microfilariae into the bloodstream. Microfilariae are 290–330 μm long and 6–7 μm wide, with tapered anterior end and straight posterior end, without cephalic hooks. They cannot develop further in the dog, but can survive in the blood stream for up to 2–3 years. They circulate throughout the body but remain primarily in the small blood vessels and capillary beds. Because they are as wide as the small capillaries, they may block blood flow. The body tissues and cells being supplied by these capillaries are thus deprived of the nutrients and oxygen normally supplied by the blood. The lungs and liver are primarily affected and destruction of lung tissue that leads to coughing. Cirrhosis of the liver causes jaundice, anemia, and general weakness because this organ is essential in maintaining a healthy animal. The kidneys may also be affected and allow poisons to accumulate in the body. These circulating microfilariae must be ingested by a mosquito (the vector) during bloodfeeding on the infected dog before they can develop further. Soon after the blood meal, the microfilariae move from the mosquito’s midgut to the Malpighian tubules where they become intracellular. At a temperature of about 27°C the microfilariae become immobile, shorten and thicken, and develop into the so-called “sausage form” larvae in about 4–5 days, with the first stage larvae continuing until a molt at about 8 days. During the second larval stage, the internal organs of the worm are formed. The second molt occurs at 11–12 days, resulting in the third stage (L3) (Fig. 50) of infective larvae that resemble miniature adults. During the next 2–3 days, they increase in length, break out of the Malpighian tubules, migrate to the hemocoel then move into

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the head capsule and accumulate in the labium (a mouthpart of the proboscis continuous with the hemocoel). The development in the mosquito can be as short as 10 days at 30°C or as long as 28 days at 18°C. Thus, in 2–3 weeks, microfilariae transform into infective larvae that are about 1300 μm long. As the infected mosquito feeds, the labium is bent back and L3 escape in a pool of hemolymph onto the skin. When the stylets are withdrawn, the L3 enter through the wound. Up to 10 to 12 L3 can be transmitted by a single mosquito. Further development of the infective larvae only takes place in the dog and related species after mosquitoes feed on the vertebrate host. Spread of the disease therefore coincides with the mosquito season. The number of dogs infected and the length of the mosquito season are directly correlated with the incidence of heartworm disease in any given area. In the dog and other carnivores, infective larvae (L3) after penetrating the skin move in the subcutaneous tissue and molt to L4 in about 10 days post infection. The L4 migrate to muscle bundles (fascial planes, muscle sheaths) and start to grow during the next 60 days and then molt to L5. The L5 migrate through venule walls by 70 days post-infection and are carried through the right ventricle of heart to pulmonary arterioles, most of them arriving there by 3–4 months post-infection. L5 mature to adults after migrating to the right ventricle and pulmonary trunk. If both sexes are present, they mate and the female can produce microfilariae after approximately 6 months postinfection, thereby completing the life cycle. These females can continue producing microfilariae for 5–7 years, which can survive for about 2 years in the blood circulation. It takes a number of years before dogs show outward signs of infection. Consequently, the disease is diagnosed mostly in 4–8 year old dogs. The disease is seldom diagnosed in a dog under 1 year of age because the larvae take up to 7 months to mature following establishment of infection in a dog. In endemic areas, the average worm burden in the dog is about 15. High worm burdens

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Dirofilariasis Dog heartworm life cycle

L5 Move to heart L3 and L4 develop in musculature Enter musculature

Heart of dog with adult worms

Aorta of dog with adult worms

Final host Penetrate skin of dog through bite wound

Mf. in blood circulation

Dead end host

Mf.ingested by mosquito

Man L4 stage move to lungs and form “coin lesion”

Mf.move in the midgut Infective larvae (L3) coming from proboscis

Mf. Malpighian tubules Intermediate host Developmental stages in mosquito

L3 L2

Midgut

Mf. L3

L1 L3 Mf. Lb

Lm Hphy

Dirofilariasis, Figure 50 Life cycle of dog heartworm (Dirofilaria immitis). Stages of filarial worm in dog: L3 = third stage larvae and L4 = fourth stage larvae in musculature and adult worms in heart and aorta of dog. Stages of filarial larvae in the mosquito: Mf = microfilariae, L1 = first stage larvae (sausage stage), L2 = second stage larvae, and L3 = third stage larvae in Malpighian tubules and microphotographs. Lm = labium, Lb = labrum, and Hphy = hypopharynx.

(more than 75) can be demonstrated in acute post-caval syndromes and chronic ascites from tricuspid valve dysfunction. Because of the in creased resistance of most animals from repeated

exposure to L3 over time, high worm burdens are most likely to occur in dogs which have not been exposed to any mosquitoes with L3 previously and are then bitten by many mosquitoes

Dirofilariasis

over a 3 month period. In that case, a dog may have as many as 300 worms. Feline dirofilariasis is a complex pathological disease, which is principally subclinical. It produces among others, pulmonary vascular disorders with complications caused by clinically significant heart, lung, liver, kidney and thoracic duct diseases as well as CNS signs and symptoms. Generally, the common signs in acute and severe cases include fainting, dyspnea, seizure, intermittent vomiting, diarrhea, blindness, rapid heart beat or syncope. The signs of the chronic stage include stress intolerance, dyspnea, lethargy, loss of appetite, quilothorax, rapid heart beat, abdominal distention (in the case of congestive right heart failure), cyanosis, abnormal liver sounds, systolic murmur (extremely rare), occasional nose bleeding, urinary retention and ascitis. In endemic areas, the average worm burden in the cat is 1–3 worms. In cats, adult worms live for approximately 2 years and sometimes produce very few microfilariae, if at all. Dirofilaria immitis microfilariae can develop to the infective stage larvae in more than 100 species of mosquitoes, out of more than 3,000 species present worldwide, and these species are considered as potential vectors. In order to be a heartworm vector, besides being resistant to infection but yet susceptible enough to allow larval development, a mosquito species must feed on infected dogs, be well adapted to the region and be abundant and preferably multivoltine. However, about 25 mosquito species mostly belonging to Aedes and Culex have been collected worldwide with developing larvae in their Malpighian tubules, hemocoel and mouthparts and they have been identified as natural vectors. These are: in North America – Aedes cana densis, Ae. cantators, Ae. excrucians, Ae. sierrensis, Ae. sticticus, Ae. stimulans, Ae. sollicitans, Ae. taeniorhynchus, Ae. trivittatus, Ae. vexans, Culex nigripalpus, Cx. quinquefasciatus, Cx. salinarius, Anopheles puntipennis, and Psorophora ferox; in Australia – Ae. annulipes, Ae. notoscriptus, Ae. vigilax, Cx. annulirostris, and Cx. quinquefasciatus; in Japan – Ae. albopictus, Ae. togoi, and

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Cx. quinquefasciatus; in South Pacific – Ae. pseudos cutellaris, Cx. annulirostris, and Cx. quinquefasciatus. Dirofilaria immitis is also an occasional parasite of humans, causing pulmonary dirofilariasis. Because infective larvae develop to a limited extent in humans, the latter are referred to as the dead end hosts. The filarial nematodes enter the subcutaneous tissue after a bite from an infected mosquito, develop to the L4 stage, and travel to the right ventricle where they die and embolize the pulmonary vasculature, causing small pulmonary infarctions that subsequently appear as solitary nodules. Although these nodules are usually identified incidentally by chest radiography in asymptomatic patients, the lesions are generally presumed to be neoplastic. The nodules of dirofilariasis are usually round called “coin lesions” in the lungs but sometimes they are dumbbellshaped. Microscopically, the nodules are granulomas composed of central coagulation necrosis and peripheral fibrosis with round cell infiltration, histiocytes, and multinucleated giant cells. Because these nodules are difficult to be differentiated from primary or metastatic lung carcinomas and the inflammation exists around the nodule, the nodule should be removed surgically. During the last 40 years, approximately 150 cases of human pulmonary dirofilariasis have been reported worldwide. Three other parasites that cause dirofilariasis, belong to subgenus Nochtiella, produce subcutaneous nodules which may be migratory both in their vertebrate hosts and in humans, are D. repens, D. tenuis and D. ursi. Dirofilaria repens, a parasite of the subcutaneous tissues of dogs and cats, is found in Europe, Asia, and Africa, especially in Mediterranean countries, Russia and Japan. Human infections by D. repens are being reported with increasing frequency in all these countries. Both males and females of this parasite are about half the size of D. immitis, the females measuring 100–170 mm in length and 0.46–0.65 mm in width and males 50–70 mm in length and 0.37–0.45 mm in width with two to six preanal papillae to the right of the anus and

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four to five to the left. The microfilariae of D. repens occur in the subcutaenous lymph spaces and in the peripheral blood. The microfilariae range in length from 268–360 μm and overlap in size that reported for D. immitis. They can be distinguished from D. immitis microfilariae by the relative positions of somatic structures such as nerve ring, the excretory cell, the G1 cell, and the anal space along the length of the microfilariae. Development of D. repens in mosquitoes follows a similar pattern as that of D. immitis in mosquitoes. However, the mosquitoes that support development of the larval stages of these parasites belong to Aedes and Culex species found in Europe, Asia, and Africa. Dirofilaria tenuis is a parasite of the subcutaneous tissues of raccoons in the southeastern United States but humans are also infected. More than 20 human cases have been reported from Florida and most of them were from southern Florida. The microfilariae are 370 ± 9 µm long and ca. 7 μm wide and are comparable in size to D. striata microfilariae. Development of D. tenuis in mosquitoes follows a similar pattern as that of D. immitis. The natural vectors of D. tenuis in south Florida is Ae. taeniorhynchus, however, several other species of mosquitoes, such as An. quadrimaculatus, Ae. triseriatus, Psorophora columbiae and Ps. Ferox, are considered potential vectors. Dirofilaria species causing subcutaneous infections in vertebrates and humans are identified primarily on the basis of structure and arrangement of the ridges. Longitudinal ridges of adult D. repens are conspicuous and sharp, separated by a space three to four times the width of the ridge itself. Dirofilaria tenuis has a distinctive pattern of low, rounded ridges in a branching network with spaces appearing narrower than the ridges themselves. The cuticle of D. immitis is smooth with ridges occurring only on the ventral aspect of the caudal extremity of the male worm. Dirofilaria ursi is a parasite of the peritracheal and perirenal tissues of bears in North America and Japan and Russia, and rarely of dogs in these

areas. Human infections with D. ursi causing subcutaneous nodules have been reported in the states and provinces along the U.S.-Canadian border. The intermediate host of D. ursi is the blackfly, Simulium venustum and perhaps other simuliids in Canada. Development of D. ursi microfilariae in simuliids is similar to that observed for other Dirofilaria species in mosquitoes, i.e., all species of Dirofilaria complete their development in the Malphighian tubules of their vector. Dirofilaria striata is found in panthers and bobcats in Florida. The adults of this species occur in the intermuscular fascia or free in the peritoneal cavity. The females of D. striata are 25–28 cm long and males are 8–9 cm wide. Microfilariae of D. striata are significantly longer and more slender than those of D. immitis (348 μm × 4–5 μm vs. 299 μm × 5–6.5 μm) and exhibit within the cephalic space two prominent nuclei separated from the main body of the nuclear column. Dirofilaria striata has been reported as an accidental parasite of dogs in Florida and adults have been recovered from deep intramuscular fascia of dogs. The potential mosquito vectors of D. striata in south Florida are Ae. taeniorhynchus, An. quadrimaculatus, Cx. nigripalpus and Cx. quinquefasciatus. Since canine cardiovascular dirofilariasis is primarily a disease of dogs and cats that are household pets, several diagnostic and preventive measures are used by veterinarians. Canine dirofilariasis can not be controlled unless the mosquito populations are completely controlled. Several diagnostic tests to determine if cats and dogs are infected are as follows: (i) demonstration of the microfilariae of D. immitis in a blood sample by concentration techniques, (ii) the detection of circulating microfilarial antigen, (iii) thoracic radiographs can be a screening tool for dogs and cats with suggestive clinical signs of heartworm disease, and (iv) echocardiograms are diagnostic with the typical “double parallel” white lines are noted in the pulmonary arteries or right ventricles of dogs or cats. Routine therapy included: (i) Pre-therapy diagnostic to determine sub-clinical disease, especially of the liver and

Diseases of Grasshoppers and Locusts

kidney. (ii) Adulticidal therapy (Immiticide®, Caparsolate®, Filaramide®) to eliminate mature worms. (iii) A rest period of 4–6 weeks to allow the animal to recover from the lung injury associated with worm death. (iv) Microfilaricidal therapy (Heartgard®, Interceptor®) if required. (v) Post-Microfilaricidal check. (vi) Antigen test to determine success of adulticidal therapy. (vii) Preventative medications (Filaribits®, Heartgard®, Interceptor®). Information on all these aspects can be obtained from your practicing local veterinarians.

References Boreham PFL, Atwell RB (1988) Dirofilariasis. CRC Press, Boca Raton, FL, 249 pp Nayar JK, Knight JW (1999) Aedes albopictus (Diptera; Culicidae): an experimental and natural vector host of Dirofilaria immitis (Filarioidea: Onchocercidae) in Florida, USA. J Med Entomol 36:441–448 Shah MK (1999) Human pulmonary dirofilariasis: review of literature. South Med J 92:276–279 Tarello W (1999) Canine Dirofilariasis due to Dirofilaria (Nochtiella) repens. Review from literature and a clinical case. Rev Med Vet 150:691–702

Discal Cell A cell, usually enlarged, that is found near the center of the wing.

Discrete Generations A series of generations in which one generation is completed before the next commences. This is common place for insects with a single generation per year, separated by a period of diapause. With insects having more than one generation per year, however, it is common to have overlapping generations, wherein the early life stages of the succeeding generation overlap the final stages of the preceding generation.

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Disease A process that represents the response of the body to injury or insult. A pathogen is not a disease, but it may cause one.

Diseases of Grasshoppers and Locusts Mark S. Goettel Agriculture and Agri-Food Canada, Lethbridge, AB, Canada The importance of grasshoppers and locusts as pests, and the increased concerns over the deleterious environmental and health effects of using chemical insecticides to control their outbreaks, recently has drawn much attention to the possibility of exploiting their pathogens as microbial control agents. Disease often is responsible for suppression of grasshopper and locust outbreaks. Disease causing agents include bacteria, fungi, protozoa and viruses.

Bacteria Two species of bacteria, Serratia marcescens Bizio and Pseudomonas aeruginosa (Schroeter) Migula have been implicated in disease epizootics observed in field populations and laboratoryreared locusts and grasshoppers. These bacteria infect their host after being ingested and often spread rapidly in laboratory colonies. However, their role in the natural suppression of grasshopper and locust populations remains unclear. Bacterial pathogens of locusts and grasshoppers received considerable attention as potential microbial control agents in the early 1900s and in the 1950s. Several attempts were made to use these bacteria to manage grasshoppers and locusts, but these studies never proceeded beyond the stage of surveys and laboratory trials. Concerns over human and environmental safety at the time, as well as product stability, led to the termination of this work.

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The commercial success of certain serovars of Bacillus thuringiensis as microbial control agents of numerous insect pests has spawned several attempts to isolate related spore-forming bacteria pathogenic to locusts and grasshoppers. Although some toxins, such as the β-exotoxin of B. thuringiensis, have a broad activity against a large number of insects, including locusts and grasshoppers, strains producing more species-specific δ-endotoxins highly active against orthopterans have not been discovered to date. However, the continued discovery of new strains of B. thuringiensis with specific activity against a broader range of pests and the recent commercial development of a new species of Serratia (Serratia entomophila) for control of grass grubs provides incentive to continue the search for orthoperan-active bacteria. But at the moment, there is no evidence of naturally occurring bacterial species or strains that would warrant exploitation for locust or grasshopper control.

Fungi Unlike most other pathogens which must be ingested to cause disease, entomopathogenic fungi generally enter their host via the external cuticle. A handful of species are common in grasshoppers and locusts and these include Beauveria bassiana (Balsamo) Vuillemin, Entomophaga grylli (Fresenius) Batko species complex, Metarhizium anisopliae (Metschnikoff) Sorokin, Metarhizium anisopliae var acridum (syn = Metarhizium flavoviride) and Sorosporella spp.

Beauveria bassiana There are numerous records of B. bassiana infecting grasshoppers and locusts and it has been documented causing epizootics amongst locust populations in Africa. The fungus is ubiquitous and infects a wide variety of insects from most orders. Aerial conidia, the infective spore stage of the fungus, adhere to the cuticle of the host, g erminate,

penetrate through the external cuticle, rapidly proliferate within the host body via hyphal growth and production of yeast-like hyphal bodies or blastospores, killing the host within 4–10 days of infection. Soon after the host dies, and under appropriate moisture conditions, the fungus emerges through the body wall and quickly sporulates, producing numerous conidia on the host surface, often appearing like a white powder completely engulfing the host cadaver. The fungus has been commercially developed and registered as a microbial control agent against numerous pest insects throughout the world. Field trials with inundative applications of an American isolate against grasshoppers in North America and Africa produced mixed results. Several studies have demonstrated that infected grasshoppers and locusts are able to escape lethal infection by basking in the sun, thereby increasing their body temperature above the thermal threshold for growth of the fungus (see below).

Entomophaga grylli Complex Fungi in the Entomophaga grylli complex are obligate grasshopper pathogens responsible for numerous widespread epizootics worldwide, and are regarded as a key factor in regulating many grasshopper populations. This complex contains several pathotypes that vary in their ability to produce both conidia and resting spores within a single season. The fungus overwinters as resting spores in the soil. A portion of the resting spores germinate each spring, while others remain dormant for two or more seasons. Germinating resting spores produce specialized spores which are forcibly ejected from the soil into the lower canopy where grasshoppers encounter them. Once these spores contact a grasshopper host they germinate, penetrating the body wall, and the fungus then rapidly proliferates within the grasshopper body cavity as protoplastic bodies. Approximately 1 week after initial exposure, infected grasshoppers climb to the top of the plant canopy where they die grasping


firmly onto the plant substrate. For this reason, this disease is often referred to as the “summit disease.” Depending on the pathotype, at this point, either resting spores are exclusively produced and the insect eventually falls to the ground, the cadaver disintegrates and the resting spores are released into the soil, or alternatively, the cadaver produces either resting spores or aerial conidia, which are responsible for within-season epizootic development. Natural epizootics of the fungus often produce high levels of mortality, and have been credited for ending grasshopper outbreaks in many North American grasshopper species. There have been several attempts at inundative application of conidia in an effort to induce epizootics (inundative microbial control), however, none were able to achieve satisfactory results. The most important limiting factors were lack of adequate mass production and application techniques and the specific environmental requirements of the fungus for survival and infectivity. Attempts at inoculative introduction (classical biological control) also were not successful. Introductions of North American isolates into Australia and vice versa failed to establish, although the introductions into North America initially were followed by population declines of key pest species. These initial studies suggest that these pathogens have potential for use in biological control, however, further studies are required.

Metarhizium anisopliae var acridum There are records of M. anisopliae var acridum (formally referred to as Metarhizium flavoviride) from grasshoppers in Africa, Australia and Brazil, and natural epizootics have been documented in Africa. The mode of pathogenesis and infection cycle is essentially the same as described above for B. bassiana, except that cadavers are covered with a powdery covering that is dark olive green rather than white. The fungus has been the subject of much research in the last decade and several commercial products for grasshopper and locust control now

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are available in Africa and Australia. A multinationally funded project, LUBILOSA, spearheaded by CABI and the International Institute of Tropical Agriculture, resulted in the discovery and development of this fungus as a commercial microbial insecticide (Green MuscleTM). During this project, many improvements in the formulation, mass production and application of this fungus were made. These developments have resulted in a commercial formulation that can be stored up to 4 years that can be applied through Ultra Low Volume (ULV) application in an oil formulation, and that also offers the conidia some protection from the sun’s harmful rays.

Protozoa Protozoans that infect grasshoppers are mainly microsporidians, but certain Amoebida, Eugregarina, Neogregarina and Ciliophora also are known from grasshoppers. Among the Microsporidia, Heterovesicula cowani Lang et al., Johenrea locustae Lange et al., Nosema acridophagus Henry, N. cuneatum Henry, N. locustae Canning, N. montanae Wang et al., N. pyrgomorphae Toguebaye et al., and Perezia dicroplusae have been described. No doubt, many more await discovery and description. The most studied microsporidian of grasshoppers has been N. locustae, and it was the basis for the first microbial pesticide (NolobaitTM) developed against grasshoppers and locusts. Ingested spores germinate in the gut whereby they release a binucleate sporoplasm into a host cell through quickly extruded polar filaments. Sporoplasms subsequently spread to and replicate in the fat body, eventually depleting the host of its fat reserves. Spores are mass produced in vivo in grasshoppers. Because the spores need to be ingested to initiate disease, commercial formulations are formulated on a wheat bran bait carrier. Extensive field-testing has taken place in North America, Argentina, China and Africa. Although at times application of spores has resulted in considerable decline in grasshopper or locust populations with

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subsequent carry over in treated areas, in other trials such impacts were not observed. Application of a pathogen such as N. locustae can be expected to result in sublethal effects such as delayed development, lower reproduction and reduced feeding. Unfortunately, many assessments measured only short term impact of N. locustae rather than long term benefits. Several other microsporidians with greater virulence than N. locustae, such as N. cuneatum, may better fit the microbial insecticide paradigm. There is also great potential of using microsporidians in the classical sense (inoculative releases) which await exploration.

Viruses Entomopoxviruses are the only DNA viruses that have been found naturally infecting grasshoppers and locusts. Nearly 15 grasshopper and locust entomopoxviruses have been reported. The most extensively studied among these has been the Melanoplus sanguinipes EPV (MsEPV). Although the precise mode of infection of grasshopper viruses has not been studied in detail, pathogenesis probably is similar to that of other entomopoxviruses; ingested viral occlusion bodies break down in the alkaline medium of the gut, releasing the individual virions which then infect midgut cells, presumably replicate, and progeny virus is then released into the hemocoel, eventually infecting the fat body tissues. Virions replicate within the fat body cells and are packaged in proteinaceous crystalline matrices, the occlusion bodies. Effects of infection vary according to dosage received. In heavily infected grasshopper populations, death can occur in two distinct modes. An initial mortality takes place between 2 and 10 days post exposure, subsides and then mortality increases again during the second mode, 14 days after initial exposure. Occlusion bodies are produced only in grasshoppers dying during the second mode. Infected grasshoppers that escape the early mortality experience a profoundly longer development period, and few develop to the adult stage. During

this delayed development period, there is a concomitant reduction of feeding. Prevalence rates of the virus in field populations are extremely low and very little is known about its epizootiology. Field evaluations on the potential of using grasshopper entomopoxviruses as microbial insecticides were carried out in the United States. The virus was mass produced by injecting grasshoppers and incubating them in an insectary. Infected cadavers were crushed and formulated in a starch granule and then dispersed in the field. Maximum prevalence levels in treated fields reached 23%, however, it is speculated that due to grasshopper dispersal between experimental plots, this may be a rather conservative estimate. At this time, the in vivo production is cost prohibitive and feasibility of developing these viruses as grasshopper control products remain questionable.

Grasshopper Thermal Ecology Locusts and grasshoppers optimize their body temperature through behavioral responses, such as basking in the sun. Recent research has demonstrated that individuals infected with a pathogen will attempt to increase their temperature even further, a phenomenon termed “behavioral fever.” Even though behavioral fever has been demonstrated in ectotherms from various taxa in response to infection by a variety of pathogens, to date only Nosema and fungi have been found to elicit such behavioral fevers in grasshoppers and locusts. Behavioral fever can result in augmentation in body temperature to the vicinity of 40°C, which usually is well above the upper limits for growth of most pathogens. Furthermore, behavioral fever may enhance the insect immune response by stimulating the production of hemocytes. Consequently, speed of kill and overall mortality can be affected drastically, depending on the environmental conditions prevalent that may or may not allow optimal thermoregulation (e.g., sun, cloud, wind, rain). In microbial control of grasshoppers and locusts, it may be possible to overcome such constraints through application of pathogen

Distiproboscis

cocktails containing pathogens or pathotypes selected for a wide range of thermal possibilities according to the environment that is being treated (e.g., day length and day/night temperatures).

References Bidochka MJ, Khatchatourians GG (1991) Microbial and protozoan pathogens of grasshoppers and locusts as potential biocontrol agents. Biocontrol Sci Technol 1:243–259 Gardner SN, Thomas MB (2002) Costs and benefits of fighting infection in locusts. Evol Ecol Res 4:109–131 Goettel MS, Johnson DL (eds) (1997) Microbial control of grasshoppers and locusts. Memoirs of the Entomological Society of Canada, vol. 171. The Entmological Society of Canada, Ottawa, Canada, 400 pp Inglis GD, Goettel MS, Erlandson MA, Weaver DK (2000) Grasshoppers and locusts. In: Lacey LA, Kaya HK (eds) Field manual of techniques for the application and evaluation of entomopathogens. Kluwer Academic Press, Dordrecht, The Netherlands, pp 651–679 Kleespies RG, Huger AM, Stephan D (2000) Diagnosis and pathology of diseases from locusts and other orthopterans. Deutsche Gesellschaft fur Technische Zusammenarbeit (GTZ) GmbH, Eschborn, Germany, 43 pp Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas M (2001) Biological control of locusts and grasshoppers. Ann Rev Entomol 46:667–702 Lomer CJ, Prior C (eds) (1992) Biological control of locusts and grasshoppers. CAB International, Wallingford, UK, 394 pp Mason PG, Erlandson MA (1994) The potential of biological control for management of grasshoppers (Orthoptera: Acrididae) in Canada. Can Entomol 126:1459–1491 Streett DA, McGuire MR (1990) Pathogenic diseases of grasshoppers. In: Chapman RF, Joern A (eds), Biology of grasshoppers. Wiley, New York, NY, pp 483–516

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Dispersal Displacement to a new habitat. Dispersal usually is multidirectional and passive, taking advantage of wind currents. The spatial patterning of individuals in a population in their habitat. This pattern can be broadly described as uniform, random or, most commonly, aggregated.

Dispersion Dispersion or distribution is a spatial property that can be quantified by explicit spatial indices, or more typically by probability models (e.g., Poisson, Negative-binomial) or empirical models (e.g. Taylor’s power law). The measurement of dispersion is dependent on the sample unit size and population density. Dispersion is an important element in the development of a sampling plan.  Sampling Arthropods

Disruptive Coloration Color patterns on an animal that confer protection by obscuring the outline of the animal. Typically it consists of strongly contrasting colors. The classic example is the black and white stripes of zebra. In insects, it may be manifested in stripes or bands, especially on larvae, on in spotted or blotchy patterns.

Disjunct Populations The geographical distribution of a species (or other taxon) consists of widely separated populations.

Disk A soil cultivator made up of many circular blades that act to break up the soil into smaller aggregates.

Distal Pertaining to the part of an appendage furthest from the body.

Distiproboscis The distal third of the proboscis in muscoid flies; this is the labellum.

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Ditomyiidae

Ditomyiidae A family of flies (order Diptera).  Flies

Diuretic Hormones Neuropeptide hormones that promote fluid formation and rapid excretion by Malpighian tubules. In Rhodnius, the hormone is released from abdominal nerves associated with the mesothoracic ganglion, but this is not the case with all insects.

Diurnal Organisms in which the period of activity occurs during daylight hours.

Diverticulum An invagination or extension of the wall of the alimentary canal with the distal portion closed. Diverticula, when present, typically are associated with the anterior region of the alimentary canal. They are useful for food storage, and especially important when an insect takes infrequent but large meals.

Dixid Midges Members of the family Dixidae (order Diptera).  Flies

Dixidae A family of flies (order Diptera). They commonly are known as dixid midges.  Flies

DNA Deoxyribonucleic acid, the genetic molecule.

DNA Probe Also called a gene probe or genetic probe. Short, specific (complementary to the desired DNA sequence) artificially produced segments of labeled DNA are used to combine with and detect the presence of a specific gene or DNA sequence within the chromosome. The presence of this labeled probe usually is detected visually.

DNAse Deoxyribonuclease, an enzyme that degrades DNA.

Dobsonflies Some members of the family Corydalidae (order Megaloptera).  Alderflies and Dobsonflies

Dobzhansky, Theodosius Grigorievich Theodosius Dobzhansky was born in Nemirov, Ukraine, on January 25, 1900. While he was still a boy, he collected butterflies and intended to study the systematics of Coccinellidae once he had an education in biology. His university education was in Kiev, where he became an instructor in 1921–1924, and began Mendelian research on Drosophila and field research on Coccinellidae. Then he moved to Russia, and taught at the University of Leningrad in 1924–1927 while continuing research on Drosophila and Coccinellidae. Then, he moved to the USA. For a year, he worked at Columbia University. He became a researcher

Donisthorpe, Horace St. John Kelly

(1928–1940) at the California Institute of Technology where he published his groundbreaking book (1937) “Genetics and the origin of species.” He moved (1940–1962) back to Columbia University, then (1962–1971) to Rockefeller University, and finally (1971–1975) to the University of California at Davis. His contribution was to demonstrate that there is much genetic variability in a population, and that this includes many potentially lethal genes. Such genes, however, confer versatility when the population is exposed to environmental change [this theme is reiterated in the work of Edmund Brisco Ford, see below]. His work on population evolution in Drosophila fruit flies and humans gave the evidence that linked Darwin’s theory with Mendel’s law of heredity. He died on December 18, 1975.

Reference Anon. Available at http://www.biography.com/search/article. do?id=9275931, accessed 26 March 2008

Dockage Reduction in value of a crop or product due to damage, as may occur when infested with insects before or after harvest.

Dog Heartworm A mosquito-transmitted cardiovascular disease of dogs caused by infection with the nematode Dirofilaria immitis.  Dirofilariasis

Dolabellopsocidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids

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Dolichopodidae A family of flies (order Diptera). They commonly are known as long-legged flies.  Flies  Long-legged Flies

Dominance Hierarchy The physical domination of some individual by others, usually for a long period of time.

Dominant A gene is dominant when it produces the same phenotype whether it is heterozygous or homozygous. The trait is expressed even if only one copy of the gene is present in the genome.

Dominant Species A species that makes up a large proportion of the assemblage, or community, biomass or numbers.

Donisthorpe, Horace St. John Kelly Horace Donisthorpe was born in 1870 and lived in various places in southern England, mainly London suburbs. He was an amateur entomologist, in the sense that amateur means he was not paid for entomological studies. He joined the Entomological Society of London in 1891 (and served in various capacities) and the Zoological Society. His major interests were in beetles, ants, and the fauna living in ant and bird nests. He was an inveterate insect collector with a curious philosophy that the only specimens he would put in his collection were those he had collected himself. His publications range from numerous small notes to books, and the total list amounts to about 800 items. His major

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works were (1913) a supplementary volume (VI) to Fowler’s “Coleoptera of the British Islands,” (1915) “British ants,” and (1927) “Guests of British ants.” The first edition of “British ants” was privately published, and in its endpages has a list of the subscribers who bought copies; perhaps because the initial edition was small, a second edition was published in 1927. “Guests of British ants” is an account of the fauna, including even reptiles, found in ant nests. He died on April 22, 1951, in a hospital in the London area.

Reference Blair KG (1951) Horace St. John Kelly Donisthorpe. Entomologist’s Monthly Magazine 87:215

Dormant To become inactive during periods of cold weather.

Dormant Oil An oil formulation that is applied to plants during the dormant season (usually winter) when the foliage is not present and thus not susceptible to injury (phytotoxicity). It is usually directed to small arthropods or their eggs, and apparently causes suffocation.  Horticultural Oil

Dorsal Referring to the upper surface.

Dorsal Diaphragm A thin cellular layer beneath the heart that aids in blood flow. It is an incomplete wall of muscle and thin cells that separates the region around the dorsal vessel from the rest of the hemocoel.

Dorsal Longitudinal Muscles Longitudinal muscles located dorsally in insect thoracic segments that power the downstroke of wings during insect flight. These are indirect flight muscles and are not attached to the wings. They are attached to apodemes at the anterior and posterior of the meso- and metathorax. When contracted, the dorsal longitudinal muscles slightly arch the thorax, causing he wings to move downward.  Dorsoventral Muscles

Dorsal Vessel: Heart and Aorta James L. Nation University of Florida, Gainesville, FL, USA The circulatory system of insects is an open system, with the hemolymph pumped by a dorsal vessel that usually (Figs. 51–53) opens into the head. From the head the hemolymph simply percolates backward, bathing all the internal organs, eventually completing the circuit by entering the dorsal vessel through small openings, the ostia. The vessel is often described as consisting of two parts, the “heart” and the “aorta.” These terms are borrowed from vertebrate cardiology, but they have little physiological meaning in describing the dorsal vessel of insects. The abdominal portion of the dorsal vessel is often referred to as the heart while the thoracic portion is the aorta. The major criteria for deciding when the heart ends and the aorta begins are the presence of alary muscles and incurrent ostia in the heart portion. The aorta does not have alary muscles and lacks incurrent ostia, but it may have excurrent ostia. Both alary muscles and incurrent ostia occur in the thoracic portion of the vessel in many Orthoptera, and nearly the entire length of the vessel can be called the heart, with a short aorta leading into the head. Typically the dorsal vessel is a simple tube, but in Orthoptera and Dictyoptera the heart has several pairs (four pairs in Blaberus sp.) of long diverticula passing

Dorsal Vessel: Heart and Aorta

Ostia

Heart

Dorsal diaphragm

Pulsatile organ

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Aorta Antennal pulsatile organ Cerebral ganglion

Ventral diaphragm

Nerve cord

Septa

Dorsal Vessel: Heart and Aorta, Figure 51 Diagram of the components of the insect circulatory system; hemolymph moves through the heart and aorta to the head, filtering back through the body cavity and back into the heart via the ostia. Pulsatile organs assist in moving hemolymph through the appendages, especially the wings (adapted from Chapman, The insects: structure and function).

Heart Heart ligament Pericardial sinus

Ostium Alary muscle

Gut Dorsal diaphragm Ventral diaphragm

Alary muscle

Dorsal Vessel: Heart and Aorta, Figure 52 Cross section of an insect abdomen, showing components of the insect circulatory system and direction of hemolymph flow (adapted from Evans, Insect biology).

out and branching around the laterally located tergo-sternal muscles and ending in fat body tissue. The posterior end of the heart is usually closed, but it is open in immatures of craneflies (Tipulidae), and in Ephemeroptera (mayflies) it divides into three branches, with one passing into each of the three caudal filaments. In the abdomen, the dorsal vessel (Fig. 53) is located just beneath the tergal cuticle, but in the thorax of some insects portions may be helical (honeybee adults) or meander in long loops

through the thoracic musculature in Lepidoptera and Coleoptera adults. The flow of hemolymph in some insects aids in thermoregulation, with thoracic loops acting as a heat exchanger to pick up heat from the thoracic musculature. Some insects can slow down the entry of relatively “cool” hemolymph from the abdomen so that the temperature of the thorax can be kept high for flight on cooler days. Many moths “shiver” by contracting the flight muscles before taking flight on cool days, utilizing the heat generated by muscle action to provide

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Dorsoventral Muscles

Heart Muscle

indirect flight muscles, and they are not attached directly to the wings.  Dorsal Longitudinal Muscles

Silk gland Midgut Visceral fat Pariental fat Nerve cord

Dorsal Vessel: Heart and Aorta, Figure 53 Cross section of a caterpillar showing the location of the dorsal vessel (here labeled heart) (adapted from Chapman, The insects: structure and function).

a favorable thoracic temperature for flight. Conversely, the thorax may need cooling on very hot days when muscle action creates too much thoracic heat. At high environmental temperatures large-bodied adult Lepidoptera such as Manduca sexta generate too much heat in the thorax, and the abdomen acts as a cooling radiator as hemolymph is allowed to flow rapidly to the abdomen which is less well insulated with scales than is the thorax. Heat is dissipated to the air surrounding the abdomen, and the cooler hemolymph is pumped back to the thorax by the heart.

References Heinrich B (1996) The thermal warriors. Strategies of insect survival. Harvard University Press, Cambridge, MA, 221 pp Heinrich B (970) Thoracic temperature stabilization by blood circulation in a free-flying moth. Science 16:580–582

Dorsoventral Muscles Muscles running from the dorsal to the ventral components of thoracic segments that power the upstroke of wings during insect flight. These are

Dorsum The anatomical upper surface of a body; opposite of ventral. The legs are considered to be associated with the lower or ventral surface, and the dorsum is the opposite surface, the top of the head and the “back” of the thorax and abdomen.

Double-Eye Moths (Lepidoptera: Amphitheridae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Double-eye moths, family Amphitheridae, are an unusual and small family of mostly tropical moths, totaling 57 species, mostly Indo-Australian (one genus occurs in Europe and another in South America). The family is part of the superfamily Tineoidea, in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small (11–22 mm wingspan), with head rough-scaled and eye usually divided; haustellum naked; maxillary palpi 1-segmented. Maculation is colorful and iridescent or duller and pale, and variously marked. Adults active diurnally. Larvae are leafminers, becoming leaf skeletonizers in later instars; host records are mostly in Betulaceae and Aceraceae. The family has been erroneously called Roeslerstammiidae, based on the single European genus, Roeslerstammia, named after the Austrian lepidopterist Joseph E. Fischer von Röslerstamm (1787–1866).

References *Heppner JB (2003) Amphitheridae. In: Lepidopterorum Catalogus, (n.s.). Fasc 28. Association for Tropical Lepidoptera, Gainesville, FL, 8 pp

Douglas-Fir Beetle, Dendroctonus pseudotsugae Hopkins (Coleoptera: Curculionidae, Scolytinae)

Kyrki J (1983) Roeslerstammia Zeller assigned to Amphitheridae, with notes on the nomenclature and systematics of the family (Lepidoptera). Entomol Scand 14:321–329 Moriuti S (1978) Amphitheridae (Lepidoptera): four new species from Asia, Telethera blepharacma Meyrick new to Japan and Formosa, and Sphenograp tis Meyrick transferred to the family. Bull Univ Osaka Prefecture B 30:1–17 Moriuti S (1987) Amphitheridae (Lepidoptera) of Thailand. Microlepidoptera Thailand 1:87–95 Viramo J (1968) Über die Verbreitung und die Wirtspflanzen von Roeslerstammia erxlebeniella F. (Lep., Acrolepiidae). Aquilo (Zool.) 6:12–17

Double Sampling A sampling approach in which an initial sample (usually small) is drawn and used to determined the necessary sample size for a subsequent sample within the same time period.  Sampling Arthropods

Douglas-Fir Beetle, Dendroctonus pseudotsugae Hopkins (Coleoptera: Curculionidae, Scolytinae) Jose F. Negron USDA Forest Service, Ft. Collins, CO, USA The Douglas-fir beetle, Dendroctonus pseudotsugae, is a bark beetle that attacks and can cause extensive mortality of its host Douglas-fir, Pseudotsuga menziesii, throughout most of its range in British Columbia, the western United States, and south to Mexico. The insect can also attack and reproduce in downed western larch, Larix occidentalis and subalpine larch, L. laricina, but is not able to complete development on standing larch trees. Western hemlock, Tsuga heterophylla, is also reported as a host. Just like with other tree-killing bark beetles, tree mortality results when the insects utilize the phloem of the tree for habitat and nourishment which results in girdling of the tree disrupting the translocation of nutrients. As the

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tree succumbs to the attack it changes in coloration within a year to a light yellow then to a bright orange before the needles begin to drop. The insect also inoculates attacked trees with blue-stain fungi Ophiostoma pseudotsugae and Leptographium abietinum, which may assist the insect in overcoming tree defenses. Under endemic population levels the insect infests scattered trees downed by windstorms or stressed by root disease, defoliation, or fire injury. As populations increase healthy trees can be killed from small groups consisting of a few trees to groups of hundreds of trees. Epidemics can be quite devastating, but they usually only last about 4 years. Initial symptoms of attack include an accumulation of brown-reddish boring dust at the base of the tree and in bark crevices. Resin flow is also often observed, but not always, as it drains from attacks higher in the tree. Attacks are not always successful as the tree is often able to repel the insects from entering the tree by the copious exudation of resin. The Douglas-fir beetle has one generation per year. There is a variation in flight periodicity from year to year and from one location to another but the primary dispersal flight usually occurs in mid- to late spring. Colonization of new trees is mediated by chemical attractants. Females initiate attacks on new hosts and after mating with a single male, begin constructing an egg gallery (Fig. 54) by tunneling up in the phloem parallel to the grain of the wood. The males assist in gallery construction at first by clearing boring dust and frass at the beginning of the gallery and then helping pack the rest of the gallery with frass. The egg galleries are usually 20–25 cm in length. As the females construct the gallery they lay eggs in niches alternately on both sides of the gallery in clusters of 5–24 eggs. The eggs are white and about 1 mm in length. Eggs hatch in 7–21 days. The larvae are white, c-shaped, and legless with shiny light brown heads. There are four larval instars. Through the summer each larva constructs its own larval gallery leading away from the egg gallery at approximately a

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Douglas-Fir Beetle, Dendroctonus pseudotsugae Hopkins (Coleoptera: Curculionidae, Scolytinae)

Douglas-Fir Beetle, Dendroctonus pseudotsugae Hopkins (Coleoptera: Curculionidae, Scolytinae), Figure 54 Douglas-fir beetle egg gallery (drawing by Joyce VanDeWater).

Douglas-Fir Beetle, Dendroctonus pseudotsugae Hopkins (Coleoptera: Curculionidae, Scolytinae), Figure 55 Douglas-fir beetle adult (drawing by Joyce VanDeWater).

right angle, pupates in a chamber at the end of the gallery, and later transform into the adult. Pupation usually occurs by August with transformation into the adult stage occurring late AugustSeptember. As the larvae develop they spread out forming a fan-shaped pattern that is distinctive of this species of bark beetle. The adult is the primary overwintering stage although some larvae may also overwinter. Newly emerged adults (Fig. 55) are light brown but later become dark brown to black with reddish elytra. Older beetles darken with time and become completely black. Adults are stout, cylindrical beetles, 4–6 mm in length. A number of natural enemies help regulate populations of the Douglas-fir beetle. The most notable include clerid beetle predators Enoclerus sphegeus and Thanasimus undulatus, the predatory

fly Metedera aldrichii, parasitoid wasps in the genus Coeloides and various woodpeckers. Infestations of Douglas-fir beetle occur most commonly in overmature stands, with high stocking, and a high proportion of Douglas-fir. The largest trees in the stands are preferred. In downed trees the insect prefers to attack the underside of the tree. Because insect populations may increase rapidly in downed trees, rapid removal of downed trees may help reduce populations. Maintaining vigorously growing stands with adequate stocking levels can help mitigate tree mortality.  Bark Beetles in the Genus Dendroctonus

References Bedard WD (1950) The Douglas-fir beetle. U.S. Department of Agriculture Circular No. 817

Dragonflies

Furniss MM, Johnson JB (2002) Field guide to the bark beetles of Idaho and adjacent regions. Idaho Forest, Wildlife, and Range Experiment Station, University of Idaho, Moscow, Idaho Ross DW, Solheim H (1997) Pathogenicity to Douglas-fir of Ophiostoma pseudotsugae and Leptographium abietinum, fungi associated with the Douglas-fir beetle. Can J Forest Res 27:39–43 Schmitz RF, Gibson KE (1996) Douglas-fir beetle. Forest insect and disease leaflet #5. U.S. Department of Agriculture Forest Service

Douglasiidae A family of moths (order Lepidoptera). They commonly are known as douglas moths.  Douglas Moths  Butterflies and Moths

Douglas, John William John Douglas was born in London on November 18, 1814. At the age of 15, he was the victim of a practical “joke” by a schoolfellow, who set alight his pocket full of firecrackers. His extensive burns kept him bedridden for 2 years and required numerous operations throughout his life. While he was bedridden, he turned to the study of botany and drew plant specimens, at which he became proficient. He found employment at Kew Botanical Garden for a few years, but his father obtained for him a better-paying job at the Customs House. He married in 1843. While at Kew, he began collecting insects, and in 1837 published his first entomological paper. Much of his work was directed to Lepidoptera. His major work, coauthored with John Scott, was perhaps “The British Hemiptera, Volume 1, Hemiptera-Heteroptera,” published by the Ray Society. Additions and corrections to this work were published from time to time in Entomologist’s Monthly Magazine, of which he became editor in 1874. He joined the Entomological Society of London and held several posts, becoming president in 1861. He died on August 28, 1905.

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Reference Saunders E (1905) In memoriam. Douglas JW. Entomologist’s Monthly Magazine 41:221–222

Douglas Moths (Lepidoptera: Douglasiidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Douglas moths, family Douglasiidae, comprise only 28 known species, mostly Palearctic (20 sp.). The family is part of the superfamily Tineoidea, in the section Tineina, subsection Tineina, of the division Ditrysia. Adults minute to small (6–15 mm wingspan), with head smooth-scaled; haustellum naked; labial palpi short; maxillary palpi reduced, 1-segmented. Maculation dull with bands of gray or tan, with venation reduced (especially in the hindwings) and with long hindwing fingers. Adults are crepuscular or diurnal. Larvae are leafminers or borers in petioles or stems. Host plants are known in Boraginaceae, Labiatae, and Rosaceae. The family and nominate genus Douglasia are named after the British lepidopterist and hemipterist John W. Douglas (1814–1905).

References Gaedike R (1974) Revision der paläarktischen Douglasiidae (Lepidoptera). Acta Faunistica Entomol Mus Natl Prague 15:79–101 *Toll S (1956) Douglasiidae. In: Klucze do Oznaczania Owadüw Polski. 27. Motyle – Lepidoptera, 40:37–50. Polskie Towardzystwo Entomologiczne [in Polish]

Dragonflies Certain members (suborder Anisoptera) of an order of insects (order Odonata).  Dragonflies and Damselflies

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Dragonflies and Damselflies (Odonata)

Dragonflies and Damselflies (Odonata) Boris C. Kondratieff Colorado State University, Fort Collins, CO, USA Adult dragonflies and damselflies are two of the most beautiful and better-known insects of world. Their kaleidoscope of colors and aerobatic abilities have fascinated people for many centuries, and much has been written about them. They are conspicuous members of most permanent lakes, ponds, and wetlands. Nymphs of many species are also found in lotic habitats. Nymphs of some species are found in water filled leaf axils of plants, moist leaf litter, and even brackish water. Some species also occur in temporary habitats. Two North American species (family Petaluridae) are found among wet leaves in seepage areas. Adults are medium to large in size, having wingspans ranging from 20 to 115 mm. Local names that have been applied to this order include, mosquito hawk, devil’s darning needle and horse stinger. The order name is Odonata, which means tooth, and refers to the large prominent jaws or mandibles of the adults. Adult dragonflies (Fig. 56) are easily recognized by two pairs of membranous elongate wings with many veins, long abdomen, bristle-like antennae and large head occupied mostly by the compound eyes. The nymphs are unique as compared to all other insect immatures by having the lower lip (labium) modified into a grasping structure that is elbowed and can be folded. The order includes two distinctive suborders in both the adults and nymphs in North America, the dragonflies or Anisoptera, and the damselflies or Zygoptera. The only other suborder of Odonata, the Anisozygoptera, includes one family, the Epiophlebiidae. This subfamily has two species, one distributed through the islands of Japan and the other in the eastern Himalayas in Nepal. Dragonfly adults are distinguished by hind wings (Fig. 57) that are wider at the base than the front wings, the abdomen long and stout, and when at rest wings are held outstretched. Nymphs are

r ecognized by a long or oval body, and no gill plates at the end of the abdomen (Fig. 57) (instead there are three short pointed structures). Adult damselflies have both the front and hind wing of the same shape and size, a long thin abdomen, and wings held “roof-like” over the body at rest. Damselfly nymphs have elongate and slender bodies and three flat, elongate gill plates at the apex of the abdomen. All Odonata adults are predators of flying insects, often small flies, but also larger insects such as wasps, butterflies, and even other dragonflies or damselflies. They use the front legs as a “basket” to scoop their prey out of the air. Sometimes adults will pick prey off plants or other substrates. Dragonfly and damselfly nymphs are accomplished visual predators of almost anything they can overpower, including microcrustaceans, other aquatic insects, to tadpoles, and even fish. They use the unique lower lip or labium to grab the prey and bring it to their mouthparts for consumption. Nymphs are either climbers or crawlers stalking their prey or, sprawlers and burrowers ambushing their prey. Dragonfly nymphs pump water in and out of a gill chamber inside the posterior portion of the abdomen. This type of “jet propulsion” can be easily observed in a pan of water. Damselfly nymphs have three flat gill plates at the apex of the abdomen, providing a larger surface area for oxygen diffusion. About 5,500 species of Odonata are known from the world grouped in 28 families, of which eleven are recorded from North America. Approximately 440 species have been recorded from North American. A summary of the North American species can be located at the website http://www.afn. org/~iori/nalist.html. Additionally, many useful links to other Odonata websites can be found at http://www.ent.orst.edu/ore_dfly/links.html. Order: Odonata Suborder: Zygoptera Family: Dicteriadidae Family: Polythoridae Family: Amphipterygidae Family: Calopterygidae Family: Lestidae

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Cer cus

Pro

Compound eye Antenna Frons Clypeus Labrum Labium Coxa Trochanters Femur Tibia Pretarsus Tarsus

notu m Mes otho raci Mes c sp e irac Mes pistern le um ople u r al s Mes utur epi e Mes meron epis t ernu Met m apl Met eural s epim ut eron ure


Metathoracic spiracle

Upper antenodal cross veins Lower Nodus

Stigma Brace vein

Arculus

Triangle

Dragonflies and Damselflies (Odonata), Figure 56 Adult dragonfly: lateral view of female (above); front and hind wings (below). Family: Perilestidae Family: Synlestidae Family: Megapodagrionidae Family: Pseudostigmatidae Family: Platystictidae Family: Protoneuridae Family: Coenagrionidae Suborder: Anisoptera Family: Petaluridae Family: Austropetaliidae Family: Aeshnidae Family: Gomphidae Family: Neopetaliidae

Family: Cordulegastridae Family: Corduliidae Family: Libellulidae

A brief synopsis of common North American families is presented below.

Family Calopterygidae (Broad-winged Damselflies) These well-known groups of familiar stream damselflies are known as the jewelwings (Calopteryx)

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Dragonflies and Damselflies (Odonata) Triangle

Antenna Labial mask

Anal loop

Eye

Labrum Movable hook of palpus

Palpus Hindwing pad Mentum

Epiproct Anal Cercus Paraproct pyramid

Dragonflies and Damselflies (Odonata), Figure 57 Base of dragonfly hind wing (above, left) showing anal loop, a diagnostic character. Diagram of dragonfly nymph (right) showing dorsal (left portion) and ventral (right portion) perspective. Head of immature dragonfly showing the mouthparts (lower left), which are modified for grasping.

and the rubyspots (Hetaerina). The large adults have metallic green bodies, the wings are not abruptly stalked at the base, and they have a skipping type of flight. The long-legged nymphs have a flat, pentagonal head, a very long first antennal segment, and are usually associated with instream aquatic plants, woody debris, and exposed roots of streamside plants. Species are characteristically associated with small to medium sized streams (Calopteryx) and larger rivers (Hetaerina). Only one generation per year is known for this group. Adults perch horizontally on twigs at the shore. The courtship behaviors of the adults have been extensively studied. The dancing flights are characteristic. Males have distinctive territorial display flights.

Family Lestidae (Spreadwinged Damselflies) Nymphs of most species inhabit marshes and swamps, temporary standing water, and slow moving

streams. The adults of these damselflies are easily recognized by their perching posture, at an oblique angle with partially spread wings. The long abdomen and petiolate part of the lower lip (prementum) easily distinguish the nymphs. One generation per year has been reported for the North American species. The two genera Archilestes and Lestes are widely distributed. Archilestes are usually found in streams of a slow current, even in isolated desert canyons of the Southwest.

Family Coenagrionidae (Narrowwinged or Pond Damselflies) This family is the most successful of all damselflies in terms of the number of different species and types of aquatic habitats occupied. These are the red, orange, yellow and blue small adult damselflies commonly seen around ponds and various types of wetlands. The adults are known by such


common names as sprites (genus Nehalennia), forktails (genus Ischnura), dancers (genus Argia), and bluets (genus Enallagma). Nymphs are usually associated with living or dead aquatic vegetation and debris. Nymphs of the genus Argia are often within rocky substrates of riffle reaches of streams. Egg-laying habits of the adult female are often astounding, with some species completely submerging and crawling about. Most species lay eggs just a few centimeters below the surface in plant material, both living and dead.

Family Aeshnidae (Darner Dragonflies) The adults of these soaring dragonflies include the largest species in North America. Genera such as Anax (green darners), Coryphaeschna (pilot darners), and Epiaeschna (swamp darners) are the giants of this group. Many darners have long slender bodies resembling a darning needle, hence the name. The adults are easily identified by the large eyes meeting on top of the head, with the bodies brown, black and striped or spotted with blue. Nymphs are easily distinguished by the combination of a flat mentum and 6 or 7-segmented antennae. Adults are strong fliers, with some species migrating long distances. Often they feed in swarms. Nymphs are climbers, and are found among living and dead submerged plant material, including woody debris. Some species that occur in streams may be found clinging to submerged logs. Adult females insert eggs into underwater portions of plants. Nymphs may require 2–4 years to complete one generation.

Family Gomphidae (Clubtail Dragonflies) Adults of clubtails get their name from the enlarged end of the abdomen in males of many species. Adults are beautifully camouflaged with brown or black marked with yellow or green. The eyes are widely spaced on top. Nymphs, like the family Aeshnidae, have a flat mentum, but the antennae are only

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4-segmented. Adults usually perch on the ground horizontally and, unlike the darners, they do not soar but skulk around trees or make short distance flights in nearby fields, squatting on stones, sometimes branches of shrubs or on logs. Nymphs are burrowers in soft silt, sand or gravel of streams of all sizes or ponds. Nymphs of the huge dragonhunter, Hagenius brevistylus, are found among accumulations of leaves in quiet margins of streams. Most species require 2 years to complete their life cycle.

Family Libellulidae (Skimmer Dragonflies) The skimmers include some of the most common dragonflies in North America. Almost every pond, lake or wetland has an assemblage of these species. A few species are found in streams. Adults of many species have prominent wing patterns, and many have brightly colored abdomens of red, blue and other colors. Adults can be easily distinguished by the characteristic boot-shaped anal loop of the hind wing. Adults usually perch on tips of stems, and have a gliding type of flight. Nymphs can be usually recognized by the scoop-like labial palps with the distal margins relatively smooth. However, nymphs are often difficult to distinguish from the Corduliidae (in some classifications only recognized as a subfamily, the Corduliinae). Nymphs are sprawlers or climbers, and found in all types of standing water, from hoof prints to the edges large lakes or reservoirs. A few species are even found in brackish water and other estuarine environments. Well-known genera are Libellula (king skimmers), Sympetrum (meadowhawks), Erythrodiplax (dragonlets), Perithemis (amberwings), Erythemis (pondhawks), Tramea (saddlebags gliders), and Celithemis (small pennants).

References Abbott JC (2005) Dragonflies and damselflies of Texas and south-central United States. Princeton University Press, Princeton, NJ, 344 pp

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Beaton G (2007) Dragonflies and damselflies of Georgia and the southeast. University of Georgia Press, Athens, Georgia, 355 pp Corbet PS (1999) Dragonflies. Behavior and ecology of Odonata. Comstock Publishing Associates, Ithaca, New York, 829 pp Dunkle SW (2000) Dragonflies through binoculars: a field guide to dragonflies of North America. Oxford University Press, New York, NY, 252 pp Garrison RW, von Ellenrieder N, Louton JA (2006) Dragonfly genera of the New World. An illustrated and annotated key to Anisoptera. Johns Hopkins University Press, Baltimore, MD, 368 pp Needham JG, Westfall MJ Jr, May M (2000) Dragonflies of North America. Scientific Publishers, Gainesville, FL, 939 pp Silsby J (2001) Dragonflies of the world. Smithsonian Institution Press, Washington, DC, 216 pp Westfall MJ Jr, May ML (1996) Damselflies of North America. Scientific Publishers, Gainesville, FL, 649 pp

Drake, Carl John Carl Drake was born on a farm in Ohio on July 28, 1885. He obtained a B.S. degree (and a Bachelor of Pedagogy) from Ohio State University in 1912, then in 1914 an M.S. degree and in 1921 a Ph.D. degree from the same institution. He worked for 4 years as specialist in entomology in the School of Forestry, Syracuse University, then from 1922 to 1946 in the Department of Zoology and Entomology at Iowa State University. In this last position, he was not only departmental head, but also head of the entomology section of the Iowa Agricultural Experiment Station. His taxonomic interests were in lace bugs and semiaquatic Hemiptera, of which he built a large collection. His experiment station obligations as applied entomologist had him working on grasshoppers, chinch bug, Hessian fly, and European corn borer. He was a member of the Central States Plant Board, the National Plant Board, and the American Association of Economic Entomologists. On retirement in 1946, he concentrated on his taxonomic interests, and in 1957 moved to work as an honorary Research Associate of the U.S. National Museum in Washington, DC. By working at the museum 61/2 days per

week (he never married), his lifetime publications list grew to exceed 500 papers. He died on October 2, 1965, in Washington, DC.

Reference *Mallis A (1971) Carl John Drake, In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 238–239

Drench Treatment Application of a liquid insecticide to an area, usually soil, until it is completely penetrated.

Drepanidae A family of moths (order Lepidoptera). They commonly are known as hook-tip moths.  Hootktip Moths  Butterflies and Moths

Driver Ants (Dorylus subgenus Anomma) (Hymenoptera: Formicidae) Caspar SchÖning University of Copenhagen, Copenhagen, Denmark Driver ants are those army ant species in the afrotropical subgenus Dorylus (Anomma) that hunt by massive swarm raids on the forest floor and up in the vegetation. Any animal capable of moving fast enough and lacking other effective protective mechanisms flees from such an advancing swarm of hundreds of thousands or even millions of ant workers in search of prey. Hence the raid swarm “drives” many animals before it. Due to their ferocious nature, these ants are recognized by their own name in many tribal

Driver Ants (Dorylus subgenus Anomma) (Hymenoptera: Formicidae)

languages in sub-Saharan Africa. In Ghana, for example, they are called “Nkran” in the Twi language. In Kenya, people in the Meru tribe use the term “Thuraku” for them. Their common English name was originally coined in 1847 by Dr. Thomas Savage in the description of his observations of D. (A.) nigricans colonies in present-day Liberia. Although other authors have subsequently applied the term to all species in the subgenus Anomma (as currently recognized) or even to all species in the genus, it is best to stick with its original meaning to avoid confusion.

Taxonomy and Phylogeny Many species in the genus Dorylus (as well as many other army ants) were described based only on a single caste or sex and the associations between these different forms have been hard to establish. Therefore, delimitating the subgenus Anomma proved difficult and several other species not showing the typical “driver ant” hunting behavior but foraging less conspicuously in the leaf-litter were also described as species in the subgenus Anomma after 1847. But recent evidence from a molecular phylogeny indicates that the subgenus Anomma as currently defined is actually paraphyletic. The species that forage in the leaf-litter are more closely related to subterranean species of the subgenus Dorylus s.s. than to the driver ants (in the sense of Savage’s original functional definition), which form a wellsupported clade. This result thus indicates that the foraging in massive surface swarms evolved only once within the genus Dorylus. Since the type species for the subgenus Anomma is a driver ant, the species hunting in the leaf-litter stratum will have to be removed from Anomma in a revised subgenus classification of the genus Dorylus. Although more than thirty nominal forms have been described under Anomma (including those taxa that turn out to be more closely related to Dorylus s.s.), there are probably only about ten species of driver ants.

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Morphology Workers Driver ant workers can be distinguished from the workers of all other Dorylus species by several qualitative and quantitative traits (these apply mostly to the largest individuals). The qualitative traits are the presence of basisternal spines, frontal carinae reduced, mesonotum in lateral view impressed, petiole long and slender, and strongly (Fig. 58) trapezoidal head shape (head width much wider anteriorly than posteriorly). Moreover, driver ant workers have relatively (i.e., for a given worker dry mass) longer mandibles, legs and antennae, and these features are probably adaptations associated with the derived driver ant foraging mode. While their longer mandibles can inflict more painful bites and thus provide better protection against predators, longer legs allow faster and more efficient locomotion, the transport of larger prey items (prey is carried slung underneath the body) and finally perhaps also better climbing of vegetation. Longer antennae, on the other hand, will help workers to follow pheromone trails at higher speed while avoiding collisions in spite of dense traffic. Being more exposed to sunlight during foraging, driver ant workers also tend to be darker than workers of species hunting in leaf-litter and soil. Like workers of all other Dorylus species, driver ant workers lack eyes. The degree of worker polymorphism in driver ants (and other Dorylus species) is among the most extreme in ants. In some species the largest workers have a dry mass 200-fold that of the smallest workers. These extreme differences in size are associated with striking differences in the number of antenna segments (varying between eight in the smallest workers and 11 in the largest), hairiness, mandible structure (with many teeth in the smallest workers and only an apical and subapical tooth in the largest), head shape (from rectangular in the smaller individuals to trapezoidal in the largest), coloration (from light brown to very dark or black) and in the relative

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Driver Ants (Dorylus Subgenus Anomma) (Hymenoptera: Formicidae), Figure 58 Driver ants: (a) Head of a Dorylus (Anomma) nigricans male in frontal view. The mandible is very long and slender and the head is high (photograph by April Nobile, from www.antweb.org); (b) Head of a large D. (A.) sjoestedti worker in frontal view. The head is much wider anteriorly and the mandible has only two teeth (photograph by April Nobile, from www.antweb.org); (c) A raid swarm of D. (A.) nigricans advancing on the forest floor in the Taï forest, Ivory Coast (photograph by Caspar Schöning).


sizes of several other body parts. In general, it is fair to say that the morphological diversity in a driver ant colony is larger than in some other entire ant genera. This substantial variation has contributed to the confusion in driver ant taxonomy because some species were described more than once based on workers belonging to different size-classes.

Males In Africa, Dorylus males are collectively referred to as sausage flies and the first Dorylus males to be found were described as a Vespa wasp species by Linné. Dorylus males possess a pair of compound eyes and three ocelli. The mandibles of driver ant males are relatively longer and more slender than those of other Dorylus species, and their heads are relatively longer than the extremely broad heads of other Dorylus males. Moreover, they are much darker.

Queens Driver ant queens are perhaps the largest ants in the world, those of D. wilverthi may be up to 6 cm long and may lay as many as 3–4 million eggs every month. Driver ant queens, like workers, do not possess eyes. It is unclear which characters in the driver ant queen caste are actually apomorphies because the queens of many Dorylus species are unknown so that comparative studies are difficult but the shape of the hypopygium of driver ant queens seems to be unique within Dorylus.

Behavior The raiding swarms of driver ants are one of the most fascinating examples of coordinated group activity shown by animals with hundreds of thousands or even a few million ant workers forming a dense carpet acting as a dragnet that sweeps through areas of 1,000 m2 or more in a single day

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in search of prey. Workers climb vegetation up to a height of several meters. The swarms can be 30 m or more wide and move forward at a speed between 7 and 25 m per hour depending on the species. The foraging distances of D. wilverthi colonies may be up to 220 m. Driver ants are almost exclusively carnivorous but they are also attracted to oily vegetative products such as palm nuts and avocadoes. Their raids appear to be an efficient strategy to harvest abundant and evenly distributed small prey (such as solitary insects) as well as rare and very patchily distributed large prey (such as mammal carcasses). Driver ant prey spectra are therefore extremely diverse. Although quantitative data are lacking, driver ant species are likely to be the most polyphagous predators on earth. Solitary insects (especially their less mobile immature stages) and earthworms make up the majority of the biomass retrieved. Most vertebrates easily escape, but sometimes small amphibians (e.g., frogs), mammals (e.g., mice) and reptiles (e.g., chameleons) fall victim to the raid swarms. Large captive animals such as snakes and monkeys have been reported to be eaten to the bones by driver ants. In the hunting behavior it becomes evident that the extreme worker polymorphism is linked to a pronounced, yet flexible, division of labor. While the proportion of larger workers is very small in the swarm, they are crucially important and disproportionately overly represented in the tasks of pinning down, dismembering and retrieving larger prey. Workers can cooperate in the transport of large prey items with large workers grabbing the item at the front and one or more small workers lifting it off the ground at the back. In the species examined so far, most of the prey biomass is transported by such groups. At irregular intervals, the entire colony migrates to a new nest site, most probably as a result of resource depletion around the nest. Migrations can last up to 4 days and include the movement of the colony’s queen, its workers and its brood carried by the workers. Unlike some army ant species in the subfamily Ecitoninae, the temporal emigration pattern is not linked to a

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rhythm in the queen’s egg-laying activity. Some migrations are triggered by predator attacks on the nests. Colonies nest in the soil, usually at the base of trees. Over the period of a nest stay, workers may bring up large amounts of soil (40 kg or more) to the surface. In the nest, the workers form a big cluster that hangs suspended from roots and contains the brood and queen. Quite often, colonies reoccupy old nests that they or other colonies had used before. Driver ants reproduce by colony fission like honeybees. Colony fission directly creates colonies with worker populations large enough for conducting swarm raids. When a colony has grown to a large enough size, the queen lays eggs that develop into queens and males. The sex ratio is highly male-biased. Only a few (two to fifty) queens, but several hundreds or up to a few thousand males, are reared. After about 4 weeks, the queen pupae hatch and all but one of the virgin queens are killed in ways not yet understood. At this point the old queen leaves the nest with about half the worker population. The remaining queen will subsequently mate with several males that fly in from foreign colonies. The males in this nest hatch after about 8 weeks and then in turn fly off at night in search of foreign nests with virgin queens ready to mate. When the males have flown off, the new queen and the remaining workers form a new functional colony and are free to migrate to new foraging grounds. Although there is a tendency for colonies to reproduce towards the end of the dry season, colony fissions take place throughout the year. In two species, colonies have been observed to produce males without a subsequent colony fission.

Ecology With a worker population of up to nine million individuals, driver ant colonies form the largest single-family insect societies on earth, and thus have a voracious appetite. The immediate effect of

their raids is a reduction of the biomass and perhaps the diversity of invertebrates in the foraging areas. Driver ants therefore create a mosaic of patches in different stages of recovery from prey extraction. By this mechanism, they may promote diversity in the invertebrate communities, but to date studies examining the effect of driver ant raids on the prey population dynamics are lacking. This issue becomes both more complex and interesting when one considers that up to three driver ant species can coexist at a site. Depending on the degree of resource partitioning between them, the combined impact on the invertebrate communities in the vegetation and on the forest floor may be very strong. Driver ant colonies are hosts to diverse assemblages of so-called myrmecophiles. These are animals (such as certain staphylinid beetles and isopods) that have evolved mechanisms to integrate into the colonies without the ants identifying them as non-nestmates. These mechanisms represent either chemical or tactile camouflage (or both). It is difficult to examine what exactly all these species are doing in the colony but it seems likely that the majority are parasitic, while others are commensals. Blind snakes of the genus Typhlops parasitize driver ant colonies by feeding on the brood or on the prey brought in by the foraging workers. The number of bird species specializing in attending the raid swarms to catch animals flushed by the advancing ants (and sometimes stealing prey from them) is much smaller than in South America where many dozens of “ant-birds” are closely associated with two swarm-raiding ant species in the subfamily Ecitoninae. The paucity of specialized ant-following birds in Africa is puzzling in view of the higher colony density and diversity of driver ants. In spite of their painful bites, driver ants are preyed on by several mammals, including pangolin, honey badger, aardvark, gorilla, Jackson’s mongoose and the common chimpanzee. The last species is the only one known to employ tools when taking driver ant prey. After opening the nest with the hands, so-called ant-dipping wands

Drosophilidae

are inserted into the mass of ants in the central nest cavity. When enough ants have climbed the wand, it is removed and the ants are swiped off the tool with the hand or mouth and then hastily eaten. The effect of mammal predation on the growth and fitness of driver ant colonies has not yet been studied. Dorylus species in the subgenus Typhlopone are the most important invertebrate predators of driver ants. They attack driver ant colonies in their nests through tunnels in the soil and sometimes destroy them. Finally, driver ants are also ecologically important because they move large amounts of soil, not only in nest construction but also when preparing their foraging and migration trails as “roads” with an even surface or as trenches and tunnels. The soil carried to the surface during nest construction is enriched with the indigestible prey remains and thus presumably rich in nitrogen and other plant nutrients.

Habitat and Distribution Driver ants are restricted to sub-Saharan Africa. Within this vast region, they occur primarily in forests and other humid habitats. Some species appear to depend strictly on forest, while others such as the East-African D. (A.) molestus live in a wide range of habitats such as scrubland in proximity to rivers, woodland, agroforestry systems (e.g., banana, cocoa and coffee) and forests from sea level up to 3,000 m altitude.

Economic Importance Driver ants provide a valuable pest-control service when invading houses and hunting in cultivated land. However, these benefits are probably outweighed by the damage they cause when attacking humans and livestock. Unlike termite alates, driver ant males are not eaten by people, although they would appear to be nutritiously rewarding. The reason is probably that their

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a vailability is far less predictable and that termite alates are much softer and easier to roast and chew.

References Gotwald WH Jr Army ants – the biology of social predation. Cornell University Press, Ithaca, New York Kronauer DJC, Schöning C, Vilhelmsen LB, Boomsma JJ (2007) A molecular phylogeny of Dorylus army ants provides evidence for multiple evolutionary transitions in foraging niche. BMC Evol Biol 7:56; http://www. biomedcentral.com/1471–2148/7/56 Leroux JM (1982) Ecologie des populations de dorylines Anomma nigricans dans la région de Lamto (Côte d’Ivoire). Publications du Laboratoire de Zoologie, No. 22. Ecole Normale Supérieure, Paris Raignier A (1972) Sur l’origine des nouvelles sociétés des fourmis voyageuses Africaines (Hymenopteres, Formicidae, Dorylinae). Insectes Soc 19:153–170 Raignier A, van Boven JKA (1955) Étude taxonomique, biologique et biométrique des Dorylus du sous-genre Anomma (Hymenoptera, Formicidae). Annales Musée Royal du Congo Belge Nouvelle Série in Quarto Sciences Zoologiques 2:1–359 Savage TS (1847) On the habits of the “drivers” or visiting ants of West Africa. Trans R Entomol Soc Lond 5:1–15 Schöning C, Njagi WM, Franks NR (2005) Temporal and spatial patterns in the emigrations of the army ant Dorylus (Anomma) molestus in the montane forest of Mt. Kenya. Ecol Entomol 30:532–540

Droplet Spermatophore A spermatophore (capsule containing sperm) that is attached to a thread-like stalk, which in turn has an adhesive base for placement on a substrate. Male Collembola often distribute their sperm in this manner.

Drosophilidae A family of flies (order Diptera). They commonly are known as small fruit flies, vinegar flies, or pomace flies.  Flies

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Drumming Communication and Intersexual Searching Behavior of Stoneflies (Plecoptera)

Drumming Communication and Intersexual Searching Behavior of Stoneflies (Plecoptera) Kenneth W. Stewart University of North Texas, Denton, TX, USA Stoneflies of the Northern Hemisphere suborder Arctoperlaria have evolved the most diverse and complex system of vibrational communication known in insects. Only leafhoppers and delphacid planthoppers possibly have evolved signals as complex as those of stoneflies, but relatively few species of those two groups have been studied. The first studies in the 1960s and 1970s that were designed to quantify the drumming communication of stoneflies established that: (i) vibrational signals were produced by percussion, with either the unmodified or specialized distal, ventral portion of the abdomen, (ii) duets were either “2-way” (male call-female answer sequences) or “3-way” (male call-female answer-male reply sequences), (iii) male calls were more complex than female answers or male replies, (iv) the signals of both sexes and their duet pattern were species-specific and therefore probably fixed action behaviors, and (v) during duetting, males searched for stationary females, establishing that the behavior was part of the mate-finding system. Intensive research in the past three decades has revealed that signals are produced in some groups by methods other than percussion, that the rhythms and exchange characteristics of both males and females vary in complex ways and that the search behaviors in relation to drumming are more than simple “bee-line homing” of the male on females. The entire mating system of stoneflies involves both their intersexual communication with vibrational signals and the associated aggregation and movement (searching-related) behaviors of both sexes. The typical system in Arctoperlaria involves the sequence of: (i) encounter site aggregation of sexes, (ii) species-specific calling by males with vibrational signals during a ranging, non-oriented

search, (iii) duet establishment when females within communicable range answer with vibrational signals, then (iv) a localized, oriented search by the moving male toward the now stationary female until location and mating are accomplished. Males are polygamous and continue calling and searching during their short reproductive lives. Typically, only virgin females answer males and, once mated, reject subsequent male advances by raising and curving their abdomens. There is obviously no fossil record for vibrational communication in stoneflies, so formulation of a paradigm on how the behavior originated and has been further developed has of necessity depended on patterns revealed from modern species. Out-group comparisons with the Grylloblattodea, other orthopteroid groups and the Southern Hemisphere stonefly suborder Antarctoperlaria, indicate that ancestral stoneflies were non-drummers. The first trace of the behavior probably resulted from males accidentally bumping their unmodified abdomen while searching for females, followed by the possible defensive response of females to the vibrations by becoming motionless and stationary. Selection progressively reinforced the male bumping and female response into behavioral actions until a relatively simple, sequenced duetting (male calls-female answers) developed, that represents an ancestral pattern. The signals of both sexes were produced by percussion and were monophasic volleys of even spacing and little amplitude modulations (Fig. 59). Out-group comparisons have indicated further that species-specificity and behavioral isolation were then derived from this ancestral pattern (and are represented in modern species) by either: (i) retention of the ancestral pattern with slight modifications of signal characteristics (number of beats, overlap of the male-female duet, changing the beat interval rhythm or amplitude modulation) in both male and female signals; (ii) major rhythm changes, particularly in male calls, by phasing or grouping of signal beats; (iii) changes in the method of signal vibration

Drumming Communication and Intersexual Searching Behavior of Stoneflies (Plecoptera)

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Female

Male

Female

Female

Male Phase 1

Male Phase 2

Female Female

Male

Male

Male

Male Rubs

Drumming Communication and Intersexual Searching Behavior of Stoneflies (Plecoptera), Figure 59 Patterns of signaling among stoneflies: upper left, ancestral-type signaling duet of Pictetiella expansa; upper right, duet with a diphasic male call of Acroneuria abnormis; lower left, symphonic exchange with grouped male call and grouped-interspersed female answers of Isogenoides zionensis; lower right, signal exchange with a 2-rub male call and female percussion answer of Doroneuria baumanni.

roduction from ancestral percussion to abdomip nal substrate stridulation (rubbing), or in rare cases, body jerking or pushups without touching the substrate (tremulation); or (iv) combinations of these changes. The result in modern arctoperlarian stonefly species is an exciting and highly derived and complex array of signal and duet patterns, each unique to particular species, and in some cases fairly uniform in pattern among particular genera or families. The most specialized male calls involve his rubbing the substrate with a specialized, and probably co-evolved, abdominal knob or hammer. Each rub probably represents a modified and prolonged ancestral percussion stroke, using the knob or hammer that may be uniquely ridged or dimpled. This produces a squeaking sound on resonant substrates. Males of various species produce one to seven rubs, always answered by their females with percussion-produced signals.

Little is known about the searching behaviors of species once duet communication between males and females has been established. Recent studies have established that the vibrational communication definitely functions to reduce the time required for males to find females, and that females can be sexually selective by not answering males that call with abortive calls, or by remaining stationary only for some specified time that allows a more fit drummingsearching male to find her. Males generally search by triangulation during duetting with females on flat surfaces. On naturally branched surfaces, such as live or dead plant stems, a male progressively calls on the main stem and on each branch just beyond each bifurcation toward an answering female, effectively determining whether her answering vibrational signal comes from in front or behind him, and therefore whether she is out on that branch or on a branch further away on the main stem. In species that use tremulation, males fly and land on riparian shrubs

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Dry Bark Beetles

and call on leaves; if a female sitting on another leaf responds, he moves toward her, testing leaf by leaf just beyond each petiole junction. Females in this case move to the petiole-leaf junction and become stationary, effectively insuring that once the male finds her correct leaf location, he does not have to search the entire leaf surface to finally make contact with her. This can be described as a “fly-tremulate-search” pattern. All stonefly species that have been studied appear to utilize an initial and specific type of sexual encounter site for initial aggregation of the sexes. This is followed by a ranging search with males intermittently calling for females, then beginning a more localized and oriented search once females answer with signals that reveal her location. Mating of stoneflies ensues almost immediately after males find females; no elaborate courtship behaviors have been discovered.  Vibrational Communication  Acoustic Communication in Insects

References Stewart KW, Maketon M (1991) Structures used by nearctic stoneflies (Plecoptera) for drumming, and their relationship to behavioral pattern diversity. Aquat Insects 13:33–53 Stewart KW (1994) Theoretical considerations of mate finding and other adult behaviors of Plecoptera. Aquat Insects 16:95–104 Stewart KW (1997) Vibrational communication in insects, epitome in the language of stoneflies? Am Entomol 43:81–91 Stewart KW (2001) Vibrational communication (drumming) and mate-searching behavior of stoneflies (Plecoptera); evolutionary considerations. In: Dominguez E (ed) Trends in research in Ephemeroptera and Plecoptera. Kluwer Academic/Plenum Publishers, Dordrecht, The Netherlands, pp 217–225 Zeigler DD, Stewart KW (1977) Drumming behavior of eleven Nearctic stonefly (Plecoptera) species. Ann Entomol Soc Am 70:495–505

Dry Bark Beetles Members of the family Bothrideridae (order Coleoptera).  Beetles

Dry-Fungus Beetles Members of the family Sphindidae (order Coleoptera).  Beetles

Dryinidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

Dryopidae A family of beetles (order Coleoptera). They commonly are known as long-toed water beetles.  Beetles

Drywood Termites A group of termites in the family Kalotermitidae known to attack dry wood that is not in contact with the soil. (contrast with dampwood and subterranean termites)  Termites

dsDNA  Double stranded DNA

Dubas Bug (Old World Date Bug), Ommatissus lybicus Bergerin (Tropiduchidae: Hemiptera) Yousif Aldryhim King Saud University, Riyadh, Saudi Arabia The Dubas bug or Old World date bug feeds on the leaves of the date palm trees, Phoenix dactyifera, in Iraq, Iran, Saudi Arabia, Bahrain, Oman, Egypt, Lybia, Algeria and Trinidad. It is closely related to Ommatissus binotatus DeBerg, which attacks the wild palm, Chamaerops humilis, in

Dubas Bug (Old World Date Bug), Ommatissus lybicus Bergerin (Tropiduchidae: Hemiptera)

North Africa, Spain, and in the southeastern region of the former Soviet Union.

Description The adult female is about 5–6 mm in length, yellowish green and has up to ten dark spots on the head and 7th and 8th abdominal segments. The adult male is about 3–3.5 mm in length. It differs from the female by the absence of the dark spots on the 7th and 8th abdominal segments, the more tapered abdomen and the greater length of the wings relative to the abdomen. The eggs are elongated, cucumber like and about 0.5–0.8 mm in length. They are bright green in color at deposition, then change to yellowish white and later to bright yellow. The nymphs are bright brown and have dark stripes on the dorsal surface of the thorax and abdomen. The tip of the abdomen terminates in an extension or cauda-like structure and has 16 white waxy filaments, each about 3 mm long. The eyes are red and the nymphs can walk and jump up to 60 cm.

Symptoms and Economical Importance The adults and nymphs feed on the sap of the leaflets and midribs of the date palm frond. At high levels of infestation, Dubas bugs attack the fruit stalks and the fruit. Dubas excrete heavy honeydew and dust sticks to it. The infested leaflets become light green and yellow green in color. Necrotic areas (damage) are noticeable on the infested fronds and are caused by egg-laying. Dubas bug is an occasional pest, meaning that it becomes an important pest for a season or two, followed by less damage in the coming seasons. At high levels of infestation, 50% of the date yield may be lost. Dubas bugs may cause indirect damage to crops that are grown under the infested date palm trees due to the dripping of honeydew.

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Biology Dubas bugs have two generations per year, a spring and autumn generation. Dubas bugs hibernate in the winter and aestivates in the summer as eggs in the axial veins and midrib of the date palm fronds. A female deposits an average of 100 eggs during its life-span. Eggs hatch in April and in September in the spring and autumn generations, respectively. Newly hatched nymphs disperse into the frond folds or onto young fruits, and commence feeding. The nymphs pass through five instars. Nymphal duration is about 6 weeks. The adults can fly, and their habitat is the same as the nymphs.

Control A small chalcidiod wasp parasitizes the eggs of the Dubas bug. The larvae of lacewings also prey on the Dubas nymphs and adults. The adult beetles of three species of the coccinellids attack the nymphs and adults of the Dubas bugs. Certain cultural practices help to keep the trees healthy. Good drainage and windbreaks help to reduce injury by this pest. Systemic insecticides can be used at high levels of infestation. Aerial application of insecticides is most useful for wide-ranging infestations, or when the height of the date palm trees makes it difficult to apply chemical pesticides from the ground. However, aerial application increases scale insect infestations because the pesticide kills their natural enemies.

References Talhouk N (1984) The most common agricultural pests in Saudi Arabia. Ministry of Agriculture and Water, 121 pp (in Arabic) Hussain A (1974) Pests of date palm trees and dates in Iraq. Baghdad University, 190 pp (in Arabic) Hammad SM, Kadous AA (1989) Studies on the biology and ecology of date palm pests in the eastern Province of

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Dudgeon Carpenterworm Moths (Lepidoptera: Dudgeoneidae)

Saudi Arabia. Research Grants Program, KACST, Riyadh, Technical Report No. 25, 142 pp Kranz JH, Schmutter, Koch W (eds) (1977) Diseases, pests and weeds in tropical crops. Verlage Paul Parey, Berlin

Dudgeon Carpenterworm Moths (Lepidoptera: Dudgeoneidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Dudgeon carpenterworm moths, family Dudgeoneidae, includes only six species in the single genus Dudgeonea, with two species from Africa, one from India, and three from Australia. The family is in the superfamily Cossoidea (series Cossiformes) in the section Cossina, subsection Cossina, of the division Ditrysia. Adults medium size (28–72 mm wingspan), with head somewhat rough-scaled; haustellum absent; labial palpi upcurved; maxillary palpi 3-segmented; antennae pectinate (rarely bipectinate). Body robust; abdomen with small tympanal organs. Wings elongated; forewings rounded at termen (Fig. 60). Maculation dark with golden or light spots; hindwing pale. Adults nocturnal as far as is known. Larvae mostly unknown, but one Australian species is a stem borer on Rubiaceae. The family and genus

Dudgeon Carpenterworm Moths (Lepidoptera: Dudgeoneidae), Figure 60 Example of dudgeon carpenterworm moths (Dudgeoneidae), Dudgeonea leucosticta Hampson from South Africa.

udgeonea are named after the British lepidopterD ist Gerald C. Dudgeon (18??-1930), who published mostly on Indian Lepidoptera.

References *Holloway JD (1986) Family Dudgeoneidae. In: Moths of Borneo, 1:41, pl 4. Malayan Nature Society (Malayan Nature Journal 40:41, pl 4), Kuala Lumpur Roepke W (1955) Notes and description of Cossidae from New Guinea (Lepidotera: Heterocera). Trans R Entomol Soc Lond 107:281–288, 2 pl [part: Dudgeonea] Schulze CH, Fiedler K (1996) First record of the family Dudgeoneidae (Lepidoptera, Ditrysia) for Borneo. Tinea 15:74–77

Dudgeoneidae A family of moths (order Lepidoptera). They also are known as Dudgeon carpenterworm moths.  Dudgeon Carpenterworm Moths  Butterflies and Moths

Dudich, Endre George Hangay Narrabeen, NSW, Australia Endre Dudich was born on the March 20, 1895 at Nagysallü, in Bars Shire, Hungary. At an early age his interest was influenced by his father, who was a medical practitioner and liked zoology. He attended college in Esztergom (Northern Hungary) continuing his studies at the Pázmány Péter University of Science. During World War I, his university studies were interrupted with three and a half years of military service, during which he served on the front. He received his diploma in 1920 and in 1922 the doctorate. Due to the friendship and encouragement of Elemér Bokor, he focused his research on the Coleoptera and the invertebrate fauna of caves. However, one of his main achievements was a

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major work on zoological taxonomy (Rendszeres állattan. Pécs, 1927), which has established him as a leading scientist of that field. In 1934 he was commissioned to establish the Institute of Zoological Taxonomy. He worked in this institute until his death. Endre Dudich pioneered modern taxonomical and zoogeographical research in Hungary and created the country’s first underground research station in the Baradla Cave (northeastern Hungary). He became a leading expert in the biological research of caves and from 1958 until 1970 he directed scientific work at the Danube Research Station at Alsü Göd, north of Budapest. He kept working until his death on the February 5, 1971.

References Balogh J (1971) Endre Dudich. Magyar Tudomány, Budapest, 6 LOKSA I (1971) Dr Dudich Endre. Karszt és Barlang. Budapest, 1 Soüs Á (1972) Megemlékezés dr. Dudich Endrérôl. Állattani Közlemények, Budapest

Dufour, Léon Jean Marie Léon Dufour was born at Saint-Sever, France, on April 11, 1780. He was a veteran of the French army, with service in Spain during the Napoleonic wars. He married and had children. His publications spanned the years 1811–1864, reported work on the anatomy, behavior, development, physiology, and taxonomy of filarial nematodes, earthworms, crustaceans, arachnids, and insects (Orthoptera, Coleoptera, Diptera, and Hymenoptera), and numbered over 230. He was awarded France’s highest medal, as an officer of the Legion d’ Honneur. He died on April 18, 1865.

References Grenier A (1865) [Mort de M. Dufour]. Bulletin de la Société Entomologique de France (1865): xx–xxi Laboulbène A (1865) Paroles d’ adieu adressées a M. Léon Dufour. Annales de la Société Entomologique de France 4(5):214–215

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Laboulbène A (1865) Travaux d’ entomologie publiés de 1811 à 1864 par M. Léon Dufour. Annales de la Société Entomologique de France 4(5):216–252

Dufour‘s Gland A gland on the posterior part of the abdomen in female Hymenoptera that is a source of various pheromones.

Dulosis A parasitic relationship wherein a parasitic (dulotic) ant species raids the nest of another species, captures brood, and raises them as slaves.

Dung Beetles Members of the subfamily Scarabaeinae, family Scarabaeidae (order Coleoptera).  Beetles

Dung Flies Members of the family Sarcophagidae (order Diptera).  Flies

Dunnage Wood used to package or support cargo. Wood crates and packing are an important entry route for invading wood-boring insects. However, wood crates can also be a harborage for egg masses and pupae of arthropods, and all motile stages of snails, facilitating movement of pests across international boundaries.  Regulatory Entomology  Risk Analysis (Assessment)  Invasive Species

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Duponchel, Philogène August-Joseph

Duponchel, Philogène August-Joseph Philogène Duponchel was born in France toward the end of 1774. At the age of 16 he was in the French army during the Revolutionary War, after his parents fled from France. He became a bureau chief in the war administration. He was not discharged from the army until 1816, but he used his free time for entomological studies. He married and had two children. His interest was especially in Lepidoptera. He was a friend of Latreille, Dejean, and Duméril, and was guided in his studies by them. He was a co-founder of the Société Entomologique Française, at one time a president of it, and held other roles in it at various times. With Chevrolat as co-author, he contributed to d’ Orbigny’s (1842) “Dictionnaire universel d’ histoire naturelle…” He died in Paris on January 10, 1846.

References Guérin-Méneville FE (1846) Discours prononcé par M. Guérin-Méneville aux funerailles de M. Duponchel. Bulletin de la Société entomologique de France (2)4:iv–vi Duméril C (1846) Allocution de M. Constant Duméril sur la tombe de M. Duponchel. Bulletin de la Société entomologique de France 2(4):vii–viii

Dust A dry pesticide formulation consisting of finely divided powder, used without additional dilution, and normally applied by a stream of air.

Duster Equipment used to apply a dust formulation of pesticide.

Dustywings Members of the family Coniopterygidae (order Neuroptera).  Lacewings, Antlions and Mantidflies

Dutch Elm Disease This fungal disease of elm trees is transmitted by bark beetles.  Transmission of Plant Diseases by Insects

Dyar, Harrison Grey Harrison Dyar was born in New York on February 14, 1866. He obtained a B.S. in chemistry from Massachusetts Institute of Technology in 1889, and an A.M. and Ph.D. From Columbia University in 1894 and 1895, respectively. His Ph.D. research was “On certain bacteria from the area of New York City,” but before that he had published (in 1894) “A classification of lepidopterous larvae,” and for that evidence of training and interest, he was offered in 1897 an unpaid position as Custodian of Lepidoptera at the U.S. National Museum. He occupied the position for the next 31 years, publishing constantly on Lepidoptera, and receiving no financial compensation for his work: he was independently wealthy. However, his other interest was in nematocerous Diptera, and he studied Culicidae, Simuliidae, Psychodidae, and Chaoboridae. With Frederick Knab, he published a four-volume work “The mosquitoes of North and central America” which was initiated as the result of a grant from the Carnegie Institution to L.O. Howard who was another of the authors. “Dyar’s rule” was the result of his studies on the growth of caterpillars, in which he stated that the “width of the head capsule of the larva follows a regular geometric progression in the successive instars.” He has been remembered by some as a

Dytiscidae

cantankerous man who was quick to criticize others. He owned and edited the entomological journal Insecutor Inscitiae Menstruus, which was published from 1913 to 1927. He died on January 21, 1929.

References Epstein ME, Henson PM (1992) Digging for Dyar. Am Entomol 38:148–169 *Mallis A (1971) Harrison Grey Dyar. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 323–326

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Dyar‘s Rule The width of the insect head capsule increases by a factor of 1.2–1.4 from one molt to another.

Dytiscidae A family of beetles (order Coleoptera). They commonly are known as predaceous diving beetles.  Beetles

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Ear Tag A popular method of distributing insecticide to livestock. The insecticide is impregnated in a plastic dispenser, which is fastened to the ear of an animal. The dispenser releases the insecticide slowly, and the animal, by moving its head, contacts other parts of its body and the body of other animals, resulting it widespread distribution of the insecticide.

Earth-Boring Dung Beetles Members of the family Geotrupidae (order Coleoptera).  Beetles

Earwigflies (Mecoptera: Meropeidae) James C. Dunford, Louis A. Somma, David Serrano University of Florida, Gainesville, FL, USA There are two known extant members of the family Meropeidae worldwide. The North American earwigfly, Merope tuber Newman, is found in eastern North America, and the Australian earwigfly, Austromerope poultoni Killington, is found in Western Australia. One additional species, Boreomerope antiqua Novokschonov, is an extinct, fossil meropeid known from the Middle Jurassic of

Siberia. The vernacular name for earwigflies is derived from the male genital claspers that superficially resemble the forficulate cerci of earwigs (Dermaptera). Meropeid genera are hypothetically closely related to Eomeropidae, probably basal to more derived mecopterans (e.g., scorpionflies, Panorpa spp.), and could provide a clue to the phylogenetic link between Mecoptera and Siphonaptera. Meropeid larval and pupal stages remain undescribed and may be an important link in better understanding the evolution of advanced holometabolous insects. The specific epithet for the North American earwigfly, tuber, Latin for swelling, knob, hump or protuberance, is a reference to the jugum, a distinct lobe on the basal posterior margin of the forewings. The jugum of M. tuber was originally described as a “tubere” and “knob” by Newman in 1838, and is used to produce audible stridulations by rubbing against a ridged portion of the thorax, or could function as part of a wing interlocking mechanism. The Australian earwigfly was named in honor of E.B. Poulton, who first collected it in southwest Western Australia in 1914. There are several morphological features that separate the two extant meropeid genera, namely wing venation and the presence of an apical spine on the basal segment of the male genital claspers of A. poultoni. Austromerope adults also bear a lobe or jugum on the base of each forewing but they are much smaller than the juga on Merope.

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Earwigflies (Mecoptera: Meropeidae)

At present, meropeid immature stages have not been described, and much of their general biology remains unknown. Merope tuber (Fig. 1a, b) adults are apparently nocturnally active and have been recorded primarily from deciduous, mesic woodlands, usually near streams. Seasonal records reported for M. tuber include dates encompassing early May through late November. For more than 150 years M. tuber were considered rare, but recent collection methods (i.e., pitfall, light, and various flight traps) reveal that this secretive mecopteran is more abundant than what was once thought. Published records of Merope previous to 1954 were for localities in or east of the Appalachian Mountains. Since that time, specimens have been collected increasingly farther west. Through 1993, the recorded range of M. tuber was from southeastern Canada to northern Georgia, west to Kansas, Minnesota and eastern Iowa, largely restricted to environmental conditions similar to

those known along the Appalachian range and eastern mesic forests. However, more recent collection records indicate that M. tuber is also found further south (e.g., Alabama and Florida) suggesting that it may have found refuge in some of these disjunct areas during glacial advances. Austromerope poultoni have been (Fig. 1c) collected in light and pitfall traps containing alcohol preservatives and taken in a wide variety of somewhat xeric habitat types, including Jarrah and Karri forests, Wandoo woodland and heath. Seasonality records for adult A. poultoni include a range of dates between July (midwinter) and December (early summer). Adults likely live within or below the litter layers in these habitats and they are not commonly encountered, but like M. tuber have recently been collected in greater numbers due to more thorough sampling efforts.  Scorpionflies

Earwigflies (Mecoptera: Meropeidae), Figure 1 (a) Female Merope tuber (dorsal view); North Carolina, USA; body length 11 mm (image by David Serrano); (b) Male Merope tuber (ventral view); Tennessee, USA; body length (excluding claspers) 8.5 mm (image by David Serrano); (c) Male Austromerope poultoni (ventral view); NE of Collie, Western Australia; body length (excluding claspers) 7.7 mm (image by Allan Wills)

Earwigflies (Mecoptera: Meropeidae)

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Earwigflies (Mecoptera: Meropeidae), Figure 2 (a) Scanning electron micrograph of M erope tuber head; Tennessee, USA (image by Louis A. Somma); (b) Jugum (ventral view) located on basal posterior margin of Merope tuber forewing; Wisconsin, USA (image by Louis A. Somma); (c) Ridges located on Merope tuber thorax (dorsal view); Wisconsin, USA (image by Louis A. Somma).

References

Byers GW (1993) Autumnal Mecoptera of southeastern

Abbott I, Burbidge T, Wills A (2007) Austromerope poultoni

Dunford JC, Kovarik PW, Somma LA, Serrano D (2007) First

(Insecta, Mecoptera) in south-west Western Australia:

state records for Merope tuber (Mecoptera: Meropeidae)

occurrence, modelled geographical distribution, and

in Florida and biogeographical implications. Fla

phenology. J R Soc West Aust 90:97–106

Entomol 90:581–584

United States. Univ Kansas Sci Bull 55:57–96

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Earwigs (Dermaptera)

Faithfull MJ, Majer JD, Postle AC (1985) Some notes on the occurrence and seasonality of Austromerope poultoni Killington (Mecoptera) in Western Australia. Aust Entomol Mag 12:57–60 Fitch A (1872) Fourteenth report on the noxious, beneficial, and other insects of the State of New York. Trans N Y State Agric Soc 1870 30:355–381 Grimaldi DA, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge, UK, 755 pp Novokschonov V(G) (1995) Der älteste Vertreter der Merop eidae (Mecoptera, Insecta). Paläeontologische Zeitschrift (Stuttgart) 69:149–152 Richards AG (1965) The proventriculus of adult Mecoptera and Siphonaptera. Entomol News 76:253–256 Sanborne PM (1982) Stridulation in Merope tuber (Mecoptera: Meropeidae). Can Entomol 114:177–180 Whiting MF (2002) Phylogeny of the holometabolous insect orders: molecular evidence. Zool Scr 31:3–15

Earwigs (Dermaptera) Earwigs are, in some respects, one of the most readily recognized orders of insects. However, this applies only to the “typical” earwigs bearing forcepslike cerci. There are some animal-parasitic groups that lack the forceps-like cerci. The order name is based on the Greek words derma (skin) and pteron (wing).

Classification

Earwigs usually are uniform black or brown, but some are striped. The antennae are moderately long, consisting of 6–15 segments. They may bear two pairs of wings, or be wingless. The forewings (when wings are present) are modified into short, thickened covers (called tegmina) for the functional hind wings. The hind wings fold beneath the tegmina and are unusually oval, with veins radiating from the central region of the wing. The legs are moderately short and unspecialized. The tarsi consist of three segments. Both males and females bear cerci. The cerci are undivided, and in most species are modified into heavily sclerotized forceps-like structures called, appropriately enough, forceps (Fig. 3). The shape of the cerci can be used to distinguish species, sex, and sometimes age. Metamorphosis is incomplete. Earwigs are predominantly tropical insects.

Labrum Clypeus

Tegmen Wing tip

There are three suborders of earwigs, but two are very small. Nearly all the 1,500 known species occur in a single suborder, Forficulina. Suborder Hemimerina consists of ten blind, wingless species that live on giant rats in tropical Africa. They have small filiform cerci. Suborder Arixenina consists of five species that live on bats in Southeast Asia. Similarly, they are nearly blind, wingless, and have straight cerci. Forceps

Characteristics Earwigs are elongate insects with biting/chewing mouthparts. They range in size from 4 to 80 mm.

Earwigs (Dermaptera), Figure 3 Diagram of an earwig, shown dorsally.

Eastern Equine Encephalitis

Biology Earwigs tend to be nocturnal, hiding during daylight in soil, leaf litter, under bark, and other cryptic, humid locations. Most are omnivorous, but a few are predatory or live on vertebrates as ectoparasites. The common name “earwig” likely is derived from the tendency of earwigs to crawl into dark crevices including, perhaps, a human ear. This rarely, if ever, occurs. Females earwigs display some elements of sociality, specifically maternal care for eggs and young earwigs. The female protects and cleans the eggs and young from her mate as well as other potential predators, but the nymphs disperse when about half grown. There are 4–5 nymphal instars. They nymphs are hard to distinguish from the wingless adults except by size. The cerci also are not completely developed, tending to be less curved than as adults. However, females display a similar tendency of having less curved cerci, relative to males, so the age of earwigs can be difficult to ascertain.

References Arnett RH Jr (2000) American insects, 2nd edn. CRC Press, Boca Raton, FL, 1003 pp Brindle A (1987) Order Dermaptera. In: Stehr FW (ed) Immature insects, vol 2. Kendall/Hunt, Dubuque, Iowa, pp 171–178 Steinmann H (1989) World catalog of Dermaptera. Kluwer Academic Publishers, Dordrecht, 933 pp

East Coast Fever This is a tick-borne protozoan disease of cattle.  Piroplasmosis

Eastern Equine Encephalitis C. Roxanne Rutledge University of Florida, Florida Medical Entomology Lab, Vero Beach, FL, USA Eastern equine encephalitis (also known as EEE, eastern encephalitis, and eastern equine

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e ncephalomyelitis) was first recognized in North America in horses from Virginia, Delaware, New Jersey, and Maryland in 1933. The virus that causes EEE was first isolated from brains of animals in 1933 and recovered from human central nervous system (CNS) tissue in 1938. The virus is transmitted through the bite of an infected mosquito. Infection in mosquitoes, wild birds, horses, and humans is uncommon, but causes a high mortality in susceptible hosts. Infection with the EEE virus can cause a range of CNS complications from mild or none at all, to severe encephalitis (swelling of the brain). EEE is sometimes referred to as eastern equine encephalomyelitis, meaning swelling of the brain and spinal cord. Vertebrate hosts that are most susceptible to severe complications include humans, horses, and some exotic birds. EEE virus has been isolated in eastern North America, eastern Canada, Central and South America, Jamaica, Trinidad and Tobago, Cuba, Haiti, and Dominican Republic.

Virus Eastern equine encephalitis virus is an RNA Alphavirus in the family Togoviridae. The virus is transmitted to mammalian hosts by mosquitoes. Avian hosts may acquire the virus from mosquitoes and in some instances, without the mosquito vector. In pheasants, the virus can spread from one bird to another through cannibalism and pecking.

Mosquito Vectors In the enzootic cycle (mosquito-bird-mosquito, present in the animal community at all times), the mosquito vector of EEE virus in the eastern United States is Culiseta melanura, a mosquito that prefers to feed on birds. Ochlerotatus (formerly Aedes) sollicitans, a salt-marsh mosquito, may be the main vector during outbreaks in humans and horses, as it will feed on birds, humans, and horses.

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Studies suggest that Coquilletidia perturbans, Ochlerotatus (formerly Aedes) canadensis, and Aedes vexans may be important vectors in southeastern Massachusetts. In tropical countries, the primary mosquito vectors are Culex nigripalpus, Culex taeniopus, and Ochlerotatus (formerly Aedes) taeniorhynchus.

Bird Hosts Birds naturally infected with EEE virus include ring necked pheasants, pigeons, chukar partridge, Pekin ducks, turkeys, a number of passerines, owls, whooping cranes and shore birds. Antibodies to EEE virus have been found in some of these bird hosts, and EEE virus has been isolated from others.

Transmission Cycle Eastern equine encephalitis virus is an arbovirus (arthropod-borne virus) that is passed from one host to another through the bite of an infected mosquito. In the eastern United States, the EEE virus circulates between birds and mosquitoes in freshwater swamps. The mosquito acquires the virus from an infected bird. Wild birds may have a viremia (the occurrence of viruses within the peripheral bloodstream of the host) without the signs of infection seen in other animals. After an incubation period in the mosquito, other hosts may then be infected when the female mosquito takes a blood meal. Mosquitoes that feed strictly on birds will maintain a local enzootic cycle of EEE. Mosquitoes that feed on a wider range of hosts may infect humans and horses, which serve as a dead-end for the virus. Neither infected humans nor horses have enough circulating virus to infect mosquitoes. The virus has an incubation period of 4–10 days once it has entered a previously uninfected vertebrate host. During the incubation period, the virus may invade the spinal cord and brain. Infection can potentially lead to death of the vertebrate host.

Disease in Humans Symptoms in humans can be mild, flu-like symptoms to severe encephalitis manifested by fever, headache, and nausea followed by drowsiness, convulsions, and coma. The case fatality rate is 35–65% of clinical cases. Some humans who are infected with the virus develop neutralizing antibodies but do not develop clinical illness. In children under 5 who survive the disease, mental retardation, convulsions, and paralysis often are observed. Estimated total costs associated with each human case is from $21,000–$3 million for severe infections. There is no human vaccine for EEE virus. There is no specific treatment for eastern equine encephalitis. This combined with the lack of a human vaccine emphasizes the importance of personal protection from mosquito bites. Personal protection using mosquito repellent is the best method for preventing infection.

Disease in Horses The disease in horses is often biphasic with fever starting 18–24 h after infection that lasts about 1 day. Four to six days post-infection, fever starts again and lasts from 1 to 4 days and nervous system signs appear: depression, head close to the ground, flaccid lips, weight loss, and a legs-apart stance. Death occurs within 5–10 days post-infection and the mortality rate is 75–90% with brain damage occurring in animals that survive. There is no specific treatment for EEE in horses. The method of prevention in horses is in the form of an effective horse vaccine that is available to all horse owners.

Disease in Birds Pheasants exhibit signs including fever, depression, diarrhea, ataxia, tremors, and paralysis of one or both extremities. Initially, infections in


pheasants occur from mosquito bites. Later on, the disease can be spread from bird to bird through pecking and cannibalism. Emus are susceptible to EEE virus and exhibit acute onset of depression, profuse hemorrhagic diarrhea, anorexia and ataxia. Terminally, these birds show extreme exhaustion, hemorrhagic diarrhea and vomiting. Infection in emus causes moderate morbidity and high mortality. Treatment is supportive only, and there is some degree of immunity provided with the equine bi- or tri-valent vaccines.

Detection/Diagnosis In humans, diagnosis of EEE is based on signs of encephalitis and virus isolation from CNS tissues or blood. A confirmed case of EEE includes the following: a clinically compatible disease (febrile illness, encephalitis) and onset of illness during a period when arbovirus transmission is likely to occur and either a stable elevated antibody titer to an arbovirus or specific IgM (antibody formed early in an immune response; it is a less persistent antibody that indicates recent or chronic infections) antibody in serum, and either a fourfold or greater change in serum antibody titer, viral isolation from tissue, blood or spinal fluid, or specific IgM antibody in the cerebrospinal fluid. Diagnosis of EEE in horses includes a history of the animal, physical exam, and lab tests to analyze blood or cerebrospinal fluid for antibodies or virus. Since the disease progresses rapidly in horses, EEE confirmation is usually made after the horse’ s death. At this point, examination of brain tissue is required to confirm brain lesions or attempt virus isolation.

Epidemics and Epizootics Massachusetts experienced an epidemic of EEE in 1938 with 38 human cases (74% mortality) and 248 horse cases (90% were fatal). In 1947, an

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epidemic occurred in Louisiana that killed 90% of the approximately 14,000 infected horses and 9 of 15 humans with the virus died. The Dominican Republic reported 9 deaths among 13 infected humans and 516 horse cases in 1948–1949. An accurate mortality rate in horses during that epidemic is not obtainable as all sick animals were ordered killed when the cause of the epizootic was determined. From 1939 to 1954, there were 27 reported epizootics in pheasants in New Jersey. An epizootic occurred in Panama in 1973 causing 40 deaths in 100 infected horses. The Centers for Disease Control reports 153 confirmed human cases spread throughout 20 states from 1964 to 1997. Fifty of the human cases occurred in Florida (33%). Small outbreaks and sporadic cases in humans continue to occur in various locations throughout the known transmission zone. The numbers of EEE horse cases are probably severely under-reported. The United States Department of Agriculture reported 26,468 cases of encephalitis in horses from 1956 to 1970. Of the mere 2,620 that could be specifically diagnosed, 605 cases were due to the EEE virus. Many horses are euthanized before a confirmation can be made. Because brain tissue is required for confirmation of EEE in horses, some horse owners are reluctant to provide the necessary tissues or to incur the expense of the laboratory confirmation.

Future Outlook EEE virus transmission likely will continue in the known transmission zones. There will be some years with many horse and human cases. As humans and animals move into EEE endemic areas near marshes and swamps, and natural wetlands are preserved, contact with infected mosquitoes is likely to continue and perhaps expand the areas of transmission. The susceptibility to EEE virus for many exotic animals is unknown; importation of such animals into EEE virus transmission zones may also subject them to the levels

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Eastern Lubber Grasshopper, Romalea microptera (Beauvois) (Orthoptera: Acrididae)

of mortality seen in emus, pheasants, and horses. Prevention of EEE through the use of vaccines in animals and personal protection in humans is increasingly more important as source reduction of mosquito larval habitats is discouraged or illegal in natural wetlands and mosquito control professionals have fewer methods for controlling the vectors of EEE virus.

References Eldridge BF, Edman JD (eds) (2000) Medical entomology. A textbook on public health and veterinary problems caused by arthropods. Kluwer Academic Publishers, Dordrecht, The Netherlands Pedro NA, Szyfres B (1987) Zoonoses and communicable diseases common to man and animals, 2nd ed, Scientific Publication No. 503. Pan American Health Organization, Washington, DC Morris CD (1992) Eastern equine encephalitis. J Fla Mosq Cont Assoc 63:23–34 Rivers TM, Horsefall FL Jr (eds) (1959) Viral and rickettsial infections of man, 3rd edn. J.B. Lippincott Company, Philadelphia, PA

Eastern Lubber Grasshopper, Romalea microptera (Beauvois) (Orthoptera: Acrididae) John L. Capinera University of Florida, Gainesville, FL, USA This grasshopper is common in the southeastern United States from North Carolina to eastern Texas, including the entire peninsula of Florida. It is common in many areas of the southeastern USA, and well known to the populace due to its large size and use in biology classrooms for dissection exercises. Unfortunately, the scientific community uses two different scientific names for the same species, and R. microptera is also called R. guttata (Houttuyn). The latter is probably the correct name, but because the former designation was used for many years, this proposed “correction” is introducing unnecessary confusion.

Life History There is one generation per year, with the egg stage overwintering. These grasshoppers are long-lived, and either nymphs or adults are present throughout most of the year in the southern portions of Florida. In northern Florida and along the Gulf Coast they may be found from March–April to about October–November. The eggs of lubber grasshoppers are yellowish or brown in color. They are elongate elliptical in shape and measure about 9.5 mm in length and 2.5 mm in width. The are laid in neatly arranged clusters, or pods, which consist of rows of eggs positioned parallel to one another, and held together by a secretion. Normally there are 30–50 eggs in each pod. Ovipositing females are reported to prefer mixed broadleaf tree-pine habitats with intermediate soil moisture levels, avoiding both lowland, moist, compact soil and upland, dry, sandy soil. The female deposits the pod in the soil at a depth of 3–5 cm and closes the oviposition hole with a frothy secretion or plug. The plug allows the young grasshoppers easy access to the soil surface when they hatch. Duration of the egg stage is 6–8 months. Young nymphs (Fig. 4) are highly gregarious, and remain gregarious through most of the nymphal period, though the intensity dissipates with time. Normally there are five instars, though occasionally six instars occur. The nymphs are mostly black with a narrow median yellow stripe along the pronotum and abdomen, along the edges of the pronotum, and on the lower side of the abdomen. The legs are well marked with red. Their color pattern is distinctly different from the adult stage, and so the nymphs commonly are mistaken for a different species than the adult form. The early instars can be distinguished by a combination of body size, the number of antennal segments, and the form of the developing wings. The nymphs measure about 10–12, 16–20, 22–25, 30–40, and 35–45 mm in length during instars 1–5, respectively. Antennal segments,

Eastern Lubber Grasshopper, Romalea microptera (Beauvois) (Orthoptera: Acrididae)

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Eastern Lubber Grasshopper, Romalea microptera (Beauvois) (Orthoptera: Acrididae), Figure 4 Adult of eastern lubber grasshopper, Romalea microptera (Beauvois).

which can be difficult to distinguish even with magnification, number 12, 14–16, 16–18, 20, and 20 per antenna during instars 1–5, respectively. The shape of the plates immediately behind the pronotum changes slightly with each molt. During the first instar the ventral surface is broadly rounded; during the second instar the ventral edges begin to narrow slightly and point slightly posteriorly, and also acquire slight indication of venation; during the third instar the ventral edges of the plates are markedly elongate, point strongly posteriorly, and the veins are pronounced. At the molt to the fourth instar the orientation of the small, developing wings shifts from pointing downward to pointing upward and posteriorly. In instar four the small forewings and hind wings are discrete and do not overlap, though the forewings may be completely or partly hidden beneath the pronotum. In instar five, the slightly larger wings overlap, appearing to be but a single pair of wings. Nymphs can complete instars 1–4 in about 7 days each, with the terminal instar requiring 10 days. However, under cool conditions 60 days are required for nymphal development. Adults often are colorful, but the color pattern varies. Often the adult eastern lubber normally is mostly yellow or tawny (Fig. 5), with black on the distal portion of the antennae, on the pronotum, and on the abdominal segments. The forewings extend two-thirds to three-fourths the length of the abdomen. The hind wings are short and incapable of providing lift for flight. The forewings tend to be pink or rose in color

Eastern Lubber Grasshopper, Romalea microptera (Beauvois) (Orthoptera: Acrididae), Figure 5 Nymph of eastern lubber grasshopper, Romalea microptera (Beauvois).

centrally whereas the hind wings are entirely rose in color. Darker forms of this species also exist, wherein the yellow color becomes the minor rather than the major color component, and in northern Florida a predominantly black form is sometimes found. Adults attain a large size, males measuring 43–55 mm in length and females often measuring 50–70 mm, sometimes 90 mm. Both sexes stridulate by rubbing the forewing against the hind wing. When alarmed, lubbers will spread their wings, hiss, and secrete foul-smelling froth from their spiracles. They can expel a fine spray of toxic chemicals for a distance of 15 cm. The chemical discharge from the tracheal system is believed to be an anti-predator defense, and to consist of chemicals both synthesized and sequestered from the diet. Vertebrate, but not invertebrate, predators are affected. Eastern lubber grasshopper has a broad host range. At least 26 species from 15 plant families containing shrubs, herbs, broadleaf weeds, and

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Ecdysial Line

grasses are eaten. A preference has been observed for pokeweed, Phytolaca americana; tread-softly, Cnidoscolus stimmulosus; pickerel weed, Pontederia cordata; lizard’s tail, Saururus sp.; sedge, Cyperus; and arrowhead, Sagittaria spp. Though its preferred habitat seems to be low, wet areas in pastures and woods and along ditches, lubbers disperse long distances during the nymphal period. They are gregarious and flightless, their migrations sometimes bringing large numbers into contact with crops where they damage vegetables, fruit trees, and ornamental plants. Lubbers seemingly display little preference among vegetable crops, feeding widely on whatever is available. In choice tests they favor broccoli, Brussels sprout, carrot, pea, and squash relative to other common vegetables. Under field conditions, they seem to display preference for corn, cowpea, and peanut. Also, they seek out and defoliate amaryllis, Amazon lily, crinum, narcissus, and related plants in flower gardens. In Florida, they sometimes damage young citrus trees. The natural enemies of lubber grasshoppers are poorly documented. Vertebrate predators such as birds and lizards learn to avoid these insects due to the production of toxic secretions. Naïve vertebrates gag, regurgitate, and sometimes die following consumption of lubbers. However, loggerhead shrikes, Lanius ludovicianus Linnaeus, capture and cache lubbers by impaling them on thorns and the barbs of barbed wire fence. After 1–2 days the toxins degrade and the dead lubbers become edible to the shrikes. Undetermined flies and nematodes have been reported from lubbers, and it is possible to infect lubbers experimentally with the grasshopper-infecting nematode Mermis nigrescens.

Damage Lubber grasshoppers are defoliators, consuming the leaf tissue of numerous plants. They climb readily, and because they are gregarious they can completely strip foliage from plants. More

c ommonly, however, they will eat irregular holes in vegetation and then move on to another leaf or plant.

Management Management practices are not well developed. Insecticides applied to the foliage or directly to the grasshopper will prove lethal. However, due to their large size they often prove difficult to kill. Insecticide treatment is more effective for young grasshoppers. Because they are dispersive, and may continue to invade an area even after it is treated with insecticide, it is difficult to afford protection to plants.  Grasshopper Pests in North America  Grasshoppers and Locusts as Agricultural Pests  Grasshoppers, Katydids, and Crickets (Orthoptera)

References Capinera JL, Scott RD, Walker TJ (2004) Field guide to the grasshoppers, katydids, and crickets of the United States. Cornell University Press, Ithaca, NY, 249 pp Hunter-Jones P (1967) The life-history of the eastern lubber grasshopper, Romalea microptera (Beauvois), (Orthoptera: Acrididae) under laboratory conditions. Proc R Entomol Soc London (A) 42:18–24 Jones CG, Whitman DW, Compton SJ, Silk PJ, Blum MS (1989) Reduction in diet breadth results in sequestration of plant chemicals and increases efficacy of chemical defense in a generalist grasshopper. J Chem Ecol 15:1811–1822 Rehn JAG, Grant HJ Jr (1961) A monograph of the Orthoptera of North America (north of Mexico), vol 1. Monograph 12, Academy of Natural Sciences of Philadelphia, 257 pp

Ecdysial Line A line of weakness that breaks during molting (ecdysis). This is found at the top of the head capsule, or a nearby area.

Ecdysone Agonists, A Novel Group of Insect Growth Regulators

Ecdysis The shedding of the old cuticle during the molting process.

Ecdysone A steroid hormone secreted by the prothoracic glands and responsible for inducing molting and the sequential expression of stage-specific genes. It is produced from cholesterol.  Endocrine Regulation of Insect Reproduction  Reproduction  Diapause  Metamorphosis

Ecdysone Agonists, A Novel Group of Insect Growth Regulators Guy Smagghe Ghent University, Ghent, Belgium The diacylhydrazines are a novel class of chemically and mechanistically new insect control agents that were discovered and characterized by researchers of the Rohm and Haas Co. (Pennsylvania, USA) in the mid-1980s. The first member of this group was RH-5849 (N-tert-butyl-N’-benzohydrazide) that had interesting foliar and root-systematic insecticide activities against a range of lepidopteran, coleopteran and dipteran pests. More recently, another more commercial analog was introduced, tebufenozide (N-tert-butyl-N’-(4-ethylbenzoyl)3,5-dimethylbenzo-hydrazide; RH-5992; MimicTM, ConfirmTM, RondamTM) that is a more potent and selective foliar caterpillar control agent. In addition, halofenozide (N-tert-butyl-N’-(4-chlorobenzoyl)benzohydrazide; RH-0345; Mach 2TM) that is a more effective soil insecticide for white grub and caterpillar control in turf, and methoxyfenozide (N-tert-butyl-N’-(3-methoxy-o-toluoyl)-3,5xylohydrazide; RH-2485; RunnerTM, IntrepidTM,

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ProdigyTM) exhibits high insecticide efficacy and selectivity against Lepidoptera including Pyralidae, Pieridae, Tortricidae and Noctuidae. In this respect, Rohm and Haas was granted a “Presidential Green Chemistry Award” from the U.S. Government for the discovery of these nonsteroidal ecdysone agonists. Due to the commercial success, screening bioassays were initiated to discover new 20E acting compounds, e.g., chromafenozide (Nippon Kayaku Co., Japan) and benzamide (3,5-di-tert-butyl-4-hydroxy-N-isobutyl-benzamide, DTBHIB, Sumitomo Co., Japan).

Chemistry and Physical Properties The dibenzoylhydrazines can be readily synthesized from tert-butylhydrazine hydrochloride and the corresponding substituent benzoyl chloride using Schotten-Bauman conditions. The presence of the bulky tert-butyl group on the hydrazine allows the acid chlorides to be reacted in a sequential and highly regio-specific manner. The dibenzoylhydrazines (Fig. 6), although not steroids, mimic actions of the insect molting hormone, 20-hydroxyecdysone, binding directly to the binding sites of 20-hydroxyecdysone and acting as full agonist at that site. As a consequence, treated larvae express all the classic symptoms of anuntimelyandsevereoverdosewith20-hydroxyecdysone, called hyperecdysonism. Treatment induces premature apolysis, which is the primary mode of action, and larvae stop feeding. Within 3–12 h after uptake, molting was initiated, and by 24 h, intoxicated larvae prematurely slip their old head capsules in an attempt to ecdyse. However, normal successful ecdysis was inhibited. In addition, abnormal cuticle deposition and other molting irregularities were seen, such as a lack of sclerotization and tanning of the new cuticle, absence or conspicuous low number of endocuticular lamellae, hindgut extrusion and loss

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OH

OH

oEC

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HO HO

EM

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H OH H

ES

O O O

O

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Ecdysone Agonists, A Novel Group of Insect Growth Regulators, Figure 6 Chemical structures of 20-hydroxyecdysone (upper left), tebufenozide (upper right), chromafenozide (lower left) and DTBHIB (lower right).

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of hemolymph and molting fluid, that results in desiccation and ultimate death.

Insecticidal Mode of Action The dibenzoylhydrazines manifest these typical effects via interaction with the molting hormone receptor complex that consists of a heterodimer of two steroid receptor superfamily members, i.e., the ecdysteroid receptor (EcR) and the Ultraspiracle (USP) protein. This hormone-protein complex binds then to the ecdysone responsive elements on the DNA. These chemicals permit the expression of genes and behavioral events that are dependent upon the presence of 20-hydroxyecdysone. However, those processes that are dependent upon the absence of 20-hydroxyecdysone, such as the expression of dopa-decarboxylase enzyme for tanning and the ecdysis behavior (production/release of the neuropeptide eclosion hormone), are prevented due to the persistence in the insect tissues (Fig. 7). In adults, the dibenzoylhydrazines caused a reduction of egg production and fertility in various target Lepidoptera, Coleoptera and Diptera. However, the exact mechanism of action is not clear.

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Ecdysone Agonists, A Novel Group of Insect Growth Regulators, Figure 7 Last instar of the beet armyworm, Spodoptera exigua (Lepidoptera), 24 h after treatment with 1 ppm methoxyfenozide. (a) Panel A is a lateral view under the light microscope with the arrow showing slipped head capsule and the unsclerotized new cuticle over the head and mouth parts. (b) Panel B is a transmission electron micrograph of the integument, showing the presence of a double cuticle, the conspicuous absence of a high number of procuticular lamellae underneath the newly secreted epicuticle and signs of epidermal cell degeneration. BL: basal lamina, DB: dense body, Epid: epidermal cell, EM: ecdysial membrane, ES: ecdysial space, MV: epidermal microvilli, N: epidermal nucleus, nEC: new epicuticle, nPC: procuticle of the new cuticle, oEC: old epicuticle of the particularly digested cuticle, V: vacuoles, bar = 3 μm.

Insecticidal Properties and Efficacy Against Target Pests The dibenzoylhydrazines were tested in larvae and adults from at least 16 different insect


orders, and toxicity is most pronounced when exposure and uptake occur via ingestion. Tebufenozide and methoxyfenozide perform a high selective toxicity against Lepidoptera. These compounds are marketed around the world for control of important agricultural caterpillar pests in cotton, vegetables, top fruit, grapes, ornamentals, forestry and rice. Targets are, for instance, beet armyworm, Spodoptera exigua, cabbage looper, Trichoplusia ni, codling moth, Cydia pomonella, grape berry moth, Lobesia botrana, spruce budworm, Choristoneura fumiferana, rice leafroller, Cnaphalocricis medinalis, and others. Use rates typically range between 30 and 300 g of active ingredient/ha depending on the target crop and pest.

Safety to Non-target Organisms Tebufenozide and methoxyfenozide had little or no effect on a panel of non-lepidopteran pests (Coleoptera, Hemiptera, mites and nematodes) when tested at high rates (from 18 to 1500-fold greater than that producing 90% mortality in Lepidoptera). Likewise, laboratory and field experiments showed that there are little or no adverse effects at normal rates on a wide range of non-lepidopteran beneficial insects such as honeybees and bumblebees (Hymenoptera), many predatory insects (Hemiptera, Coleoptera, Neuroptera, Odonata, Plecoptera, Trichoptera, Ephemeroptera) and mites (Acarina), several caterpillar endoparasitoids (Hymenoptera) and certain insect predators such as spiders (Arachnida). These compounds appear to be highly caterpillar selective and highly compatible for integrated pest management (IPM). Treatment also was found to be safe towards several nonarthropod invertebrates such as earthworms and nematodes, and has a low acute toxicity for a representative crustacean (Daphnia magna). For vertebrates, several representative mammals, bird and fish species (rat, quail and

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trout) were, at a minimum, four orders of magnitude less susceptible to methoxyfenozide and tebufenozide than is a representative lepidopteran species. These compounds are nonirritating (rabbit), non-sensitizing (guinea pig), non-mutagenic and non-oncogenic (mouse, rat and dog). Methoxyfenozide has a dietary no effect level (NOEL) of 1950 mg/kg in a two-generation rat development bioassay. In retrospect, this relative lack of vertebrate toxicity might have been anticipated since such organisms do not synthesize or utilize 20E, the ecdysone receptor complex (EcR and USP) or any other closely homologous substances.  Ecdysteroids  Metamorphosis  Endocrine Regulation of Insect Reproduction  Diapause  Insecticides

References Carlson GR (2000) Tebufenozide: a novel caterpillar control agent with unusually high target selectivity. In: Anastas PT, Heine LG, Williamson TC (eds) ACS Symposium Series 767, Green chemical syntheses and processes. American Chemical Society, Washington, DC, pp 8–17 Carlson GR, Dhadialla TS, Hunter R, Jansson RK, Jany CS, Lidert Z, Slawecki R (2001) The chemical and biological properties of methoxyfenozide. Pest Manag Sci 57:115–119 Dhadialla TS, Carlson GR, Le DP (1998) New insecticides with ecdysteroidal and juvenile hormone activity. Annu Rev Entomol 43:545–569 Mikitani K (1996) A new nonsteroidal chemical class of ligand for the ecdysteroid receptor 3,5-di-tert-butyl-4hydroxy-N-isobutyl-benzamide. Biochem Biophys Res Commun 227:427–432 Palli SR, Retnakaran A (2001) Ecdysteroid and juvenile hormone receptors: properties and importance in developing novel insecticides. In: Ishaaya I (ed) Biochemical sites of insecticide action and resistance. Springer-Verlag, Berlin, Germany, pp 107–132 Smagghe G, Degheele D (1998) Ecdysone agonists: mechanism and biological activity. In: Ishaaya I, Degheele D (eds) Insecticides with novel modes of action. SpringerVerlag, Berlin, Germany, pp. 25–39

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Williams CM (1968) Ecdysones and ecdysone analogues. Their assay and action on diapausing pupae in the Cynthia silkworm. Biol Bull 134:344–355

Ecdysozoa The concept of a superphylum called Ecdysozoa was proposed only in 1997, following molecular analyses that suggested close relatedness among some invertebrates that shed their three-layered cuticle periodically. However, a similar concept had been proposed 100 years earlier based on morphology. The characteristics that link the ecdysozoans, in addition to the three-layered sheddable cuticle composed of organic material, include the absence of locomotory cilia, production of amoeboid sperm, and the absence of spiral cleavage in the embryonic stage. There are two major groups within this scheme of classification, encompassing several phyla. Only the Arthropoda (over 6 million species) and Nematoda (over 20,000 species) are speciose, the other phyla being fairly minor in importance. The phyla involved are: Ecdysozoa Panarthropoda Arthropoda Onychophora Tardigrada Cycloneuralia Kinophora Priapulida Loricifera Nematoda Nematomorpha This grouping has yet to win wide acceptance, as these taxa seem to be polyphyletic.

Reference Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, and Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493

Ecdysteroids Eli Shaaya The Volcani Center, Bet Dagan, Israel Ecdysteroids are hormones that regulate a wide variety of cellular processes in the life cycle of arthropods. Pulses of ecdysteroids coordinate the complex events during molting and metamorphosis in postembryonic development which are essential in the life of the insects. Two of the most common and studied ecdysteroids hormones in insects are ecdysone = (α -ecdysone) and 20-OHecdysone = (ecdysterone, crustecdysone). Research on insect hormones began in 1934, when V.B. Wigglesworth, in his study on the physiology of ecdysis in the Hemipteran Rhodnius prolixus described the metamorphosis in this blood sucking bug. One year later, G. Fraenkel published a study of the hormone causing pupation in the blowfly Calliphora erythrocephala. From P. Karlson’s autobiography we learn that, in 1943 he started the work on the isolation of the molting hormone of insects, and only in 1954, Bütenandt and Karlson had succeeded in isolating a crystalline form of ecdysone. In order to obtain reasonable amounts of the hormone, they had to use 500 kg of male silk worm pupae, (Bombyx mori). The exact structure of ecdysone was fully elucidated in 1965, independently by the Karlson group, and the crystallographers Hüber and Hoppe. Later, in the year 1966, the structure of 20-OH-ecdysone(20E), which is regarded in most arthropods as the predominant active hormone, was sequentially established by Dennis Horn’ s group as crustecdysone and Hoffmeister group as ecdysterone. The concept of steroid hormone action on gene expression was first developed by studies on the mode of action of ecdysteroids in Dipteran flies. This was due to the findings in 1960 of Clever and Karlson, that ecdysteroids can activate transcription in polytene chromosomes of the midge, Chironomus tentans. Evidence to support this concept was the visible enlargement of specific regions of polytene chromosome puffs of the target cells.

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Ecdysteroids

Origin and Site of Synthesis

development. In flies, higher insects, the prothoracic glands is a part of an organ, the ring gland, which also includes the corpus cardiacum and corpus allatum. The latter is the site of ecdysteroids release to the hemolymph. In some insects, epidermal, oenocytes and gonadal cells are alternative sites for ecdysteroids production, especially during adult life, at a time the prothoracic glands are no longer present. In female ovaries, the epithelium of the follicle cells produces ecdysteroids, which play a crucial role in the induction of vitellogenesis. During embryogenesis, in the absence

Cholesterol, originating either from the insect diet or from the conversion of dietary C28 and C29 phytosterol, is the common precursor of ecdysteroids (Fig. 8). All insects and other arthropods are unable to synthesize de novo the steroid nucleus, therefore require exogenous or dietary source of sterol for normal growth. The prothoracic glands, comprising a single steroidogenic cell type in most insects, are the predominant site of ecdysteroids biosynthesis during postembryonic

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Ecdysteroids, Figure 8 Structural formulae of some important phytosterols, ecdysteroids and cholesterol.

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of any differentiated site of ecdysteroids biosynthesis, many insects are able to elevate their ecdysone titer by metabolizing maternal ecdysteroid conjugates to active hormones. In crustaceans, ecdysteroids are produced by the Y-organ glands, and control a number of processes in the life cycle of the animals, similar to insects.

The Regulation of Ecdysteroid Synthesis The regulation of ecdysteroids synthesis is very complex, and under the control of peptide hormones as well as the sesquiterpenoid juvenile hormone (JH). Ecdysteroids are mainly synthesized by the prothoracic glands and released into the hemolymph upon stimulation by the prothoracicotropic hormone (PTTH), a neuropeptide produced by the insect brain. The periodic increase in ecdysteroids titer critical to insect development reflect to a large degree the activation of the prothoracic gland by PTTH. The structure and mode of action of PTTH has been investigated in a number of insects. PTTH is synthesized as a preprohormone and it is expressed in a number of neurosecretory cells of the brain. It occurs in multiple forms large and small, some are active others not, depending on the insect species. Binding of PTTH to the membrane receptor elevates intracellular Ca2+ influx, and the action in turn enhances cAMP formation. As a consequence cAMP-dependent protein kinase is stimulated. The activated kinase stimulates ecdysteroid production. PTTH acts at critical steps in the regulation of ecdysteroids levels in developing insects. The concentration of active ecdysteroids is modified by target cell specific hormone metabolism. The prohormones ecdysone, 3-dehydroecdysone and 3-dehydro-20 hydroxyecdysone, which are secreted into the hemolymph, are metabolized to the more active compound 20E, which is in most arthopods the predominant active hormone. In various species of Hemiptera, Makisterone A is

regarded as the major molting hormone. Like vertebrates, a series of cytochrome P450 is involved in the various steps of 20E synthesis from cholesterol. There are indications that at least two cephalic factors are able to stimulate ovarian ecdysteroidogenesis in the blow fly: one acting via cAMP independent mechanism, and the other using cAMP as a second messenger. Although the ecdysteroids have been characterized, ecdysteroids biosynthetic pathways and enzymes involved in the hormones biosynthesis are not yet fully elucidated. Also, little is known about the genes involved in the biosynthesis of the hormones. PTTH is not the sole regulator of ecdysone biosynthesis. JH exerts an indirect tropic effect on the prothoracic glands, probably mediated by a stimulatory protein in the hemolymph, possibly a precursor steroid carrier. Also, the developmental state of the prothoracic glands to respond to the regulatory effectors appears to be a key factor in the regulation of ecdysone synthesis. During larval-pupal development, regulatory effectors, hormone interactions, and competence of the prothoracic glands may all be integrated to regulate the ecdysteroid titers. There is experimental evidence for the existence of a neuroendocrine regulation of ecdysteroid synthesis in ovaries of Aedes ageptii and Locusta migratoria. It may be significant to mention that in Locusta there are structural similarities between the larval (PTTH) and adult ecdysiotropins. In crustaceans, ecdysteroid synthesis is regulated by molt-inhibiting hormone (MIH). This neurohormone exerts opposite effects compared to PTTH in insects by inhibiting ecdysteroid synthesis in the Y-organs. MIH also increases cAMP second messenger which activates protein kinases, following alteration of cellular Ca2+ levels. The contrasting steroidogenic effects of PTTH and MIH probably arises from differences in the cellular kinase substrates. In insects such substrates enhance ecdysteroid secretion by increasing the translation of granular protein. In crustacea, MIH stimulates changes leading to the inhibition of both protein synthesis and steroidogenesis.

Ecdysteroids

Ecdysteroids Metabolism Activation The metabolism of the prohormones ecdy sone, 3-dehydroecdysone and 3-dehydro20hydroxyecdysone to 20-hydroxyecdysone, is regarded as an activation mechanism, converting the poorly active precursors, to the highly active 20-hydroxyecdysone, the principle molting hormone. This refers mainly to higher insect species like Dipterans. Other insect species use both ecdysone and 20-hydroxyecdysone as hormonal messengers. There are speculations that during evolution in higher insects ecdysone lost its hormonal role and is merely a prohormone.

Inactivation Mechanism Inactivation mechanisms of ecdysteroids are common in the various insects tested. Ecdysone and/or 20-hydroxyecdysone are inactivated primarily by: 1. Esterification, acetylation, posphorylation. 2. Epimerization, oxidation followed by isomeric reduction of the C-3 hydroxyl group. 3. Hydroxylation of the C-26 methyl group followed by oxidation to ecdysonoic acid. 4. To a lesser extent by esterification of the C-2 hydroxyl group on the A nucleus of the molecule.

Inactivation of ecdysteroids varies according to the tissue and developmental stage. In other arthropods, the inactivation mechanism of the active ecdysteroids is similar to insects.

Storage Mechanisms A large portion, up to 98% in some insect spp., of the ovarian ecdysteroids are esterified to phosphate conjugates at the C-22 hydroxyl group. Occasionally, more complex conjugates bearing

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nucleotides on the phosphates are found together with the 22-phosphates. These ovarian conjugates are present in newly laid eggs, and gradually metabolized during embryogenesis to the active hormone. It may be relevant that the eggs contains enzymes involved in ecdysteroid metabolism.

Mode of Action of Ecdysteroids: Molecular Aspects Metamorphosis transforms the insect larva into a reproductive adult through a complex series of developmental events involving cell proliferation, differentiation, remodeling of structures for new functions, and finally programmed cell death. In insects, these developmental processes are coordinated by pulses of ecdysteroids that include the principle hormone 20E and in some insects ecdysone, which have morphogenetic functions of its own, and also JH. The ecdysteroids cause molting (Fig. 9) and also are responsible for the changes in the genetic programs that are necessary for metamorphosis, whereas the presence of JH in the larva prevents these changes from taking place, but does not prevent the molting response. Thus, metamorphosis ensues when ecdysteroids rise in the absence of JH in the final larval instar. In most insects, exogenous JH at this time causes the formation of a supernumerary larva, but in the higher Diptera JH does not prevent pupariation nor pupation, but disrupts the development of the adult organs, thereby causing the death of the insect. The target tissues of ecdysteroids contain proteins which bind to the hormone. The binding has a high affinity for the hormone, and a limited number of binding sites per target cell, which is characteristic of steroid hormone receptors. In addition, the binding proteins exhibit a differential affinity for the various ecdysteroids, depending on their biological activity. Determination of the mode of action of ecdysteroids at the genomic level was based on a series of pioneering studies using Chironomus and Drosophila which showed that in polytene

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Ecdysteroids, Figure 9 Schematic diagram of the principal endocrine organs of L epidopteran insects and the regulation of metamorphosis by their hormones. Ecdys. = ecdysteroids; JH = juvenile hormone.

chromosomes certain stage-dependent puffs could be induced by exogenous ecdysone. This model interaction of the hormone with the hormone- receptor complex recognizes specific DNA response elements, and triggers a cascade of gene activity that directs the molting process. Over one hundred different genes are known to be regulated by ecdysteroids. Hormonal regulation is gene and tissue specific, and is modified according to the developmental stage of the insect. The general molecular

mechanism of steroid hormone action must be diversified to adapt hormone action according to the physiological needs. Target cell specific hormone metabolism is one way to adapt molting hormone action in a tissue specific manner. Beside molting, ecdysteroids regulate a large number of processes including spermatogenesis, oogenesis, reproduction, embryogenesis, diapause, change in insect color, behavior, metabolism and cell death. Ecdysteroids also regulate the concentration of

Ecdysteroids

enzymes responsible for the synthesis and degradation of 20E, and thus modulate ecdysteroid titer; regulate the central nervous system sensitivity to eclosion hormone and ecdysis triggering hormone; and the regulation of melanization by the induction of the enzyme dopa decarboxylase. The relatively simple ecdysone-inducible genes of salivary gland glue proteins or larval serum proteins-1 of fat body, for example, have a single transcript. However, other ecdysone-inducible genes show a complex pattern of transcription and stretch over regions of 50 kb or more.

Involvement of Ecdysteroids in the Control of Reproduction and Embryogenesis Vitellogenic ovaries synthesize ecdysteroids at a given stage of their development. In some dipteran species, ecdysteroids synthesis starts at almost the same time as the onset of vitellogenin synthesis, whereas in other species like orthopterans the synthesis starts only towards the end of vitellogenin uptake. These ecdysteroids are either released into the blood of the female or accumulate inside the oocytes and are transferred in the newly laid eggs. This situation is common in most insect species. However, the ratio of the amounts released into the blood, to those retained in the oocytes seem to vary between insect orders. In locusts, for example, only 2% of the ecdysteroids produced by the ovary is released into the blood of the female, the other 98% accumulates in the newly laid eggs. In Galleria (Lepidoptera), this ratio is 1:1. It should be mentioned, however, that in most insect species most ovarian ecdysteroids are conjugates, and may escape detection. In higher insect orders, like the Diptera, ovarian ecdysteroids play a role in the control of vitellogenin synthesis, whereas in other orders they play a role in the early events of embryogenesis. Ecdysteroids also control additional events in a variety of insect species. For example, in mosquitoes, separation of incipient follicles from the

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g ermarium, and control of release of ovulation hormone, is controlled by ecdysteroids. As regards the possible involvement of ecdysteroids in the control of vitellogenesis in dipterans, ecdysteroids can stimulate the synthesis of vitellogenin mRNA, both in females and males. In female Diptera, ecdysteroids stimulate the fat body to synthesize increased amounts of vitellogenin; it is possible that the fat body has to be primed by JH to become responsive to ecdysteroids. The involvement of ovarian ecdysteroids (Fig. 10) in the early events of embryogenesis is based on the remarkably high concentrations, about 10−4 M of ecdysteroid conjugates of ovarian origin, present in newly laid eggs. As embryogenesis proceeds, the conjugates are then hydrolyzed by enzymatic activity, resulting in the surge of free ecdysteroids. The presence of enzymes responsible for these transformations has been monitored in a number of insects. In the newly laid eggs, the maternal conjugate first is hydrolyzed to the active ecdysteroid needed to trigger some specific processes, then it metabolized to an inactive molecule. Indeed, during embryogenesis there are a certain number of peaks of ecdysone and/or 20-hydroxyecdysone which coincide with cuticle deposition, either by the serosa or by the embryonic epidermis. Thus, via a large supply of ecdysteroid conjugates, the mother controls ecdysone-triggered events of embryogenesis which occur prior to the stage when the embryo has acquired its own capacity to biosynthesize ecdysone de novo.

Ecdysteroids in Non-arthropods Metazoans Many protostomians contain ecdysteroids; the main ecdysteroids which were identified in nonarthropods are similar to those found in the different insects such as ecdysone, 2-deoxy-ecdysone, Ponasterone A, 20-hydroxyecdysone and 20, 26-dihydroxyecdysone. As in arthropods, these ecdysteroids are found both in free or esterified (polar or non-polar) forms. The concentration of

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Ecdysteroids, Figure 10 Simplified scheme of ecdysteroid production in insect molting and reproduction.

ecdysteroids recorded in non-arthropods are generally lower than those found in arthropods. Titre fluctuations have been recorded in relation to reproductive cycles, embryonic metamorphosis and integumental events. This indicates that in non-arthropods ecdysteroids might play roles similar to those that they exert in arthropods. It is of interest to mention that human patients infested by trematodes, cestodes and nematodes contained ecdysteroids in their blood and urine. The potential of this finding for diagnosis, and possibly even for interfering with the parasite’ s development or reproduction, is of interest. The detection of ecdysteroids in sera or urine of humans may contribute to diagnosis of helminth infection. It is premature to speculate that these finding open a novel way of fighting parasitic infection. It is questionable whether or not these parasites use ecdysteroids for the control of their reproduction and development.

Phytoecdysteroids Analogues of ecdysteroids occur in a variety of plants: pteridophyta, gymnosperms, and angiosperms. The ecdysteroids isolated from plants

are ecdysone, 20E, 3-epi-20-hydroxyecdysone, 20-hydroxyecdysone 22 acetate, ponasteron A and many others of less importance. The physiological relevance of these phytoecdysteroids in the plants, which are identical to the zooecdysteroids, is not thoroughly studied. A high concentration of ecdysteroids may contribute to the protection of the plant against invertebrate predators by mimicking the natural hormones and disturbing the hormonal balance within the insect. They can act as antifeedants or antagonize the action of the ecdysteroid hormones.  Ecdysone Agonists  Prothoraciotropic Hormone  Diapause  Endocrine Regulation of Insect Reproduction  Metamorphosis

References Barker GC, Chitwood DJ, Rees HH (1990) Ecdysteroids in helminthes and annelids. Invertebr Reprod Dev 18:1–11 Dinan L (2001) Phytoecdysteroids: biological aspects. Phytochemistry 57:325–339 Gilbert LI, Ryberynski R, Warren TJ (2002) Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 47:883–916

Ecology

Harshman LG (1998) Differential gene expression in insects. Annu Rev Entomol 43:671–700 Henrich VC, Rybezynski R, Gilbert LI (1999) Peptide hormones, steroid hormones and puffs: mechanisms and models in insect development. Vitam horm 55:73–125 Lafont R (2000) Understanding insect endocrine systems: molecular approaches. Entomol Exp Appl 97:123–136 Smith AW, Sedlmeier D (1990) Neurohormonal control of ecdysone production: comparison of insects and crustaceans. Invertebr Reprod Dev 18:77–89

Echinophthiriidae A family of sucking lice (order Phthiraptera). They sometimes are called seal lice.  Chewing and Sucking Lice

Eclosion Egg hatching. Escape of the immature insect from the egg chorion. This term also is sometimes used to describe emergence of the adult from the pupal stage.

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Ecological Homologues Species that have niche parameters that are almost identical. Such species typically do not coexist, and evolve in different geographic regions.

Ecological Management This term is equivalent to cultural management or cultural control. This is the manipulation of the environment or practices to prevent invasion, minimize damage, or eliminate pests. It depends on the use of normal planting, production, harvesting practices rather than specialized equipment or techniques. A good example of ecological management would be manipulation of planting dates, making them either earlier or later depending on circumstances, to avoid infestation.  Cultural Control of Insect Pests

Ecological Niche The role of an organism including the resources used and habitat occupied.

Eclosion Hormone A neurosecretory polypeptide produced by the brain and released into the hemolyph, stimulating molting.  Metamorphosis

Ecnomidae A family of caddisflies (order Trichoptera).  Caddisflies

Ecological Community A group of populations that interact within a certain geographic area. The biotic portion of an ecosystem. It is also called a community.

Ecological Succession Replacement of members of a community over time in response to community change. This process is normally thought of as a botanical phenomenon, wherein grasses are replaced by small shrubs, then large shrubs, then small trees, and finally large trees. However, insects display corresponding changes as other members of the community change. It is also called succession.

Ecology The study of organisms in relation to their environment. News writers often substitute the term ecology when they mean environment.

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Economic Injury Level (EIL)

Economic Injury Level (EIL) A level of pest abundance or damage at which the cost of control equals the crop value gained from instituting the control procedure.  Economic Injury Level (EIL) and Economic Threshold (ET) Concepts in Pest Management

Economic Damage Damage that exceeds a visual or aesthetic effect, causing a monetary loss.  Economic Injury Level (EIL) and Economic Threshold (ET) Concepts in Pest Management

Economic Injury Level (EIL) and Economic Threshold (ET) Concepts in Pest Management David G. Riley University of Georgia, Tifton, GA, USA

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One of the fundamental concepts of integrated pest management is that each pest species has a definable relationship in terms of damage to the plant or animal host that it attacks. This relationship is often referred to as the damage curve (Fig. 11), which is often determined relative to yield loss. This damage curve can take several forms, but was summarized by Higley and Peterson as having a tolerance or overcompensation phase ([1] no yield response, or [2] positive yield response to injury), a linearity phase ([3] e.g., yield loss = − a (unit injury) + b), and a desensitization and an inherent impunity phase ([4] decreasing and finally [5] no additional yield loss per unit injury). The curve can be used with various methods to determine whether or not any action or pest management tactic (e.g., pesticide, biological control, cultural control, etc.) is needed to reduce the damage associated with this pest. Also, this relationship is uniquely characterized by a critical point, the economic injury level (EIL), or the

point in the agricultural production system where the costs associated with pest management equal the benefits from the pest management actions. In other words, below the pest population represented by the EIL there is no need to take pest control actions because they are not economically justified, but economic damage can occur when the pest population densities are above the EIL. A simple, robust model of the EIL relationship between pest control costs and benefits from control actions was developed by Pedigo et al. as: where C = management cost per production unit, V = market value per production unit, D = damage per unit injury, I = injury per pest equivalent, and K = proportional reduction in injury with management. They later combined D + I into a single variable, Dʹ = percent yield loss per pest. A variation on this formula that is often used that assumes 100% control is: EIL = (C × N)/(V × I), where N = the number of pests causing injury, and I = percent yield loss (similar to the Dʹ value above). In an example using the EIL = C/VDʹ K formula, if a seasonal average of one insect/plant causes a

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conomic Injury Level (EIL) and Economic E Threshold (ET) Concepts in Pest Management, Figure 11 Example of a pest damage curve (thick line) and associated cost of pest control (thin line) used to estimate at economic injury level (EIL).

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10% reduction in yield, the market value of the crop is $0.4/lb fruit and you expect 5 lb fruit/ plant yield, the cost of control is $0.04/plant, and you can count on a 75% reduction in damage with the control tactic used, then: EIL = $0.04 cost per plant/($0.4/lb×0.5lb/ insect × 0.75) = 0.27 insects/plant Notice that if you halve the number of insects required to inflict 10% yield loss, you halve the EIL value. In contrast, if you double the cost of control you double the EIL value, again balancing the tradeoff between control costs and benefits. In reality, the EIL value can be difficult to calculate exactly because of the temporal and dynamic nature of pest damage and crop value. In the example above, an early season average of one insect might result in 15% yield while late season results in only 5% yield, so the estimate based on a seasonal mean would not be very precise for a given period during the season. One way to avoid large seasonal differences is to calculate an early-season and a late-season EIL, for example: EIL1 = C/VD1ʹK and EIL2 = C/VD2ʹK or EIL1 = $0.04 cost per plant/($0.4/lb×0.75 lb/ insect × 0.75) = 0.18 insects/plant EIL2 = $0.04 cost per plant/($0.4/lb×0.25lb/ insect × 0.75) = 0.5 insects/plant The EIL can be based on a single, seasonal mean, based on periods during the season with similar responses (e.g., seedling, vegetative, fruit formation, or simply early versus late season), or be accurately calculated over time for the life span of the affected host. This latter determination of a dynamic EIL requires a great deal of data and is seldom accomplished for most crop or livestock systems. In addition, the EIL formulas often assume a linear response to injury at any given time during the season, which may not be entirely

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accurate. Even so, an assumption of linearity can be generally sufficient for the range of pest injury critical for an EIL determination. Estimates based on the aforementioned EIL formulas are in use for many agricultural pests and have successfully provided pest management decision criteria for many production systems, mainly because of both their effectiveness and ease of use. It should be noted that in commercial production systems, economic injury levels are likely to be close to a maximum allowable pest management cost because these systems have traditionally focused on maximizing returns and reducing risks to production. What is often lacking in these estimates of EILs is an environmental cost factor. The environmental cost would adjust the pest management cost by taking into consideration not just what the farm spends on management tactics, but also an estimated average cost to the environment or agro-ecosystem where the farm exists. Using the environmental economic injury level: EIL = (C+EC)/VDIK proposed by Higley and Wintersteen and adding an environmental cost of $0.04/plant would increase the EIL to 0.53 or double its previous level in the aforementioned example. There will likely be a high degree subjectivity in this kind of environmental cost estimate. Even with its complications, the EIL is fundamental for understanding the interaction of pests with their host, but the calculation of economic thresholds from these data is quite a different problem, which will be discussed in the next section. An economic threshold (ET) is typically the pest population density at which a pest control action (e.g., pesticide, biological control, cultural control, etc.) should be taken in order to prevent an increasing pest population from reaching economically damaging levels, which is the economic injury level (EIL). As shown in the diagram of the two-level fixed economic threshold (Fig. 12), two different fixed economic thresholds are esti-

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control actions

EIL-1

untreated

ET-2

EIL-2

treated

ET-1 Time (early to late production season)

Economic Injury Level (EIL) and Economic Threshold (ET) Concepts in Pest Management, Figure 12 A two-level, fixed economic threshold with treated (narrow line), i.e., effectively controlled to stay below the EIL, and untreated (thick line) pest populations.

mated for a single pest in a given cropping season depending on if the time frame is early season (ET-1) or late season (ET-2) as: ET1 = 90% × EIL1 = 0.16 insects/plant ET2 = 90% × EIL2 = 0.48 insects/plant Also as an example, the pest population levels of a treated field (control actions taken) versus an untreated field (no control action) are indicated by the narrow and solid lines, respectively (Fig. 12). What can be seen from this example is that, on several levels, time is as critical a component in the estimation of economic thresholds as pest numbers. Also, it is clear that frequent pest monitoring or scouting will be required to track pest population density through time with some accuracy. In this example, it is assumed that approximately twice as many insects are required to cause an equal amount of yield loss in late season (EIL-2) as early season (EIL-1). Another aspect of time is that there may be an increase in the pest population or damage over time, and will tend to increase at a determined rate, excluding massive emigration events, as the season progresses. Finally, there is a time component in the duration of delay from when a pest population reaches an economic threshold, when control

actions are actually implemented, and when the reduction of the pest population begins to occur. This can directly affect the threshold value, because the purpose of the threshold is to prevent the pest population density from reaching the EIL. As Pedigo stated, “the ET actually represents the time for taking action against a pest; population density serves as a convenient index of that time.” Economic thresholds for agricultural pests vary greatly in their accuracy (how close the estimate is to a true ET) and their precision (degree of variation around an estimated value) depending on the method used for its development. In the broadest sense, thresholds in the literature are either more subjective (based on an educated guess or “guesstimate”) or more objective (based on research data used to estimate an EIL and an effective method for relating the EIL to a threshold level for initiating pest management actions). In either case, the objective is to prevent the pest population from reaching an economically damaging level. However, a low level of accuracy, often associated with subjective estimates called “nominal thresholds,” can lead to either underestimating or overestimating the pest population level where action should be taken. An underestimate will result in more control costs than is economically justified, whereas an overestimate will result in crop or livestock damage that could have been avoided economically with the appropriate timing of an effective control tactic. Even though an objective ET can be more accurate than a subjective ET, the objective ET’ s precision can be greatly influenced by the method in which an EIL is calculated. An EIL based on seasonal population means relative to final yield loss can be very accurate, but not very precise for individual dates during the season. Using the previous example of 15% yield loss during early season and 5% yield loss during late season for an equal number of pests, the calculated EIL values for early and late season are 0.18 and 0.53, respectively. If a single EIL = 0.27 is used for the entire season, then there will be an overestimated ET early in the season and


an underestimated ET late in the season, causing the same problem as a lack of accuracy, even if it is likely to a lesser degree. A subjective ET can be based on effective observational data as, for example, by adjusting the threshold higher or lower after each production season based on yield response, so that a reasonably accurate ET is developed through a long term process of iteration. Generally, a subjective ET is fixed at a value or named by consensus for a given use period and is thus referred to as a nominal threshold. In fact, a significant number of thresholds in use today are based on this method. The problem with this method is that it does not define the mechanism behind the EIL and ET, and can thus be affected by changes in production factors, e.g., crop variety, climate, market-driven planting dates, etc., to some unknown degree from year to year. At the very least, a subjective ET can be a starting point for threshold development, and potentially provide significant pest management benefits. Although objective determinations of ET are research-based, they also can have a range of sophistication and complexity beginning with a simple fixed ET. The fixed ET is set at a specific percentage of the determined EIL, usually based on conservative estimates for preventing significant crop loss. In the example for a single seasonal EIL determination described in the previous section, the estimated EIL = 0.27 insects per plant would result in 2.7% yield loss that cannot be economically prevented within the conditions of the example. If there was a relatively high risk of loss, for example above 10%, a conservative threshold might be set at half, regardless of whether or not the additional control actions are economically justified. High levels of threats of injury can even lead to abandoning the ET altogether. In the other direction, if a new, highly effective (100% control) and inexpensive ($0.01/plant) control product is introduced into the system, not only does the EIL drop to 0.05, the expected yield loss at this level is so low at 0.5% that the tendency will be to leave the ET at or even above the EIL = 0.05. In this case,

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increasing the EIL could be justified by using other decision criteria, like environmental costs that have not been included in the initial EIL determination. Subjective judgments on the overall percentage crop loss that can be tolerated tend to vary more at the low injury levels than the high injury levels since high injury levels are not commercially tolerated. What is not considered in detail with the fixed ET is the actual time between control actions and the time it takes for the pest population to increase to the predicted EIL. In most cropping systems, weekly scouting reports are followed by weekly curative actions in the form of pesticide applications. If a cultural or biological control tactic is used that needs time to affect the overall pest population, the estimation of this time becomes critical. In this case, more descriptive thresholds based on the mechanisms of pest population dynamics are needed to accurately predict when the population level will reach the EIL. Descriptive thresholds are of two general types, stochastic and deterministic. The deterministic model assumes a fixed and unique outcome, whereas a stochastic model incorporates probabilities based on demographics. Thus, the stochastic ET is based on an estimated pest population growth based on average population dynamics, with an associated probability of error. An economic threshold based on sequential sampling of a pest population is a good, fairly complex example of a stochastic ET. A simple example, based on highly predictable pest population dynamics, would be if a pest population prior to reaching an EIL is known to increase at a given exponential rate that doubles the population (y = 2x where y = pest numbers and x = generation time) after each generation time and the scouting interval (e.g., 7 days), is equal to one generation time. Then using the EIL = 0.27, the threshold would simply be: ET = EIL − (EIL/2) = 0.27 − (0.135) This simplistic example only works if the control action and response can occur between scouting

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intervals, that you can accurately predict that the EIL will be reached by the next scouting event, and that there is no great need to modify the value to include an additional margin of error based on a probability analysis. The deterministic ET relies on knowledge of age-specific parameters and life processes of the pest population. It can still require probability estimates for specific processes, such as the average mortality of a beneficial insect that would affect the estimate of “K” in the calculation of an EIL, but the key mechanisms that determine pest population growth are defined. Biological control or long term cultural control tactics could benefit from the use of this type of threshold. A typical difference in the response time for a biological control tactic versus a chemical control tactic is illustrated in Fig. 13. In this example, both tactics provide equally high levels of control, but the response to the pesticide is fast, so the ET could be set closer to the EIL value than it can with the biological control. To estimate the biological control response it might be necessary to calculate life table data for both the predator and prey species (crop pest) and relate this to temperature, time and spatial dynamics; a fairly complex proposition. As the time increases between the initiation date of an effective control action and the

Pest Population Density

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pesticide treatment

biocontol treatment

EIL

ET

response to pesticide

response to biocontrol

Time

conomic Injury Level (EIL) and Economic E Threshold (ET) Concepts in Pest Management, Figure 13 Delayed response to a biological control tactic.

control response of the pest, these descriptive thresholds can become more crucial.

References Higley LG, Pedigo LP (1996) The EIL concept. In: Higley LG, Pedigo LP (eds) Economic thresholds for integrated pest management. University of Nebraska Press, Lincoln, NE, pp 9–21 Higley LG, Peterson RKD (1996) The biological basis for the EIL. In: Higley LG, Pedigo LP (eds) Economic thresholds for integrated pest management. University of Nebraska Press, Lincoln, NE, pp 22–40 Higley LG, Wintersteen WK (1992) A novel approach to environmental risk assessment of pesticides as a basis for incorporating environmental costs into economic injury levels. Am Entomol 38:34–39 Pedigo LP, Higley LG (1992) A new perspective of the economic injury level concept and environmental quality. Am Entomol 38:12–21 Pedigo LP (1996) General models of economic thresholds. In: Higley LG, Pedigo LP (eds) Economic thresholds for integrated pest management. University of Nebraska Press, Lincoln, NE, pp 41–57 Southwood TRE (1978) Ecological methods. Chapman and Hall, New York, NY, 524 pp Stern VM, Smith RF, van den Bosch R, Hagen KS (1959) The integrated control concept. Hilgardia 29:81–101

Economic Threshold (ET) The point at which corrective measures must be taken to prevent damage from attaining or exceeding the economic injury level; a level of damage or insect abundance that warns the agriculturist of impending problems.  Economic Injury Level (EIL) and Economic Threshold (ET) Concepts in Pest Management

Ecosystem A complex of organisms and their physical environment that interact as a defined ecological unit. Ecosystems may be natural, or modified by human activity. Ecosystems generally are not defined by political boundaries. The biotic and abiotic components and their interactions

Edwards, Henry

within a certain geographic area. Ecological communities pluts their physical environment.

Ecotone The transition zone between two different communities. An example of an ecotone is fresh water marshes that serve as a transition between grassland and lakes.

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the Entognatha (collembolans, diplurans, proturans), which have recessed mouths.

Ectotherm An organism that uses energy from the environment rather than metabolic heat to regulate its body temperature. Insects are generally considered to be ectotherms, but some display endothermic behavior and physiology.  Thermoregulation in Insects

Ectadene (pl. ectadenia) Accessory glands of ectodermal origin found in the male reproductive system of some insects.  Accessory Gland  Reproduction

Ectophagous Feeding on the outside of a host.

Ectopsocidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids

Ectoparasite A parasite that develops externally on the host. Typical ectoparasites include fleas, lice and ticks of vertebrates. However, some ectoparasites affect insects, particularly some mites. Insects that develop externally on their insect hosts (usually wasps) are more correctly called ectoparasitoids, but usually are called ectoparasites, too.

Edaphic Pertaining to the soil.

Edwards, Henry Ecotype A subspecies or race that is adapted to a particular set of environmental conditions.

Ectognathous A hexapod with mouthparts that are not recessed into the head; rather, they are exposed. This is also known as ectotrophus. Such mouthparts are typically found in insects. This type of mouthparts distinguishes them from some related hexapods,

Henry Edwards was born in the country of Herefordshire, England, on August 27, 1830. He studied law, but he worked as an actor and his hobby was the collection of butterflies, in both of which occupations he became nationally rated in the US. In 1853, he travelled with a theatrical company to Australia, Peru, Panama, California, and Mexico, and managed to collect butterflies (and various other invertebrates) in all these places. From 1865, he lived in California, and was associated with the “Old California Theatre.” His butterfly collection, eventually consisting of 250,000 specinmens, became one of the finest in the US. In 1867 he was

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elected member of the California Academy of Sciences, and he published a series of papers entitled “Descriptions of Pacific coast Lepidoptera.” In 1877, he moved to the U.S. east coast, joined the New York Entomological Society, and edited the journal “Papilio” (1881–1883). In 1881–1882 he published an important paper on Aegeriidae, and in 1889 (after a sojourn in Australia), he published a “Bibliographical catalogue of the described transformations of North American Lepidoptera.” He died in New York city on June 9, 1891. His butterfly collection was bought by his friends (for benefit of his wife) and presented to the American Museum of Natural History in New York.

Reference Essig Eo (1931) Edwards Henry, 611– 613 in A history of entomology. The Macmillan company, New York, 1029 pp

Edwards, William Henry William Edwards was born in the state of New York on March 15, 1822, and took an early interest in natural history. He attended Williams College in Massachusetts, graduating in 1842. Then in the city of New York he studied law and was admitted to the bar in 1847. In 1846, after leaving college, he journeyed to Brazil to collect birds, butterflies, and other specimens. This resulted in his first book, “Voyage up the Amazon” in 1847, which influenced soon-to-be travellers Bates and Wallace. As a practicing lawyer, he had time to indulge his passion for butterfly collecting, and later for rearing butterflies from their eggs, and during his lifetime published some 200 papers. His major work was a three-volume book “The butterflies of North America” which appeared between 1872 and 1897, and received accolades. He died on April 2, 1909.

Reference Mallis A (1971) William Henry Edwards, pp. 288–292 in American entomologists. Rutgers University Press, New Brunswick, New Jersey, 549 pp

Eelworm A nematode.

Efficiency A measure of the level of precision or accuracy per unit of cost (time or currency).  Sampling Arthropods

Egg The first free-living stage of most insects, contained within a chorion (shell).

Egg Burster A raised area such as a ridge or bump on the head of an embryo that is used to mechanically rupture an egg shell during hatching.

Egg Case The case or covering secreted by an insect that contains or protects the egg cluster. It is most commonly found in orthopteroid insects. The egg case is also known as an oötheca.

Egg Pod A clutch of eggs surrounded by a capsule. Also called egg case or ootheca. This term is generally reserved for orthopteroid insects.  Eggs of Insects

Eggs of Insects

Eggs of Insects John L. Capinera University of Florida, Gainesville, FL, USA Nearly all insects produce eggs (oviparity) during the adult stage, though some seemingly can produce living offspring (viviparity) indefinitely, and a few retain their eggs internally until after they hatch (ovoviviparity), depositing partly grown progeny (e.g., sheep keds and tsetse flies). Eggs are a common means of passing through unfavorable (dry season or winter) periods when food is unavailable, though because other stages of insects can enter diapause, egg-overwintering is by no means universal. Most eggs are spherical, oval, or elongate. The degree of sculpturing and ornamentation varies, as does their color. They may have ancillary structures such as anchors (e.g., wasp parasitoids) or floats (e.g., mosquitoes). They may be deposited singly or in batches, but typically a species is consistent in its pattern of oviposition.

The Egg Shell The egg shell, or chorion, of insects is proteinaceous. It apparently lacks chitin, the polysaccharide responsible for the hardness of the exoskeleton. The insect egg shell suffers from the same problem faced by other terrestrial egg-layers: because the water molecule is smaller than the oxygen molecule, the gas exchange needed for respiration also results in dehydration (water loss). There is no ready means to allow gas exchange without some moisture loss. Thus, insects have evolved various means to facilitate gas exchange while minimizing water loss. Their challenge is appreciably more difficult than for birds and reptiles because their eggs are much smaller and therefore have a much larger surface to volume ratio, leading to greater potential for water loss. Insects tend to have mores complex egg shells than birds and reptiles to accommodate this challenge. In general, insects have solved the surface area to volume ratio problem with respect to their larval

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and adult forms by evolving a waxy covering over their entire body. To solve the gas exchange problem, they have closable spiracular openings that allow bursts of gas exchange with minimal water loss. However, insects generally have opportunity to feed and ingest additional moisture, so the spiracle-based system does not have to be absolutely efficient. It does require that the insects be well enough developed that the closure mechanisms function reliably. With embryos and their chorion, this solution does not work, necessitating a modification. This is not to say that the eggs do not have a waxy covering, because they do, but there are no functional spiracles associated with the chorion. Most terrestrial eggs, but not most eggs laid in water, have air-containing meshworks within the chorion. The chorionic meshwork contains a layer of gas, and has holes (aeropyles) that connect it to the outside. The holes, which measure less than a micron to several microns in size, provide continuity with the ambient atmosphere, allowing gas exchange. Their small size and small number help in water conservation. Often there are vertical columns within the chorion; they connect the external, relatively impervious layer of the chorion with the internal serosa (membrane covering of the embryo), and between the columns the gas is free to move. Not surprisingly, the chorionic meshwork system has undergone considerable modification in the different taxa, ranging from complex multi-layered systems to stalked aeropyles and the absence of meshwork. Eggs that are found in water or likely to be submerged often are adapted to function with the aid of a plastron. A plastron is a film (bubble) of gas that has an extensive water-air interface that aids in the extraction of oxygen from water. The plastron is usually held in place by hairs or meshworks, and largely maintains its volume during use. It functions as a physical gill; as the insect withdraws oxygen from the plastron the relative concentration of nitrogen increases, stimulating more oxygen to flow into the plastron from the surrounding water, and nitrogen to flow out of the plastron into the water. Aquatic insects with plastron respiration in their eggs are normally found in fast-flowing, oxygen-rich water

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or along the edges of ponds and lakes where the water level changes. It may seem surprising that terrestrial eggs also often have adaptations that allow plastron function, but it is not unusual for rain to wet eggs and the eggs to remain wet for hours or even days, so it is a useful adaptation even in the terrestrial environment. In addition to facilitating gas exchange and water conservation, the chorion must, in some cases, allow uptake of water or liquid nutrients from the environment. Hydropyles, structures that allow the uptake of water, are found on some eggs. Water is absorbed when the embryo is rapidly growing, and the egg enlarges in size. The eggs of most aquatic insects absorb water, but terrestrial insects that deposit their eggs where moisture may occur (e.g., grasshopper eggs in soil) also may have eggs that enlarge. The hydropyle is formed interiorly from the serosal (Fig. 14) layer, but may be visible externally by an extension of the chorion. Uptake of water sometimes causes the chorion to crack, leaving the embryo protected principally by the membranes. Some moisture can be absorbed from the air; partly desiccated eggs may reabsorb moisture from the air if the humidity is adequately high. On the outside of the chorion the female may also secrete glue that attaches the egg to a substrate. Also secreted in some cases are jelly-like materials, oothecae, pods, or egg cases containing

Eggs of Insects, Figure 14 Cross section of an egg shell of showing air-containing meshwork. Note that the chorionic columns support the outer layer of the eggshell (above) above the internal serosa (below). The air in the meshwork is connected to the outside by small holes (aeropyles) as shown (left center of diagram) (adapted from Hinton 1981).

the individual eggs. The glands that secrete these are known by various names including accessory, mucous, cement, and collateral glands.

Defenses of Eggs Various protective devices are evident in eggs, mostly to avoid predation. The defenses against predation can be grouped into three general types: deceptive devices, chemical protection, and mechanical protection. Most species seek to conceal their eggs. They may be deposited in soil, plant tissue, or beneath stones, for example. They may be cryptically colored to avoid being seen. Some are essentially transparent, so they resemble the substrate. Several Lepidoptera have eggs with a black spot apically, purportedly resembling eggs from which a parasite has emerged. Eggs strung together resemble plant organs such as tendrils. Egg deposited apically on a plant may appear to be seeds. Some eggs resemble plant galls (Fig. 15). Insects are sometimes poisonous or distasteful, so it is not surprising that chemicals are sometimes found on or in the eggs. For example, adult blister beetles (Coleoptera: Meloidae) are well known to contain cantharidin, and this occurs in the egg stage as well. Similarly, cardiac glycosides from milkweed plants deter birds from eating caterpillars, and their eggs are not only invested with these chemicals but they advertise their presence by being bright yellow colored. A few moths use the poisonous setae from the molted exoskeleton of the larval stage to protect their eggs by spreading the setae over the eggs. Mechanical protection of eggs can be gained by layering eggs with non-poisonous setae or scales. The moth Aesicopa patulana (Lepidoptera: Torticidae) rings its eggs with a palisade of erect scales. The ootheca of cockroaches (Blattodea) and mantids (Mantodea) deter predation by all but the most determined predators. Plant structures are useful mechanical barriers against predation. Bark beetles (Coleoptera: Curculionidae: Scolytinae) oviposit

Eggs of Insects

Eggs of Insects, Figure 15 Representative insect eggs: (a) fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae); (b) beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae); (c) garden fleahopper, Halictus brachtatus (Hemiptera: Miridae); (d) beet leafminer, Pegomya betae (Diptera: Anthomyiidae); (e) garden webworm, Achyra rantalis (Lepidoptera: Crambidae); (f) hop vine borer, H ydraecia immanis (Lepidoptera: Noctuidae) dorsal view; (g) hop vine borer, Hydraecia immanis (Lepidoptera: Noctuidae) lateral view; (h) greenhouse whitefly, Trialeurodes vaporariorum (Hemiptera:

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beneath bark, making access by predators difficult. Adults of the sugarcane rootstalk borer weevil, Diaprepes abbreviatus (Coleoptera: Curculionidae) oviposit between two leaves that are glued together; for access to the eggs, predators and parasitoids must penetrate the leaf tissue first. The chorion of a few eggs, such as those of range caterpillar, Hemileuca oliviae (Lepidoptera: Saturniidae) are so hard that many predators avoid feeding on them.

Size of Eggs Formerly, it was postulated that hemimetabolous (exopterygote) insects had proportionally more yolk available to the developing embryo and the neonates were well advanced in development, producing a young insect that closely resembled the adult form. In concert with this logic, holometabolous (endopterygote) insects were considered to be yolk-deficient, and the young were forced to hatch earlier in development, and therefore forced to produce young that were not miniature adults, but more embryonic in form. This line of reasoning is no longer accepted, and indeed there is no evidence that hemimetabolous insects produce larger eggs than holometabolous insects. Insect egg size is best correlated with the size of the female parent; large insect species typically produce larger eggs (Table 1). This is only a correlation, however, and there is considerable variation, as can be seen in the accompanying table, in which egg length is presented as a function of adult body length. Thus, micro type tachinid eggs are only about 1% of the length of the adult body, whereas at the other extreme, aphid eggs average 44% of the length of the adult.

To give insect egg size some perspective, consider that the length of a newborn human is about 50 cm, or 30% the size of the average human mother. If a human were to give birth to offspring in proportion to the size of aphids, it would measure 73 cm, nearly 50% larger. On the other hand, if humans gave birth to babies on the scale of some tachinid flies, they would measure only 2.2 cm, less than 5% of the length of the average newborn. Surely the range in insect egg size is considerable. It is difficult to determine which insects produce the smallest and largest eggs, due in part to Eggs of Insects, Table 1 Mean insect egg length as a proportion (%) of adult body length

No. of species

Mean

S.D.

3

1.35

1.3

17

2.15

1.1

Tachinidae (macrotype)

5

8.66

1.9

Pentatomidae

5

11.30

1.5

Tenebrionidae

4

11.56

3.8

Acrididae

5

13.09

2.9

Staphylinidae

5

13.90

1.8

Aphelinidae

4

14.34

3.1

Dermestidae

10

16.84

5.2

6

20.50

5.8

12

22.26

8.6

Muscidae

9

25.61

5.9

Lathridiidae

6

26.98

5.1

Anisotomidae

5

34.60

6.6

Aphididae

6

44.00

12.8

Tachinidae (microtype) Ephemeroptera

Psocidae Tettigoniidae

Adapted from Hinton 1981

Aleyrodidae); (i) alfalfa caterpillar egg, Colias eurytheme (Lepidoptera: Pieridae); ( j) harlequin bug, Murgantia histrionica (Hemiptera: Pentatomidae); (k) southern corn billbug, Sphenophorus callosus (Coleoptera: Curculionidae); (l) Eurytoma sp (Hymenoptera: Eurytomidae); (m) spotted asparagus beetle, Crioceris duodecimpunctata (Coleoptera: Chrysomelidae); (n) southwestern corn borer, Diatraea grandiosella (Lepidoptera: Crambidae); (o) range caterpillar, Hemileuca oliviae (Lepidoptera: Saturniidae); (p) Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae); (q) migratory grasshopper, Melanoplus sanguinipes (Orthoptera: Acrididae).

Eggs of Insects

the paucity of data but also because it can be calculated based on actual dimensions or on a proportional basis. Likely the smallest eggs are the microtype tachinid eggs, both in absolute terms and proportionally. For example, the eggs of Zenilla pullata (Tachinidae) are only 0.027 by 0.020 mm. However, more data on (Fig. 15) the eggs of some of the smallest insects such as trichogrammatids and mymarids (Hymenoptera) should be obtained, as these are especially minute insects. On the other extreme, the eggs of carpenter bees (Hymenoptera: Apidae: Xylocopinae) are reputed to be the largest, at least in terms of absolute size. For example, Xylocopa auripennis and X. latipes produce eggs that measure about 3.0 mm in width and 16.5 mm in length. These are large bees, but by no means are they particularly large insects. As noted previously, aphids likely produce the largest eggs if the size of the female is considered. Egg size is affected by latitude, particularly by mean temperatures. Insects occurring in cooler climates (closer to the north or south pole) tend to produce larger eggs than those inhabiting warm climates (closer to the equator), at least if comparisons are made within a species or closely related forms. At the coldest part of the range inhabited by insects, however, which is perhaps less hospitable, egg size begins to diminish. Thus, for most species, optimal (largest) egg size is at the cooler end of the range, but not the very coldest. Intraspecific variation in egg size at a single location or within a single egg cluster also occurs, though it is less well documented. Environmental quality affects mean egg size, as does maternal age. With poor food quality, inadequate food availability, or old age, insects tend to produce smaller eggs. There is also a heritability component to egg size; individuals developing from smaller eggs have longer development times, develop into smaller individuals, have a higher mortality rate, and produce smaller eggs. One might expect, then, that resource-limited female insects would produce only a smaller number of large eggs rather than produce any small eggs. However, optimal egg size

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(i.e., that which confers increased fitness), varies with environmental conditions. Thus, the traditional view that progeny from large eggs are qualitatively superior or more vigorous, though largely true, is subject to qualification. Phenetic variation results in production of progeny that are able to cope effectively with unpredictable but recurrent instabilities in their environment. In short, there are some circumstances when smaller eggs produce individuals that are more, not less, fit under those particular circumstances. Under cool weather conditions the larvae from some insects have been shown to be more fit. Also, the slower growing larvae from small eggs sometimes live longer, grow larger, and produce more eggs. Thus, there is selective pressure for variation in egg size.

Number of Eggs The number of eggs produced by a female insect (fecundity) varies considerably (Table 2). Undoubtedly, social insects are the most fecund. Although data on fecundity of social insects is often lacking, data on honey bees are reliable, so the estimate of up to 2,000 eggs per day, or 220,000 per year, or about 600,000 eggs in a lifetime seems reasonable. Termites, on the other hand, can produce 30,000 eggs per day and live 15–20 years, so their reproductive output is likely unsurpassed. Ants have a more modest reproductive output, perhaps several hundred eggs per year and 5,000–6,000 over the course of a lifetime. To maintain a stable population, a female need produce only two eggs that will result in reproductively successful adults. However, some species encounter extraordinary mortality, so they produce large numbers, as mentioned above. On average, most insects produce 50 to several hundred eggs, and their reproductive output is correlated with their life style (niche). The effects of life style and mortality rate are clearly demonstrated by beetles in the family Meloidae. Those that feed on grasshopper eggs (principally Epicauta spp.) are deposited by females after she

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Eggs of Insects

Eggs of Insects, Table 2 The mean number of eggs deposited by different insects Aeropus sibericuas (Orthoptera: Acrididae)

Number of eggs 30

Schistocerca gregaria (Orthoptera: Acrididae)

317

Locusta migratorioides (Orthoptera: Acrididae)

1000

Anechura bipunctata (Dermaptera: Forficulidae)

55

Pediculus pubis (Phthiraptera: Pthiridae)

26

Rhodococcus bulgariensis (Hemiptera: Coccidae)

1135

Geocoris punctipes (Hemiptera: Geocoridae)

178

Chrysopa oculata (Neuroptera: Chrysopidae)

185

Oryctes rhinoceros (Coleptera: Scarabaeidae)

90

Lyctus linearis (Coleoptera: Bostrichidae)

20

Carpophilus hemipterus (Coleoptera: Nitidulidae)

1071

Coccinella septempunctata (Coleoptera: Coccinellidae)

750

Leptintarsa decemlineata (Coleoptera: Chrysomelidae)

1300

Pediobius foveolatus (Hymenoptera: Eulophidae)

30

Ooencyrtus kuwanai (Hymenoptera: Encyrtidae)

224

Diatraea saccharalis (Lepidoptera: Crambidae)

300

Trichoplusia ni (Lepidoptera: Noctuidae)

500

Aedes aegypti (Diptera: Culicidae) Delia antiqua (Diptera: Anthomyiidae)

1360 123

Adapted from Hinton 1981.

has located a grasshopper egg pod in the soil. Thus, the likelihood of survival is relatively good because the meloid offspring do not have to search to find a host, and the female may deposit less than 100 eggs per batch. In contrast, those species that feed on bees must climb up on flowers and attach to a visiting bee to obtain a ride back to the bee’s cell where it can attack larval bees. This obviously is a more precarious existence, and such meloids produce 2,000–3,000 eggs per batch. Similarly, those tachinids that oviposit directly on hosts lay a few hundred eggs over the course of their life span, whereas those that scatter them about on food plants in hope that they will be consumed and infect a host insect produce many more eggs, perhaps 5,000–6,000. Some examples of fecundity are shown in the following table.

When considering intraspecific variation in fecundity, reproductive output is positively correlated with the size of the insect pupa or adult. High fecundity can lead to crowding and intraspecific competition for food resources, however, causing a reduction in pupal or adult mass and reduction in fecundity. Thus, in the absence of regulatory mechanisms such as specific parasitoids and disease, populations tend to cycle markedly, with periods of high fecundity preceding crowding and reduction of fecundity following crowding. The resulting low population, then, is freed from the competition and fecundity again cycles upward. Some insects seem to be competition limited, and demonstrate violent swings in abundance. More commonly, however, the swings in abundance are ameliorated by natural enemies.

Eggs of Insects

Mating normally stimulates oviposition, and females that are not mated usually delay oviposition, scatter their eggs in an abnormal manner, and lay fewer eggs. Not all species display this pattern of oviposition, however. Not surprisingly, those that display facultative parthenogenesis may not be influenced by mating status. But, surprisingly, some insects oviposit normally even when not mated and producing nonviable eggs.

··

Oviposition The site of egg deposition is incredibly varied, reflecting the vast diversity of life styles displayed by insects. Deposition ranges from apparently random, as when stick insects (Phasmida) drop eggs to the ground while feeding in tree tops, to highly selective, as when wasp (Hymenoptera) hyperparasites select specific locations on specific ages of parasitoids within specific hosts in specific habitats, and also check to determine that the prospective host is not already parasitized before ovipositing. Some of the interesting locations for egg deposition include: ··

··

··

··

Under water, glued to a substrate such as plant tissue. This is common among insects where both the adult and immature stages dwell in the water such as predaceous diving beetles (Coleoptera: Dytiscidae) and backswimmers (Hemiptera: Notonectidae). Dropped into water, or near the water and in a location likely to be flooded. This occurs in mosquitoes (Diptera: Culicidae), horse flies and deer flies (Diptera: Tabanidae), and caddisflies (Trichoptera). Deposited on or in a host insect. This is common among parasitic Hymenoptera and Diptera, and they may deposit their egg free within the host insect’s hemocoel, within a specific organ, attached to the body wall internally or externally, or only within a certain stage (e.g., the host egg). The parasitic insect oviposits on the host while the latter is flying. This requires that the female be

··

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equipped with claspers to hold the host while egg deposition occurs, as in thick-headed flies (Diptera: Conopidae). The insect is phoretic rather than parasitic, and oviposits on an insect to take advantage of the phoretic insect’s behavior. This occurs with human bot flies (Dermatobia hominis [Diptera: Oestridae]) in South America, which oviposit on mosquitoes that then seek out humans and other mammals, the eventual host of the bot fly. The truly clever aspect of this is that the bot fly egg hatches when the mosquito is blood-feeding, and falls onto the host where it burrows in and feeds. The female deposits her eggs on the back of the male, as in some giant water bugs (Hemiptera: Belostomatidae), which then provide aeration and protection for the eggs.

Distribution of Eggs Eggs can be deposited individually, in small clusters, or in large clusters. Often, ovipositional cues stimulate egg laying, and the cues may be physical, chemical or biological. Aggregation pheromones are among the best-known stimuli affecting oviposition. For example, bark beetles (Coleoptera: Curculionide: Scolytinae) release pheromones that, in conjunction with host plant volatiles, stimulate mass attack and oviposition, allowing the beetles to overcome the innate resistance of trees to attack, and facilitating survival of their brood. Indeed, many insects benefit from the mutual stimulation of feeding siblings, and are better able to overcome structural defenses of plants when they feed as part of a group. There may also be some benefits to gregariousness of young larvae because they are able to present a collective defense against predation. Plant allelochemicals deter feeding by generalist herbivores, but herbivore species that adapt to such chemical defenses often come to use the defensive chemicals as attractants, feeding stimulants and oviposition stimulants. Other factors affecting egg laying include host sex pheromones,

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host-produced sounds, surface texture, surface color, and light intensity.  Allelochemicals  Embryogenesis  Oogenesis  Gregarious Behavior in Insects  Mosquito Oviposition  Parental Care in Heteroptera  Phenotypic Plasticity

References Capinera JL (1979) Qualitative variation in plants and insects: effect of propagule size on ecological plasticity. Am Nat 114:350–361 Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369 Hinton HE (1981) The biology of insect eggs. Pergamon Press, Oxford, UK, 1500 pp

Ehrlichiosis A disease caused by one of several rickettsial organisms in the genus Ehrlichia.  Ticks

Eickwort, George C George Eickwort was born in New York City on June 8, 1940. An early interest in entomology persuaded him to study at the University of Michigan, where he obtained a B.S. in 1962 and M.S. in 1963. He then went to the University of Kansas and obtained a Ph.D. in 1967. He was hired as assistant professor in the Department of Entomology of Cornell University. He was heavily involved in teaching at undergraduate and graduate levels, and in 1986 received a Distinguished Achievement Award in teaching from the Entomological Society of America. He guided 24 Ph.D. and six M.S. students. His research centered on Halictidae (sweat bees). In summers, he taught at the Rocky Mountain Biological Laboratory. He died in a car accident in Jamaica on July 11, 1994.

Reference Brown WL, Franclemont JG, Tauber MJ, Liebherr JK (1995) George C. Eickwort. Am Entomol 41:190–191

Ejaculatory Duct A median duct or tube (Fig. 16) that carries sperm from the region of the testes to the exterior of the insect.  Reproduction  Testis

Elachistidae A family of moths (order Lepidoptera). They commonly are known as grass miner moths.  Grass Miner Moths  Butterflies  Moths

Elasmidae A family of wasps (order Hymenoptera).  Wasps Mesadene Ectadene

Testis lobe

Seminal vesicle

Vas deferens Ejaculatory duct

Ejaculatory Duct, Figure 16 Diagram of a male reproductive system as found in Tenebrio (Coleoptera) (adapted from Chapman, The insects: structure and function).

Elm Leaf Beetle, Xanthogaleruca (=Pyrrhalta) Luteola (Müller) (Coleoptera: Chrysomelidae)

 Ants  Bees  Sawflies

Elephantiasis Obstruction of the lymphatic vessels due to infection by nematodes that are transmitted by mosquitoes.  Human Lymphatic Filariasis

Elateridae A family of beetles (order Coleoptera). They commonly are known as click beetles, though many of the larvae are known as wireworms.  Beetles

Elateriform Larva A larva that is heavily sclerotized, with few body hairs and short legs. Such larvae resemble wireworms (Elateridae).

Elfins Some members of the family Lycaenidae (order Lepidoptera).  Gossamer-Winged Butterflies  Butterflies  Moths

Elipsocidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids

Elaters Members of Coleoptera).  Beetles

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the family Elateridae (order

Elbowed Antennae Antennae with a long basal segment, and additional smaller segments extending at a distinct angle (sometimes ninety degrees) from the basal segment. Such antennae are common among ants.  Antennae of Hexapods

Electrophoresis The separation of molecules in an electric field. Electrophoresis can be used to separate proteins or DNA molecules.

Elenchidae A family of insects in the order Strepsiptera.  Stylopids

Elmidae A family of beetles (order Coleoptera). They commonly are known as riffle beetles.  Beetles

Elm Leaf Beetle, Xanthogaleruca (=Pyrrhalta) luteola (Müller) (Coleoptera: Chrysomelidae). Steve H. Dreistadt University of California, Davis, CA, USA The elm leaf beetle is the primary defoliator of elm trees. Its range includes Canada, Central Asia, Europe, the Middle East, North Africa, Siberia and the United States. More recently, this insect has become established in Australia and South America. The elm leaf beetle feeds only on elms (Ulmus spp.) and occasionally, on Zelkova serrata, also an Ulmaceae. Other key pests that attack only elms include the European elm scale, Gossyparia spuria

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(Modeer); the European elm bark beetle, Scolytus multistriatus (Marsham); and Dutch elm disease, Ophiostoma (=Ceratocystis) ulmi (Buisman), a pathogen vectored by the elm bark beetle. However, there is great variability in pest susceptibility among and within elm species. Elms of Asian origin generally are more resistant (in some instances virtually immune) to both the elm leaf beetle and Dutch elm disease, while many Eurasian and North American elms are highly susceptible. Many pest-resistant elm cultivars have been developed and elms continue to be selectively bred to replace the hundreds of thousands of American elms, Ulmus americana, killed by Dutch elm disease. Elm leaf beetle larvae skeletonize the lower leaf surface, while the adults chew entirely through the leaf, often in a shot hole pattern. Defoliation eliminates summer shade, reduces the aesthetic value of trees and causes annoying leaf drop. Repeated, extensive defoliation weakens elms, causing the trees to decline. Severe defoliation possibly increases tree susceptibility to elm bark beetles and Dutch elm disease. The adult beetles are about 8 mm long and are olive-green with black margins on each wing cover. The females lay yellowish eggs in double rows of about 5–25 on the underside of leaves. Each egg is about 1 mm wide and 1.5 mm tall and becomes grayish before hatch. The larvae appear black initially, but after feeding, become a dull yellow or green with rows of tiny, dark tubercles (projections). The larvae develop through three instars (Fig. 17). Third instars are up to about 1 cm long and have dense rows of dark tubercles that resemble a black stripe down each side, making them easy to distinguish from first- and second-instar larvae. The pupae are about 6 mm long and are bright yellow to dull orange in color. Adult elm leaf beetles commonly overwinter in bark crevices, litter, woodpiles, or in buildings. The adults fly to foliage in the spring to feed and lay eggs. After feeding in the canopy for several weeks, mature larvae crawl down the tree trunk, become curled inactive prepupae, and then develop into yellowish pupae. After about 10 days, the adult

beetles emerge from the pupae around the tree base and fly to the canopy to feed and (during spring and summer) lay eggs. The elm leaf beetle has about two annual generations in much of its range, but this varies with weather and location. For example, typically there is only one complete generation a year in northeastern California, while up to three generations can occur in central and southern California. Temperature monitoring can predict the seasonal emergence of adults and when each life stage occurs in the field, but are locationspecific. Good cultural care of trees is an essential component of integrated pest management. Many European and American elm species are adapted to summer rainfall and require proper irrigation to grow well in Mediterranean climates such as California and parts of Australia. Avoid pruning elms during the spring and summer as the European elm bark beetle is attracted at this time to fresh pruning wounds, and can introduce Dutch elm disease. If planting or replacing elms, consider using cultivars resistant to both Dutch elm disease and the elm leaf beetle (e.g., “Frontier,” “Prospector”). Avoid elms that are highly susceptible to both the elm leaf beetle and Dutch elm disease (e.g., English elm, Ulmus procera, and Scotch elm, U. glabra). Several natural enemies kill elm leaf beetles, but generally do not provide adequate control by themselves. A small, black tachinid fly, Erynniopsis antennata, oviposits on larvae, feeds inside, and emerges from mature beetle larvae or prepupae. Erynniopsis antennata is native to Eurasia and has been introduced in parts of the United States. Its black to reddish, cylinder- or teardrop-shaped pupae occur during spring and summer at the base of trees. Erynniopsis antennata overwinters in adult beetles, emerging as adults in spring, although this is not readily observed. Erynniopsis antennata is the most important elm leaf beetle parasitoid in California, but its effectiveness is limited by a secondary parasitoid, Baryscapus (=Tetrastichus) erynniae, and some apparent asynchrony between the host and the parasite life cycles.


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Egg cluster

First instars

Adult Second instar

Pupa Prepupa

Third instar

Elm Leaf Beetle, Xanthogaleruca (=Pyrrhalta) Luteola (Müller) (Coleoptera: Chrysomelidae), Figure 17 Elm leaf beetle stages and life cycle. adult, larvae: L.O. Howard. 1895. The shade-tree insect problem in the eastern United States. The Yearbook of Agriculture. USDA. Washington, DC. eggs, prepupa: F. Silvestri. 1910. Contribuzioni alla conoscenza degli insetti dannosi e dei loro simbionti. Bollettino del Laboratario di Zoologia Generale e Agraria Portici 4:246–288. pupa: G.W. Herrick. 1913. Control of two elm-tree pests. Cornell University Agricultural Experiment Station Bulletin 333.

Oomyzus (=Tetrastichus) brevistigma para sitizes mature elm leaf beetle larvae and pupae. One or more small, round holes in the beetle pupae can indicate where this parasitoid has emerged. This species is of uncertain origin, but is the most important elm leaf beetle parasitoid in the eastern United States. Oomyzus brevistigma can be laboratory-reared in large numbers and cold-stored for several weeks, suggesting it is a good candidate for inundative biological control of its host. An egg parasitoid, Oomyzus (=Tetrastichus) gallerucae, occurs in Eurasia and scattered locations where it has been introduced in the United States. It leaves round holes when it emerges from the beetle eggs, which remain golden. When the beetle larvae have emerged, the egg shell is whitish

with more ragged holes. Erynniopsis antennata and Oomyzus brevistigma have been introduced to Australia and Argentina in an effort to provide classical biological control of the elm leaf beetle. Historically, this pest was managed by foliar application of broad-spectrum insecticides, including lead arsenate beginning in the late 1800s, DDT starting in the 1940s, and more recently, various organophosphates (e.g., acephate and malathion), carbamates (carbaryl) and pyrethroids (e.g., bifenthrin, fluvalinate). Current recommendations are to use an integrated program that incorporates resistant elms, good cultural practices, conservation of natural enemies and regular monitoring. For example, presence-absence egg sampling can be used in California to predict the extent of defoliation and treatment need based on the

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Elongate-Bodied Springtails

percentage of one-foot branch terminals infested with beetle eggs. If needed, controls include foliar spraying with Bacillus thuringiensis subspecies tenebrionis, or spot application to bark (bark banding) with a broad-spectrum insecticide to kill larvae migrating down the trunk. Systemic insecticides (e.g., abamectin, imidacloprid) that are applied without spraying minimize environmental contamination, and if applied to soil, avoid the tree injury that occurs during injecting or implanting insecticide into roots or trunks. Where beetles entering buildings to overwinter is a problem, they can be excluded by screening openings and sealing exterior cracks and crevices. University Cooperative Extension services can provide more specific pest management recommendations.

Hamerski MR, Hall RW, Keeney GD (1990) Laboratory biology and rearing of Tetrastichus brevistigma (Hymenoptera: Eulophidae), a larval-pupal parasitoid of the elm leaf beetle (Coleoptera: Chrysomelidae). J Econ Entomol 83:2196–2199 Miller F, Ware G (1999) Resistance of elms of the Ulmus davidiana complex to defoliation by the adult elm leaf beetle (Coleoptera: Chrysomelidae). J Econ Entomol 92:1147–1150

Elongate-Bodied Springtails A family of springtails (Hypogasturidae) in the order Collembola.  Springtail

Elytron (pl. elytra)

References Dahlsten DL, Rowney DL, Lawson AB (1998) IPM helps control elm leaf beetle. Calif Agric 52:18–24 Dreistadt SH, Dahlsten DL (1990) Relationships of temperature to elm leaf beetle (Coleoptera: Chrysomelidae) development and damage in the field. J Econ Entomol 83:837–841 Dreistadt SH, Dahlsten DL, Lawson AB (2001) Elm leaf beetle. University of California DANR Pest Notes Publi cation 7403. Available at http://www.ipm.ucdavis.edu/ PMG/PESTNOTES/pn7403.html (accessed 10 March 2008), http://www.ipm.ucdavis.edu/PMG/selectnewpest. home.html

The thickened front (Fig. 18) wing of beetles, serving primarily for protection of the hind wings or flight wings.  Wings of Insects

Elytron/Femur Ratio (E/F) The ratio of the length of the front wing (more correctly called tegmen) to the length of the femur. Left elytron

Pronotum Compound eye Femur

Tibia

Coxa Trochanter

Pretarsus

Antenna “Beak” Tarsus

Mouth parts

Elytron(pl. elytra), Figure 18 Side view of a weevil (Curculionidae).

Embryogenesis

This character is used to determine the morphological phase status of locusts.

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Embryogenesis Susanne D. Dyby Beaulieu-sur-mer, France

Emarginate A structure that is indented or notched.

Embiidae A family of web-spinners (order Embiidina).  Web-Spinners

Embiidina An order of insects, formerly known as Embioptera. They commonly are known as web-spinners.  Web-Spinners

Embolium The leading edge of the corium region (Fig. 19) on the hemelytra of Hemiptera.  Wings of Insects

Embioptera  Embiidina

Embryogenesis in insects starts with an intricate, ordered building of the egg by the female. The female fills an egg with cytoplasm and yolk, beginning with the future posterior end of the embryo. The egg also is supplied with cytoplasmic determinants by the mother, and specific types of determinants are more concentrated in one end of the egg than the other. Cytoplasmic determinants are ribonucleic acid particles (RNPs) that code for transcription or translation factors, gene regulators, growth factors, kinases and other enzymes. These cytoplasmic determinants specify the anterior-posterior and the dorsal-ventral body axes: they initiate a developmental sequence that activate specific zygotic regulatory genes in a region-specific pattern. This pattern narrows and becomes refined with time, because each new set of activated genes allows the establishment of more developmental fates, and for an increasingly precise allocation of fates within each region. In many holometabolous insects, the basic body plan of the larva is specified very early in development, before and during the cellular blastoderm stage. Some of the genes that regulate early development are known as “gap genes,” “pair rule genes” and “homeobox genes.” Along the ventral-dorsal axis in hemimetabolous and

Embolium

Cuneus

R

Sc

r-m

M

R-M

M

M Corium

Cu 1A

Fracture

P

Membrane

Cu 1A

Clavus Anal ridge

Embolium, Figure 19 Front wing of a bug (Hemiptera: suborder Heteroptera), thickened basally and membranous distally.

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Embryogenesis

holometabolous insects, the future mesoderm lies ventral-most. Ventrolaterally lies a band of nuclei/cells committed to neural development, and located more dorsally is the ectoderm and extraembryonic ectoderm. Endoderm is derived from a small region anterior and posterior to the mesoderm as well as from the inner yolky region of the egg. The initial allocation of fates along the anterior-posterior axis is set by gap genes, which code for regulatory proteins. Gap genes divide the embryo into several large regions (loss of a functional gap gene leads to a loss of a large portion of the body). Gap genes induce, but also restrict the expression domains of primary pair rule genes, narrowing these domains to a bisegmental pattern. The primary pair rule genes induce other pair rule genes. Each pair rule gene has a bisegmental pattern of activity that overlaps some, but not all, of the other domains. Their combined expression patterns create a series of stripes and establish the segmental nature of the insect body. Pair rule genes activate segment polarity genes that maintain anterior to posterior patterning within each segment. Segment polarity genes must remain active until the adult stage. Gap genes and pair rule genes also activate homeobox genes (e.g., selector genes) that regulate the anatomical characteristics of segments. Within each insect segment, one finds that each nucleus has received an almost unique developmental address. Such positional information collectively builds an organized body plan. A number of genes that set up the body axes and segments in Drosophila have conserved functions in a diversity of animals from centipedes and horseshoe crabs to other hemimetabolous and holometabolous insects, and likewise vertebrates and humans. Although developmentally crucial genes in hemimetabolous orders are similar to those in holometabolous embryos, their temporal expressions are different. Hemimetabolous embryos may take more than two months to complete embryogenesis at room temperature. In hemimetabolous insects, the onset of pattern

f ormation is not simultaneous across the entire body, but proceeds in an anterior to posterior direction. In orders such as Blattodea, Dermaptera, Isoptera, and Embiidina, segments are added by means of posteriorly directed growth and must include de novo DNA synthesis. In others orders such as Phasmida, Orthoptera and Hemiptera, the basic body regions are unrefined but present. Segments develop larger size and anatomical complexity one by one. In contrast, a Drosophila larva breaks out of its egg shell approximately 22 h after fertilization. In such quickly developing insects, segmentation proceeds almost simultaneously across the body. Insect cells have been thought of as having a mosaic form of development, that is, exhibiting a fixed and invariant commitment to a particular fate that is not altered by, for example, transplantation to other regions of the embryo, even during early embryogenesis. In holometabolous orders, this specificity is due to the flurry of genetic activity that occurs during early development (described briefly above). However, some embryonic tissues from holometabolous insects are able to regulate, i.e., develop variably in response to the surrounding cells. For instance, cell-cell communication between different cell types is essential for normal development of the midgut and mesoderm. In hemimetabolous insects, there is a far greater ability within the egg to regulate the cells’ final fate. Krause’s experiments with stone crickets (Gryllacrididae, Orthoptera) induced embryonic twinning, partial duplications, and triplications, thereby demonstrating that embryonic cells produced flexible responses to new developmental circumstances. Early development in animals is characterized by cleavage divisions, whereby the single large egg is subdivided into a host of small cells, which is followed by morphogenetic movements that reshape the embryo. Insects are special in that they undergo 10–13 rounds of nuclear divisions before forming cells. Most nuclei migrate to the periphery of the egg, and cells are formed when the egg’s plasma membrane folds inward to separate and

Embryogenesis

enclose individual nuclei. The cellularization process takes approximately one hour in Drosophila (Fig. 22), but in other insects there can be regionspecific differences in the onset of cell formation. The cellularization process produces the cellular blastoderm, consisting of an embryonic and extraembryonic component. In termites (Isoptera) and walking sticks (Phasmida), an uneven distribution of nuclei precedes the separation into the embryo and extraembryonic tissue after the cellular blastoderm stage. In other hemimetabolous orders (for example, Odonata, Plecoptera, Orthoptera) and in most holometabolous insects, the distribution of nuclei is practically uniform. However, in parasitic Hymenoptera, cleaving nuclei associate into clusters and form cells. Each cluster gives rise to one embryo, and two (as in Platygastridae) to 1,500 (as in Encyrtidae) young can emerge from a single egg. This phenomenon of polyembryony is another example of regulative, as opposed to mosaic development, within holometabolous orders. Most insect eggs have a substantial amount of yolk that lies to the interior of the cellular blastoderm (Fig. 20). Eggs of hemimetabolous insects tend to contain more yolk than eggs of holometabolous insects. Insects are defined as

100% EL

EL = egg length

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engaged in meroblastic cleavage – incomplete cleavage of the yolky region, and in superficial cleavage – the yolk lies interior to the cellular blastoderm, filling the central region of the egg. Extraembryonic cells develop into the serosa that line the inner surface of the egg, the amnion that encloses the embryo, and vitellophages and yolk cells. Vitellophages will form a provisional inner lining of the future midgut and aid in the digestion of yolk. They are usually digested before hatching, but may become incorporated into the epithelial lining of the gut in Odonata. In Drosophila, signals from yolk nuclei (vitellophages or yolk cells) are essential for the proper cell migration by prospective gut tissue so that a digestive tube is formed. Morphogenesis, the creation of form, describes the cell movements that must take place to create an ordered body plan. At the blastoderm stage (Fig. 21), the embryo consists of a single layer of cells. In hemimetabolous insects, the separation between the extraembryonic component and the embryo involves a convergence of the embryonic cells toward the ventral and posterior side of the egg. In holometabolous insects like coleopterans, lepidopterans and dipterans, embryonic cells also converge toward the ventral side, but this

75%

0%

100 µm

Embryogenesis, Figure 20 Cellular blastoderm stage in the fruit fly Drosophila m elanogaster. Anterior region is to the left and the dorsal side is up (Scanning electron micrograph by S. Dyby).

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Embryogenesis

Embryogenesis, Figure 21 Steps in the early embryogenesis of insects. Top row: v entral view of egg, anterior end up. Bottom row: diagrammatic cross sections at the levels indicated by bars in top row. (a) Multiplication and migration of nuclei within the ooplasm. (b) Cellularization of the s uperficial part of the ooplasm. The resulting blastoderm initially consists of uniform cells but soon regional differences in cell density and shape indicate segregation into germ anlage and prospective e mbryonic covers. (c) The prospective mesoderm starts to invaginate along the midline of the germ a nlage (gastrulation). (d) Germ band after gastrulation, with segment borders and amniotic folds f orming. The folds shown over head lobes (top) and abdomen approach each other and finally fuse, thereby c losing the amniotic cavity. (e) Advanced germ band stage, with appendage buds, transient coelom anlagen, and amniotic cavity (Modified from Sander, 1976). 2h30’

30

1

4 3h15’

1h10’

2

5 1h30’

3

2h30’

5(1)

5(2) 5(3) 3h15’ 2h45’ 3h

Embryogenesis, Figure 22 Early development of a fly embryo, showing stages from 1 to 5 (Modified from Lawrence, 1992).

migration movement occurs in concert with an extension movement along the anterior-posterior axis that dramatically lengthens the embryo, now described as the germ band. Germ band elongation allows for body segmentation to take place

without a process of segment-by-segment addition. This is defined as a long-germ band development. In contrast, when the majority of body segments forms one after the other, this is described as the short-germ band type.

Embryogenesis

The germ band develops an inner mesodermal and outer ectodermal cell layer during gastrulation. The entire mesodermal cell sheet invaginates, that is, the cell sheet buckles inward in some species; in others, mesodermal cells ingress individually once a midventral groove has formed by means of cell shape changes. The mesodermal cells rearrange to line the inner surface of the ectoderm, then engage in cell divisions. They form segmentally reiterated clusters of cells called somites. The ventral-most component of the somites – the visceral or splanchnic mesoderm – will differentiate into the musculature of the midgut, fat body, gonads, and blood, whereas the rest – the somitic mesoderm – form segmental muscles, the dorsal vessel (heart muscle), and musculature of the foregut, hindgut and genitalia. Limb musculature is derived from the ventrolateral region of the somites. Cephalic mesoderm contributes to the musculature of the head, pharynx, mouthparts and the anterior portions of the foregut. A ventrolateral region of the ectoderm is neurogenic and gives rise to the nervous system. In hemimetabolous embryos, neuroblasts generally ingress while the mesodermal somites are forming and each region of the germ band matures. In holometabolous embryos, neuroblasts ingress just after the mesoderm cells line the inner surface of the ectoderm, that is, after gastrulation and an accompanying rapid elongation of the germ band. In the procephalic region where the brain develops, the neuroblasts stay on the surface longer. Ingressed neuroblasts divide several times and give rise to ganglion mother cells. The latter divide symmetrically or asymmetrically, with the asymmetrical division producing a ganglion cell or neuron. Neuroblasts and ganglion cells associate into neuromeres, which are segmentally reiterated cell clusters separated by intersegmental ridges. The neuromeres become connected by axonal bundles that build longitudinal connectives and transverse commissures. This early arrangement of the central nervous system is altered by fusion of specific neuromeres to bring about the final arrangement of ganglia. The

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optic lobes of the brain connect to two thickened ectodermal cell plates that develop into lateral ocelli. An extensive peripheral nervous system is established, beginning with the appearance of somatic muscle cells and the progenitors of sensory cells. The rest of the ectoderm turns into epidermis, apodemes, glands, sensory organs, tracheal system, Malpighian tubules, and epithelia of the foregut and hindgut. The non-neurogenic ectoderm cells tend to stay connected as a cell sheet (epithelium) so that the primary morphogenetic changes occur by epithelial invaginations or evaginations. Limb formation and gnathal appendages begin as an evagination or a budding outward by the ectoderm. The Malpighian tubules begin as flat outpocketings of the hindgut epithelium and elongate into long convoluted tubes during late embryogenesis. The salivary glands derive and invaginate from the labium. They elongate into two long tubes that join into a common duct by the labium. The first invaginations of the tracheal system appear as tracheal pits, one for each thoracic and abdominal segment. Further internal tracheal branching continues by invagination, cell migration, and rearrangements. Cell fusions produce the final tracheal network, followed by deposition of cuticle and tanning. The insect gut consists of the foregut, midgut and hindgut. Aspects of gut development are similar across most insect orders, although the final anatomy and physiology of the gut vary with the type of food that the juvenile insect ingests, digests, absorbs, and excretes. The gut primordia are found at the anterioventral side of the embryo and at its posterior extremity. The primordia invaginate and involute during or just after gastrulation, forming hollow sacs. The innermost part of these sacs is endoderm, which dissociates from the prospective foregut and hindgut and migrates along the inner body wall and comes in contact with the visceral mesoderm that becomes the musculature of the midgut. Together with the visceral mesoderm, the midgut endoderm forms a tube around the yolk that lies inside the embryo. The encircling of the

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Embolemidae

yolk proceeds in a ventral to dorsal direction. The foregut and hindgut epithelium are ectoderm derivatives, whereas most of the midgut epithelium is endodermal in origin. The anterior portion of the midgut epithelium has both endoderm and ectoderm contributing to gastric caeca, outpocketings of the gut that often harbor a bacterial community. The foregut and hindgut musculature differentiates before the midgut is entirely formed. In lepidopterans, the contractions of foregut and hindgut help turn and reposition the embryo within the extraembryonic membranes during mid-embryogenesis. The stomodael nervous system derives from the dorsal roof of the foregut, and develops into the endocrine glands, corpora cardiaca and corpora allata, a frontal ganglion, connectives, and a recurrent nerve that loops back to the brain. The germ band is open dorsally in both hemiand holometabolous orders. The amnion covers this dorsal opening, and is replaced by embryonic cells during a process called dorsal closure. The ectodermal cells rearrange and migrate dorsally, as do the cardioblasts and the midgut mesoderm and endoderm. In insects with long-germ band development, dorsal closure is preceded by germ band shortening. The germ band not only shortens, but also expands, and the embryo takes up room previously occupied by yolk. Once dorsal closure is completed, it is tissue organization and differentiation, rather than morphogenetic reshaping of the germ band, that occupies most the time left before the juvenile insect hatches from its egg. In lepidopterans and other orders, an embryonic molt of newly formed cuticle occurs during late embryogenesis. Tanning and pigmentation occur in the tracheal tree, mouthparts, head capsule, setae, integument, and other cuticular elements. Diapause is common during the egg stage. A complex mix of environmental and genetic factors influence the female’s laying of eggs that are capable of diapause. The stage of developmental arrest is usually determined genetically and may occur during early, mid-, or late embryogenesis.

Some insects can withstand drying-out. The eggs of some African locusts, for example, remain viable after three years of desiccation.  Diapause  Endocrine Regulation of Insect Reproduction  Oogenesis  Nervous system  Reproduction  Sterile Insect Technique

References Anderson DT (1972) The development of hemimetabolous insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects, vol 1. Academic Press, London, UK, pp 95–163 Anderson DT (1972) The development of holometabolous insects. In: Counce SJ, Waddington CH (eds) Developmental systems: insects, vol 1, Academic Press, London, UK, pp 165–242 Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer Verlag, Berlin, Germany, 405 pp Counce SJ (1972) The causal analysis of insect embryogenesis. In: Counce SJ, Waddington CH (eds) Developmental systems: insects, vol 2. Academic Press, London, UK, pp. 2–125 Kalthoff K (1996) Genetic and molecular analysis of pattern formation in the Drosophila embryo, Ch 21. Analysis of biological development, 1st edn. McGraw-Hill, New York, NY, pp 493–542 Patel NH, Hayward DC, Lall S, Pirkl NR, DiPietro D, Ball EE (2001) Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 129:3459–3472 Sander K (1984) Embryonic pattern formation in insects, Ch 10. In: Malacinski GM, Bryant SV (eds) Pattern formation: a primer in developmental biology. Macmillan, New York, NY Walker SS, Lee KK, Descai RN, Erickson JW (2000) The Drosophila melanogaster sex determination gene sisA is required in yolk nuclei for midgut formation. Genetics 155:191–202

Embolemidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

Emperor Moths (Lepidoptera: Saturniidae)

Embonychidae A family of web-spinners (order Embiidina).  Web-Spinners

Emergence Escape of the adult from the body covering of the terminal immature stage or pupa; sometimes used to describe eclosion.

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by his s econd wife, Eleanor, whom he married in 1950. His termite collection of about a million specimens, representing 1,745 species, was given to the American Museum of Natural History.

Reference Wilson EO, Michener CD (1982) Alfred Edwards Emerson December 31, 1896 – October 3, 1976 [with bibliography]. National Academy Press, Biogr Mem 53:159–176

Emery’s Rule Emerson, Alfred Edwards Alfred Emerson was born in the state of New York, USA, on December 31, 1896. He moved with his parents to Chicago in 1905. In a family of artists, he was the first scientist. In 1914 he went to Cornell University with the objective of studying poultry science, but chose entomology instead. While he was at Cornell, he visited the New York Zoological Station in Guyana, met zoologist William Beebe, and at the latter’s suggestion began to study termites. In 1920, he completed his M.A. degree, married, and took his new wife on his second trip to Guyana. A third trip followed, in 1924, but meanwhile he had in 1921 accepted a position as instructor at the University of Pittsburgh. He completed requirements for a Ph.D. degree from Cornell in 1925, then moved to the University of Chicago, where he stayed for the rest of his career. His major contribution to entomology was the over 100 papers he published on the systematics, phylogeny, distribution and natural history of termites, including fossil species. He co-authored (1949) “Principles of animal ecology” which was the major North American text on the subject of its time. But, his first wife died of a heart condition that year. He received numerous awards and was elected to the National Academy of Sciences in 1962. He died in New York state on October 3, 1976, survived by two children from his first marriage and

This postulates that in colonies of social insects, their social parasites are similar in appearance to the hosts and closely related phylogenetically.

Emigration Movement of individuals out of an area to another location (contrast with immigration).

Emperor Moths (Lepidoptera: Saturniidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Emperor moths, family Saturniidae (also called giant silk moths, and including Buck moths, io moths, and royal moths), include 1,435 species worldwide, but are predominately Neotropical (860 sp.). The family is in the superfamily Bombycoidea (series Saturniiformes), in the section Cossina, subsection Bombycina, of the division Ditrysia. There are seven subfamilies: Arsenurinae, Ceratocampinae, and Hemileucinae are all New World, plus Agliinae (Palearctic), Ludiinae (Afrotopical), Salassinae (Oriental), and Saturniinae.

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Emperor Moths (Lepidoptera: Saturniidae)

The larger species, in the subfamily Saturniinae, are more diverse in Africa (225 sp.) and tropical Asia (125 sp.), yet are the only subfamily found in all regions of the world. Hemileucinae forms the largest subfamily, with 630 species, mostly Neotropical. Adults medium size to very large (30–300 mm wingspan), with head vertex roughened; haustellum absent or short; labial palpi short; maxillary palpi vestigial; antennae bipectinate (some actually quadripectinate), smaller in females; body robust, with long hair-like scales. Wings broadly triangular, often with apex falcate (especially in males of some genera), or more rounded; hindwings rounded but sometimes with tails (sometimes extremely long) (Fig. 23). The longest hindwing tail lengths are about 130 mm (not counting the basal area of the hindwing), equally long and thin in the Neotropical genus Copiopteryx and in the African genus Eudaemonia, and

long but wider tails in the giant Madagascan Argema. Maculation various, but mostly shades of brown with eyepots (sometimes hyaline) and terminal border bands, or white with spots, or other coloration; hindwings often with large eyespots (especially in Hemileucinae). Adults mostly nocturnal or crepuscular, but some are diurnal. Larvae are leaf feeders and many are polyphagous, some being communal or gregarious; many are extremely large. Many larvae have bizarre spines and scoli; many are urticating (especially in Hemileucinae). Host plants are extremely varied, particularly in broadleaf forest tree families, but at least 48 plant families are involved. Some species are economic for agriculture, but major urticating larvae are involved in dermatitis and more severe allergic reactions (the most toxic seem to be the genus Lonomia in Brazil), and in a few cases even from adult scales.

Emperor Moths (Lepidoptera: Saturniidae), Figure 23 Examples of Emperor moths (Saturniidae): top left, (subfamily Hemileucinae), Automeris cecrops (Boisduval) from Arizona, USA; top right, Hemileuca maia (Drury) from Florida, USA; lower left, (subfamily Saturniinae), Actias luna (Linnaeus) from Florida, USA; lower right, Hyalophora cecropia ( Linnaeus) from Florida, USA.

Encephalitis

References D’ Abrera B (1995–1998) Saturniidae mundi: saturniid moths of the world, 2 vol. Goecke & Evers, Keltern Lemaire C (1978–2002) Les Saturniidae Américains, the Saturniidae of America. Los Saturniidae Americanos, Neuilly-sur-Seine (1978 vol 1; 1980 vol 2); Museo Nac. Costa Rica, San Jose. (1988. Vol. 3); Goecke & Evers, Keltern (2002. Volume 4). Peigler RS, Wang HY (1996) Saturniid moths of Southeastern Asia. Taiwan Museum, Taipei, 262 pp Pinhey ECG (1972) The emperor moths of South and Central Africa. C. Struik, Capetown, 150 pp, 43 pl *Seitz, A. (ed.). (1911–1928). Familie: Saturniidae. In: Die GrossSchmetterlinge der Erde, 2:209–226, pl. 31–34 (1911); 2 (suppl.):129–133, pl. 11, 14 (1932); 6:713–827, pl. 101–137, 142 (1929–30); 10:497–520, pl. 52–56 (1926–28); 14:313–347, pl. 48–59 (1927). A. Kernen, Stuttgart Tuskes PM, Tuttle JP, Collins MM (1996) The wild silk moths of North America: a natural history of the Saturniidae of the United States and Canada. Cornell University Press, Ithaca, NY, 250 pp, 30 pl

Empididae A family of flies (order Diptera). They commonly are known as dance flies.  Flies

Empusidae A family of praying mantids (Mantodea).  Praying Mantids

Empodium A single spine or pad-like structure found between the tarsi of Diptera.  Legs of Hexapods

Emulsifier A surfactant used to stabilize the distribution of one liquid in another (i.e., create an emulsion).

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Emulsion A pesticide formulation in which droplets of one liquid are dispersed within another liquid (e.g., oil in water).

Emulsifiable Concentrate An insecticide formulation in which an emulsifying agent has been added to allow an active ingredient and solvent that normally would not mix with water to be effectively dispersed in water.

Encapsulated Pesticide Enclosure of a small amount of pesticide within a covering such as polyvinyl to provide controlled (prolonged) release of the toxicant. Such formulations are also referred to as micro-encapsulated.

Encapsulation The enclosure of an invader, usually a parasitoid larva, within the blood of the host insect by a layer of hemocytes.

Encephalitis A group of arthropod-borne viruses (arboviruses) affecting the nervous system of vertebrate animals, including humans. Often these viruses are spread by mosquitoes. Signs and symptoms of infection include stiff neck, headache, confusion, rash, fever, arthritis, inflammation of the brain, coma, paralysis, and death. Some of the viruses and diseases include: Alphaviruses Eastern equine encephalitis

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Encyrtidae

Western equine encephalitis Venezuelan equine encephalitis Flaviviruses St. Louis encephalitis Japanese encephalitis West Nile fever Yellow fever Dengue Bunyaviruses LaCrosse encephalitis Reoviruses Colorado tick fever African horse sickness viruses Although vaccines are available for some arboviruses, prevention hinges mostly on limiting or eliminating exposure to blood-feeding arthropods.  Dengue  Eastern Equine Encephalitis  Japanese Encephalitis  Lacrosse Encephalitis  St. Louis Encephalitis  Yellow Fever  West Nile Fever  African Horse Sickness Viruses  Mosquitoes  Mosquitoes as Vectors of Viral Pathogens

Encyrtidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

Endangered Area An area where ecological factors favor the establishment of a pest that, if established, will cause an economically important loss in the area.  Invasive Species  Regulatory Entomology  Risk Analysis (Assessment)

Endangered Species Endangered species are those considered to be at risk of extinction in a relatively short period of time. Other species experiencing population decline are considered to be at less risk, and are classified as threatened, or are placed in another category to designate that they or their habitat is at risk. Following (Table 3) is a list of insects “of concern” established by the United States Fish and Wildlife Service. [STATUS: E is endangered; T is threatened; C is candidate taxon, ready for proposal; DA is delisted taxon; PE is proposed endangered; EmE is emergency listing, endangered; PE is proposed endangered.

Endemic Populations occurring at low levels of abundance in an area, though on occasion they may move to a more abundant state (an outbreak or epidemic). This term is sometimes, but incorrectly, used to describe indigenous or precinctive populations.

Endemism The condition of being indigenous to, and restricted to, a specific area.  Precinction

Enderleinellidae A family of sucking lice (order Phthiraptera). They sometimes are called squirrel lice.  Chewing and Sucking Lice

Endocrine Gland A gland that discharges its products, generally hormones, into the inside of an insect (Fig. 24) (contrast with exocrine gland).  Endocrine Regulation of Insect Reproduction

Endocrine Gland

Endangered Species, Table 3 Threatened and endangered insect species in the United States Inverted common name

Scientific name

Listing status

Current range

Beetle, American burying

Nicrophorus americanus

E

AR, MA, MI, NE, OH, RI, SD, Canada (Ont.)

Beetle, Coffin Cave mold

Batrisodes texanus

E

TX

Beetle, Comal Springs dryopid

Stygoparnus comalensis

E

TX

Beetle, Comal Springs riffle

Heterelmis comalensis

E

TX

Beetle, delta green ground

Elaphrus viridis

T

CA

Beetle, Hungerford‘s crawling water Brychius hungerfordi

E

MI, Canada

Beetle, Kretschmarr Cave mold

Texamaurops reddelli

E

TX

Beetle, Mount Hermon June

Polyphylla barbata

E

CA

Beetle, Tooth Cave ground

Rhadine persephone

E

TX

Beetle, valley elderberry longhorn

Desmocerus californicus dimorphus

T

CA

Beetle, Warm Springs Zaitzevian riffle Zaitzevia thermae

C

MT

Bug, Wekiu

Nysius wekiuicola

C

HI

Butterfly, Bahama swallowtail

Heraclides andraemon bonhotei

DA

FL

Butterfly, bay checkerspot

Euphydryas editha bayensis

T

CA

Butterfly, Behren‘s silverspot

Speyeria zerene behrensii

E

CA

Butterfly, callippe silverspot

Speyeria callippe callippe

E

CA

Butterfly, Corsican swallowtail

Papilio hospiton

E

France (Corsica), Italy (Sardinia)

Butterfly, El Segundo blue

Euphilotes battoides allyni

E

CA

Butterfly, Fender‘s blue

Icaricia icarioides fenderi

E

OR

Butterfly, Homerus swallowtail

Papilio homerus

E

Jamaica

Butterfly, Karner blue

Lycaeides melissa samuelis

E

IL, IN, MI, MN, NH, NY, OH, WI, Canada (Ont.)

Butterfly, Lange‘s metalmark

Apodemia mormo langei

E

CA

Butterfly, lotus blue

Lycaeides argyrognomon lotis E

CA

Butterfly, Luzon peacock swallowtail

Papilio chikae

E

Philippines

Butterfly, Mariana eight-spot

Hypolimnas octucula mariannensis

C

GU

Butterfly, Mariana wandering

Vagrans egestina

C

GU, MP

Butterfly, mission blue

Icaricia icarioides missionensis

E

CA

Butterfly, Mitchell‘s satyr

Neonympha mitchellii mitchellii

E

IN, MI, OH

Butterfly, Myrtle‘s silverspot

Speyeria zerene myrtleae

E

CA

E

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Endocrine Gland

Endangered Species, Endangered Species, Table 3 Threatened and endangered insect species in the United States (Continued) Inverted common name

Scientific name

Listing status

Current range

Butterfly, Oregon silverspot

Speyeria zerene hippolyta

T

CA, OR, WA

Butterfly, Palos Verdes blue

Glaucopsyche lygdamus palosverdesensis

E

CA

Butterfly, Queen Alexandra‘s birdwing

Troides alexandrae

E

Papua New Guinea

Butterfly, Quino checkerspot

Euphydryas editha quino (=E. e. wrighti)

E

CA, Mexico

Butterfly, Sacramento Mountains checkerspot

Euphydryas anicia cloudcrofti

PE

NM

Butterfly, Saint Francis’ satyr

Neonympha mitchellii francisci

E

NC

Butterfly, San Bruno elfin

Callophrys mossii bayensis

E

CA

Butterfly, Schaus swallowtail

Heraclides aristodemus ponceanus

E

FL

Butterfly, Smith‘s blue

Euphilotes enoptes smithi

E

CA

Butterfly, Uncompahgre fritillary

Boloria acrocnema

E

CO

Butterfly, Whulge checkerspot (=Taylor‘s)

Euphydryas editha taylori

C

No data

Caddisfly, Sequatchie

Glyphopsyche sequatchie

C

TN

Cave beetle, beaver

Pseudanophthalmus major C

KY

Cave beetle, Clifton

Pseudanophthalmus caecus

C

KY

Cave beetle, greater Adams

Pseudanophthalmus pholeter

C

KY

Cave beetle, Holsinger‘s

Pseudanophthalmus holsingeri

C

VA

Cave beetle, icebox

Pseudanophthalmus frigidus

C

KY

Cave beetle, inquirer

Pseudanophthalmus inquisitor

C

TN

Cave beetle, lesser Adams

Pseudanophthalmus cataryctos

C

KY

Cave beetle, Louisville

Pseudanophthalmus troglodytes

C

KY

Cave beetle, surprising

Pseudanophthalmus inexpectatus

C

KY

Cave beetle, Tatum

Pseudanophthalmus parvus

C

KY

Damselfly, blackline Hawaiian

Megalagrion nigrohamatum nigrolineatum

C

HI

Endocrine Gland

E


Scientific name

Listing status

Current range

Damselfly, crimson Hawaiian

Megalagrion leptodemus

C

HI

Damselfly, flying earwig Hawaiian

Megalagrion nesiotes

C

HI

Damselfly, oceanic Hawaiian

Megalagrion oceanicum

C

HI

Damselfly, orange black Hawaiian

Megalagrion xanthomelas

C

HI

Damselfly, Pacific Hawaiian

Megalagrion pacificum

C

HI

Dragonfly, Hine‘s emerald

Somatochlora hineana

E

IL, OH, WI

Fly, Delhi Sands flower-loving

Rhaphiomidas terminatus abdominalis

E

CA

Gall fly, Po’ olanui

Phaeogramma sp.

C

HI

Grasshopper, Zayante band-winged Trimerotropis infantilis

E

CA

Ground beetle, [unnamed]

Rhadine exilis

E

TX

Ground beetle, [unnamed]

Rhadine infernalis

E

TX

Mold beetle, Helotes

Batrisodes venyivi

E

TX

Moth, Blackburn‘s sphinx

Manduca blackburni

E

HI

Moth, Kern primrose sphinx

Euproserpinus euterpe

T

CA

Naucorid, Ash Meadows

Ambrysus amargosus

T

NV

Pomace fly, [unnamed]

Drosophilia aglaia

PE

HI


Drosophila attigua

C

HI


Drosophila differens

PE

HI


Drosophila digressa

C

HI


Drosophila hemipeza

PE

HI

Pomace fly [unnamed]

Drosophila heteroneura

PE

HI


Drosophila montgomeryi

PE

HI


Drosophila mulli

PE

HI


Drosophila musaphila

PE

HI


Drosophila neoclavisetae

PE

HI


Drosophila obatai

PE

HI


Drosophila ochrobsis

PE

HI


Drosophila substenoptera

PE

HI


Drosophila tarphytrichia

PE

HI

Riffle beetle, Stephan’ s

Heterelmis stephani

C

AZ

Skipper, Carson wandering

Pseudocopaeodes eunus obscurus

EmE, PE EmE = CA, NV, Washoe Co., NV and Lassen Co., CA; PE = CA, NV, Washoe Co., NV and Lassen Co., CA

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Endocrine Gland


Scientific name

Listing status

Current range

Skipper, Dakota

Hesperia dacotae

C

MN, ND, SD, Canada

Skipper, Laguna Mountains

Pyrgus ruralis lagunae

E

CA

Skipper, Mardon

Polites mardon

C

CA, OR, WA

Skipper, Pawnee montane

Hesperia leonardus Montana

T

CO

Tiger beetle, Coral Pink Sand Dunes Cicindela limbata albissima

C

UT

Tiger beetle, highlands

Cicindela highlandensis

C

FL

Tiger beetle, northeastern beach

Cicindela dorsalis dorsalis

T

CT, MA, MD, NJ, RI, VA

Tiger beetle, Ohlone

Cicindela ohlone

E

CA

Tiger beetle, Puritan

Cicindela puritana

T

CT, MA, MD, NH, VT

Tiger beetle, Salt Creek

Cicindela nevadica lincolniana

C

NE

Optic lobe Pars intercerebralis Median neurosecretory cells Corpus pedunculatum Lateral neurosecretory cells Axons of neurosecretory cells Aorta Corpus cardiacum Cut end of aorta Hypocerebral ganglion Corpus allatum Esophagus Circumesophageal connective Prothoracic gland Subesophageal ganglion Groups of neurosecretory cells Interganglionic connective

Endocrine Gland, Figure 24 Cross section showing the relationships of the principal endocrine glands with the brain (adapted from Chapman, The insects: structure and function).

Endocrine Regulation of Insect Reproduction


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which produces juvenile hormones (JH). Insects also have hybrids of endocrine glands and nerve cells that are called neurosecretory cells. These cells synthesize neurohormones and release them from specialized neurohemal organs into the bloodstream, affecting distant target tissues. Examples of neurosecretory cells are the medial neurosecretory cells of the brain that release the neurohormone prothoraciotropic hormone from the corpus cardiacum, its neurohemal organ. Receptors present on target cells specifically bind the hormones and produce a biological effect, but non-target cells that lack these receptors are unable to receive the message.

Marc J. Klowden University of Idaho, Moscow, ID, USA Insects dominate our planet largely because of their enormous reproductive capacity, which is made possible by a most efficient reproductive system. This reproductive efficiency results from the synchronization of the endocrine system that controls reproduction with both environmental signals and the internal physiological state of the insect, so that reproduction is triggered only when it is environmentally and biologically appropriate.

Endocrine Regulation of Male Reproduction

Sites Where Hormones are Released in insects Insects release hormones from conventional endocrine glands, which are tissues that specialize in the secretion of hormones that are transported by the blood and that act on receptor-bearing target tissues elsewhere in the body. Examples of endocrine glands in insects are the prothoracic glands, which produce ecdysteroids, and the corpus allatum,

The production of spermatozoa occurs within the follicles of the male testes (see diagram of male reproductive system). Apical stem cells in the anterior stem cell niche of the follicle divide mitotically to form spermatogonia. As these spermatogonia move down through the testes (Fig. 25), they become enclosed by somatic cells that produce cysts around them. The remainder of the

Vas efferens

Testis

Spermatozoa Vas deferens Accessory glands

Zone of transformation

Spermatids Seminal vesicle

Zone of maturation Spermatocytes

Ejaculatory duct

Zone of growth

Cysts

a

Aedeagus

Germarium

Spermatogonia

b

Endocrine Regulation of Insect Reproduction, Figure 25 (a). The generalized male reproductive system. (b). A single testicular follicle showing the zones of sperm maturation (From Snodgrass, 1935).

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testicular follicle can be divided into zones containing these cysts in successive regions of sperm development. In zone I, the zone of growth, the spermatogonia divide mitotically six to eight times within each cyst to form spermatocytes, each of which remains connected by cytoplasmic bridges, or ring canals. The number of divisions within a cyst is species specific; in Rhodnius the spermatocyte stage is reached at eight divisions, or 128 cells per cyst. In zone II, the zone of maturation, the spermatocytes divide meiotically to form haploid spermatids. The cysts continue to move toward the vas deferens within zone III, the zone of transformation, and the haploid spermatids within them differentiate into flagellated spermatozoa. As this differentiation proceeds, the cysts elongate and eventually rupture, releasing the spermatozoa into the vas efferens. These spermatozoa then migrate to the seminal vesicles where they remain until mating takes place. Spermatogenesis is thus a multi-step process of meiotic and mitotic divisions and cell differentiation. In some short-lived insect species that do not feed as adults, spermatogenesis may occur early during the larval and pupal stages. Sperm are produced throughout the adult lives of longer-lived males. Because the hormonal conditions that exist during these immature and adult periods are vastly different, it has been difficult to generalize a scheme for the hormonal control of insect spermatogenesis. Indeed, it has been suggested that insect spermatogenesis may be a sequential process of differentiation that is completely independent of hormones. There have been some reports of the effects of hormones in a few species of insects, but relatively little is known compared to our knowledge of how hormones control the reproductive system in females. The few studies that have examined the endocrine control of spermatogenesis suggest that the rate of mitotic divisions of spermatogonia to form spermatocytes is increased by high levels of 20-hydroxyecdysone, but when JH titers are also high, this increase is abolished. In some larval insects, the meiotic divisions of spermatocytes are arrested

at prophase until they reach the end of their larval period. A release of 20-hydroxyecdysone unblocks meiosis and allows the cells to proceed to metaphase. An ecdysiotropin produced by the brain induces the synthesis of ecdysteroids by the testis sheaths of several lepidopteran species. While most effects of JH on spermatogenesis are inhibitory, JH has been reported to accelerate spermatogenesis in some insects. The release of mature spermatozoa from the cysts in the testes may display a circadian rhythmicity that is initially inhibited by 20-hydroxyecdysone. The decline of 20-hydroxyecdysone is thus necessary in order for sperm to be released. The male accessory glands are involved in the synthesis of seminal fluid, the spermatophore, and vaginal mating plugs. They also produce various peptides that have physiological effects on the female when they are transferred during mating. The development and secretions of the male accessory glands are often controlled by JH. The accumulation of some secretory peptides in the glands is enhanced by JH and inhibited by 20-hydroxyecdysone. Many insect species undergo a diapause, which is a physiologically programmed developmental arrest that occurs prior to the onset of unfavorable environmental conditions. Spermatogenesis is interrupted in those lepidopterans that undergo a larval or pupal diapause but it resumes once diapause has been completed. It is the lysis of developing gametes before they become mature, rather than any developmental activity, that causes this interruption. The renewal of spermatogenesis occurs as a result of the increasing titers of 20-hydroxyecdysone that occur when diapause is terminated. There are two different kinds of sperm produced by the single fused testes of lepidopterans. The conventional eupyrene sperm fertilize the egg, but the apyrene sperm have no nuclei and thus no genetic function in fertilization. It has been speculated that by traveling with the eupyrene sperm, they may increase their motility within the female reproductive tract, or provide the eupyrene sperm with nutrients. The differentiation of apyrene sperm


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from eupyrene sperm in the testis occurs as a result of their exposure to a hemolymph-borne apyrenespermatogenesis-inducing factor. In some other species, individual males produce sperm of varying lengths, a factor that may contribute to speciation.

Endocrine Regulation of Female Reproduction The production of oocytes in the female begins within the germarium of the ovariole, where the haploid oocytes are produced from stem cells (see Fig. 26). As they descend through the vitellarium, they take up the vitellogenin that is deposited in the cytoplasm as yolk. The yolk is used by the developing embryo as precursors and energy for growth. Vitellogenin is usually produced by the fat body and released into the hemolymph, from where it is specifically taken up by the oocyte by receptor-mediated exocytosis. The process of vitellogenesis is closely regulated by hormones to insure that reproduction only occurs when all systems are ready. There is a tremendous amount of ecological variability among insect species and it is not surprising that there is a comparable variability and complexity in the systems that regulate their reproduction. There are but a few generalizations that can be made regarding the endocrine control of female insect reproduction. In short-lived insects that do not feed as adults, the yolk must be derived from reserves that are acquired during the larval stage. In these insects, vitellogenesis occurs while the pharate adult is still within the pupal skin and the adult emerges with a full complement of eggs. In the lepidopteran Hyalophora cecropia, this pre-emergence egg development appears to occur in the absence of any identifiable hormonal controls and may simply be a developmental program that is followed by the fat body. In longerlived insects that undergo multiple cycles of reproduction, vitellogenesis occurs when the fat body is activated by hormones that allow the vitellogenins to be produced cyclically.

Endocrine Regulation of Insect Reproduction, Figure 26 The generalized female reproductive system. The brain regulates the production of JH by nervous control as well as with the various peptides that activate JH synthesis (allatotropins) and inhibit JH synthesis (allatostatins). The JH acts on both the fatty body and the ovaries. An o varian ecdysteroidogenic hormone (OEH) released by the brain activates the synthesis of ovarian ecdysteroids that act on the fat body to cause the transcription of vitellogenin genes (Modified from Snodgrass, 1935).

The specific hormones that are involved in cyclical vitellogenesis vary considerably among insects, and again there is no single mechanism of hormonal control that can be described. However, there are two general approaches to cyclical egg production. In some insects, the production of vitellogenins is dependent on JH alone, such as in grasshoppers, cockroaches, some lepidopterans, and Rhodnius. JH acts directly on the fat body cells, causing them to initiate the translation and secretion of vitellogenin. In contrast, there are a few other insects, including the gypsy moth, Lymantria dispar, where low or declining titers of

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JH in the last larval instar have been shown to be necessary for vitellogenin production by the fat body. The release of JH from the corpora allata is controlled by the brain, either neurally or hormonally by its production of allatotropins that turn the corpora allata on and allatostatins that turn the corpora allata off. In many other insects, including most dipterans, both JH and 20-hydroxyecdysone are involved in reproduction. JH regulates the formation of new endoplasmic reticulum in the fat body and the sequestration of the vitellogenin produced, while 20-hydroxyecdysone regulates the rate of its production. Variations in the control of vitellogenesis by 20-hydroxyecdysone are common. Vitellogenin production in the Indian meal moth, P. interpunctella, coincides with a decline in the ecdysteroid titer of the pharate adult. Vitellogenin synthesis in the silkworm, Bombyx mori, coincides with a rise of 20-hydroxyecdysone. The control of vitellogenesis in the female mosquito is a good example of the complexity of the mechanisms that have evolved to coordinate reproduction with nutritional state. Vitellogenesis only occurs in female mosquitoes after a blood meal has been periodically acquired, so blood ingestion consequently serves as an experimental method of synchronizing the reproduction of many individuals so that the coordinated events can be better observed in the laboratory. The blood meal provides the precursors for yolk synthesis that are lacking after larval development is completed. After the adult female emerges, the JH that is released by the paired corpora allata during the first few days of life prepare both the fat body and the ovary for vitellogenesis. In response to an early peak of JH, the fat body cells become polyploid to provide more templates for DNA synthesis during vitellogenesis. JH also stimulates the induction of mRNA in fat body cells, the proliferation of ribosomes, and a development of its responsiveness to 20-hydroxyecdysone. The follicle cells that surround the oocyte-nurse cell syncytium are relatively undifferentiated at emergence, but in response to JH, they begin to differentiate and increase in size.

There are endocrine cells dispersed throughout the midgut epithelium, and in response to the ingestion of a blood meal these cells may trigger the release of the neurohormone ovarian ecdysteroidogenic hormone from the brain, which acts on the ovaries to increase their synthesis of protein and stimulate their production of ecdysone. Although the prothoracic glands, the site of ecdysteroid synthesis in larvae, degenerate and are absent in adult insects, the follicular epithelium of the ovary produces these ecdysteroids in adults. The 20-hydroxyecdysone then activates the transcription of vitellogenin genes in the fat body. The most abundant fat body transcript is a 6.5 kb vitellogenin mRNA that is translated into a 224 kDA pro-vitellogenin and subsequently cleaved and then repackaged into a 380 kDa vitellogenin. The 20-hydroxyecdysone peak also stimulates the follicle cells of the ovary to synthesize the vitelline envelope, the inner layer of the chorion, and acts again on the germarium to cause the creation of a new, secondary follicle. During the later stages of egg development, an oostatic hormone is produced that prevents the maturation of any secondary follicles until the maturing eggs have been laid, and avoids the burden of developing so many eggs that the female could no longer fly.  Reproduction  Ecdysteroids  Diapause  Embryogenesis  Meiotic Drive in Insects  Reproduction  Oogenesis  Juvenile Hormone  Nervous System  Prothoraciotropic Hormone

References Brown MR, Graf R, Swiderek KM, Fendley D, Stracker TH, Champagne DE, Lea AO (1998) Identification of a steroidogenic neurohormone in female mosquitoes. J Biol Chem 273:3967–3971

Endophytic Fungi and Grass-Feeding Insects

Davey KG (1997) Hormonal controls on reproduction in female heteroptera. Arch Insect Biochem Physiol 35:443–453 Davey KG, Sevala VL, Gordon DRB (1993) The action of juvenile hormone and antigonadotropin on the follicle cells of Locusta migratoria. Invertebr Reprod Dev 24:39–46 De Cuevas M, Lily MA, Spradling AC (1997) Germline cyst formation in Drosophila. Annu Rev Genet 31:405–428 Dumser JB (1980) The regulation of spermatogenesis in insects. Annu Rev Entomol 25:341–369 Friedlander M (1997) Control of eupyrene-apyrene sperm dimorphism in Lepidoptera. J Insect Physiol 43:1085–1092 Gade G, Hoffmann KH, Spring JH (1997) Hormonal regulation in insects: facts, gaps, and future directions. Physiol Rev 77:963–1032 Gillott C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163–184 Happ GM (1992) Maturation of the male reproductive system and its endocrine regulation. Annu Rev Entomol 37:303–320 Klowden MJ (1997) Endocrine aspects of mosquito reproduction. Arch Insect Biochem Physiol 35:491–512 Klowden MJ, Chambers GM (2004) Production of polymorphic sperm by anopheline mosquitoes and their fate within the female genital tract. J Insect Physiol 50:1163–1170 Koch EA, Smith PA, King RC (1967) The division and differentiation of Drosophila cystocytes. J Morphol 121:55–70 Meola R, Lea AO (1972) Humoral inhibition of egg development in mosquitoes. J Med Entomol 9:99–103 Raikhel AS, Snigirevskaya ES (1998) Vitellogenesis. In: Harrison FW, Locke M (eds) Microscopic anatomy of invertebrates, vol 2c. Wiley-Liss, New York, NY. pp 933–955 Raikhel AS, Miura K (1999) Nuclear receptors in mosquito vitellogenesis. Am Zool 39:722–735 Sappington TW, Raikhel AS (1998) Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem Mol Biol 28:277–300 Yamashita YM, Fuller MT, Jones DL (2005) Signaling in stem cell niches: lessons from the Drosophila germline. J Cell Sci 118:665–672

Endogenous A property inherent in an organism (contrast with exogenous).

Endogenous Rhythm Biological rhythms that arise independently of external stimulation.

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Endomychidae A family of beetles (order Coleoptera). They commonly are known as handsome fungus beetles.  Beetles

Endoparasite A parasite that lives inside the host.

Endophagous Feeding within the body of a host, often on the internal organs.

Endophallus The eversible inner lining of the aedeagus.

Endophytic Fungi and Grass-Feeding Insects Stephen L. Clement U.S. Department of Agriculture, Agricultural Research Service Pullman, Washington, DC, USA Nature had shaped plant defense mechanisms for warding off attack by plant-feeding insects long before humans started domesticating wild plants for food production about 10,000 years ago. As early farmers began developing agrarian societies, they probably observed that cultivated plants differed in their abilities to resist insect attacks. It remained, however, for twentieth century science to determine that variation in plant susceptibility to insect herbivores is often genetically based and results from natural plant chemistry and plant morphological traits (thorns, trichomes). Today, a rich body of literature exists on these plant defense mechanisms and abiotic (light, temperature, moisture, plant

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nutrient status, air pollutants) factors that influence plant susceptibility to insect attack. The role of plant microorganisms in determining the outcome of some plant/insect encounters was not widely recognized by entomologists and other scientists until the 1980s. By the beginning of the twenty-first century, however, microorganisms were included in major scientific discussions of plant defensive mechanisms against insect attack. Fungal endophytes (Epichloë species and their asexual Neotyphodium forms) of grasses are one of the best known microbial groups that adversely affect insect survival. These endophytes (endo [within] and phyte [plant]) live for some or all of their life cycle within grasses and are mostly selfperpetuated through maternal transmission in seed. They are invisible because their host plants show no outward signs of infection. It was not until microbiologists and animal scientists associated Neotyphodium infection (Fig. 27) in pasture grasses with toxic disorders of grazing cattle and sheep in the late 1970s and early 1980s that entomologists and grass breeders linked these fungal endophytes with enhanced grass resistance to insect pests. The first reports appeared in 1982 (New Zealand) and 1983 (United States) and documented enhanced field resistance to the Argentine stem weevil, Listronotus bonariensis, and

Endophytic Fungi and Grass-Feeding Insects, Figure 27 Section through a tall fescue seed showing mycelium of Neotyphodium coenophaialum between the aleurone cells (X100).

sod webworm, Crambus sp., in Neotyphodiuminfected forage and turf perennial ryegrasses, Lolium perenne, compared to endophyte-free plants. Interestingly, before endophytes were implicated in ryegrass resistance to the Argentine stem weevil, some investigators attributed variability among ryegrass lines for susceptibility to weevil attack to traits based on plant genes. After the first reports of Neotyphodium based resistance to insects, entomologists and other scientists accelerated the pace of research to generate more information on the extent and nature of specific grass/endophyte/insect associations. These efforts greatly expanded the list of insects negatively affected by endophyte-infected grasses, so, by the year 2000, it contained more than 40 species in five orders (Coleoptera, Lepidoptera, Diptera, Hemiptera, and Orthoptera) of the class Insecta. Concurrent research isolated and identified the chemical constituents (i.e., indole diterpenes, peramine, and pyrrolizidine and ergot alkaloids) of endophyte/host grass associations and characterized the responses of endophyte-infected grasses to a range of abiotic and biotic stresses. An outgrowth of research on the anti-mammalian and anti-insect properties of endophyte-infected grasses was the “defensive mutualism hypothesis,” which viewed alkaloids produced by endophytes as defense chemicals that provide adaptive advantage to the infected host grass. Under this hypothesis, the fitness enhancing and anti-herbivore properties of endophyte infection would lead to higher frequencies of infected plants in grass populations. The accompanying figure (Fig. 28) illustrates the known benefits of grass/endophyte associations, which are viewed as symbiota to reflect the intimate association of the two partners. Most of the existing information about grass/Neotyphodium symbiota comes from work on forage and turf grasses in the genera Lolium (especially perennial ryegrass) and Festuca (especially tall fescue, F. arundinaceae, and fine fescue species). Although researchers are far from fully understanding the range of insect responses to endophyte-infected grasses, they have developed a


Endophytic Fungi and Grass-Feeding Insects, Figure 28 Known benefits to each symbiotic partner. Not every Neotyphodium-infected grass host has all of the benefits shown.

good information base on the outcome of many interactions between grasses, endophytes, and insects. For example, research has shown that both insect deterrence and toxicity result from the production of alkaloids, and that the host grass genotype or species, and the endophyte strain involved in the interaction affect the expression and the type of insect resistance. Three examples illustrate the diversity of responses by plant-feeding insects. As previously mentioned, the first linkage between endophyte infection and insect resistance involved the Argentine stem weevil. This weevil maintains a close association with perennial ryegrass throughout its life cycle in New Zealand, where it is a significant pest of this important pasture grass. Adult weevils prefer to feed and oviposit on ryegrass plants that are free of endophytes, compared to endophyte-infected plants. A chemical, peramine, in endophyte-infected plants appears to be a powerful feeding deterrent to adult weevils. In another example, young larvae of the fall armyworm, Spodoptera frugiperda, a caterpillar that feeds on many grass species, prefer feeding on endophytefree tall fescue, whereas older larvae do not display preference with respect to endophyte infection. This example shows that different life stages of some insects are affected differently by exposure to endophyte-infected grasses. Finally, Neotyphodium infection in wild barley, Hordeum spp., does not always kill the Russian wheat aphid, Diuraphis noxia, a primary pest of wheat and barley, as

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experiments showed that the aphid was sensitive to some, but not all, Neotyphodium/wild barley associations. Although most of the early insect work emphasized the protective role of endophytes, a few studies documented insect insensitivity to endophyte infection in the late 1980s. Researchers continue to add to the list of insects unaffected by Neotyphodium infection in host grasses, thus revealing the variable nature of grass/endophyte/ insect interactions, and the fact that endophyteproduced alkaloids do not always function as plant defensive chemicals. The absolute function of most chemicals produced by endophytes is still very much open for discussion and more scientific investigation. Grass breeders and seed companies quickly developed and marketed Neotyphodium-infected Lolium and Festuca turf grasses after they recognized the benefits associated with endophyte infection. Today, turf grass professionals and homeowners in the United States routinely establish endophyteinfected grasses on golf courses, lawns, and playfields for better stand persistence and insect resistance. Additionally, scientists and commercial seed companies are beginning to take advantage of a vast diversity of Neotyphodium species and strains that differ in their ability to produce particular alkaloids. They are doing this by developing and marketing new forage grasses that are Neotyphodium combinations with “non-toxic endophytes” that do not produce toxins (e.g., ergot alkaloids) harmful to mammals, but do produce the necessary metabolites for better stand persistence and insect resistance. An expanding area of investigation involves biotechnological manipulations of endophytes for the commercial production of large pools of new grass-endophyte associations for specific purposes, including insect resistance.

References Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16

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Clement SL, Kaiser WJ, Eichenseer H (1994) Acremonium endophytes in germplasms of major grasses and their utilization for insect resistance. In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton, FL, pp 185–199 Clement SL, Wilson AD, Lester DG, Davitt CM (1997) Fungal endophytes of wild barley and their effects on Diuraphis noxia population development. Entomol Exp Appl 82:275–281 Popay AJ, Rowan DD (1994) Endophytic fungi as mediators of plant-insect interactions. In: Bernays EA (ed) Insectplant interactions, vol 5. CRC Press, Boca Raton, FL, pp 83–103 Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

the nuclear envelope. If the outer surfaces of the ER membranes are coated with ribosomes, the ER is “rough-surfaced”; otherwise it is called smoothsurfaced.

Endoproteases Protein digesting enzymes that attack large proteins internally at the linkage between certain amino acids, breaking the protein into smaller polypeptides.

Endopterygota Endocuticle The inner portion of the procuticle (Fig. 29), a region that is softer and lighter in color than the exocuticle. The endocuticle is not sclerotized, so it can be resorbed prior to the insect molt, and used to make new cuticle.  Integument: Structure and Function  Epicuticle

A division of Insecta in which the wings develop internally during the immature stages. Holometabolous insects.  Metamorphosis

Endoskeleton An internal portion of the skeleton. The chitinous processes extending internally.

Endoplasmic Reticulum (ER) A system of sacs (cisternae) in the cytoplasm of eukaryotic cells in which the ER is continuous with the plasma membrane and the outer membrane of

Endotherm An organism that produces metabolic heat for thermoregulation. Mammals and birds are common Epicuticle Exocuticle Pore canal Endocuticle Schmidt’s layer Epidermis Basement membrane

Endocuticle, Figure 29 Cross section of the insect cuticle and epidermis (adapted from Chapman, The insects: structure and function).

Endrő dy-Younga, Sebastian (Sebestyén Endrő dy-Younga, Sebestyén Endrő dy)

examples of endotherms, and although insects generally are considered to be ectotherms rather than endotherms, some display endothermic be havior and physiology.  Thermoregulation in Insects

Endotoxins Substances produced by microorganisms which are not secreted into the surrounding medium but are confined within the microbial cell; they are released after autolysis.

Endrő di, Sebő (Sebastian Endrő di) George Hangay, Ottó Merkl1 1 Hungarian Natural History Museum, Budapest, Hungary Sebő Endrő di was born on the October 18, 1903 in Kassa, Hungary, now Kosice, Slovac Republic. He graduated in law from the Pázmány Péter University of Science, Budapest in 1931. He was a keen amateur coleopterist, working as a lawyer for the Danube Steamship Company from 1931 until 1948, then as a lecturer at the College of Horticulture, Budapest (1949–1956) and at the University of Agricultural Science at Göd, North of Budapest (1956–1961). From 1961 until his retirement in 1966 he was employed by the Ministry of Agriculture’s Plant Protection Service in Budapest. After his retirement he had a room in the Hungarian Natural History Museum’s Zoological Collections, where he conducted research until his death. His first entomological research focused on the beetle fauna of the Börzsöny Mountains, North of Budapest, where his family had a summer house. He set out to explore the beetles of this area together with his son, Sebastian Endrő dyYounga. Through his long and productive life as a coleopterist, he has studied various sections of the beetle fauna of the Carpathian Basin and of the lands of historical Hungary as well as the scarabaeoid

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fauna of the World, publishing 222 scientific works. His achievements were highly respected by his colleagues and he was awarded with the Frivaldszky Memorial Plaque (Silver) by the Hungarian Entomological Society in 1967 and with the “In Scientia Entomofaunistica Excellenti” medal by the VIII. Central-European Entomofaunistic Symposium in 1979. Sebő Endrő di is known mainly by his work on the Scarabaeoidea, especially the Dynastinae. His greatest work was the revision of this subfamily of beetles, which was published in the German language in 20 sections, and consisted of 1,600 pages in eight journals. A shorter version of 800 pages in English was published in 1985 (The Dynastinae of the World, Budapest-Hagen, 1985). Dr. Endrő di passed away on the of December 12, 1984 in Budapest. He was a kind and helpful man with an immense knowledge of beetles.

References Kaszab Z (1984) Dr. Endrő di Sebő (1903–1984). Folia Entomol Hung 46:2, 5–16 Kaszab Z, Papp CS (1986) Sebő Endrő di (1903–1984). Entomography 4:379–397 Kaszab Z, Zunino M (1986) L’ opera scarabeologica di Sebő Endrő di (1903–1984). Mem Soc Entomol Ital 64:45–52

Endrő dy-Younga, Sebastian (Sebestyén Endrő dy-Younga, Sebestyén Endrő dy) George Hangay, Ottó Merkl1 1 Hungarian Natural History Museum, Budapest, Hungary Sebestyén Endrő dy was born on the 26th of June, 26 1934 in Budapest. He became interested in beetles early in his life, following the footsteps of his father, Sebő Endrő di with whom he studied the coleoptera fauna of the Börzsöny Mountains, a wilderness region North of Budapest. He completed

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his formal studies by receiving his doctoral degree at the Eötvös Lóránt University of Science in Budapest, in 1958. From 1957 until 1965 he was employed by the Hungarian Natural History museum and worked closely with Dr. Zoltán Kaszab. He also published some papers regarding the beetles of the Börzsöny Mountains. In order to distinguish father and son, his father changed the spelling of their family name by replacing the last letter of Endrődy with an i, consequently he became Endrődi and Sebastian added his mother’s maiden name by a hyphen to the original family name, thus forming the name Endrő dy-Younga, by which name he was known for the rest of his life. His Christian name Sebestyén is the Hungarian equal to Sebastian. He used the former in his Hungarian publications and the latter in his many works in English and German as well as in everyday life after he left Hungary. For his family and friends he was known as Sebő. In 1965, he accepted the position of senior research officer at the Ghana Academy of Science’s Crops Research Institute in Ghana, and in 1973 together with his family he moved to the Republic of South Africa. He joined the Transvaal Museum in Pretoria in the same year, and became the Chief Curator of its Coleoptera Department in 1974. He held this position until 1998 when he resigned from it due to ill health. Endrő dy-Younga was a gifted coleopterist, blessed with a sharp mind and extraordinary memory. He was athletic and therefore a very effective, never-tiring field worker, well and truly belonging to the “Kaszab School” of extremely hard-working field entomologists. While in Ghana, he collected hundreds of thousands of specimens, which were sent back to the museum in Budapest. His beetle studies were chiefly focused on the Clambidae, Cybocephalidae and Tenebrionidae but he also researched the coleoptera fauna of the Carpathian Basin, publishing on various families. His 93 publications include major monographs and revisions. From the material that he collected through his life, 1,318 new species were described either by him or by colleagues, and 153 species and six genera were named after him. He received

the Frivaldszky Memorial Plaque from the Hungarian Entomological Society. This seemingly frugal formal recognition does not reflect on his popularity as a colleague and friend, and the respect given to him as a coleopterist of immense knowledge. The international community of coleop terists suffered a great loss when he passed away on the February 26 1999.

References *Bellamy CL, Jäch M (1999) In: memoriam Sebastian Endrő dy-Younga (1934–1999). Koleopterol Rundsch 69:209–214 Brain R (2000) Tribute to Dr Sebastian Endrő dy-Younga. Ann Transvaal Mus 37: 4–5 Breytenbach E (2000) Sebastian Endrő dy-Younga. 1934–1999. Afr Entomol 8:1, 151–156 Merkl O (1999) Dr. Endrő dy-Younga Sebestyén (1934–1999). Rovarász Híradó 25:1–3 Anon E-Y (2000) Publications of Sebastian E.-Y. Ann Transvaal Mus 37: 6–8

Endromidae A family of moths (order Lepidoptera) also known as glory moths.  Glory Moths  Butterflies and Moths

Enemy Impact Hypothesis The concept that community stability is enhanced by diversity, and that plant diversity favors the presence of natural enemies which can moderate the abundance of herbivores.

English Grain Aphid, Sitobion avenae (Fabricius) (Hemiptera: Aphididae) This is an important pest of small grain crops world wide.  Wheat Pests and their Management

Enhanced Biodegradation of Soil-Applied Pesticides

Enhanced Biodegradation of Soil-Applied Pesticides John N. Matthiessen Commonwealth Scientific and Industrial Reasearch Organization, Floreat, WA, Australia Pesticides are broken down in the environment by physical action such as heat and light, but biological degradation is often a primary means of dissipating such compounds. This is particularly the case for pesticides applied into soil. Microbes usually cause such biological breakdown. In the past, many pesticides were not readily degraded by either physical or biological action because of their molecular structure. The most notable examples of such persistent compounds were the chlorinated hydrocarbon and cyclodiene insecticides. Since the 1970s these compounds have gradually been phased out by regulation and replaced by toxic, yet biodegradable, pesticides. While agricultural producers and environmentalists could feel relieved that the major problem of persistent residues in soil, waterways and produce, and accumulation in animal tissue, was now a thing of the past, a strange new twist occurred in some situations. Some pesticides, particularly those applied to soil to control soil-borne pests and diseases, were no longer controlling pests as effectively as they once had. The problem was first noticed in agricultural systems that required preventative application and longevity of pesticide to protect plant roots from insect damage, such as where soil-dwelling pest insects colonized the crop during the course of its growth. The phenomenon was puzzling – the pests could be shown to still be susceptible to the pesticide (i.e., they had not developed resistance because of prolonged or repeated exposure) and it seemed related only to particular fields, leading to them being labeled “problem” soils. It was some time, and some disastrous pest damage to many crops, before an explanation for these pesticide failures was revealed. It was all to do with repeated applications of a pesticide to the same area of soil.

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Enhanced Biodegradation Soil is a diverse ecosystem intimately involved in the cycling of organic matter, nutrients and moisture. Since it is known that pesticides are mainly dissipated from soil by microbiological metabolism, it is clear that some microbes can utilize apparently toxic compounds as a nutrient or carbon source. Microbes form a highly diverse component of the soil biota, intricately linked to soil processes and complex food webs. By the very nature of their rapid reproduction by cell division, populations of microbial organisms such as bacteria can respond and adapt very quickly to changes in their environment. This is the basis of enhanced (also known as accelerated) biodegradation. Repeated applications of a pesticide to soil can stimulate the microbes that are able to metabolize the compound. This enrichment of the microbial population can reach a point where degradation of the pesticide occurs too fast to allow it to exert its desired pest control effect. The paradox is that the apparently positive general effect of biodegradation can be transformed into the negative local problem of enhanced biodegradation. Unfortunately, once enhanced biodegradation is induced, there is very little that can be done to cure the problem short of sterilizing the soil – hardly a desirable thing to do. Enhanced biodegradation differs fundamentally from resistance to pesticides. In situations where resistance develops as a result of repeated exposure to a pesticide, individuals within the pest population carrying the genetic capacity to detoxify the compound have a selective advantage and gradually come to dominate the population. Enhanced biodegradation does not involve the pest directly. The causative organisms are otherwise innocuous members of the soil microbial community that “feed” on the pesticide and take it out before it can exert its toxic action sufficiently on pests to prevent crop damage. Pesticide resistance comes at a metabolic cost to an organism – energy must be expended to

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detoxify a compound that has no intrinsic nutritional worth to the organism. Consequently, pesticide resistant genotypes are less fit and will diminish in the population once the selection pressure is removed. Enhanced biodegradation, on the other hand, is a consequence of a nutritional benefit causing proliferation of the adapted organisms. Although they too will diminish in response to reduction in the favored source of nutrition, it is simply a response to resource shortage and not because they are less fit. A characteristic of enhanced biodegradation is that the effect gradually diminishes if the affected soil is given no further treatments of the pesticide. However, bacteria are mainly responsible and they can form resting stages. Consequently, the phenomenon can rapidly reactivate at an immediately high level if the pesticide is once again applied to the soil. Prevention of the phenomenon is the only sure way of avoiding it. Unfortunately, enhanced biodegradation approaches by stealth and it is difficult to know what rate of removal of a pesticide from the environment will constitute a problem for control of a pest. The issue will most likely be crop and pestspecific. Acutely toxic pesticides applied when the pest is present are unlikely to suffer the problem, whereas pesticides that need to be applied prophylactically pre-planting to act later in the life of the crop will be at much greater risk. Soil characteristics affect the risk of onset of enhanced biodegradation. A major factor increasing the risk is high soil pH, which favors proliferation of bacteria over fungi. However, it is known that calcium is an important element in the nutrition of bacteria and calcium content of soil is normally positively correlated with elevated pH. Recent studies confirm that the combined effect of calcium and high pH is required to enhance the risk of enhanced biodegradation. Generally, it seems that sandy soils are more at risk of the phenomenon but this is a broad characteristic that is not easily quantified. A significant related issue is the phenomenon of cross-degradation, where other pesticides are

degraded at an accelerated rate in soil in which they have never been used, but which has enhanced biodegradation to another pesticide. Usually this occurs to structurally related compounds, meaning that new variations of a family of pesticides may be rendered ineffective before being used. This is what occurred to many of the carbamate insecticides used for control of corn rootworm in the American Corn Belt.

An Example Metham (metam) sodium is a fumigant-like broad-spectrum pesticide widely used for the control of soil-borne pests and diseases. The principal use is in horticulture, which is often characterized by intense production systems with little or no crop rotation. Metham sodium is a somewhat unusual pesticide in that it is not the active pesticidal compound. Rather, it reacts in moist soil to form the toxin methyl isothiocyanate (MITC). Metham sodium, or more accurately the MITC, has been shown to suffer severely from enhanced biodegradation in an intensive horticultural production system where the soil is sandy and its pH is relatively high. It offers a good example of the principles of the phenomenon of enhanced biodegradation. The accompanying figure shows the percentage of MITC produced and its fate when metham sodium is applied to soil that has either not been previously treated (Fig. 30) and the same type of soil from an adjacent field (Fig. 31) that had been treated approximately annually for about ten years. In the previously untreated soil the MITC was formed at almost 100% of theoretical within about one hour, and it degraded slowly over about 17 days. In contrast, in the previously treated soil only around 45% of the potential MITC was formed and it was completely dissipated within a mere seven hours. The biological origin of the phenomenon was confirmed by sterilizing a sample of the degrading soil by autoclaving. When subsequently treated with


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80 Soil treated several times with metham sodium % MITC

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Enhanced Biodegradation of Soil-Applied Pesticides, Figure 30 Production and fate of MITC toxin after application of metham sodium to soil never previously treated, soil treated numerous times in the previous ten years, and the previously treated soil after being sterilized. 80 70

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Enhanced Biodegradation of Soil-Applied Pesticides, Figure 31 Amount of MITC remaining in soil 24 h after treatment with metham sodium for a single soil type amended to four pH levels.

metham sodium, the production and fate of MITC in the soil was identical to the pattern in the soil that had never previously been exposed to the pesticide. Several species of bacteria that could be readily

maintained in culture with MITC as the sole nutrient source were isolated from the degrading soil. The clear influence of high pH (including non-limiting calcium) in exacerbating the risk of

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enhanced biodegradation is shown in the other figure. Sub-samples of a naturally acidic (pH 4.8) soil were modified to a range of higher pH values and then treated with metham sodium at monthly intervals, with the MITC being measured after 24 h. The highest pH soil developed enhanced biodegradation after only four applications, and the effect was proportional to pH in the other soils.

Implications The most important aspect of enhanced biodegradation is for those involved in pesticides applied to soil to recognize the reality of the issue, be alert to the warning signs and to understand key risk factors (e.g., high soil pH). Too often in the past the control failures were put down to such things as unfavorable weather, poor application techniques, insufficient chemical or pesticide resistance. This can lead to repeated applications or increased doses – both of which simply exacerbate the problem. The only option for management of enhanced biodegradation is prevention. One way that this can be achieved is by rotation of pesticides, so long as different types are alternated. However, this often requires a cooperative approach by competing pesticide manufacturers. Other methods that farmers can adopt is lengthening the time between applications of the same pesticide to an area of land through the use of longer crop rotations, and avoiding reliance on a pesticideonly approach by using rotation crops antagonistic to pest organisms.  Detoxification Mechanisms in Insects

References Felsot AS (1989) Enhanced biodegradation of insecticides in soil: implications for agroecosystems. Annu Rev Entomol 34:453–476 Racke KD, Coats JR (1990) Enhanced biodegradation of pesticides in the environment. American Chemical Society, Washington, DC

Enicocephalidae A family of bugs (order Hemiptera). They sometimes are called gnat bugs or unique-headed bugs.  Bugs

Ensiform This term is usually applied to structures that are sword-like in appearance. They are flattened with thin edges and taper to a point distally. Most often this term is applied to antennal structures.

Ensign Coccids Members of the family Ortheziidae, superfamily Coccoidae (order Hemiptera).  Bugs

Ensign Wasps Members of the family Evaniidae Hymenoptera).  Wasps, Ants, Bees and Sawflies

(order

Enteric This term refers to the digestive system or alimentary canal.

Entognatha This is a taxon of superclass Hexapoda containing the primitive arthropods closely related to insects. Entognatha is usually considered to be a class, corresponding to the class Insecta, and consisting of the orders Collembola, Protura, and Diplura

Entomodeltiology

(Entotrophi). However, these orders are sometimes considered to be classes, or orders within Insecta.

Entognathous Mouthparts that are sunk into the head. This is also known as entotrophous. Such mouthparts are found generally in hexapod organisms that are close relatives of insects, such as Collembola, Diplura, and Protura. This is a major feature differentiating these insect-like groups from true insects, which have ectognathous (extruded) mouthparts.

Entomobryidae A family of springtails in the order Collembola. They commonly are known as slender springtails.  Springtails

Entomodeltiology Dale H. Habeck University of Florida, Gainesville, FL, USA Many entomologists, ecologists, naturalists and amateurs collect insects because they find insects fascinating. Entomodeltiology, a combination of entomo = insect and deltiology = the hobby of collecting postcards, is another way to collect insects. Just as catching rare or unusual insects is challenging, finding postcards is equally challenging. Insects can be found on regular postcards and even on postcards made of leather, wood or ceramic. Picture postcards were placed on sale at the Columbian Exposition in Chicago, Illinois, on May 1, 1893. Although there were earlier scattered issues, this was the real beginning of the postcard. Illustrations were placed on government printed cards or privately printed souvenir cards. The back of the card was for address only. In 1898, private printers in the U.S. were allowed to print and sell cards with the inscription “Private

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Mailing Card,” and in 1901, private printers were granted permission to use the words “Post Card.” Writing on the back was still limited to the address. Postcards as we know them, with a vertical line down the middle of the back side with a space for the address on the right and a message on the left, were permitted beginning March 1, 1907. Millions of cards were printed from 1907 to 1915, mostly in Germany, where lithographic processes were far superior to those in America. The First World War stopped the printing and importation of post cards from Germany. Most cards were printed in England and the United States. Several other eras followed including the white border era (1915–1930). Printers saved ink by leaving a white border around the picture or illustration. These cards were of poor quality and many publishers went out of business. This was followed by the linen era (1930–1944) where cards with a high rag content caused the cards to have a linen-like finish. Many historical events were depicted on these cards. Finally (1945 to the present), the photochrome era. These color photographs are very appealing to the collectors and some postcard dealers specialize only in chromes. Deltiology from 1915 to 1970 was not a popular hobby. Around 1970, interest began to grow. At present there are over 100 postcard clubs worldwide. Numerous postcard shows are held each year where collectors can peruse hundreds of thousands of postcards. Two magazines, Barr’s Post Card News and Postcard Collector, are published. Subject interest is highest in geographic areas (cities, counties, states). Others limit their collecting to churches, schools, hotels, etc., in a particular area. There is hardly a topic that someone doesn’t collect and that includes animals from the largest mammals to insects as diverse as butterflies and fleas. Interest in insect postcards appears to be increasing as more and more dealers have an insect category in their topical offerings. A few years ago, if you inquired about insects on postcards, you would probably be referred to the animal category. The number of dealers who have a butterfly

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Entomodeltiology, Figure 32 Some postcards depicting insects: top row and second row left, educational postcards showing important or particularly interesting insects; second row right, postcards showing the “art” of capturing tiger beetles; bottom row, portrayal of insects for aesthetic value in oriental art (left) or photography (right). Note that the bottom right postcard is incorrectly labeled; this is a swallowtail rather than a monarch.

Entomodeltiology

Entomodeltiology, Figure 33 Additional postcards depicting insects: top two rows show humor, which often is associated with mosquitoes, particularly oversized mosquitoes; third row left, insects attired as humans; third row right, a “giant” grasshopper, a common source of humor in areas commonly infested with grasshoppers; bottom left, ladybeetles harnessed, another example of humor; bottom right, a colorful holiday greeting.

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c ategory has increased in recent years and it is unusual to find a dealer without such a category. Considering the beauty of butterflies and moths, it is not surprising that they are favorites among insect postcard collectors. Examples range from chromes of live butterflies and sometimes their larvae, to artistic renderings of butterflies to the inclusion of small non-descript butterflies added to scenery pictures. Monarch butterflies are a favorite subject, especially on the newer chrome cards. Butterflies and other insects (especially lady beetles and various bees and wasps) may be depicted on general greeting postcards (Fig. 32, Fig. 33) as well as birthday, Easter, Valentines, with only a few on Christmas, Thanksgiving, New Years, and St. Patrick’ s Day. Mosquitoes are frequently found on postcards in areas where tourists abound. A fairly common card has a giant stylized mosquito labeled as the state bird of (insert any state or province). Amazingly, these are usually labeled as Aedes vexans, apparently the only species known to postcard illustrators. Other old cards depict mosquitoes attacking people. Honey bees are not left out. Most are humorous with someone being attacked by a swarm of angry bees. Another comic card shows a man fighting bed bugs. Germany produced many postcards with scarab beetles performing as people. Other themes found among insect postcards include fantasy (e.g., children with butterfly wings), exaggeration (e.g., giant grasshoppers), stamps, Asian art (insects are nearly as common as flowers), humor, and education (e.g., series of images produced by scientific institutes, government, and agrochemical companies). New postcards may be found in any store that sells cards. Another good source is in the gift shops in natural history museums and butterfly houses. The British Museum of Natural History has issued over two dozen sets of insect postcards based on their vast worldwide collection of insects. Old postcards are often found in antique shops or at postcard shows. Postcard prices range

from 25 cents up to hundreds of dollars depending on rarity, condition, topic and age. Collecting postcards with insects is a challenging hobby. Unlike collecting insects on stamps, where catalogs are available listing every issue, the insect postcard collector is on his own.

Entomogenous Refers to microbes or nematodes growing in or on the bodies of insects. This term connotes parasitic or other intimate symbiotic relationship, but not necessarily a pathogenic one. Though popular in recent history, this term is now rarely used, and is best considered obsolete (contrast with entomophilous and entomopathogenic).

Entomoparasitic This term denotes a parasitic relationship between an insect and a parasite, though it usually is used to describe the relationship with insect parasitoids. Although entomoparasitic insects kill their hosts (i.e., they are pathogenic), they are never referred to as entomopathogenic. Some nematodes (the ones that do not kill quickly, instead functioning more like insect parasitoids) are correctly referred to as entomoparasitic (contrast with entomopathogenic, entomophilic).

Entomopathogenic A relationship between an insect and a microbe, or an insect and a nematode, that results in the death of the insect. It is best considered a subset of entomophilic organisms. Some prefer to limit this term to insect-killing nematodes which harbor and release a pathogenic bacterium: nematodes in the families Steinernematidae and Heterorhabditidae. Although entomoparasitic insects kill their hosts (i.e., they are pathogenic), they are never referred to as entomopathogenic (contrast with and entomophilic).

Entomopathogenic Fungi and their Host Cuticle

Entomopathogenic Fungi and their Host Cuticle Nicolas Pedrini, M. Patricia Juarez Instituto de Investigaciones Bioquimicas de La Plata, CONICET, National University of La Plata, La Plata, Argentina Entomopathogenic fungi are a very diverse group of insect pathogens that include approximately 700 species in almost 100 genera. They occur in most fungal taxonomic groups, with an ample variation in host range, thus providing a large number of microorganisms potentially useful as control agents against different insect orders. Insect pests infesting areas where it is difficult or unsafe to implement control using currently available insecticides are particularly good targets for mycoinsecticides. Among them, there is interest in targeting disease vectors that co-habit with humans (mosquitoes, flies and kissing bugs), mostly due to the health risk of toxic chemical use in human dwellings. There also is growing interest in use of mycoinsecticides to control pests affecting greenhouses, small orchards and organic farms (particularly aphids, whiteflies, a variety of beetles and caterpillars). Unlike other insect-pathogenic microorganisms that must be ingested to initiate the disease (virus, bacteria, nematodes and protozoa), entomopathogenic fungi normally invade by penetrating through the host cuticle. Surface structure and the chemical composition of the cuticle are both believed to affect the attachment of fungal propagules. Initial events can be divided into three successive stages: (i) Adsorption at the interface between the propagules and the insect epicuticle. This first step involves physical and chemical characteristics of both propagules and host surfaces. The process may involve specific receptor-ligand and/or nonspecific hydrophobic and electrostatic mechanisms. This stage is characterized by the secretion of mucus by fungal cells and the initial dissolution of the surrounding epicuticle by this mucoid substance. Ungerminated conidia deposited on

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the cuticular surface are able to produce esterases, lipases, and N-acetylglycosaminidase. Thus, enzymatic activities might be implicated early in adhesion processes. (ii) Fungal germination and development on the insect cuticle. Early events in spore germination require an exogenous carbon source. Both germination stimulators and inhibitors have been detected on the cuticle. In general, high relative humidity (over 90%) is needed for germination. However, an adequate microclimate to promote infection can be found on the intersegmental membranes of the insect’s cuticle. Both adsorption and germination must occur, but success here does not guarantee successful fungal infection. Fungal germination on non-host cuticle, without further penetration into the insect internal tissues, has been reported. (iii) Fungal penetration. Germ tubes must pass through the different cuticular layers. This process depends both on the intrinsic properties of the germ tube and on the physiological state of the host and is essential for infection occurrence. The most common cuticular reaction to fungal penetration is a localized melanization around and in front of the penetration peg. Successful pathogens overcome any defensive reaction and penetrate into the hemocoel. Finally, the fungus replicates as budding hyphal bodies invading the entire cavity; insect death takes place shortly after.

Fungal Enzymes Involved in Cuticle Degradation Although the major bulk components of the insect cuticle are protein and chitin, the outermost epicuticular surface layer comprises a complex mixture of non polar lipids, mainly composed by very long chain hydrocarbons (20 to more than 40 carbons). Entomopathogenic fungi are also able to degrade insect epicuticular hydrocarbons, incorporating them into cellular components (Fig. 34) as well as utilizing them for energy

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Entomopathogenic Fungi and their Host Cuticle RCH3

RCH2OH

RCHO

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R CO-SCoA

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Entomopathogenic Fungi and their Host Cuticle, Figure 34 Proposed pathway for hydrocarbon degradation by entomopathogenic fungi. RCH3: hydrocarbon, RCH2OH: fatty alcohol, RCHO: fatty aldehyde, RCOOH: fatty acid, RCO-SCoA: fatty acyl-CoA, CH3CO-CoA: acetyl-CoA, TCA: tricarboxylic acid.

production. Insect hydrocarbons were shown to be the preferred cuticular lipid fraction for fungal growth. Employing radiolabeled analogues of insect hydrocarbons, they were shown to be incorporated into a variety of fungal lipid components. Depending on the substrate assayed, complete oxidation (CO2 production) was also detected. The fungal enzymes involved in insect-like hydrocarbon breakdown have not yet been identified and characterized. In analogy to yeast systems, the first oxidation round is presumably carried out by a microsomal cytochrome P450 enzyme system, producing a fatty alcohol as the primary oxidation product. The alcohol, or eventually the fatty acid, will traverse the peroxisomal membrane, and after successive transformations by the concerted action of alcohol dehydrogenase, aldehyde dehydrogenase, and acyl-CoA synthetases, will eventually provide the appropriate fatty acylCoA for degradation in the peroxisomes, the site of β-oxidation in fungi. In Beauveria bassiana,

Entomopathogenic Fungi and their Host Cuticle, Figure 35 Electron micrographs of Beauveria bassiana comparing fungi grown either in an easily usable carbon source (glucose) or in insect-like hydrocarbon as the sole carbon source. Diaminobenzidine was used to stain peroxisomes. (a) Glucose-grown cells show scarce peroxisomes; (b) Hydrocarbon-grown cells show a large number of small size peroxisomes. P: peroxisomes, M: mitochondrion, ER: endoplasmic reticulum.

development of peroxisomes is clearly stimulated in alkane-grown fungi; electron micrographs (Fig. 35) show diaminobenzidine-stained peroxisomal particles closely associated to endoplasmic reticulum. Furthermore, peroxisomal marker enzymes (i.e., catalase and acyl CoA oxidase) are induced in fungi grown on media containing insect-like hydrocarbons as the sole carbon source. Penetration of exocuticle and endocuticle involves both physical and enzymatic activities.

Entomopathogenic Fungi and their Host Cuticle

The lack of data on the former makes it difficult to envisage its precise role in the whole process. To study enzyme production, fungal preparations are incubated either with insect cuticle or with chemical analogues, thus providing the required carbon and/or nitrogen sources. A variety of hydrolytic enzymes responsible for the degradation of the major cuticular components are induced sequentially: proteases and esterases are produced within the first day, whereas chitinase and lipase activities appear substantially later (4–5 d). Some of them act synergistically during degradation events. First, proteases hydrolyze most of the protein crosslinkages of the procuticle; afterwards, the chitinolytic complex is activated. A number of proteases and chitinases have been identified after expressed sequence tag (EST) analyses of cDNA libraries obtained from fungal cultures incubated with insect cuticle. In this growth condition, at least three kinds of proteases are expressed: subtilisin-like proteases, trypsin-like serine proteases and thermolysin-like metalloproteases. Subtilisin-related enzymes show the greatest activity against insect cuticle, having a crucial role in pathogenesis. Trypsin-related proteases have no ability to degrade intact cuticle, but act on partially hydrolyzed cuticular proteins. Their association with (Fig. 36) appressoria suggests they might be available during early stages of cuticle colonization. Both types of proteases might be part of a cascade of pathogen reactions facilitating the penetration of host cuticles. A similar situation is found with the complex mixture of endo- and

Entomopathogenic Fungi and their Host Cuticle, Figure 36 Initial events of the interaction between entomopathogenic fungi and insect cuticle.

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exo-chitinases produced by entomopathogenic fungi during growth on the insect cuticle. Helping penetration, endo-chitinases are likely to be the most effective degrading cuticle polymers. Oligomers released by the endoacting enzymes might be further degraded by exo-chitinases resulting in small molecules (i.e., N-acetylglycosamine) usable for nutrition.

Mycoinsecticide Improvement Fungal virulence can be understood as the degree of pathogenicity against a potential insect host. Variation in fungal virulence toward a variety of insect hosts is related to enzyme production, growth conditions, temperature, relative humidity, and the presence of other microorganisms, among other factors. Insect mortality, the time period required achieving this goal, or fungal dose are frequently used as virulence parameters. The potential to enhance virulence has been addressed either by fungal adaptation to grow on a cuticle-like medium, or in a more sophisticated way, by adding insecticidal genes encoding specific cuticle-degrading enzymes (chitinases and proteases). These approaches resulted in 25–50% reduction in the time to kill and/or a similar percentage reduction in other mortality parameters. The major barrier role of the cuticle in insect survival is well known; furthermore, the ability of fungal degrading enzymes to breach the insect cuticle is already recognized. Improving this set of tools by favoring the initial steps of fungal penetration will help increase mycoinsecticide performance. This goal may be attained through genetic modification, in addition to formulation optimization. Several methods can be applied for genetically improving strains, and recently, transformation methods have been used for the insertion of homologous or heterologous genes in fungal biocontrol agents. Overexpression of virulence-related fungal enzymes will be

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advantageous, since no safety concern to using genetically modified fungi has been provided, and hence it is an ecologically safe alternative to chemical pesticides.

References Fargues J (1984) Adhesion of the fungal spore to the insect cuticle in relation to pathogenicity. In: Roberts DW, Aist JR (eds) Infection processes of fungi. The Rockefeller Foundation, New York, NY, pp 90–110 Lomer CJ, Bateman RP, Johnson DL, Langewald JL, Thomas M (2001) Biological control of locusts and grasshoppers. Annu Rev Entomol 46:667–702 Pedrini N, Crespo R, Juárez MP (2007) Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comp Biochem Physiol C 146: 124–137 Roberts DW, Humber RA (1984) Entomopathogenic fungi. In: Roberts DW, Aist JR (eds) Infection processes of fungi. The Rockefeller Foundation, New York, NY, pp 1–12 St Leger RJ, Screen S (2001) Prospects for strain improvement of fungal pathogens of insects and weeds. In: Butt TM, Jackson C, Morgan N (eds) Fungal biocontrol agents: progress, problems and potential. CAB International, Wallingford, UK, pp 219–238

Entomopathogenic Nematodes and Insect Management David I. Shapiro-Ilan, 1 Parwinder S. Grewal, 2 United States Department of Agriculture, Agricultural Research Service, Byron, GA, USA 2 The Ohio State University, Columbus, OH, USA

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Entomopathogenic nematodes are small round worms comprising three genera in the order Rhabditida: Heterorhabditis Poinar, Steinernema Travassos, and Neosteinernema Nguyen and Smart. More than 35 species of entomopathogenic nematodes have been described. These nematodes are widespread and have been isolated from soil or natural hosts in every continent except Antarctica. In nature, these nematodes are obligate pathogens of insects, and thus have been developed as bioinsecticides to suppress arthropod pests. Entomopathogenic nematodes kill their hosts with

the aid of a symbiotic bacterium. Heterorhabditid nematodes are associated with the bacteria Photorhabdus spp. And steinernematids are associated with Xenorhabdus spp. The bacterial symbiont associated with neosteinernematids has yet to be described.

Biology A generalized life cycle of entomopathogenic nematodes is depicted in the accompanying figure (Fig. 37). The infective (Fig. 38) juvenile nematode, which is the only free-living stage, enters the host via natural openings, i.e., mouth, anus, spiracles, or occasionally through the insect cuticle. Once the nematodes penetrate into the host’ s hemocoel, the symbiotic bacteria (carried in the infective juvenile’ s intestine) are released and multiply rapidly, nematode development is initiated, and the host dies within 24–72 h. After the nematodes complete one to three generations within the insect cadaver, infective juveniles exit to find new hosts. The nematode life cycles differ among the genera in that the steinernematids contain only amphimictic forms (males and females), whereas the first generation of heterorhabditids (arising from infective juveniles) contain only hermaphrodites, and subsequent generations may contain amphimictic and hermaphroditic forms. Only one species of neosteinernematids has been described to date; their life cycle is similar to the steinernematids except that only one generation occurs in the host, and infective juveniles arise in female nematodes that have exited the host cadaver. The relationship between the nematodes and their natural bacterial symbionts is mutualistic. The bacteria provide nutrients to the nematodes, produce antibiotics that inhibit competing microbes, and kill the host through septicemia (occasionally a bacterial toxemia precedes septicemia). Although the nematodes may also contribute to host death through suppression of the immune system and toxin production, the most important role they play in the mutualism is serving as vectors for the


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Entomopathogenic Nematodes and Insect Management, Figure 37 A generalized life cycle of entomopathogenic nematodes.

Entomopathogenic Nematodes and Insect Management, Figure 38 An infective juvenile steinernematid nematode.

bacteria. Without the nematodes the bacteria cannot survive well outside of the host, e.g., in soil, and the nematodes are required for entry into the host hemocoel (few bacteria strains are pathogenic when ingested by a host). The relationship between nematode and bacterium is highly specific. Each steinernematid or heterorhabditid species is primarily associated with a single bacterial species, although

some (Fig. 38) bacterial species can be associated with more than one nematode. The specificity of particular bacteria for growth and compatibility with nematodes can vary further on a strain level. The bacteria cells occur as two phenotypic variants: primary and secondary, which differ in dye absorption, response to biochemical tests, and antibiotic production. Although entomopathogenic nematodes have been reported to grow on secondary cells or even on certain non-symbiotic bacteria, the primary cells are most conducive to nematode growth. Infective juveniles only retain the primary cells.

Commerical Develoment and Efficacy Entomopathogenic nematodes possess many positive attributes as biological control agents. They are safe to humans and are generally safe to other non-target organisms and the environment. Additionally, entomopathogenic nematodes have

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a wide host range, a durable infective stage, and can be applied using standard agricultural and horticultural equipment. Another beneficial quality that entomopathogenic nematodes possess as biological control agents is amenability to mass production. The nematodebacteria complex is mass-produced using in vivo (i.e., in insects) or in vitro methods (solid or liquid fermentation). In vivo production requires a low level of technology and relatively little capital outlay. However, cost efficiency using in vivo methodology is low due to space and labor requirements. Some of the factors that can affect nematode yield in vivo include choice of insect host and nematode species, nematode inoculum concentration, and environmental factors (humidity and temperature). The most common host used for in vivo production is the greater waxmoth, Galleria mellonella (L.); depending on nematode species, yields in G. mellonella vary from approximately 40,000 to 300,000 infective juveniles per insect. In vitro solid culture, i.e., growing the nematodes and bacteria on crumbled polyurethane foam infused with a liquid medium, offers an intermediate level of technology and costs between in vivo and liquid culture. Nematode yield using solid fermentation is affected by inoculum size, culture time, and media composition. Yields can vary from approximately 200,000 to 500,000 infective juveniles per gram of media. In vitro liquid culture is the most cost efficient production method but requires the largest startup capital outlay. Factors that affect nematode yields in liquid fermentation include nematode species, mixing (bioreactor design), aeration, and media. Entomopathogenic nematodes have been successfully cultured in bioreactors with capacities as large 80,000 liters, and yields of up to 300,000 infective juveniles per ml have been reported. For small-scale or laboratory purposes, entomopathogenic nematodes are generally produced in vivo and stored in aqueous suspension (with sufficient exposure to oxygen) prior to use. Commercially produced nematodes, however, must be formulated prior to delivery and application. An effective formulation provides a suitable shelf life,

stability of product from transport to application, and ease of handling. Increased shelf life, in most entomopathogenic nematode formulations, is obtained by reducing nematode metabolism and immobilization, which may be accomplished through refrigeration and partial desiccation. Optimum storage temperature for formulated nematodes varies according to species: generally, steinernematids tend to store best at 4–8°C whereas heterorhabditids have longer shelf life at 10–15°C. Various formulations for entomopathogenic nematodes have been reported, including activated charcoal, alginate and polyacrylamide gels, baits, clay, peat, polyurethane sponge, vermiculite, and water-dispersible granules. Depending on the formulation and nematode species, successful storage under refrigeration ranges from one to seven months. The efficacy of entomopathogenic nematodes in suppressing insects depends on selection of the appropriate nematode for the target pest. A suitable nematode must possess a high degree of virulence (killing power) to the host. The nematode must be able to effectively invade and overcome the host immune system under field conditions (laboratory virulence does not necessarily predict field efficacy). Although many entomopathogenic nematodes possess a broad host range spanning several taxonomic orders, the nematode most suited to a particular pest will often be species and strain dependant. Not all entomopathogenic nematodes have broad host ranges, e.g., S. kushidai Mamiya appears to be specific for scarab beetles (Coleoptera: Scarabaeidae) and S. scapterisci Nguyen and Smart is most suitable to two-clawed mole cricket hosts (Scapteriscus spp.). The ability of entomopathogenic nematodes to persist in the environment may also contribute to host suitability. Indeed, in some cases enhanced persistence may even compensate for lower virulence. Generally, high levels of efficacy persist for only two to six weeks following nematode application. However, there have been some reports of prolonged pest control over several seasons or years. Nematode persistence depends on the nematode


species or strain, host density, and environmental factors (e.g., temperature, moisture, etc.). Additionally, the suitability of an entomopathogenic nematode to control a particular pest depends on the nematode’ s foraging strategy. Foraging strategies exhibited by entomopathogenic nematodes exist along a continuum from ambushers to cruisers. Ambushers use a sit and wait strategy; they usually stand on their tails (nictating) and wait until a host comes close before infecting. Cruisers actively seek out their hosts and cue into certain target volatiles (e.g., CO2) prior to contacting the host. Examples of nematodes that exhibit foraging behavior characteristic of ambushers include S. carpocapsae (Weiser) and S. scapterisci, those exhibiting behavior typical of cruisers include H. bacteriophora Poinar, H. megidis Poinar, Jackson, and Klein, and S. glaseri (Steiner), and those with intermediate search behavior include S. feltiae (Filipjev), and S. riobrave Cabanillas, Poinar, and Raulston. Ambushers tend to be most successful at infecting mobile insects on or near the soil surface, whereas cruisers tend to be most successful at infecting sessile insects below the soil surface. Abiotic factors are critical in determining efficacy of entomopathogenic nematode applications. These nematodes are highly sensitive to desiccation and ultraviolet light. Thus, applications made to soil or other cryptic habitats (and made during the early morning or evening) tend to be most successful. Temperature extremes (e.g., below 20°C and above 30°C) can be detrimental to nematodes. The optimum temperature for maximum efficacy depends on nematode species or strain; some nematodes are relatively heat tolerant such as H. indica Poinar, Karunakar, and David, and S. riobrave, whereas others are relatively cold tolerant, e.g., H. megidis and S. feltiae. Soil characteristics can also be important in determining efficacy, e.g., coarse soils with high sand content facilitate nematode movement and allow for air exchange. Nematodes require oxygen for survival, and thus factors that reduce airflow such as compacted or water-saturated soil are detrimental. Other pesticides or fertilizers used in conjunction with entomopathogenic nematodes may

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affect efficacy antagonistically, additively, or synergistically, depending on the agent(s) involved. Following is a list of some insect pests for which high levels of suppression (greater than or equal to 80%) were achieved under field conditions using entomopathogenic nematodes (Table 4). A high degree of efficacy in pest suppression, however, does not necessitate an opportunity for successful application on a commercial scale; economic factors are also important. Generally, to achieve a high degree of efficacy, at least 25 infective juveniles must be applied per cm2 of treated area (= 2.5 × 109 per hectare). Based on the number of nematodes required for successful pest control, and current production methods, the cost of entomopathogenic nematodes tends to be relatively high compared with many chemical insecticides. Therefore, commercial use of entomopathogenic nematodes has been cost prohibitive in many low-value crops (e.g., row crops such as cotton and corn), and has been most successful in certain high value crops or niche markets. Some examples of pests and markets where entomopathogenic nematodes have been successfully commercialized include billbugs (Sphenophorus spp.) in turf, black vine weevil, Otiorhynchus sulcatus (F.), in cranberries and ornamental plants, diaprepes root weevil, Diaprepes abbreviatus (L.), in citrus, fungus gnats (Diptera: Sciaridae) in mushrooms, Scapteriscus mole crickets in turf, and white grubs (Coleoptera: Scarabaeidae) in turf and ornamental plants. Several measures can improve entomopathogenic nematode efficacy. Advances in production, formulation, and application technology can enable more viable nematodes to be applied to the same area for an equal or lower cost. Discovery of new nematode strains or species with superior beneficial traits such as virulence, persistence, or environmental tolerance, can enhance the potential for successful pest suppression. Beneficial traits may also be developed in entomopathogenic nematodes through genetic methods, i.e., artificial selection, hybridization, mutagenesis, and genetic transformation.

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Entomopathogenic Nematodes and Insect Management, Table 4 A list of some pests for which at least 80% suppression was reported using entomopathogenic nematodes under field conditionsa Pest common name

Pest scientific name

Nematode(s)b

Artichoke plume moth

Platyptilia carduidactyla (Riley)

Sc

Banana moth

Opogona sachari Bojer

Hb, Sc

Banana root borer

Cosmopolites sordidus (Gemar)

Sc, Sf, Sg

Black cutworm

Agrotis ipsilon (Hufnagel)

Sc

Black vine weevil

Otiorhynchus sulcatus (F.)

Hb, Hm

Borers

Synanthedon spp.

Hb, Sc, Sf

Codling moth

Cydia pomonella (L.)

Sc

Corn earworm

Helicoverpa zea (Boddie)

Sr

Diamondback moth

Plutella xylostela (L.)

Sc

Fungus gnats

Diptera: Sciaridae

Sf, Hb

Japanese beetle

Popillia japonica Newman

Hb, Sg

Leafminer

Liriomyza spp.

Sc

Mole crickets

Scapteriscus spp.

Sc, Sr, Ss

Root-knot nematodes

Meloidogyne spp.

Sc, Sf, Sr

At least one scientific paper reported ≥80% suppression of these pests. Hb = Heterorhabditis bacteriophora, Hm = H. marelatus, Sc = Steinernema carpocapsae, Sf = S. feltiae, Sg = S. glaseri, Sr = S. riobrave, Ss = S. scapterisci. a

b

Through continued research the use of entomopathogenic nematodes is expanding. In addition to controlling harmful insect pests, novel uses of entomopathogenic nematodes, and more so, their symbiotic bacteria or associated metabolites, are being pursued to suppress plant parasitic nematodes, and as anti-microbial agents in pesticide and pharmaceutical applications. Furthermore, toxins produced by the bacteria are being studied for their suitability as alternatives to other orally active insecticides such as toxins produced by Bacillus thuringiensis.

References Gaugler R (ed) (2002) Entomopathogenic nematology. CABI, New York, NY, 388 pp Gaugler R, Kaya HK (eds) (1990) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, FL, 363 pp

Georgis R, Gaugler R (1991) Predictability in biological control using entomopathogenic nematodes. J Econ Entomol 84:713–720 Kaya HK, Gaugler R (1993) Entomopathogenic nematodes. Annu Rev Entomol 38:181–206 Kaya HK, Stock SP (1997) Techniques in insect nematology. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic Press, San Diego, CA, pp 281–324 Shapiro-Ilan DI, Gaugler R (2002) Production technology for entomopathogenic nematodes and their bacterial symbionts. J Ind Microbiol Biotechnol 28:137–146

Entomophagous Insectivorous; the consumption of insects or their parts. Though formerly used to describe a broad range of associations that resulted in insects being killed, it now is used mostly to indicate predation of insects. Parasitic relationships are best described as entomoparasitic (for parasitoids) or entomophilic/ entomopathogenic (for nematodes and microbial pathogens).

Entomophagy: Human Consumption of Insects

Entomophagy Consumption of insects by other animals and carnivorous plants.

Entomophagy: Human Consumption of Insects Jun Mitsuhashi Tokyo University of Agriculture, Tokyo, Japan In ancient times, when humans first appeared on the earth, insects might have been important foods for them, because they had neither tools to hunt large animals, nor techniques for agriculture. Since then, entomophagy has continued up to the present time all over the world. Human coprolites, which were found in some caves in the USA and Mexico, give evidence to the above consideration. From the coprolites found in caves of the Ozark Mountains located between Arkansas and Missouri, ants, larvae of beetles, lice, ticks and mites were isolated. On the wall of a cave of Artamila in North Spain, a picture showing the collection of wild bee nests was found. It is said that the picture was drawn about 9,000 to 30,000 years B.C. At that time people might have eaten bee larvae and pupae together with the honey. In Shanxi Province, China, cocoons of a wild silkworm, Theophila religiosae, were found from the ruins of 2,000 to 2,500 years B.C. Each cocoon had a large hole on it, suggesting that people ate pupae of the silkworms. People ate various insects everywhere in the world, and this developed into traditional entomophagy. Some traditional entomophagy has been handed down to the present. Most insect species are edible, but some are toxic. More than 1,000 species have been consumed as foods. However, identification of the species is difficult, because in many cases edible insects are given vernacular names. Some of more important groups include grasshoppers; caterpillars; beetles (larvae and adults); termites; bee, wasp and ant brood (larvae, pupae and sometimes winged adults); cicadas; and various aquatic insects.

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Present entomophagy may be divided into two categories. One is consumption of insects as necessary nutrients, and the other is uptake of insects as a condiment. In the former case, insects are consumed as protein sources in the area where malnourished people live, or at the time of famine. For example, locust outbreaks are common in Africa and the Middle East, and edible plants are scarce after migration of locusts. Under these circumstances, people catch locusts for their food. However, sometimes local government sprays insecticides against locusts. The insecticidesprayed locusts are no longer suitable for food. Then there will be conflicts between people and the government. In the latter case, insects appear as cuisine in restaurants in big cities, and are also sold as processed food. In restaurants, insect dishes are always more expensive than beefsteak. The popular insects served in restaurants are maguey worms (Cossus redtenbachi and Aegiale hesperiaris), ants (Liometopum apiculatum) in Mexico; wasps (Vespa sorror), wild silkworm pupae (Antheraea pernyi), and pyralid moth larvae (Chilo fuscidentalis) in China; wasps (Vespa sp.), bees (Apis dorsata), giant water bugs (Lethocerus (Belostoma) indicus), pyralid moth larvae (C. fuscidentalis) in Thailand. The processed insects also are expensive compared with other food. As processed insect foods, the followings are commercially available; canned rice grasshoppers (Oxya yezoensis), wasps (Vespa lewisi), silkworm pupae and adults (Bombyx mori), and larvae of Trichoptera from Japan; canned silkworm pupae (B. mori) from Korea; canned spice (namphric) containing giant water bugs (L. indicus) from Thailand; canned mopany worms (Goninbrasia belina) from South Africa; bottles of mezcal containing maguey worms (C. redtenbachi) from Mexico; canned soup containing witjuti (witchetty) grubs (larvae of large cossid moth) from Australia; candies containing mealworms (Tenebrio molitor) or crickets (Acheta domesticus) and fried snacks of some lepidopteran larvae from the USA.

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Insects are eaten raw or cooked. In tropical regions where palm weevils (Coleoptera: Rhynchophoridae) are distributed, the larvae are eaten raw by native people joyfully at the moment when captured. In Papua New Guinea, children eat small grasshoppers as a favorite food. Many other species are consumed raw by people in developing countries. The simplest and most primitive form of food preparation is roasting. It is common to roast insects in a fire or to throw them into hot ash. A more subtle way is to smother by burying insects in the soil with heated stones. Roasting insects by skewering them is popular too. Insects are also boiled or simmered in water or soup. They are often cooked with some vegetables and spices. Frying is also a popular cooking way of insects. Any species or any stage of edible insects can be eaten by frying. In many cases, fried insects with a bit of salt or spices are acceptable. Insects are also fried with vegetables. Some edible insects can be preserved by desiccation. In some places dried insects are commercially available in markets: e.g., mopany worms in South Africa, chipmi (Gynanisa maja, Saturniidae) in Zambia, small water bugs (ahuahutle) and their eggs in Mexico. Although cooking methods for insects are similar in many places, traditions have developed in some areas. Some examples of traditional entomophagy follow. In Japan, rice grasshoppers, wasps (V. lewisi), silkworm pupae and trichopteran larvae have been consumed from old times. All these insects are cooked with soy sauce, sugar and rice wine. These insects were used as a protein source by people who lived in mountainous areas and had limited access to fish. In Africa, termites are widely consumed. People collect termites when these insects swarm out of their nests at the first rain after the dry season. People eat them raw or fried. In Africa there are very many species of Saturniidae, whose larvae are large. Among these species, the mopany worm is famous. The mopany worm is distributed in southern Africa (i.e., South Africa, Botswana, Zimbabwe and Zambia). The worms are relished,

and people collect them to a greater extent when the worms reach full-grown stage. In addition to the consumption by the collector themselves, many dried larvae are exported to neighboring areas where the mopany worm does not occur. The mopany worm is prepared mostly by stewing. In Lake Nyassa, when the midge Chaoboris edulis is very abundant, Tanzanians collect flies, press them into cakes, and dry them under the sun. The products are called “kungu,” and are said to have taste of caviar. Also, Malawians collect ephemeropteran adults, and make cakes. This is also called kungu. In Thailand and surrounding areas, giant water bugs have been consumed widely. People not only eat intact insects, but also make spices (namplaa sauce or namphric) from the scent glands of males. In Australia, the aboriginal people still keep the custom of eating witjuty grubs (large cossid moth larvae) and a honey pot ant, Camponotus inflatus. People eat the witjuty grubs by roasting them, while the honey pot ants are consumed raw. The bogong moth, Agrotis infusa, is a well-known insect food for Aborigines. Every year, the adults migrate to the Australian Alps for summer estivation. Aborigines gather in the Alps to collect the estivating moths in interstices of rocks. They eat the moths by roasting them on heated ash. In the USA, the Paiute Indians living in the Sierra and Cascade Mountains used to collect the pandora moth larvae, Coloradia pandora lindseyi, from conifer trees. Like mopany worms, pandora moth larvae are consumed by roasting or by boiling (the boiled larvae are called “pe-ag-gie” or “piuga”). Modoc Indians in California used to consume the adult of a fly, Atherix sp., which is easily collected along rivers. People eat them by making loaves and roasting them. It is said that the taste is similar to headcheese. In California, Mono Lake Indians who lives near alkaline and saline lakes used to consume pupae of a brine fly, Ephydra hianus. A colossal number of the pupae are thrown up on the shore of the lake in late summer. The Indians harvested the pupae, removed puparia by rubbing, and ate them. This food is called “koo-chah-bee.”

Entomophilic

In Thailand, especially in northern part of the country, many insect species are consumed as food. One weaver ant, Oecophylla smaragdina, is commonly eaten raw or rubbed with salt, chili or pepper. A grasshopper, Patanga succincta, is also a popular edible insect and consumed by frying. A cricket, Brachytrupes portentosus has been commonly consumed. In China, cicadas, ants and wasps have been consumed since ancient times, and these insects are still served in restaurants. Insect foods can generally be said to be nutritious, because insects are rich in protein, lipid and vitamin. Although the chemical composition of insects varies with developmental stages and sexes even in the same species, protein is about 30–75% and lipid 5–60% of dry weight of insects. Among amino acid constituting insect protein, leucine, lysine and aspartic acid are said to be rich, while cystine and tryptophan are poor. However, some insect protein (for example, that of the house fly, Musca domestica) is said to have similar amino acid composition to beef protein. Lipids contained in insects resemble the lipids we take from usual food. For examples, fatty acid composition of the house fly pupae is said similar to that of fish fat. Carbohydrate is minor component of the insect body and is not an important nutrient in insect food. In general, insects contain a few percent of ash. Among minerals, the content of phosphate is commonly high. Insects contain considerable amount of Na, but only a little NaCl. Insects are rich in vitamins A, B1, B2 and D. Larvae of the bee, Apis mellifera, are said to have vitamin D ten times of that of cod liver oil, and vitamin A several times of that of egg yolk. These facts suggest that insects will be considered as a source of protein in the future. Most medicinal use of insects is a part of entomophagy. However, only a few substances have been identified as effective components of the insects used for medicines. Some insects are apparently used as medicines based on the superstition. Cantharidin from meloid beetles, and pederin from a staphilinid beetle, Paederus paralelus,

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are known to have fungistatic action. The former was once used as aphrodisiac, too. Crickets are said to contain a substance called grypin, which acts as antifebrile. A scale insect, Dactylopius coccus, contains red pigment called cochineal, which is used as cough medicine, and for trouble with nerves and kidneys. Cordyceps is not an insect but entomogenous fungus. It is used for various diseases; an effective substance, cordycepin, has been identified. There are many insect medicines based on superstition. For example, a cicada is used as a diuretic, because a cicada often excretes urine when it flies away, and people who have disuria might want to be able to urinate easily. Silkworm moths copulate soon after adult emergence, and for a long time. People used silkworm adults as an aphrodisiac, because impotent people envy their sexual strength.  Midges as Human Food  Native American Culture and Insects  Nutrient Content of Insects  Blister Beetles  Bogong Moth

References Bodenheimer FS (1951) Insects as human food. Dr. W. Junk Publishers, The Hague, The Netherlands, 352 pp Comby B (1990) Delicieux insectes. Editions Jouvence, Geneve, Switzerland, 156 pp Mitsuhashi J (1984) Edible insects of the world. Kokon Shoin, Tokyo, Japan, 270 pp (in Japanese) Paoletti MG, Bukkens SGF (eds) (1997) Minilivestock. Ecol Food Nutr (Special Issue) 36:95–346 Ramos-Erolduy J (1991) Los insectos como fuente de proteinas, 2nd edn. Editorial Limusa, Mexico City, Mexico, 148 pp Taylor RL (1975) Butterflies in my stomach. Woodbridge Press Publishing Co., Santa Barbara, CA, 224 pp

Entomophilic This term denotes an association of microbes or nematodes with insects (and also known as entomophilous). It is used to describe a phoretic or

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mutualistic association, but sometimes includes pathogenic associations. Thus, it is a very broad category that includes many types of associations, and for that reason, is not very descriptive. It is better to describe pathogenic associations as entomopathogenic rather than entomophilous or entomophilic.

Entomophobia Abnormal fear of insects and mites. It may be manifested in dermatitis induced by physical irritants or allergens, but also may result in hysterical reactions caused by the sight of the actual or purported organisms. The occurrence of invisible “cable mites,” “paper mites,” and “computer mites,” are sometimes associated with this affliction.  Delusory Parasitosis

Entomophthorales Most of the entomopathogenic genera within the Zygomycetes belong to a large order, the Entomophthorales. A second order in the Zygomycetes is the Mucorales, most of which are saprophytic; one genus, Sporodiniella, however, does infect membracids. Members of the Entomophthorales, with the exception of the genus Massospora, are characterized by the presence of forcibly discharged conidia; in Massospora, conidia are formed within the abdomens of periodical cicadas in the genus Magicicada. In addition to conidia, the Entomophthorales also produce zygospores (sexual) and azygospore-type resting spores, and mycelia are usually coenocytic, i.e., non-septate. The order is separated into six families depending upon nuclear cytology, characteristics of vegetative cells, and the modes of formation and germination of resting spores. Most notably, species in the genus Entomophthora (Entomophthoraceae), which was once the largest genus in the order, have been separated and moved into other genera.

Members of the Entomophthorales can attack a wide variety of insect hosts, including species from Hemiptera, Diptera, Lepidoptera, Coleoptera, Orthoptera and Hymenoptera. The host range of some fungal species may be limited to a specific host insect or may be broad enough to extend to non-target insects. A fungus tentatively identified as Entomophthora was found on a termite (Isoptera) embedded in 25 million-year-old amber. The Entomophthorales are especially important pathogens of aphids, grasshoppers, muscoid flies and lepidopteran larvae, and can function as biocontrol agents against these pests. Interestingly, one species of Entomophthorales, Entomophaga maimaiga, was introduced into New England from Japan in 1910–1911 in order to control the gypsy moth (Lymantria dispar). At this time, the fungus could not be grown in the lab, so researchers depended upon its overwintering in the field to produce new spores for inoculum. However, the fungus disappeared until 1989, when it was recovered from the field in areas with established gypsy moth populations. It is suggested that either the fungus introduced in 1910 developed into a more aggressive strain that has only recently caused obvious, widespread outbreaks, or that a more aggressive strain has been introduced at some point. Some Entomophthorales will attack animals other than arthropods and can even infect mammals, including humans. Entomophthoromycosis in humans is caused by species of Conidiobolus or Basidiobolus, and occurs most often in tropical and subtropical regions. Infections usually are restricted to subcutaneous tissues such as those overlaying the paranasal sinuses, but it also has been reported to disseminate into the deep organs, i.e., lymph nodes, lungs, liver and intestines. As entomopathogens, the Entomophthorales can infect larvae, pupae or adult hosts. Some species have broad host ranges while others, such as Massospora, can infect only one insect species. Insects attacked by some Entomophthorales may not show any symptoms until late in the infection process. Infected grasshoppers and Lepidopteran

Entomopoxvirus

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Entomophthorales, Figure 39 Entomophthorales infected Plutella larvae. Note the halo of primary conidia that have been actively discharged from conidiophores on the diseased insect. For comparison, see healthy insect above the cadaver surrounded by discharged conidia.

larvae often display summit disease syndrome, meaning they have a tendency to climb to high positions, where they attach and die. Conidia from such cadavers then can disseminate easily to uninfected insects closer to the ground. The appearance of Entomophthorales-infected cadavers also depends upon whether they have surface conidia or internal resting spores. Insects from which conidia have been forcibly discharged may be surrounded by a halo of these propagules that forms as they settle on the substrate (Fig. 39). Diseased insects that produce the resting spore stage darken and liquefy internally.

References Andreadis TG, Weseloh RM (1990) Discovery of Entomophaga maimaiga in North American gypsy moth, Lymantria dispar. Proc Natl Acad Sci USA 87:2461–2465 Brobyn PJ, Wilding N (1983) Invasive and developmental processes of Entomophthora muscae infecting houseflies (Musca domestica). Trans Br Mycol Soc 80:1–8

Humber RA (1989) Synopsis of a revised classification for the Entomophthorales (Zygomycotina). Mycotaxon 34:441–460 Latgé J-P, Cole GT, Horisberger M, Prevost M-C (1986) Ultrastructure and chemical composition of the ballistospore wall of Conidiobolus obscurus. Exp Mycol 10:99–113 Samson RA, Evans HC, Latgé J-P (1988) Atlas of entomopathogenic fungi. Springer-Verlag, Berlin, Germany

Entomopoxvirus At present, the family Poxviridae is divided into two subfamilies: the Chordopoxvirinae, composed of eight genera of vertebrate viruses, and the Entomopoxvirinae, containing three genera, A, B, and C, of insect poxviruses. Comparative analysis among the vertebrate and Entomopoxvirus groups has suggested low levels of genomic homology. To date, over 30 insect poxviruses have been detected in Coleoptera (A), Lepidoptera (B), Orthoptera (B), and Diptera (C), and have been placed in genera A, B, or C on the basis of virus morphology. Members within genus A are characterized

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by oval-shaped virus particles containing a unilateral concave core region and a single lateral body. Members of genus B, isolated from both lepidopteran and orthopteran hosts, have ovalshaped virus particles with a rectangular core region that lacks a discrete lateral body. Genus C members possess a cuboidal or cushion-shaped virus particle, a dumbbell-shaped core region, and two lateral regions. Poxviruses are the largest and most complex viruses. Poxviruses encapsidate large (130–375 kbp) linear dsDNA molecules. The typical ovalshaped poxvirus measuring 200–400 nm in length may contain over 100 structural proteins. The biconcave or dumbbell-shaped core region contains tightly compressed nucleoprotein. The function of the lateral bodies is unknown. Surrounding the core and lateral body is a lipid bilayer referred to as the outer membrane. Extracellular poxviruses, released via budding, contain a second lipoprotein envelope. The majority of entomopoxviruses produce occlusion bodies at the late stage of infection. These Type B occlusions, also termed spheroids, are composed of the 115 kDa matrix protein spheroidin and numerous enveloped virus particles. The spheroidin component of the different entomopoxviruses appears to be conserved and all entomopoxviruses are sensitive to alkali treatment. It should be mentioned that the vertebrate poxviruses produce acid-sensitive Type A inclusions composed of individual viral particles encoated by a late viral protein. In addition to spheroids, members within genera A and B of the entomopoxviruses may produce virus-free, spindle-shaped inclusions. The 50 kDa protein fusolin (French fuseau = spindle) is the major component of spindles and represents, when present, one of the most abundant EPV proteins. The entomopoxviruses, like other poxviruses, replicate in the cytoplasm of host cells. This property mandates that poxviruses encapsidate a complete transcriptional system capable of producing functional viral m-RNAs. Poxviruses contain a DNA-dependent RNA polymerase composed of

multiple subunits which transcribes only ssDNA. Several of the subunits have been demonstrated to be homologous to eukaryotic RNA polymerases. A second enzyme is the multifunctional capping and methylation complex. This enzyme transfers guanosine and catalyzes the methylation of the terminal ribose molecules of the viral RNAs. The poly-A-polymerase, comprised of two subunits, adds adenylate residues (poly-A) to the 3ʹ end of the viral m-RNAs. Several encapsidated enzymes, including the monomeric DNA topoisomerase (333 aa), modify the topology via breaking and rejoining of DNA that allows the relaxation of the + and − strands of the supercoiled DNA. The topoisomerase of the AmEPV possesses structural features similar to the vaccinia virus enzyme. Various nucleotide triphosphate phosphohydrolases (NPH 1, 2), including a DNAdependent ATPase (NPH1), are present in poxviruses. The NPH1 and NPH-II cleave the NTPs into NDPs and free phosphate. A virally encoded protein kinase functions to phosphorylate several virion-specific proteins. Additional enzymes affiliated with poxvirus particles include endoribonucleases, deoxyribonucleases, and alkaline proteases. The endogenous alkaline protease, associated with the entomopoxvirus viral inclusions (spheroids), is derived from host insects. This host-derived protease, activated by alkaline gut conditions, assists in the degradation of the spheroidin (115 kDa) and the subsequent release of virus particles. Tissue culture-produced spheroids lack such alkaline protease activity.

References Bawden AL, Glassberg KJ, Diggans J, Shaw R, Farmerie W, Moyer RW (2000) Complete genomic sequence of the Amsacta moorei entomopoxvirus: analysis and comparison with other poxviruses. Virology 274:120–139 Mitsuhashi W (2002) Further evidence that spindles of an entomopoxvirus enhance its infectivity in a host insect. J Invertebr Pathol 79:59–61

Environmental Influences on Behavioral Development in Insects

Moss B (1990) Poxviridae and their replication. In: Fields BN, Knipe DM (eds) Virology, 2nd edn. Raven Press, New York, NY, pp 2079–2111

Entotrophi An order of hexapods in the class Entognatha, but sometimes considered to be insects. This is an alternate name for the order Diplura. They commonly are called diplurans.  Diplurans

Enumeration Sampling Sampling based on the complete counting of all individuals in the sample unit (contrast with binomial sampling).  Sampling Arthropods

Envelope A covering of carton or wax around the nest of a social insect, especially a social wasp.

Envenomization The toxic effects caused by stings, secretions, bites, stinging (urticating) hairs or other effects of poisonous arthropods. The same term is used to describe poisoning by other animals, including vertebrates.

Environmental Sex Determination A method of sex deternmination in which the environment, such as temperature, has a significant effect on the developmental process leading to one or the other sex.

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Environmental Influences on Behavioral Development in Insects Helmut V. B. Hirsch1, Helen Ghiradella2, Martin Barth2 1 State University of New York, Albany, NY, USA 2 Friedrich-Miescher-Laboratorium der Max-Planck-Gesellschaft, Tübingen, Germany Information stored in the genome cannot be altered over the course of a lifetime, but only across a multitude of generations. Thus, the genome can give rise to developmental programs that will result in an organism, but it cannot optimize this organism for the conditions it may meet during its particular lifetime. It has long been assumed that if that lifetime is short, such optimization may not be necessary and that such short-lived animals as insects are developmentally inflexible, ensuring genetic survival by fecundity, rather than by investment in the perfection of individuals. As we shall see, this is not the case; like vertebrates, insects steer, rather than aim, development, even of behavior, which will be our special focus here. Developmental plasticity of behavior is especially significant to the organism, indeed to the whole community, since even subtle changes in behavior can have significant effects on an animal’s success in obtaining food, escaping predation, or finding a mate. And we are now coming to realize that in insects, even as in vertebrates, behavioral development is the result of a series of “dialogs” between the nervous system and the outside world.

Background In vertebrates, early experience is known to affect development of brain and behavior; impoverishment of stimulation generally diminishes performance of the adult, while enhanced stimulation can be beneficial. “Normal” early

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experience is important for normal vision, social interaction, homing, development of song… the list is very long. But what of the invertebrates, especially the small, short-lived ones? Because of the above m entioned assumption of inflexibility, they have received little study; indeed they represent a new and hitherto unexplored world, one holding immense promise for broadening our understanding of the development of behavior. The common laboratory fruit fly, Drosophila melanogaster, is a wonderful starting point for such a journey of discovery and will allow us to explore the importance of environmental factors – sensory, social and chemical – in guiding devel opment. Drosophila has many advantages as a model system for an analysis of developmental plasticity. First it has a rich and varied repertoire of behaviors that are both reproducible and quantifiable. Second, its short generation time (~10 days at 25°C), the ease with which it can be cultured and the large numbers of individuals that can be maintained under the same environmental conditions at different stages of the life cycle, help pinpoint the nature of the inputs needed for optimum development and the timeframes within which they are effective (the so-called sensitive or critical periods). Third, there are numerous Drosophila nervous system mutants, many affecting vision and learning, which are useful tools in determining the mechanisms of experience-dependent development. Fourth, the Drosophila nervous system consists of a relatively small number (perhaps a few hundred thousand) of neurons many of which are identifiable and can be compared across individuals raised in different environments. Finally, we “higher animals” share many genes with Drosophila – for example genes critical to visual development in Drosophila have similar function in mice, zebra fish, frogs, turtles, quail, rats, squid, and even nematodes, so that it is not unlikely that genes involved in developmental plasticity in Drosophila are conserved. For these reasons, we propose that Drosophila can make yet another contribution to

biology by serving as a model of experiencedependent plasticity of brain and behavior. In Drosophila, courtship seems particularly appropriate for the study of developmental plasticity. It has obvious significance in the organism’s life history, it is easily studied in the laboratory and, because of its complexity, there is a good chance that even relatively subtle environmental variations may alter its expression. And, of course, what we are studying in the laboratory are manifestations of a neural plasticity that has long been selected for because it is advantageous in the flies’ natural habitat. Courtship matures gradually during the first few days of the adult stage; flies do not become fully competent to court or to be receptive to copulation until several days after they eclose from their pupal cases. This makes it possible that experience before and during the appearance of these behaviors could play a role in their development, much as it does for singing and mate choice in birds. Let us now look at the actual behaviors involved in Drosophila courtship.

Courtship Behavior in Drosophila Courtship of Drosophila can easily be studied under a dissecting microscope by placing two or more flies into a small (0.2 cm3) chamber. Shortly after being placed into the chamber, the male approaches the female, chases her, maintains his focus on her if she moves about, and orients his body so that he is facing her abdomen. He taps her abdomen with one of his foretarsi and (Fig. 40) vibrates the wing closest to her to produce a courtship song. After a few minutes, he may lick the female’s genitalia, attempt to copulate, or suddenly move in a semicircle to wind up in front of her, “eye-to-eye.” If his courtship stimulates her to become receptive, she slows down and eventually permits copulation by opening her vaginal plates.


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three: effects on a newly emerged male of the presence of adult males, effects of the presence or absence of early visual stimulation on courtship effectiveness, and effects of low levels of the neurotoxin lead on courtship behavior.

Effects of Homosexual Courtship During the First Hours of Adult Life on the Male

Environmental Influences on Behavioral Development in Insects, Figure 40 Diagrammatic representation of some common male courtship behaviors in Drosophila melanogaster. Early stages are characterized by chasing, orientation-back, and singing by the male; if the female becomes more receptive and slows down, the male will engage in orientation-front, licking, and making repeated copulation attempts until the female finally opens her vaginal plates, permitting him to mate.

We can view these behaviors, which involve visual, auditory, chemical and tactile stimulation, as an exchange of sensory information. Males use visual, and to a lesser extent chemical, information to identify and to orient to the female; the absence of this information (as in a male with mutationinduced sensory losses) reduces the likelihood of copulation. Female receptivity is also influenced by such visual cues as the reflection from, and shape of, the male’s eyes. Obviously, in a complex environment many agents may modify the development of courtship behaviors. We will look at

Drosophila melanogaster males do not court only virgin females, they also court newly eclosed males (The young males do gradually lose their “sex appeal” and by the time they are sexually mature are no longer attractive to other males.) One obvious question is why this behavior exists; this “homosexual” courtship expends time and energy and renders the courting male more vulnerable to predation, so it must have some positive evolutionary significance. With such experience, immature males grow up to mate more quickly than do males without homosexual courtship experience. The courtship song, produced by vibration of the courting male’ s wing, is one of the stimuli that affect the immature male, which suggests that early exposure to the visual and/or auditory stimuli associated with courtship song is important for development of effective courtship in males. The observation that adult male flies that experience homosexual courtship during early adult life perform better when courting females has striking similarities to what others have observed studying the development of bird song. In both cases, the immature male receives the stimulation during early life (Fig. 41), before he expresses the behaviors that are influenced by the exposure. In birds, this has been explained by postulating that the young male lays down an auditory template and later compares his own output to that template, modifying the output until there is an adequate match. We suggest that male Drosophila may be engaged in a similar process. During the episodes of homosexual courtship, they may be storing something analogous to a neural template

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Time to copulate (minutes)

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0 Exposure history of male Not courted by males Courted by non-singing males

ship behavior, during the first four days of adult life we kept flies either in total darkness (darkrearing - DD), in constant illumination (lightrearing - LL), or as a control in normal cycling illumination (12 h light/12 h dark-LD). We subsequently scored (Fig. 42) them for copulation latency, i.e., the time taken from the initiation of courtship to copulation. Surprisingly, what affects this most is the similarity in the experience of both members of the pair. Pairs in which the male and the female received the same visual exposure (both LD, both LL, or both DD) mate more quickly than do those whose early experience differed, i.e., “culturally” similar flies mated more readily. Furthermore, these studies revealed the presence of a critical period during which alterations in normal exposure are particularly effective in causing behavioral changes.

Courted by singing males

Environmental Influences on Behavioral Development in Insects, Figure 41 Latency to begin copulation with a female of males raised in the absence of older males, with older males that courted them but could not sing, with older males that courted them and could sing. Note that males copulate faster when they have been reared with older males that can sing while they court; other stimuli must also be important because being courted without singing is better than nothing (Data summarized in Hirsch and Tompkins, 1994).

of courtship; when they mature, this template in some way facilitates their own behavior. This remains an open question, as the relevant experiments remain to be done.

Effects of Visual Experience During the First Days of Adult Life Vision is important during courtship, and to determine whether early visual experience is important for the normal development of court-

Ecological Implications of Mate Choice The influence of genotype on mate choice is well-documented, while that of early experience is less well understood, except for a few studies on effects of early social interactions on mate preferences of avian and mammalian females. From the studies discussed above, we conclude that otherwise normal Drosophila raised in any of our three light regimes (LL, LD, DD) prefer to mate with partners with similar experience. Since females typically copulate on their food source, and then lay eggs in it, their newly eclosed offspring will find themselves in the same environment in which their parents chose mates. Given that flies growing up in this environment are apparently well adapted to it, then perhaps preference for mates with similar backgrounds, including environmental exposure histories, will enhance the fitness of their offspring, assuming the environment has not changed drastically. Thus, what we have learned about developmental plasticity of mate choice may help us to better understand the mechanisms regulating fitness in this species.


Time to copulate (seconds)

360 300 240 180 120 60 0

LL

LD DD Exposure history of female

Same history

Different history

Environmental Influences on Behavioral Development in Insects, Figure 42 Latency to begin copulation with a male of females raised in constant light (LL), in normal cycling illumination (LD), and in total darkness (DD). Note that the less light exposure, the faster females tend to copulate, and that independent of exposure history females copulate faster with males sharing their “culture.” (Redrawn from Hirsch et al., 2001.)

Developmental Effects of Exposure to Low Levels of Lead As a result of human activity, lead has become ubiquitous in the biosphere. At higher concentrations it can be very toxic, but even at very low concentrations chronic exposure during early life can have significant effects, including cognitive effects, in humans and in other mammals. Given that developmental plasticity is not exclusive to vertebrate animals, does developmental exposure to lead affect complex behaviors of Drosophila, in particular courtship? We choose courtship because it may provide an assay of cognitive function for Drosophila, in effect a fly equivalent of an IQ test. Courtship requires that male and female assess one another and reach a decision about whether to mate. Since consequences of this decision can have important consequences for both participants, and especially for the female who

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does not mate very often in her lifetime, factors influencing the decision-making process can affect fitness of the male and the female. The effects of lead exposure during development of Drosophila may be tested by exposing flies from egg stages until well into adulthood to a leadcontaminated food source. One then assays courtship by seeing how many flies will mate in a given time interval. The results are both striking and significant: the number of pairs mating after exposure to low concentrations of lead is greater than in controls, while after exposure to higher concentrations of lead it is lower. One possible explanation for the increase in mating speed after exposure to low concentrations of lead is that it reduces the female’s selectivity in choosing a mate; she may mate more indiscriminately than do control females. Exposure to higher lead concentrations, on the other hand, may debilitate both sexes sufficiently that courtship is slowed down. Lead also has a non-linear (in this case biphasic) effect on fecundity of Drosophila, increasing it at low concentrations, and having no clear effect at higher concentrations. The details of insect response to such toxicants as lead are as yet barely studied, but it is clear that insects such as Drosophila are indeed good model systems for the studies that need to be done.

Conclusions We began by noting that developmental programs that are limited to information in the genome are limited in their ability to optimize the organism for the conditions prevailing during its particular lifetime. We argue that a first step in optimizing development is by providing it with sensitivity to environmental experience. Learning and sensory adaptation enable the process of optimization to continue throughout the organism’s lifetime. In effect, these processes match the nervous system to those features of its environment which cannot be predicted far enough in advance to be incorporated into the genetic information base. Genetic information, which reflects adaptation to past conditions, is

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combined and integrated with epigenetic information, which is more immediately predictive of future conditions. There are clear precedents for such interpretation of developmental processes. For example, it is known that in the cat, initial development of nerve cells responding to the orientation of a visual image is under genetic control, but completion of development requires visual experience, which fine-tunes the system to respond best to those orientations it saw during the first months of life. In effect, these cells become an internal model of the animal’s early visual world. Because it was generated during a critical period after which it cannot be changed, this model has a life-long influence on the animal’s behavior. In the fly, initial development of the photoreceptors and of their connections with a target structure, the lamina, is likely to be under control of intrinsic developmental programs, whereas experience modifies both the synapses from the photoreceptors onto special lamina cells, the monopolar cells, and the feedback synapses going back to the photoreceptors themselves. Thus, there is a flexible link between the sensor and the nervous system, a link that can be optimized on the basis of information about the prevailing environment. Consistent with this idea, some behavioral sensitivities are enhanced under test conditions that mimic those present during the animal’s early life. Flies deprived of light exposure are more sensitive to light than controls, and the operating range of their visual systems is shifted to allow a better response at lower light levels. These effects are apparently long-term, being present three weeks later. The findings for both cat and fly support the hypothesis that during early stages of adult life the response properties of the visual system are adjusted to function optimally under the conditions prevailing in the animal’s visual world; other sensory systems undoubtedly show similar tunability. The last forty years, which have seen great changes in our understanding of how experience might affect the developing nervous system, have also witnessed the discovery of many model systems for the study of such development. These first

included the retinogeniculocortical pathway in the cat, and to a lesser degree in the monkey. In the early 1980s it became clear that lower vertebrates, such as fish and frogs, also constituted good model systems for studying experience-dependent development, and now it is clear that invertebrates can also serve this role. Experience-dependent behavioral plasticity, once assumed to be a curiosity playing at most a minor role in the development of insect brain and behavior, is known to exist in many regions of the adult brain in Drosophila and in other invertebrates. Indeed, it seems to be the rule rather than the exception that in all animals experience is needed to complete development of adult brain structures. A corollary of this view is that the ability to undergo experience-dependent development is itself heritable, and that it should be possible to select strains of flies or other invertebrates that are more or less modifiable by early experience, thereby generating additional models for studying developmental plasticity. One major task will now be to unravel the molecular mechanisms underlying the developmental adjustments in model systems such as Drosophila, and thereby to learn more about the often less accessible mechanisms underlying plastic processes in vertebrate brains. On a molecular level, there are likely to be several systems responsible for structural plasticity (for example, in Drosophila the cyclic AMP cascade seems to be involved in the central brain, but not in the optic lobes). There is a rich future for research in unraveling the genes involved in the plasticity of the visual system, and Drosophila is likely to continue to be a central figure in attempts to identify and characterize these genes. Among the many powerful techniques available with Drosophila is the capability of selectively expressing any cloned gene in specific regions of the fly, thus providing very fine “molecular scalpels.” The usefulness of these lessons from the world of insects will underscore the basic unity of the mechanisms that appear to govern the link between brain and behavior in all organisms. A very important lesson that we can learn as we come to understand more about brains and about

Ephemerythidae

what is needed to ensure their development, is that “higher” and “lower” animals have much more in common than had been thought possible 20 years ago. This commonality in our origins, and especially the realization that we are all affected by our environment during development, and that we update the information in the genome and enhance our ability to make accurate predictions about the world we live in, means that we have much to learn not only from our closest relatives, but from those who appear on the surface much more distant, and even alien. We hope it means also that our respect for these life forms – so like us in their vulnerability during development – will be enhanced, for in protecting and conserving them we are protecting and conserving ourselves.

References Greenspan RJ, Ferveur J-F (2000) Courtship in Drosophila. Annu Rev Genet 34:205–232 Hirsch HVB, Tompkins L (1994) The flexible fly: experiencedependent development of complex behaviors in Drosophila melanogaster. J Exp Biol 195:1–18 Hirsch HVB, Tieman SB, Barth M, Ghiradella H (2001) Tunable seers: activity-dependent development of vision in fly and cat. In: Blass E (ed) Developmental psychobiology, handbook of behavioral neurobiology, vol 13. Kluwer Academic/Plenum Publishers, New York, NY, pp 81–142 Waddell S, Quinn WG (2001) Flies, genes, and learning. Annu Rev Neurosci 24:1283–1309

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Eomeropidae A family of insects in the order Mecoptera.  Scorpionflies

Eosentomidae A family of proturans (order Protura).  Proturans

Epermeniidae A family of moths (order Lepidoptera). They commonly are known as fringe-tufted moths.  Fringe-Tufted Moths  Butterflies and Moths

Ephemerellidae A family of mayflies (order Ephemeroptera).  Mayflies

Ephemeridae A family of mayflies (order Ephemeroptera).  Mayflies

Enzootic Disease A disease (usually in low prevalence) which is constantly present in a population.

Enzyme A protein catalyst that is not itself used up in a reaction. Enzymes are produced by living cells to catalyze specific biochemical reactions. Enzymes may also contain nonprotein components called coenzymes that are essential for catalytic activity.

Ephemeroptera An order of insects. They commonly are known as mayflies.  Mayflies

Ephemerythidae A family of mayflies (order Ephemeroptera).  Mayflies

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Ephydridae

Ephydridae A family of flies (order Diptera). They commonly are known as shore flies.  Flies

Epicopeiidae A family of moths (order Lepidoptera) also known as Oriental swallowtail moths.  Oriental Swallowtail Moths  Butterflies and Moths

as well as a proteinaceous layer imbedded with lipids called the cuticulin layer.  Cuticle  Integument: Structure and Function

Epicuticular Filaments Lipoprotein running from the epidermal cells through the pore canals and fusing with the inner edge of the cuticulin. The filaments (and the pore canal) can serve as a conduit for transport of materials such as wax from the epidermal cells to the procuticle and epicuticle.

Epicranial Suture A Y-shaped suture on the upper surface of the head. The arms of the “Y” diverge toward the front of the head.  Head of Hexapods

Epicranium The upper portion of the head.  Head of Hexapods

Epicuticle The thin, outermost layer of cuticle. It is rich in lipid and protein but lacking in chitin. It consists of a shellac-like cement layer externally (Fig. 43, Fig 44)

Epidemic A period of unusually great abundance, especially of pests such as microbial disease agents.

Epidemic Hemorrhagic Fever A form of hemorrhagic fever endemic to northeastern Asia that is caused by a Hantavirus arbovirus transmitted by mites. It is characterized in its early stages by fever, sweating, thirst, abdominal pain, nausea, and vomiting, and in its later stages by hemorrhage, shock, and kidney failure. It is also called “Korean hemorrhagic fever.”  Mites Epicuticle Exocuticle Pore canal Endocuticle Schmidt’s layer Epidermis Basement membrane

Epicuticle, Figure 43 Cross section of the insect cuticle and epidermis (adapted from Chapman, The insects: structure and function).

Epimeron

Cement Wax Orientated wax Outer epicuticle Inner epicuticle Epicuticular filament

Procuticle Pore canal

Epicuticle, Figure 44 Cross section of the insect epicuticle (adapted from Chapman, The insects: structure and function).

Epidemic Relapsing Fever This disease is caused by a spirochete (Borrelia recurrentis) and is transmitted by human body lice. Once common in eastern Europe and Russia, it now occurs mostly in eastern Africa, China, and South America. An endemic form is caused by several forms of spirochete and is transmitted by Ornithodorus ticks. Symptoms include chills, fever, headache, muscle pain, nausea, vomiting, and weight loss.  Chewing and Sucking Lice

Epidemic Typhus A rickettsial disease (Rickettsia prowazekii) transmitted to humans by the human body louse. It occurs most frequently in cooler climates, where heavy clothing is commonly worn. It becomes epidemic during periods of strife, when warfare results in crowding and poor sanitation. It also can develop in prisons and on ships due to lack of sanitation and crowding, where it is known as “prison fever” and “ship fever.” The disease is transmitted through the feces of the lice when humans

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scratch and rub the louse or louse feces into a wound. The lice are not affected by the Rickettsia. A variant of this is transmitted from flying squirrels to humans when squirrels take up residence in cabins or houses. Symptoms of epidemic typhus include chills, fever, headache, rash, stupor, and delirium.  Chewing and Sucking Lice

Epidemiology In entomology, the study of diseases affecting insects, especially the factors affecting outbreak and spread of the disease, or of diseases spread by insects to animals (humans, wildlife, livestock) or plants.

Epidermis The layer of living cells (epidermal cells) of the integument, situated beneath the cuticle (Fig. 43), that secretes the cuticle at each molt. In addition, the epidermal cells secrete lipids (waxes), cement, and additional cuticular components.  Cuticle  Integument: Structure and Function

Epigaeic Living, or at least foraging, primarily above-ground (contrast with hypogaeic).

Epigynum In spiders, the external female genitalia.

Epimeron The posterior portion of a thoracic pleuron. It is usually small, narrow, or triangular.

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Epimorphosis

Epimorphosis A type of development wherein the insect ecloses from the egg with a full complement of body segments (the opposite of anamorphosis).

Epipharynx A mouthpart structure attached to the inner surface of the labrum or clypeus.

Epiphysis A pad occurring on the inner aspect of the front tibiae in some Lepidoptera.

Epiplemidae A family of moths (order Lepidoptera). They commonly are known as crenulate moths.  Crenulate Moths  Butterflies and Moths

Epipleura (pl. epipleurae) The lateral margins of the eytra, which are bent downward.

Epiproct The dorsal portion of the eleventh abdominal segment in insects. This is also known as the supraanal plate and the pygidium. This tergite often covers the anus.

Epipsocidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice or Psocids

Epipyropidae A family of moths (order Lepidoptera). They commonly are known as planthopper parasite moths.  Planthopper Parasite Moths  Butterflies and Moths

Episternum (pl. episterna) The anterior-most sclerite of the thoracic pleuron.  Thorax of Hexapods

Epistoma The portion of the lower face between the eyes and the mouth.

Epizootic An outbreak or widespread occurrence of disease in which there is an unusually large number of cases. A disease, or a phase of a disease, with high morbidity, and one that is only irregularly present in recognizable form.

Epizootic Bovine Abortion A bacterial disease transmitted by ticks to cattle in the western USA.  Ticks

Epizootiology The field concerned with the study of diseases of animals and their pattern of occurrence.

Equilibrium Position (EP) An expression used to describe the average density of pests relative to the economic injury level

Erichson, Wilhelm Ferdinand

and economic threshold. Some insects have a low equilibrium position and rarely cause damage, whereas others have a high equilibrium position and regularly inflict injury if they are not managed. The concept of EP is most useful when considering insects that do not vary greatly in density or damage, but some insects display highly variable densities, and the equilibrium position is not very descriptive of their population tendencies.

Eradication Elimination of an organism after it has become established.

Ergatogyne Among social insects, a form that is intermediate between the worker and queen.

Eremiaphilidae A family of praying mantids (Mantodea).  Praying Mantids

Ergatoid Reproductive Among termites, a supplementary reproductive that is larval in form, without any trace of wing buds, and with a distinctly rounded head.

Ergot of Cereals A fungal disease of grains that can be transmitted by insects.  Transmission of Plant Diseases by Insects

Erichson, Wilhelm Ferdinand Wilhelm Erichson was born on November 26, 1809, in Stralsund, Germany, the son of a senator.

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After education at the Gymnasium [“high school”] of Stralsund, he entered the Universität zu Berlin in October 1928, obtaining by December 1832 a degree “Doktor der Medizin und Chirurgie” [“Doctor of Medicine and Surgery”]. By April 1834 he was licensed as a medical prac titioner. During his university years, he was heavily involved in entomological studies, publishing (with J.F. Brant) in 1831 “Monographia generis Meloes” and then in 1832 “Genera Dyticeorum.” In 1837 he obtained a degree “Doktor der Philosophie” from Universität Jena. In 1838, he was awarded the degree of “Privatdocent” [a degree permitting him to lecture at a university] from the philosophical faculty of the Universität zu Berlin, and in 1842 was appointed adjunct professor. The scholastic requirements at German and other European universities were much more rigorous at that time than in the USA. Then, leaving medicine behind, his lectures concentrated on entomology and helminthology. He has been acclaimed by Herman (2001) as a genius, the equivalent of a Mozart in music and, like Mozart, dying young, perhaps the most important entomologist of all time. Although he died before he was 40, his works were prodigious and profoundly important. He worked on Arachnida and Myriapoda as well as on the insect orders Coleoptera, Hymenoptera, Neuroptera, Hemiptera, Strepsiptera, Thysanoptera, Thysanura, and Siphonaptera. He published about 45 books and other papers. Two of them were “Die Käfer der Mark Brandenburg” (740 pages) and “Genera et species Staphylinorum” (954 pages) in which he proposed for the first time a classification that in general still stands of the huge family Staphylinidae. He died in Berlin on November 18, 1849.

Reference Herman LH (2001) Erichson, Wilhelm Ferdinand. Bull Am Mus Nat Hist 265:60–61

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Eriococcidae

Eriococcidae A family of insects in the superfamily Coccoidae (order Hemiptera).  Bugs

Eriocottidae A family of moths (order Lepidoptera). They also are known as Old World spiny-winged moths.  Old World Spiny-Winged Moths  Butterflies and Moths

Eriocraniidae A family of moths (order Lepidoptera). They commonly are known as sparkling archaic sun moths.  Sparkling Archaic Sun Moths  Butterflies and Moths

Eri Silkworm, philosamia ricini (Lepidoptera: Saturniidae) Tipvadee Attathom Kasetsart University, Nakhon Pathom, Thailand Silk is a smooth, shining, fabulous and unique natural fiber produced by several species of silkworm. Silk fiber generally is produced by the mulberry silkworm, Bombyx mori, which was domesticated nearly 2,000 years ago in China. Silkworm rearing and silk weaving, called sericulture, is an environmentally sustainable agro-industrial activity practiced in four major regions globally, with the highest production in Asia and the Pacific. Sericulture provides substantial contributions to a number of national economies while preserving the centuries-old history and tradition of many countries. It is beneficial to the rural population in climatically suitable agricultural sectors because it

provides either a primary or secondary source of income for many workers, regardless of age and gender. In addition to the renowned mulberry silkworm, Bombyx mori, there are at least eight species of wild silkworms that provide silk of high economic and commercial values. They are: Antheraea pernyi, A. yamamai, A. proylei, A. assamensis, A. mylitta, A. proylei, Philosamia ricini and P. cynthia. The eri silkworm, P. ricini, is the only completely domesticated silkworm that is not dependent on mulberry for food. This polyphagous insect feeds on several varieties of food plants in the family Euphorbiaeae, including castor (Ricinus communis), kesseru (Heteropanax fragrans), payam (Evodia flaxinifolia) and tapioca (Manihot utilissima). Castor is, by far, the best food plant to promote cocoons that are large in size and rich in silk content. Eri silkworm has four stages: the egg, larva, pupa (encased in the cocoon), and the adult or moth. The moth lays white eggs which turn grey and then black just before hatching. Eggs hatch in seven days in hot weather, but may take as long as 24 days in cold weather. Female moths lay eggs in clusters that may contain as many as 100 or more eggs. The number of eggs per moth varies, however, the average for a well-fed, healthy moth is about 300. Eri silkworm molts four times during its larval stage. When molting, the larvae stop eating and become motionless. This state may last for 24–48 h. Toward the end of this state, the larvae begin to cast their skins off by continued undulatory movements and wriggling. During the first to third larval stage, the head is black and shiny but eventually will turn greenish-yellow or yellow with a blackish patch on each cheek when they reach the fourth and fifth stages. On each thoracic and abdominal segment, there are four to six conspicuous tubercular spines mounted with a varying number of hairs and arranged in longitudinal rows. In the fifth stage, the larvae eat enormously and grow very quickly to reach their maximum stage of development. The well-fed (Fig. 45), full-grown

Eri Silkworm, philosamia ricini (Lepidoptera: Saturniidae)

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Eri Silkworm, philosamia ricini (Lepidoptera: Saturniidae), Figure 45 Larvae of eri silkworm, Philosamia ricini feed on cassava leaves.

Eri Silkworm, philosamia ricini (Lepidoptera: Saturniidae), Figure 46 Cocoons of eri silkworm cut to show the pupae inside.

larvae are cylindrical and about 95–100 mm long. The general body color is white which turns yellow before spinning. When the larvae get ready for spinning, they cease feeding and empty their digestive tract. The larvae then become active and roam about in search of a suitable place, and settle down to form cocoons. The cocoon is formed by exuding secretion from the silk gland through the spinneret which forms a fine filament of thread when it comes in contact with the air. The larvae finish spinning in about three days and rest inside the cocoon before turning into pupae (Fig. 46 and 47). The thread of the cocoon consists of a core of fibroin and a covering of sericin or gum. The eri cocoon is tapered at one end and is slightly flat and round at the other. It can not be reeled because the cocoon is not formed of a long continuous thread as in mulberry silk, but instead is spun by the larvae in layers. It is also an open cocoon in which the moth can push its way through one end without softening or cutting the fibers. Since eri cocoons are unreelable, they can only be spun by hand. They form a good and highly desirable raw material for millspun silk which is in high demand all over the world. Moth emergence from the cocoon takes place after about two weeks from the cocoon formation. Male moths emerge earlier than female moths. The eri moth is a big moth with a wingspread of

Eri Silkworm, philosamia ricini (Lepidoptera: Saturniidae), Figure 47 Container provided to eri silkworm for cocoon formation.

100–125 mm. The wings are blackish-brown, crossed in the middle with a white band. In the middle of each wing is a crescent-shaped yellow and white spot bordered with a black line. The abdomen of the male is narrower than that of the female. After emergence, the males are more active. They flutter their wings rapidly and rest for an hour or two in a vertical position until their wings are dry. The male moths then start fluttering their wings again in search of female moths to mate with. Mating (Fig. 48) occurs a few hours after moth emergence and female moths lay eggs during the night. The oviposition

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Erimine Moths (Lepidoptera: Yponomeutidae)

insects, can be raised in laboratories using eri larvae as food. Furthermore, due to their high protein content, eri larva and pupa are eaten by people, especially those in the Asian countries. They also can be developed as animal feeds or food supplements for poultry, swine and fish which help to reduce production costs in these farms. The eri silkworm, therefore, can create several operations of high income potential. Many countries, therefore, are highly interested in the national industrialization of eri silkworm culture. Eri Silkworm, philosamia ricini (Lepidoptera: Saturniidae), Figure 48 Male and female eri silkworm shown mating. The female lays eggs on the wood stick.

can go on for two or three nights. The moths do not fly away and do not eat. The complete life cycle of the eri silkworm lasts about 44 days in the summer and 85 days in the winter. It is a multivoltine species which can be reared four to five generations all year round where the climatic conditions are favorable. Eri silkworm cultivation has several profitable advantages. Since the worms feed on castor and tapioca or cassava leaves, eri silkworm cultivation can be practiced as a subsidiary cottage industry by the castor and cassava growers. With its excellent blending properties with both cotton and synthetics, the fabrics made from eri silk yarn are very soft and silky, far more durable than mulberry silk and far more resistant to perspiration and dust. Eri silk is also readily dyed with a large range of colors. All these unique characteristics make the cloths suited not only for dresses but also for shawls, cloaks, rugs, etc. In addition to finished fabrics, eri silk can also become the source of other essential products such as medicines and cosmetics. Eri silkworms play a significant role in the research on the biological control of noxious insects. Eri egg and larva can be used to mass produce some parasitic and predatory insects. The predatory bug, Eocanthecona furcellata, which preys on several species of noxious lepidopteran

References Maxwell-Lefroy H, Ghosh CC(1912) Eri silk. Memoirs of the Department of Agriculture in India, Entomological Series 4, vol 1, 130 pp Sarkar DC (1988) Eri culture in India. Central Silk Board. Grafo Printers, Bangalore, India, 51 pp Sengupta K (1985) Non-mulberry sericulture – its problems and prospects. Sericologia 25:89–94

Ermine Moths (Lepidoptera: Yponomeutidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Ermine moths, family Yponomeutidae, total 395 species worldwide; actual fauna likely exceeds 500 species. Three subfamilies are recognized: Saridoscelinae, Yponomeutinae, and Cedestinae. The family is part of the superfamily Yponomeutoidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small to medium size (8 to 31 mm wingspan), with head mostly smooth-scaled; haustellum naked; labial palpi upcurved; maxillary palpi 1 to 2-segmented (rarely reduced). Wings elongated, sometimes with long hindwing fringes (Fig. 49) in species with more lanceolate hindwings. Maculation is often white or gray with many small dark spots, or more monotone shades of brown or gray. Adults are mostly nocturnal. Larvae are leaf

Esaki, Teiso

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Eruciform Larva A larval body form with a cylindrical body, well developed head, and usually with thoracic legs and abdominal prolegs. Often they are sluggish, and found in the soil or living in burrows within fruit, seeds or wood. Caterpillars and white grubs are typical of eruciform larvae.

Ermine Moths (Lepidoptera: Yponomeutidae), Figure 49 Example of ermine moths (Yponomeutidae), Yponomeuta cagnagella (Hübner) from Italy.

skeletonizers and leaf webbers, but some are leafminers or needleminers. Hosts include many different plant families. A few species are economic, particularly in the genus Yponomeuta (often misspelled as Hyponomeuta in older literature).

References Clarke JFG (1965) Hyponomeutidae [sic]. In: Clarke JFG, Catalogue of the type specimens of Microlepidoptera in the British Museum (Natural History) described by Edward Meyrick, vol 5, 257–413 [part]. British Museum (Natural History), London Gershenson ZS, Ulenberg SA (1998) The Yponomeutinae (Lepidoptera) of the world exclusive of the Americas. Nederl. Academie Wetensch, Amsterdam, 202 pp, 3 pl Huemer P, Tarmann G (1991) Westpaläarktische Gespinstmotten der Gattung Kessleria Nowicki: Taxonomie, Ökologie, Verbreitung (Lepidoptera, Yponomeutidae). Mitteilungen der Münchner Entomologische Gesellschaft 81:5–110 Martouret D (1966) Sous-Famille des Hyponomeutinae [sic]. In: Balachowsky AS (ed) Entomologique Appliquee a l’ Agriculture, vol 2. Masson, Paris, pp 102–199 *Moriuti S (1977) Yponomeutidae s. lat (Insecta: Lepidoptera). In: Fauna Japonica. Keigaku, Tokyo, 327 pp, 95 pl

Erotylidae A family of beetles (order Coleoptera). They commonly are known as pleasing fungus beetles.  Beetles

Esaki, Teiso Teiso Esaki was born in Tokyo on July 15, 1899. His father was a government forestry official. Teiso grew up at first in Tokyo and then in Osaka. He published his first entomological note at the age of ten, in the journal Gifu (“Insect World”), which may be a record for young entomologists. He continued studying insects, especially Hemiptera, and publishing on them, while he was in middle school in Osaka. In 1920 he entered the Imperial University of Tokyo, and studied zoology. In 1923 he was appointed associate professor in Kyushu Imperial University, and in 1924–1927 was sent to Europe (especially Budapest and London) to study in the main museums and institutions. Then with his new, German, wife Charlotte, he returned to Japan via the USA. Eventually they had four children. He was elected to the council of the entomological society of Japan, and in 1951 was its president. In 1928, he was appointed chairman of entomology in Kyushu Imperial University, and in 1930 professor of entomology. He was appointed Japanese representative and commissioner to the International Commission of Zoological Nomenclature. He was interested in many aspects of natural history, and especially in zoogeography, zoological nomenclature, the history of biology, Hemiptera, Lepidoptera, and fossil insects, but his specialty was in aquatic Hemiptera, on which he became a world authority. He published about 130 important papers on Hemiptera. He died in Fukuoka, Japan, on December 14, 1957.

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Esophagus

Reference China WE (1958) Obituary. Entomologist’s Monthly Magazine 94:132

Esophagus A portion of the foregut behind the pharynx and leading to the crop.

Essential Amino Acids The amino acids that insects must have in their diet (i.e., they cannot synthesize these). They are the same as those required by rats: arginine, histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine. However, some insects benefit from inclusion of so-called nonessential amino acids, which are actually essential for some species.

Estuarine Community A group of organisms inhabiting an estuary (edge/inlet of the sea or juncture of a river and an ocean), as opposed to the open sea (called pelagic).

Ethiopian Realm The zoogeographic region of Africa, though this does not include northernmost Africa, which is more similar to Europe (and considered to be part of the Palearctic realm). The Ethiopian realm is characterized by having antelopes, giraffes, elephants, rhinoceros, gorillas, dogs, and cats.  Zoogeographic Realms

Etiology The study of the causes of disease.

Essential Oils These are terpenes distilled or pressed from plants. They are hydrophobic, and generally aromatic. Many repel insects, and some are insecticidal. In their unrefined state, they often are the basis for folk remedies for repelling insects. Examples include peppermint oil, white cedar oil, red thyme oil, bourbon geranium oil, and linalool.

Estimation A sampling plan that numerically estimates population density or intensity. Commonly used for detailed population dynamic and experimental studies (contrast with classification) The term can also denote the process of calculating various statistical parameters such as variance.  Sampling Arthropods

Eucharitidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

Eucinetidae A family of beetles (order Coleoptera). They commonly are known as plate-thigh beetles.  Beetles

Eucnemidae A family of beetles (order Coleoptera). They commonly are known as false click beetles.  Beetles

Eurasian Spruce Bark Beetle, Ips typographus Linnaeus (Coleoptera: Curculionidae, Scolytinae)

Eucoilidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

Eukaryote An organism with cells containing a membranebound nucleus that reproduces by meiosis. Cells divide by mitosis.

Eulichadid Beetles Members of the family Eulichadidae (order Coleoptera).  Beetles

Eulichadidae A family of beetles (order Coleoptera). They commonly are known as eulichadid beetles.  Beetles

Eulophidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

Eumastacidae A family of grasshoppers (order Orthoptera). They commonly are known as monkey grasshoppers.  Grasshoppers, Katydids and Crickets

Eupelmidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

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Euplantulae Small pad-like structures beneath the tarsal segments.

Eupterotidae A family of moths (order Lepidoptera) also known as giant lappet moths.  Giant Lappet Moths  Butterflies and Moths

Eurasian Spruce Bark Beetle, Ips typographus Linnaeus (Coleoptera: Curculionidae, Scolytinae) Erik Christiansen Norwegian Forest Research Institute, Ås, Norway Among thousands of bark beetle species worldwide, only a handful is able to attack and kill trees on a large scale. One of these is the 8-toothed spruce bark beetle, Ips typographus L., indigenous to the Palaearctic forests and recently introduced into North America (Fig. 50). In Europe, the main host is the Norway spruce, Picea abies (Linnaeus) Karsten; in Eastern Asia, including Japan, the main hosts are spruces of the P. jezoensis group. In unmanaged forests, these beetles play an important ecological role by killing old trees and stands, thus promoting biomass recycling and ecosystem rejuvenation. Foresters who are faced with extensive tree mortality do not, however, welcome this activity: managed forests of Europe have lost hundreds of millions of trees in recurring outbreaks.

Hibernation In the colder areas, the beetles emerging from killed, standing trees most often hibernate in the

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Eurasian Spruce Bark Beetle, Ips typographus Linnaeus (Coleoptera: Curculionidae, Scolytinae)

Breeding

Eurasian Spruce Bark Beetle, Ips typographus Linneaus (Coleoptera: Curculionidae, Scolytinae), Figure 50 Ips typographus adults are 5 to 6 mm long, hairy, and dark brown to black. The tip of each elytron has four teeth.

litter of the forest floor where a good snow cover offers protection. Beetles hatching from grounded stems or logs more often remain under the bark during the winter. In warmer parts of its range, the spruce beetle is more prone to stay in standing trees. The adult beetles in Finland tolerate temperatures down to −30°C, while the larvae will die at temperatures around −15°C. The mortality rate during hibernation is generally not well known.

Voltinism The beetles leave their winter quarters in early spring, but flight only occurs when maximum air temperatures exceed 20°C. In Central Europe where flight may occur as early as mid-April, a new generation of beetles may hatch by midsummer to start a second annual generation. A third generation may be initiated in unusually hot summers. In colder areas such as Fennoscandia, spring flight occurs in May and June and only one generation is produced per year. Here, an occasional second generation that remains in the larval stage at the onset of winter will die in the low temperatures.

During the flight period, the beetles search for a breeding site. Flight distances are highly variable depending on energy reserves and the availability of fresh breeding substrate; i.e., timber with bark, logging debris, windfalls and live trees. Healthy trees have powerful defense mechanisms, but can be overcome when beetle populations reach epidemic levels. In this polygamous species, gallery construction starts with the male excavating a nuptial chamber in the phloem, and is joined by one to four females. After mating, each female excavates a gallery and deposits her eggs singly in little niches as she moves along. Maternal galleries, running in the axial direction of the stem, are about 6–15 cm long, depending on attack density. The males remove frass from the galleries and also guard the entrance holes. Space permitting, a female may lay her full complement of about 100 eggs in one gallery. The 5–10 cm long larval mines start at right angles from the maternal gallery. The phloem, in which the larvae feed, is high in stored energy, and larval densities may exceed 500 galleries per square meter of bark surface. I. typographus often utilizes most of the stem, but shuns the lower 1–1.5 m as well as the top where the bark becomes too thin for gallery construction. In the upper stem, the galleries overlap with those of other bark beetles, particularly the smaller Pityogenes chalcographus (L.), which most often utilizes the thin-barked top section. During an ongoing attack, parent beetles may be induced to re-emerge after a couple of weeks, particularly in warm weather and when crowding occurs. Males dominate among the reemerging beetles. They may re-attack the tree from which they emerged, or fly to adjacent ones. Females are more prone to stay in their original host tree, but may also leave to construct new galleries, giving rise to “sister broods.” Occasionally, a second re-emergence may take place, resulting in a third sister brood. As a consequence,

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Eurasian Spruce Bark Beetle, Ips typographus Linneaus (Coleoptera: Curculionidae, Scolytinae)

Pheromones Govern Beetle Attacks During their initial search for a breeding site, volatile substances emanating from host material guide the beetles. However, upon successfully entering a suitable substrate, a “pioneer” male will emit a chemical bouquet of three volatiles, which act as population aggregation pheromones, summoning both sexes for a joint attack. At a later stage of the attack, two other substances with a repellent effect may be produced. This apparently contributes to the regulation of attack density by inducing latecomers to seek out other sites. The pheromones of the spruce bark beetle were isolated and identified in the 1970s, and have subsequently been used for bait in beetle traps. To some extent, they also attract other scolytids, and also act as kairomones for predators such as clerids.

The Epidemic Threshold At low population levels, the beetles are unable to kill trees with intact defenses, and their breeding is therefore restricted to undefended substrates such as logging debris, windfalls and timber. High standards of forest hygiene may help to maintain this non-epidemic state. However, environmental calamities such as large-scale wind-felling and prolonged drought may upset even the best regime of hygiene (Fig. 51), boosting the beetle population to exceed the “Threshold of Successful Attack.” Above this level, healthy trees can be overwhelmed in a massattack. The threshold is lowered when tree defenses are weakened by prolonged periods of drought, or when tree roots are damaged by strong winds. When Ips typographus attacks a living tree, only two outcomes are possible: the tree is killed

2500 Attacks per Standard Tree

cohorts in different stages of development may occur simultaneously, even in areas with only one annual generation.

2000 1500 1000 500 0

0

5

10 Resistance

15

20

Eurasian Spruce Bark Beetle, Ips typographus Linneaus (Coleoptera: Curculionidae, Scolytinae), Figure 51 Threshold of successful attack on Norway spruce by Ips typographus. Black dots represent killed trees, white dots are surviving trees. A standard tree is 20 cm in diameter at breast height. Resistance is defined by growth efficiency, as measured at breast height, i.e., previous year’s increment of stem cross-sectional area as a percentage of sapwood cross-sectional area. Redrawn by Alan A. Berryman after Mulock and Christiansen, 1986.

and the beetles produce a new generation, or the tree survives and no offspring are generated. In other words: if the number of assailants exceeds the “Threshold of Successful Attack,” the beetles win, if not, they are driven away or die.

Fungal Associates During attack and gallery construction, Ips typographus spreads spores of a variety of microorganisms, among which, species of the fungal family Ophiostomataceae are particularly important. Because concentrations of hyphae often give a bluish stain to the wood, the fungi are referred to as “blue-stain fungi.” When a new generation of beetles emerges, the sticky spores adhere to the body surface. Spores are also ingested by callow adults and carried in their guts. Some blue-stain fungi are capable of growing in fresh bark and

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Eurasian Spruce Bark Beetle, Ips typographus Linneaus (Coleoptera: Curculionidae, Scolytinae)

wood and at least one species, Ceratocystis polonica (Siem.) C. Moreau, may kill healthy trees when artificially inoculated into the bark. Blue-stain fungi do not attack cell walls, but rather utilize the contents of bark and wood parenchyma cells, which are storage organs for starch, sugars and lipids and hence, the primary target for both beetles and fungi.

Host Tree Defense Over the eons, conifers have developed elaborate defense mechanisms to cope with wounding and infection. Thick cork bark, often with abundant stone cells, is an obstacle to invasion. Also inside the living phloem, chemical defenses of both preformed and inducible nature await intruding organisms. An interconnected system of ducts stores constitutive resin, which may repel or immobilize attacking insects. Moreover, the phloem parenchyma cells, a primary energy source for both beetles an fungi, are active in synthesis, storage and modification of phenolics in response to wounding and infection. This renders the phloem inhospitable to intruders. Parenchyma cells may form new periderms including cork layers, thus compartmentalizing the infected area where they release fungistatic substances. Superficial wounds and infections, including aborted beetle attacks, are enveloped and rendered harmless by these reactions. Moreover, the underlying cambium produces numerous traumatic resin ducts in the xylem. Above the “Threshold of Successful Attack,” the host defenses collapse. This critical level is defined by the host tree’s genetic constitution and by the environment surrounding it. Sub-lethal beetle attacks may rise the threshold level thereby inducing local acquired resistance in attacked stems.

Control of Damage By maintaining a high standard of forest hygiene, foresters attempt to keep beetle populations in

a permanent non-epidemic state. Forest hygiene is generally dependent on the removal of potential breeding material. Ideally, no such material should be found in the forest when the beetles fly, and a minimum requirement is that any breeding substrate should be removed from the forest before the next generation emerges. However, even the most painstaking efforts may be in vain when a gale strikes, most often in winter, leaving large numbers of fallen trees. In rugged terrain with no roads, even dedicated managers may not be able to salvage all fallen trees before the onset of the beetles’ flight season. Under such circumstances, downed breeding material may boost propagation, pushing the population across the “Threshold of Successful Attack.” Trap trees and beetle traps may be useful for keeping non-epidemic populations down and for mopping up restricted, local populations of beetles, but in case of a full-fledged epidemic, these measures must be combined with large-scale salvage/sanitation cutting.

References Annila E (1969) Influence of temperature upon the development and voltinism of Ips typographus L. (Coleoptera, Scolytidae). Annales Zoologici Fennici 6:161–208 Bakke A, Frøyen P, Skattebøl L (1977) Field response to a new pheromonal compound isolated from Ips typographus. Naturwissenschaften 64:98 Christiansen E, Bakke A (1988) The spruce bark beetle of Eurasia. In Berryman AA (ed), Dynamics of forest insect populations. Plenum Press, New York, NY, pp 479–503 Horntvedt R, Christiansen E, Solheim H, Wang S (1983) Artificial inoculation with Ips typographus-associated blue-stain fungi can kill healthy Norway spruce trees. Meddelelser fra Norsk institutt for skogforskning 38:1–20 Mulock P, Christiansen E (1986) The threshold of successful attack by Ips typographus on Picea abies: a field experiment. For Ecol Manage 14:125–132 Solheim H (1991) The early stages of fungal invasion in Norway spruce infested by the bark beetle Ips typographus. Can J Bot 70:1–5 Thalenhorst W (1958) Grundzuge der Populationdynamik des grossen Fichtenborkenkafers Ips typographus L. SchrReihe forstl. Fak. University of Gottingen 21:1–126

European Cherry Fruit Fly, Rhagoletis cerasi (L.) (Diptera: Tephritidae)

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European Castor Bean Tick, Ixodes ricinus (Linnaeus) (Acari: Ixodidae) This species transmits several diseases to livestock in Europe and nearby areas  Ticks

European Chafer, Rhizotrogus majalis Razoumowsky (Coleoptera: Scarabaeidae) This species has become an important turfgrass pest in eastern North America.  Turfgrass Insects and their Management

European Cherry Fruit Fly, Rhagoletis cerasi (L.) (Diptera: Tephritidae) Byron Katsoyannos Aristotle University of Thessaloniki, Thessaloniki, Greece The European cherry fruit fly is a univoltine, oligophagous, carpophagous species. Its larvae develop in the pulp of ripening or ripe wild and cultivated sweet (Prunus avium L.) and sour cherries (P. cerasus L.) (Rosaceae) as well as into honeysuckle berries (Lonicera spp. Caprifoliaceae), especially L. xylosteum L. and L. tartarica. L. This insect is native to the temperate West Palearctic Regions, including all European countries where its hosts occur (from southern parts, such as Cyprus, to as far North as Norway and Sweden) as well as in some Asian countries (such as Turkey and Iran). Races of the fly specializing in Prunus or Lonicera spp. may occur, and the existence of geographic races exhibiting unidirectional cytoplasmatic incompatibility has been demonstrated. The adult is about 3–5 mm in body (Fig. 52) length, glossy black in color with characteristic patterned wings and a peculiar yellow scutellum (metathorax). The elongated larva (three instars) is

European Cherry Fruit Fly, Rhagoletis cerasi (L.) (Diptera: Tephritidae), Figure 52 Rhagoletis cerasi female.

typical of cyclorrhaphous Diptera. The last instar is about 5–6 mm long. The pupae are coarctate. The fly overwinters in the pupal stage in the soil beneath its host plants. Adults emerge in spring and their appearance coincides with the presence of fruits suitable for oviposition. A few days after emergence, the males release a volatile sex pheromone to attract virgin females for mating. Adults feed upon plant exudates and honeydews from other insects. Mating occurs when females are about 5–10 days old. Visual stimuli are of predominant importance for host location. The shape, size and color of host fruits are important cues for their location by gravid females. Oviposition takes place into ripening host fruit. Usually only one egg is deposited into each fruit. After oviposition, the female deposits onto the fruit surface a non-volatile, long persisting, host marking pheromone, which discourages further egg laying into already oviposited fruits. Due to this pheromone, which also plays a role in the mating behavior by functioning as a male arrestant, a uniform distribution of eggs among available fruits in achieved and hence an optimal use of the resources available for larval development. The possibility of using natural or synthetic host marking pheromone for control purposes has been assessed with promising results. Adults live about two months under optimal conditions (25°C) and each female lays about

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European Earwig, Forficula auricularia Linnaeus (Dermaptera: Forficulidae)

200–250 eggs in her lifespan. Under field conditions, first instar larvae hatch in about 5–10 days after oviposition and larval development lasts two to three weeks. Developed larvae leave the fruit and drop to the soil where they pupate at a shallow depth. They undergo diapause and most adults emerge in the next spring. However, a small proportion may emerge after two or even three years, thus assuring persistence of the population during years of fruit scarcity or absence. The European cherry fruit fly is the most important pest of cherries in Europe, causing fruit damage that may reach 100% of fruit production. Therefore, control measures are frequently required. Early ripening cherry varieties usually escape infestation. In late-ripening varieties, however, control measures are required frequently. This is usually made using insecticides either in the form of proteinaceous bait sprays or as a cover spray applied three weeks before harvest. Based on the strong attraction of the fly to yellow panels reported, an effective, sticky-coated, 3-dimensional visual trap (the Rebell trap, Fig. 53) has been developed in Switzerland by E.F. Boller and his collaborators. The effectiveness of this trap can be enhanced by adding food attractants such as a dispenser containing ammonium acetate. The Rebell trap is widely used in Europe for adult population monitoring and mass trapping (in non commercial orchards). Intervention thresholds for

European Cherry Fruit Fly, Rhagoletis cerasi (L.) (Diptera: Tephritidae), Figure 53 Rebell visual trap.

late varieties are very low (one to two flies per trap or mere presence of flies).

References Aluja M, Boller EF (1992) Host marking pheromone of Rhagoletis cerasi. Field deployment of synthetic pheromone as a novel cherry fruit fly management strategy. Entomologia Experimentalis et Applicata 65:141–147 Boller EF, Bush GL (1974) Evidence for genetic variation in populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera: Tephritidae) based on physiological parameters and hybridization experiments. Entomologia Experimentalis et Applicata 17:279–273 Katsoyannos BI (1975) Oviposition-deterring, male-arresting, fruit-marking pheromone in Rhagoletis cerasi. Environ Entomol 4:801–807 Katsoyannos BI, Boller EF (1976) First field application of oviposition-deterring marking pheromone of European cherry fruit fly. Environ Entomol 5:151–152 Katsoyannos BI, Papadopoulos NT, Stavridis D (2000) Evaluation of trap types and food attractants for Rhagoletis cerasi (Diptera, Tephritidae). J Econ Entomol 93:1005–1010 Prokopy RJ (1969) Visual responses of European cherry fruit flies, Rhagoletis cerasi L. (Diptera, Trypetidae). Bull P Entomol Soc 39:539–566

European Earwig, Forficula auricularia Linnaeus (Dermaptera: Forficulidae) John L. Capinera University of Florida, Gainesville, FL, USA European earwig is native to Europe, western Asia, and northern Africa, but also has been introduced to Australia, New Zealand, and North America. Once introduced, it can spread very rapidly. For example, European earwig was first observed in North America at Seattle, Washington, in 1907. It spread quickly across the United States, being discovered in Rhode Island in 1911, New York in 1912, and most other provinces of Canada and northern states in the USA in the 1930s and 1940s. Presently it occurs south to North Carolina, Arizona and southern California, but due to its


preference for temperate climates it is unlikely to become abundant in the southeastern states. Also, it is not very tolerant of arid environments, but survives where irrigation is practiced.

Life History One generation is completed annually, and overwintering occurs in the adult stage. In British Columbia, Canada, eggs are deposited in late winter, hatch in May, and nymphs attain the adult stage in August. The overwintering females may also produce an additional brood; these eggs hatch in June and also mature by the end of August. In Washington, USA, these events occur about one month earlier. In colder climates such as Quebec, Canada, only a single brood of eggs is produced. The egg is pearly white, and oval to elliptical. The egg measures 1.13 mm long and 0.85 mm wide when first deposited, but absorbs water, swells, and nearly doubles in volume before hatching. Eggs are deposited in a cell in the soil, in a single cluster, usually within 5 cm of the surface. Mean number of eggs per cluster is reported to range from 30 to 60 eggs in the first cluster. The second cluster, if produced, contains only half as many eggs. Duration of the egg stage under winter field conditions in British Columbia averages 72.8 days (range 56–85 days). The second or spring brood of eggs requires only 20 days to hatch. Eggs are attended by the female, which frequently moves the eggs around the cell, and apparently keeps mold from developing on the eggs. Females guard their eggs from other earwigs, and fight with any intruders. The nymphal stages, which are four in number, have the same general form as adults except that the wings increase in size with maturity. The body color darkens, gradually changing from grayish brown to dark brown, as the nymph matures. The legs are pale throughout. The wing pads are first evident in the fourth instar. Mean head capsule width is 0.91, 1.14, 1.5, and 1.9 mm in instars 1–4, respectively. Mean body length is 4.2, 6.0, 9.0, and 9–11 mm, respectively. The number of antennal

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segments is 8, 10, 11, and 12 in instars one to four. Mean duration (range) of instars under laboratory temperatures of 15–21°C is 12.0 (11–15), 10.2 (8–14), 11.2 (9–15), and 16.2 (14–19) days for instars one to four. However, development time is considerably longer under field conditions, requiring 18–24, 14–21, 15–20, and about 21 days for the corresponding instars. Young nymphs are guarded by the mother earwig, which remains in or near the cell where the eggs are deposited until the nymph’s second instar is attained. The adult normally measures 13–14 mm in length, exclusive of the pincher-like cerci (forceps), though some individuals (Fig. 54) are markedly smaller. The head measures about 2.2 mm in width. Adults, including the legs, are dark brown or reddish brown in color, though paler ventrally. The antennae have 14 segments. The pronounced cerci are the most distinctive feature of earwigs; in the male the cerci are strongly curved whereas in the female they curve only slightly. Despite the appearance of being wingless, adults bear long hind wings folded beneath the abbreviated forewings. When ready to fly, adults usually climb and take off from an elevated object. The hind wings are opened

European Earwig, Forficula auricularia Linnaeus (Dermaptera: Forficulidae), Figure 54 Adult male of European earwig, Forficula auricularia Linnaeus.

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and closed quickly, so it is difficult to observe the wings. Adults bear a set of cerci at the tip of the abdomen. Adults can use the cerci in defense, twisting the abdomen forward over the head or sideways to engage an enemy, often another earwig. Earwigs are nocturnal, spending the day hidden under leaf debris, in cracks and crevices, and in other dark locations. Their nighttime activity is influenced by weather. Stable temperature encourages activity, and activity was favored by higher minimum temperatures but discouraged by higher maximum temperatures. High relative humidity seemed to suppress movement whereas higher wind velocities and greater cloud cover encouraged earwig activity. They produce an aggregation pheromone in their feces that is attractive to both sexes and to nymphs, and release quinones as defensive chemicals from abdominal glands. Social behavior is weakly developed in the European earwig. Males and females mate in late summer or autumn, and then construct a subterranean tunnel (nest) in which they overwinter. The female drives the male from the nest at the time of oviposition. The eggs are manipulated frequently, apparently cleaning them to prevent growth of fungi. She will relocate the eggs in an attempt to provide optimal temperature and humidity for the eggs. Although the female normally keeps the eggs in a pile, as the time for hatching approaches she spreads the eggs in a single layer. After hatching, females continue to guard the nymphs and provide them with food. Food is provided by females carrying objects into the nest, and by regurgitation. Thus, there is parental care, but no cooperative brood care. Several natural enemies are known, including some that were imported from Europe in an attempt to limit the destructive habits of this earwig in North America. Some authors have suggested that the most important natural enemy is the European parasitoid Bigonicheta spinipennis (Meigen) (Diptera: Tachinidae), which has been reported to parasitize 10–50% of the earwigs in British Columbia; others, however, report low

incidence of parasitism. Another fly, Ocytata pallipes (Fallen) (Diptera: Tachinidae) also was successfully established, but causes little mortality. Under the cool, wet conditions of Oregon, Washington, and British Columbia, the fungi Erynia forficulae and Metarhizium anisopliae also infect earwigs. The nematode Mermis nigrescens appears to be an important mortality factor in Ontario, where 10–63% of earwigs were infected during a 2-year period; however, this nematode has not been reported from earwigs elsewhere. Avian predation can be significant.

Damage This insect is omnivorous, feeding on a wide variety of plant and animal matter. Although its predatory habits do offset its phytophagous behavior to some degree, on occasion European earwig can inflict significant injury to vegetables, fruit, and flowers. Bean, beet, cabbage, celery, chard, cauliflower, cucumber, lettuce, pea, potato, rhubarb, and tomato are among the vegetable crops sometimes injured. Seedlings and plants providing the earwigs with good shelter, such as the heads of cauliflower, the stem bases of chard, and the ears of corn, are particularly likely to be eaten, and also to be contaminated with fecal material. Among the flowers most often injured are dahlia, carnation, pinks, sweet william, and zinnia. Ripe fruit such as apple, apricot, peach, plum, pear, and strawberry are sometimes reported to be damaged. European earwig is reported to consume aphids, caterpillar pupae, scale insects, spiders, and springtails as well as vegetable matter. Aphid consumption is especially frequent and well documented. In addition to the higher plants mentioned above, earwigs consume algae and fungi, and often consume vegetable and animal matter in equal proportions. The economic status of earwigs is subject to dispute. Undoubtedly earwigs sometimes damage vegetable and flower crops, both by leaf consumption and fruit injury. Foliage injury is usually in

European Corn Borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae)

the form of numerous small holes. Tender foliage may be completely devoured except for major veins. However, the physical presence of earwigs as crop contaminants is perhaps even more important, because most people find their presence and odor to be repulsive. The annoyance associated with their presence is exacerbated by the tendency of earwigs to aggregate, often in association with human habitations; most people simply find them to be annoying. Their propensity to consume other insects, particularly aphids, is an important element in offsetting their reputation as a crop pest. However, augmenting the earwig population by field release, and providing them with additional shelter to enhance survival, have had mixed success in suppressing aphid populations.

Management Population monitoring can be accomplished with baits and traps. Small piles of baits distributed in dense vegetation often attract large numbers of earwigs, which can be checked during the evening. Wheat bran or oatmeal can serve as bait. Traps take advantage of the natural tendency of earwigs to hide in crevices and dark spots, and can be used to detect presence of earwigs, and to estimate abundance. Residual foliar insecticides and baits containing toxicants can be used to suppress earwigs. Of numerous baits evaluated, wheat bran flakes plus toxicant and a small amount of fish oil is reported to be optimal. However, others have suggested that fish oil is unnecessary but suggested addition of glycerin and molasses. Commercial products are rarely formulated specifically for earwigs because they rarely are a severe problem. Rather, products sold for grasshoppers, cutworms, slugs, and sowbugs are applied for earwig control. Bait is most effective if applied in the evening. On residential property or in small gardens, persistent trapping can be used to reduce earwig abundance, though this approach is not likely to be effective if the initial earwig density is high.

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Boards placed on the soil will be attractive to earwigs seeking shelter. Even more earwigs will accumulate if there are narrow grooves or channels in the board. Moistened, rolled-up newspaper placed in the garden in the evening and disposed of in the morning makes a convenient earwig trap for home gardens. A particularly effective technique is to fill a flower pot with wood shavings and invert the pot over a short stake that has been driven into the soil. Traps can also be placed in trees because earwigs favor this habitat.  Vegetable Pests and their Management  Earwigs (Dermaptera)

References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, 729 pp Crumb SE, Eide PM, Bonn AE (1941) The European earwig. USDA Tech Bull 766, 76 pp

European Corn Borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae) John L. Capinera University of Florida, Gainesville, FL, USA European corn borer is native to Europe, where it is widespread. It also occurs in northern Africa. In neither area is it a serious pest. However, it gained access to North America near Boston, Massachusetts, in 1917 where it quickly became troublesome. European corn borer quickly spread to the Great Lakes region. By 1948 it was established throughout the midwestern corn-growing region and eastern Canada. It now has spread as far west as the Rocky Mountains in both Canada and the United States, and south to the Gulf Coast states. The North American European corn borer population is thought to have resulted from multiple introductions from more than one area of Europe. Thus, there are at least two, and possibly more, strains

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present. The presence of an eastern or New York strain, and a mid western or Iowa strain, is evident because different pheromone blends are required to capture moths from each population. Both strains sometimes occur in the same area.

Host Plants European corn borer has a very wide host range, attacking practically all herbaceous plants with a stem large enough for the larvae to enter. However, the eastern strain accounts for most of the wide host range, with the western strain feeding primarily on corn. Crops other than corn tend to be infested if they are abundant before corn is available, or late in the season when senescent corn becomes unattractive for oviposition; snap and lima beans, pepper, and potato are especially damaged. In North Carolina, for example, potato is more attractive than corn at peak emergence of the first moth flight, and more heavily damaged. Other crops sometimes attacked include buckwheat, grain corn, hop, oat, millet, and soybean, and such flowers as aster, cosmos, dahlia, gladiolus, hollyhock, and zinnia. Corn is the most preferred host, but many thick-stemmed weeds and grasses also will support European corn borer, especially if they are growing amongst, or adjacent to, corn. Some of the common weeds infested include barnyardgrass, Echinochoa crusgalli; beggarticks, Bidens spp.; cocklebur, Xanthium spp.; dock, Rumex spp.; jimsonweed, Datura spp.; panic grass, Panicum spp.; pigweed, Amaranthus spp.; smartweed, Polygonum spp.; and others.

Natural Enemies Native predators and parasites exert some effect on European corn borer populations, but imported parasitoids seem to be more important. Native parasitoids include Bracon caulicola (Gahan), B. gelechiae Ashmead, B. mellitor Say, Chelonus annulipes Wesmael, Macrocentrus delicatus Cresson, and Meteorus campestris Viereck (all Hymenoptera:

Braconidae); Gambrus ultimus (Cresson), G. bituminosus (Cushman), Itoplectis conquisitor (Say), Campoletis flavicincta (Ashmead), Nepiera oblonga (Viereck), Rubicundiella perturbatrix Heindrich, Vulgichneumon brevicinctor (Say) (all Hymenoptera: Ichneumonidae); Dibrachys carus (Walker) and Eupteromalus tachinae Gahan (both Hymenoptera: Pteromalidae); Syntomosphyrum clisiocampe (Ashmead) (Hymenoptera: Eulophidae); Scambus pterophori (Ashmead) (Hymenoptera: Hybrizontidae); Trichogramma nubilale Ertle and Davis and T. minutum Riley (both Hymenoptera: Trichogrammatidae); and Archytas marmoratus (Townsend) and Lixophaga sp. (both Diptera: Tachinidae). Although many species of native parasitoids are known, native parasitoids rarely cause high levels of corn borer mortality. Exotic parasitoids numbering about 24 species have been imported and released to augment native parasitoids. About six species have successfully established. Among the potentially important species is Lydella thompsoni Herting (Diptera: Tachinidae), which may kill up to 30% of second generation borers in some areas, but has disappeared or gone into periods of low abundance in other areas. Other exotic parasitoids that sometimes account for more than trivial levels of parasitism are Eriborus terebrans Gravenhorst (Hymenoptera: Ichneumonidae), Simpiesis viridula (Hymenoptera: Eulophidae), and Macrocentris grandii Goidanich (Hymenoptera: Braconidae). Avian predators such as downy woodpecker, Dendrocopos pubescent (Linnaeus); hairy woodpecker, D. villosus (Linnaeus); and yellow shafted flicker, Colaptes auratus (Linnaeus) have been known to eliminate 20–30% of overwintering larvae. Several microbial disease agents are known from corn borer populations. The common fungi Beauveria bassiana and Metarhizium anisopliae are sometimes observed, especially in overwintering larvae. The most important pathogen seems to be the microsporidian Nosema pyrausta, which often attains 30% infection of larvae and sometimes 80–95% infection. It creates chronic, debilitating infections that reduce longevity and fecundity of


adults, and reduces survival of larvae that are under environmental. Unfortunately, N. pyrausta also infects the parasitoid M. grandii. Life table studies conducted on corn borer populations in Quebec with a single annual generation perhaps provide insight into the relative importance of mortality factors. These workers demonstrated that egg mortality (about 15%) was low, stable and due mostly to predators and parasites. Similarly, mortality of young larvae, due principally to dispersal, dislodgement, and plant resistance to feeding was fairly low (about 15%) but more variable. Mortality of large larvae during the autumn (about 22%) and following spring (about 42%) was due to a number of factors including frost, disease and parasitoids, but parasitism levels were low. Pupal mortality (about 10%) was low and stable among generations. The factor that best accounted for population trends was survival of adults. Dispersal of moths and disruption of moth emergence by heavy rainfall are thought to account for high and variable mortality (68–98%, with a mean of 95%), which largely determines population size of the subsequent generation. Overall generation mortality levels were high, averaging 98.7%.

Life Cycle and Description The number of generations varies from 1 to 4, with only one generation occurring in northern New England and Minnesota and in northern areas of Canada, three to four generations in Virginia and other southern locations, and usually two generations in the northern United States and southern Canada. In many areas generation number varies depending on weather, and there is considerable adaptation for local climate conditions even within strains. For example, although the developmental rates of single-generation strains are lower than multiple-generation strains, at northern locations such as Prince Edward Island the single-generation strain develops quickly. European corn borer overwinters in the larval stage, with pupation and

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emergence of adults in early spring. Diapause apparently is induced by exposure of last instar larvae to long days, but there also is a genetic component. Moth flights and oviposition usually occur during June to July, and August to September, in areas with one to two generations annually. In southern locations with three generations, moth flights and oviposition typically occur in May, late June, and August. In locations with four generations, adults are active in April, June, July, and August-September.

Egg Eggs are deposited in irregular clusters of about 15–20. The eggs are oval, flattened, and creamy white in color, usually with an iridescent appearance. The eggs darken to beige or orangeish tan. Eggs normally are deposited on the underside of leaves, and overlap like shingles on a roof or fish scales. Eggs measure about 1.0 mm in length and 0.75 m in width. The developmental threshold for eggs is about 15°C. Eggs hatch in four to nine days.

Larva Larvae are light brown or pinkish gray in color dorsally, with a brown to black head capsule and a yellowish brown thoracic plate. The body is marked with round dark spots on each body segment. The developmental threshold for larvae is about 11°C. Larvae normally display six instars, but four to seven instars have been observed. Head capsule widths are about 0.30, 0.46, 0.68, 1.03, 1.66, and 2.19 mm in instars one to six, respectively. For populations with only five instars, mean head capsule widths are 0.29, 0.44, 0.80, 1.27, and 2.00 mm, respectively. Young larvae tend to feed initially within the whorl, especially on the tassel. When the tassel emerges from the whorl, larvae disperse downward where they burrow into the stalk and the ear. Mortality tends to be high during the first

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few days of life, but once larvae establish a feeding site within the plant survival rates improve. Larvae in the final instar overwinter within a tunnel in the stalk of corn, or in the stem of another suitable host. Duration of the instars varies with temperature. Under field conditions in New York, development time was estimated at 9.0, 7.8, 6.0, 8.8, 8.5, and 12.3 days for instars one to six, respectively, for a mean total development period of about 50 days. In contrast, during the next year development time at the same site was 4.4, 4.3, 4.6, 5.8, 8.5 and 9.0 days for the six instars, for a mean total larval development period of about 35 days.

European Corn Borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), Figure 55 Adult male of European corn borer, Ostrinia nubilalis.

Pupa Pupae usually occur in April or May, and then later in the year if more than one generation occurs. The pupa is yellowish brown in color. The pupa measures 13–14 mm in length and 2–2.5 mm in width in males and 16–17 mm in length and 3.5–4 mm in width in females. The tip of the abdomen bears five to eight recurved spines that are used to anchor the pupa to its cocoon. The pupa is ordinarily, but not always, enveloped in a thin cocoon formed within the larval tunnel. Duration of the pupal stage under field conditions is usually about 12 days. The developmental threshold for pupae is about 13°C.

Adult The moths are fairly small, with males measuring 20–26 mm in wingspan, and females 25–34 mm. Female moths (Fig. 56) are pale yellow to light brown in color, with both the forewing and hind wing crossed by dark zigzag lines and bearing pale, often yellowish, patches. The male (Fig. 55) is darker in color, usually pale brown or grayish brown, but also with dark zigzag lines and yellowish patches. Secondary host plants and adjacent grassy areas play a significant role in the mating behavior of adults, as adults rest and mating takes place in such areas of dense vegetation, called “action sites.” Retention of

European Corn Borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), Figure 56 Adult female of European corn borer, Ostrinia nubilalis.

droplets from rainfall and dew in this dense vegetation stimulates the sexual activity of females. Moths are most active during the first 3–5 h of darkness. The sex pheromone has been identified as 11-tetradecenyl acetate, but eastern and western strains differ in production of Z and E isomers. The western strain produces a blend that approximates 97:3 Z:E, whereas the eastern strain uses a blend of 3:97 Z:E. The preoviposition period averages about 3.5 days. Duration of oviposition is about 14 days, with oviposition averaging 20–50 eggs per day. The female often deposits 400–600 eggs during her life span, though there are also estimates of mean fecundity of about 150 eggs in some locations. Total adult longevity is normally 18–24 days.


Damage

Management

This is a very serious pest of both sweet corn and grain corn, and before the availability of modern insecticides this insect caused very marked reductions in corn production. Young larvae feed on tassels, whorl and leaf sheath tissue; they also mine midribs and eat pollen that collects behind the leaf sheath. Sometimes they feed on silk, kernels, and cobs, or enter the stalk. Older larvae tend to burrow into the stalk and sometimes the base of the corn ear, or into the ear cob or kernels. Feeding by older larvae is usually considered to be most damaging, but tunneling by even young larvae can result in broken tassels. The presence of one to two larvae within a corn stalk is tolerable, but the presence of any larvae within the ear of sweet corn is considered intolerable by commercial growers, and is their major concern. European corn borer is considered to be the most important sweet corn pest in northern production areas of North America, and second-generation borers are the principal source of ear damage. Heavily tunneled stalks of grain corn suffer from lodging, reducing the capacity for machine harvesting. Lodging is not a serious threat to sweet corn. Boring by corn borers also allows several fungi to affect corn plants. In crops other than corn, the pattern of damage is variable. European corn borer larvae damage both the stem and fruit of beans, pepper, and cowpea. The temporal occurrence of fruit affects susceptibility to injury, of course; in Wisconsin, snap beans 14–30 days from harvest were susceptible to damage by larvae, but young plants and fruit near harvest suffered little damage. In celery, potato, rhubarb, Swiss chard, and tomato, it is usually the stem tissue that is damaged. In beet, spinach, and rhubarb, leaf tissue may be injured. Entry of borers into plant tissue facilitates entry of plant pathogens. The incidence of potato blackleg caused by the bacterium Erwinia carotovora atroseptica, for example, is higher in potato fields with stems heavily infested by corn borers. Direct damage by corn borers to potato vines, however, results in negligible yield loss.

Sampling

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Moths can be sampled with blacklight and pheromone traps, and catches by these traps are correlated. Pheromone-baited water pan traps seem to be the most efficient method of adult. Trap catches are usually used to initiate intensive in-field scouting for egg masses, as moth catches are only roughly correlated with density. Thermal summations are also highly predictive. Moths seek shelter during the daylight hours in dense grass and weeds near corn fields. Flushing moths from such habitats gives an estimate of population densities. Eggs can be sampled by visual examination, but this is a very time-consuming effort.

Insecticides Liquid formulations of insecticide are commonly applied to protect against damage to sweet corn, particularly from the period of early tassel formation until the corn silks are dry. Recommendations vary from a single application prior to silking, to weekly. Liquid applications are usually made to coincide with egg hatch in an effort to prevent infestation. If corn borers are present in a field, however, the critical treatment time is just before the tassels emerge, or at tassel emergence from the whorl. This plant growth period is significant because the larvae are active at this time and more likely to contact insecticide. A popular alternative to liquid insecticides is the use of granular formulations, which can be dropped into the whorl for effective control of first generation larvae because this is where young larvae tend to congregate. Insecticide is more persistent when applied in a granular formulation.

Cultural practices Destruction of stalks, the overwintering site of larvae, has long been recognized as an important

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element of corn borer management. Disking is not adequate; plowing to a depth of 20 cm is necessary for destruction of larvae. Mowing of stalks close to the soil surface eliminates greater than 75% of larvae, and is especially effective when combined with. Minimum tillage procedures, which leave considerable crop residue on the surface, enhance borer survival. Early planted corn is taller and attractive to ovipositing female moths, so late planting has been recommended, but this is useful mostly in areas with only a single generation per year. If a second generation occurs, such late-planted corn is heavily damaged. Planting border rows of a highly attractive variety of corn to surround a less attractive variety has been investigated in France. The attractive variety, especially if it is an early-flowering cultivar, receives most of the eggs of moths dispersing into the field. If treated with insecticide or destroyed, this border row trap could provide protection for the main corn crop.

Host plant resistance Extensive breeding research has been conducted, and resistance has been incorporated into grain corn, especially against corn borer populations with only a single annual generation. A principal factor in seedling resistance to young larvae is a chemical known as DIMBOA, which functions as a repellent and feeding deterrent. It has proven difficult to incorporate the known resistance factors into sweet corn without degradation of quality. However, some progress has been made in producing commercially acceptable resistant cultivars, especially when host plant resistance is complemented by use of other suppressive tactics such as application of Bacillus thuringiensis.

Biological control Biological control has been attempted repeatedly in sweet corn and other vegetables susceptible to

European corn borer attack. Bacillus thuringiensis products can be as effective as many chemical insecticides, but often prove to be less effective. Most single-factor approaches, with the exception of newer formulations of Bacillus thuringiensis, have proven to be erratic.  Vegetable Pests and their Management

References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, CA, 729 pp Hudon M, LeRoux EJ (1986) Biology and population dynamics of the European corn borer (Ostrinia nubilalis) with special reference to sweet corn in Quebec. I. Systematics, morphology, geographical distribution, host range, economic importance. Phytoprotection 67:39–54 Hudon M, LeRoux EJ (1986) Biology and population dynamics of the European corn borer (Ostrinia nubilalis) with special reference to sweet corn in Quebec. II. Bionomics. Phytoprotection 67:81–92 Hudon M, LeRoux EJ (1986) Biology and population dynamics of the European corn borer (Ostrinia nubilalis) with special reference to sweet corn in Quebec. III. Population dynamics and spatial distribution. Phytoprotection 67:93–115 Hudon M, LeRoux EJ, Harcourt DG (1989) Seventy years of European corn borer (Ostrinia nubilalis) research in North America. In: Russell GE (ed) Agricultural zoology reviews, vol 3. Intercept, Wimborne, Dorset, UK, pp 53–96

European Honey Bee This is Apis mellifera mellifera Linnaeus (Hy menoptera: Apidae), the common honey bee in most parts of the world. The species originated in the tropics of Africa, but the European strain, bred to be docile and an effective producer of honey, was developed in Europe. It is also known as the Italian honey bee. It has been replaced by the African strain (Apis mellifera scutellata) in South and Central America, and is now spreading in North America where it is replacing the European strain.  Honey Bee  Apiculture  African Honey Bee

Eusocial Behavior

European Foulbrood Unlike American foulbrood, European foulbrood is not considered to be a serious disease of honey bees. It is caused by the bacterium Melissococcus pluton, often appearing in the spring and early summer, then dissipating over the summer. It is found throughout the world. This disease affects very young larvae, and prevents the colonies from growing. It is initiated when the larvae feed on contaminated brood food, and by hive robbing. Infected bees are sometimes discarded by the nurse bees, but it is these nurses that also transmit the disease while feeding the larvae. Bacteria overwinter in the hives. The disease is also spread by contaminated equipment. It also tends to affect colonies that lack adequate nutrition. Infected bees are discolored, but lack the distinct ropiness of bees infected with American foulbrood. The presence of a sour odor and damaged or uncapped cells is symptomatic, but does not serve to distinguish European foulbrood from American foulbrood. However, the dead bee larva forms a rubbery scale in the bottom of the cell, unlike the hard scale of American foulbrood. Often beekeepers do not treat European foulbrood, but antibiotics are curative.  Honey Bees  Apiculture

Reference Morse RA and Nowogrodzki R (1990) Honey bee pests, predators and diseases, 2nd ed. Cornell University Press, Ithaca, New York. 474 pp

European Red Mite, Panonychus ulmi (Koch) (Acari: Tetranychidae) This is a foliar pest of fruit trees.  Apple Pests and their Management

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European Sheep Tick, Ixodes ricinus (Linnaeus) (Acari: Ixodidae) This species, also known as European castor bean tick, is a livestock pest in Europe.  Ticks

European Wheat Stem Sawfly  Wheat Pests and their Management

Eurybrachidae A family of bugs (order Hemiptera, suborder Fulgoromorpha). All members of the suborder are referred to as planthoppers.  Bugs

Eurychoromyiidae A family of flies (order Diptera).  Flies

Eurytomidae A family of wasps (order Hymenoptera). They commonly are called seed chalcids.  Wasps, Ants, Bees and Sawflies

Eusocial Behavior Advanced social behavior that entails nest sharing; division of labor including a caste system with sterile worker caste caring for offspring of the reproductive caste; and overlapping generations so that offspring assist parents. The truly social insects displaying eusocial behavior, include the termites, the ants, and some of the highly organized bees and wasps.  Solitary  Subsocial  Communal  Quasisocial

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Eustheniidae

 Semisocial  Parasocial Behavior  Sociality in Insects  Castes

Eustheniidae A family of stoneflies (order Plecoptera).  Stoneflies

Euthyplociidae A family of mayflies (order Ephemeroptera).  Mayflies

Evagination An outward extension or sac-like structure on the outside of a structure; the opposite of invagination.

Evaniidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

Evans, Howard Ensign Howard Evans was born in Hartford, Connecticut, on February 23, 1919. He received M.S. and Ph.D. degrees from Cornell University in 1941 and 1949, respectively, and served in the U.S. army from 1942 to 1945. He was a faculty member of Kansas State University (1949–1952), Cornell University (1952–1960), Harvard University (1960–1973), and Colorado State University (1973–1986). His awards included his appointment at Harvard University

as Alexander Agassiz Professor of Zoology, his appointment at Colorado State University as Distinguished Professor, an award in 1976 of the Daniel Giraud Medal from the National Academy of Sciences for recognition of published work in zoology or paleontology, and his appointment as a fellow of the National Academy of Sciences (1977). His main research was on systematics and behavior of Hymenoptera, especially the families Sphecidae, Pompilidae, and Bethylidae, and he described one family (Scolebythidae), 31 genera, and almost 800 species. He published more than 255 scientific papers, 13 books and some dozens of popular articles. Two of his books, “Wasp farm” (1963) and “Life on a little-known planet” (1968) achieved popular acclaim. He died on July 18, 2002, survived by his wife, Mary Alice, and three children.

Reference Kondratieff BC (2002) Howard Ensign Evans. American Entomologist 48:188–189

Eversible Capable of being turned inside out, everted, or projected outward.

Excitorepellency The tendency of some insecticides to excite insects so that they fly away prior to acquisition of a dose adequate for knockdown. This property is seen especially with DDT and some pyrethroids.

Ex Larva A Latin phrase meaning out of the larva. It is normally encountered mostly on insect labels in museums, and is used to designate specimens that were reared from the larval stage of the host. The similar term “ex ovum” designates specimens reared from host eggs.

Exogenous

Eye-Cap Moths (Lepidoptera: Opostegidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Eye-cap moths, family Opostegidae, are minute moths with a total of 122 known species, and known from all faunal regions but with many from the Australian region. The likely world total is over 175 species. The family, together with Nepticulidae, forms the superfamily Nepticuloidea, in the section Nepticulina of division Monotrysia, in the infraorder Heteroneura. Adults minute to small (3–16 mm wingspan), with head rough-scaled, with very large eye-caps on the antennal bases; haustellum short and naked (unscaled); labial palpi short and drooping and 3-segmented; maxillary palpi 5-segmented and folded. Wing venation is very reduced, with pseudofrenular bristles as the wing coupling. Maculation is generally white with bands or wing tip iridescences, although some species are dark. Adults are diurnally active. The few larvae known are leafminers, but some are stem borers.

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the name suggests, frequent the eyes (also sores and wounds) of mammals, where they feed at secretions. Their persistence makes them a nuisance, and they also have been implicated in the mechanical transmission of some diseases such as pinkeye.  Flies  Veterinary Pests and their Management

Exarate Pupa A pupa in which the appendages are free, and not attached or adhering to the body (contrast with obtect pupa).

Excretion The process of elimination of materials from the body. Excreted materials include metabolites and wastes, excessive and unnecessary nutrients, water, and allelochemicals. The principal organs of excretion are the Malpighian tubules and the hindgut.

References Davis DR (1987) Family Opostegidae. In: Stehr FW Jr (ed) Immature insects, vol 1. Kendall/Hunt Publishing, Dubuque, IA Davis DR (1989) Generic revision of the Opostegidae, with a synoptic catalog of the world’ s species (Lepidoptera: Nepticulidae). Smithson Contrib Zool 478:1–97 Eyer JR (1964) A pictorial key to the North American moths of the family Opostegidae. Journal of the Lepidopterists’ Society 17:237–242 (1963) Puplesis R, Robinson GS (1999) Revision of the Oriental Opostegidae (Lepidoptera) with general comments on phylogeny within the family. Bull Nat Hist Mus, Entomol 68:1–92

Eye Gnats These are Hippelates species (Diptera: Chloropidae) flies. They are found in the New World and as

Exocrine Gland A gland that discharges its products to the outside of the insect (contrast with endocrine gland).

Exocuticle The layer of sclerotized cuticle between the endocuticle and the epicuticle.

Exogenous Originating outside an organism; extrinsic (contrast with endogenous).

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Exogenous DNA

Exogenous DNA DNA from an outside source. In genetic engineering, DNA from one organism is often inserted into another by a variety of methods.

Exopeptidases Protein digesting enzymes that attack small pieces of proteins by cutting off the terminal amino acid.

Exopterygota A division of Insecta in which the wings develop externally during the immature stages. Hemimetabolous insects.  Metamorphosis

Exoskeleton A skeleton on the exterior of the body. The muscles are attached on the interior surfaces. A general term used to describe the hard body covering of insects, as is the term cuticle.

Exotic Organisms that are native of elsewhere. Other terms used to describe this condition are alien and foreign.

Exotoxins Poisonous substances produced by the microbial cell and liberated into the surrounding environment without destruction of the cell.

Exploratory Learning Orientation behavior of social insects as they first leave the nest and become oriented to their surroundings.

Exploratory Trail An odor trail produced continuously by advance workers from a foraging group (contrast with recruitment trail).

Exponential Growth Population growth under ideal circumstances, without limitation. The population size increases at an increasing rate. The curve describing this relationship (number of individuals and time) is J-shaped.

Expression Vector Vectors that are designed to promote the expression of gene inserts. Usually an expression vector has the regulatory sequence of a gene ligated into a plasmid that contains the gene of interest. This gene lacks its own regulatory sequence. The plasmid with this new combination (regulatory sequence + gene) is placed into a host cell such as E. coli or yeast, where the protein product is produced.

Extra-oral Digestion Digestion of food before it is taken into the insect’s body. This is accomplished by injection of hydrolytic enzymes into the food source, and then sucking up the digested products. Some insects continuously reflux the digestive enzymes by continuously re-injecting and sucking up the liquified juices.

Extrafloral Nectary A nectar-producing gland found outside the flower.  Plant Extrafloral Nectaries

Eyes and Vision

Extrinsic Factors Factors outside an organism, such as weather and other organisms. Exogenous elements.

Exuviae The discarded or shed body covering after molting. Sometimes the terms “exuvium” or “exuvia” are used for the singular form, but this is not correct.

Eyes The organs of sight in insects. The principal eyes of insects are (usually) large, multi-faceted “compound eyes.” Auxiliary organs of vision, with much less utility for the insect, are the “simple eyes”; these are more correctly called “ocelli.” Also, there are small, simple eyes found on the side of the head of larvae of holometabolous insects; these are more correctly called stemmata.  Head of Hexapods

Eyes and Vision James L. Nation University of Florida, Gainesville, FL, USA The ultimate source of light on earth is the sun, and both plants and animals evolved physical and biochemical mechanisms to capture light and make responses to its presence or absence. Light causes phototropic movements of leaves and stems and timing of flowering in many plants, and wavelengths in the 600–700 nm range promote photosynthesis. Light often influences sexual reproductive cycles, biological and seasonal rhythms, color changes in the skin, hormone secretion, and various chemical reactions (for

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example, synthesis of vitamin D in the skin of humans) in animals. Even the simplest plant and animal forms have pigments that enable them to respond to light. The electromagnetic radiation from the sun encompasses a wide spectrum from gamma rays and x-rays (200 μm long in the tephritid fruit fly Anastrepha suspensa. The visual pigment, rhodopsin, is contained in the rhabdomere, a special region of retinula cells that is convoluted into thousands of microvilli or microtubules ending blindly near the center of the circle formed by the retinula cells in a single ommatidium. The tubules typically are about 40–120 nm in diameter along all or part of the length of the cell. In D. melanogaster, there are about 60,000 microvilli along the length of each retinula cell, and about 80,000 in each rhabdomere of the American cockroach. A vast surface area is presented by these numerous folds of the cell membrane, and it is in the membrane of these tubules that the molecules of visual pigment, estimated by some researchers to be up to 100 million molecules of rhodopsin per cell, occur. In some insects, the rhabdomeres of retinula cells in an ommatidium touch or fuse at the center of the circle to form a closed or fused rhabdom, as in honeybees, Lepidoptera, and many other insects. In Diptera and Hemiptera the rhabdomeres do not fuse, but face a central hollow cylinder in the ommatidium. When light strikes the visual pigment, the retinula cell undergoes a depolarization. The depolarizing effect of light is in contrast to the polarizing effect that light has upon the receptors in vertebrate eyes. Resting potentials ranging from 25 to 70 mv have been recorded across the membranes of retinula cells. The inside of the cell is negative relative to the outside during resting conditions in the dark. An electroretinogram (ERG) of electrical activity in response to stimuli can be recorded by placing one electrode on or into the eye and the reference electrode somewhere else in the head. An ERG is a summation of potentials from many retinula cells, and possibly of electrical activity within the optic lobe.

better ability to see objects in the environment and to navigate, capture prey, and chase a potential mate in flight. Insect eyes, however, do not even come close to having the acuity and resolving power of human eyes. The principal factors that determine visual acuity of compound eyes include the angle between two adjacent ommatidia, the optical quality of the dioptric structures that focus the light, dimensions of the rhabdom, the light level, and speed of movement across facets of the eye. The small size of facets of the compound eyes severely limits visual acuity, and larger facets increase visual acuity. The diameter of facets in compound eyes of many insects vary over different parts of the eyes. The angle between two adjacent ommatidia (Fig. 61) is one important factor that determines acuity of vision. Dragonflies are among the insects that have the most acute vision, with an

Visual Acuity

Eyes and Vision, Figure 61 The interommatidial angle between two adjacent ommatidia or facets in the compound eye. Smaller values for the angle Δф increase the possibility for greater visual acuity.

Visual acuity is a measure of how well objects can be resolved. Put simply, higher visual acuity means

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Eyes and Vision, Figure 62 A scanning electron micrograph of the left compound eye, and a portion of the right eye, of a male horsefly Tabanus lineola showing the larger facets in front and extending to the top of the eye. Note smaller facets near the lower rim of the eye. Larger facets represent a fovea or area of the compound eyes with greater visual acuity. The eyes from each side of the head meet in males, but not in females (Photo courtesy of Dr. Jerry Butler, University of Florida.)

interommatidial angle as small as 0.24°. Most insects have considerably larger interommatidial angles of several degrees up to tens of degrees. The smaller the interommatidial angle, all other factors being equal, the greater the distance at which objects such as prey, a predator, or the surrounding vegetation can be resolved. The very small nature of the lens in compound eyes severely limits resolving power because of diffraction. A human eye has much greater resolving power than a single facet of a compound eye because it is larger, has a larger opening to let light in, and has a single lens. Compound eyes are excellent motion detectors, but the fast movement of objects over the eyes causes any image to be blurred, just as movement of objects, or of the camera, causes blurring in photographs. Insect compound eyes perform poorly in very dim light, but insects that are active at night or at dusk have special adaptations for vision in dim light. These may include wider facets and wider

rhabdoms that increase sensitivity by up to 1–2 log units. Some insects have variations that provide zones of greater acuity of vision (a “fovea”) in certain parts of the eye than other parts. The fovea refers to the region in the human eye with the greatest density of cones (color and bright light sensitive) where resolution is greatest when the eyes are focused directly on the object. An “acute zone” has evolved in the forward facing, and sometimes upward looking, part of the compound eyes in some fast flying insects, particularly those that capture prey in flight, or chase flying potential mates. An insect in relatively straight line flight has a relatively stationary field of view straight in front, but highly blurred vision at the sides of the eyes as objects in the environment flash across the field of view. Bees, butterflies and some acridid grasshoppers have an acute zone in the front of the compound eyes, and better vertical acuity in a band around the equator of the eye. Male blowflies, drone honeybees, male hoverflies, some tabanid flies, and some other male insects that look for potential mates while flying have an acute zone that probably enables them to see the female better, particularly against the sky as a background. Both sexes of mantids, dragonflies, and robber-flies have higher visual acuity near the forward part of the eye that likely enable them to see and capture prey more effectively. The fast flying dragonfly Anax junius has 28,672 ommatidia per compound eye, with the smallest known interommatidial angles, and they have an acute zone in the dorsal part of the eye with relatively large facets as much as 62 μm across. This gives the dragonfly ability to catch mosquitoes and other small insects in flight. Another insect with good vision is the praying mantis Tenodera australasiae. Facet diameters in the acute visual zone in the front of the eyes measures up to 50 μm across and they have overlapping acute zones in the large binocular looking eyes that enable them to determine distance of a prey object by binocular triangulation. They strike and capture the prey with the prothoracic pair of forelegs.

Eyes and Vision

The Optic Lobe The optic lobes extending out toward the compound eyes are large in those insects with large eyes. These optic lobes are part of the protocerebrum, the dorsal part of the brain. Three large neuropils in the optic lobes are sites of synaptic connections. The largest of the neuropils is the lamina ganglionaris, and it is the first synaptic region for incoming axons from the photoreceptors. There is a great deal of crossing of axons as they pass from the retinula cells to the lamina ganglionaris, so that axons from the same ommatidium do not converge upon a single monopolar interneuron. Additional crossing of axons occurs after synaptic connections in the next two neuropils, so that the signals from the individual ommatidia are not conveyed to the integrative centers of the brain as a direct representation of each ommatidium. Although we cannot know exactly what image an insect sees, it is reasonable to assume that its brain synthesizes the information into some sort of whole rather than seeing 28,672 little images (the number of ommatidia in each compound eye of the dragonfly Anax junius). The large amount of crossing of neural fibers in the optic lobe of insects is not peculiar to insects, but it is a general feature of visual systems in other animals including humans. Its function is not clearly understood, but it would appear to provide a great deal of back-up security if only some parts of either the external eye or brain receiving the input suffer damage.

Ocelli and Stemmata Ocelli and stemmata share some similarities with a single ommatidium in a compound eye. The cuticle covering the ocelli and stemmata acts like a lens, focusing the light. Retinula cells below the cuticlar covering have a rhabdomere region of tubules where the visual pigment occurs. The axons from the retinula cells in an ocellus are gathered into the ocellar nerve that projects into the protocerebrum.

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The evidence suggests that any image formed is focused beneath the layer of retinula cells in an ocellus, and thus probably cannot be transmitted to the brain. Retinula cells show spontaneous electrical activity in the dark, and stimulation by a light beam leads to a more stable and increased transmembrane electrical potential rather than a depolarizing effect as shown by retinula cells in the compound eye. Ocelli likely function to signal light on-off information, intensity of illumination, and possibly in some insects they convey wavelength of stimulating light. The number of retinula cells in an ocellus is variable in different insects; honeybees, for example, have three ocelli and each contains about 800 retinula cells. Stemmata are eyes in the larvae of some holometabolous insects, with one to six occurring on the head of different larvae. Stemmata have an overlying transparent cuticle and a few retinula cells with rhabdomere regions. Some stemmata have a crystalline lens, and some larvae have two separate rhabdoms, a distal one and a proximal one. An image that falls on the rhabdomere surfaces seems likely, but because of so few photosensitive cells, it is probably poorly, if at all, represented in the brain of the larva. Caterpillars frequently move the head from side to side, which may be a behavior that aids them in obtaining a wider field of view with small, multiple stemmata.

The Chemical Cascade Leading to Vision The chromophore in insect eyes is 11-cis-retinal, or in some insects, 11-cis-3-hydroxyretinal. When a photon of light is absorbed by rhodopsin, 11-cisretinal is isomerized to 11-trans-retinal. Contrary to the light absorbing reaction in vertebrate eyes, retinal and opsin do not separate from each other in light-activated insect eyes. Light stimulated rhodopsin in insects is called metarhodopsin, and it is a catalyst that activates a fast cascade of chemical reactions in the retinula cells, resulting

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in generation of a nerve impulse. This signaling pathway is extremely fast, and can be turned on and off, and repeated, many times per second. Measurements in D. melanogaster indicate that it takes only several tens of milliseconds to proceed from light activation of rhodopsin to the generation of a nerve impulse. The fact that portions of the visual cascade involves a number of enzyme reactions means that an initial stimulus is amplified as much as 100–1,000 times, turning a few photons of light into a barrage of nerve impulses to the optic lobe. In vertebrate eyes the 11-trans-retinal must be reconverted through a series of enzymatic steps in the dark part of the eye into 11-cis-retinal, which is combined with opsin to form a new molecule of rhodopsin. In insects, rhodopsin and metarhodopsin are in a dynamic state of equilibrium, and another photon of light can be absorbed by the metarhodopsin/11-trans-retinal complex and become converted into rhodopsin/11-cis-retinal, a process called photoisomerization. Although the anatomical structure of eyes seems to have evolved a number of times independently, the chemistry of vision is nearly the same in all organisms, and thus provides a link between invertebrates and vertebrates.

Color Vision Color vision is the ability to discriminate between two wavelengths of light. Color vision may have existed in some insects since the Devonian period, about 300 million years ago. Many insects probably have color vision, but only a few have been studied enough to be certain. Behavior tests, electrophysiology, and molecular characterization of the visual pigment molecules have been used to characterize color vision. Retinal is held to the opsin in a “pocket” by the ε-amino group of the amino acid lysine in the opsin molecule. The absorption maximum of 11-cis-retinal alone is at 380 nm and it absorbs little light longer than 400 nm. When complexed with opsin, however, the opsin tunes the absorption

from 360 nm to about 640 nm. Certain amino acid substitutions in locations near the binding pocket for the chromophore influence the absorption spectrum as well, and screening pigments in the cells surrounding the circle of retinula cells in some insects seem to be able to alter the spectral sensitivity of rhodopsin. Insects usually have at least three, and sometimes more rhodopsins, each showing a different absorption maximum. All insect orders that have been tested have greensensitive photoreceptor cells, and probably most have UV sensitive rhodopsin, which explains why entomologists can use UV lights to attract many kinds of insects. Most, but not all, insects also seem to have a blue-sensitive rhodopsin, but some appear to have lost the blue sensitive pigment over time. The painted lady butterfly, Vanessa cardui, has one rhodopsin that absorbs light maximally in the UV region at 360 nm, another absorbs in the blue region maximally at about 470 nm, and one is maximally sensitive in the green part of the spectrum at about 530 nm. The nymphalid butterfly Heliconius erato has three rhodopsins, with peak absorptions in the UV range, one in the bluegreen range, and one absorbing maximally at long wavelengths between 590 and 640. Although the butterfly has only one rhodopsin for absorption in the red region, it has been shown experimentally that the butterfly can discriminate colored light at 590 nm, 620 nm, and 640 nm. This means it can distinguish yellow-orange from orange from orange-red with only one rhodospin, which would not be expected to give this ability to discriminate shades of red; Vanessa atalanta, another lady butterfly, can distinguish red color from green and blue, but cannot distinguish the differences in the red part of the spectrum as can H. erato. The Japanese yellow swallowtail butterfly, Papilio xuthus, has receptor cells in which rhodopsins are present that absorb maximally in the UV at 360 nm, violet range at 400 nm (sensitivity to violet color may be because the receptor pigment is being tuned by filtering pigments; a rhodopsin with a spectral peak at 400 nm is not common in insects), blue range at 460 nm, green range at 520 nm,

Eyes and Vision

CH3

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Eyes and Vision, Figure 63 Chemical structure of 11-cis-retinal (above) and 11-cis-3-hydroxy retinal (below). When combined with the protein opsin, the visual pigment rhodopsin is formed.

and red range at 600 nm. The butterflies were trained by Japanese workers to feed on sugar water from dishes placed on colored discs of paper in the laboratory. The butterflies most easily learned to look for food on red and yellow colors, but training to other colors required more training time, and they lost the ability to distinguish blue when the intensity of the color was reduced to 80% of the training intensity (intensity was reduced by placing neutral density filters over the color). Another swallowtail, Papilio glaucus, has rhodopsins with maximal absorption at approximately the same maxima as P. xuthus, except it does not have one absorbing in the violet range at 400 nm. Most moths are not sensitive to red. Sensitivity may not be very important in dim light because it cannot be distinguished from black; humans lose the ability to distinguish most colors in dim light because the cone cells in the retina that contain the rhodopsins sensitive to color do not work well

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in dim light. The tobacco hornworm, Manduca sexta, has UV, blue, and green receptors, but no red receptor. Honeybees have color vision and were one of the first insects in which perception of color was demonstrated with behavioral tests. The German scientist and behaviorist Karl von Frisch (who received the Nobel prize for this and subsequent behavioral work with bees) trained honeybees to come to sugar water in a small dish placed on a sheet of blue paper lying on a table outdoors. After the bees had communicated the location to others in their hive (by the bee dance) and had recruited a regular stream of visitors to the dish, von Frisch replaced the blue paper with a clean one and an empty dish (the bees might have left an odor on the previous paper after alighting on it many times, and they might somehow smell the sugar solution or have added some olfactory cue to it by their feeding). He also made a checkerboard arrangement around the blue paper with gray papers of the same size as the blue one and graded in intensity from white to black. Each paper contained an empty dish. Von Frisch reasoned that color blind bees would confuse the blue paper with one or more of the gray papers, and probably would alight on the wrong dish or paper in their search for sugar solution. They were not confused, however, but flew directly to the dish (now without sugar water) on the blue paper. He performed many variations of this experiment, and found that the bees could be trained to come to sugar water on some other colored papers, but they could not distinguish red from black or dark gray colored papers. Subsequent work including electrophysiological analysis of the spectral sensitivity of the honeybee compound eye demonstrated that they have receptors that show maximum sensitivity at 344 nm (UV), 436 nm (blue), and 544 nm (green). They do not have a red-sensitive receptor, which explains why von Frisch could not train them to discriminate red papers containing sugar water. Evolution of red receptors in insects has been relatively recent, and sporadic with respect to which groups have red receptors. Red receptors

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evolved at least four times in Lepidoptera, but some Lepidoptera may have subsequently lost the red receptor. Duplications of the green sensitive opsin, and occasional substitution of amino acids at crucial sites in some of the duplicates, probably led to the evolution of a red-sensitive rhodopsin in some insects. Visual stimuli have been shown to be important to insects in various behavioral experiments. In flight tunnel tests, M. sexta moths responded best by flying up wind when visual cues (a white paper flower) were presented with an olfactory stimulus (oil of bergamot, a known attractant for the moths). When the two stimuli were presented spatially or temporally separate from each other, the moths showed a response to both, but less than to both presented together. The authors of the study concluded that the visual stimulus was the ultimate indicator of a nectar (food) source. The pine weevil, Hylobius abietis, when seeking an oviposition site, also showed the best (walking) response when a visual stimulus (a green wire with green plastic twigs to simulate a young pine seedling) was presented with pine odor. The response to the two together was additive, with reduced response to either stimulus presented alone. Attraction to the visual stimulus alone was clearly demonstrated, however.

Detection of Plane Polarized Light by Insects Many invertebrates are able to detect plane polarized light, but humans can only detect it with instruments, not with their eyes. Most of the light from the sun is not polarized, and the waves vibrate in every conceivable direction, but a small percentage of the light becomes polarized by molecules and particles in the atmosphere. Light reflected from waxy and shiny surfaces, such as leaves, or other objects in the environment, also has a polarized component. Polarized waves vibrate in a specific plane, and the e-vector (vibration plane) and intensity of polarization vary with

the position of the sun above the horizon, and consequently they change constantly. It is remarkable that so many invertebrates have evolved the ability to detect the plane of polarization, and some, such as honeybees, use a celestial (sun) clock to track both time and plane of polarization. When honeybees fly out from the hive to collect nectar, they often wander from site to site and spend considerable time away from the hive. The plane of polarization and the position of the sun above the horizon will have changed since their outbound flight, and they cannot find the hive again by following the old data from the outward flight. They update the data and fly back in the socalled “bee line” dictated by the new position of the sun and new plane of polarization. Houseflies, Photurus pennsylvanicus, fireflies, Japanese beetles, and several species of ants orient to plane polarized light under conditions that prevent them from using background reflections as orientation cues, but whether they use it in a sophisticated manner as do honeybees has not been demonstrated. Another insect that uses celestial navigation and polarization for homing after foraging is the ant Cataglyphis bicolor, which is found in North African deserts. It uses plane-polarized light to travel a direct path to its nest in the ground after having wandered, with many turns, up to 100 m in search of food. In most, if not all cases observed, it is the UV sensitive photoreceptor cells in the dorsal rim area of the compound eyes that seem to most often be the cells that detect the plane of polarization. When a UV absorbing shield was held over ants in the field, they began to wander aimlessly, unable to locate their underground nest. The red wood ant, Formica polyctena, of northern Europe uses polarized light as a compass. The precise way in which these insects determine the plane of polarization and how they measure time lapse is not known with certainty. The desert locust, Schistocerca gregaria, responds to polarized light, especially with two identified neurons named Tutu1 and LoTu1. These neurons respond to both polarized and ordinary light, and their response to plane polarized light is based on

Eyes and Vision

blue-sensitive photoreceptors in the dorsal rim area of the compound eyes. The LoTu1 neurons showed approximately two log units greater sensitivity to polarized light than to nonpolarized light. In what ways other than homing could polarized light be useful to invertebrates? Desert locusts, for example, do not show homing behavior, but they might use polarized light during migrations, and reflected polarized light from plant food sources may be processed by the polarization receptors. The red swamp crayfish (not an insect of course), is sensitive to plane polarized light in behavioral tests. How the crayfish might benefit from detecting polarized light is not clear from experiments, but they may be able to detect transparent prey by the reflection of polarized light from their bodies, and may detect predator fish by reflection of polarized light from their silvery scales. Their compound eyes are similar to the compound eyes in insects, and the dorsal rim area of the eyes appears to be a site for detection of plane polarized light. Monarch butterflies use a time-compensated sun compass during long migratory flights to Mexico, but behavioral experiments in a flight simulator that allowed the butterflies to take off in flight when exposed to patch of naturally polarized light from the sky, to artificial polarizers, or to the open sky did not indicate that the plane of polarization made any difference in their orientation. When the dorsal rim area of the compound eyes was painted with black paint, they still used their time-compensated sun compass in orientation, but presumably could not detect the plane of polarization. The authors of these experiments concluded that the butterflies do not need polarized light cues to orient in their flight, but the ability to detect the e-vector of polarization might still be useful in some ecological way that these experiments did not probe. Neotropical butterflies (family Nymphalidae) in Costa Rican tropical forests appear to use polarized light reflected from the shiny surfaces of leaves and the surface of insects to detect forage and oviposition sites, and to identify conspecifics in the

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low light intensity of the forest foliage. Polarized light may be useful in motion detection, particularly in dim light. Mayflies (order Ephemeroptera) probably use reflected polarized light to identify water surfaces where they can lay their eggs. Unfortunately, they also can be fooled into laying them in the wrong place; mayflies in one location were discovered laying masses of eggs on asphalt road surfaces near the stream from which they emerged. Measurements with instruments designed to measure polarized light indicated that the asphalt surface with the sun shining on it reflected plane polarized light in much the same way that the sunlit water surface in their stream did. Thus, some mayflies were laying their eggs in an environment where they had no chance to hatch. The dung beetle Scarabaeus zambesianus forages for fresh animal dung around sunset, a time when light intensity is low and the polarization pattern in the sky is the simplest of the day, with light of the entire sky polarized in one direction. When the beetles locate fresh dung, they quickly make a ball and roll it away in a straight line, apparently an adaptive mechanism to avoid competition and possible predator or parasite detection at the fresh dung. Experiments with polarization filters that change the e-vector of polarization, show that the beetles are sensitive to the e-vector and reorient their rolling behavior in response to an experimental change in the e-vector. The dorsal rim area of the compound eyes has photoreceptor cells with large rhabdom surfaces, a lack of screening pigments in surrounding cells, and the microvilli in the rhabdoms oriented orthogonal to each other (perpendicular to each other), all features providing the best arrangement for detecting the contrast in e-vector of polarized light. The beetles cease foraging about 40–50 min after sunset, when the degree of polarization at the zenith of the sky decreases from 45% to 5% within 15 min. The change in polarization, of course, might not be the sole factor involved in their behavior. In the field cricket Gryllus campestris, photoreceptor cells have orthogonally oriented microvilli in the dorsal rim area of the compound eyes with a blue-sensitive rhodopsin (λmax about 440 nm).

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The cells show strong sensitivity to the e-vector of polarized light, and their input converges on polarization sensitive neurons in the optic lobes of the brain. Inputs from about 200 ommatidia converge upon the optic lobe neurons, which increases the signal-to-noise ratio and sensitivity to the e-vector.

References Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510 Douglas JM, Cronin TW, Chiou T-H, Dominy NJ (2007) Light habitats and the role of polarized iridescence in the

sensory ecology of neotropical nymphalid butterflies (Lepidoptera: Nymphalidae). J Exp Biol 210:788–799 Gilbert C (1994) Form and function of stemmata in larvae of holometabolous insects. Annu Rev Entomol 39:323–349 Kinoshita M, Pfeiffer K, Homberg U (2007) Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria. J Exp Biol 210:1350–1361 Land MF (1997) Visual acuity in insects. Annu Rev Entomol 42:147–177 Wolken JJ (1995) Light detectors, photoreceptors, and imaging systems in nature. Oxford University Press, New York, NY, 259 pp Zaccardi G, Kelber A, Sison-Mangus MP, Briscoe AD (2006) Color discrimination in the red range with only one longwavelength sensitive opsin. J Exp Biol 209:1944–1955

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Fabre, Jean-Henri Casimir Jean-Henri Fabre was born at Saint-Léons, southern France, on December 22, 1823. He received little education in school, and taught himself several subjects as a trainee teacher in Avignon. For this, he received a diploma, and found low-paying jobs as a schoolteacher. He married Marie Villard, another teacher. Now, he devoted his free time to studying insects. This gained him no recognition from his employers, but brought him attention from scientists. He was recognized in Paris, and given a high award: the Légion d’ Honneur medal. Relations with his employers worsened and, in 1870, when he admitted girls to his science classes, he was fired. An English economist, philosopher and friend, John Stuart Mill, lent him money. Royalties from his numerous popular books on scientific subjects, and his teaching of evening classes, allowed him to live with his family, repay Mill, and even buy a small house on a plot of land. In 1879 he retired from teaching, and went to live in that house, and published the first of what became a series of works on entomology, called “Souvenirs entomologiques.” But his wife Marie, who had borne five children, died. “Souvenirs entomologiques,” which eventually ran to 10 volumes, contains careful accounts of insect behavior and life cycles, made from his field observations close to his home, and for that are admirable. At the age of 65, he married MarieJoséphine Daudel, and they had three children. Unfortunately, his books were selling poorly, now because of his antievolutionary viewpoint. Then, in 1909, his fortunes changed. He was “discovered” by

national writers and lauded. He was awarded a government pension, and his books began to sell again. But his second wife died in 1912, and he on October 11, 1915.

References Favret F (1999) Jean-Henri Fabre: his life experiences and predisposition against Darwin. Am Entomol 45:38–48 Teale EW (1949) The insect world of J. Henri Fabre. Dodd, Mead & Co, New York, xvi + 333 pp

Fabricius, Johann Christian Johann Fabricius (Fig. 1) was born in Tondern, Denmark, on January 7, 1745. He obtained his university education in Copenhagen and Uppsala, at the latter being a student of Linné. He worked as a professor at the universities of Copenhagen (1770) and Kiel (1775). These professorships (at both universities) were in natural history, economy and finance, evidencing the philosophy of the times. Whereas Linné had general interests in the description and classification of plants and animals, Fabricius specialized in insects. With this specialization, he described and named almost 10,000 species of insects contrasted with the 3,000 named by Linné. He also developed insect classification substantially; whereas Linné used characters provided by the wings, Fabricius added characters provided by the mouthparts to do this. He wrote several books, developing and expanding his

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“in Hafnia,” but it is an error to say that it was published “in Hafniae.”

References Herman LH (2001) Fabricius, Johann Christian. Bull Am Mus Nat Hist 265:61–62 Tuxen SL (1967) The entomologist J.C. Fabricius. Ann Rev Entomol 9:1–16

Face The front of the head, below the frontal suture (Fig. 2).  Head of Hexapods

Fabricius, Johann Christian, Figure 1 Johann C. Fabricius.

classification of insects. They were (1775) “Systema entomologiae,” (1776) “Genera insectorum,” (1781) “Species insectorum,” (1787) “Mantissa insectorum,” (1792–1799) “Entomologia systematica” and “Supplementum,” (1801) “Systema rhyngotorum” (Hemiptera), (1804) “Systema piezatorum” (Hymenoptera), (1805) “Systema antliatorum” (Diptera), and (1807) “Systema glossatorum” (Lepidoptera, which was never finished). They were written in Latin, which was then the international language of science. The major ones were published in Copenhagen, Kiel, and Leipzig, whose Latinized names are Hafnia, Kilia, and Lipsia. The title pages of the books, following names of the publishing companies, give these Latinized names in the genitive case, Hafniae (meaning “of Copenhagen”), Kiliae, and Lipsiae, a detail that eludes many modern bibliographers. In other words, a book may be said to have been published in Copenhagen (English spelling, used if you are writing in English) or København (Danish spelling, used if you write in a Scandinavian language) or even (if you must be incredibly pedantic this spelling is not wrong)

Face Fly, Musca autumnalis De Geer (Diptera: Muscidae) E. S. Krafsur1, R. D. Moon2 1 Iowa State University, Ames, IA, USA University of Minnesota Saint Paul, MN, USA Face fly, Musca (Eumusca) autumnalis De Geer, is one of only two Musca species recorded in North America, the other being the house fly, M. (Musca) domestica L. Three M. autumnalis subspecies have been described; two occur in Uganda and a third in Somalia (Fig. 3). We doubt their status because of the great distance from other conspecific populations, all of which occupy temperate regions and undergo a facultative reproductive diapause when daylengths approach 12 h. Recent genetic research utilizing mitochondrial nucleotide sequence variation suggests the occurrence of a morphologically indistinguishable sibling species in southeastern Kazakhstan. In gross appearance, face flies look much like house flies but they tend to be larger and are found in different habitats. Eyes of female face flies are more completely holoptic than in house flies, and the male face flies are completely holoptic, unlike house flies. The basal abdominal pleuron of female

Face Fly, Musca autumnalis De Geer (Diptera: Muscidae)

Vertex Frons

F

Flagellum Pedicel Scape

Antenna

Median ocellus

Face Anterior tentorior pit Frontoclypeal suture Clypeolabral suture

Basimandibular sclerite Mandible Clypeus Labrum

Maxillary palpus Maxilla Labial palpus

Face, Figure 2 Front view of the head of an adult grasshopper, showing some major elements.

Face Fly, Musca autumnalis De Geer (Diptera: Muscidae), Figure 3 Old World distribution of Musca autumnalis. The occurrence of a presumptive sibling species to M. autumnalis is indicated by the question mark in Kazakhstan (modified after Krafsur and Moon, Annu. Rev. Entomol. 42).

face flies is yellow, and succeeding pleura are grayblack, whereas the lateral pleura of house fly females more frequently are cream in color. The abdominal pleura of male face flies are bright

yellow against a distinctly black dorsal stripe, a trait not commonly shown by male house flies. Face flies differ greatly from house flies in habits and biology. Face flies are exophagic and

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exophilic, occurring around bison, pastured cattle and horses. They oviposit only in fresh bovine dung where larval development occurs. Only overwintering face flies in diapause may be found in human or livestock dwellings. In contrast, house flies are ubiquitous in and around human and animal habitations and oviposit and develop as larvae in many kinds of fermenting organic matter. The veterinary and economic importance of face flies is related to the feeding habits of females, which seek protein from the eyes, noses and other orifices of cattle and horses. In so doing they can serve as vectors of eyeworms (Thelazia spp.), hemorrhagic bovine filariasis (Parafilaria bovicola), and the agents of “pinkeye” or infectious bovine keratoconjunctivitis (Moraxella bovis). When abundant, face flies annoy cattle and horses and are said to disrupt grazing patterns, but the economic significance of this remains to be demonstrated. Female face flies seek protein to support egg development and they do so in each successive gonotrophic cycle. Thus, the vectorial capacity of a face fly is related to her reproductive age. Sex ratios of adults around hosts are highly biased during the breeding season, from April to mid-September. Male face flies do not seek protein but can be found near animals albeit in much smaller numbers than the females. Males are found in much greater numbers perching at the margins of woods, on fences, and other sunlit surfaces. In these locations females are comparatively few and most are virgins. In very late summer, autumn, winter, and early spring, face flies may also be found on sunlit windows and walls in some human dwellings where diapausing flies are thought to have sought overwintering sites. Here the sexes occur in equal numbers.

Distribution and Colonization of North America Musca autumnalis s.s. is Palearctic, occurring from the British Isles south to northern Africa and east to Pakistan, Kazakhstan, northern India, and Nepal. Face flies colonized North America

only recently. They were first detected in Nova Scotia in 1952, and secondarily recorded in New York in 1953. They rapidly spread through the northern tier of states in North America and southern regions of Canada, to about 53°N and were detected in the Pacific Northwest in 1967, having spread westward at a yearly average rate of c. 250 km per year. Spread southward was much slower. Their current North American distribution extends as far south as about 35°N, including Georgia, Tennessee, Arkansas, Oklahoma, Utah, northern Nevada, and southern California (Fig. 4). Genetic diversities in North American populations are substantial and indicate a large founding population of the order 102–103 or more reproducing females, a conclusion supported by the simultaneous introduction of the entomopathic nematode Paraiotonchium autumnalis (Tylenchida: Allantonematidae) that is found in about 2–4% of adult face flies. North American populations exhibit little genetic differentiation, testifying to their rapid spread from a likely single, genetically diverse population. Old World populations, however, showed much genetic diversity partitioned among English, Russian, and Kazakhstan populations. Mitochondrial sequence variation suggests the origin of New World face flies was the United Kingdom or Western Europe and a likely scenario is that a large cluster or clusters of diapausing flies were introduced via wartime or postwar shipping between the UK and maritime provinces of Canada.

Reproductive Biology Face fly females become inseminated only once. Thereafter, females require exogenous protein to undergo vitellogenesis. Ovaries are paired, and average 12–13 ovarioles each. Hence, mean egg production per clutch is about 25, averaged over the breeding season. Ovarioles develop in synchrony, and flies may undergo repeated cycles of vitellogenesis and oviposition. Ovariole number varies with body size


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Face Fly, Musca autumnalis De Geer (Diptera: Muscidae), Figure 4 North American distribution of Musca autumnalis. The first detections of face flies are indicated. Seasonal numbers of generations are shown, estimated by calculating degree-day sums (modified after Krafsur and Moon, Annu. Rev. Entomol. 42).

and body size varies with the quality of larval nutrition. Late spring and early summer flies tend to be the largest and, therefore, have the most ovarioles. Microscopic examination of female reproductive systems and chemical analysis of their heads provides the means to estimate reproductive ages and phenology. Because ovarian development is temperature dependent, it is possible to estimate, to a rough approximation, the calendar ages of flies in a sample if the temperature history of the sampling location is known. The first ovipositions in spring require about 77 degree-days (DD) above a threshold of 12°C. The previtellogenic phase requires 30 degree-days and vitellogenesis another 47 DD. Subsequent ovipositions require about 40 DD above the 12°C threshold. Calendar ages may be estimated more accurately by measuring spectrofluorometrically the concentration of pteridines in flies’ head capsules. These substances accumulate in the eyes at a rate determined by temperature integrated over time. The

pteridine method, applied to flies in the upper Midwestern states, indicated that during the main breeding season males lived an average of 10 days and females 11 days and completed two to three gonotrophic cycles. Development of eggs, larvae, and pupae also are temperature dependent, requiring 57 DD above a 10°C threshold for egg hatch and larval development and a further 134 DD for pupal development. Thus, egg to adult development requires an average 14 days at summer temperatures. Day degree summations indicate that the number of generations annually varies from about three to four in the northernmost part of the range to 8–12 in the south.

Phenology and Overwintering Face flies overwinter as adults in reproductive diapause. In the field, short day lengths induce reproductive diapause. Both sexes develop

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hypertrophied fat bodies and do not demonstrate sexual behavior. They become increasingly photonegative and seek out hibernaculae, which may include human dwellings. It is unlikely, however, that many of the flies that enter buildings in autumn survive over winter, because they are unable to replace water and easily escape to the outdoors. Moreover, diapausing flies are killed by exposures to –10°C (14°F) for 7 h or longer. In much of their northern temperate range, temperatures often drop below –10°C for many hours to days. Thus, successful overwintering in heated or unheated structures seems unlikely in the northern regions of face fly distribution. It is more plausible that successful face fly overwintering in the cold climates occurs in subnivean environments or below ground where temperature extremes are much more moderate. In late winter and early spring, diapausing flies can be found perching outdoors on sunny days when air temperatures approach 12°C. Spring warmth allows the flies to break diapause and seek mates. Females then obtain proteinacious meals from cattle and horses. Gravid flies oviposit on fresh bovine dung. These overwintered flies have

survived approximately 7–8 months as adults. Larval and pupal development is temperature dependent. First generation flies then appear about a month later and undergo the same mating, feeding, and gonotrophic cycle, giving rise to overlapping generations. Repeated cycles occur until day lengths decline to 12.5 h in September. Then, newly eclosed flies undergo facultatively gonadotrophic dissociation and develop hypertrophied fat body. Annually replicated studies in Iowa have shown that sharp variations in prevailing daily temperatures have no detectable effects on the sudden switch to diapause development.

Veterinary Significance The importance of face flies is related to the feeding habits of females on the eyes of cattle (Fig. 5) and horses. They will also imbibe saliva, blood from wounds, and discarded placenta and fetal membranes (afterbirth). Face flies are obligate developmental vectors of eyeworms Thelazia gulosa, T. scrjabini, and T. lacrymalis. The former two species occur in cattle, whereas the latter species

Face Fly, Musca autumnalis De Geer (Diptera: Muscidae), Figure 5 Face flies clustered around the head of a cow, where they feed on secretions of the eyes and nose.

Factitious

occurs in horses. Adult nematodes reside in the lachrymal ducts of their hosts and shed eggs that develop to infective larvae that develop in the hemocoele of face flies. Third stage larvae migrate to the head of adult flies and depart when flies feed on cattle or horses. The clinical significance of Thelazia spp. is considered to be small. All three species are endemic in the Old World, and have been introduced into North America. In Europe, the face fly is also the developmental host and vector for Parafilaria bovicola (Nematoda: Filaroidea). This nematode, detected in quarantined imported Charolais cattle in Ontario, causes cutaneous bleeding in cattle and lesions in the surfaces of carcasses, thereby reducing their value. Parafilaria bovicola has been recorded in France, Sweden, Eastern Europe, India, Pakistan, the Philippines, North, West and East Africa, and South Africa. Reports in North America of increased pinkeye incidence after the appearance of face flies led to research focused on the causes and transmission of pinkeye, caused largely by the bacterium Moraxella bovis. Converging evidence is that Moraxella does not infect and replicate in face flies. Rather, the flies are readily contaminated with Moraxella from infected animals, and contaminated flies can assist in mechanical spread of the bacterium from infected to susceptible cattle. Similarly, the agent of bovine brucellosis, Brucella abortis, cannot replicate in face flies and ingested bacteria are rapidly degraded. Apart from causing annoyance when populations are dense, face flies do not seem to cause detectably significant economic damage.

Management Extensive studies of ear tags of various formulations for face fly control have been carried out for 25 years. Backrubbers and dustbags charged with various insecticides have also been evaluated. Treatments are usually assessed by comparing visual counts of flies on animals’ faces among treated and untreated herds. No treatment has proved

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particularly efficacious. It is probable that face fly populations were not effectively reduced largely because females spend little time directly on host animals, which minimizes exposure to insecticides on treated animals. The sterile insect technique (SIT) has been considered as a means of eradication. Treatment of puparia containing pharate adults to 21 Gy of ionizing radiation in an anoxic atmosphere induced 95% sterility in both sexes with minimal cost in reduced longevity and competitiveness compared with unirradiated flies. Although a release strategy has been developed, simulation modeling and methods for mass rearing and genetic sexing remain to be developed. The great propensity for dispersal demonstrated by face flies does not favor SIT as an efficacious way of eliminating face flies and the economic benefits of doing so are not likely to justify costs of the rearing, sterilization and release methods currently available.

References Cummings MA, Moon RD, Krafsur ES (2005) North American face flies Old World origins: mitochondrial evidence. Med Vet Entomol 19:48–52 Hall RD (1984) Relationship of the face fly (Diptera: Muscidae) to pinkeye in cattle: a review and synthesis of the relevant literature. J Med Entomol 21:361–365 Krafsur ES, Moon RD (1997) Bionomics of the face fly, Musca autumnalis. Ann Rev Entomol 42:503–523

Facet The external surface of an individual ommatidium on a compound eye.

Factitious An abnormal host for a parasitoid, specifically a non-normal host that biological control prac– titioners use to culture biological control agents in the laboratory because it is more convenient than the natural host.

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Factitious Host

Factitious Host Abnormal host. Insects, and biological control agents of insects or plants, sometimes are produced on abnormal hosts due to ease or economy of culture.

Facultative Agents A term used by Howard and Fiske to describe mortality factors that increase in intensity as population density rises; density-dependent mortality factors.

Facultative Diapause Optional occurrence of diapause (arrested development), brought about by adverse conditions or conditions signifying the onset of adverse conditions. Facultative diapause occurs where adverse conditions do not occur regularly or predictably, or where insects have several generations per year and continue with their life cycle until some trigger stimulates induction of diapause.  Diapause  Obligatory Diapause

Facultative Myiasis Myiasis in which the maggots dwell for some time in the gut or nasal passages of living animals if they are able to gain access.  Myiasis

Facultative Parasitism Optionally a parasite. A condition in which normally free-living organisms may become parasites.

Facultative Predators R. Albajes1, O. Alomar2 1 Universitat de Lleida, Lleida, Catalonia, Spain 2 IRTA, Cabrils, Catalonia, Spain Omnivory, or trophic omnivory, is defined as the capacity of organisms to feed on more than one trophic level. True omnivory is a special case of trophic omnivory in which the consumer feeds on both plants and animal prey. The alternation of prey-feeding and plant-feeding stages during development is relatively common among animals. For example, many predatory insects feed upon plants at the adult stage by consuming floral or extra-floral nectar, pollen, seeds, plant saps and other plant materials, whereas they are carnivorous in juvenile stages. Less frequently, but not rarely, other insect predators may feed on plants and/or on prey at the same developmental stage; these are called facultative predators. The key feature that characterizes facultative predators is their capacity to feed on both plants and prey. Other closely related terms that are sometimes used to describe facultative predators are zoophytophages, phytozoophages, plantfeeding omnivores and opportunistic predators. More recently, omnivory has been structured into three types: life-history, temporal, and permanent omnivory. The differences between these terms come from the prevalent feeding regime observed in each species. Thus, zoophytophages eat mostly prey, but also take vegetable resources. Conversely, in phytozoophages, the diet is mainly composed of plant materials to which prey are added. In practice, however, the relative amount of vegetable and animal consumption has rarely been determined, and the term applied to a species seems to reflect the perception of the observer rather than the real proportion of plant versus prey food ingested. In fact, species that may feed facultatively on both plants and prey are located in a continuum of feeding

Facultative Predators Strict zoophages

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Strict phytophages

1

Zoophytophages

Phytozoophages

Facultative Predators, Figure 6 Trophic continuum of feeding habits by predators according to the relative consumption of animal and plant resources.

habits (Fig. 6) between strict zoophagy and strict phytophagy. Some authors use the term facultative predator to refer to predators that usually have a well-defined diet, but may also consume a broader range of prey. Parasitoids that are able to feed on the host may be regarded as facu ltative predators, as females can switch bet ween predation and parasitism when a host is found.

Insect and Arachnid Groups Containing Facultative Predators It is difficult to review the cases of facultative predation contained in the literature because many references report occasional observations of predators feeding on plants, or of phytophages feeding on animals, but rarely are there more continuous observations on the concurrence of plant and prey feeding at the same developmental stage. However, a list is provided of insect and arachnid groups containing at least one species with facultative predaceous habits (Table 1). Cases of cannibalism, hematophagy and hostfeeding parasitoids have not been considered, whereas the cases of saprophagy are included. The list includes 18 orders and 84 families of mostly insects, but also arachnids. This would mean that facultative predation is more widespread among terrestrial insect predators than might be thought, due to the scarcity of studies on this feeding behavior.

Functions and Role of Facultative Predation To understand functions of the capacity to feed on both plants and prey, it is important first to understand the benefits and costs derived from feeding on plants in facultative predators. At least some of the benefits confer adaptive advantages because a number of facultative predators have retained or acquired morphological (particularly mouth parts), or physiological (amylases, pectinases, symbiotes) traits of herbivores. Consequently, trophic switching capacity may itself constitute an adaptive strategy of some predators living in habitats with high variability in food type abundance. Benefits may derive from nutritional considerations. Facultative predators may obtain complementary or supplementary nutrients, or other substances like vitamins, water, minerals, symbiotes, or enzymes from alternative plant or prey food. As a result of mixing prey and plant diets, facultative predators enhance one, or several, of their fitness components such as developmental rate, survival, fecundity, and longevity. These benefits in some fitness components, however, may be counterbalanced by costs in the decrease of other components as a result of the poorer quality of plant food. Another cost of facultative predation is a narrower range of prey as a consequence of their greater dependence on host plants than nonplant feeding predators (e.g., Orius species avoid foraging on tomato though it hosts suitable prey). The possibility of switching from prey to plant feeding may represent an additional benefit as it

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Facultative Predators

Facultative Predators, Table 1 The known distribution of facultative predation in insects and arachnids Order/Family

Source

Acariformes

Tydeidae

Order/Family

(3)

Parasitiformes

Phytoseiidae

(3)(4)

Araneida

Source

Blattidae

(4)

Mantidae

(4)

Diptera

Tipulidae

(1)

Anyphaenidae

(4)

Ceratopogonidae

(1)

Araneidae

(4)

Empididae

(1)

Coleoptera

Mydaidae

(1)

Anthribidae

(4)

Antohmyiidae

(1)

Anthicidae

(1)

Calliphoridae

(5)

Brentidae

(1)

Muscidae

(5)

Cleridae

(1)

Phoridae

(5)

Endomycidae

(1)

Syrphidae

(3)

Melyridae

(1)

Hemiptera

Colydiidae

(1)

Anthocoridae

(1)

Cantharidae

(4)

Berytidae

(1)

Carabidae

(3)(4)

Lygaeidae

(1)

Cerambycidae

(2)(4)

Mesoveliidae

(1)

Chrysomelidae

(4)

Miridae

(1)

Coccinellidae

(1)(3)(4)

Nabidae

(1)

Curculionidae

(4)

Pentatomidae

Lampyridae

(1)

Phymatidae

(5)

Pedilidae

(1)

Reduviidae

(1)(4)

Pyrochroidae

(1)

Aphidoidae

(2)(4)

Silphidae

(1)

Hymenoptera

Lathridiidae

(1)

Anthophoridae

(2)

Elateridae

(2)(3)(4)

(1)(4)

Chalcidoidea

(4)

Malachiidae

(4)

Eurythomidae

(4)

Staphylinidae

(3)

Vespidae

(1)

Tenebrionidae

(4)

Eumenidae

(1)

Formicidae

(1)

Entomobryidae

(1)

Lepidoptera

Isotomidae

(1)

Arctiidae

(2)(4)

Dermaptera

Geometridae

(2)(4)

Collembola

Carcinophoridae

(3)

Lycaenidae

(4)

Forficulidae

(1)(3)(4)

Noctuidae

(2)(4)

Labiduridae

(3)

Psychidae

(4)

Dictyoptera

Tortricidae

(2)(4)


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Facultative Predators, Table 1 The known distribution of facultative predation in insects and arachnids (Continued) Order/Family

Source

Order/Family

Source

Neuroptera

Psocoptera

Chrysopidae

(1)(3)(4)

Atropidae

(1)

Myrmeleontidae

(1)

Caeciliidae

(1)

Nemopteridae

(1)

Liposcelidae

(1)

Osmylidae

(1)

Thysanoptera

Coniopterygidae

(1)

Aeolothripidae

(3)

Mantispidae

(4)

Phlaeothripidae

(1)

Orthoptera

Thripidae

(3)

Acrididae

(1)(2)(4)

Thysanura

(4)

Gryllidae

(1)(2)(3)(4)

Lepismatidae

(1)

Gryllotalpidae

(4)

Tricoptera

Gryllacrididae

(1)

Limnephilidae

(4)

Pyrgomorphidae

(4)

Zoraptera

(1)

Tettigoniidae

(1)

Sources: (1) Hagen (1987); (2) Whitman et al. (1994); (3) Hagen et al. (1999); (4) Coll and Guershon (2002); (5) Original additions

diminishes competition among predators for prey. Other benefits come from the feature that most facultative predators are generalists and are better adapted to changing and ephemeral habitats. The occurrence of facultative predation in food webs influences various interactions among components of the system. For instance, predator and prey may share a common resource and competition may thus occur (e.g., intraguild predation). Systems with facultative predators differ in four ways from those with strict predators: (i) it is unlikely that the relative sizes of prey and plants have a major effect on the tendency of a plant-feeding omnivore to switch between plant and prey feeding; (ii) unlike animal prey, plants are not usually removed after a feeding event, thus the probability of finding a plant does not change; (iii) the location of plant and prey sources is not independent: plants define the prey’s habitat; and (iv) the chemical properties of plants and prey differ greatly, and their relative nutritional values for the facultative predator are likely to be a major determinate of the proportion of its plant and

prey consumption in the continuum between herbivorous and predaceous habits. Facultative predators may make different and contradictory contributions to the stability of food webs. As they can link species in the community that would otherwise be unconnected, the occurrence of facultative predators may stabilize systems. Their role in shortening food chains may also contribute to stability. The possibility of switching between prey and plant feeding may allow prey populations to escape predation at low density, resulting in a stabilizing mechanism for the prey population. Other stabilizing and destabilizing effects of facultative predators come from their characteristics as generalist predators.

Facultative Predators for Biological Pest Control The potential of facultative predators for biological pest control has traditionally been neglected,

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mainly due to the risk that feeding on the crop may result in economic damage or because predation has been overlooked when compared to plant feeding. However, facultative predators have some advantages for use in biological control, so management programs must minimize their risks and maximize their benefits. Facultative predators have two main advantages for their use in biological control. One is their capacity to establish themselves early in the crop fields and thus prevent pests from building up high populations. This is a particularly positive trait of biocontrol agents in ephemeral crops such as annual crops that have to be recolonized every season. A second advantage of facultative predators concerns their possibility of feeding on plants when prey are at low density, thus preventing predator extinction or migration. Most observations on the role of plant feeding in early predator establishment and persistence on the crop relate to pollen-feeding predators such as many phytoseiid mites or anthocorids and coccinellids. For instance, the establishment and persistence of Orius insidiosus at low prey densities may be due to the ability of the predator to feed on pollen. Similarly, the failure and success of establishing and maintaining O. laevigatus on cucumber and pepper has been attributed to the lack or presence of pollen in the flowers, respectively. However, such behavior has proved to be less evident in non-pollen feeding predators. For instance, the foraging times of adults of the facultative predator Dicyphus tamaninii in cucumber patches of low and high prey density were compared and no differences were found even though this predator spent some time feeding on the plant. The main disadvantage of facultative predators for biological control stems from their capacity to damage crops during plant feeding. Such a risk depends on various factors such as the relative amount of plant vs. prey feeding, the host-plant species and cultivar, the time of plant feeding and crop phenology, and the plant tissue fed on by the predator. Relationships between the amount of plant and prey feeding are a function of the nature

of nutrients derived from plants by facultative predators. When the nutrients derived from the plant are complementary to those obtained in the prey, plant feeding occurs independently of prey feeding, as has been found in Campylomma verbasci, which feeds on apple fruitlets regardless of the availability of prey. When predators switch between plant and prey as alternative sources, the relationship between the two types of feeding will be negative. If prey are preferred to plants, phytophagy will only occur when prey are scarce. This is the case for the mirid bug D. tamaninii, which only feeds on tomato fruit when its main prey, greenhouse whitefly, is not abundant. On the other hand, plant feeding may increase with prey feeding when plants provide an element (e.g., water) that is needed for prey consumption, as noted for D. hesperus. Consequences of plant feeding on pest suppression, and thus success of facultative predators in biological control, are difficult to predict. Positive effects of plant feeding on facultative predator performance do not necessarily lead to enhanced biological control because per capita prey consumption may be reduced by ingestion of plant food. On the other hand, reduced per-capita prey consumption can be balanced by improved numerical response. Further investigations should address relationships between plant feeding, prey consumption and pest suppression. Some facultative predators show clear preferences to feed on some crop species and cultivars, which are thus more exposed to their injury than the less preferred ones. Such is the case for D. tamaninii, which may damage tomato, but rarely French cucumber varieties. Similarly, C. verbasci nymphs injure apples – differently according to the variety – by feeding on the flower parts and fruitlets, whereas injuries are rarely observed on pears. The influence of plant-feeding timing on crop damage can be exemplified by C. verbasci, which causes the greatest damage during the bloom period, whereas little or no damage occurs after the fruit reaches a certain size. Finally, risk of crop damage is determined by the plant tissue that is preferred by the facultative predator. Feeding on

Fairchild, Alexander Graham Bell

pollen or extra floral nectar, for example, will rarely lead to high crop damage, whereas damage will be high if fruit is the plant part preferred by the facultative predator, or moderate or even nil if leaves are preferred. Most facultative predators that have been studied are also generalists regarding prey range. As such, they have traditionally been considered as unable to regulate pests and thus of little use in biological control. This belief, however, is not fully supported by the theory, and is refuted by detailed studies on the role of single species or assemblages of generalist predators. In contraposition with specific natural enemies, generalist predators have positive traits – e.g., quick response to sudden pest population increases, high dispersal capacity, aggregative responses to patched prey distribution, ability to survive at low target-prey density – in essence,for adaptation to changing environments and prey densities, such as those found in ephemeral crops.

Conclusions Facultative predation is defined as a special case of true omnivory in which plant and prey feeding co-occur within the same developmental stage so that individuals may choose between the two types of food. Facultative predation is relatively common among terrestrial predaceous arthropods as it is found in at least 18 orders and 84 families. The functions of zoophytophagy are still poorly understood, but there are many examples of fitness enhancement in the literature when diets mix vegetable and animal resources. The occurrence of facultative predation in food webs influences various interactions among components of the system and its contribution to stability may be contradictory. The role of facultative predation in biological control has been neglected mainly due to the risks of damage to the crop. These are functions of various factors that should be better known in order to develop programs for managing facultative

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predator populations in order to minimize risks and benefit from their advantages as agents of conservation biocontrol. In particular, understanding when facultative predators switch from prey to plant consumption, and how biological control is affected, are of crucial importance.  Predation: The Role of Generalist Predators in Biodiversity and Biological Control

References Albajes R, Alomar O (1999) Use and potentialities of polyphagous predators. In: Albajes R, Gullino ML, van Lenteren JC, Elad Y (eds) Integrated pest and disease management in greenhouse crops. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 265–275 Alomar O, Wiedenmann RN (eds) (1996) Zoophytophagous Heteroptera: implications for life history and integrated pest management. Proceedings of the Thomas Say Publications in Entomology, Lanham, MD, 202 pp Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Ann Rev Entomol 47:267–297 Hagen KS (1987) Nutritional ecology of terrestrial insect predators. In: Slansky F, Rodríguez JG (eds) Nutritional ecology of insects, mites, spiders and related invertebrates. Wiley, New York, NY, pp 533–543 Hagen KS, Mills NJ, Gordh G, McMurtry JA (1999) Terrestrial arthropod predators of insect and mite pests. In: Bellows TS, Fisher TW (eds) Handbook of biological control. Academic Press, San Diego, CA, pp 383–503 Wäckers FL, van Rijn PCJ, Bruin J (eds) (2005) Plant-provided food for carnivorous insects: a protective mutualism and its applications. Cambridge University Press, Cambridge, UK, 356 pp Whitman DW, Blum MS, Slansky F Jr (1994) Carnivory in phytophagous insects. In: Ananthakrishnan TN (ed) Functional dynamics of phytophagous insects. Science Publishers, Lebanon, New Hampshire, pp 161–205

Fairchild, Alexander Graham Bell Alexander Fairchild, known to family and friends as Sandy, was born in Washington, DC, on August 17, 1906. His father, David Fairchild, was a botanist with the U.S. Department of Agriculture, who was interested in many aspects of natural history and had even published a book of insect

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photographs. It was he who encouraged Sandy’s interest in nature. In 1921 and again in 1924 he visited Panama, where his father was working. From September 1924 to 1926 he accompanied his parents on a voyage to England and thence to Indonesia, with many stops and side-trips to parts of western Europe, and northern Africa. His opportunities to collect insects were not wasted, and he knew by then that he wanted to become an entomologist. His education to this point had been slight, and in 1926 he entered a preparatory school to acquire enough education to enter university. In 1928 he entered Harvard University, and received a B.S. degree in biology in 1932. At Harvard he encountered Charles Brues, Frank Carpenter, and Joseph Bequaert. One of the latter’s interests was Tabanidae, and it was this that inspired Sandy’s decision to study tabanid taxonomy for his graduate research at Harvard. Requirements for his Ph.D. degree were completed in 1934, but the dissertation was not completed until 1941. In the intervening 6 years, he held several jobs, and he married Elva Whitman in 1938. The first job (1934–1935) at the University of Florida’s Agricultural Experiment Station at Monticello, was as entomologist studying control of insect pests of pecan. In 1935–1937 he worked for the International Health Division of the Rockefeller Foundation, studying insect vectors of “jungle” yellow fever in Brazil. With his wife, in September 1938, he moved to Panama, and began a 32-year association with the Gorgas Memorial Laboratory. His work continued to be on the taxonomy of biting insects (and ticks). He worked on phlebotomine sand flies, simuliid black flies, and tabanids. During World War II he held a U.S. army commission, and he focused on control of mosquitoes, black flies, and sand flies. This took him to Peru and Guatemala as well as Panama. In 1949–1950 he took a leave of absence to teach medical entomology at the University of Minnesota. In 1953, his work on tabanids progressed with visits to examine type specimens in the museums of London and Paris, in 1959 to Rio de Janeiro, and in 1964 to Denmark,

The Netherlands, Belgium, Germany, France, Austria and Italy. This work on the type specimens was published in several papers, and in 1971 was crowned with his catalog of Neotropical Tabanidae. He retired from Gorgas Memorial Laboratory in 1970 and moved to Gainesville, Florida, where he was given an office which he used until 1988 for further tabanid studies (and for guidance to graduate students). Then, in 1988 he moved some blocks away to the Florida State Collection of Arthropods in a building of the Florida Department of Agriculture’s Division of Plant Industry. Here, his large collection is housed. He died on February 10, 1994, a few days before putting the finishing touches to a revised catalog of Neotropical Tabanidae which, coauthored with J. F. Burger, was published later that year. Elva and their two children survived him.

Reference Burger JF (1999) Alexander Graham Bell (“Sandy”) Fairchild: a biography. In: Burger JR (ed) Contributions to the knowledge of Diptera. A collection of articles on Diptera commemorating the life and work of Graham B. Fairchild, pp 1–41. Memoirs on Entomology, International 14: i–viii, 1–648

Fairmaire, Léon Léon Fairmaire was born in Paris on June 20, 1820. He received training in law, but the 1848 war ruined his family financially, so he became a public servant, eventually retiring as a hospital administrator. He became an active member of the Société Entomologique de France, was president, and honorary president from 1893 to 1906. Most of his very numerous publications (more than 450) contained unintegrated species descriptions of beetles, not just from Europe but from worldwide localities. However, with Laboulbène he published in 1854 the Coleoptera section of “Faune entomologique française,” which was a

Fairyflies (Hymenoptera: Mymaridae)

major analytical work. He collaborated with Jacquelin du Val in “Genera des coléoptères d’ Europe” and with Germain in “Coléoptères du Chili.” His collection is housed at the Muséum National d’ Histoire Naturelle in Paris. He died in Paris on April 1, 1906.

Reference Herman LH (2001) Fairmaire, Léon. Bull Am Mus Nat Hist 265:63–64

Fairyflies (Hymenoptera: Mymaridae) Elisabetta Chiappini1, John Huber2 Universita Cattolica del Sacro Cuore, Piacenza, Italy 2 Canadian Forestry Service, Ottawa, ON, Canada

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The family Mymaridae is cosmopolitan, occurring in all terrestrial habitats and also in freshwater ponds and streams. The greatest generic diversity occurs in Australia, New Zealand and South America, but the greatest number of species is probably in tropical forests. The northern hemisphere, particularly Europe, is relatively depauperate, with about one quarter of the genera. Mymarids form an important component of any chalcid fauna, making up at least 5–10% of the individuals of Chalcidoidea collected by methods such as Malaise traps or pan traps. This family is one of the few chalcids groups with a common name – fairyflies – derived from the fact that individuals of most of the species are such small insects that most people have never seen them. Indeed, the family includes the smallest recorded insect: the wingless, eyeless males of Dichopomorpha echmepterygis Mockford, that live as parasites in barklouse (Psocoptera) eggs. Four males lined up end to end would extend the diameter of a period.

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Diagnosis Mymaridae are small to minute, mostly delicate wasps that are 0.13–5.4 mm long (average 0.5–1.0 mm), usually without metallic coloration, and usually winged but sometimes wingless. The antennae are usually at least as long as the body, those of the females have a distinct club, and those of the males are filiform. The most important diagnostic feature distinguishing mymarids from other Hymenoptera is the head structure. Dark bars of cuticle (trabeculae) and associated sutures arranged in an H-like pattern divide the vertex and the frons into two distinct sclerites. Mymarid wings are also characteristic, with long fringes of hairs. The forewing usually has a distinct, backward projecting seta (hypochaeta) on the ventral surface of the wing blade in front of the marginal vein. The hind wing is almost always very narrow and stalked, and the wing membrane does not extend the wing base.

Classification The family contains about 1,400 described species, currently classified in about 100 genera. These have been grouped into tribes and subfamilies based upon either tarsal number or metasomal attachment. Depending on which character is used first, the five tribes and two subfamilies will contain different groupings of genera. A different classification, with three subfamilies, has also been proposed, based on male genitalia. One fossil subfamily was also described, based on a fossil genus in Canadian Cretaceous amber. Regardless of the system followed, the previously proposed tribes and subfamilies need to be critically reviewed to take into better account the diverse fauna from the Australian region, which includes the most primitive genera. Keys to genera are given by Annecke & Doutt (1961) for the world (outdated), Yoshimoto (1990) for the Western Hemisphere, Schauff (1984) for the Holarctic Region, Subba Rao & Hayat (1983)

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for the Oriental Region, and Noyes & Valentine (1989) for New Zealand. The largest and most common genera are Anagrus, Anaphes, Gonatocerus, and Polynema. These four account for over half of all the species. Another five, Alaptus, Camptoptera, Erythmelus, Ooctonus, and Stethynium make up another quarter of the species.

mymarids are unusual because they often have two different types of larval instars and two different kinds of preimaginal development. In Anaphes, a secondary immobile sacciform larva follows an active first instar “mymariform” larva. In Anagrus, the opposite occurs – an immobile first instar followed by a second, very active “hystriobdellid” instar.

Life History and Habits

Economic Importance

Mymarids are found in all terrestrial habitats from deserts to rainforests, and in most cultivated areas. Members of the genus Caraphractus live in ponds where the adults use their wings as paddles to swim under water. Many species can be collected in great numbers using Malaise traps or pan traps, but because of their small size, they are rarely seen and are difficult to study when alive. As a result, there is a tremendous amount of new information to be discovered about every aspect of their life history. The biology of very few species (in Alaptus, Anagrus, Anaphes, Caraphractus, Gonatocerus, and Polynema) has been studied in detail. Otherwise, most information on hosts, habits, or microhabitats occupied can be obtained only from the little biological information associated with specimens in museum collections. Hosts are known for species in only about one quarter of the genera, mainly in the four largest ones. Many host records need confirmation, however. Host records suggest that Hemiptera, especially Auchenorrhyncha, are the most commonly used hosts, but this could be because this group has been better studied than other hemimetabolous orders. Other host orders known for certain are Coleoptera, Diptera, Odonata, Psocoptera, and Thysanoptera. All mymarids are internal, solitary or gregarious, egg parasitoids of other insects. Development is completed entirely within a host egg. There may be several generations per year, often on different hosts. As holometabolous insects,

Most of the biological literature on mymarids focuses on Anagrus and Anaphes species because these two genera are the most used in biological control against economically important pests. About ten species of mymarids have been used in classical biological control attempts against insect pests such as Curculionidae, Chrysomelidae, Cicadellidae and Delphacidae. Anagrus is most important in vineyards against leafhoppers (Cicadellidae) in North America and Europe (where up to 90% egg parasitism may occur) and against planthoppers (Delphacidae) and leafhoppers of rice in Asia and Central America. Anaphes spp. are among the most effective parasitoids of leaf beetles (Chrysomelidae) in cereals and carrots in North America, often with 50–90% parasitism rates. The best-known example of successful biological control using mym arids is that of Anaphes nitens Girault) against the eucalyptus snout beetle, Gonipterus scutellatus Gyllenhal, in parts of Africa, South America and southern Europe. Anaphes iole Girault and Anagrus atomus L. are commercially reared for sale and mass release against Lygus bugs and leafhoppers in North America and Europe, respectively.

References Annecke DP, Doutt RL (1961) The genera of the Mymaridae. Hymenoptera: Chalcidoidea. Entomology Memoirs. Department of Agricultural Technical Services, Republic of South Africa, vol 5, pp 1–71

Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae)

Huber JT (1986) Systematics, biology, and hosts of the Mymaridae and Mymarommatidae (Insecta: Hymeno-ptera): 1758–1984. Entomography: Ann Rev Biosyst 4:185–243 Noyes JS, Valentine EW (1989) Mymaridae (Insecta: Hymenoptera) – introduction, and review of genera. Fauna of New Zealand, vol 17, 95 pp Subba Rao BR, Hayat M (1983) Key to the genera of Oriental Mymaridae, with a preliminary catalog (Hymenoptera: Chalcidoidea). Contrib Am Entomol Inst 20:125–150 Yoshimoto CM (1990) A review of the genera of New World Mymaridae (Hymenoptera: Chalcidoidea). Flora & fauna handbook no. 7. Sandhill Crane Press, Gainesville, FA, 166 pp

Falciform This term is used to express a sickle-shaped appearance.

Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) John L. Capinera University of Florida Gainesville, FL, USA The fall armyworm is native to the tropical regions of the western hemisphere from the United States to Argentina. It normally overwinters successfully in tropical areas; in the United States overwintering occurs only in southern Florida and southern Texas. The fall armyworm is a strong flier, and disperses long distances annually during the summer months. Thus, in the USA it is recorded from virtually all states east of the Rocky Mountains. However, as a regular and serious pest, its range tends to be mostly the southeastern states.

Life Cycle and Description The life cycle is completed in about 30 days during the summer, but 60 days in the spring and autumn, and 80–90 days during the winter. The number of generations occurring in an area varies with the appearance of the dispersing adults. The ability to

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diapause is not present in this species. In northern areas, where fall armyworm moths do not appear until August, there may be but a single generation. The number of generations is reported to be one to two in Kansas, three in South Carolina, and four in Louisiana. In coastal areas of north Florida, moths are abundant from April to December, but some are found even during the winter months.

Egg The egg is dome shaped; the base is flattened and the egg curves upward to a broadly rounded point at the apex. The egg measures about 0.4 mm in diameter and 0.3 m in height. The number of eggs per mass varies considerably but is often 100–200, and total egg production per female averages about 1,500. The eggs are sometimes deposited in layers, but most eggs are spread over a single layer attached to foliage. The female also deposits a layer of grayish scales between the eggs and over the egg mass, imparting a furry or moldy appearance. Duration of the egg stage is only 2–3 days during the summer months.

Larva There usually are six instars in fall armyworm. Head capsule widths are about 0.35, 0.45, 0.75, 1.3, 2.0, and 2.6 mm, respectively, for instars 1–6. Larvae attain lengths of about 1.7, 3.5, 6.4, 10.0, 17.2, and 34.2 mm, respectively, during these instars. Young larvae are greenish with a blackhead, the head turning orangish in the second instar. In the second, but particularly the third instar, the dorsal surface of the body becomes brownish, and lateral white lines begin to form. In the fourth to the sixth instars the head is reddish brown, mottled with white, and the brownish body bears white subdorsal and lateral lines (Fig. 8). Elevated spots occur dorsally on the body; they are usually dark in color, and bear spines. The face of the mature larva is also marked with a white inverted “Y” and the

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e pidermis of the larva is rough or granular in texture when examined closely. However, this larva does not feel rough to the touch, as does corn earworm, Helicoverpa zea (Boddie), because it lacks the microspines found in the similar appearing corn earworm. The appearance of this insect is quite variable. Duration of the larval stage tends to be about 14 days during the summer and 30 days during cool weather. Mean development time was determined to be 3.3, 1.7, 1.5, 1.5, 2.0, and 3.7 days for instars 1–6, respectively, when larvae were reared at 25°C.

Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), Figure 7 Adult fall armyworm, Spodoptera frugiperda.

Pupa Pupation normally takes place in the soil, at a depth 2–8 cm. The larva constructs a loose cocoon, oval in shape and 20–30 mm in length, by tying together particles of soil with silk. If the soil is too hard, larvae may web together leaf debris and other material to form a cocoon on the soil surface. The pupa is reddish brown in color, and measures 14–18 mm in length and about 4.5 mm in width. Duration of the pupal stage is about 8–9 days during the summer.

Adult The moths have a wingspan of 32–40 mm. In the male moth, the forewing generally is shaded gray and brown, with a triangular white spots at the tip and near the center of the wing (Fig. 7). The forewings of females are less distinctly marked, ranging from a uniform grayish brown to a fine mottling of gray and brown. The hind wing is iridescent silver-white with an narrow dark border in both sexes. Adults are nocturnal, and are most active during warm, humid evenings. After a preoviposition period of 3–4 days, the female normally deposits most of her eggs during the first 4–5 days of life, but some oviposition occurs for up to 3 weeks. Duration of adult life is estimated to average about 10 days.

Fall Armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), Figure 8 Fall armyworm larva.

Host Plants This species seemingly displays a very wide host range, with over 80 plants recorded, but clearly prefers grasses. The most frequently consumed plants are field corn and sweet corn, sorghum, Bermudagrass, and grass weeds such as crabgrass, Digitaria spp. When the larvae are very numerous they defoliate the preferred plants, acquire an “armyworm” habit and disperse in large numbers, consuming nearly all vegetation in their path Field crops are frequently injured, including alfalfa, barley, Bermuda grass, buckwheat, cotton, clover, corn, oat, millet, peanut, rice, ryegrass, sorghum, sugarbeet, sudangrass, soybean, sugarcane, timothy, tobacco, and wheat. Among vegetable crops, only sweet corn is regularly damaged. Other crops sometimes injured are apple, grape, orange, papaya, peach, strawberry and a number of flowers. There is some evidence that fall armyworm strains exist, based


primarily on their host plant preference. One strain feeds principally on corn, but also on sorghum, cotton and a few other hosts if they are found growing near the primary hosts. The other strain feeds principally on rice, Bermudagrass, and Johnson grass.

Damage Larvae cause damage by consuming foliage. Young larvae initially consume leaf tissue from one side, leaving the opposite epidermal layer intact. By the second or third instar, larvae begin to make holes in leaves, and eat from the edge of the leaves inward. Feeding in the whorl of corn often produces a characteristic row of perforations in the leaves. Larval densities are usually reduced to one to two per plant when larvae feed in close proximity to one another, due to cannibalistic behavior. Older larvae cause extensive defoliation, often leaving only the ribs and stalks of cornplants, or a ragged, torn appearance. In corn, they sometimes burrow into the ear, feeding on kernels in the same manner as corn earworm, Helicoverpa zea. Unlike corn earworm, which tends to feed down through the silk before attacking the kernels at the tip of the ear, fall armyworm will feed by burrowing through the husk on the side of the ear.

Natural Enemies Cool, wet springs followed by warm, humid weather in the overwintering areas favor survival and reproduction of fall armyworm, allowing it to escape suppression by natural enemies. Once dispersal northward begins, the natural enemies are left behind. Therefore, although fall armyworm has many natural enemies, few act effectively enough to prevent crop injury. Numerous species of parasitoids affect fall armyworm. The wasp parasitoids most frequently reared from larvae

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in the United States are Cotesia marginiventris (Cresson) and Chelonus texanus (Cresson) (both Hymenoptera: Braconidae), species that are also associated with other noctuid species. Among fly parasitoids, the most abundant is usually Archytas marmoratus (Townsend) (Diptera: Tachinidae). However, the dominant parasitoid often varies from place to place and from year to year.

Management Sampling Moth populations can be sampled with blacklight traps and pheromone traps; the latter are more efficient. Pheromone traps should be suspended at canopy height, preferably in corn during the whorl stage. Catches are not necessarily good indicators of density, but indicate the presence of moths in an area. Once moths are detected it is advisable to search for eggs and larvae.

Insecticides Insecticides are usually applied to sweet corn in the southeastern USA to protect against damage by fall armyworm, sometimes as frequently as daily during the silking stage. In Florida, fall armyworm is the most important pest of corn. It is often necessary to protect both the early vegetative stages and reproductive stage of corn. Because larvae feed deep in the whorl of young corn plants, a high volume of liquid insecticide may be required to obtain adequate penetration.

Cultural Techniques The most important cultural practice, employed widely in southern states, is early planting and/or early maturing varieties. Early harvest allows many corn ears to escape the higher armyworm densities that develop later in the season. Partial

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Fall, Henry Clinton

resistance is present in some sweet cornv arieties, but is inadequate for complete protection.

Biological Control Although several pathogens have been shown experimentally to reduce the abundance of fall armyworm larvae in corn, only Bacillus thuringiensis presently is feasible, and success depends on having the product on the foliage when the larvae first appear.  Vegetable Pests and Their Management  Turfgrass Pests and Their Management

References Ashley TR, Wiseman BR, Davis FM, Andrews KL (1989) The fall armyworm: a bibliography. Fla Entomol 72:152–202 Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, CA, 729 pp Luginbill P (1928) The fall armyworm. USDA Tech Bull 34, 91 pp Sparks AN (1979) A review of the biology of the fall armyworm. Fla Entomol 62:82–87

Fall, Henry Clinton Henry Fall was born in New Hampshire on December 25, 1862. In 1884 he received a B.S. degree from Dartmouth College, New Hampshire. For the next 5 years he taught physics and mathematics in Chicago schools, and for the 28 after that, physics and chemistry at schools in California. In 1917, he retired to New England. He had numerous hobbies, among which was collecting beetles. He accumulated about 250,000 specimens, described 1,484 species, and wrote 144 publications. He received an honorary Ph.D. degree from Dartmouth College in 1929 and died in Massachusetts in 1939. His insect collection and papers were left to the Museum of Comparative Zoology of Harvard University.

Reference *Mallis A (1971) Henry Clinton fall. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 266–269

Fallow Cultivated land allowed to remain free of crops during the normal growing season.

False Blister Beetles Members of the family Oedemeridae (order Coleoptera).  Beetles

False Burnet Moths (Lepidptera: Urodidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA False burnet moths, family Urodidae, total only about 80 species, primarily Neotropical (mostly the genus Urodus), but with a few species in North America and in Eurasia (subfamily Galacticinae).

False Burnet Moths (Lepidptera: Urodidae), Figure 9 Example of false burnet moths (Urodidae), U rodus isthmiella (Busck) from Panama.

False Diamondback Moths (Lepidoptera: Acrolepiidae)

Only two subfamiles are named: Galacticinae and Urodinae. The family is in the superfamily Sesioidea in the section Tineina, subsection Sesiina, of the division Ditrysia. Adults small (10–37 mm wingspan), with head smooth-scaled; haustellum naked; labial palpi upcurved; maxillary palpi 1–2-segmented. Wings somewhat elongated (Fig. 9). Maculation mostly unicolorous in shades of gray, but a few with various spots; some with metallic-iridescence or lustrous scales. Adults may be crepuscular or mostly nocturnal, but a few possibly diurnal. Larvae are leaf webbers or skeletonizers, but few are known biologically. Pupation is in a specialized filigreed cocoon. Host plants known in Lauraceae, Leguminosae, Salicaceae, Sapotaceae, and Theaceae. A few are minor pests.

References Frost SW (1972) Notes on Urodus parvula (Herny Edwards) (Yponomeutidae). J Lepid Soc 26:173–177 Heppner JB (1997) Wockia asperipunctella in North America (Lepidoptera: Urodidae: Galacticinae). Holarctic Lepid 4:81–82 *HeppnerJB (2003) Urodidae. In: Lepidopterorum Catalogus (n.s.), Fasc 66. Association for Tropical Lepidoptera, Gainesville, FL, 16 pp Kyrki J (1988) The systematic position of Wockia Heinemann, 1870, and related genera (Lepidoptera: Ditrysia: Yponomeutidae auct.). Nota Lepid 11:45–69 Moriuti S (1963) Remarks on the Paraprays anisocentra (Meyrick, 1922) (Plutellidae), with descriptions of its larva and pupa. Trans Lepid Soc Jpn 14(3):52–59 [in Japanese]

False Darkling Beetles Members of the family Melandryidae (order Coleoptera).  Beetles

False Diamondback Moths (Lepidoptera: Acrolepiidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA False diamondback moths, family Acrolepiidae, include 96 species, mostly Palearctic. The family is part of the superfamily Yponomeutoidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small (10–25 mm wingspan), with head smooth-scaled; haustellum naked; labial palpi upcurved; maxillary palpi 4-segmented. Wings elongated, with longer fringes (Fig. 10) on the pointed hindwings. Maculation various shades of brown with lighter markings. Adults are crepuscular or diurnal. Larvae mostly leafminers, but some are borers in seeds, stems and flower buds. Several hostplant groups are used, but mostly on Compositae. Very few are economic.

False Click Beetles Members of the family Eucnemidae (order Coleoptera).  Beetles

False Clown Beetles Members of the family Sphaeritidae (order Coleoptera).  Beetles

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False Diamondback Moths (Lepidoptera: Acrolepiidae), Figure 10 Example of false diamondback moths (Acrolepiidae), Acrolepia autumnitella Curtis from Austria.

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False Firefly Beetles

References Gaedike R (1970) Revision der paläarktischen Acrolepiidae (Lepidoptera). Entomol Abhandlungen 38:1–54 Gaedike R (1984) Revision von nearktischen und neotropischen Acrolepiidae (Lepidoptera). Entomol Abhandlungen 47:179–194 Gaedike R (1986) Die Typen der orientalischen, australischen und äthiopischen Acrolepiidae (Lepidoptera). Beiträge zur Entomol 36:63–68 Gaedike R (1988) Beitrag zur Kenntnis afrikanischer Acrolepiidae (Lepidoptera). Beiträge zur Entomol 38:83–87 *Gaedike R (1997) Acrolepiidae. In: Lepidopterorum catalogus, (n.s.). Fasc 55. Association for Tropical Lepidoptera, Gainesville, FL, 16 pp

False Firefly Beetles Members of the family Omethridae (order Coleoptera).  Beetles

False Flower Beetles Members of the family Scraptiidae (order Coleoptera).  Beetles

False Ground Beetles Members of the family Trachpachidae (order Coleoptera).  Beetles

False Metallic Wood-Boring Beetles Members of the family Throscidae (order Coleoptera).  Beetles

False Owlet Moths (Lepidoptera: Thyatiridae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA False owlet moths, family Thyatiridae, comprise 224 species from all regions (absent in Australia), but most are tropical Oriental (199 sp.); the actual fauna probably exceeds 275 species. Two subfamilies are recognized: Thyatirinae and Polyplocinae. The family is in the superfamily Drepanoidea, in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults medium size (28–52 mm wingspan), with head scaling normal; maxillary palpi vestigial; antennae serrate or filiform; body robust. Wings elongate-triangular, mostly with acute forewing apex; hindwings subtriangular and rounded. Maculation varies but mostly (Fig. 11) shades of brown and gray, with various spotting and striae; sometimes more colorful and with

False Katydids A subfamily (Phanopterinae) of katydids in the order Orthoptera: Tettigoniidae.  Grasshoppers, Katydids and Crickets

False Long-Horned Beetles Members of the family Stenotrachelidae (order Coleoptera).  Beetles

False Owlet Moths (Lepidoptera: Thyatiridae), Figure 11 Example of false owlet moths ( Thyatiridae), Thyatira batis (Linnaeus) from Taiwan.

False Skin Beetles

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lustrous color patches or iridescence; hindwings mostly unicolorous and pale or dark. Superficially, the moths appear similar to owlet moths, thus the derivation of their common name. Adults are nocturnal. Larvae are mostly nocturnal leaf feeders. Host plants are recorded in a number of plant groups with forest trees, including Betulaceae, Caprifoliaceae, Cornaceae, Ebenaceae, Fagaceae, Juglandaceae, Rosaceae, and Salicaceae.

References Bryner R (1997) Thyatiridae – Wollrückenspinner. In: Schmetterlinge und ihre Lebensräume: Arten-Gefährdung-Schutz. Schweiz und angrenzenden Gebiete, 2:477–512, pl 12. Pro Natura-Schweizerische Bund fuer Naturschutz, Basel Clarke JFG, Benjamin FH (1938) A study of some North American moths allied to the thyatirid genus Bombycia Hübner. Bull Southern California Acad Sci 37:55–73 *Houlbert C (1921) Revision monographie de la famille des Cymatophoridae. In: études de Lépidoptères Comparée, 18(2):23–244, pl 988–989. Rennes Seitz A (ed) (1912–36) Familie: Cymatophoridae. In: Die Gross-Schmetterlinge der Erde, 2:321–33, pl 49, 55–56 (1912); 2(suppl):187–195, 286, pl 11, 14–15 (1933–34); 6:1171–1175, pl 172 (1936); 10:657–663, pl 85 (1930). A. Kernen, Stuttgart Soltys E (1965) Thyatiridae. In: Klucze do Oznaczania Owadów Polski. 27. Motyle – Lepidoptera, 49:1–53 [part]. Polskie Towardzystwo Entomologiczne [in Polish], Warsaw

False Pit Scales Members of the family Lecanodiaspididae, superfamily Coccoidae (order Hemiptera).  Bugs

False Plume Moths (Lepidoptera: Tineodidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA False plume moths, family Tineodidae, include only 11 species, all from Australia. The family is in the

False Plume Moths (Lepidoptera: Tineodidae), Figure 12 Example of false plume moths ( Tineodidae), Tineodes adactylis Guenée from Australia.

superfamily Pterophoroidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small (15–34 mm wingspan), with head scaling average; haustellum naked; labial palpi porrect; maxillary palpi 4-segmented. Forewings elongate (Fig. 12) and pointed termens can be falcate. Maculation mostly mottled shades of tan and gray. Adults possibly diurnal or crepuscular. Larvae are leaftiers, but most are not known biologically. Only recorded host plants are in Euphorbiaceae and Oleaceae.

References *Common IFB (1990) Family Tineodidae. In: Moths of Australia, 322–325 [part]. Melbourne University Press, Melbourne. *Heppner JB (1998) Tineodidae. In: Lepidopterorum Catalogus, (n.s.). Fasc. 61. Association for Tropical Lepidoptera, Gainesville, FL, 8 pp

False Skin Beetles Members of the family Biphyllidae (order Coleoptera).  Beetles

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False Soft Scales

False Soft Scales

Heart Muscle

Members of the family Stictococcidae, superfamily Coccoidae (order Hemiptera).  Bugs

Silk gland Midgut Visceral fat Parietal fat

False Wireworm False wireworms are beetle larvae in the Family Tenebrionidae. So-called “true” wireworms are beetle larvae in the Family Elateridae.  Wheat Pests and Their Management

Nerve cord

Fat Body, Figure 13 Cross section of caterpillar larva showing distribution of fat tissue ( adapted from Chapman, The insects: structure and function).

Fat Body Family A subdivision of an order, containing a group of related genera. Family names end in -idae.  Classification

An aggregation of large cells in the body cavity that stores metabolites (Fig. 13) and is a center of intermediary metabolism.  Internal Anatomy

Fatty Acid Binding Proteins Fanniidae A family of flies (order Diptera).  Flies

Fast-Footed Bugs Members of the family Velocipedidae (order Hemiptera).  Bugs

Fastigium The anterior dorsal surface of the head, below the antennae. In many insects, this is the extreme anterior point.  Head of Hexapods

Norbert H. Haunerland Simon Fraser University, Burnaby, BC, Canada The flight muscles of insects usually depend on fatty acids to fuel migratory flight. These fatty acids are obtained prior to migration from the diet and stored as triacylglycerol in the fat body. During flight, the lipids are converted to diacylglycerol that is released into the hemolymph and transported by the lipoprotein lipophorin to the flight muscle. There, diacylglycerol is hydrolyzed, and free fatty acids enter the muscle cell. Once fatty acids have crossed the plasma membrane, they need to move through the hydrophilic cytosol to the mitochondria where β-oxidation takes place. Because fatty acids are only poorly soluble in water, an intracellular mechanism in needed for their transport through the cytosol. Similarly, a transport process is required in the midgut cells, to facilitate the uptake of fatty acids from the diet

Fatty Acid Binding Proteins

and their subsequent delivery to the fat body. The intracellular transport of fatty acids is mediated by fatty acid binding proteins (FABPs). FABPs are ubiquitous proteins in many vertebrate and invertebrate tissues, with separate genes encoding the FABPs found in various tissues. In insects, distinct FABPs have been identified and characterized in midgut cells and in flight muscle cells. Two midgut FABPs have been isolated from Manduca sexta, and their amino acid sequence and tertiary structure have been determined. Best characterized of the muscle FABPs is the FABP from flight muscles of locusts (Schistocerca gregaria and Locusta migratoria), but analogous proteins have also been found in Lepidoptera (Helicoverpa zea, Acherontia atropos), Hymenoptera (Apis mellifera), and Heteroptera (Dipetalogaster maximus). Their structures and function in insect metabolism are described below. Locust muscle FABPs are very similar in their characteristics to mammalian FABPs. They are small, acidic proteins (Mr 15,000; pI 5.2–5.8) with a single binding site for fatty acids. Locust FABP was crystallized and its structure solved at 2.1 Å resolution. The protein displays the characteristic β-barrel motif common to all FABP. Two perpendicularly oriented β-sheets form a barrel-like structure; within this barrel the fatty acid binding site is located. The β-barrel itself is open to one side, but this (Fig. 14) opening is closed off by a helix-turn-helix motif. The overall structure is similar to the midgut FABPs from Manduca sexta, and their mammalian counterparts. Locusts metabolize fatty acids at extremely high levels during migratory flight, and FABP is required for their rapid transport. Indeed, FABP is the most prominent flight muscle protein in mature adult locusts, amounting to as much as 20% of all cytosolic proteins. Yet, it is completely absent in immature locusts and in newly emerged adults. FABP expression commences immediately after adult ecdysis, and continues at high rates for almost 2 weeks. During this period, the FABP concentration gradually increases to its final concentration. This increase in the FABP concentration is concomitant with the

F

Fatty Acid Binding Proteins, Figure 14 Structure of locust muscle FABP. All FABPs have a typical beta-barrel structure. The binding site for a single fatty acid molecule is in the cavity formed by the beta-strands; the site is closed by a helix-turn-helix motif. Structure drawn from Brookhaven Protein Data Bank file ftp1.

flight ability of the insect. Locusts cannot fly for longer time periods during the first 10 days of adult life, and one of the reasons for this may be the lack of an efficient intracellular fatty acid transport mechanism. Once FABP reaches a significant concentration, it becomes possible to use large amounts of fatty acids and hence to fly for long time periods. In mature adults, flight activity for periods exceeding 2 h further increases FABP expression. When 20 day-old locusts were exercised in tethered flight, the levels of FABP mRNA increased more than 12-fold. Flight times shorter than 1 h, however, had no influence on FABP expression. The latter flights are fueled by carbohydrates, while longer flight periods depend on the β-oxidation of lipids, and hence an efficient fatty acid transport. It was shown that a similar, strong accumulation of FABP mRNA could be induced by adipokinetic hormone, which mobilizes fatty acid from the fat body and stimulates their transport to the flight muscle, and even by an increased lipid supply alone. Thus, it appears that FABP expression is stimulated when the concentration of free fatty acid in the cell exceeds the amount of available FABP. The molecular mechanisms by which this activation occurs have been partially elucidated.

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Fauriellidae

The promoter of the FABP gene of the locust contains a fatty acid response element that is necessary for the induction of gene expression by fatty acids. The fatty acid response element is a 19 basepair inverted repeat with two hexanucleotide halfsites interspersed by three nucleotides, similar to steroid hormone response elements. It is likely that two different factors bind to the fatty acid response element, at least one of these is activated by the binding of long chain fatty acids. Fatty acids (Fig. 15) are required for full activity, and their availability to nuclear proteins depends on the intracellular concentration of FABP. FABP appears to have free access to the nuclear lumen, and thus this proteins contribution must be considered. While for many FABP-types the exact functions have not been elucidated, it is generally accepted

FA

CO2 FABP

ATP

FABP

mt

cytosol FABP

FAAR FAAR

?

nucleus transcription

FARE

5’ gg AGTGGT agt TCCCAT cc 3’ 3’ cc TCACCA tca AGGGTA gg 5’

Fatty Acid Binding Proteins, Figure 15 Regulation of the locust muscle FABP gene. Shown is a schematic drawing of a muscle cell. Most of the fatty acid is bound by FABP and delivered to the mitochondrion for beta-oxidation. FABP also acts as a sensor of the fatty acid concentration in the nucleus. In the presence of an excess of fatty acid, nuclear transcription factors are activated, and the FABP gene is expressed. Abbreviations: FA = Fatty acid, FAAR = fatty acid activated receptor, FARE = fatty acid response element, mt = mitochondrion.

that muscle FABP serves the following three purposes: FABP increases the solubility of fatty acids and thus lead to a more rapid transport through the cytosol. Moreover, it serves as an intracellular acceptor for free fatty acids that have passed through the plasma membrane. Without such an acceptor, fatty acids would mostly remain in the membrane and not dissolve in the aqueous cytosol. Finally, the binding protein acts as a buffer for free fatty acids, both to assure the presence of fuel molecules prior to muscle activity, and to prevent the build-up of high concentrations of unbound fatty acids afterwards. With their hydrophilic carboxy-group and the hydrophobic tail, free fatty acids are amphiphilic molecules that, by detergent-like interactions, could destroy membrane structures within a muscle cell. The extremely high concentrations of FABP found in locust flight muscle support these functions, and the up-regulation of FABP gene expression by fatty acids represents an elegant physiological mechanism to handle high fatty acid fluxes safely and efficiently.  Locomotion and Muscles

References Haunerland NH (1997) Transport and utilization of lipids in insect flight muscles. Comp Biochem Physiol 117B:475–482 Haunerland NH (1994) Fatty acid binding protein in locust and mammalian muscle. Comparison of structure, function and regulation. Comp Biochem Physiol 109B:199–208 Smith AF, Tsuchida K, Hanneman E, Suzuki TC, Wells MA (1992) Nucleotide, protein isolation, characterization, and cDNA sequence of two fatty acid-binding proteins from the midgut of Manduca sexta larvae. J Biol Chem 267:380–384 Wu Q, Haunerland NH (2001) A novel fatty acid response element controls the expression of the flight muscle FABP gene of the desert locust, Schistocerca gregaria. Eur J Biochem 268:5894–5900

Fauriellidae A family of thrips (order Thysanoptera).  Thrips

Felt, Ephraim Porter

Fauvel, Charles Adolphe Albert Charles Adolphe Albert Fauvel was born in Caën, France, in 1840 and died there on January 4, 1921. A lawyer by profession, he was a prolific describer of insects, founding the journal “Revue d’ Entomologie” as an outlet for many of his works. By 1900, under the name Albert Fauvel, he had published at least 246 papers, mostly on Coleoptera, and on Staphylinidae in particular. His major book was “Faune gallo-rhénane,” in several volumes, which, unfortunately, was never completed. Other major works are on the staphylinid faunas of northwestern Africa, Australia and Polynesia, the Moluccas and New Guinea, and New Caledonia, material for which he obtained from collectors in those areas. In 1910, he abruptly stopped publication of Revue d’ Entomologie, withdrew from scientific contacts, and remained secluded until his death. He described 96 genera and 1,851 species of Staphylinidae. His collection is now in the Institut Royal des Sciences Naturelles de Belgique.

Reference Herman LH (2001) Fauvel, Charles Alphonse Albert. Bull Am Mus Nat Hist 265:65–66

Feather-Winged Beetles Members of Coleoptera).  Beetles

the

family

Ptilinidae

(order

Feces The excrement of insects produced by the digestive system and passed out the anus. It is also known as excreta. When it is mixed with an abundance of indigestable plant fragments it is commonly called frass.  Frass

 Alimentary Canal  Digestion

F

Fecundity The reproductive capacity of an organism, often taken to mean the number of eggs produced by a female during her lifetime (contrast with fertility).

Feeding Deterrents Chemicals that inhibit feeding but do not necessarily repel insects  Host Plant Selection by Insects

Felt, Ephraim Porter Ephraim Felt was born in Massachusetts on January 7, 1868. He graduated from Massachusetts State Agricultural College with a B.Sc. degree in 1891 and then became assistant to Fernald and studied the gypsy moth. In 1892 he was awarded a fellowship to Cornell University, studied with Comstock, and received a D.Sc. in 1894. From 1893 to 1895 he taught natural science at the Clinton Liberal Institute, and then worked in the office of the State Entomologist (Fig. 16) of New York, becoming State Entomologist (a job he held for 30 years) when the incumbent, J.A. Lintner, died in 1898. In 1904 appeared in print his “The mosquitoes or Culicidae of New York State” and in 1906 his two-volume “Insect affecting park and woodland trees.” His work on gall midges (Cecidomyiidae) was copious, and in his life he described 1,060 species of them, publishing in 1940 “Plant galls and gall makers.” Additionally, he wrote several books on trees, and worked on wind-borne insects, the role of insects as vectors of human diseases, and gypsy moth. He was editor of Journal of Economic Entomology from 1908 to 1935, an active member of the New York Entomological Society, a frequent contributor to the New York Times, and

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Femur (pl., femora)

Felt, Ephraim Porter, Figure 16 Ephraim P. Felt.

entomological editor of “Country Gentleman.” He married in 1908 and had four children. He died on December 14, 1943.

Reference *Mallis A (1971) Ephraim Porter Felt. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 399–402

Femur (pl., femora) A segment of the leg between the trochanter and tibia. The third leg segment and one of the two largest portions (Fig. 17) of the insect leg, often expanded to enhance leaping or prey capture.  Legs of Hexapods

Fenichel, Sámuel George Hangay Narrabeen, NSW, Australia

Sámuel Fenichel was born on the 25th of August 1868 in Nagyenyed, Alsó-Fehér Shire, in Transylvania, then Hungary, now Romania. He received excellent education in natural history in the highly respected Bethlen College of his hometown. In 1888, he was invited to join the Museum of Archaeology in Bucharest, Romania. For 2 years he lead the excavations and research of the ruins of Tropea, a fortress and settlement built by the Romans in Dobrudja (Romania). During this work he met Albert Grubauer, a naturalist from Munich, who was planning a zoological expedition to New Guinea. Fenichel was young, with a keen interest of natural history and an expert preparator of zoological specimens; therefore, he seemed to be an ideal companion to Grubauer, who consequently asked him to join his expedition. Fenichel resigned from his museum post and travelled to Budapest (Hungary) where he received further training in the Hungarian National Museum. The museum also commissioned him to collect zoological and ethnographical material for its collections. Grubauer and Fenichel arrived to German New Guinea (Kaiser Wilhelmsland) in December 1891. Fenichel started to work immediately by collecting zoological specimens, mainly insects, but Grubauer fell ill and left the island. He also took with him the 200,000 Marks, which were to support the expedition, leaving only 100 Marks for Fenichel. Despite this setback, Fenichel stayed and continued his work alone. He concentrated on entomological work mainly, accumulating more than 25,000 specimens. He explored the country around Astrolabe Bay, Friedrich-Wilhelmshafen (today Madang), Konstantinhafen, Erima and Stephansort. He collected in the Finisterre Mountains, where only two other European naturalists worked before him, the Russian N.N. Mikhulo-Maklai (1846–1888) and the German Otto Finsch (1839–1917). As most field zoologists of that age, he also collected ethnographical objects, the number of items in his collection were over 3,000. Most of Fenichel’s specimens reached the Hungarian National Museum and a few went to his Alma Mater in Nagyenyed. His promising carrier as an entomologist and

Fennah, Ronald Gordon

F

1 2 Hidden true segment 4 Coxa

3

5

Trochanter Femur Tibia 4 5 1 2 3 Tarsus

Pretarsus

Femur (pl., femora), Figure 17 Leg of a beetle (Coleoptera: Scarabaeidae) leg showing its component parts, and a close-up of one type of beetle tarsus (foot).

naturalist was cut short by malaria. Fenichel died in Stephansort on the March 12, 1893. A memorial plaque on the wall of the Port Moresby University commemorates the life and work of Sámuel Fenichel, the first Hungarian entomologist in New Guinea.

Reference Balogh J, Allodiatoris I (1972) In Memoriam Lajos Bíró and Sámuel Fenichel. Acta Zoologica, XVIII:1–2. Budapest, Hungary

Fennah, Ronald Gordon Ronald Fennah was born in Ludlow, England, in 1910. He graduated from Cambridge University in 1935 with a bachelor’s degree and was appointed lecturer in zoology at the Imperial College of Tropical Agriculture, Trinidad. While employed there, he was seconded in 1937–1942 as citrus entomologist and in 1942–1948 as food crop pests entomologist to the Windward Islands, and then (1948–1951) entomologist to the Trinidad Department of Agriculture and (1951–1958)

e ntomologist to the cocoa research scheme, Trinidad. These postings involved him in surveys for citrus pests, a (1947) book “The insect pests of food crops in the Lesser Antilles,” trials of the resistance of sugarcane varieties to froghoppers (Cercopidae), and studies of the insect pests of cacao in relation to cacao physiology. In 1944, he tested DDT against insect pests of food crops. To test its safety to humans, he deliberately ingested DDT, and painted an emulsion on his skin, during a period of 13 months. He detected no effect. In Trinidad, he developed an interest in the taxonomy of Hemiptera and began publishing on this subject, ultimately producing over 120 papers on this subject, mostly on Fulgoroidea. In 1958 he was appointed assistant director of the Commonwealth Institute of Entomology in London, its director in 1969, and he retired in 1975. Retirement did not stop his taxonomic contributions. Cambridge University awarded him an Sc.D. degree in 1967. He died on August 19, 1987, survived by his wife, Louie May.

References Wilson MR (1988) Dr. Ronald Gordon Fennah (1910–1987) [with bibliography]. Entomologist’s Monthly Magazine 124:167–176

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Feral

Wilson MR, Harris KM (1988) Ronald Gordon Fennah (1910–1987) Antenna 12:4

Feral Animals or plants that have escaped domestication and reverted to natural behavior. In entomology, this is used most commonly in reference to swarms of honey bees that escape domestication.

Fergusoninidae A family of flies (order Diptera).  Flies

Fernald, Charles Henry Charles Fernald was born in Maine on March 16, 1838. At 21, he entered Maine Wesleyan Seminary with the intent of becoming a ship’s captain. After 3 years of study he joined the Union Navy and served 3 years during the American Civil War. In the Navy, he also was able to take courses, completing the requirements of Bowdoin College for a B.A. degree, which he received. After the war he became principal of Litchfield Academy, then of Houlton Academy, both in Maine. In the last of the positions, he studied geology, botany, zoology and entomology on his own, and then received in 1871 a M.A. degree from Bowdoin College. That same year, he was made a professor of natural history in Maine State College. In addition to teaching, he studied and published on insects. In 1886 he moved to Massachusetts Agricultural College as professor of zoology and lecturer (Fig. 18) in veterinary science, and occupied this position until his retirement in 1910. The Hatch Act made Federal funds available to state agricultural colleges for experiment stations, and Charles was appointed entomologist to the Massachusetts station. This gave him responsibility for research in applied entomology. A main part of his research was aimed

Fernald, Charles Henry, Figure 18 Charles H. Fernald.

at the gypsy moth, whose presence in Massachusetts was due to its importation by Leopold Trouvelot and subsequent escape from confinement. This research, and Fernald’s teaching of entomology made Massachusetts a center for the training of entomologists. His wife, Maria, made her own mark on entomology, with moths of the families Tortricidae and Tineidae, and especially by publication of “A catalogue of the Coccidae of the world.” Their son, Henry Torsey Fernald, born on April 17, 1866, in Maine, became first head of the Department of Entomology at Massachusetts Agricultural College in 1899 while his father was professor of zoology. Charles Fernald died on February 22, 1921.

Reference *Mallis A (1971) Charles Henry Fernald and Henry Torsey Fernald. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 141–150

Fideliidae

Fern Scale, Pinnaspis aspidistrae (Signoret) (Hemiptera: Diaspididae) These scale insects affect the foliage and fruit of citrus.  Citrus Pests and Their Management

Ferris, Gordon Floyd

Fertility

F

The number of offspring produced, often taken to mean the number of eggs that hatch (living offspring) during the lifetime of the female. (contrast with fecundity)

Fertilization

Gordon Ferris was born in Kansas on January 2, 1893, then moved to Missouri with his family and four siblings. His mother died there in childbirth. Gordon moved at the age of 13 to live with his brother Leslie on a farm in Kansas. In 1909, he entered Ottawa University in Kansas but soon dropped out and went to work for a power company in Colorado. The power company funded education for its employees, and in 1912 sent Gordon to Stanford University in California. In 1917, he obtained the degree of M.A., became a teaching assistant there, and remained there for the rest of his 42-year academic career. He was a taxonomist and teacher. He worked on Anoplura, Mallophaga, Coccoidea, Diptera-Pupipara, Cimicidae, and Polyctenidae, being an excellent collector of the insects that he studied. His collecting trips took him throughout the southwest of the USA, and to Mexico and China, and his museum study trips took him to the Natural History Museum (London) and to Cambridge University. He published 275 works, of which his 4-volume “Atlas of the scale insects of North America” (1950–1953) is one of the most outstanding. He died on May 21, 1958.

The union of the haploid male and female gametes to produce a diploid zygote, marking the start of the development of a new individual and the beginning of cell differentiation.

Reference

A proteinaceous component of insect silk. It usually is covered by seracin.  Silk

*Mallis A (1971) Gordon Floyd Ferris. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 169–173

Ferruginous A rusty or reddish brown color.

Festoons Uniform rectangular regions, separated by sulci (grooves), and located on the posterior margin of most hard ticks.

Fetid A disagreeable or offensive odor to humans, though such odors may be quite attractive to insects. Such odors are often associated with decaying animals or plant material, but some plants produce fetid odors to attract pollinators.

Fibroin

Fideliidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees and Sawflies

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Field Capacity

Field Capacity A property of soils. Soil that contains all the moisture it can retain after draining freely under gravity. Saturated soil.

Field Crickets A subfamily of crickets (Gryllinae) in the order Orthoptera: Gryllidae.  Grasshoppers, Katydids and Crickets

Fig Rots Several fungi affect fig fruit, causing the fruit to rot. Insects are implicated in causing these diseases.  Transmission of Plant Diseases by Insects

Fig Wasps Hannah Nadel USDA-ARS, San Joaquin Valley Science Center, Parlier, CA, USA Miniscule wasps (order Hymenoptera) that breed exclusively in association with the flask-shaped floral receptacle (fig, syconium) of fig plants (Ficus spp.). The group is composed of about 3,000 species of Chalcidoidea in the families Agaonidae, Pteromalidae, Torymidae, Ormyridae, Eurytomidae, and the unplaced subfamilies Epichrysomallinae and Sycophaginae. The Agaonidae are mutualistic partners of figs, pollinating the flowers while laying their eggs in the ovules inside the receptacle. The other species feed on syconial tissues, parasitize the Agaonidae or each other, or parasitize a small number of other insects developing in the syconia. Non-pollinators mostly oviposit from the exterior of the fig wall, and hence have long ovipositors that evolved in length to match the thickness of the fig wall. Some resemble

pollinators in form and habit, entering the syconia to lay their eggs. Many have apterous or dimorphic males. Only 20–30% of fig wasp species have been described. A few species of Braconidae (Ichneumonoidea) have also been reared from syconia.  Wasps, Ants, Bees and Sawflies  Agaonidae

References Bouček Z (1993) The genera of chalcidoid wasps from Ficus fruit in the New World. J Nat Hist 27:173–217 Weiblen GD (2002) How to be a fig wasp. Ann Rev Entomol 47:299–330 West SA, Herre EA, Windsor DM, Green PRS (1996) The ecology and evolution of the New World non-pollinating fig wasp communities. J Biogeogr 23:447–458

Filariasis Disease caused by infection with nematodes (filarial worms), and transmitted by flies.  Dirofi lariasis  Onchocerciasis  Human Lymphatic Filariasis (Elephantiasis)

File A file-like ridge on the underside of the tegmina, near the base. The file is part of the stridulating mechanism in katydids and crickets.

Filiform Thread-like, slender, and nearly uniform in diameter. A term usually used in reference to antennae.  Antennae of Hexapods

Filter Chamber A modification of the gut in sap-feeding insects that allows much of the water and some of the

Filter Rearing System for Sterile Insect Technology

excess carbohydrate ingested by the insect to bypass the midgut, resulting in production of honeydew.  Alimentary Canal and Digestion

Filter Feeders Insects in aquatic communities that collect particulate matter from water with the aid of mouth brushes, leg brushes, or webs.

Filter Rearing System for Sterile Insect Technology Carlos Caceres International Atomic Energy Agency, Seibersdorf, Austria Genetic sexing strains (GSS), which produce only males, are now being used on a large scale for the control of the medfly, Ceratitis capitata using the sterile insect technique (SIT). The use of these strains has had a major impact on the overall efficiency of the technique by increasing significantly the amount of sterility induced in field populations and by reducing operational costs. GSS are based on the use of male linked chromosomal translocations, which make possible the linkage of selectable marker genes to the male sex. Two selectable genes have been incorporated into functional sexing strains specifically, white pupae (wp), which allows males and females to be discriminated based on pupal color, and temperature sensitive lethal (tsl), which allows the females to be killed by an increase in ambient temperature. GSS are not 100% stable due to the occurrence of a low level of genetic recombination between the selectable marker and the translocation breakpoint. This results in the loss of the sexing characteristics of the strain. The Filter Rearing System (FRS) was designed to solve the problem of genetic recombination (Fig. 19) when GSS are mass reared for

F

SIT programs. The principle of the FRS is to maintain a small colony of a GSS, with zero recombination, which can continually be amplified to rear a large colony from which males are produced for irradiation and release. In principle, the FRS creates a one-way system for production to ensure that any recombinants are not reintroduced into the colony. The FRS also has other applications for improving the quality of mass reared insects. In a GSS, males emerge from brown pupae and females from white pupae. In the filter, any flies emerging from the wrong colored pupae are removed every generation. Pupae are separated by color 2–3 days before adult emergence and individual pupae are placed in plastic grids with 100 holes/grid. The holes are 1 cm2. The grid is covered with a transparent plexiglass lid and the bottom of the grid is sealed with metal gauze. After adults have emerged, they are examined under a magnifying glass and recombinant individuals are killed with a burst of compressed air through the metallic grid. The adult flies emerging from the correct pupal color are transferred to a cage to start the amplification of the population for the subsequent release of sterilized males. Since it is impossible to screen the very large colonies for operational programs the FRS is based on the sequential amplification of a relatively small backup colony which is cleaned of recombinant individuals. The backup colony (Clean Stream) must be cleaned each generation, but must be large enough to produce sufficient offspring to provide for itself and to initiate the colony amplification sequence. The number of amplifications (Initiation and Injection Streams) depends upon the size of the backup colony in relation to the size of the final colony (Release Stream) required to produce the desired number of males for release, and the rate at which recombinants accumulate at each amplification stage. The FRS has now been introduced into all of the facilities rearing medfly GSS where it has been shown to be a viable and operational

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Filter Rearing System for Sterile Insect Technology

Adults from both sexes are cleaned and returned to Clean Stream

Clean Steam

20,000 females

Excess of material is sent to the ampilifications process

First amplification= 6X

Initiation Stream

123,000 females

Second amplification= 8X

Injection Stream

1 � 106 females

Third amplification= 8X

Release Stream

8 � 106 females

Apply thermal treatment to eggs to kill the females (34�C/12h)

Fourth Magnification= 13X

Expected sterile male Pupae weekly production = 100�106

Sterile male pupae to field release

Filter Rearing System for Sterile Insect Technology, Figure 19 The continuous Filter Rearing System (FRS) for medfly male-only production.

s ystem to guarantee the accurate production of only males (> 99.5% males) during release operations.

References Caceres C, Fisher K, Rendon P (2000) Mass rearing of the medfly temperature sensitive lethal genetic sexing strain

in Guatemala. In: Tan KH (ed) Area-wide control of fruit flies and other pests. Penerbit Universiti Sains Malaysia, Penang, Malaysia, pp 551–558 Fisher K, Caceres C, Rendon P (2000) A filter rearing system for mass reared sexing strains of Mediterranean fruit fly (Diptera: Tephritidae). In: Tan KH (ed) Area-wide control of fruit flies and other pests. Penerbit Universiti Sains Malaysia, Penang, Malaysia, pp 543–550 Robinson AS, Franz G, Fisher K (1999) Genetic sexing strains in the medfly, Ceratitis capitata: development, mass rearing and field applications. Trend Entomol 2:81–104

Filth Fly Parasitoids (Hymenoptera: Pteromalidae) in North America

Filth Fly Parasitoids (Hymenoptera: Pteromalidae) in North America Kevin D. Floate1, Gary A. P. Gibson2 Agriculture and Agri-Food Canada Lethbridge Research Centre, Lethbridge, AB, Canada 2 Agriculture and Agri-Food Canada Eastern Cereals and Oilseeds Research Centre, Ottawa, ON, Canada 1

Chalcidoid wasps (Hymenoptera: Chalcidoidea) of the family Pteromalidae comprise the principle parasitoids of pest flies (Diptera) associated with livestock. At least 15 native species of filth fly parasitoids have been identified and a few foreign species have been introduced into North America for classical biological control. Species reported to occur, or which may occur, in North America are listed in Table 2. Several surveys have been conducted throughout North America to determine species compositions, which appear to be influenced by climatic conditions. Species of Spalangia typically are associated with warmer regions and, with species of Muscidifurax, dominate the parasitoid complexes in the United States and parts of Canada. The nonchalcidoid species, Phygadeuon fumator Gravenhorst (Hymenoptera: Ichneumonidae), also is important in northeastern United States and Canada, and Trichomalopsis sarcophagae (Gahan) is common in Alberta, Canada. Microhabitat conditions, such as type of substrate, moisture and light levels also influence species composition within different regions. Natural levels of parasitism typically are low, with season-long values usually 25% of the leaf area eaten at the cotyledon to third true leaf stage. Economic thresholds at crop maturity have not been determined, but if oilseed pods are still green, heavy feeding on them may decrease seed yields or quality. In cole crop production, late feeding can cause cosmetic damage that will downgrade head quality. An average

Flea Beetles (Coleoptera: Chrysomelidae: Alticinae)

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flea beetle numbers, but may not be practical for agronomic reasons. Seeding rate and date does not significantly affect the abundance of new generation flea beetles. For cole vegetable and salad greens production, such cultural methods as the use of vigorous transplants, row covers, and exclusion fencing can protect seedlings physically until they become large enough to withstand feeding. Irrigation applied under warm, dry conditions may drown beetles when they are most active. Crop rotation and intercropping crucifers with plants from other families such as clovers, marigolds, or tomatoes may decrease flea beetle numbers. Protection of brassica greens such as arugula or bok choi from cosmetic damage may be necessary throughout the season, but is difficult by cultural means.

ematodes have been recorded attacking eight n Phyllotreta species in an intensive European study. The braconid wasp Townselitis bicolour (Wesm.) parasitized up to 50% of adult flea beetles in summer in Germany. Microsporidean, eugregarine, and nematode infections have been reported from Phyllotreta species in Sweden. In North America, crucifer flea beetles are attacked but not controlled by a suite of natural enemies, including predators such as lacewing (Chrysopa) larvae, big-eyed bug (Geocoris) sp., Collops vittatus Say beetles, and field crickets (Gryllus spp.). The native braconid wasp Microctonus vittatus Mues. normally parasitizes 300,000 named species), Lepidoptera (>120,000 species), Hymenoptera (>120,000 species), and Diptera (>150,000 species) containing the most species. Insects are diverse, numerous, and ancient. An understanding of their systematics and phylogeny will require the combined use of the fossil record, traditional morphological data, and molecular methods.

References Jarzembowski E, Ross A (1994) Progressive palaeontology. Antenna 18:123–126 Kukalova-Peck J (1991) Fossil history and the evolution of hexapod structures. In: The insects of Australia, 2nd edn. Melbourne University Press, Melbourne, Australia, vol 1, pp 141–179

Labandeira CC, Sepkoski JJ Jr (1993) Insect diversity in the fossil record. Science 261:310–315 Labandeira CC, Beall BS, Hueber FM (1988) Early insect diversification: evidence from a lower Devonian bristletail from Quebec. Science 242:913–916

Fossorial Adapted for digging; usually used in reference to legs.

Founder Effect The genetic pattern resulting from introduction of a small population into a new area, and the subsequent divergence from the parental stock. The new population, after a period of time, may no longer be compatible with the original population and is incapable of interbreeding.

Foundress Among social insects, a fertilized female that founds a new colony. All the offspring in the colony are the sons and daughters of the foundress.

Fourcroy, Antoine-François (Comte De) Antoine-François Fourcroy was born in France in 1755 and grew up in poverty. He studied medicine, assisted financially by a benefactor, and received a medical degree in 1780. He was appointed professor of chemistry in 1784 at the Jardin du Roi, later Jardin des Plantes, and still later Museum National d’ Histoire Naturelle in Paris. He worked with Lavoisier and others in studying chemicals of animal and plant products, classifying them, and reforming the system of chemical nomenclature. He published major works on chemistry in 1792 and 1801. He also was interested in the classification of animals, and published (1785)

Four-Legged Mites (Eriophyoidea or Tetrapodili)

“Entomologia Parisiensis; sive catalogus insectorum quae in agro Parisiensi reperiuntur; secundum method Geoffraeanam…” in two volumes; Geoffroy contributed descriptions of new species in pages 1–231 of the first volume. He was a strong supporter of the French revolution, held public offices in it, and became director-general of public education in 1901. In 1908, he was made a count, and became known as Antoine-François de Fourcroy. He died in 1809.

Reference Nordenskiöld E (1935) The history of biology: a survey. Tudor, New York, 629 pp

Four-Legged Mites (Eriophyoidea or Tetrapodili) Marjorie A. Hoy University of Florida, Gainesville, FL, USA The Eriophyoidea or Tetrapodili are unusual mites because they have only two pairs of legs as adults instead of the normal four pairs. Eriophyoid mites are second only to the spider mites in their economic importance as plant pests around the world. Eriophyoid mites are minute, and highly specialized to feed on plants. They are the smallest arthropods that feed on plants, averaging 100–500 μm in length and, despite their very small size which could lead to rapid water loss, some can survive in relatively exposed environments on leaves. The mouthparts of eriophyoids consist of a pair of stylet-like chelicerae and a pair of accessory stylets which are modified palps. The small size of the stylets allows eriophyids to penetrate only about 5 μm into the leaf, so feeding occurs in the plant epidermis (Fig. 84). The Eriophyoidea contain three families, the Phytoptidae (consisting of about 20 species of primitive forms often found on conifers), the Eriophyidae (consisting of about 85% of the known

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species) and the Diptilomiopidae (consisting of about 16 species that are vagrants on leaves). Approximately 3,000 species in 230 genera of eriophyoid mites have been described, yet the biology of many remains relatively unknown. Most eriophyoid females deposit eggs, from which larvae hatch. After larvae feed they enter a quiescent resting stage from which a nymph emerges and feeds. After another resting stage, adults emerge. The spheroid eggs are laid on leaves or on buds and very small (about 20–60 μm in diameter), but large in comparison to the size of the female depositing them. Immatures are similar to adults in appearance, but smaller and lacking external genitalia. The immatures of many species have never been studied. Adults consist of females and males, but females are more numerous and males of some species have not been found. Males are usually similar to females, although smaller. The basic life cycle consists of egg, larva, nymph, adult, but eriophyoids may have more complex life cycles, with two different types of adult females. Females of species in which there are two types of adult females are called protogyne and deutogyne. The protogyne female form usually is similar to that of the male. The second type of adult female is the deutogyne, and she often looks very different from the protogyne. This has created taxonomic confusion. This type of life cycle was discovered in the plum nursery mite, Aculus foceui; the deutogyne female is the overwintering or hibernating form of A. foceui, developing when the foliage begins to harden in the hottest part of the summer. Deutogynes do not deposit eggs prior to overwintering and have a different body form than the protogynes. In the buckeye rust mite, Tegonotus aesculifoliae, the two forms were sufficiently different that they were given different genus names. In general, the main differences between proto- and deutogynes is in the microtuberculation (shape of micro ridges on the exoskeleton, which are important taxonomic characters); deutogynes have a reduced microtuberculation, or the microtubercles are

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a different shape. Deutogynes appear to be adapted to survive adverse conditions perhaps because the reduced microtubercles limit water loss. Leaf hardening, particularly in the case of eriophyoid species that are leaf vagrants or rust mites, triggers the production of deutogynes in late spring or summer, usually in association with rising temperatures. In some species, particularly those in erinea or galls, the trigger is the onset of cool conditions in the fall of the year and the deutogynes appear later in the year. Deutogynes move off leaves into sheltered crevices on twigs, under bud scales, or other protected sites where they hibernate or aestivate. The deutogyne females mate prior to entering the protected sites and the males don’ t go with them. If females fail to mate, they produce only male progeny, indicating that they are arrhenotokous. Initially, it was assumed that deutogynes were produced only in those species that lived on

Microtubercle Legs Genital region

Four-Legged Mites (Eriophyoidea or Tetrapodili), Figure 84 Eriophyoid mites are wormlike, with only two pair of legs (right) close to the chelicerae, the piercing mouthparts. The posterior of the mite has anal pads that allow the mites to adhere to the leaf surface. The exoskeleton has distinctive microtubercles that are useful in identifying eriophyoids. The size and shape of these tubercles may differ between the two types of females, called protogynes and deutogynes, found in some species.

deciduous host plants. Later, however, it was discovered that deuterogyny occurs in species on evergreen plants and in species on tropical plants. The deutogynes in the tropical or subtropical species differ from the deutogynes in temperate climates. For example the mango-leaf-coating eriophyid, Cisaberoptus kenyae, is found on mango leaves and is widespread in the tropics; in C. kenyae, however, the deutogynes deposit eggs. In this species, the deutogyne is the commonest form seen and seems to tend the white coating, keeping the coating raised enough to provide space for other colony members. Finally, some species have less distinctive forms of deutogynes, making it difficult to resolve whether there are actually two types of females. It is possible that the less-distinctive deutogynes are suited for dispersal rather than hibernation or aestivation. Only a relatively few eriophyoid species have been studied in sufficient detail that their biology and ecology is well known. Eriophyoids disperse by walking, or are wind distributed. At least one, Aceria litchii, can be moved about on the bodies of honeybees after the bees forage in infested flower panicles of lychees in Australia. Eriophyoid mites can be transported easily on plant materials, as well. Wind dispersal in some species appears to be a matter of choice with mites assuming a distinctive upright posture to facilitate their aerial dispersal. Eriophyoids are called blister mites, rust mites, bud mites or gall mites because their feeding causes distinctive damage to plants (Table 8). Fusiform eriophyoids are found wandering on the leaf or bud surfaces of their hosts and are classified as rust mites or leaf vagrants. Examples include the citrus rust mite, a pest of citrus in many parts of the world. Soft bodied worm-like eriophyoids also are found within buds, in blisters, or in galls, and are called bud or gall mites. They are most often found on perennial plants and are generally quite host specific. In fact, eriophyoids are sufficiently host specific that a key is available that shows photographs of the damage on each host plant; this key allows one to identify the species in North


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Four-Legged Mites (Eriophyoidea or Tetrapodili), Table 8 Some eriophyoid mite species, their hosts, and damage in North America Host plant species

Mite species

Damage

Acer campestre, hedge maple

Eriophyes macrochelus

Leaf gall

Acer rubrum, red maple

Eriophyes major

Erineum, or hairy growth on leaf surface

Avena sativa, oats and other grasses

Eriophyes tulipae

Wheat-streak-mosaic virus disease

Carya illinoinensis, pecan

Eriophyes caryae

Leaf edge, spotting

Citrus spp., citrus

Phyllocoptruta oleivora

Bronzing, russeting of fruit, leaves and twigs

Eriophyes sheldoni

Deformed buds, flowers, fruit and leaves

Corylus avellana, hazelnut

Phytocoptella avellanae

Big bud or bud gall

Cynodon dactylon, Bermuda grass

Eriophyes cynodonis

Leaf blade and terminal shoot distortion

Eriophyes cynodoniensis

Leaf sheath and stem gall

Fagus grandifolia, American beech

Acalitus fagerinea

Erineum

Ficus carica, fig

Eriophyes ficus

Mosaic-virus disease

Fraxinus americana, white ash

Eriophyes chondriphora

Leaf gall

Gossypium spp., wild and cultivated cotton

Acalitus gossypii

Bud injury, foliage deformation, leaf blister

Juglans californica, California walnut

Eriophyes neobeevori

Catkin gall

Eriophyes brachytarsus

Leaf gall

Juglans nigra, black walnut

Eriophyes caulis

Petiole gall

Juglans regia, English walnut

Eriophyes erineus

Erineum

Lycopersicon lycopersicum, tomato also Datura, Petunia, nightshade and potato

Aculops lycopersici

Foliage browning, withering and fruit russeting

Malus pumila, apple

Calepitrimerus baileyi

Browning underside of leaves

Aculus schlechtendali

Injured terminal growth, leaf curl, russeting

Medicago sativa, alfalfa

Eriophyes medicaginis

Witch‘s broom

Pinus clausa, sand pine

Trisetacus floridanus

Aborted buds, rosette gall, stunted needles

Pinus monticola, Western white pine

Trisetacus alborum

ditto

Prunus domestica, plum

Acalitus phloeocoptes

Bud gall

Phytoptus emarginatae

Leaf gall

Quercus agrifolia, California live oak

Eriophyes paramackiei

Brooming at lower tree level

Eriophyes mackiei

Erineum

Rhus radicans, poison ivy

Aculops toxicophagus

Leaf gall

Tulipa sp., tulip

Eriophyes tulipae

Bulb damage

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Four-Legged Mites (Eriophyoidea or Tetrapodili), Table 8 Some eriophyoid mite species, their hosts, and damage in North America (Continued) Host plant species

Mite species

Damage

Vaccinium spp., blueberry

Acalitus vaccinii

Bud blister, rosette fruit deformation

Vitus spp., grape

Calepitrimerus vitus

Abnormal growth, bunched foliage, injured flowers, short internodes

Colmerus vitus

Deformed bud clusters and leaves, erineum

America (unless the mite is a new invasive pest). Even where two eriophyoids occur on a plant, their feeding damage and location on the plant usually is so distinctive that the different species can be discriminated easily. These very tiny mites cannot be seen readily on leaf surfaces without magnification, however. Because galls or blisters remain on leaves even after the mites have died or dispersed, feeding damage can be seen until the deciduous plant defoliates.

Leaf injury Injury caused by eriophyoid feeding affects the surface (epidermis) of the leaf because the stylets (modified chelicerae) of these mites are short. Damage to foliage may be quite specific to the mite and host plant: the peach rust mite, Vasates cornutus, causes browning or silvering of the peach leaf surfaces by its feeding. Aceria brachytarsus causes pocketing of leaf tissues (purse galls) on walnut leaves. Eriophyes pyri, the pear blister mite, invades the mesophyll of pear leaves and causes serious injury. Hairy patches, called erinea, on the underside of grape leaves infested with Eriophyes vitis represent open galls in which the pocketing of the leaf tissue is minimal. Eriophyoids also injure buds by feeding on their surface and can cause gall formation. The citrus bud mite, Aceria sheldoni, causes fruit and leaf malformation in California citrus groves. Eriophyoids also cause “witches broom” of twigs, flower galls, shortening of internodes, or secondary development of leaf hairs.

Vectors of Plant Disease Eriophyoids are vectors of plant viruses (poty viruses from the genus Rymovirus). Each virus has a limited host plant range and a single mite vector species usually is known for each virus. The best studied eriophyoid-virus relationship is the wheatstreak-mosaic virus and the wheat-spot-mosaic viruslike pathogen, both of which are transmitted by Eriophyes (= Aceria) tulipae. These viruses can be acquired after a few minutes of feeding, but longer access to plants results in higher transmission rates. Viruses are retained by the mites following a molt, but are not transovarially transmitted. The virus persists (Fig. 85) about one week at room temperature or for several weeks at lower temperatures in the vectors and must be acquired by one of the two nymphal stages if subsequent transmission by adults is to occur. Because adults cannot acquire and transmit virus, spread of the virus must originate from the original host of the individual mite. Dispersal of eriophyoids, and thus spread of virus, depends on temperature and wind. Although eriophyoids are wingless, during daylight hours they “stand up” on their anal papilla and allow themselves to be distributed by wind. Aceria tulipae transmits kernel-red streak of corn as well as wheat-spot, and wheat-streak mosaic viruses. Other important plant-disease vectors include: Aceria ficus transmits fig-mosaic virus; currantreversion virus is transmitted by Phytoptus ribis; peach-mosaic virus is transmitted by Eriophyes insidiosus; and ryegrass-mosaic virus is transmitted by Abacarus hystrix. The disease called “High Plains


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of the virus appears to include corn, wheat, barley, rye and oats, as well as cheat grass (Bromus secalinus) and yellow foxtail (Setaria glauca). The virus can be seedborne. Resistant cultivars have been identified and integrated pest management is possible using host plant resistance, elimination of v olunteer plants, isolation from small grains (sources of the virus and vector), and modification of planting date.

Some Major Pests Phyllocoptruta oleivora (Citrus Rust Mite)

Four-Legged Mites (Eriophyoidea or Tetrapodili), Figure 85 Citrus rust mite and damage. (above) Discoloration of oranges caused by citrus rust mite feeding. (middle) Citrus rust mites as seen under a light microscope. (below) Citrus rust mite killed by Hirsutella fungus as seen under a scanning electron microscope.

disease” is now known to be consistently associated with a virus and an eriophyoid mite, Aceria tosichella. Prior to 1993, no corn virus diseases were found in Colorado but a disease, initially diagnosed as wheat-streak mosaic, was found. The host range

The citrus rust mite is one of the most important and widespread citrus pests in the world. It reproduces rapidly and causes damage to the exterior of the fruit, which causes fresh market fruit to be downgraded. The interior quality of the fruit is not affected, so if the fruit is grown for juice, mite densities are less important. Citrus rust mite eggs are laid in groups in indentations on fruits and on the ventral surfaces of leaves. The life cycle requires about 7–10 days in summer and females live about 20 days, depositing 20–30 eggs. The mites do well in warm, humid conditions. Severely infested fruits have a powdery appearance as a result of the exuviae left behind by the molting immatures. Mites do not tolerate bright sunlight well, so they choose undersurfaces of leaves and shaded areas of the fruit, which can result in a typical damage pattern in these areas. Feeding damage affects only the surface of the fruit and damaged fruits become silver, reddish brown or purplish black depending on the mite density. The rust mite is able to colonize very young fruit and, thus, control measures should be applied early, if natural enemies such as predator mites or the fungal pathogen Hirsutella is not suppressing populations sufficiently. In South Africa, the predatory mite Amblyseius citri feeds on rust mite, although it is not fully effective. In Florida, the rust mite is controlled in part by the fungus Hirsutella thompsoni. Unfortunately, the fungus often is eliminated if sprays are applied to control fungal pathogens of citrus. The rust mite is thought to have

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originated in southeast Asia, but little information is available on the natural enemies of this pest there.

Aculus cornutus (Peach Silver Mite) This mite attacks peaches and almonds. The mites are found on leaves and their feeding causes the leaf surface to appear silvery when high populations are found. High densities can reduce tree growth and reduce fruit size. These mites can serve as prey for phytoseiid predators, such as the phytoseiid Metaseiulus occidentalis in California almond orchards, and thus rarely becomes a pest in almond orchards where these predators are abundant.

Aculops lycopersici (Tomato Rust Mite) Tomato rust mites are pests of tomatoes around the world. Unlike many other eriophyoid mite species, the tomato rust mite attacks various plant species in the family Solanaceae. It can easily kill tomato plants and damages peppers, potatoes, egg plants, tobacco, and petunias. It is often found on Ipomoea purpurea (morning glory) in field margins. The morning glory is a natural host and these weeds can serve as a reservoir of the pest. Tomato rust mites are dispersed by the wind and also by farm workers and agricultural tools. When the tomato plant begins to die, the rust mites migrate to the top of the plant, holding their bodies perpendicular to the leaf surface and adhering to the surface by the anal lobes. In this posture, they are more likely to be blown off the leaf surface. On occasion they form chains by crawling up each other to disperse. Tomato rust mites prefer warm weather and are able to feed on the upper surfaces of leaves in direct sunlight. Symptoms of rust mite damage on tomatoes include: bronzing of leaves, withering, and change of stem color from green to brown. Defoliation takes place, so eventually only young growth remains. The fruits are then sunburned, plant growth is slowed, and fruit production is reduced. If the fruits are attacked, the skin

becomes brown. On potatoes, the tomato rust mite does not cause browning, but the leaves may become dry and the whole plant can die. Sulfur dusts or oils can be used to control the tomato rust mite.

Aculus schlechtendali (Apple Rust Mite) These mites feed on flowers, fruits and leaves of apple. It causes apple leaves to roll up longitudinally and become rusty brown on the lower side and russeting of fruit. Aculus schlechtendali is considered a beneficial species in Washington apple orchards under an integrated mite management program because these mites serve as prey for the predatory phytoseiid Metaseiulus (= Typhlodromus or Galendromus) occidentalis. Apple rust mites provide alternative food for these important and effective predators early in the growing season and allow predator populations to increase so they can suppress the spider mite pests (Panonychus ulmi and Tetranychus spp.) on apples later in the growing season. Apple rust mite populations must become relatively large before they cause significant damage. Likewise, in the northeastern USA, A. schlechtendali is an alternative food source for the phytoseiid Typhlodromus pyri early in the growing season; this phytoseiid is an important predator of European red mite, Panonychus ulmi, in this apple-growing area.

Pesticides and Pesticide Resistance Various insecticides, fungicides and miticides (acaricides) can be used to control eriophyoid mite pests. Generally, oils and sulfur are effective and have been used against eriophyoid mites for many years, although care must be taken to avoid phytotoxicity from both products. Eriophyoid mite populations that are exposed to repeated and consistent applications of pesticides can develop a genetically based resistance to particular products. For example, some populations of the peach silver mite (Aculus cornutus) in


North America have become resistant to organophosphorous insecticides, and the apple rust mite (Aculus schlechtendali) in British Columbia and Washington state in the USA has become resistant to a variety of pesticides used in apple orchards. Likewise, the pear rust mite (Epitrimerus pyri) in Washington state is resistant to various pesticides. In citrus groves around the world, the citrus rust mite (Phyllocoptruta oleivora) has become resistant to several pesticides, including zineb, dicofol and chlorobenzilate, making control difficult. Developing effective management programs for these agricultural pests may require several tactics in order to delay the development of resistance in eriophyoid pest populations.

Invasive Species The small size of eriophyoids makes them easy to transport on fruits and foliage without detection and eriophyoids can invade new geographic regions regularly. For example, the eriophyoid Tegolophus perseaflorae was found recently in flowers and fruits of avocado in Dade County, Florida. The mites feed on buds, causing necrotic spots on apical leaves and subcircular, irregular openings on mature leaves. Mites are also found on petioles and the undersides of leaves and fruitlets. The feeding causes fruit deformation and discoloration. It was speculated that avocado grafting material was the source of this new pest.

Biological Control of Weeds by Eriophyoids Not all eriophyoids are considered pests. Many species remain unnoticed, while others are used for biological control of weeds. Attributes that contribute to their success as natural enemies of weeds include: eriophyoids are often host-specific, even to the level of race of plant and host tissue they attack. They are easily distributed by the wind; they can be used with other biological control

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agents; and some species are able to transmit specific plant viruses to the weed. Negative aspects include the fact that they are relatively slow-acting and must often be used in conjunction with other natural enemies. They are also quite sensitive to low relative humidities because of their small size. The eriophyoid Aceria chrondrillae has been used in the biological control of the Eurasian rush skeleton weed, Chrondrilla juncea, in Australia and in the USA. Feeding on skeleton weed induces gall formation in the vegetative and flower buds, causing plant stunting, reduction in seed formation and weakness. Mites appear to be very specific to particular geographic races of the weed; a strain originating from Greece was most suitable against the weed in Australia, but this strain did not perform well in the USA. An Italian strain has been introduced to control the weed population in the USA. Other eriophyoids have been considered as control agents of weeds, including Aceria acroptiloni which suppressed Russian knapweed (Centaurea repens) and was introduced into the Crimea from Central Asia. Aceria centaureae and A. thessalonicae have been evaluated for control of diffuse knapweed (Centaurea diffusa) in the USA and Canada. Eriophyes boycei was shipped from the USA to Russia for ragweed (Ambrosia spp.) control and Aceria convolvuli has been released for control of field bindweed (Convolvulus arvensis) in the USA. The European St. John’s wort, Hypericum perforatum, is a weed in eastern Australia and, although the defoliating beetle Chrysolina quadrigeminata has become established and provides substantial control, the mite Aculus hyperici has been evaluated as an additional natural enemy. Host specificity trials indicate that A. hyperici is specific to the genus Hypericum. Other species of eriophyoid mites could become useful natural enemies of weeds once additional information on their taxonomy, host range, and detrimental effects on target weeds have been obtained. In addition, the combination of a host-specific eriophyoid mite as a vector of a specific viral disease of the weed could result in enhanced biological control of weeds.

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Fovea

Identification of Eriophyoids If you know the plant species and the location of the mite on the plant, you are likely to be able to identify the eriophyoid mite to species. For example, it is usually possible to identify North American eriophyoids without having to use a key because a list of host plants, symptoms of injury, and mite species in North America is available. Of course, this method won’t work if the eriophyoid you are trying to identify is a new pest in the USA.

References Keifer HH, Baker EW, Kono T, Delfinado M, Styer WE (1982) An illustrated guide to plant abnormalities caused by eriophyid mites in North America. USDA handbook 573, 178 pp Lindquist EE, Sabelis MW, Bruin J (1996) Eriophyoid mites. Their biology, natural enemies and control, Elsevier Science, vol 6. Amsterdam, The Netherlands, 822 pp Nault LR (1997) Arthropod transmission of plant viruses: a new synthesis. Ann Entomol Soc Am 90:521–541 Oldfield GN (1970) Mite transmission of plant viruses. Ann Rev Entomol 15:343–380

Fovea A deep pit or depression on the integument of insects. A small pit is called a “foveola.” Surfaces bearing fovea or foveola are said to be “foveolate.”

Frass Whitney Cranshaw Colorado State University, Ft. Collins, CO, USA Frass is the solid excrement (fecal material) produced by various insects that feed on wood, foliage and other solid materials. Frass is produced in various shapes (Fig. 86), and moisture content varies with the diet. It is commonly produced in pellet form by various leaf-feeding caterpillars, sawflies

Frass, Figure 86 Frass, or excrement, can be of diagnostic value. Above is termite frass p roduced by subterranean termites; note that it has i rregular edges and is dry. Middle image is moist frass produced by the blue cactus borer, and extruded from the tunnel by the larva; it is very moist. Bottom image is frass from d rywood termites; it is produced in smooth-edged pellets and is very dry. (Termite frass photos by J.L. Castner, University of Florida; cactus borer frass photo by J.L. Capinera, University of Florida.)

Fringe-Winged Beetles

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and beetles, and the shape can be diagnostic of certain genera. The term is probably more widely used to describe excrement produced by various wood boring beetles and certain termites.

Frenate Bearing a frenulum.

Frenular Hook A hook or fold into which the frenulum is fitted. This structure occurs in the males of some Lepidoptera.  Wings of Insects

Frenulum A spine-like process in Lepidoptera in which the spine arises from the base of the hind wing, protrudes beneath the forewing, and serves to couple the fore- and hind wings during flight.  Wings of Insects

Fringe-Tufted Moths (Lepidoptera: Epermeniidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Fringe-tufted moths, family Epermeniidae, total 102 species, with many being Palearctic (36 sp.) and Australian (23 sp.). There are two subfamilies: Epermeniinae and Ochromolopinae. The family is part of the superfamily Copromorphoidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small (8–20 mm wingspan), with head smooth-scaled; haustellum naked; labial palpi upturned; maxillary palpi 3-segmented. Wings narrow, with fringes longer on hindwings

Fringe-Tufted Moths (Lepidoptera: E permeniidae), Figure 87 Example of fringe-tufted moths (Epermeniidae), Sinicaepermenia taiwanella Heppner from Taiwan.

and scale tufts on forewing margin (Fig. 87). Maculation rather somber shades of brown, with various mostly darker markings. Adults are diurnal or crepuscular. Larvae are leafminers, leaf skeletonizers, or borers of seeds, fruits, or buds; a few are gall makers. Host records include several plant families.

References Buszko J, Skalski AW (1980) Epermeniidae, Schreckensteiniidae. In: Klucze do Oznaczania Owadów Polski. 27. Motyle – Lepidoptera,22–23:1–35.Polskie Towardzystwo Entomologiczne [in Polish] Gaedike R (1966) Die Genitalien der europäischen Epermeniidae (Lepidoptera: Epermeniidae). Beiträge zur Entomologie 16:633–692 Gaedike R (1976) Die Epermeniidae der äthiopischen Region (Lepidoptera). Beiträge zur Entomologie 26:451–454 Gaedike R (1977) de Revision der nearktischen und neotropischen Epermeniidae (Lepidoptera). Beiträge zur Entomologie 27:301–312 Gaedike R (1996) de Epermeniidae. In: Lepidopterorum Catalogus, (n.s.). Fasc 48 [47] Association for Tropical Lepidoptera, Gainesville, 20 pp

Fringe-Winged Beetles Members of the family Clambidae (order Coleoptera).  Beetles

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Frisch, K. Von

Frisch, K. Von Karl von Frisch was born in Vienna on November 20, 1886. After his schooling, he entered Universität Wien to study medicine, at the insistence of his father, although he preferred zoology. After 3 years of study in Vienna, his father relented and allowed him to transfer to Munich to study zoology. Now with a degree, he returned to Vienna in 1909 as a graduate student. In 1910 he was awarded a Ph.D. for a thesis on color changes in fishes. He returned to Munich as assistant professor of zoology, was promoted to associate professor by 1912. During World War I he worked at a Red Cross hospital in Vienna. In 1921 he became professor and director of the zoological institute of Universität Rostock, in 1923 he moved to a similar position at Breslau (now Wroclaw in Poland), and in 1925 he returned to Munich. That last city was heavily damaged in World War II, and he transferred to Graz in Austria. However, in 1950 he returned to Munich to help reconstruct the institute. His official retirement was in 1958, but he continued to publish research results until shortly before he died. He performed research and published on sensory physiology and animal behavior, producing 158 papers and 16 books. His best-known work is on the means by which bees navigate and communicate. His book (English edition 1966), “The dancing bee” and (English edition 1967) “Dance language and the orientation of bees” gained him much acclaim. His awards included a Nobel prize, six honorary doctorates, the Austrian medal of honor, and many others. He died on June 12, 1982.

Reference Fergusson NDM (1983) Karl von Frisch, 1886–1982. Antenna 7:63

Frit Fly, Oscinella frit (L.) (Diptera: Chloropidae) This insect damages the stem of wheat plants, principally in Europe.  Wheat Pests and Their Management

Frivaldszky, Imre George Hangay Narrabeen, NSW, Australia Imre Frivaldszky was born on the 6th of February 1799 at Bacskó, in Zemplén Shire, Hungary. He began his studies in the highly regarded Piarist C ollege in Sátoraljaújhely where he met the greatest Hungarian botanists of the time. During the many botanical excursions his interest toward natural history deepened and although in 1816 he enrolled as a student in the Budapest University of Medical Sciences, he spent most of his spare time outdoors, studying plants and animals. In 1823, he was awarded with the Doctor of Medicine degree, but he never became a practitioner. Instead, he devoted his life to natural history, especially to the study of Coleoptera. He became a curator of the Hungarian National Museum’s natural history section, and he spent the first 10 years in this office by surveying the flora of the country. The resulting collection was outstanding by European standards, but Frivaldszky – and consequently Hungarian science - benefited even more from this work, as during the years of plant collecting, he gradually became a committed entomologist. In 1838 he was admitted into the Hungarian Academy of Science. His achievements in entomology were awarded by many learned societies in Hungary and abroad, and in 1847 he became the Director of the Hungarian National Museum. He expa nded his sphere of interest to other countries as well. He organised a number of collecting expeditions to the Balkans, the Near East, the Mediterranean region and the neighbouring lands. His last expedition, at the age of 74, took him to Turkey. Shortly after this journey, on the 19th of October 1870, he passed away. Frivaldszky’s life achievement was not only a huge natural history collection that formed the backbone of the museum, but also his tremendous fundamental work, which established entomology as a science in his country. His impetus to Hungarian

Froggatt, Walter Wilson

entomology was so great that it was unparalleled for almost a century, until Zoltán Kaszab’s directorship begun in the Hungarian Natural History Museum.

References Balázs D (ed) (1993) Magyar utazók lexikona. Panoráma. Budapest, Hungary, pp 126–127 Szinnyei J (1980) Magyar írók élete és munkái. I-XIV. 1891–1914 Budapest, Facsimile edition. Budapest, Hungary

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szerzeményeknek, melyekkel Xántus János az MNM állattani osztályát gazdagította. Pest, 1865.). Later in his life he studied ornithology and produced a concise work on the avifauna of Hungary (Aves Hungariae (Magyarország madarai). Budapest, 1891.). In recognition of his life-time achievements in zoology he was admitted in to the Hungarian Academy of Science, first as a corresponding member in 1865 and finally in 1875 as full member. He passed away on the 29th of March 1895 in Budapest.

Reference Frivaldszky, János George Hangay Narrabeen, NSW, Australia János Frivaldszky was born on the 17th of June 1822, at Rajec, in Trencsén Shire, Hungary. He was introduced to natural history at an early age by his uncle, Imre Frivaldszky. He completed his formal studies at the University of Technology and received his diploma of engineering. But, he didn’t become an engineer, instead choosing the study of zoology as his life-long career. He assisted his uncle in the processing and researching of the various collections brought back from his expeditions and became an expert entomologist and conservator. From 1850 onwards he often acted in his frequently sick uncle’s museum position. Upon Imre Frivaldszky’s retirement, in 1852 he became the assistant director of the Hungarian National Museum’s Zoological Collections. János Frivaldszky was especially interested in the arthropods of Hungary and he set out to survey the country’s fauna, with special attention to cave dwelling organisms. Due to his labors the museum’s collections and entomological knowledge of the Hungarian fauna increased considerably. When the great collections of János Xántus arrived at the museum, Frivaldszky curated them and published the results (Rövid vázlata azon

Horváth G (1897) Emlékbeszéd Frivaldszky Jánosról. Akadémiai Értekezések, VIII. Budapest, Hungary

Froggatt, Walter Wilson George Hangay Narrabeen, NSW, Australia Walter Wilson Froggatt was born in 1858 in Melbourne, Australia. He had a keen interest in natural history, especially entomology, and led the adventurous life of a professional collector. In 1885 he joined the Royal Geographical Society’s New Guinea Expedition and not much after that he was employed by Sir William John Macleay as a collector. Beginning in April 1887 he spent more than a year in the wildest parts of northwest Australia, working for Macleay. He spent most of his life in the field, either as a free-lance entomologist or in the service of institutes, museums or private collectors. Usually he traveled alone either by horse or on foot, carrying his equipment and supplies. He collected an enormous number of specimens, which are distributed amongst the many collections in Australia and overseas. In 1907, he published a popular book, the “Australian Insects” and in 1923 another on “Forest Insects of Australia.” He was an avid writer, producing a record number of published entomological articles. From 1923 until 1927

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Froghoppers

Front The front of the head capsule, below the base of the antennae and above the mouth parts. This is also called the frons (Fig. 89).  Head of Hexapods

Frontal Suture

Froggatt, Walter Wilson, Figure 88 William Froggatt.

he was Forest Entomologist (Fig. 88) of the New South Wales Forestry Commission. He passed away in 1937 in Croydon, New South Wales, Australia. Froggatt had a remarkably adventuresome life and he is remembered as a pioneer of Australian Entomology.

References Froggatt WW (1934) A Naturalist in Kimberley in 1887. Aus Nat 9:69–92 Walkom AB (1942) Walter Wilson Froggatt (1858–1937) Proc Linn Soc NSW 67:77–81 Wilson FE (1929) The Froggatt entomological collection. Vic Nat 45:117–119

Froghoppers Members of the family Cercopidae (order Hemiptera).  Bugs

Frons The front of the head capsule, below the base of the antennae (Fig. 89) and above the mouth parts. This is also called the front.  Head of Hexapods

A suture shaped like an inverted “U,” with the base of the “U” positioned just above the antennal bases and the arms of the “U” extending downward.  Head of Hexapods

Frugivory Feeding on fruit. Such arthropods are said to be frugivorous or frugivores.  Food Habits of Insects

Fruit Flies (Diptera: Tephritidae) Gary J. Steck Florida State Collection of Arthropods, Gainesville, FL, USA The family Tephritidae is a member of the large and phylogenetically complicated group known as acalyptrate flies. Order: Diptera Suborder: Brachycera Infraorder: Muscomorpha Section: Schizophora Subsection: Acalyptratae Superfamily: Tephritoidea

Other families included in the same superfamily are Lonchaeidae, Pallopteridae, Piophilidae, Platystomatidae, Pyrgotidae, Richardiidae, and Ulidiidae (= Otitidae). The family comprises over 4,300 described species, which are distributed throughout temperate and tropical regions of the world. The Tephritidae may be further subdivided into six subfamilies,

Fruit Flies (Diptera: Tephritidae)

Vertex

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Flagellum Antenna

Frons

Pedicel Scape

Median ocellus

Face Anterior tentorior pit Basimandibular sclerite Frontoclypeal suture Clypeolabral suture

Mandible Clypeus Labrum

Maxillary palpus Maxilla Labial palpus

Frons, Figure 89 Front view of the head of an adult grasshopper, showing some major elements.

Tachiniscinae, Blepharoneurinae, Phytalmiinae, Trypetinae, Dacinae, and Tephritinae. Only the subfamilies Trypetinae and Tephritinae are represented in all of the major biogeographic regions. Other insects are sometimes called “fruit flies,” particularly the Drosophilidae, but they are not closely related.

Adult One of the prominent features of the family is the presence in females of a chitinized ovipositor sheath and a needle-like ovipositor that allows them to oviposit into healthy plant tissues. Most species have “picture wings” that are prominently patterned with stripes or spots, and bodies with strongly contrasting colors, such as yellow stripes or spots on a dark background, as in species of Toxotrypana, which likely mimic wasps, or bold black stripes on the wings, as in some species of Rhagoletis and Zonosemata, that mimic jumping spiders. Identification to species level in some groups, including important pest groups such as

Anastrepha, relies on features specific to the female sex (ovipositor). Sexual dimorphism is common, in which males may be ornamented with specialized combs or bristles on the legs (e.g., some Ceratitis species) or elaborate antler-like projections on the head (e.g., some Phytalmia species). Adult size varies from about 2–25 mm in length.

Immature stages Eggs are typically white and elongate-cylindrical, sometimes with long, tail-like extensions. The egg stage lasts only a few days for most species. Active feeding and growth occurs during three larval instars inside the host plant tissues. Body shapes range from vermiform in stem-mining species to globose in gall-makers. Identification to genus or species level usually requires knowledge of the host and may be possible using characteristics of the spiracles, the cephalic segment and various surface features. Larvae may pupate inside the host plant, as is common in many flower infesters and gall makers, or they may exit the host to pupate in the soil, as is typical for most fruit infesters.

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Plant Relationships The family Tephritidae is best known for its pest species that attack a wide array of commercial and wild fruits and vegetables in many different plant families (Figs. 90 and 91). However, the great majority of species are not pests, and the majority are not even fruit infesters. Over half of the members of the family use non-fruit plant tissues as larval feeding sites. These include a large number of flower and seed feeders, and also gall-makers, and stem- and leaf-miners that infest members of the plant family Asteraceae. Members of the tribe Gastrozonini breed in bamboo stems. A few saprophagous and parasitic species are also known.

to the host plant, which may be used as a meeting site for males and females and may be a defendable resource for males. Males of many species display territorial behavior on the host plants and some engage in “boxing” matches to defend them. Lek-like mating aggregations, in which males compete for females, have been described for a number of fruit infesters including the Mediterranean fruit fly, Ceratitis capitata (Figs. 90 and 91). Many other aspects of fly behavior are also tightly linked to their host plants, for example, dispersal, feeding, pheromone release and response,

Life History The duration and timing of the various life stages of tephritid flies depend on their host plant relationships. Many polyphagous, tropical fruit infesters, for example, breed year round, and have long-lived (several months) adults that are able to use a series of different host fruits for oviposition; their egg to pupa stages last only a few weeks, and all life stages are present simultaneously and throughout the year. Other species, both temperate and tropical, are restricted to a single host plant, they are univoltine, and most of their developmental stages are of short duration and synchronized. The adult flight period lasts only a few weeks during the period when the appropriate developmental stage of its host plant is available for ovi position. For most such species, most of the year is passed in the pupal stage. Some temperate species undergo obligatory diapause in the pupal stage that may last for several years.

Fruit Flies (Diptera: Tephritidae), Figure 90 Oriental fruit fly, Bactrocera dorsalis.

Behavior Courtship and mating behavior are very complex and elaborate in some species and may continue for hours. The behavior of many species is linked

Fruit Flies (Diptera: Tephritidae), Figure 91 Mediterranean fruit fly, Ceratitis capitata.


viposition, and co-occurrence of other tephritid o species that utilize the same host plant.

Control Because of their economic importance, a great deal of effort has gone into study of the biology, genetics and control of pest species. The sterile insect technique (SIT) is widely used in population suppression and eradication programs, especially for the Mediterranean fruit fly. This involves mass rearing of fruit flies, sometimes by the hundreds of millions and sometimes using genetically modified all-male strains, followed by irradiation during the pupal stage to induce sterility. These flies are released into infested areas where sterile males outnumber their wild, fertile counterparts, thus reducing the number of successful matings and limiting population growth or even driving the population to extinction. Another control/eradication technique, known as “male annihilation,” is based on attraction of males to highly potent parapheromones, such as methyl eugenol.“Bait stations” using a mixture of the attractant and an insecticide can quickly remove most or all males from a population and drive it to extinction. This technique has been used very successfully against the Oriental fruit fly, Bactrocera dorsalis. Classical biological control using hymenopteran parasitoids that attack the immature stages of fruit flies has been used with varying degrees of success.

Evolutionary Studies The genus Rhagoletis has figured prominently in studies of evolutionary biology as a possible model of sympatric speciation. Because the mating, phenology, and biology of tephritid flies is so tightly linked to their host plants, it has been proposed that a shift in host-plant relationships could effectively isolate subpopulations even within a geographic area and lead to genetically distinct host races and ultimately to separate species.

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Importance to Humans Nearly all known members of the family are intimately associated with their host plant taxa, which serve as a feeding substrate for the larval stages. For this reason, many species of Tephritidae are highly damaging plant pests, and are widely known as “fruit flies.” Some of the most important genera and examples of fruit and vegetable pest species are: Anastrepha with over 200 species occurring in the Americas, including A. fraterculus, the South American fruit fly, and A. ludens, the Mexican fruit fly; Bactrocera with over 500 species mostly in tropical Asia, Australia and islands of the Pacific Ocean, including B. dorsalis, the Oriental fruit fly, B. cucurbitae, the melon fly, and B. oleae, the olive fly; Ceratitis with about 80 species, all African in origin, including C. capitata, the Mediterranean fruit fly; Dacus with about 250 species, mostly African, including D. bivittatus, the pumpkin fly; Rhagoletis with more than 60 species, mostly Holarctic, but also present in Central and South America, including R. pomonella, the apple maggot; and Toxotrypana with 13 or more species in tropical America, including T. curvicauda, the papaya fruit fly. Some tephritid host plants are invasive weeds with severe impact especially in pasture and rangelands. Various tephritid flies whose larvae feed on buds or seeds or produce galls have been intentionally promulgated into these weed populations as biological control agents, for example various Urophora species that attack thistles.  Mediterranean Fruit Fly  Melon Fly

References Aluja M, Norrbom AL (eds) (1999) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton, FL Foote RH, Blanc FL, Norrbom AL (1993) Handbook of the fruit flies (Diptera: Tephritidae) of America north of Mexico. Cornell University Press, Ithaca, New York Robinson AS, Hooper G (eds) (1989) In: Helle W (ed) Fruit flies. Their biology, natural enemies, and control. World crop pests, vol 3(A) & vol 3(B). Elsevier, Amsterdam, The Netherlands

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Fruit Stalk Borer, Oryectes elegans Prell (Coleoptera: Scarabaeidae)

Tan KH (ed) (2000) Area-wide control of fruit flies and other insect pests. Penerbit Universiti Sains Malaysia, Pulau Pinang, Malaysia Thompson FC (ed) (1999) Fruit fly expert identification system and systematic information database, Myia, vol 9. Backhuys Publishers, Leiden, The Netherlands White IM, Elson-Harris M (1992) Fruit flies of economic significance: their identification and bionomics. International Institute of Entomology, London, UK

Fruit Stalk Borer, Oryectes elegans Prell (Coleoptera: Scarabaeidae) Yousif Aldryhim King Saud University, Riyadh, Saudi Arabia The fruit stalk borer is found in the Arabian Peninsula as well as in Iraq and Iran. The adult is a stoutly built rhinoceros beetle that is shiny and reddish brown in color. The body length is about 34–36 mm in the female and 28–34 mm in the male. Adults have a horn-like structure on the head which is longer in females. The dorsum of the first thoracic segment has a depression that is deep and large in the female and shallow and small in the male. Mature larvae are about 55–65 mm in length, creamy white in color with brown heads, curved in shape and the last three abdominal segments are thicker than the remaining segments. Two cellulose destroying fungi, Chaetomium elatum and C. murorum, are found in the frass of fruit stalk borer larvae. The adults hide during the day in damp, organic soils. The adults are attracted to light from April to September and do great damage by boring through the leaf-bases and stems of inflorescences in the crown of the tree.

Importance and Damage The importance of the fruit stalk borer as a pest varies from year to year. It causes severe damage in damp and neglected fields. The adults cause more damage than the larvae. However, the larvae may

cause a huge cavity in the infested trunk that will ultimately cause its collapse. The adults make surface mines in the midrib of the fronds and the fruit stalks. Attacked fruit stalks may be broken or the fruits may be small and droop and shrivel. The adults also make holes at the base of the growing heart leaves and enter the stem. The larvae do not cause real damage unless they are numerous in one trunk. The larvae also feed on decomposing materials in the soil. There are other problems that the stalk borer might cause. The most common one is the tapered cut (crosscut) at the lower part of the fruit stalk fruit. However, it was reported from the United States of America, Pakistan, Iraq and a few other countries in the Middle East that these cuts are due to a physiological disorder. Another problem is the detachment of the fruit stalk from the growing point of the tree. There is no strong evidence that such damage is caused by the fruit stalk borer.

Biology The life-cycle of the fruit stalk borer may require more than 1 year. Females start laying eggs a week after emergence. The eggs are laid singly in wet soil around the roots of date palm trees or on rotten trunks. The eggs that are laid in early spring may reach the adult stage in autumn, while those laid later may reach the adult stage the following spring. The larval stage may take up to 10 months. Pupal longevity is up to three weeks.

Control In most cases, there is no need for control. But under certain conditions such as high humidity due to rainfall, the fruit stalk borer may cause serious damage. Also, damage by the fruit stalk borer facilitates entry by the red palm weevil, Rhynchophorus ferrugineus. A light trap can be used to reduce the number of flying adults, and to predict the occurrence of

Fulgoroidea

the fruit stalk borer outbreak. Most captures usually occur in April, a time when the greatest damage occurs. Food or shelter traps also can be used. These traps consist of wet organic materials mixed with wet, small pieces of date palm trunk covered by fronds. The adults are attracted to this trap in the early morning as a hiding place during the day, and females may even lay eggs in these traps. Pesticides may be added to the traps to kill the attracted adults.

References

naked; labial palpi porrect; maxillary palpi 1-segmented. Wing venation has reduction of two median veins in the hindwings and hindwings somewhat pointed apically. Maculation shades of gray and brown on forewings, plus some scale tufts; hindwings mostly pale. Adults are nocturnal or crepuscular. Larvae are borers in fruits, seeds, buds, or trunks and limbs, but a few are leafminers. Hosts include a variety of plants. A few species are economic.

References

Talhouk N (1984) The most common agricultural pests in Saudi Arabia. Ministry of Agriculture and Water, 121 pp (in Arabic) Hussain A (1974) Pests of date palm trees and dates in Iraq. Bagdad University, 190 pp (in Arabic) Hammad SM, Kadous AA (1989) Studies on the biology and ecology of date palm pests in the eastern Province of Saudi Arabia. Research Grants Program, Technical Report No 25. KACST, Riyadh, Saudi Arabia, 142 pp

Fruitworm Beetles Members of Coleoptera).  Beetles

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the

family

Byturidae

Cho S, Park KT (1990) The systematics of Korean Carposinidae (Lepidoptera). Insecta Koreana 7:87–103 Davis DR (1969) A revision of American moths of the family Carposinidae (Lepidoptera: Carposinoidea). Bull United States Natl Mus 289:1–105 Diakonoff AN (1989) Revision of the Palaearctic Carposinidae with description of a new genus and new species (Lepidoptera: Pyraloidea). Zool Verhandlingen 251:1–155 Kuznetsov VI (1986) Carposinidae. In: Identification Keys to Insects of European Russia. 4. Lepidoptera, 3:18–25 Academie Nauk [in Russian], St. Petersburg Zimmerman EC (1978) Carposinidae In: Insects of Hawaii 9:792–876

(order

Fruitworm Moths (Lepidoptera: Carposinidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Fruitworm moths, family Carposinidae, total about 279 species from all regions, but most are Australian and South Pacific. The family is part of the superfamily Copromorphoidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small to medium (10–40 mm wingspan), with head smooth-scaled; haustellum

Fulgoridae A family of insects in the superfamily Fulgoroidae (order Hemiptera). They sometimes are called planthoppers.  Bugs

Fulgoroidea A superfamily of insects in the order Hemiptera. Included in this superfamily are families such as Delphacidae, Derbidae, Cixiidae, Kinnaridae, Dictyopharidae, Fulgoridae, Acilidae, Tropiduchidae, Flatidae, Acanalonidae, and Issidae. They sometimes are called planthoppers.  Bugs

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Fuller Rose Beetle, Asynonychus godmani (Crotch) (Coleoptera: Curculionidae)

Fuller Rose Beetle, Asynonychus godmani (Crotch) (Coleoptera: Curculionidae) Though not a serious pest, this species affects the ability of North American citrus producers to ship their products.  Citrus Pests and Their Management

Fumigant A liquid or solid chemical that forms toxic gas or vapor upon exposure to air, and is used to disperse insecticide in difficult-to-penetrate substrates such as stored grain and soil.

Fumigation Treatment that uses a pesticide applied in a gaseous form.

Functional Genomics Study of what traits/functions are conferred on an organism by specific DNA sequences. Typically functional genomics occurs after the DNA sequences have been identified.

Functional Response A behavioral response of predators or parasitoids to the presence of prey. Searching and prey handling behavior is modified, resulting in increased efficiency of prey destruction. Learning, and more active search in the presence of prey, are implicated in functional responses. (contrast with numerical response)

Fundatrix (pl., fundatrigeniae) In aphids, the stem mother or first viviparous parthenogenetic generation developing from the fertilized egg.  Aphids

Fungal Pathogens of Insects Donald C. Steinkraus University of Arkansas, Fayetteville, AR, USA Fungi are eukaryotic, heterotrophic, absorptive organisms. Most grow vegetatively as fine hyphal filaments and reproduce by means of spores. Fungi are vital parts of ecosystems, often playing a valuable role in decomposition. They include common important organisms such as bread and wine yeasts, edible mushrooms, the causative agents of ringworm and athlete’s foot, and fungi which produce antibiotics such as penicillin. The classification of fungi is complicated and still imperfectly understood. Many different classifications and names have been proposed. Current authorities place the fungi in their own Kingdom, the Fungi or Eumycota. There are more than 56,000 described species placed in four phyla: the Ascomycota, Basidiomycota, the Chytridiomycota, and the Zygomycota. The Deuteromycota is an additional informal polyphyletic phylum. Aquatic entomopathogenic fungi, such as Lagenidium (Oomycota) that infect aquatic insects, are no longer considered fungi by some mycologists and are placed in the Kingdom Chromista. Modern classification schemes no longer consider the Oomycota to be a phylum in the Fungi, but instead members of the Kingdom Chromista. Fungi and insects interact symbiotically in many ways including mutualism, parasitism, commensalism, and predation. Some insects are totally dependent on fungi for their food. For instance, the leaf-cutting ants Acromyrmex and Atta spp., and termites in the Macrotermitinae, are mutualists with the fungi Attamyces and Termitomyces,

Fungal Pathogens of Insects

respectively. These important groups of insects are utterly dependent on fungi for their survival, and similarly, these fungal species are found only in association with their insect “farmers.” On the other hand, many fungi exploit and “feed” on insects. Such fungi are called pathogens and are the subject of this section (Table 9). Fungal entomopathogens are microorganisms that are capable of causing disease in otherwise healthy host insects. They possess the ability to

invade, reproduce in, and escape from a host, while overcoming or avoiding the host’s defenses. In order to do this, fungal pathogens have spores that are able to mechanically and enzymatically penetrate an insect’s exoskeleton, and vegetative hyphae that can survive and grow within a host. After killing a host, the fungus produces spores that are dispersed to new hosts. Often fungi that have little or no ability to infect living healthy insects are found growing on dead insects. These are called

Fungal Pathogens of Insects, Table 9 Simplified classification of entomopathogenic fungi and their arthropod hosts Phylum/Order Oomycota Lagenidiales Saprolegniales Chytridiomycota Blastocladiales Zygomycota Entomophthorales

Basidiomycota Septobasidiales Ascomycota Laboulbeniales Ascosphaerales Sphaeriales Deuteromycota Sphaeropsidales Moniliales

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Genus Lagenidium Leptolegnia

Hosts mosquito larvae mosquito larvae

Coelomomyces Coelomycidium Conidiobolus Entomophaga Entomophthora Erynia Massospora Neozygites Strongwellsea Zoophthora Septobasidium many genera Ascosphaera Cordyceps Aschersonia Beauveria Hirsutella Metarhizium Nomuraea Paecilomyces Verticillium

mosquito larvae black fly larvae aphids and others moths, grasshoppers adult flies, aphids many insects periodical cicadas aphids, thrips, mites adult flies many insects scales many insects bee larvae many insects scales and whiteflies many insects mites and scales many insects Lepidoptera larvae many insects aphids, whiteflies

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saprophytic fungi. Most microbial pathogens, such as viruses, protozoa and bacteria, enter the host via the mouth during ingestion, an entry method called per os. Fungi, along with certain nematodes, have the ability to directly penetrate the exoskeleton of an arthropod. This makes the fungi particularly important pathogens of insects such as aphids, cicadas, and other sucking insects that do not chew leaves and other substrates, and are, therefore, unlikely to ingest microbial pathogens.

Life Cycle and Invasion of the Host The life cycle of fungal pathogens begins with a spore. Spores vary in size and shape, and these characteristics are important in determining the species of a fungus. When a spore contacts a suitable host, it attaches to the host integument, forms an appressorium, and penetrates the insect’s integument via a germ tube or penetration peg. Usually, enzymes are produced by the spore to soften or dissolve the insect’s cuticle, then a germ tube mechanically penetrates the host’s exoskeleton. This can be a complicated process. In some fungal species, adhesion of spores is non-specific, while in others the spores “recognize” an appropriate host’s integument and begin the germination process. Once inside the host, the fungus grows vegetatively as filaments, called hyphae, or as yeast-like hyphal bodies. Within 3–7 days, the fungus has filled the host’s body cavity (hemocoel), resulting in the host’s death. Fungal toxins are sometimes involved, particularly with Beauveria and Metarhizium. Beauveria produces a number of toxic metabolites: beauvericin, a cyclic depsipeptide which is toxic to mosquito larvae; bassianolide, which is toxic to lepidopteran larvae; and cyclosporin, an immunosuppressant. Metarhizium produces toxins called destruxins that can paralyze insect larvae. Usually after the host’s death, the fungus produces spore-bearing hyphae called conidiophores that grow out of the host. Depending on the fungal species, spores are either explosively discharged (as in the Zygomycota: Entomophthorales) or are

passively discharged (as in the Deuteromycota and Ascomycota). In some genera, such as Massospora in periodical cicadas and Strongwellsea in various adult flies, conidia (spores) are produced while the host is still living and mobile. The host in such cases helps disseminate the pathogen.

Epizootics, Biological Control, and Population Regulation Fungal pathogens that prey on insects often cause readily observed epizootics. An epizootic is defined as an unexpectedly large proportion of diseased insects in a population. Fungal epizootics are often spectacular because: (i) large numbers of insects may be killed; (ii) insects killed by fungi are frequently held in elevated sites by fungal holdfasts; (iii) fungi sporulating on insect hosts are often colorful (white, green, or other colors); and (iv) because insects killed by fungi are usually firm, mummified, and persist for days to months. Because fungal pathogens kill large numbers of many insect pests, they are frequently important regulators of insect populations and are valuable biological control agents. Fungi are among the most important natural enemies of arthropods such as gypsy moth larvae, periodical cicadas, whiteflies, aphids, spider mites, and many others (Table 10). Why are fungi so efficient at causing epizootics? First, because their life cycles are usually relatively short compared to the host; sometimes, as is the case with Neozygites fresenii, a pathogen of aphids, they kill the host within 3–4 days. Second, many spores, thousands to millions, are produced from each infected host. Third, because many entomopathogenic fungi have developed specialized structures, such as rhizoids, that fasten a host where the opportunities are maximized for spores to contact new hosts. Fourth, spores of many fungi are rapidly spread by air or water to new hosts. Importantly, many fungal pathogens (Figs. 92 and 93) of insects have a narrow host range, infecting insects in only a limited number of insect species. A limited host range is beneficial because


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Fungal Pathogens of Insects, Table 10 Examples of fungi that cause natural epizootics in important insects and mites Host

Host name

Fungal species

Twospotted spider mite

Tetranychus urticae

Neozygites floridana

Citrus rust mite

Phyllocoptruta

Hirsutella thompsonii

Caddisfly adults

Trichoptera

Erynia rhizospora

Gypsy moth larvae

Lymantria dispar

Entomophaga maimaiga

Grasshoppers

Acrididae

Entomophaga grylli

Aphids

Aphididae

Neozygites fresenii

Aphids

Aphididae

Erynia neoaphidis

Aphids

Aphididae

Condiobolus obscurus

Aphids

Aphididae

Entomophthora planchoniana

Periodical cicadas

Magicicada spp.

Massospora cicadina

House fly

Musca domestica

Entomophthora muscae

Mosquito larvae

Culicidae

Erynia aquatica

Mosquito larvae

Culicidae

Coelomomyces spp.

Mosquito larvae

Culicidae

Lagenidium spp.

Black fly larvae

Simuliidae

Coelomycidium spp.

Noctuid moths

Noctuidae

Nomuraea rileyi

Whiteflies

Aleyrodidae

Aschersonia aleyrodis

Diverse insects

Lepidoptera, Aleyrodidae

Paecilomyces spp.

Aphids, Whiteflies

Aphididae, Aleyrodidae

Verticillium lecanii

Honey bees

Apis mellifera

Ascosphaera apis

Solitary bees

Megachilidae

Ascosphaera aggregate

Diverse insects

Scarabaeidae, Formicidae

Cordyceps spp.

Alfalfa weevil

Hypera postica

Zoophthora phytonomi

non-target organisms such as plants, beneficial insects, and vertebrates are not harmed. Nearly all fungal pathogens of insects are safe for man, his animals and plants. For instance, Neozygites floridana and Hirsutella thompsonii have a host range limited to mites, Neozygites fresenii is limited to aphids, and Nomuraea rileyi is limited to lepidopteran larvae. However, fungal entomopathogens are not risk free. There are rare reports of Beauveria causing fatal respiratory infections in cold-blooded animals such as alligators and crocodiles, causing allergic reactions in people, and infections in the nasal passages of mammals. Beauveria does not grow well at temperatures above 37°C, which limits its dangers to mammals

and birds. Strains of entomopathogenic fungi that grow well at 37°C or above could pose risks and probably should not be used in biological control programs. Fungal species and structures within a species vary widely in their sensitivity to, and ability to survive, environmental conditions such as temperature, relative humidity, and sunlight. Conidia are relatively short-lived in the environment. Therefore, many fungi have the capability to produce longer-lived, environmentally resistant spores, called resting spores. In some cases these can remain viable for years before infecting a host. Fungal pathogens also can survive in the mummified bodies of their hosts (Fig. 92).

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Fungal Pathogens of Insects, Figure 92 Some insect pathogens: (upper left) Larvae of the Indian meal moth, Plodia interpunctella (Pyralidae). The top larva was inoculated with spores of Paecilomyces sp. (Deuteromycota: Hyphomycetes) and the lower larva was not inoculated. Note the black spots on the integument of the inoculated larva. Each spot represents a melanization defense response of the host to the penetration activity of a Paecilomyces spore. This is one example of host defenses against infection;


Ecology Entomopathogenic fungi occur in many habitats, including lakes, streams, ponds, snowpools, woodlands, tropical rain forests, agricultural landscapes, and the soil. Lagenidium giganteum (Oomycota) is highly pathogenic to mosquito larvae. Lagenidium produces motile zoospores that encyst on the cuticle of young mosquito larvae, and penetrate mechanically and enzymatically into the host hemocoel. Mosquito larvae defend themselves by producing melanin at the encystment sites. Mycelia of Lagenidium fills the body of the mosquito larva, breaking down the host tissues with fungal protease enzymes. No toxins are thought to be involved. Other fungal

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pathogens occur adjacent to aquatic habitats. Erynia rhizospora is a pathogen of adult Trichoptera; Erynia conica attacks various adult Tipulids and Chironomids; Erynia curvispora attacks black fly adults; and E. aquatica is a pathogen of mosquito pupae and adults. Frequently, infected insects can be discovered attached to rocks and logs near streams, waterfalls, and lakes (Fig. 93). Forests, both tropical and temperate, are habitats for a variety of entomopathogenic fungi. Cordyceps spp. are fascinating pathogens of many insects in tropical and subtropical forests. These Ascomycota produce interesting club-like fruiting bodies (stromata) that emerge from infected hosts (often larvae or pupae of

(upper right) A house fly, Musca domestica (Muscidae), killed by and held to a window by the fungus, Entomophthora schizophorae (Zygomycota: Entomophthorales). When the fly died, specialized hyphal rhizoids (fungal holdfasts) grew out of the mouthparts of the fly and glued it to the glass. Then spore-bearing hyphae grew out of the host and produced thousands of spores (primary conidia) that were explosively discharged and are visible as a white halo around the dead fly. Fungal-mediated changes in host behavior and structures, such as holding the host in an elevated position, improve the odds of spores contacting new hosts; (second row left) Conidia of Erynia aquatica (Zygomycota: Entomophthorales), a pathogen of mosquitoes. Each spore is about 35 μm long. Note the difference in size and shape compared to the conidia of Entomophaga grylli; (second row right) Primary conidia of the grasshopper pathogen, Entomophaga grylli (Zygomycota: Entomophthorales). These spores are about 30 μm long. The shape and size of fungal spores are important characters used in their identification; (third row left) Photomicrograph of spore-bearing hyphae (conidiophores) of E. schizophorae. At the tips of the conidiophores the primary conidia are formed and then explosively discharged into the air. Each conidium contains 5 nuclei and is about 23 μm long. Nuclei, visible within the conidiophore, move into the developing conidium, prior to conidial discharge; (third row right) Resting spores of E. aquatica. Thick-walled resting spores can remain viable in mud and debris near mosquito breeding sites during the winter, then germinate and infect mosquito larvae in the spring; (bottom left) Spores of Beauveria bassiana and other Deuteromycota tend to be smaller than those of the Entomophthorales. These conidia, still attached to their conidiophores, are about 2–4 μm and are globose in shape. The spores of the Deuteromycota, unlike the Entomophthorales, are not explosively discharged from the host into the air; (bottom right) Beauveria bassiana (Deuteromycota) is one of the most commonly encountered entomopathogenic fungi, particularly in soil insects. This fungus has a very wide host range (several hundred species of insects at least) and there are several commercial products based on it. Commercialization of B. bassiana is possible because it is easily cultured in vitro, its spores are relatively small and easily formulated, and it has a wide host range. The dead hosts, in this case house flies, are covered by a white layer of fungal spores and mycelium. Note the similar appearance of these infected flies. Host insects killed by entomopathogenic fungi usually do not present a shaggy appearance, like saprophytic fungi do.

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Fungal Pathogens of Insects, Figure 93 Some additional insect pathogens: (upper left) Entomophthora schizophorae causes epizootics in muscoid flies, especially the house fly. Like the grasshopper killed by E. grylli, hosts killed by E. schizophorae are held to substrates, in this case by fungal rhizoids that grow out of the mouthparts (the lobes of the labellum) of the fly. In addition, dead infected flies appear life-like, have raised wings, and the infected females are attractive to males, who will sometimes engage in copulation with dead females, with obvious implications for the spread of the pathogen. Here you see a male house fly copulating with a dead infected female; (upper right) Entomophthoralean fungi in the genus Erynia are commonly found infecting insects that occur in moist situations, such as along stream


Lepidoptera or Coleoptera) in the soil. In China, larvae of hepialid moths infected with Cordyceps sinensis have been collected and used medicinally for thousands of years. Especially important in the temperate forests of North America is the fungus Entomophaga maimaiga, which causes large-scale epizootics in larval populations of the gypsy moth, Lymantria dispar. This fungus is one of the most valuable natural enemies of this pest. Various other Entomophthorales cause epizootics in tent caterpillars, aphids, and other forest pests. In agricultural habitats, fungi play an important role in regulating populations of various pests: whiteflies are attacked by Aschersonia spp.; spider mites are attacked by Neozygites floridana; and citrus rust mites by Hirsutella thompsonii. Various lepidopteran larvae are frequently decimated on soybean by Nomuraea rileyi, while the alfalfa weevil, Hypera postica, is heavily attacked by Erynia phytonomi.

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Techniques for Studying Fungal Pathogens of Insects Identification of entomopathogenic fungi is best accomplished when the host species is known, the gross signs of the fungus on the host (such as color, texture, attachment structures) are noted, and when microscopic fungal structures (spores, rhizoids, hyphae, cystidia) are examined with a phase microscope. Small amounts of fungal material are removed from the host, using an insect pin or minuten mounted in a wooden dowel, placed in a mounting medium (such as lactophenol) on a glass slide under a coverslip. The coverslip may be sealed with nailpolish to make it semi-permanent. Phase microscopes (usually at 100–400x) are used to examine the spores (conidia), conidiophores (spore-bearing hyphae), rhizoids, hyphae or hyphal bodies, and other structures. The size, shape, and color of spores are particularly important in identification using appropriate keys.

banks, waterfalls, and lakes. Erynia aquatica infects mosquitoes (Culicidae) that breed in snow pools. Here you see a mosquito that died in the pupal stage from this fungus. The dead mosquito pupa floats on the water surface, the spores are discharged from the dead host, and infect newly emerged mosquito adults; (second row left) Pandora neoaphidis (Zygomycota: Entomophthorales) is one of the most important pathogens of aphids. These are green peach aphids, Myzus persicae, killed during an e pizootic of P. neoaphidis, in a spinach field. The infected aphids are held firmly to the leaf by fungal rhizoid holdfasts; (second row right) Metarhizium anisopliae (Deuteromycota) is a very common pathogen of soil insects and has a wide host range. The photograph shows a green June beetle larva, Cotinus nitida (Scarabaeidae), in its pupation chamber, killed by M. anisopliae. Note the white areas of hyphae where the fungus has not yet sporulated. The mature spores cover the host with millions of green spores; (bottom left) Nomuraea rileyi (Deuteromycota: Hyphomycetes) is a common pathogen of Lepidoptera larvae in southern field crops. Host larvae are covered with pale green spores. Note that this host larva, a soybean looper, is attached to a leaf, is firm, is covered with powdery light green masses of spores; (bottom center) Ascosphaera apis (Ascomycota: Ascosphaerales) causes chalkbrood in honey bee larvae (brood). The mummified bee larvae resemble pieces of chalk in front of the hive, hence the name chalkbrood. Note the firm, “preserved” appearance of the dead insect. Other diseases of bee larvae, such as American foulbrood, caused by a bacterium, result in the larva becoming “gooey” and having a foul smell; (bottom right) Entomophaga grylli attacks grasshoppers. Infected hosts often are found clinging to the tops of grasses, and the dead hosts appear to be alive. There are no fungal holdfasts produced. However, the fungus mysteriously makes its grasshopper victim tightly grasp a plant with its legs before it dies. Upon dissection, large numbers of resting spores were found within the host’s abdomen. Another Entomophaga sp., E. maimaiga, is the cause of major epizootics in gypsy moth larvae and is considered one of the most important natural enemies of this pest.

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Fungicide

Many entomopathogenic fungi can be cultured in vitro on mycological media, such as Sabouraud dextrose agar. Some such as Beauveria, Metarhizium, and Paecilomyces grow readily on media. Others such as Pandora neoaphidis and Erynia curvispora can be grown relatively easily in vitro, while others such as Entomophthora muscae are difficult to culture, and yet others, such as Neozygites fresenii are almost impossible to culture in vitro. Isolating pure cultures of entomopathogenic fungi can be difficult depending on the species of fungus involved and the state of the host. Contamination of cultures by bacteria or unwanted fungi is a frequent problem. Selective media, such as oatmeal agar amended with dodine, are frequently used to isolate fungi such as Beauveria, while Entomophthorales are frequently isolated on coagulated egg yolk media. Most media used for isolation include broad spectrum antibiotics such as tetracycline and streptomycin to reduce the chance for bacteria to contaminate the culture. Fungal spores can be transferred from the host to the culture media using a needle. One of the best methods to isolate Entomophthorales is to place the sterile isolation media above the host cadaver, so that conidia are discharged from the host onto the media surface above. Cultures can be preserved by regular serial transfers onto fresh media, by storing culture slants under a layer of sterile mineral oil, by freeze-drying, or in ultra cold freezers. The USDA maintains a collection of entomopathogenic fungal cultures called the USDA-ARS Collection of Entomopathogenic Fungal Cultures, in Ithaca, New York.  Pathogens of Whiteflies  Diseases of Grasshoppers and Locusts  Beauveria  Coelomomyces  Culicinomyces  Hirsutella  Metarhizium  Nomurea  Paecilomyces

 Trichomyces  Verticillium lecanii

References Boucias, DG, Pendland JC (1998) Principles of insect pathology, 1st edn. Kluwer, Boston, MA, pp 181–183 Lacey LA (ed) (1997) Manual of techniques in insect pathology. Academic Press, San Diego, CA Lacey LA, Kaya HK (2000) Field manual of techniques in invertebrate pathology. Kluwer, Boston, MA Keller S (1987) Arthropod-pathogenic Entomophthorales of Switzerland. I. Conidiobolus, Entomophaga and Entomophthora. Sydowia 40:122–167 Pell JK, Eilenberg J, Hajek AE, Steinkraus DC (2001) Biology, ecology, and pest management potential of Entomophthorales. In: Butt TM, Jackson C, Magan N (eds) Fungi as biocontrol agents, progress, problems and potential. CABI Publishing, Wallingford, UK, pp 71–153 Samson RA, Evans HC, Latgé JP (1988) Atlas of entomopathogenic fungi. Springer-Verlag, Berlin, Germany Steinkraus DC (2000) Documentation of naturally-occurring pathogens and their impact in agroecosystems. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology. Kluwer Academic, Dordrecht, The Netherlands, pp 303–320 Tanada Y, Kaya HK (1993) Insect pathology. Academic Press, San Diego, CA Wilding N, Collins NM, Hammond PM, Webber JF (eds) (1989) Insect-fungus interactions. Academic Press, London, UK

Fungicide A pesticide used to manage growth of fungi.

Fungivorous Feeding on fungi.

Fungivory Fungus or mushroom feeding. Such arthropods are said to be fungivorous or fungivores.  Food Habits of Insects

Fungus Gnats (Diptera: Mycetophilidae and Others)

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Fungus gnats (Mycetophilidae, Bolitophilidae, Ditomyiidae, Diadocidiidae, Keroplatidae, and Lygistorrhinidae) are a diverse and abundant group of insects in the order Diptera, suborder Nematocera. Adults are usually recognized by their hump-backed appearance, stout and elongate coxae and well-developed tibial spurs (Figs. 94–98 ). Fungus gnats are primarily forest dwellers but can

be found in a variety of ecosystems, often in association with fungal habitats, although most of their natural history secrets remain untold. They occur on all continents except Antarctica. The adults often attain large populations and play an important role in the food web of forest environments. Traditionally, fungus gnats have been treated as a single family, the Mycetophilidae, and along with Sciaridae (dark-winged fung,us gnats) and Cecidomyiidae (gall midges), make up the superfamily Sciaroidea, within the infraorder Bibionomorpha. Fungus gnats formerly placed in Mycetophilidae, however, have been shown to be composed of several distinct lineages that are now treated as six separate families: Mycetophilidae, Bolitophilidae, Ditomyiidae, Diadocidiidae, Keroplatidae, and Lygistorrhinidae. More families may be recognized in the near future as more study and greater understanding of the Heterotrichagroup taxa is developed. The Heterotricha-group is a heterogeneous assemblage of at least 12 genera

Fungus Gnats (Diptera: Mycetophilidae and Others), Figure 94 An adult male fungus gnat, Mycetophila sp. (Mycetophilidae) (photo by P.H. Kerr).

Fungus Gnats (Diptera: Mycetophilidae and Others), Figure 95 Adult male of Sceptonia johannseni Garrett (Mycetophilidae) (photo by P.H. Kerr).

Fungus Beetles Members of the family Anthribidae (order Coleoptera).  Beetles

Fungus Gnats (Diptera: Mycetophilidae and Others) Peter H. Kerr California Department of Food and Agriculture, Sacramento, CA, USA

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Fungus Gnats (Diptera: Mycetophilidae and Others), Figure 96 Adult female of Novakia miloi Kerr (Mycetophilidae) (photo by P.H. Kerr).

Fungus Gnats (Diptera: Mycetophilidae and Others), Figure 98 Adult male of Platyura pectoralis Coquillett (Keroplatidae) (photo by P.H. Kerr). Family: Mycetophilidae Family: Bolitophilidae Family: Ditomyiidae Family: Diadocidiidae Family: Keroplatidae Family: Lygistorrhinidae

Fungus Gnats (Diptera: Mycetophilidae and Others), Figure 97 Adult male of Macrocera sp. (Keroplatidae) (photo by P.H. Kerr).

that are now incertae sedis within the superfamily Sciaroidea. Order: Diptera Infraorder: Bibionomorpha Superfamily: Sciaroidea

In total, approximately 5,000 species of fungus gnats have been formally named and described. Mycetophilidae remains the largest family in terms of species number with approximately 3,500 species worldwide, in approximately 136 genera. Undoubtedly the number of fungus gnat species will increase significantly as more study is devoted to the family. The number of genera is also expected to increase. Currently, there are at least several genera that are widely suspected to be artificial groupings of two or more disparate lineages (e.g., Boletina, Dziedzickia,


Sciophila). These genera are in need of systematic revision. The largest genus, Mycetophila, contains over 700 species and is distributed worldwide. The Palearctic Region is the area of greatest fungus gnat diversity. This may be a result of heightened local interest and expertise in the group more than actual taxonomic diversity but it is interesting to note that in Europe, fungus gnat diversity does not increase as one approaches lower latitudes (a typical pattern for many groups) and it may be that in general, the temperate regions are more diverse for fungus gnats than the tropics. Currently, Finland has the richest fauna of Mycetophilidae recorded among the nations of Europe. In forested areas throughout the world, fungus gnats are both abundant and diverse. Even in North America, it is not uncommon for two dozen or more fungus gnat genera to be collected over the course of a season from a single Malaise trap. In Finland, one survey effort captured 209 different species of mycetophilid gnats in a single trap in one season. This represents over 30% of the entire mycetophilid species total recorded for Finland. Fungus gnats are sensitive to forestry practices however, and the diversity of gnats may be suppressed for many decades or even permanently after clear-cutting forests. As their name implies, most fungus gnats are dependent on fungi for their development, either in mushroom fruiting bodies themselves, in the ground on mycorrhizae, or in or on wood or decomposing hummus where they feed on fungal mycelia. Many species appear restricted to certain ecological or systematic groups of fungi. Furthermore, within a particular host fungus, there may be a succession of fungus gnat species that specialize in particular decomposition stages. However, fungus gnats are not restricted to fungal environments. Larvae have also reportedly been found in birds’ nests and mammals’ burrows (where they may be mycetophagous), and on algae, mosses, liverworts and possibly on lichens. Curiously, field mushrooms (Agaricus spp.) do not serve as hosts. Some larvae, such as members of the genus Leptomorphus (Mycetophilidae), spin webs underneath bracket fungi where fungal spores are caught and

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eaten. Some members of Keroplatidae (e.g., Asindulum and others) take this one step further and also spin webs to capture small living invertebrate prey. Possibly the most famous of all fungus gnat larvae, the New Zealand glow worm, Arachnocampa luminosa, is predaceous and uses its own bioluminescence to lure midges and other small flies into a sticky silk thread that the larva spins and hangs from overhanging rocks (e.g., in caves and hollows). The glow worm silk strands may be up to 50 cm long and are coated with sticky poisonous droplets that paralyze trapped prey so that the surrounding snares remain intact. Other keroplatids, such as some Orfelia spp. also have predaceous, bioluminescent larvae and may be found in caves in North America. Still other keroplatid larvae are associated with ant-plants. Perhaps most outlandish of all fungus gnat lifestyles is exhibited by the larva of Planarivora insignis (Keroplatidae), a Tasmanian species that lives endoparasitically in land planarians. Approximately 80% of fungus gnat hosts are still unknown. Fungus gnat larvae are usually slender and white, with ventral welts and a dark head capsule. Larvae pass through five instars. Development time for larvae may be rapid and passed in as little time as a week if the host fungus is ephemeral or in as long as 8–9 months for some keroplatids. Pupation usually takes place in the ground but may be within the host fungus or hanging from the host fungus in a web of salivary threads. The form of the cocoon is generally dependent on the pupal environment; the pupa is enclosed in a dense or weak cocoon or may be encased within a web, without a cocoon. Many cocoons may be found together within the tissue of non-deliquescent fungi. Fungus gnats may have several generations in summer and fall and generally overwinter in the larval or pupal stage, although some troglophilic species may overwinter as adults. Adults are slender to moderately robust flies that are black, brown, orange, yellow or a combination of these colors, and may have dark markings on the wings. Some are quite showy and probably mimic Hymenoptera (e.g., Platyura, Keroplatidae).

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Fungus Moths (Lepidoptera: Tineidae)

They range in size from 2 to 13.5 mm. Most are crepuscular. During the day, many species prefer moist dark places such as caves, overhanging stream banks, or cavities under tree roots. These areas often support dancing swarms of gnats. Sometimes species of several genera, in one or more families appear to swarm together and can be swept up in one motion with a collecting net. The adults of some genera, especially those with elongate mouthparts (e.g., Antlemon and Asindulum, Keroplatidae; Gnoriste, Mycetophilidae; Lygistorrhina, Lygistorrhinidae), presumably visit flowers to feed on nectar. Fungus gnats may be drawn to red or yellow pan traps and/or to light traps (mercury vapor or blacklight) by night. They may also be readily collected by sweeping in the appropriate habitat with an insect collecting net. However, the best way to collect high numbers of fungus gnats is by Malaise trapping. In the fossil record, the earliest fungus gnats appear in the late Jurassic, at least 150 million years ago. Fungus gnats are rare but already well diversified in Cretaceous ambers, and by the Eocene it appears they were quite abundant. Fungus gnats belonging to recent genera are relatively common in Baltic amber.

References Blagoderov V, Grimaldi D (2004) Fossil Sciaroidea (Diptera) in Cretaceous ambers, exclusive of Cecidomyiidae, Sciaridae, and Keroplatidae. Am Mus Novitates 3433:1–76 Hutson AM, Ackland DM, Kidd LN (1980) Mycetophilidae (Bolitophilinae, Ditomyiinae, Diadocidiinae, Keroplatinae, Sciophilinae and Manotinae) Diptera, Nematocera. Handbook for the Identification of British Insects Royal Entomological Society of London, vol 9(3), pp 1–109 Jaklovlev J, Siitonen J (2004) Finnish fungus gnats (Diptera, Mycetophilidae, etc.): faunistics, habitat requirements and threat status. Lammi Notes 30:3–7 Matile L (1990) Recherches sur la systematique et l’evolution des Keroplatidae (Diptera, Mycetophiloidea). Memoires du Museum National d’Histoire Naturelle Serie A Zoologie 148:1–682 Økland B (1994) Mycetophilidae (Diptera), an insect group vulnerable to forestry practices? A comparison of clearcut, managed and semi-natural spruce forests in southern Norway. Biodivers Conserv 3:68–85

Søli GE (1997) The adult morphology of Mycetophilidae (s. str.), with a tentative phylogeny of the family (Diptera, Sciaroidea). Entomol Scand Suppl 50:5–55 Vockeroth JR (1981) Mycetophilidae. In: McAlpine JF, Peterson BV, Shewell GE, Teskey HJ, Vockeroth JR, Wood DM (eds) Manual of nearctic Diptera, vol 1, Monograph 27. Research Branch Agriculture Canada, Ottawa, ON, pp 223–247

Fungus Moths (Lepidoptera: Tineidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Fungus moths (Fig. 99), family Tineidae, comprise the first very large family of Lepidoptera, with about 2,160 described species; actual world fauna probably exceeds 4,000 species. The family is part of the superfamily Tineoidea, in the section Tineina, subsection Tineina, of the division Ditrysia. The family is divided into 16 subfamilies (many have been considered as separate families by some specialists in the past): Euplocaminae, Myrmecozelinae, Harmacloninae, Meessiinae, Dryadaulinae, Scardiinae, Nemapogoninae, Tineinae, Setomorphinae, Perissomasticinae, Hapsiferinae, Hieroxestinae, Erechthiinae, Siloscinae, Stathmopolitinae, and Teichobiinae. Adults minute to medium size (5–54 mm wingspan), usually with rough head scaling (a few have smooth-scaled heads); haustellum naked (unscaled); maxillary palpi long, 5-segmented (rarely 3-segmented). Maculation mostly somber grays or brown shades, with various speckling spots, but some tropical species colorful (e.g., genus Coryptilum from Southeast Asia). Adults are nocturnal or crepuscular; rarely diurnal. Larval habits vary greatly, but most are detritus feeders, some making cases, tunnels, or silken tubes; also, odd groups are coprophagous, keratophagous, woolen feeders, and even myrmecophilous and termitophilous larvae are known. The smooth-headed and more colorful Hieroxestinae and related groups are leafminers. Included among Tineidae are some of the most well

Furanocoumarins

Fungus Moths (Lepidoptera: Tineidae), Figure 99 Example of fungus moths (Tineidae), Euplocamus ophisa (Cramer) from Albania.

known household pest species, such as clothes moths and grain moths.

References Davis DR (1978) The North American moths of the genera Phaeoses, Opogona, and Oinophila, with a discussion of their supergeneric affinities (Lepidoptera: Tineidae). Smithsonian Contrib Zool 282:1–39 Gozmány LA, Vári L (1973) The Tineidae of the Ethiopian region. Transvaal Mus Mem 18:1–238 Robinson GS (1979) Clothes-moths of the Tinea pellionella complex: a revision of the world’s species (Lepidoptera: Tineidae). Bull British Mus (Nat Hist), Entomology 38: 57–128. Robinson GS, Nielsen ES (1993) Tineid Genera of Australia. In: Monographs of Australian Lepidoptera, vol 2. CSIRO, Melbourne, 344 pp Zagulajev AK (1960–1979) Tineidae. In: Fauna USSR. Lepidoptera, 4(3):1–267 (1960); 4(2):1–424 (1964); 4(4):1–126 (1973); 4(6):1–408 (1979). Academie Nauk USSR, [in Russian], St. Petersburg

edicinal, public health, and environmental viewm points because of their high photobiological activity. Wavelengths in the near ultraviolet (i.e., UV-A: 320–380 nm) are the most effective spectra, even though furanocoumarins absorb relatively poorly in this region. Although plants containing photosensitizing furanocoumarins have been used by Indian and Egyptian civilizations for more than 3,000 years to treat certain skin disorders, it was only in the middle of the last century (late 1940s) that the photosensitizing and pigment-stimulating agents in these plants were identified. Extensive research on different aspects of furanocoumarins has been conducted since this discovery. Furanocoumarins are a group of heterocyclic compounds in which the furan ring is fused with coumarin. They arise in nature from two configurations of the basic tricyclic ring structure, e.g., linear (psoralen: e.g., xanthotoxin) and angular (isopsoralen: e.g., angelicin) (Fig. 100). Based on available data, the linear furanocoumarins are more biologically active than their angular analogs. Furthermore, substitutions that increase polarity of the molecules usually decrease the activity. Naturally occurring phototoxins are an integrated part of our environment and they are apparently used by plants as defense mechanisms against herbivores. For instance, the biosynthesis of furanocoumarins and polyacetylenes, which are well established as phytoalexins, are drastically enhanced following plant infection with pathogens.

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Furanocoumarins (or furocoumarins) are known to exert photodynamic action. Furanocoumarins are of special interest from entomological,

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OCH3

Furanocoumarins Cyrus Abivardi Swiss Federal Institute of Technology, Zurich, Switzerland

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Furanocoumarins, Figure 100 Chemical structure of two classes of furanocoumarins: above, linear (e.g., 8-methoxypsoralen, known as 8-MOP or xanthotoxin); below, angular (e.g., angelicin).

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Furanocoumarins

Occurrence in Plants Photoactive furanocoumarins have been isolated from at least a hundred plant species from eight families, including Apiaceae (Umbelliferae), Rutaceae, Leguminose (Papilionaceae), Moraceae, and Orchidaceae, but find their greatest diversity in the Apiaceae and Rutaceae. The seeds and roots are major sources of furanocoumarins in some of the clinically important plants species that are cultivated solely to obtain these photosensitizers.

Effects of Furanocoumarins Since the discovery of the photosensitizing and the pigment-stimulating activities of furanocoumarins in 1940, entomological, medicinal and veterinary medicinal aspects have been the focus of different investigations.

Insects Xanthotoxin, a linear furanocoumarin also known as 8-methoxypsoralen (or 8-MOP), was the first natural phototoxin that was shown to have insecticidal properties in 1978. When this compound was administered at a rate of 0.1% to the larvae of the southern armyworm (Spodoptera eridania), a low level of toxicity was observed. The activity was, however, greatly enhanced when the larvae were irradiated with near UV light. It also was shown that the southern armyworm will feed on carrot which does not contain furanocoumarins. It will not, however, feed on parsnip that does contain these compounds. A very low concentration of 8-methoxypsoralen has ovicidal activity against Drosophila melanogaster when exposed to light, but much higher concentrations are inactive in darkness. Studies on insects also have determined how furanocoumarin-tolerant species avoid phototoxicity. There are several mechanisms for the resistance of insects to photosensitizers. While dark coloration due to the deposition of melanin is

suggested to govern the resistance of Papilio machaon and Manducta sexta to phototoxic furanocoumarins, rapid metabolism of these toxins is considered to be the biochemical reason for Papilio machaon, P. polyxenes, Depressaria pastinacella and Pastinaca sativa to feed on umbelliferous host plants known to contain furanocoumarins. Nevertheless, the larvae of the furanocoumarinsensitive fall armyworm (Spodoptera frugiperda) which also metabolize linear furanocoumarins by similar pathways, fail to avoid the toxicity due to a slower metabolism.

Domestic Animals As early as 1946, it was suggested that ingestion of furanocoumarin-containing plants was a significant cause of photosensitization in domestic animals. For example, the furanocoumarin-containing plant spring parsley, Cymopterus watsonii, is a serious problem to domestic animals in the western USA, and Ammi majus is an important photosensitization source in cattle in the USA. While both cases involve severe blistering, the latter case also may lead to blindness. It is likely that most wildlife species have adapted through evolutionary pressures to avoid such plants. Nevertheless, it has been demonstrated that furanocoumarins, upon activation by light, are powerful antimicrobial agents, nematicides, molluscicides, piscicides, and powerful skin photosensitizers against humans and animals.

Photodynamic Therapy The various photobiological actions exhibited by furanocoumarins have contributed to their extensive range of actual and potential uses in human medicine. Xanthotoxin (8-MOP) plus UV light, known as PUVA therapy, is now the treatment of choice for severe psoriasis. PUVA therapy has also been potentially beneficial for treatment of numerous human disorders including mycosis, atopic

Furanocoumarins

dermatisis, herpes simplex and lymphoma. Studies have shown that DNA and RNA viruses, both enveloped and non-enveloped, in nearly all major virus families have been successfully inactivated by psoralen derivatives in tissue culture medium and in blood products such as serum. The only viruses resistant to psoralen inactivation observed to date are picornaviruses. There is evidence to suggest that this resistance is due to the failure of psoralen to penetrate the exceptionally dense coat of this virus. Inactivation of human hepatitis viruses (B and non-A and non-B: i.e., C) by 8-MOP was successful in an in vivo chimpanzee infectivity model (Fig. 101).

Mode of Action Although furanocoumarins are primarily known for their light-dependent activity, their biological activities in the absence of light, even though moderate, have also been demonstrated. They are, however, of special interest from agricultural, medicinal, public health, and environmental viewpoints for their highly photobiological activity. λ nm 200

UV-C

UV-BUV-A 300 400

VISIBLE 500 600 700

900

Epidermis

Dermis Subcutaneous Tissue

10% 20%

32%

1%

77%

65%

5%

21%

Furanocoumarins, Figure 101 Extent of penetration of ultraviolet (UV) and visible light into human skin. (Drawing from the late B.E. Johnson, Department of Dermatology, University of Dundee, Scotland, U.K., courtesy of Springer-Verlag and G. Moreno, R.H. Pottier, T.G. Truscott (eds.), 1988, Photosensitisation: molecular, cellular and medical aspects.)

F

Wavelengths in the near ultraviolet (320–360 nm) range are the most effective ones, even though the absorption of these compounds in this region is relatively poor. Psoralens readily pass through membrane structure (e.g., cell wall and virus coats), to photoreact preferentially with nucleic acids. Studies have shown that diadducts and mono-adducts (bound to a single pyrimidine) block nucleic acid replication and transcription. Consequently, the infectious quality of the virus is lot, while the surface and structure of the virus may remain largely unmodified. At least a major part of the photobiological actions of furanocoumarins results from their intercalation into the double helix of DNA where, upon light activation, they form cyclobutane adducts with pyrimidine bases. Although there is clearly no direct involvement of oxygen in this interaction, which is governed by the Type I reaction, photogeneration of singlet oxygen by furanocoumarins has also been well demonstrated. The latter reaction (Type II) which involves singlet oxygen, may potentially be responsible for enzyme inactivation and membrane disruption.

Risks and Benefits Associated With Furanocoumarins Photodynamic agents demonstrate a drastic increase in toxicity (usually 2–3 orders of magnitude) in the presence of UV-A or visible light. This is a property which should not be overlooked in assessment of toxicological data for the safety of these compounds. Although in the absence of light the oral LD50 for a furanocoumarin [i.e., xanthotoxin (8-MOP)] ranges between 300and 600 mg/kg body weight in rats, an oral dose of only about 1 mg/kg of body weight can be dangerous for humans with as little as 1 h of subsequent sunlight exposure. Phototoxicity symptoms include severe erythema followed by blistering and peeling of the skin. Fair-skinned individuals are much more likely to suffer sunburn and blistering reactions from furanocoumarin exposure than are more pigmented individuals.

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Furcate

The level of furanocoumarins in celery (originally 1 mg/kg) can increase about 100-fold if the celery is stressed or diseased. Many cases of contact photodermatitis have been reported in humans who have had dermal contact with furanocoumarin- containing plants. For example, celery pickers and handlers suffer from periodic outbreaks of celery dermatitis by the appearance of skin rashes on their arms when exposed to diseased celery. The causative agents have been identified as xanthotoxin (8-MOP) and trisoralen, which celery produces in response to “pink rot” infection with Sclerotina sclerotiorum. There is up to 25-fold increase of several photocarcinogenic furanocoumarins (including 8-MOP and psoralen used in PUVA therapy) in the roots of diseased parsnips when compared with those isolated from the roots of healthy plants. In some instances, the amounts are so high that mixed crystals of furanocoumarins can be detected on the surface of parsnip roots by light microscopy. Linear furanocoumarins such as psoralen derivatives, which are widespread in plants of the Umbelliferae family, are potent light-activated carcinogens and mutagens. Skin cancer in animals and probably in humans are known consequences of photosensitization with furanocoumarins. Xanthotoxin (8-MOP), as well as other naturally occurring photosensitizers such as cercosporin, hypericin, polyacetylenes and their thiophenes, may represent a hazard to health as they possess the ability to induce genetic damage and mutations.

Side Effects of Photodynamic Therapy Patients treated by photodynamic therapy normally suffer from different side effects of phototoxicity, such as nausea, hair loss, erythema, etc. In addition, numerous types of damage at the cellular level have been observed. For example, nuclear aberrations, single-strand breaks, interference with repair processes, DNA-protein cross-links, and injury to cell membrane, mitochondria and the nucleus have been documented.

Naturally occurring photosensitizers, such as 8-MOP, currently used in the treatment of psoriasis (PUVA therapy) also may represent a hazard to health as they possess the ability to induce genetic damage and mutations. Low concentrations of 8-MOP, mediated by UV-A, were sufficient to induce an increase in the frequency of chromosome aberrations in Syrian hamsters. There is no question that major changes occur to both tumor and surrounding normal microvasculature during and following photodynamic therapy. Changes to the endothelium, smooth muscle contraction and increased capillary permeability also have been observed during therapy. Thus, PUVA therapy should be used with caution.

References Ames BN (1983) Dietary carcinogens and anticarcinogens: oxygen radicals and degenerative diseases. Science 221:1256–1264 Blum HF (1964) Photodynamic action and diseases caused by light. Hafner Publishing Co, New York, NY, 309 pp Heitz JR, Downum KR (eds) (1987) Light-activated pesticides. ACS Symposium Series 339, Washington, DC, 339 pp Ivie GW (1978) Toxicological significance of plant furocoumarins. In: KeelerRF, van Kampen KR, James LF (eds) Effects of poisonous plants on livestock. Academic Press, London, UK, pp 475–485 North J, Neyndorff J, Levy JG (1993) Photosensitzers as virucidal agents. J Photochem Photobiol B 17:99–108 Young AR (1990) Photocarcinogenicity of psoralens used in PUVA treatment: present status in mouse and man. J Photochem Photobiol B 6:237–247

Furcate Having a forked appearance.

Furcula A forked structure found beneath the abdomen of springtails (Collembola), attached apically, and used for leaping (Fig. 102).  Abdomen of Hexapods

Fusiform

F

Furniture Beetles

Antenna Pretarsus Tibiotarsus Femur Trochanter

Eye Pronotum Mesonotum

Coxa Precoxae Collophore

Metanotum

An alternative name for beetles of the family Anobiidae, or death-watch beetles. They feed on dry substances such as cereal grains or wood, including furniture.  Beetles  Food Habits of Insects

Tenaculum (catch)

Fused This term usually is used to indicate structures that were once (in an evolutionary sense) separate, but are now joined, and lack indication of former separation.

Manubrium Dens Mucro

Furcula (spring)

Furcula, Figure 102 Lateral view of a springtail (Collembola).

Fusiform This term describes a structure that is widest at the midpoint, and narrowed at both ends.

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Gahan, Arthur Burton Arthur Gahan was born into a large farm family in Kansas on December 9, 1880. He attended Kansas State College, graduating in 1903. Then in 1904 he became assistant in the Department of Entomology of Maryland Agricultural Col lege, and received an M.S. from that institu tion in 1906. He remained there as Assistant Entomologist, becoming interested in “parasitic” Hymenoptera in general and braconid parasi toids of aphids in particular. In 1913 he accepted a position with the U.S. Department of Agricul ture, to work as a taxonomist at the U.S. National Museum. There, he worked on various groups of “parasitic” Hymenoptera, but ultimately concen trated on Chalcidoidea and became a leading authority of them and publishing copiously. He married in 1908, was active in civic affairs and the Entomological Society of Washington, becoming its president in 1922. He died on May 23, 1960, and was survived by his wife and two children.

Reference Mallis A (1971) Arthur Burton Gahan. In: American ento mologists. Rutgers University Press, New Brunswick, NJ, pp 373–374

Galápagos Islands Insects: Colonization, Structure, and Evolution Stewart B. Peck Carleton University, Ottawa, ON, Canada The Galápagos archipelago of Ecuador has an interesting insect fauna that is now rather well known. The archipelago is composed of 19 islands larger than 1 km2, with a total land area of 7,882 km2. It is the world’s only remaining tropical oceanic archipelago that is little altered by humans. The present islands, 800–1,000 km west of the Pacific coast of Ecuador, have been available for terres trial colonization for 3–4 million years. The archi pelago is a model system for assessing the dynamics of biotic dispersal to, and differentiation on, oce anic islands. They are a natural experiment which has been running in oceanic near-isolation for about 3 Ma. Each island (Fig. 1) is a replicate of an experiment in biotic dispersal, colonization, and differentiation. The present plants and animals can be seen to be a record of the successes in dispersal to the islands, and of the dynamics of their subse quent evolution in isolation. The story has been well (or even exhaustively) reported for many of the larger plants and vertebrates. This story, however, has not been well studied for the vast majority of insects and other terrestrial invertebrates.

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Galápagos Islands Insects: Colonization, Structure, and Evolution

Galápagos Islands Insects: Colonization, Structure, and Evolution, Figure 1 Map of Galápagos Archipelago.

The insect fauna (Tables 1 and 2) is now known to contain 23 of the world’s 31 orders of insects, with at least 255 families, 1,057 genera, and 1,853 species, of which 736+ are endemic, 818+ are indigenous, and 295+ are introduced. Within the beetles (Coleoptera), the islands have 56 fami lies, 297 genera, and 486 species (266 endemics, 110 indigenous, and 110 introduced species). The 376 native beetle species (indigenous and endemics combined) represent a rate of species accumulation of about one every 9,260 years (through successful colonization plus speciation through about 3.5 million years). Charles Darwin is known to have been a keen collector of insects and especially beetles. However, as he wrote in his 1845 book “Voyage

of the Beagle,” he was not impressed by the abundance or diversity of the insects of the Galápagos Archipelago. In fact, the entire biota of the Galápagos is generally not very impres sive in appearance. But there are a few excep tions and these have received exceptional publicity. Most of the organisms are, however, small or drab when compared with those of the luxuriant tropical forests of mainland South America. This is partly a reflection of the isola tion of the islands (800–1,000 km west of the coast of Ecuador), their youth (only 3–4 million years), the difficulty of dispersing to them, their seasonally harsh and semi-arid tropical climate, and the difficulty of establishment by colonizing species.


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Galápagos Islands Insects: Colonization, Structure, and Evolution, Table 1 Numbers of native (endemics plus indigenous) genera, species, and single-island endemic beetle diversity, arranged by increasing island size . The larger islands have more genera, more species, more single-island endemics, and more species per genus. These generalizations also occur in the rest of the native insects fauna Island

Area

Total native

Total native

Single-island species/

(km )

Genera

Species

Endemics

Genus ratio

Caamaño

0.045

9

10

0

1.11

Beagle

0.08

1

1

0

1.0

Campeón

0.095

16

16

0

1.0

Plazas Sur

0.119

17

17

0

1.0

Eden

0.23

8

8

0

1.0

Daphne Major

0.330

3

4

0

1.33

Gardner at Floreana

0.812

7

7

0

1.0

Darwin

1.063

15

15

2

1.0

Bartolomé

1.24

16

17

0

1.06

Tortuga

1.298

3

3

0

1.0

Wolf

1.344

17

17

2

1.0

Seymour

1.838

31

33

0

1.06

Rábida

4.993

46

48

0

1.04

Genovesa

14.10

44

48

2

1.09

Pinzón

18.15

42

44

2

1.05

Santa Fé

24.13

40

48

2

1.20

Baltra

26.19

28

32

0

1.14

Pinta

59.40

76

87

0

1.15

Española

60.48

55

65

4

1.18

Marchena

129.96

56

63

2

1.13

Floreana

172.53

114

141

5

1.24

San Cristóbal

528.09

123

153

17

1.24

Santiago

584.65

119

148

14

1.24

Fernandina

642.48

72

80

1

1.11

Santa Cruz

985.55

186

258

27

1.39

Isabela

4,588.0

158

205

24

1.30

2

Colonization Processes How do insects get to oceanic islands? The pro cesses of colonization and any subsequent evolu tion on islands can seldom be directly observed. Usually, they are deduced from an analysis of the distributional and ecological patterns of the

rganisms in conjunction with evolutionary and o ecological theory. There are two general groups of hypotheses about processes which place biotas on islands. One of these, the “Continental Drift” process of distribu tion of ancient biotas, is irrelevant for the Galapágos because of their geological youth and oceanic origin.

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Galápagos Islands Insects: Colonization, Structure, and Evolution, Table 2 Summary of numbers of species and native genera of the insect orders of the Galápagos islands. Some orders have a disproportionate number of introduced species, especially on the islands with human settlement. A figure of 1.00 in the column of native species/native genus ratios shows that there has been no speciation in many insect orders after the natural colonization event of a single species in each genus, and comparatively little in the other orders Order

Introduced

Native

Native

Species/Genus

Species

species

Genera

Ratio

Collembola

3

35

22

1.57

Diplura

1

2

2

1.00

Archeognatha

0

1

1

1.00

Thysanura

1

2

2

1.00

Odonata

0

8

7

1.14

Orthoptera

4

29

13

2.23

Mantodea

0

1

1

1.00

Blattodea

11

7

3

2.33

Isoptera

0

4

3

1.33

Dermaptera

4

3

2

1.50

Embioptera

1

1

1

1.00

Zoraptera

0

1

1

1.00

Psocoptera

14

26

22

1.18

Thysanoptera

8

42

42?

1.00?

Hemiptera

118

198

86

2.30

Phthiraptera

8

80?

40?

2.00?

Neuroptera

0

8

5

1.6

Strepsiptera

0

1

1

1.00

Siphonaptera

3

1

1

1.00

Coleoptera

111

378

226

1.67

Lepidoptera

64

±300?

160?

1.88?

Diptera

66

±200?

150?

1.33?

Hymenoptera

46

±250?

160?

1.56?

Thus, all terrestrial colonists have crossed the oce anic water gap by one of four general dispersal mechanisms. The method of dispersal is a property of all the ecological, behavioral, and physiological characteristics of the species and of its mode and frequency of transport opportunity. Colonization is a property of both the life history requirements of the species and the characteristics of the new environment.

Aerial Transport (Actively by Flight and/ or Passively by Wind) This probably accounts for about half of the insects of the Galápagos. The mean body size of Galápagos insects appears to be smaller than for a mainland Ecuadorian fauna (but measurements are available for neither). Darwin first noted the small size of the insect fauna. The smaller body size would support


the idea that the majority of the insect colonists were carried as flying individuals by winds. In contrast to its importance for insects, it may seem surprising that wind transport may account for only 9% of natural seed-plant colonizations of the Galápagos.

Marine Transport A significant component of the total insect fauna probably arrived on the sea surface, either on rafts of vegetation and flotsam or by floating them selves (as pleuston). This may be the most impor tant mode for most of the flightless terrestrial arthropods. For the insects themselves, it is esti mated that marine transport may also account for about half of the original colonists. Flightless or poorly flying groups of large-bodied beetles such as weevils and darkling beetles probably used this mode, as did millipedes, centipedes, terrestrial isopods, oribatid mites and others. Bostrichids, cerambycids and various other wood-boring and wood-associated beetles probably arrived by raft ing in wood as adults or immatures. Flightless Gerstaeckeria weevils may have arrived on rafting pieces of their Opuntia cactus host plants. Several groups of large-bodied wingless bee tles such as endemic Galapaganus weevils and the three genera of Darwin’s darkling beetles (genera of Tenebrionidae containing nine species that were first collected by Darwin: Stomion, Ammophorus, and Blapstinus) are represented by species that occur on more than one island. Such cases are usually within the older eastern and central group of islands. It is logical that these species originated (speciated) on one island and that they have then moved from this to another island, probably after being washed to sea during heavy El Niño rainstorms and floods.

Transport on or in Other Animals Insect ectoparasites, such as all of the 80 species of Phthiraptera (chewing bird-lice) and the 8 species

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of Hippoboscidae (louse flies, Diptera), as well as bird ticks, reptile ticks and chigger mites, undoubt edly arrived on their vertebrate hosts. Bird trans port has also been important for seed-plants, because it is estimated that 79% of the angio sperms arrived as propagules with birds, either on or in their feathers or in their digestive tracts. Raft ing terrestrial mammals and reptiles seem to have carried a few arachnid and insect ectoparasites. And invertebrate colonists themselves have also carried some of their own arthropod parasites. Examples are one strepsipteran (in leafhoppers), several dryinid wasps and some pipunculid flies (in leafhoppers). Among the beetles, there are two examples: one meloid blister beetle (on Xylocopa carpenter bees), and two rhipiphorid beetles (in wood-boring beetle larvae) probably arrived as parasitic immatures on or in their host insects. The parasitized bee hosts themselves probably arrived by rafting on floating wood and the hosts of the rhipiphorids in lumber imported for construction of buildings.

Human Mediated Transport Humans have intentionally introduced many domestic animals and agricultural or horticul tural plants to the Galápagos. Some of these have escaped and become feral. But there is only one example of the intentional introduction of an arthropod: the vedalia beetle (Coccinellidae) for the bio-control of the cottony cushion scale (Icerya purchasi, Hemiptera), an introduced pest. By 1998 there were at least 292 recognized exam ples of unintentional introductions of insect species and the number in 2004 was at 450 spe cies of introduced insects. Such species are here called introduced species, but the term “adven tive” has also been used for these. The first such introduced insect may have arrived with the first European landings of Bishop Tomas de Berlanga and his party in 1535, as Dermestes (dermestid) and Necrobia (clerid) beetles and cockroaches. These were all commonly associated with

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humans and stored products in their sailing ships. Pirates, who used the islands from shortly after the time of their discovery until the early 1700s, and whalers and sealers, from the mid 1700s to mid 1800s, may have brought an allecu lid beetle (and other dry-wood insects such as bark-beetles) in logs or firewood from the mainland. Ships transporting both supplies and tour ists have taken insects attracted to ships’ lights to and between the islands. The orders with the largest number of introduced species are Coleoptera, Hemiptera, Lepidoptera, and Dip tera. Some 111 beetle species are among the more commonly encountered species of insects introduced to date. Not all of the introduced species seem to have become permanently estab lished; some long-horned beetles have not been found since their original collection. The intro duced species occur in greatest diversity on the four large islands with permanent human settle ments. There is now a program of agricultural quarantine control and inspection of goods and materials coming into the Galápagos in an attempt to limit future introductions of alien arthropods.

Sources of the Colonists There is limited detailed data on the mainland distributions of either indigenous Galápagos insects or mainland sister species of the endemic species. The data now available seem to indicate that only a few of the Galápagos colonist insects came from southern South America (arid coastal Peru or Chile). Most of the faunal relationships are with the lowland semi-arid and seasonal Neotropics, along the Pacific coast from Mexico to Ecuador. The best phylogenetic and biogeo graphic analyses show a general biogeographic pattern of a western Neotropical source area and that the Galápagos species are relatively recently derived species.

Stochastic (Random) Processes in Colonization and Distribution Colonization is seldom strictly predictable or linear even if the islands themselves are relatively linear in age or geography. As an example, one would predict that insect colonization was first to San Cristóbal and Española, which are the oldest and most easterly islands, and that the other islands were colonized sequentially northwestward as stepping stones as they formed through time. Exceptions to these predicted patterns do exist. This shows the lack of absolute predictability in present distributions through the randomness of the processes of either past dispersal, or coloniza tion success, or extinction. For instance, the cara bid beetle genera Platynus and Scarites are on Isabela and San Cristóbal islands, and not on Santa Cruz, which lies between them. The indige nous carabid Halocoryza acapuliana Whitehead is known only from small and central Rabida Island. Neighbor islands are more likely to share endemic species. This is clear in a number of shared beetle species limited to island pairs such as Darwin and Wolf (the tenebrionid Stomion cribicollis Van Dyke and the weevil Galapaganus darwini Lanteri), and Marchena and Pinta (the tenebrionid Stomion rugosum Van Dyke). The isolation of Genovesa is evident in its failure to be colonized by flightless Ammophorus beetles and other insect groups. Flightless Galapaganus wee vils are seemingly absent from Pinta and Marchena. Pinzón is famous for not having the widespread palo santo tree (Bursera graveolens), but this island’s insects are not well enough known to evaluate a pattern of absence of insect species there. Randomness is evident in the fact that some colonizations have been across the archipelago (from one side of the archipelago to the other). Molecular data suggest that Pinta Island was colonized by tortoises by oceanic transport from Española, and cladistic analysis suggests the same pattern in flightless Stomion beetles.


Structure of the Insect Fauna An Unbalanced Fauna Insect representation at the family level in the Galá pagos is vastly different from that in the Neotropical fauna. The cause is the inequality of families in their ability to successfully complete both the sequential processes of dispersal and then colonization. When compared to the fauna of the Neotropical continen tal source area, it is evident that the Galápagos fauna is unbalanced (or disharmonic) and impoverished. This means that the taxonomic composition of the archipelago is significantly different in its makeup and proportions from that of the mainland. The probable reasons for the absence of many insect families, subfamilies, and tribes are diverse. Difficulties of long-distance over-water dispersal and colonization must lie at the core of the reasons. Long distance dispersal is unlikely for many taxa and the lack of diverse and suitable habitats in the Galápagos is of undoubted importance. The absence of suitable food plants or prey items is involved. The taxa which are present can be viewed as able disper salists, rugged colonists, and adaptable in acceptance of available microhabitats and food materials.

Trophic Generalists Colonization is probably easier for trophic general ists (scavengers and predators) than for herbivores which are more likely to be specialist feeders. Island insect faunas in general tend not to be as rich in herbivores as the faunas on continents. In Galápagos beetles there are more trophic generalists (scavengers and predators) than herbivores. However, in Het eropteran bugs, colonization of islands by herbivores seems to be more successful than by predators.

Trophic Specialists There is little evidence that Galápagos insects have narrow or restricted feeding niches. The few

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examples are Gerstaeckeria weevils which feed only on the tissues of Opuntia cactus, and some host specific seed feeding bruchids and scolytids. Ataenius scarabs, usually associated with herbivo rous mammal dung, feed on the dung of the herbivorous giant tortoises and land iguanas. This may or may not represent a shift to a new food type. Tortoise and land iguana dung appears similar to that of ungulates because it is mostly composed of poorly digested plant materials.

Ecological Escape Plant or animal colonists on islands may be eco logically “released” through escape from their con tinental herbivores, parasites, predators, and competitors. Many cases of escape from insect herbivores or predators must exist, but few are rec ognized. One example is the seed-producing legume plants which have escaped many (but not all) of their seed predator bruchid beetles. The bruchid Megacerus leucospilus (Sharp) feeds on the seeds of the widespread beach morning-glory Ipomoea pes-caprae in Central America, but the plant seems not to have this seed predator on the Galápagos.

Parthenogenesis If females of a species can reproduce without the presence of individuals of the male sex, the species is more likely to establish itself as a colonist. Several of the Galápagos insects are known to be parthe nogenetic. But there is no apparent evidence that this has been disproportionately important in the colonization of the Galápagos.

Vegetational Zonation and Diversity Terrestrial communities in the Galápagos are usu ally characterized according to the elevation- related (precipitation and temperature controlled)

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zonation of the flora. The archipelago may possess the strongest or most compressed floristic zonation to be found anywhere in the world, passing through its six major vegetation zones in an elevational rise of only about 700 m; the littoral, arid, transition, humid forest, evergreen shrub, and above-treeline fern-sedge (“pampa”) zones. Insect diversity also seems to display some zonation, with fewer species being known from the higher elevations. The arid zone has the largest area in the islands and the most native insect species. The other zones, at higher altitudes, have progressively less area and proportionally fewer species, but sampling has not been equivalent. This probably indicates that the arid zone has been a bigger target for colonization for a longer period of time. The introduced species are more evenly distributed in all zones. This might be a reflection of the more eurytopic (adaptable) nature of the introduced species. Plants also support diversity in that they pro vide various structural parts that may be fed upon by feeding specialists. Host-specific plant-feeding insects could be expected to exhibit the same zonation as their hosts, but almost all Galápagos phytophagous insects seem to feed on several spe cies of host plant. Data for genus and family-level host-plant diversity are not available. Host speci ficity, to be expected in groups which elsewhere are usually monophagous or stenophagous plantfeeders, such as chrysomelids, is slight in Galápa gos phytophagous beetles. There is no additional evidence for host specificity in indigenous phy tophagous insects other than in Gerstaeckeria weevils on Opuntia cactus and some bruchids and scolytids. Thus, phytophagous species are in the minority, few are host specific, and none seem to have co-evolved with the endemic vegetation.

June. With the arrival of the Galápagos rainy sea son, insect activity increases and there are large and noteworthy outbreaks of beetles and other insects, which seem to be short-lived. These include Calosoma ground beetles, Camponotus ants, Disclisioprocta stellata Guenée (a geometrid moth), vari ous sphinx moths, and other insects. These mass emergences are best noticed at lights at night and are environmentally triggered, but they also occur annually in coastal mainland Ecuador and seasonal forests elsewhere in Central and South America, so they are not a unique island feature.

Seasonality

Species Level Endemism

Environmental conditions regulate periods of insect activity. Most adult insect species are present or active during the rainy months of January to

Most insect colonization has not been followed by much species multiplication; the mean for the native beetle fauna is about 1.35 species per

Evolutionary Dynamics Genus Level Endemism Endemics are taxa limited to the geographic area under discussion. Genera endemic to the Galápa gos probably represent an earlier time of coloniza tion and a more prolonged period of isolation. Galápagos endemic genera are proportionally more frequent in the vertebrates and less frequent in the insects. This could mean that vertebrates differen tiate at a faster rate or under stronger selective pressures, but more probably is a reflection of the more finely divided subjective criteria for what defines a vertebrate genus. Some endemic insect genera do exist. Among these endemics are some which can be called phylogenetic relicts or paleoendemics and which have no close relatives, such as the eyeless cave staphylinid Pinostygus of Isla Santa Cruz, and the Neoryctes dynastine scarabs which occur as four species on four islands. Some genera, once thought to be Galápagos endemics, have since been found in mainland Neotropical localities and others may yet be detected.


colonizing ancestor. About half the naturally occurring species are endemic, depending on the insect order. These evolved to endemic status following the colonization event of the ancestral species. The factors suppressing speciation in general in the Galápagos (as compared with other archipelagos) seem to be, in probable order of importance: lack of great ecological diversity, closeness to mainland source areas, and geological youth of the islands. Different groups of organisms need not pres ent equivalent amounts of endemism. This is obvi ously a result of differences in their vagility and the amount of gene flow between continental and island populations. In beetles, the good dispersers have lower levels of endemism, while poorer dis persers have higher levels. Comparison of the Galápagos and Hawaiian archipelagos shows a much larger mean number of speciation events from a single colonist ancestor in Hawaii. This is probably the result of Hawaii’s greater age, area, ecological diversity, and isolation (this is to say that colonist arrival is less frequent, and that genetic dilution of island populations by mainland genomes is also less frequent).

Speciation Most insect genera in the Galápagos are repre sented by only a single species. This shows that most colonization of the islands has usually been by only one species in a genus. This pattern was first noted by Darwin. Only a minority of the native insect genera which are present contain more than one species, either through multiple colonization, or species multiplication on the islands. The pro cess of forming several species by allopatric specia tion on a single individual island has not been a dominant evolutionary process in Galápagos bee tles, while it has been a spectacularly exuberant process in the Hawaiian Archipelago. Nevertheless, there are several insect genera which have undergone appreciable subspecia tion or speciation in the Galápagos but none of

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these approach the dramatic swarms of species (descended from a single ancestor species) of insects, snails, or birds that have evolved in Hawaii. For instance, while hundreds of species of Drosophila occur in Hawaii, there are only 13 spe cies (many cosmopolitan) of in these in Galápagos.

Winged Endemic Species In the winged insects the most common pattern of distribution is for a species to occur on more than one island. This is easy to understand. It is most likely that these evolved on a single island and then dispersed to other islands, usually by flight. Loss of Wings Loss of flight ability is one of the more pronounced phenomena associated with island insects. This is seemingly not a property of island life itself, but of habitat stability and homogeneity. Flightlessness also frequently occurs in insects in desert and semi-arid habitats. This last is the best single char acterization of Galápagos environments, and bee tles are prime examples. Flightlessness in some South African desert dwelling scarab beetles is a morphological correlate with water conservation capabilities. This may also be true and part of the adaptive strategies of such flightless Galápagos beetles as tenebrionids, carabids, and weevils. Beetle examples of more speciation in less vagile groups are in flightless carabids, weevils, and Darwin’s darkling beetles (Stomion, Ammophorus, and Blapstinus). Interestingly, even within flight less genera in the arid lowlands, many species do occur on more than one island, and these are prob ably evidence of inter-island oceanic transport following the origin of the species on one island. The single island endemics are usually restricted to either the arid lowlands or the moist uplands (of high islands). Groups that are actively in the process of losing flight ability, such as Ataenius and Neoryctes scarabs, show discrete poly morphic stages in reduction of hind wings. So, loss of flight ability in Galápagos insects is a significant

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evolutionary theme. This has not always sponsored a major burst of species multiplication, but it has happened more often in groups that lost their flight ability on the Galápagos as a convergence rather than in groups that arrived already in a flightless condition. There is a parallel in birds: rails have reached many oceanic islands and then convergently experienced a reduction in wings and loss of flight ability. Speciation and Flightlessness Flightless terrestrial arthropods would certainly appear to have less dispersal potential than winged ones, and most species proliferation has occurred in the Galápagos beetles that are secondarily wingless. Nine genera of beetles probably colonized in a flight less condition, but only four of these have undergone island multiplication to three or more species. These groups have produced an average of 3.0 species per colonization event. Another 14 genera appear to have become flightless after colonization and these show even more species proliferation, with a mean of 3.6 species per colonization event.

Adaptive Radiation Adaptive radiation is a common phenomenon on islands. But it is important to note that adaptive radiation is much more than just the simple allo patric species multiplication that follows genetic isolation on separate islands. It is here defined as the set of evolutionary changes which occur in the diversification of a lineage that facilitate the exploi tation of new resource types with different mor phological or physiological traits. Thus, along with the morphological, physiological, and/or behav ioral changes accompanying speciation must also come changes in either or both niche and habitat use. This is what has happened in the famous text book example of Darwin’s finches. Other examples can include the striking adaptive radiation in Scalesia trees and shrubs, and perhaps arguably in Opuntia cactus. In contrast, the famous giant

tortoises and less famous lava lizards have under gone much speciation or subspeciation, but there is little evidence for true adaptive radiation in these examples. Adaptive radiation is probably enhanced by competition for limited resources, as in the case of the finches, especially in times of drought. But, it is difficult to envision intense competition between generalist scavenger or generalist predator insects. Are the few examples of adaptive radiation indicative of a generalization, or are they excep tions? How many of the monophyletic species swarms in the insects of the archipelago have undergone significant ecological, morphological, or behavioral differentiation that promotes life in a new niche or new habitat? In short, there seem to be very few examples within the insects in general. In the three genera of Darwin’s darkling beetles (Ammophorus, Stomion, Blapstinus) there are some cases of congeneric species sympatry and there is some habitat separation between species based on preferences for different substrate types (sand ver sus volcanic ash), habitat distance from the sea coast, and elevation. Most Ammophorus species inhabit the arid zone, but two are restricted to the moist highlands of San Cristóbal and Santa Cruz Islands. The same occurs in Galapaganus weevils. Thus, while the Galápagos are famous for having provided a classic example of the process and results of adaptive radiation in Darwin’s finches, this is an exception. It is only a very infrequent or arguable result in Galápagos insects.

Subterranean Arthropods A diverse assemblage of many eyeless arthropods occurs in the extensive systems of caves and rock crevices in the volcanic basalt bedrock of the Galá pagos. Some ten species of arthropods such as geophilomorph centipedes, polydesmoid milli pedes, soil dwelling earwigs, and darkling and carabid beetles are in eyeless (Fig. 2) genera which must have colonized the Archipelago in an alreadyeyeless condition. But at least another 23 species of


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Extinction

Galápagos Islands Insects: Colonization, Structure, and Evolution, Figure 2 The staphylinid beetle Pinostygus galapagoensis Campbell and Peck from a lava tube cave on Santa Cruz island. This eyeless and flightless subterranean endemic genus and species has probably changed more from its ancestral colonizing species than any other Galápagos animal. The beetle belongs to a group of visually hunting and flying arboreal predators which live in the canopy of tropical South American rainforests. No other members of its tribe occur in the Galápagos. The body length is about 2.5 cm, and this is the world’s largest eyeless-wingless staphylinid beetle.

eyeless terrestrial arthropods, including seven beetle genera, are in normally eyed groups. These must have lost their eyes after colonizing the islands, and during the process of adapting to soil, litter or subterranean habitats.

Extinction through time is a natural process and is to be expected. But extinction caused by human action is different and should be of great concern in the Galápagos. Insect species extinction through human causes is probable, but no documented individual examples are known. Some of the intro duced insects, such as Wasmannia fire ants and Polistes wasps, are preying on or competing with indigenous and endemic insects. Feral vertebrates have had a two-fold effect on beetles and other insects. (i) The vertebrates have caused the near or complete loss of insect host plants, such as Opuntia cactus on most of Floreana and San Cristóbal (eaten by feral goats and donkeys). This has led to the concomitant loss of host-specific insects such as Gerstaeckaria weevils. (ii) The verte brates have also had an effect by being predators, such as mice or rats or pigs, feeding on Neoryctes scarab beetles or other large-bodied insects. Despite these examples, there is presently no strong or direct evidence of the actual archipelago-wide extinction of an insect species on the Galápagos through an action ultimately caused by human activity. Human-caused habitat alteration has had a sig nificant, but unmeasured effect on the native insect populations. The clearing of large areas of Scalesia forest for agriculture and pastures and the replace ment of large areas of native vegetation by intro duced crop plants, grasses and weeds on Floreana, Santa Cruz, San Cristóbal, and Isabela must have had some impact. The importance of all of these introductions and alterations has not been measured or even estimated for the beetles or other insects.

Future Research Although much is now known about Galápagos insects, there is still much to learn, especially about the life histories and evolutionary relationships of the species and in comparing them with the conti nental South American insect fauna. The Galápagos National Park Service and Charles Darwin Research

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Galea (pl. galeae)

Station invite international research proposals and scientific collaboration with Ecuadorian personnel, students, and researchers. Information on past and present entomology research programs and details for scientific research permit applications can be found at http://www.darwinfoundation.org/terrest/ entomology.html. Research proposals of an applied and conservation orientation are especially wel come. General collecting without a research pur pose is not permitted.

in Diptera, Lepidoptera and Hymenoptera. It forms the elongate, coiled proboscis in Lepidoptera.  Mouthparts of Hexapods

Gall An abnormal growth on a plant induced by insect or mite feeding, or a plant pathogen.

References Causton CE, Peck SB, Sinclair BJ, Roque-Albelo L, Hodgson CJ, Landry B (2006) Alien insects: threats and implications for conservation of Galápagos Islands. Ann Entomol Soc Am 99:121–143 Peck SB (2001) Smaller orders of insects of the Galápagos Islands, Ecuador: evolution, ecology, and diversity. Scientific Monograph Series, National Research Coun cil Press, Ottawa, Ontario, Canada, 278 pp Peck SB (2006) The beetles of the Galápagos Archipelago, Ecua dor; evolution, ecology, and diversity (Insecta: Coleoptera). Scientific Monograph Series, National Research Council Press, Ottawa, Ontario, Canada, 313 pp

Galea (pl. galeae) The outer region of the maxilla, often a lobe (Fig. 3), and sometimes highly modified (Fig. 4) for feeding cardo stipes palpifer lacinia

subgalea galea

palpus

Galea (pl. galeae), Figure 3 External lateral aspect of the left maxilla in an adult grasshopper, showing some major elements.

Gall Formation carol c. mapes Kutztown University of Pennsylvania, Kutztown, PA, USA Galls are structures that form as a result of the abnormal growth activities of plants in response to gall-inducing organisms. Most galls are caused by nematodes, insects and mites, while a very small percentage are caused by bacteria, fungi and viruses. There are thousands of species of insects in the world that induce gall formation on the roots, stems, leaves, buds, flowers and fruits of plants in a wide variety of plant families. Insect galls range in complexity from simple outgrowths to more highly differentiated structures such as those typified by many of the cynipid wasp galls. Despite the large numbers and types of insect- induced galls, very little is known regarding the underlying mechanism or mechanisms of insect gall formation. In contrast, the mechanism of crown gall formation by the bacterium Agrobacterium tumefaciens, has been well characterized. An understanding of the mechanism of crown gall formation may provide some clues to the mecha nism or mechanisms of insect gall formation. Crown galls form as a result of wound inocu lation on many species of plants by the soil dwell ing bacterium Agrobacterium tumefaciens. Early studies showed that crown gall tissues exhibit autonomous growth and retain their tumorous

Gall Formation

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antenna ocellus

compound eye clypeus

epipharynx labrum labial palpus

galea

Galea (pl. galeae), Figure 4 The head of a moth (Lepidoptera) showing some components.

characteristics in the absence of the inducing bac terium. The ability of the bacterium to induce gall formation subsequently has been shown to be encoded by a tumor-inducing (Ti) plasmid that is transferred into the plant tissue. A small fragment (the T-DNA) of the Ti plasmid is integrated into the plant cell genome within the nucleus and is stably maintained and transcribed. It has been shown that the T-DNA contains genes that code for the production of plant hormones, the auxin indole-3-acetic acid (IAA) and for cytokinins. Cytokinins promote cell division in plant cells while auxins play a role in cell enlargement. Both of these hormones also affect tissue differentiation in plants as well as many other processes. Cytoki nins have been shown to be produced by addi tional species of gall forming bacteria including Erwinia herbicola pv. gysophilae, Pseudomonas savastonoi and Rhodococcus fascians. A linear plasmid with a cytokinin synthesis gene has been found in R. fascians, a bacterium that induces leafy galls. While an understanding of the mechanism of crown gall formation may provide some clues to the mechanism of insect gall formation, it should be noted that insect galls have some important dif ferences compared to crown galls. Unlike crown

galls, insect galls are organized structures, often with very complex morphologies. In addition, early studies have shown that unlike crown galls, insect-induced galls do not exhibit the autono mous growth that is characteristic of crown galls. Gall growth does not continue indefinitely once the gall-inducing insect is no longer present. The physical presence of the insect within the gall tis sue is another unique factor that may play a role in the mechanism of insect gall formation, but the role of mechanical tissue disruption in the process of insect-induced gall formation has not been well studied. Instead, studies have focused on the role of chemicals in insect-induced gall formation.

Studies of Insect Extracts and Secretions A number of studies have been undertaken to test insect extracts and secretions for gall inducing chemicals. Larvae of Mikiola fagi, a midge that forms leaf galls (Fig. 5) on the European beech (Fagus sylvatica), have been tested to determine if they secrete cecidogenetic (gall-forming) chemi cals. When the larvae were placed on a lanolin

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Gall Formation

Gall Formation, Figure 5 Leaf gall caused by Mikiola fagi on the European beech (Fagus sylvatica).

Gall Formation, Figure 6 The eastern spruce gall caused by Adelges abietes on Norway spruce (Picea excelsa).

paste on leaves of beech and when a paste that lar vae had previously been on, was repeatedly applied to leaves, changes involving cell division and cell elongation resulted, but galls did not form. Studies of the eastern spruce gall on Norway spruce (Picea excelsa) have provided evidence for the presence of cecidogenetic activity associated with the salivary glands of the gall-forming adelgid Adelges abietes. The characteristic needle swelling associated with the early stages of gall formation (Fig. 6) has been mimicked by injecting spruce buds with a solution containing macerated adelgid salivary glands. The willow leaf gall, caused by Pontania pacifica, is initiated by the accessory gland secretions of the ovipositing female sawfly while further development of the gall is dependent on the presence and activity of the larvae. When gland sacs were placed in developing galls from which larvae had been removed, galls continued to grow. If the glandular material was repeatedly injected over a period of several days, the galls continued to develop to normal size. Extracts of young Pontania larvae and extracts of female accessory glands were able to promote the continued growth of galls from which the larvae had been removed. Mixtures of chemicals were tested to see if they played a role in willow leaf gall formation. Rapid and sustained growth of galls was obtained with a periodic injection of a mixture containing a synthetic cytokinin kinetin, a naturally occurring auxin indole-3-acetic acid and adenine.

While the examples noted above provide evi dence for gall-inducing factors associated with extracts and secretions, the specific cecidogenetic chemicals have not yet been identified. In addi tion, while there is evidence for cecidogenetic properties associated with glandular extracts and secretions, no one has been able to mimic the entire process of gall formation with an extract or secretion. This is not surprising given the difficul ties associated with attempting to simulate the continual release of a gall-inducing stimulus from the precise location where the insect is normally active within the plant tissue.

Studies of Auxin and Cytokinin Involvement in Insect Gall Formation Given the importance of plant hormones in plant development as well as in the mechanism of crown gall formation, a number of studies have focused on the roles of the plant hormones auxins and cytokinins in insect gall formation. There were some early reports that applications of auxins to plant tissues resulted in structures simi lar to galls, while others reported failure in their attempts to induce galls with auxin. Applications of auxins to plant tissues have not resulted in the for mation of structures that exhibited the complexity and the degree of hyperplasia of insect galls. Extracts

Gall Formation

of the saliva of gall-inducing aphid species have pro vided evidence for the presence of the auxin indole3-acetic acid (IAA) and some have concluded that IAA was the active cecidogenetic factor in the aphid species studied. However, it was not determined whether the aphids produced the auxin, or whether they accumulated it from the plant tissue. IAA has been detected and analyzed in other galls and gall formers. Oak apple galls caused by Cynips quercusfolii on Quercus robur and Quercus sessiliflora were shown to contain twice as much auxin activity as normal leaf tissues, while Pinus edulis needles with galls induced by larvae of the midge Janetiella sp. near J. coloradensis were found to con tain 3.7 times higher concentrations of auxin bioac tivity compared to needles lacking galls on a fresh tissue weight basis, and 17 times more auxin activity per needle. IAA was detected in Cynips quercusfolii, but was not detected in the larvae of the midge Janetiella sp. near J. coloradensis. In a study of the goldenrod ball gall induced by larvae of the dipteran Eurosta solidaginis, the gall-forming larvae were shown to contain high levels of IAA with detection by gas chromatography-mass spectrometry (GCMS). Concentrations of IAA in the gall tissues were higher than in the stem tissues on a weight per stem length basis, but not on a weight per weight basis. Some studies have shown high levels of cytoki nins in gall tissues. Levels of four cytokinins were shown to be higher in developing galls induced by Pontania proxima compared to levels in leaf tissue. Levels of the cytokinin isopentenyladenosine were shown to be much higher in hackberry (Celtis occidentalis) gall tissues than in control leaf tissues. However, others have not found higher levels of cytokinins in gall tissues compared to normal tissues. Levels of cytokinin bioactivity found in galls formed by Mikiola fagi were not elevated when compared to healthy leaves, while cytokinin concentrations in gall tissues formed by a chalcid wasp on Erythrina latissima were lower than those in surrounding leaf tissues. Levels of four cytokinins were shown to be higher on a weight per stem length basis in golden rod ball galls compared to normal stem tissues, but were not higher on a weight per weight basis.

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Studies have also shown evidence for cytoki nins associated with gall-inducing insects. Cytoki nins have been detected in the oriental chestnut gall wasp (Dryocosmus kuriphilus) and in the larvae of a chalcid wasp that forms leaf galls on E. latissima. The high concentration of cytokinins in the larvae of the chalcid wasp could be responsible for nutrient mobilization by the larvae within the galls, and may also be responsible for the fact that galls containing larvae remain as green islands on senescing leaves, while those without larvae, senesce rapidly. Four different cytokinins have been detected by GCMS in the larvae of Eurosta solidaginis, the dipteran responsible for the formation of goldenrod ball galls (Fig. 7). The cytokinin isopentenyladenine was shown to be present at much higher concentrations in first instar larvae than in normal stem tissues. In contrast, in a study of willow galls induced by Pontania pacifica, growth promotion was found to be associated with two unidentified adenine derivatives in the female accessory glands of the sawfly, but no significant cytokinin bioactivity of gland extracts was detected. In summary, studies have provided evidence for yet-to-be-identified gall-inducing factors associ ated with extracts and secretions of gall-inducing insects. In addition, there have been numerous reports of the presence of plant hormones in gallinducing insects and gall tissues with detection not only by bioassay, but also by sophisticated stateof-the-art techniques. However, it remains to be seen whether gall-inducing insects have the ability to synthesize plant hormones such as auxins and/or

Gall Formation, Figure 7 The goldenrod ball gall caused by Eurosta solidaginis on Solidago altissima.

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Gall Midges (Diptera: Cecidomyiidae)

cytokinins, whether the gall-formers induce synthe sis of the hormones in the surrounding plant tissue, or whether the hormones that have been detected in the gall-formers have just been accumulated from the plant tissue. The high levels that have been found in some species of gall-inducing insects are sugges tive of synthetic capabilities. Despite the evidence for plant hormones in galls and gall-inducing insects, the specific role of plant hormones in the develop ment of insect galls has not been determined. Given the important role that auxins and cytokinins play in normal developmental processes in plants as well as their well- characterized role in crown gall formation, it seems likely that they play an impor tant role in insect gall development as well. As the evidence for the involvement of auxins and cytoki nins in insect gall formation is more convincing for some of the gall systems that have been studied than for others, it is most probably the case that other yet-to-be-determined cecidogenetic agents will be identified as playing important roles in the mecha nism of gall formation for certain types of insect galls.  Gall Midges (Diptera: Cecidomyiidae)  Gall wasps (Hymenoptera: Cynipidae)

References Boysen JP (1948) Formation of galls by Mikiola fagi. Physiol Plant 1:95–108 Leitch IJ (1994) Induction and development of the bean gall caused by Pontania proxima. In: Williams MAJ (ed) Plant galls: organisms, interactions, populations. Clarendon Press, Oxford, UK, pp 283–300 Mani J (1964) Ecology of plant galls. Junk, The Hague, The Netherlands, 434 pp Mapes CC, Davies PJ (2001) Indole-3-acetic acid and ball gall development on Solidago altissima. New Phytol 151:195–202 McCalla DR, Genthe M, Hovanitz W (1962) Chemical nature of an insect gall growth-factor. Plant Physiol 37:98–103 Plumb GH (1953) The formation and development of the Norway Spruce gall caused by Adelges abietes L. Con necticut Agric Exp Station Bull 557:2–77 Van Staden J, Davey JE (1978) Endogenous cytokinins in the laminae and galls of Erythrina latissima leaves. Bot Gaz 139:36–41

Gall Midges (Diptera: Cecidomyiidae) netta dorchin Museum Koenig, Bonn, Germany Cecidomyiidae are one of the largest families in the order Diptera, with more than 5,700 described species and many more undescribed and unknown species worldwide. The family belongs to the suborder Nematocera, and its closest relatives within it are the fungus-feeding gnats in the families Sciaridae and Mycetophilidae (in the broad sense). According to fossils from the Jurassic period, the family is at least 150 mil lion years old, but has apparently experienced explosive speciation during the Cretaceous, with the appearance of flowering plants. Cecidomyii dae have a cosmopolitan distribution, although only the faunas of Europe and North America are fairly well known. This situation makes it impossible to estimate the actual number of spe cies in the family. The common name “gall midges” refers to the gall-inducing habit of most species, which constitute the largest group of gall-inducing organisms. However, the family also contains many species that are fungus-feeders, predators, or feed on plants without inducing galls.

Classification The Cecidomyiidae are divided into four sub families: The Catotrichinae constitute the oldest sub family and are considered ancestral to all other subfamilies. This group contains one genus (Catotricha) and seven species, which are known from the Holarctic region and from Australia. The Lestremiinae are a diverse group of about 630 species that is ancestral to the remaining two subfamilies. Although many genera and species in this group are common and widespread, it is still largely unknown, and dozens of species belonging to it are yet to be described from the


Holarctic and the Australasian regions. Faunas of other parts of the world are poorly known. Les tremiinae are fungus or detritus feeders, and their larvae are found in decaying organic matter. The Porricondylinae constitute a diverse, paraphyletic group of 635 species that are similar in habits to the Lestremiinae. A few species are consistently found in association with plants, such as in already infested fruit or in conifer cones, but are assumed to feed on decaying organic matter in these niches. Several species are known as fossils from the upper and lower Cretaceous. The subfam ily is poorly known outside the Palearctic region, and relationships among its tribes are unclear. The Cecidomyiinae are the youngest, largest, and most diverse subfamily of gall midges, with more than 4,400 described species worldwide. This is a monophyletic group that includes all the plant-feeding species in the family, as well as several unrelated groups of fungus feeders and predators. The Cecidomyiinae are divided into four supertribes: the species-poor Stomatosema tidi and Brachineuridi, whose biology is largely unknown, and the very large and biologically diverse Cecidomyiidi and Lasiopteridi.

Morphology Adult gall midges are tiny, fragile flies, usually 2–5 mm in length.Most species are inconspicuously colored, but some groups have color patterns, especially black and white, resulting from dense covering of scales and hairs. The head is made up largely of compound eyes that often touch at the vertex. The antennae usually number 12 flagellom eres, but their number vary among groups and sometimes also within the same species and even the same individual. Male flagellomeres are often composed of a large node and a long narrow neck, whereas female flagellomeres are mostly cylindri cal with much shorter necks. Males of many species have two nodes on each flagellomere, each bearing sensory setae and circumfila – sensory hairs that girdle the flagellomere and sometimes

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form very long loops. Male antennae of some groups in the family resemble those of the female. Mouthparts are usually greatly reduced and are only capable of liquid consumption; the adults of most plant-feeding species may not feed at all. The wing is usually transparent and has greatly reduced venation in most groups, with only 2–5 long veins, and long hairs along its margin. The legs are usually long and slender and comprise five tar someres. In the subfamilies Porricondylinae and Cecidomyiinae, the first tarsomere is considerably shorter than the second, and legs are easily broken beyond it. Tarsal claws are variably shaped, some with 1–2 additional teeth at their base. The oviposi tor varies in length and is usually retracted inside the abdomen. Different groups have developed various modifications of the ovipositor, including conspicuous setation, or needle-like or sword-like parts to aid in oviposition. The male genitalia include gonopods that clasp the female during mating. Larvae pass through three instars. They are legless and have a greatly reduced head capsule with no eyes, very short antennae, and mouth parts that are suited for piercing and sucking liquids. They are often bright yellow, orange, or red, but they may also be white, depending on the species. The third instar larva usually has a spatula, a dark, sclerotized structure on the ven tral side of the prothorax, which is unique to the Cecidomyiidae. The spatula, which varies in shape and size among species, is used for digging in the soil or cutting through plant tissue, but many taxa have lost it altogether. Pupae may have diagnostic characters on their head and abdomen in the form of horns and spines that aid in cutting through plant material prior to adult emergence.

Biology The gall-inducing guild within the Cecidomyii dae has received more attention than any other group in the family due to the large number of species and the remarkable diversity of host

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plants, gall structures, and life-history strategies exhibited by its members (Fig. 8). Roughly 70% of the known species in the family are gall induc ers, most of which are monophagous (restricted to a single host), or oligophagous (feeding on a few related plant species). A few species are known to use a larger number of hosts that belong to several different families, either simultane ously or at different stages of their life cycle. Gall midges are found on hundreds of plant families all over the world, but certain families, such as the Asteraceae, Chenopodiaceae, Fabaceae, and Salicaceae, support especially high numbers of species. Galls range from simple leaf swellings, leaf curls, and unopened flowers to complex stem and bud galls that may comprise from one to many larval chambers and vary in the extent of tissue differentiation. Galls may be tiny or very conspicuous, green to bright red, hairy or smooth, and they may resemble the original structure of the affected plant organ or greatly deviate from it. The only other group of gall inducers exhibiting similar diversity in gall shapes and forms is the gall wasps (Cynipidae), but these are less speciesrich and, as a group, are associated with much fewer plant taxa. Although plant-feeding is by far the most common strategy in the family, feeding habits among cecidomyiid larvae are extremely diverse. Larvae of all Catotrichinae, Lestremiinae, and Porricondylinae, as well as some of the Cecid omyiinae, feed on fungi or decaying organic matter, while all plant feeders and predators belong to the Cecidomyiinae. Some species feed on or in plants without gall induction, or develop as inquilines, invading galls of other arthropods and feeding on gall tissues at the expense of the gall inducer. Inquilinism has evolved indepen dently many times in the family, and while some genera are entirely or mostly composed of inquilinous species, others include both gallinducers and inquilines. Predatory larvae occur in many unrelated groups within the Cecid omyiinae and are either specialists or generalists that feed on various arthropods, particularly

Homoptera and mites. Certain groups within the subfamily are secondarily associated with sym biotic fungi that develop in their galls (e.g., many species in the tribes Asphondyliini and Lasiop terini), but larvae in these galls seem to feed on plant tissues rather than on the fungus, and the nature of this association is still unclear. The life cycle of phytophagous gall midges is closely associated with that of their host plants. Species that are associated with trees are usually univoltine, whereas those that are associated with shrubs and herbaceous plants are often bivoltine or multivoltine, since these plants may continuously offer tissues that are suitable for galling. Females usually emerge from the pupae with their eggs fully mature and mate directly or after some courtship with males that wait for them on the host plant or on the ground. Sex ratios among emerging adults are often skewed towards females, and females of some species produce strictly unisexual (all male or all female) progeny throughout their lifetime, a phenome non known as monogeny. While all Cecidomyii dae reproduce sexually, a few species in the Porricondylinae that feed on fungi may also reproduce by paedogenesis, a much shortened and simplified parthenogenetic life cycle during which larvae or pupae give rise to daughter lar vae. This situation has evolved at least twice in the family and seems to be regulated by the avail ability of food; when food becomes scarce the population switches to normal, sexual reproduc tion through the development of adults. Mated females cease to attract males and immediately engage in host seeking for oviposi tion. In most phytophagous species, the eggs are laid on the surface of plants or in between their scales or leaves. Some species in the tribe Aspho ndyliini have evolved a piercing ovipositor and insert the eggs directly into plant tissues. Whether eggs are laid individually or in batches is a spe cies-specific trait, as is the morphogenesis of the resulting gall and its final shape and structure. Larval feeding cause modification of plant tissues around them to produce the gall, which often


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Gall Midges (Diptera: Cecidomyiidae), Figure 8 Representative galls induced by gall midges ( Diptera: Cecidomyiidae). Top left, leaf gall on Solidago altissima cut open to show a pupa of Asphondylia solidaginis; top right, flower galls on Solidago rugosa induced by Schizomyia racemicola; second row left, leaf gall on Suaeda monoica induced by Stefaniola siliqua; second row right; stem gall on Atriplex halimus induced by Stefaniella atriplicis; third row left, stem gall on Carpobrotus acinaciformis induced by Asphondylia sp.; third row right, bud galls on Artemisia sieberi induced by Rhopalomyia navasi; bottom row left, stem gall on Deverra tortuosa induced by Paraschizomyia buboniae; bottom row right, bud galls on Artemisia princeps induced by Rhopalomyia longitubifex.

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Gall Moths (Lepidoptera: Cecidosidae)

reaches its final size when the larvae are still first instars. Both the physical and the chemical stimu lation applied by the larvae are necessary for gall induction, and galls will cease to develop if the larvae are killed. Mature larvae either pupate in the gall or drop to the ground and pupate in the soil, depending on the species, and in some multi voltine species also on the time of year. Larvae of many species, especially in temperate areas, enter diapause in the soil or inside the plant for a cer tain part of the year until suitable plant tissues become available again. In multivoltine species, larvae of the last generation, and/or a certain pro portion of the larvae in each generation, may enter diapause until the following year, and in some species dormancy may last several years.

example, is a biological control agent that is available commercially against numerous aphid pests. Adults of this species efficiently locate aphid infestations where females lay their eggs, and individual larvae may each consume dozens of aphids throughout their lifetime. Some phy tophagous gall midges are successfully used as biological control agents of invasive weeds, although their impact is often too weak when not combined with other agents. Successful weed control projects involving cecidomyiid agents include the bud galler Spurgia esulae Gagné against leafy spurge in North America, and the flower-galling Dasineura dielsi Rübsaamen against the Australian wattle Acacia cyclops in South Africa.

Economic Importance

References

Many gall midges are pests of agricultural and food crops, ornamental plants, and forest trees. One of the most serious pests in the family is the Hessian fly, Mayetiola destructor (Say), whose lar vae feed in the stems of wheat, and kill the plants or severely reduce their productivity. This species was introduced from Europe to North America during the Revolutionary War, presumably in Hessian soldiers’ mattresses that contained infested wheat stems. Another serious European pest that was introduced into North America is the sorghum midge, Contarinia sorghicola (Coquillet), one of the most important pests of grains in the world, whose larvae feed in seeds and hinder their development. Gall midges from the genus Orseolia that develop in buds and stems of rice plants are serious pests of this crop in Asia and Africa. Control of pest species may be achieved by using natural enemies or chemicals, but control has been most efficient with the use of resistant plant strains and modifications of management practices. Certain predatory gall midges are consid ered beneficial because they prey on agricultural pests. Aphidoletes aphidimyza (Rondani), for

Barnes HF (1946–1956) Gall midges of economic impor tance, vols 1–7. Crosby Lockwood and Son, London Gagné RJ (1989) The plant-feeding gall midges of North America. Cornell University Press, Ithaca, NY Gagné RJ (1994) The gall midges of the Neotropical Region. Cornell University Press, Ithaca, NY Gagné RJ (2004) A catalog of the Cecidomyiidae (Diptera) of the World. Mem Ent Soc Wash 25:1–408 Harris KM (1966) Gall midge genera of economic impor tance (Diptera, Cecidomyiidae) Part 1: Introduction and subfamily Cecidomyiinae; supertribe Cecidomyiidi. Trans R Entomol Soc London 118:313–358 Yukawa J, Rohfritsch O (2005) Biology and ecology of gall inducing Cecidomyiidae (Diptera). In: Raman A, Schaefer CW, Withers TM (eds) Biology, ecology, and evolution of gall-inducing arthropods. Science Publish ers, Inc., Enfield, New Hampshire, pp 273–304

Gall Moths (Lepidoptera: Cecidosidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Gall moths, family Cecidosidae, total only seven species, with five species from southern South

Gall Wasps (Hymenoptera: Cynipidae)

America and two from South Africa. The family is in the superfamily Incurvarioidea, in the sec tion Incurvariina, of division Monotrysia, infraorder Heteroneura. Adults small (7– 26 mm wingspan), with rough head scaling; haustellum reduced, scaled; labial palpi short; maxillary palpi vestigial, 1- segmented. Maculation is som ber, usually without spots but often with irides cence. Adults are probably diurnal. Larvae are gall makers on Schinus (Anacradiaceae) in Argentina.

References Becker VO (1977) The taxonomic position of the Cecidosidae Brèthes (Lepidoptera). Polskie Pismo Entomologiczne 47:79–86 Parra LE (1998) A redescription of Cecidoses argentinana (Cecidosidae) and its early stages, with comments on its taxonomic position. Nota Lepidopterologica 21:206–214 Wille J (1926) Cecidoses eremita Curt., und ihre Galle an Schinus dependens Ortega. Zeitschrift für Morpholgie und Ökolologie der Tiere 7:1–101

Gall Wasps (Hymenoptera: Cynipidae) Eileen A. Buss University of Florida, Gainesville, FL, USA The Cynipoidea [Hymenoptera: Apocrita (Parasitica)] superfamily contains plant-feeding (phytophagous) and parasitic wasp species, but is best known for the gall wasps (family Cynipidae). The superfamily includes about 3,000 described species. The number of families within the Cyn ipoidea is a matter of debate. Some researchers subdivide the group into six families: Cynipidae, Ibaliidae, Liopteridae, Figitidae, Charipidae, and Eucoilidae. Others use different classifications, including four families (Cynipidae, Ibaliidae, Figitidae, and Himalocynipidae), or five families (Austrocynipidae, Ibaliidae, Liopteridae, Cynipidae, and Figitidae).

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Order: Hymenoptera Suborder: Apocrita (Parasitica) Superfamily: Cynipoidea Family: Cynipidae

In general, cynipids are either gall-makers or inquilines in galls made by other species. About 1,360 species have been described, but it is esti mated that 3,000–6,000 species actually exist. Gallmaking cynipids (Cynipinae) are similar to true parasitoids in that they inject a kind of venom with their eggs into plant tissue. A gall forms because of the plant’ s response to the wasp’ s egg laying, pres ence of the egg, and/or feeding stimulation by the larva. Plant cells are usually modified and enlarged, the plant tissue surrounds the egg or larva, and the gall protects and provides nutritive cells for the gall-maker. Inquilines (e.g., Synerginae) cannot make their own galls on plants. Females lay eggs into other galls, and their larvae feed on gall tissue, sometimes changing the normal shape or size of the gall.

Gall Diversity Cynipid galls come in a wide variety of forms, the shape and complexity being determined by the species of gall wasp that feeds within. Commonly attacked structures include catkins, seeds, flowers, petioles, branches, stems, and roots, but most galls occur on leaves and buds. The galls that cynipids make are generally described as blister, bud, bullet, oak apple, roly-poly, rosette, twig or stem galls. More than one gall species may also occupy a leaf or other structure. Some galls are single- chambered (monothalamous) and contain only one gall-maker, and others are multi-chambered (polythalamous) and contain many gall-makers. Those plants most often infested by cynipids are in the families Rosaceae, Asteraceae, Salicaceae, and Fagaceae. Oaks (Fagaceae: Quercus spp.), however, support the greatest diversity of gall-makers in North America, numbering at least 717 cynipid species.

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Gall Wasps (Hymenoptera: Cynipidae)

Biology Cynipid adults are small (1–6 mm), hard-bodied insects, with compressed abdomen, reduced wing venation, and simple, filiform antennae (Fig. 9). Most are drab-colored (e.g., black, brown, dark red, amber, or straw yellow), and may be either dull or shiny, but never metallic. Antennae of females are usually 13-segmented and males have 14 or 15 segments with the third often elongated and bent. The larvae are about 1-4 mm long, white, lack legs, and have distinct head and chewing mouthparts. Each larva develops within a discrete chamber of a gall, even when multiple gall-maker larvae develop in the same, polythalamous gall. Larvae apparently feed continuously, but do not produce fecal matter until pupation. Pupation always occurs in the gall, wherever the gall is located (e.g., on the plant or in the litter layer). Adults usually chew a circular hole upon exiting the gall. The life cycle of many cynipids is complex, and involves heterogeny or alternation of generations. As such, a bisexual generation (both males and females) alternates with a unisexual generation (all

females). The female generation reproduces by parthenogenesis, and the unfertilized eggs develop into sexual offspring. Because of the haplo-diploid genetics of wasps, all males can develop from unfer tilized eggs. However, females result from the repli cation of chromosomes inside an unfertilized egg’ s nucleus. The wasps of the two generations often look morphologically different and may attack the same or different plant structures and make very different galls. As a result, the insects of both gen erations have occasionally been falsely described as separate species.

Gall Inhabitants Galls are good nutrient sources, and can be inhab ited by other insects that feed on gall tissues or use the gall for shelter. Some of these insects can kill some or all of the gall-making larvae, either directly or indirectly by competition for resources. In addi tion to inquilines (e.g., Synergus spp. and Ceroptres spp. in oak galls), other insects feed opportunisti cally on gall tissue, including clearwing borers, longhorned beetles, metallic wood-boring beetles, weevils, gall midges, and others. Some of these opportunistic insects may have broad host ranges and also be pests on other plant species (e.g., dog wood borer). Some additional arthropods live externally on gall surfaces (e.g., mites, collembola), or in old, dry galls (e.g., ants). Natural enemies, especially parasitoid complexes, also inhabit galls and increase gall-maker mortality.

Abundance and Distribution

Gall Wasps (Hymenoptera: Cynipidae), Figure 9 Adult Diplolepis rosae, which develops in the mossy rose gall.

Populations of cynipids are sometimes greater on certain plants within a species than others, and sev eral reasons why this occurs have been proposed. One possibility involves the adult female’ s choice of ovipositional sites and her ability to distinguish between host plants or structures that vary in size, nutritional quality, or defensive capability. Because her offspring are embedded in plant tissue, her

Gamagrass Leafhopper Dalbulus quinquenotatus Delong & Nault (Hemiptera: Cicadellidae)

“choices” determine where eggs and subsequent offspring are dispersed. Especially important for those species that oviposit into buds before leaf flush is synchrony between insect hatch or emer gence and plant budburst or leaf and shoot elon gation. However, the plant’ s genotype and ability to form a gall may still limit its use as a host for gall-makers. Thus, an egg may be laid into a bud, but the plant may not react to the stimulus to make a gall. In addition, because cynipids have limited sexual reproduction and dispersal ability, genetic variation within the population may be reduced, resulting in less adaptation to a variety of hosts and greater specialization on isolated host plants.

Economic Importance Some galls and gall-makers are beneficial, and are used in biological control programs for weeds. And, historically, those galls containing tannic acid (e.g., oak galls) were used to make inks and dyes, and to tan leather. Although galling insects are usually not con sidered pests, certain species can reach outbreak levels and cause either physical or aesthetic damage to high-value plants. Galling insects have been known to reduce photosynthesis and acorn pro duction, discolor foliage, cause defoliation, branch dieback, and plant death. For example, the jump ing oak gall wasp, Neuroterus saltatorius (Edwards) attacks Garry oak (Q. garryana Douglas) in the western United States and Canada, and causes severe and chronic mid-summer leaf scorching and partial defoliation. The rough oak bulletgall wasp, Disholcaspis quercusmamma (Walsh), forms galls on bur oak (Q. macrocarpa Michaux) and swamp white oak (Q. bicolor Willd) that disfigure trees and produce a sticky exudate, which attracts stinging insects. Other galls may host inquilines that are pests of other plants. In addition, aesthetic disfigurement can be enough to prevent the sale of infested nursery stock. At present, little information exists on the effective management of galling insect

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pests; pruning is labor-intensive and insecticide use may disrupt the natural enemy population, poten tially leading to additional outbreaks.

References Abrahamson WG, Weis AE (1987) Nutritional ecology of arthropod gall makers. In: Slansky F Jr., Rodriguez JG (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, NY, pp 235–258 Askew RR (1984) The biology of gall wasps. In: Anan thakrishnan TN (ed) Biology of gall insects. Edward Arnold, Baltimore, MD, pp 223–271 Rohfritsch O (1992) Patterns in gall development. In: Shorthouse JD, Rohfritsch O (eds) Biology of insectinduced galls. Oxford, New York, pp 60–86 Ronquist F (1999) Phylogeny, classification and evolution of the Cynipoidea. Zoologica Scripta 28:139–164 Wiebes-Rijks AA, Shorthouse JD (1992) Ecological relation ships of insects inhabiting cynipid galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford, New York, pp 238–257

Gamagrass Leafhopper, Dalbulus quinquenotatus Delong & Nault (Hemiptera: Cicadellidae) Gustavo Moya-Raygoza University of Guadalajara, Jalisco, Mexico The gamagrass leafhopper is a small (length 3.0– 4.3 mm) deltocephaline, brownish orange in color, with five black spots on the head (Fig. 10). This species is found at low elevations (125–1,975 m) and occurs in central and southern Mexico and in Costa Rica. Its developmental time from egg to adult eclosion is about 34 days at 24°C. Nymphs begin hatching on day 12 and peak nymphal abundance is reached on day 16. Generations develop continuously through the year on perennial gamagrasses (Tripsacum spp.). This leafhopper has particular behavioral and ecological importance because it is among the few leafhopper species tended by ants. Unlike its nontended congeners, D. quinquenotatus responds to

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Gamagrass Leafhopper Dalbulus quinquenotatus Delong & Nault (Hemiptera: Cicadellidae)

Gamagrass Leafhopper Dalbulus quinquenotatus Delong & Nault (Hemiptera: Cicadellidae), Figure 10 Dalbulus quinquenotatus.

stroking of the abdomen by ants’ antennae by excreting and holding honeydew droplets until droplets are removed by ants. Dalbulus quinquenotatus excretes three to six times the volume of honeydew as do non-tended species. Moreover, droplets of D. quinquenotatus are about 23% larger in diameter and are excreted two to four times more frequently than its non-tended sister species. Nymphs and adults are sedentary and gregarious. They aggregate within leaves at the bases of Tripsacum spp. Sedentary and gregarious behaviors are typical in other hemipterans tended by ants such as aphids (Aphididae), treehoppers (Mem bracidae), and scales (Coccidae), but rare in leaf hoppers. Because it has been broadly investigated, the gamagrass leafhopper can serve as model in the study of other hoppers tended by ants in the tropical and temperate regions.

The gamagrass leafhopper is tended by 18 ant species from four different subfamilies; however, the two most commonly associated ant species are Brachymyrmex obscurior Forel and Solenopsis geminata (F.). Other insects also inhabit the leaves at the bases of Tripsacum spp. where D. quinquenotatus is tended by ants. These include the decom posers Coproporus sp. (Staphylinidae), Carpophilus sp. (Nitidulidae), and Haptoncus sp. (Nitidulidae). These taxa occur during the wet season, and of these Carpophilus sp. is the most abundant. This species feeds mainly on the fermenting fluid of plants. The source of fermentation in this case is the carbohydrate contained in the honeydew excreted by D. quinquenotatus. The mutualistic association (Fig. 11) between D. quinquenotatus and ants occurs because both receive benefits. The gamagrass offers habitat and food in the form of sap for the leafhopper most of the time, except at the end of the dry season, when gamagrass populations dry up. The sap is trans formed by the leafhopper into honeydew and prey. The honeydew provides water, sugars, amino acids, lipids, and vitamins to ants. Moreover, ants con sume some nymphs and adults thereby obtaining

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LEAFHOPPER (D. quinquenotatus)

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H a Fo bita od t (s ap

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Food (honeydew+prey) Remove honeydew (plant)

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ANTS (many species)

Predator protection Expel herbivores Population regulation

Gamagrass Leafhopper Dalbulus q uinquenotatus Delong & Nault (Hemiptera: C icadellidae), Figure 11 Beneficial effects of the D. quinquenotatus- ants-gamagrass relationship.

Gallinipper

protein and reducing the leafhopper population. Ants remove the honeydew produced by the gamagrass leafhopper. This leafhopper oviposits its eggs in clusters on the upper surface of midribs of basal leaves; therefore, removal of honeydew by ants reduces the death of leafhopper eggs by suffocation from accumulated honeydew and the formation of sooty mold on host leaves. Also, when the honeydew is removed the sooty mold is eliminated, facilitating plant photosynthesis. Ants protect D. quinquenotatus from arthropod predators such as spiders and nabids (Nabidae). Predators not only are expelled by ants when they try to approach D. quinquenotatus, but also are captured and transported to the ant nest and presumably used as food. Ants tending D. quinquenotatus also expel the related leafhoppers D. gelbus and D. guzmani that inhabit the canopy of Tripsacum spp. Adults of these two species respond readily to mechanical stimuli and avoid capture and predation by ants, especially on large gamagrasses. The mutualistic association between D. quinquenotatus and ants on gamagrasses is affected by biotic and abiotic factors. Under greenhouse conditions, diet influences the response of ants to population of D. quinquenotatus. When ants are denied food, they prey upon and extinguish pop ulations of D. quinquenotatus, but when supplied with prey (dead yellowjackets), large numbers of ants tend leafhopper populations that grow in size. Few ants tend leafhoppers when supplied with insect prey and honey. In natural conditions ants exploit other food resources to replace D. quinquenotatus honeydew during the driest months, when D. quinquenotatus populations are lower. That resource is nectar produced in extra floral nectaries by the plants Acacia pennatula, Leucaena esculenta, Lobelia laxiflora, and Lysilona sp. that grow in the gamagrass community. In the wet season, when the host plants contain abundant green foliage, D. quinquenotatus and ants are most abundant on Tripsacum spp. The gamagrass populations, which grow in open areas in patches alongside herbaceous plants, shrubs,

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and trees, tend to be maintained in an early state of succession because of frequently occurring fires during the dry winter months in Mexico. Burned gamagrass populations are colonized better than unburned gamagrasses by the gamagrass leafhopper and tending ants. Five months after fire, the mutualistic association is higher in burned than unburned gamagrass pop ulations. Populations of leafhopper adults and ants are equal on gamagrass plants given extra doses of phosphorous, nitrogen, or potassium. This suggests that the mutualistic association between ants and gamagrass leafhoppers is not affected by plant nutrients.

References Larsen KJ, Heady SE, Nault LR (1992) Influence of ants (Hymenoptera: Formicidae) on honeydew excretion and escape behaviors in a myrmecophile, Dalbulus quinquenotatus (Homoptera: Cicadellidae), and its con geners. J Insect Behav 5:109–122 Larsen KJ, Vega FE, Moya-Raygoza G Nault LR (1991) Ants (Hymenoptera: Formicidae) associated with the leaf hopper Dalbulus quinquenotatus (Homoptera: Cicadel lidae) on gamagrasses in Mexico. Ann Entomol Soc Am 84:498–501 Moya-Raygoza G (1995) Fire effects on insect associated with the gamagrass Tripsacum dactyloides in Mexico. Ann Entomol Soc Am 88:434–440 Moya-Raygoza G, Nault LR (2000) Obligatory mutualism between Dalbulus quinquenotatus. (Homoptera: Cicadel lidae) and attendant ants. Ann Entomol Soc Am 93:929–940 Moya-Raygoza G, Larsen KJ (2001) Temporal resource switching by ants between honeydew produced by the fivespotted gamagrass leafhopper (Dalbulus quinquenotatus) and nectar produced by plants with extrafloral nectaries. Am Midl Nat 146:311–320 Triplehorn BW, Nault LR (1985) Phylogenetic classification of the genus Dalbulus (Homoptera: Cicadellidae), and notes on the phylogeny of the Macrostelini. Ann Ento mol Soc Am 78:291–315

Gallinipper This name is sometimes applied to any large mos quito, but it is more correctly applied to Psorophora

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ciliata, a large and ferocious mosquito inhabiting most of the New World. Apparently it is America’s largest mosquito. It is distinguished not only by its large size and painful bite, but by its hairy or shaggy legs. Interestingly, an American warship was named Gallinipper. It was part of a “mosquito fleet,” a group of small boats, equipped with both sails and oars, which operated from Florida and patrolled the Caribbean in pursuit of pirates in the 1820s.

Gamete A germ or reproductive cell, i.e., the sperm and ovum or egg.

(which later was renamed Naturhistorisches Museum) and by 1881 had begun publishing on the taxonomy of Coleoptera. These early publications gained him acclaim, and in 1898 he was named Kustos in the zoology department, in 1904 head of the zoology department, and in 1906 director. In 1881 he became one of the founders of the journal Wiener Entomolo gische Zeitung, and served as one of the editors for three years. His major work, a four-volume book “Die Käfer von Mitteleuropa” (1892–1905), was unfin ished because of his early death, in Vienna on June 5, 1912. The published volumes are still widely used.

Reference Herman LH (2001) Ganglbauer, Ludwig. Bull Am Mus Nat Hist 265:68–69

Gamma Taxonomy Ganglion (pl. ganglia)

Study of the evolution and biology of taxa.  Alpha Taxonomy  Beta Taxonomy

Ganglbauer, Ludwig Ludwig Ganglbauer was born in Vienna on October 1, 1856. By the age of six, he had become interested in plants and beetles. He was educated at the Schot tengymnasium in Vienna, obtained a teaching diploma in zoology and botany from Universität Wien, and taught for a few years at a high school. He accepted a position at the Wiener Hofmuseum Local interneurons Motor interneurons

A mass of nervous tissue, and the basic functional unit of the central nervous system. Many insects have three thoracic ganglia (the pro-, meso-, and metathoracic ganglia) in the thoracic region, though in others the meso- and metathoracic ganglia are fused. Each thoracic ganglion (Fig. 12) sends motor axons to the leg muscles of its respective segment, and receives input from sensor receptors in the legs. The meso- and metathoracic ganglia innervate the wing muscles. Ganglia also are found in the abdominal segments, though fusion of ganglia occurs here also. Nearly all ganglia support nerves carrying

Intersegmental interneurons

Ventral sensory interneurons Interganglionic neurons (ascending sensory)

Descending interneuron connective Dorsal root (mainly motor) Ventral root (mainly sensory) Sensory axon terminations Ventral connective

Ganglion (pl. ganglia), Figure 12 Diagram showing the position of nervous tracts within a ventral ganglion.

Gene Duplication

both sensory and motor neurons laterally in the insect’s body.

Garden Symphylan, Scutigerella immaculata (Newport) (Symphyla: Scutigerellidae)  Potato Pests and their Management  Symphylans

Gaster The swollen, terminal abdominal segments of Hymenoptera; the region behind the constriction or pedicel.  Abdomen of Hexapods

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Gelechiidae A family of moths (order Lepidoptera). They com monly are known as twirler moths.  Twirler Moths  Butterflies and Moths

Gel Electrophoresis The separation of molecules on the basis of size and electrical charge.

Gena The side of the head (Fig. 13) beneath the com pound eyes. The “cheek.”  Head of Hexapods

Gasteruptiidae A family of wasps (order Hymenoptera).  Wasps, Ants, Bees, and Sawflies

Gastric Caecum (pl. gastric caeca) Bladder-like extensions of the midgut that func tion in food absorption.  Alimentary Canal and Digestion

Gause’s Principle The principle that no two competing organisms can coexist in a stable environment without one species replacing the other. If seemingly equiva lent species do co-exist, this implies that there are differences in their niches.

Gelastocoridae A family of bugs (order Hemiptera). They some times are called toad bugs.  Bugs

Gene Amplification The production of multiple copies of genes in order to increase the rate of expression of a gene. Numerous genes are amplified in the developing oocyte of the mothers ovaries, providing for rapid translation of the genetic message into proteins for rapid embryonic development.

Gene Cloning Insertion of a fragment of DNA containing a gene into a cloning vector and subsequent propagation of the recombinant DNA molecule in a host organ ism. Recently, cloning of a DNA fragment by the polymerase chain reaction has simplified the technology.

Gene Duplication The duplication of a DNA segment coding for a gene; gene duplication produces two identical

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Lateral ocellus

Compound eye Postocular area Cervix Gena

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Cervical sclerites Tentorial suture Basimandibular sclerite Maxilla Labium

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Gena, Figure 13 Side view of the head of an adult grasshopper, showing some major elements.

copies which may retain their original function allowing the organism to produce larger amounts of a specific protein. Alternatively, one of the gene copies may be lost by mutation and become a pseudogene or a duplicated gene can evolve to perform a different task.

Gene Expression The process by which the information carried by a gene is made available to the organism through transcription and translation.

Gene Flow The movement of genes within and among popu lations as a result of cross fertilization.

Gene Gun A method of propelling microscopic particles coated with DNA into cells, tissues, and organelles to produce transformation of the recipients.

Gene Library A collection of recombinant clones derived from genomic DNA or from the cDNA transcript of an mRNA preparation. A complete genetic library is sufficiently large to have a high probability of con taining every gene in the genome.

Gene Regulation The mechanisms that determine the level and tim ing of gene expression.

General-Use Pesticide This terminology was developed by the US Envi ronmental Protection Agency to describe pesti cides that are considered to be sufficiently safe that they can be used by the public without special training. Pesticides in this class can be purchased and used without license or permit. In contrast, more toxic or hazardous material are classified as “restricted-use pesticides” and can be purchased and used only by persons who are certified by the

Genetic Modification of Drosophila by P Elements

appropriate regulatory agency in the state in which they work.  Insecticides  Regulations Affecting Use of Pesticides

Generalist An insect that occupies a broad niche, or con sumes a wide range of food.

Generation The length of time from any given life stage to the same stage in its offspring, though it is usually considered to be egg to egg or adult to adult.

Genetic Modification of Drosophila by P Elements marjorie a. hoy University of Florida, Gainesville, FL, USA It became possible to genetically modify Drosophila melanogaster using recombinant DNA methods in 1982 when P elements (described below) were iden tified and genetically altered to serve as mechanisms (vectors) for inserting genes into the nuclear genome of Drosophila. The use of P-element vectors provides a powerful tool that has modernized Drosophila genetics and made it possible to study the role of many genes important in development and behavior. In addition, the P-element system has served as a model for scientists wanting to geneti cally modify other insects for use in pest manage ment programs (Transgenic Insects).

P Elements are Disposable Elements P elements are transposable (movable) elements that have been harnessed as a tool for genetically

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modifying the fruitfly Drosophila melanogaster in a consistent manner. Transposable elements are independent genetic elements that can move within and between genomes; some call them selfish genetic elements. The development of P elements as tools (vectors) for inserting genes into D. melanogaster has revolutionized research on this important model insect, allowing funda mental studies of development and evolution. Intact P elements are 2,907 bp long and encode a single polypeptide that has transposase (an enzyme that facilitates the movement of the element from one chromosome to another) activ ity. There are four exons (DNA sequences that are transcribed into protein, numbered from 0 to 3) flanked by inverted repeats 31 bp long. The pres ence of intact inverted repeats is required if the P element is to transpose (move). Multiple copies of P elements (30–60) are dispersed throughout the genome of certain strains (called P) of D. melanogaster, but are not active because transposition is suppressed by factors in the P cytotype. Many P elements in D. melanogaster, and other Drosophila species, have some sequences deleted (are mutated), which also makes them incapable of transposing. Movements of P elements cause mutations by inactivating genes, altering rates of transcription, or developmental- or tissue-specific gene expres sion. P-element movements can break chromo somes and cause chromosome rearrangements and germ cell (oocyte or sperm) death. Transposi tion of P elements in somatic cells reduces the life span of D. melanogaster males, as well as reducing fitness, mating activity and locomotion.

Hybrid Dysgenesis P elements initiate a syndrome called hybrid dysgenesis in D. melanogaster. Hybrid dysgenesis occurs when males from a strain that contains P ele ments (P males) are mated with females lacking P (M females). Their progeny have high rates of mutation, chromosomal abnormalities and, sometimes, are

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completely sterile. These abnormalities are caused by movement of P elements in the chromosomes of the ovaries or testes. The reciprocal cross does not generate hybrid dysgenesis because the P female’ s cytotype suppresses movement of the P elements.

CATGATGAAATAACATAAGGTGGTCCCGTCG 1 31 ATTAACCCTTA 136 126

Exon 0

Exon 1

CGACGGGACCACCTTATGTTATTTCATCATG 2907 2877 TAAGGGTTAAT 2763 2773

Exon 2

Exon 3

1

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Genetic Modification of Drosophila by P Elements, Figure 14 P-element vector diagram.

P Element Structure Varies Many P elements in the Drosophila genome are defective. Some have internal deletions and are unable to produce their own transposase but, if they retain their 31 bp terminal repeats, they can move if supplied with transposase by intact P ele ments. P elements with defective 31 bp terminal repeats are unable to move because these repeats are the site of action of the transposase enzyme and important in movement and insertion of the elements into the chromosomes.

Transposition Method P elements move from site to site in the genome (jump) by a “cut and paste” method. When a P jumps, it leaves behind a double-stranded gap in the DNA. The gap is repaired by using a matching sequence as a template. This matching sequence can occur on the sister chromatid or elsewhere in the genome. If the transposition occurs in an individual that is heterozygous for the P insertion, and the matching site on the homologous chromosome is used as the template for DNA replication and repair, there can be a precise loss of the P element sequence in the origi nal site. There is no net loss in the genome because the P element has simply changed locations. If a P jumps after the chromosomes have duplicated, but before the cell divides, one of the sister chromatids will still have a P in its original position. In this situation, the homologous P may serve as the template for filling in the (Fig. 14) hole left when the P moved to a new position elsewhere in the genome. Under these circumstances, the number of P elements in the genome is increased by one. The P element is replaced in its original site

by gap repair and now is present in a new site in the genome, as well. The cut and paste mechanism of transposition implies that P elements don’ t have to confer an advantage on the organism to invade and persist in the genome. In fact, a mathematical simulation model indicates that P elements can become fixed in popu lations even when fitness is reduced by 50% and many laboratory studies have shown that colonies can change from M to P strains relatively rapidly. The location of the P-element in the chromo some is important in determining the frequency of transposition. Although transposition is moreor-less at random, P-element vectors containing specific gene sequences-show some specificity by frequently inserting near the parent gene (which is called homing). P elements also tend to insert into upstream promoter regions of genes.

How Did P Elements Invade D. melanogaster? P elements are relatively new to D. melanogaster populations. Surveys indicate laboratory strains of D. melanogaster collected before 1950 lack P ele ments, but most colonies collected from the wild within approximately the past 50 years have P ele ments. By contrast, P elements are relatively com mon in many other species of Drosophila. Surveys indicate that very closely-related, full sized and potentially active P elements are in D. willistoni, D. guanche, D. bifasciata and Scaptomyza pallida. P elements have been found in other dipteran families, including Opomizydae and Trixoscelidi dae. Inactive P elements were found in the sheep blowfly Lucilia cuprina (Calliphoridae) and the


housefly Musca domestica (Muscidae). The presence of P elements in families other than Drosophilidae suggests that P elements may be more widely distributed than currently thought. Phylogenetic analyses of DNA sequences from P elements in 17 Drosophila species in the melanogaster species group show that sequences from the P element family fall into distinct subfamilies or clades which are characteristic for particular species sub groups. These clades indicate that vertical transmis sion of P elements has occurred, but in some cases the P phylogeny is not congruent with the species phylogeny. More than one subfamily of P elements may exist within a group, with DNA sequences dif fering by as much as 36%, suggesting that horizontal transfer (movement between species) has occurred. In fact, horizontal transfer may be essential to the long-term survival of transposable elements. P elements invaded D. melanogaster within the past 50 years. The donor species that provided a P element to D. melanogaster is thought to be in the willistoni group, which is not closely related to D. melanogaster. Because these species diverged from each other about 60 million years ago, there should have been sufficient time for considerable sequence divergence in the P elements if they had been present in both genomes prior to divergence (and transmitted vertically). However, DNA sequences of the P elements from melanogaster and willistoni are nearly identical, supporting the hypoth esis of horizontal transfer. It is thought that the invasion of D. melanogaster by P occurred after D. melanogaster was introduced into the Americas. Two mechanisms have been proposed to explain how the P element could have infected D. melanogaster. One involves horizontal transfer and the other involves interspecific crosses. Both D. melanogaster and D. willistoni now overlap in their geographical ranges in Florida and in Cen tral and South America, but they apparently are unable to interbreed. Horizontal transfer could have been effected by a viral, bacterial, fungal, pro tozoan, spiroplasmal, mycoplasmal, or a small arthropod vector (perhaps a hymenopteran para sitoid or predatory mites). One candidate for

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orizontal vector may be the mite Proctolaelaps h regalis. P. regalis is associated with both Drosophila species; it has been found in laboratory colonies and in the field associated with fallen or rotting fruit, which is the natural habitat for Drosophila. Laboratory observations indicate that P. regalis feeds on fly eggs and can make rapid thrusts of its mouth parts into a series of adjacent eggs. This brief feeding on multiple hosts might allow it to pick up DNA from one egg and inject it into another. Mites from colonies of Drosophila with P elements in their genome were analyzed with several molecular methods that indicated the mites carried both P element and Drosophila ribosomal DNA sequences. Mites isolated from M colonies (which lack P elements) lacked P sequences. For the mite P. regalis to have transferred P ele ments to D. melanogaster from D. willistoni, a num ber of events had to occur in the proper sequence. Females of D. melanogaster and D. willistoni had to deposit their eggs in close proximity and mites had to feed sequentially on one and then the other, in the correct order. The recipient egg had to be less than 3 h old, the germ line of the recipient embryo had to incorporate a complete copy of the P, the transformed individual had to survive to adult hood, and the adult had to reproduce. Another potential mechanism for horizontal transfer of P involves interspecific crosses. Crosses between the sibling species D. simulans and D. mauritiana produce sterile males, but fertile females. When F1 females are backcrossed to males of either species, a few fertile males are produced. Hybridization, although rare, occurs between some Drosophila species. Although D. melanogaster and D. willistoni are unable to cross, inter specific crosses may have allowed the transfer of other types of TEs between Drosophila species.

P Element Vectors and Genetic Modification of D. melanogaster P-elements have been genetically engineered to serve as vectors to insert genes into the germ line

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of D. melanogaster. A number of (Fig. 15) different vectors with different genetic characteristics have been produced subsequently. Isolating pure Drosophila lines containing a single P-element insertion with a gene(s) of inter est requires a sequence of steps over several gen erations. A P-element vector containing the gene(s) of interest inserted into it are microinjected into dechorionated eggs along with a helper plasmid that contains a complete DNA sequence coding for the transposase. The helper vector is unable to insert into Drosophila chromosomes by normal transposition methods because it lacks part of one inverted terminal repeat and lacks transposase (the gene of interest is typically inserted into the location of the transposase gene). Embryos used for injection should be in the preblastoderm (an early embryonic stage prior to the development of the ectoderm, endoderm and mesoderm), when the embryo is still a syncytium Go Prepare P vector with wild type gene for white eyes (white +) + Helper plasmid (pπ25.7wc)

Microinject

Male or female embryos with white eyes

Male surviving adults with white males or females

G1 white + males or females

Select only flies with white + eyes and male them

G2 Select white + isolines

G3 localize insert(s), analyze DNA of single insert lines

G4+ Homozygous stocks

G4+ Balanced stocks

Genetic Modification of Drosophila by P Elements, Figure 15 Steps in transformation of D. melanogaster with a P-element vector.

(the nuclei have divided rapidly but cell walls have not formed between them yet). Some of the injected eggs die, but those that survive to produce adults may contain some individuals that contain the introduced gene(s) of interest. These adults (called G0) are mated individu ally to uninjected males or females and their prog eny are reared and evaluated to determine if they carry the injected gene, or any injected “marker” genes designed to allow discrimination between genetically modified and unmodified flies. The resulting G1 progeny will be screened to determine if they carry the gene(s) of interest and the marker genes. Because insertion of the transgenes into the chromosome occurs nearly at random, multiple individual lines of transformed flies will need to be evaluated for fitness and level of expression of the inserted DNA as well as their stability. Insertion of the genes into germ line chromo somes is enhanced if preblastoderm embryos are microinjected. At that stage, the cleavage nuclei are in asyncytium (lacking nuclear membranes) and exogenous DNA can more easily be inserted into the chromosomes. The preblastoderm embryos are in the process of forming the pole cells (cells that will give rise to the ovaries and testes). Inser tion of exogenous DNA into the chromosomes of the germ line results in stable transformation, meaning that the transgenes are likely to be trans mitted each generation. If only somatic cells con tain the introduced genes, the flies cannot transmit the new trait to their progeny. Such adult flies may exhibit the trait, but are only transiently transformed. Only a portion of the P-element vector inserts into the chromosome. The DNA inserted consists of the P sequences contained within the inverted terminal repeats. The plasmid DNA outside the inverted repeats should not insert and is lost dur ing subsequent development. Once transformed fly lines are obtained, the transgenic fly lines should be stable unless trans posase is provided in some manner. Sometimes an experimenter wants to induce movements of the inserted DNA, and secondary transpositions can


be induced if transposase is introduced by inject ing helper elements containing the transposase gene into preblastoderm embryos. Transformation success rates vary from experiment to experiment and experimenter to experimenter. Usually, it is important to obtain at least ten lines containing the gene(s) of interest. This may require microinjecting 600 or more embryos, because survival of embryos after micro injection averages 30–70% and, of these, only 50–60% survive to adulthood (G0). Even after G0 adults are obtained, damage caused by microinjec tion may result in early death or sterility in 30–50% of the adults. Transformation may not take place in all germ line cells in an injected embryo. Usually only a small fraction of the germ line cells of a G0 indi vidual produces transformed G1 progeny. Thus, it is important to maximize the recovery of G1 prog eny from each G0 individual to increase the prob ability of detecting progeny in which integration of P elements occurred. The size of the introduced P element is another factor that may influence transformation success; the larger the construct, the less frequent the insertion. Detailed information on the life history and culture of Drosophila are available in a variety of references, as are detailed protocols for trans forming Drosophila with P-element vectors. The protocols provide complete information on the appropriate equipment for microinjection, how to prepare the embryos for injection, align them on slides, desiccate them, and inject them in the region that contains the pole cells. Directions are available for preparing the DNA for injection and for pulling the very fine glass needles required. P elements have been engineered to provide an array of vectors with different characteristics and functions.

Uses for P Element Vectors When a P-element vector inserts into a nuclear gene, it has been tagged. This allows the researcher

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to isolate and clone specific genes if the altered gene exhibits an altered phenotype in D. melanogaster. This process is called transposon tagging. Genetic engineering with P-element vectors in D. melanogaster also permit the expression of foreign genes from a variety of organisms. P-element vectors also can be used to evalu ate the effects of position on expression of a trans gene by moving stably-inserted transgenes to other sites within the genome. The ability to replace or modify genes in their normal chromosomal locations in D. melanogaster is a very valuable genetic tool.

Transformation of Other Insects by P Elements DNA from D. melanogaster has been introduced into other species of Drosophila with P-element vectors. Unfortunately, efforts to use P-element vectors to transform arthropod species outside the genus Drosophila have failed and research has shifted to the use of other types of transposable element vectors for this purpose. See the entry on Transgenic Arthropods for additional information on this topic.

Evolution of Resistance to P Elements The spread of P elements throughout populations of D. melanogaster during the past 50 years has been remarkable, particularly since intact P ele ments can induce a variety of severe disadvantages in individuals in newly invaded populations. If P elements invade a small population, that popula tion usually goes extinct. If evolution of repression systems (resistance to transposition) fail to occur quickly enough, larger populations also can go extinct. In fact, several types of P repressor systems (resistance mechanisms) have been identified; they either are transmitted cytoplasmically (maternally

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inherited) or through the nuclear genome, in which case the transmission is biparental. The repressor systems have been classified as P, Mʹ or Q. P fly strains have a strong maternally inher ited system called P cytotype. P cytotype is medi ated by a protein produced by differential splicing of the transcript of the complete element. When P females are crossed to a strong P line, less than 10% of the ovaries in their progeny become dys genic, indicating that P strains strongly repress hybrid dysgenesis. By contrast, if P males are crossed to M females, more than 90% of the ova ries in their progeny are dysgenic. Mʹ strains con tain repressor elements of P, as well. Transposition repression in Mʹ strains is due to the KP element. Mʹ strains display intermediate levels of repres sion of dysgenesis when crossed to P males. Both males and females from Mʹ strains are able to pass the repressing factor to their progeny. Q strains can strongly repress transposition and also display a low induction of transposition. Some Q strains show a maternal mode of inheritance of repres sion while others have biparental mode of inheri tance. It thought that a repressor (SR) results from a deletion in the P element. The SR repressor cannot produce functional transposase but can produce the repressor protein and a novel protein, both of which may be involved in Q type repression. Evolution of P, Q and Mʹ repression systems was evaluated during two surveys of D. melanogaster populations conducted along a 2,900 km cline along the eastern coast of Australia. The first survey was conducted in 1983 and the second in 1993. In 1983, P populations were found in the north, Q populations at central locations, and Mʹ populations in the south. After 10 years, Q and Mʹ populations had increased their range at the expense of P lines. The surveyors speculated that the P and Mʹ mechanisms of repression may be early, emergency responses to the harmful effects of transposition by P. The surviving D. melanogaster populations then may have the opportunity to evolve a superior mechanism to improve fitness by acquiring the biparentally transmitted Q repres sion system.

In many species of Drosophila, in which P e lements have been present for a longer time than in D. melanogaster, no complete functional P ele ments have been found. Instead, many populations contain mutated elements which might encode repressor activity. These results reinforce the notion that active transposition of P is highly det rimental to species of Drosophila in the wild.

Using P Elements to Drive Genes into Populations The interest in using transposable elements, such as P, as drivers for inserting engineered genes into natural populations for insect pest control has led to some computer simulation and empirical studies using D. melanogaster as a model system. Several different computer simulations suggest that transposable elements may be used success fully to drive specific genes into pest populations, including populations with different sizes, repro ductive rates, density dependence and transposi tion frequency. Typically an equilibrium was reached quickly (usually within 50 generations), especially if 5 or 10% of the population carried the transposable element. However, if the “sweep” of elements does not occur rapidly, resistance mech anisms might develop that could reduce the effec tiveness of the pest management program.

References Ashburner M (1989) Drosophila. A laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Har bor, New York Carareto CMA, Kim W, Wojciechowski MF, Grady PO, Prokchorova AV, Silva JC, Kidwell MG (1997) Testing transposable elements as genetic drive mechanisms using Drosophila P element constructs as a model sys tem. Genetica 101:13–33 Engels WR (1997) Invasions of P elements. Genetics 145:11–15 Fujioka MJ, Jaynes B, Bejsovec A, Weir M (2000) Production of transgenic Drosophila. In: Tuan RS, Lo CW (eds) Methods in molecular biology, vol 126: Developmental

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biology protocols, vol 2. Humana Press, Totowa, NJ, pp 353–363 Houck MA, Clark JB, Peterson KR, Kidwell MG (1991) Pos sible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis. Science 253:1125–1129 Hoy MA (2003) Insect molecular genetics, 2nd edn. Academic Press, San Diego, CA Karess RE (1987) P element mediated germline transforma tion of Drosophila. In: Glover DM (ed) DNA cloning, vol 2. A practical approach. IRL Press, Oxford, UK, pp 121–141 Roberts DB (ed) (1986) Drosophila. A practical approach. IRL Press, Oxford, UK

Genetic Code The rules that determine which triplet of nucleotides code for which amino acid during translation. There are more than 20 different amino acids and four bases (adenine, thymine, cytosine and guanine). There are 64 potential combinations of the four bases in triplets (4 × 4 × 4). A doublet code would only be able to code for 16 (4 × 4) amino acids. Since only 20 amino acids exist, there is redundancy in the system so that some amino acids are coded for by two or more different triplets (codons).

Genetic Control A method of pest control that uses strains of insects with genetic mutations rendering them sterile or disadvantaged. When released into the natural populations of the target insect, the sterile insects mate with wild insects and produce sterile or disadvantaged offspring.

Genetic Distance A measure of the evolutionary divergence of dif ferent populations of a species, as indicated by the number of allelic substitutions that have occurred per locus in the two populations. The most widely used measure of genetic distance is that of Nei (1972), D = -ln(I).

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Genetic Engineering The deliberate modification of genes by man. Also called gene splicing, gene manipulation, recombi nant DNA technology.

Genetic Linkage Genes are located together on the same chromosome.

Genetic Marker An allele whose phenotype is recognized and which can be used to monitor the inheritance of its gene during genetic crosses between organisms with different alleles.

Genetic Sexing gerald franz International Atomic Energy Agency, Seibersdorf, Austria Genetic sexing refers to the methodologies enabling the separation of large numbers of insects according to sex (e.g., the separation or killing of females so that an all male population is pro duced). It is especially relevant for the Sterile Insect Technique (SIT) which is used to control or eradi cate key insect pests by introducing genetic steril ity into the target population. The primary active agent in the SIT is the sterile male, although in practice, both sexes have been released. A role for the sterile female in the SIT was sometimes debated, but direct evidence shows that females do not contribute significantly to the sterility induced in the wild population. In fact, releasing both sexes together at the high overflooding ratios required for the SIT to be effective leads to assortative mat ing among the released flies and, consequently, dilutes their effectiveness.

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Genetic sexing can be achieved by utilizing natural differences between males and females (e.g., the time of emergence of tsetse flies, or the size of the pupae of certain Lepidoptera and mosquitoes). If such differences do not exist, then specific strains have to be developed using classi cal Mendelian genetic techniques. Two indepen dent genetic modifications are required, the induction of a mutation that can be used as a selectable marker (e.g., affecting pupal color, or temperature dependent viability), and a chromo some re-arrangement (reciprocal Y-autosome translocation) that links the selectable marker to the male-determining Y chromosome. The most advanced and operational genetic sexing strains (GSS) are available for the Mediterranean fruit fly, Ceratitis capitata (medfly). In this species, two mutations, white pupae (wp) and a temperature sensitive lethal (tsl), are used either to separate the sexes at the pupal stage using optical sorting machines, or to kill the females at the embryo stage by incubating the eggs at slightly elevated temperatures. Both mutations are found on chro mosome 5. In the males of a GSS, the wild type alleles of these selectable markers, wp+ and tsl+, are linked to the Y chromosome.

Structure of GSS Based on the Selectable Markers wp and tsl

the useful life of a GSS in mass rearing factories. The structure of the translocation also deter mines the rearing efficiency. Ideally, the sterility linked to such chromosome re-arrangements occurs as early as possible with minimal affect on the rearing process/quality. The choice of the most appropriate selectable marker influences the cost effectiveness and the accuracy of the sex ing procedure. The tsl-based strains currently in use in most medfly facilities allow females to be killed with an accuracy of 99.5% even at produc tion levels of over 500 million males per week, and only inexpensive equipment (a water bath) is needed. For the application of the SIT, the use of GSS offers the following advantages: ··

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The structure of this Y-autosome translocation determines the stability of the GSS over time. Genetic recombination in the male between the selectable marker and the translocation break point, leads to a reversal of the male and female phenotypes. Over several generations, such recombinants can accumulate and the GSS reverts to a standard bi-sexual strain. By choosing trans locations where the selectable marker and the breakpoint are close together, and by incorporat ing recombination suppressors (inversions), GSS can be generated that are stable enough for large scale rearing as required for the SIT. The inclu sion of a Filter Rearing System greatly increases

Sterility is introduced more efficiently into the target population. Data show that 3 to 4 times more sterility can be induced if only sterile males are released. Production, handling and release costs are reduced. Only the active agents, the males, in the SIT have to be dealt with. Monitoring costs, in combination with female specific traps, are reduced, as only wild females are trapped and not sterile males. The males can be aged before release without mat ing, and as a consequence, they are released closer to sexual maturity. Sterile stings by females are eliminated, and SIT can be used for control as well as eradication.

GSS for the medfly are now used in most of the mass rearing facilities worldwide. In 2001, the overall production capacity was 1,400 million males per week. Research is ongoing to generate improved GSS (e.g., by introducing a marker for the discrimination of wild and released flies). In the future, it may be possible to use genetic trans formation techniques to produce GSS for SIT pro grams. In addition, efforts have begun to construct GSS for other key pest species such as the screw worm fly.  Sterile Insect Technique

Genetic Transformation

References Fisher K, Caceres C (2000) A filter rearing system for mass reared medfly. In: Tan KH (ed) Area-wide control of fruit flies and other insect pests. Joint Proceedings of the 1998 International Conference on Area-wide Control of Insect Pests and of the Fifth International Symposium on Fruit Flies of Economic Importance. Penang, Malaysia, pp 543–550 Franz G, Gencheva E, Kerremans Ph (1994) Improved stabil ity of sex-separation strains for the Mediterranean fruit fly, Ceratitis capitata. Genome 37:72–82 Knipling EF (1959) The sterile male method of population control. Science 130:902–904 McInnis DO, Tam SYT, Grace C, Miyashita D (1994) Popula tion suppression and sterility rates induced by variable sex ratio, sterile insect releases of Ceratitis capitata (Dip tera: Tephritidae) in Hawaii. Ann Entomol Soc Am 87:231–240 Rendon P, McInnis DO, Lance DL, Stewart J (2000) Compari son of medfly male-only and bisexual releases in large scale field trials. In: Tan KH (ed) Area-wide control of fruit flies and other insect pests. Joint Proceedings of the 1998 International Conference on Area-wide Control of Insect Pests and of the Fifth International Symposium on Fruit Flies of Economic Importance. Penang, Malaysia, pp 517–525 Robinson AS, Franz G, Fisher K (1999) Genetic sexing strains in the medfly, Ceratitis capitata: development, mass rearing and field application. Trends Entomol 2:81–104

Genetic Transformation alfred m. handler USDA, Agricultural Research Service, Gainesville, FL, USA Genetic transformation is a process that involves the introduction and expression of foreign genes in a host organism. This expression can result from the extrachromosomal, or episomal, presence of genes in nuclei that may persist if the introduced DNA has a mechanism for replication. Extrachro mosomal expression, however, is most often tran sient as the DNA becomes diluted with cell division. Expression also can result from the integration of foreign DNA into somatic chromosomes that can persist through the lifetime of the organism, but not be inherited. Alternatively, foreign genes may

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be stably inherited if incorporated into the genome of the germ-line, known as germ-line transforma tion. This is the most common type of genetic transformation in insects. Transient or somatic transformation can be achieved in several ways, and most often is used for testing promoter regulatory sequences. Most simply, DNA, usually in the form of circular plas mid molecules, is introduced into tissue by microinjection, biolistic bombardment, or elec troporation. The DNA within those plasmids that is taken up into nuclei usually are subject to transcription similar to chromosomal DNA. DNA also can be integrated into viral vectors that may persist extrachromosomally or integrate into somatic chromosomes, and this presents an effec tive means of transient gene expression. Viral vectors for this purpose include densoviruses, subgenomic Sindbis virus, and pantropic Molo ney murine leukemia virus (MoMLV). Transient expression in a foreign host also is possible by gene expression from bacterial symbionts in what is called “paratransgenesis.” This may be inherit able if the genes of interest are stably incorpo rated into the symbiont, and if the symbiont population is inherited. Examples of paratrans genesis include the expression of foreign genes in the bug, Rhodnius prolixis, via the bacterial sym biont Rhodococcus rhodnii, and the potential for foreign gene expression in Wolbachia. Germ-line transformation that is stable and inheritable most commonly is achieved using transposable element, or transposon, based vector systems. This was first developed for Drosophila melanogaster using the P element transposon dis covered in the same species. The P element belongs to a class of transposons that transpose in a precise or nearly precise fashion by using a DNA interme diate. These elements share general structural fea tures including inverted terminal repeat sequences that surround a transcriptional unit that encodes a transposase enzyme. Transposases act at or near the terminal sequences to catalyze the transposi tion process that includes excision of the entire element from one chromosomal site and insertion

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Genetic Transformation

into another site. All of the transposons currently in use for germ-line transformation belong to this general class of elements, and are used in a binary vector-transposase helper system. In this system the transposon vector plasmid includes the inverted terminal repeat sequences and subtermi nal sequences required for mobility that surround a selectable marker gene and other sequences of interest. The transposase gene within the vector is either deleted or made defective, and vector trans position depends upon a separate helper plasmid that includes the complete transposase gene but not the terminal sequences necessary for integra tion. Thus, when transiently expressed in the germ cells, the helper transposase can catalyze chromo somal integration of the vector, but is lost in sub sequent cell divisions allowing the vector integration to remain stable. Currently, the two transposon systems devel oped for Drosophila melanogaster transformation, based on the P and hobo elements, do not function or are highly inefficient in other insect species. Four other transposon systems, discovered in other Drosophila species or other insects, function in a wide range of insects including Drosophila. These include the Hermes element from Musca domestica, the mariner Mos1 element from Drosophila mauritiana, Minos from Drosophila hydei, and piggyBac from Trichoplusia ni. Together, these systems currently have been used for germ-line transformation of more than 20 species within the Diptera, Lepidoptera, Coleoptera, and most recently, the Hymenoptera. A critical component of transformation is the use of selectable marker systems used to identify transformed, or transgenic, individuals. Eye color markers are used routinely in Drosophila, and sim ilar markers were used in the first transformation of tephritid fruit flies and mosquitoes. This was possible owing to the existence of mutant eye color strains and their wild type alleles cloned as recom binant DNA. Vectors carrying the wild type marker gene integrated into a mutant host strain allow transformed insects to be identified by visible detection of their wild type eye-color phenotype.

Later transformations in species not amenable to such “mutant rescue” selections relied on the use of dominant-acting visible marker genes. These include the green fluorescent protein (GFP) from the jellyfish, Aequora victoria, and variants of this gene that emit blue (BFP), yellow (YFP), and cyan (CYP) light under epifluorescence optics. The most recent fluorescent protein in use is the DsRed fluorescent protein from the coral Discosoma striata. Chemical and drug-resistance genes also have been used as dominant-acting selections, but these often have proven to be unreliable owing to natural resistance mechanisms resulting in the selection of non-transformed individuals. In addition to the initial selection of transfor mant insects by marker detection or selection, transformation must be verified by molecular tests that include DNA Southern hybridization, DNA sequencing of the chromosomal integration site, and chromosomal in situ hybridization. These tests confirm chromosomal integration, determine the number of integrations, and assess whether integration has occurred by a transposon-mediated process. The latter confirmation is possible since most transposons duplicate their insertion site sequence, with some transposons integrating solely into a defined nucleotide sequence such as TA or TTAA. In some instances vectors integrate by a random or fortuitous recombination event resulting in integration of the entire vector plas mid, and often in a rearranged fashion. Such inte grations can be useful, but may be problematic since rearrangements can disrupt genes within the vector, and in some cases the selection marker may remain intact while other genes of interest become nonfunctional. The potential for vector integra tion by recombination exists for all insect species, but thus far it is most prevalent in mosquitoes. Transgenic insects have a wide potential of uses for basic biological analysis and practical application for pest and beneficial species. Transposon-mediated germ-line transformation is especially useful for insertional mutagenesis for functional genomics analysis. Transposon vectors are mutagenic since they can disrupt gene function

Gene Transfer

as a result of chromosomal insertion. Genes and regulatory sequences of interest that are inter rupted in this way can be identified by a mutant phenotype or reporter gene expression, and iso lated by probing for or amplifying the transposon vector sequences. Numerous genes and genetic pathways involved in development and behavior have been investigated in this way in Drosophila, and the availability of transformation vectors for nondrosophilid species now makes the use of these methods, and sophisticated genetic analysis, possible for a wide range of insects. In addition to further investigating insect genetics and biology by functional genomics studies, strategies also are being modeled and tested in Drosophila for the use of transgenic insects for biological control. The first of these will improve existing programs such as the sterile insect technique (SIT) by creating strains that are genetically marked, and allow for genetic-sexing (due to female lethality) or male sterility. Sexing and male sterility should occur in response to a conditional or suppressible gene expression sys tem so that the strain could breed normally under permissive conditions. Of considerable interest is the possibility for new strategies for biocontrol, also based on conditional systems integrated into transgenic strains, that result in the death of the released insects and their offspring in response to changes in diet or environmental conditions. The most common strategies at present include those utilizing a lethal gene expression system that is suppressed by the antibiotic tetracycline, or its analogs, which can be provided in diet but is not present in the field. Other strategies include use of temperature sensitive lethal genes that result in death of host insects at elevated field tempera tures, but where strains can survive at lower laboratory rearing temperatures. The greatest challenge for the effective use of transgenic insects in such highly promising strate gies will be the comprehensive ecological risk assessment necessary for the field release of such strains. Transposons that are used as vectors are naturally mobile genetic elements, and many have

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become distributed among insects and other spe cies by horizontal transfer. Thus, a primary concern for their use in practical application will be the potential for vector movement into unintended host organisms. Vector mobilization or instability also will have serious consequences relating to the effectiveness of the transgenic strain, since the desired traits will be lost with the vector. These con cerns for vector stability are diminished by use of vectors that are defective, so that they can be mobi lized only by an exogenous source of transposase, or helper plasmid, such as that used for the trans formation event. While the helper transposase should not persist in the host, the same or related transposon system may exist in the host or a symbi ont or infectious organism resulting in mobiliza tion, or instability, of the vector. Methods to more thoroughly evaluate vector stability, and the cre ation of new vectors that cannot be re-mobilized, will be our greatest challenge for the effective use of genetic transformation techniques to control pests and improve beneficial insect species.

References Atkinson PW, Pinkerton AC, Brochta DAO (2001) Genetic transformation systems in insects. Annu Rev Entomol 46:317–346 Handler AM (2000) An introduction to the history and meth odology of insect gene transfer. In: Handler AM, James AA (eds) Insect transgenesis: methods and applications. CRC Press, Boca Raton, FL, pp 3–26 Handler AM (2001) A current perspective on insect gene transfer. Insect Biochem Mol Biol 31:111–128 Handler AM, James AA (2000) Insect transgenesis: methods and applications. CRC Press, Boca Raton, FL O’ Brochta DA, Atkinson PW (1996) Transposable elements and gene transformation in non-drosophilids. Insect Biochem Mol Biol 26:739–753

Gene Transfer The movement of a gene or group of genes from a donor to a recipient.

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Gengidae A family of bugs (order Hemiptera, suborder Ful goromorpha). All members of the suborder are referred to as planthoppers.  Bugs

Geniculate Elbowed or abruptly bent. When used with anten nae it is equivalent to elbowed antennae.

Genitalia The modified abdominal segments used in copu lation and release of sperm or eggs.

Genome The total complement of DNA in an organism. The total genetic composition of the chromosomes.

Genomes of Insects marjorie a. hoy University of Florida, Gainesville, FL, USA The total complement of DNA in an insect is the genome. Nuclear genomes in insects consist of the chromosomes, consisting of DNA and proteins. The nuclear genome is the largest contributor of genetic information within an insect. However, mitochondria, which are organelles in the cyto plasm, also are components of the genome. Mito chondria are derived from bacteria that became essential symbionts of eukaryotic organisms and contain a number of genes essential to the insect. Finally, in addition to the nucleus and mitochon dria, many insects contain intracellular and extra cellular microorganisms that provide essential services to the insect. Symbionts may be bacteria, viruses, fungi or spiroplasmas that live in or on

their insect hosts. Many insect symbionts are unable to survive outside their host and many insects cannot survive without the services of their symbionts. Thus, insects contain genetic informa tion from several sources.

Nuclear Genome Size and Content The nuclear genome is the most important and largest source of genetic information in the insect. However, the nuclear genome size in arthropods seems to bear little relationship to the complexity of arthropod morphology or to the number of genes encoded. Nuclear genome size varies widely among insects, with up to 250-fold differences in C values known. C stands for constant or charac teristic and denotes the fact that the DNA content (size) of the haploid nuclear genome is fairly con stant within a species. C values vary widely among insect species. Size is usually measured in picograms (pg) of DNA or in kilobases (kb) of DNA sequence. For example, the locust Schistocerca gregaria has a C value of 9,300,000 kb, 52-fold more than that of the fruitfly Drosophila melanogaster yet it is unlikely that the locust is more complex geneti cally. Likewise, nuclear DNA content varies by five-fold among tenebrionid beetle species. Genome size also can vary within insect spe cies; diploid cells in the mosquito Aedes albopictus contain 0.18–6 pg of DNA and C values vary by three-fold (0.62–1.6 pg) among different popula tions. The amount of DNA in insect cells is diffi cult to measure because many tissues are polyploid (containing more than the normal two copies of each chromosome), with different tissues having different degrees of ploidy. DNA consists of four types of nucleotides containing the bases guanine (G), cytosine (C), thymine (T) and adenine (A). The base ratios in insect DNA are lower than those found in verte brates, with guanine + cytosine bases (G + C) comprising from 32 to 42% of the DNA bases, compared to 45% for vertebrates. If DNA base

Genomes of Insects

composition were random, 50% of arthropod DNA would be G + C.

Sequencing Nuclear Genomes The entire nuclear genomes of several model species, including humans, the mouse, the fruitfly Drosophila melanogaster and the nematode Caenorhabditis elegans, have been sequenced in an effort to understand the evolution of genes and genome function. To make the immense amounts of DNA sequence data available to scientists, databanks for depositing the sequences are expanding rapidly. There are three major database sites on the world wide web: the DNA Data Bank of Japan (DDBJ), the European Molecular Biology Laboratory Nucleotide Sequence Data Library (EMBL) and the GenBank Genetic Sequence Data Bank (GenBank). Subsets of the databases also have been organized. For example, there is a database of mitochondrial DNA sequences, a eukaryotic promoter database, a database of restriction enzymes, a database for intron sequences and a database for homeodomains. The nuclear genome of only one insect, Drosophila melanogaster, had been sequenced completely by the date of this writing (2002). The genomes of other species may be sequenced in the future when costs for sequencing decline. The D. melanogaster genome contains approximately 180 megabases (Mb or million bases) of DNA located on four chro mosomes. A third of the DNA is noncoding hetero chromatin, meaning that it does not code for a protein. Heterochromatin typically is found in the centromeres, telomeres and other regions of the chromosomes that do not contain functional genes. Heterochromatin was named this because it stains differently than euchromatin, which is DNA that contains coding sequences. The 120 Mb of coding DNA is on the two large autosomes and the X chro mosome; the fourth chromosome is mostly hetero chromatin, with only about 1 Mb of coding DNA. Prior to the start of the Drosophila Genome Project, approximately 3,800 different D. melanogaster genes had been mapped and many had been

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associated cytogenetically with one of the 5,000 bands visible on stained polytene salivary gland chromosomes. Approximately 3,000 transcription units (DNA sequences that are transcribed into messenger RNA) had been placed on the cytoge netic map by localizing the DNA on specific poly tene chromosomes by a molecular process called in situ hybridization. Nearly 10% of the total, 1,300 genes, already had been cloned and sequenced by individual laboratories. The Genome Project initially was controversial because some feared that it would take funding away from individual research projects, would cost too much, and take too long. Despite this controversy, a Drosophila Genome Project was initiated as a col laborative effort among academic and government scientists with public funding. Later, a commercial company (Celera) initiated its own Drosophila Genome Project using a different approach. The actual sequencing of the Drosophila genome by Celera began in May 1999. By late fall of 1999, sequencing was completed and multiple computers had assembled the DNA sequences in order! This amazingly rapid conclusion to the project was facilitated by the availability of the sequences produced by the public consortium. The genome sequences were published in the jour nal Science in March of 2000 and the project rep resents a major scientific milestone. The entire Drosophila sequence is available in GenBank and at FlyBase on the worldwide web. FlyBase is a database of genetic and molecular information and includes information on genes, alleles (varia tions of genes), phenotypes, transposons (movable genetic elements present in the genome), clones, stock lists, the locations of Drosophila workers, and bibliographic references (Table 3). Several unexpected results were found in the Drosophila genome. Early analyses of the Drosophila genome suggest that there are only 13,600 genes, which is slightly fewer than the number found in the nematode Caenorhabditis elegans. This number (13,600) is far fewer than the 30,000 originally estimated for D. melanogaster. However, Drosophila has a relatively large number of

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verlapping genes, so additions eventually may be o made to the total. Immediately after obtaining the D. melanogaster-genome sequences, a comparison was made to the genomes of C. elegans and the yeast S. cerevisiae in the context of cellular, developmental and evolutionary processes. These comparisons indi cated there are many genes left to be studied in Drosophila. Analysis of the Drosophila sequences also indicated this insect is surprisingly relevant to the study of genes and metabolic pathways involved in tumor formation and development in humans. Many of the well-studied signal pathways in tumor development in humans are conserved between flies and humans: at least 76 Drosophila genes are homologs to mammalian cancer genes and are under intensive study. Furthermore, 178 (62%) of the 287 known human disease genes can be found in Drosophila, including genes causing neurologi cal problems (Alzheimer’ s disease, Huntington’ s disease, Duchenne muscular dystrophy, juvenileonset Parkinson’ s disease). In addition, analysis of the D. melanogaster genome may prove useful in the study of renal, cardiovascular, metabolic and immune diseases, malformation syndromes, and cancer. The D. melanogaster genome represents a treasure trove of information that can be mined for years to come.

Chromosome Systems in Arthropods Many insects are diploid (2n) in their somatic cells and haploid (n) in their gametes (eggs or sperm). Diploidy means that each chromosome type is represented twice. Diploid insects undergo meio sis prior to producing haploid eggs and sperm. Some insect groups are parthenogenetic (females are able to reproduce without mating) and may be polyploid. Species in the Orthoptera (Blaberidae, Tettigoniidae), Hemiptera (Coccidae Delpha cidae), Embioptera (Oligotomidae), Lepidoptera (Psychidae), Diptera (Chamaemyiidae, Chironomidae,

Psychodidae, Simuliidae), Coleoptera (Ptinidae, Chrysomelidae, Curculionidae), and Hymenoptera (Diprionidae, Apidae) may be parthenogenetic. Polyploid insects usually are 3n or 4n, but exceptions include curculionid weevil species that are 5n and 6n. Parthenogenesis has not been found in the Diplura, Protura, Odonata, Plecoptera, Dermaptera, Grylloblattodea, Zoraptera, Megaloptera, Mecoptera and Siphonaptera, although it is not clear that spe cies in these groups have been examined carefully for this attribute.

Parthenogenesis Parthenogenesis is reproduction in which prog eny are produced by unfertilized females. The mechanisms involved in parthenogenesis are diverse but can be divided into three major types: arrhenotoky, thelytoky, deuterotoky. Deuterotoky involves the development of unfertilized eggs into either males or females, and at least one insect, a mayfly, is reported to exhibit facultative deuterotoky. In the more common arrhenotoky, insects are haplo-diploid, with males developing from unfertilized eggs and females developing from fertilized eggs. The entire order Hymenoptera and many species in the Hemiptera, Thysanoptera, and Coleoptera are arrhenotokous. When the male of a species is haploid, its germ line nuclei contain half the number of chromosomes pres ent in the corresponding diploid nuclei of the female and meiosis is modified so that the sperm remain haploid and do not undergo the typical reductional division. Insects that exhibit thelytoky have females only. Thelytoky has arisen repeatedly in evolution and consists of several types. Thelytoky can be induced experimentally in a number of ways. In some cases of thelytoky, eggs only develop after penetration by a sperm (pseudogamy or gynogen esis), but the sperm nucleus degenerates without fusing with the egg nucleus so that the sperm makes no genetic contribution to the embryo. The sperm may be derived from the testis or ovotestis

Genomes of Insects

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of a hermaphrodite or from a male of a different, but closely related, species. Thelytoky may be the sole mode of reproduc tion in a species or it may alternate with sexual reproduction in regular manner (cyclical thely toky). Cyclical thelytoky is found in aphids, gall wasps and some cecidomyiids. In species that reproduce by cyclical thelytoky, genetic recombi nation is possible. In species with complete thely toky, there is no way in which mutations that have occurred in two unrelated individuals can be com bined in a third. Thelytokous reproduction can be induced in the eggs of many insect species by pricking the egg, or by exposing it to chemical agents or heat. In a number of normally bisexual insects, a few eggs deposited by virgin females can hatch spontaneously; the incidence of such egg hatch can be increased by artificial selection. The capacity for artificial parthenogenesis, induced thelytoky, or facultative thelytoky indicates that some capacity for parthenogenesis is probably present in all eggs. Thelytokous species or thely tokous populations of bisexual species have been found in the Diptera, Hymenoptera, Lepidoptera, Orthoptera and Coleoptera. In the Hemiptera, both arrhenotoky and thelytoky occur, but even more complex genetic systems are found. For example, in mealybugs (Pseudococcidae), both males and females develop from fertilized eggs but, in the embryos that develop into males, the paternally derived chro mosomes become heterochromatic (stain differ ently with a dye), are genetically inactive and not transmitted to male progeny. This genetic system has been called parahaploidy. Some method of chromosome imprinting is probably involved to ensure that the paternally derived chromosomes are eliminated in parahaploidy and not the mater nally derived ones.

multiples of the haploid (n) number. The discus sion of chromosome number (ploidy) is confusing because, in most insects, some of the somatic tissues exhibit high levels of endopolyploidy (multiple copies, greater than 2n, of chromosomes may be present in some cells) while other cells may be diploid. For example, haploid male honeybees (which have one copy of each chromosome in their testes cells) have about the same amount of DNA as dip loid females (which are 2n in the ovaries) in some of their other tissues. This increase in chromosome number occurs because nuclei in some of the tissues of the male undergo repeated cell divisions so that equal amounts of DNA are present compared to the diploid (2n) females. In some cases, haploid insect males exhibit higher levels of endopoly ploidy than the females of the same species. Polyploidy of all cells in the body occurs when the chromosome number in an organism increases over the usual diploid (2n) amount, usually by duplicating the number of chromosomes to 3n or 4n. Thus, polyploidy can occur in all cells of an insect or in just some tissues (endopolyploidy). A few insects are polyploid in all tissues, but many have polyploid tissues. For example, the diploid blood cells of the silkworm Bombyx mori contain 1 pg of DNA per blood cell, but a polyploid silk gland cell, which is metabolically much more active, in the same individual contains 170,000 pg of DNA. DNA content within cells also varies with developmental stage. At metamorphosis, the amount of DNA in B. mori declines by 81% after adults emerge from the pupal stage, which is prob ably due to histolysis of the polyploid larval silk glands and other polyploid cells that are not needed by the adult moth.

Endopolyploidy in Arthropods

DNA in the nuclear genome can be coding or non coding. Coding DNA sequences code for enzymes (proteins that facilitate metabolic processes) and structural proteins. Coding DNA is transcribed

Cells within insects may contain the typical dip loid (2n) number of chromosomes or may contain

Noncoding DNA

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into messenger RNA and then translated into pro teins. In addition, the coding DNA is transcribed and the resulting RNA is used directly (without translation into a protein) as transfer RNAs or ribosomal RNAs. Noncoding DNA does not code for any known product, although it may have a function or func tions. Noncoding DNA can constitute 30% to more than 90% of the insect nuclear genome. Noncoding DNA has been called junk or parasitic or selfish. There are several hypotheses to explain its persis tence in nuclear genomes. One suggests that the noncoding DNA performs essential functions, such as regulating gene expression. A second hypothesis is that the noncoding DNA is maintained because it is linked physically to functional genes; the excess DNA is not eliminated because it does not affect fit ness of the organism. A third hypothesis suggests that noncoding DNA is a functionless parasite that accumulates and is actively maintained by selection. A fourth hypothesis is that noncoding DNA has a structural function, perhaps for compartmentaliz ing genes within the nucleus, or for maintaining a structural organization (nucleoskeleton) within the nucleus. The lack of correlation between genome size, complexity and gene number remains a puzzle. Unless the noncoding DNA has a function, it should constitute a load upon the insect and be lost over evolutionary time. Much of the noncoding heterochromatic DNA in insects is repetitive DNA, DNA sequences that are repeated several times to millions of times. Repetitive DNA is found in heterochromatin near centromeres (regions of the chromosomes to which spindle fibers attach so that chromosomes can be distributed to the daughter cells during mitosis or meiosis), telomeres (the ends of chro mosomes) and other heterochromatic regions. Some repetitive DNA sequences are repeated 100 to 10,000 times and include genes that code for ribosomal RNA and transfer RNA. Species vary in the amount of repetitive DNA in their genome. For example, Drosophila melanogaster has about 30% of its genome as heterochro matic DNA, but about 60% of the genome of

Drosophila nasutoides is repetitive DNA. Aphids have small amounts of repetitive DNA, and scien tists have speculated that this reduced amount of repetitive DNA could be associated with a faster development time. Satellite DNA is a type of highly repetitive DNA that differs sufficiently in its base composition from the majority of DNA in an insect that it separates out as one or more distinct bands when DNA is iso lated by centrifugation with cesium chloride. Satel lite DNA is rich in either A + T or in G + C sequences, and is found in long tandem arrays within the heterochromatic regions of chromosomes. Even within an insect family, genome organi zation can vary. Total DNA in the genome of four mosquito species (Anopheles quadrimaculatus, Culex pipiens, Aedes albopictus and A. triseriatus) varies from 0.19 to 0.90 pg with the amount of repetitive elements varying from 0.01 to 0.15 pg. Generally, the amounts of repetitive DNA increase linearly with genome size in these mosquitoes. Intraspecific variation in the amount of highly repetitive DNA was found in A. albopictus colo nies and may be due to differences in the number or type of transposable elements. Transposable elements are independent DNA or RNA elements that can move from one site to another in the genome and between genomes. The amounts of repetitive DNA in mosquitoes varies from 20% in An. quadrimaculatus to 84% in A. triseriatus. Because genome organization of relatively few insect species has been studied, it is difficult to determine the significance of these patterns.

Mitochondria In addition to the nuclear genome, insects contain mitochondria in the cytoplasm. Mitochondrial chromosomes are circular, supercoiled, doublestranded DNA molecules. The mitochondrial chromosome of Drosophila contains approxi mately 18.5 kb of DNA and each mitochondrion contains several copies of the chromosome. Mito chondrial genes in insects lack introns (segments

Genomes of Insects

of DNA in the middle of coding regions that are normally removed prior to translation into pro teins) and intergenic regions (noncoding regions between coding regions) are small or absent. The ribosomes found in the mitochondria are smaller than the ribosomes in the cytoplasm. Mitochon dria contain distinctive ribosomes, transfer RNAs, and aminoacyl-tRNA synthetases. Mitochondria have their own genetic code that differs slightly from the universal genetic code. The complete sequences of a number of insect mitochondria are known, which allows compari sons of the organization and evolution of insect mitochondrial genomes. These complete mito chondrial genome sequences can be found in GenBank. One of the first mitochondria to be completely sequences was that of Drosophila yakuba which was found to have 37 genes: 2 are ribosomal RNA genes, 22 are transfer RNA genes, and 13 are protein genes that code for subunits of enzymes functioning in electron transport or ATP synthesis. Partial DNA sequences of mitochondria have been obtained from many insects and also can be found in GenBank (Table 3). Mitochondrial DNA is thought to be inher ited only through the mother (in the oocyte) and males are not expected to transmit mitochondria to their progeny via the sperm. However, two stud ies have shown incomplete maternal inheritance of mitochondrial DNA occurs in Drosophila simulans. Most eggs and somatic cells contain hundreds or thousands of mitochondria, so a new mutation can result in a situation in which two or more mitochondrial genotypes coexist within an indi vidual (heteroplasmy). Heteroplasmy, however, is

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apparently a transitory state. Thus, the majority of individuals are effectively haploid with regard to the number of types of mitochondria transmitted to the next generation. Mitochondrial DNA evolves faster than single copy nuclear DNA because mitochondria are rela tively inefficient in repairing errors during DNA replication or after DNA damage. In Hawaiian Drosophila, mitochondrial DNA appears to evolve about three times faster than coding sequences in nuclear DNA. Because mitochondrial DNA does not code for proteins involved directly in its own replication, transcription or translation, it often contains a large number of mutations. Mitochondrial DNA has been extensively used for systematics or population genetic studies. Genes can be amplified easily from mitochondria by the polymerase chain reaction (PCR) because there are multiple copies in each cell. Mitochon dria are easier to purify than a specific segment of nuclear DNA.

Transposable Elements Every genome probably contains several types of transposable elements. Transposable elements are genetic elements that can move from one site to another in the genome. Transposable elements have been divided into two classes, those that transpose with an RNA intermediate and those that transpose as DNA. Transposable elements have been found in the genomes of most organ isms, including humans, bacteria, frogs, mice, maize, nematodes, protozoans and insects. An

Genomes of Insects, Table 3 Some relevant world wide web sites that provide information on insect genomes The Interactive Fly is at: sdb.bio.purdue.edu/fly/aimain/1aahome.htm FlyBase is at: flybase.bio.indiana.edu Drosophila Virtual Library is at: ceolas.org/fly/ The SWISS-PROT protein sequence database is available at: http://www.expasy.ch/sprot/http://www. expasy.ch//sprot/ and http://www.ebi.ac.uk/swissprot/ The Protein Information Resource is available at: http://pir.georgetown.edu http: pir.georgetown.edu and http://www.mips.biochem.mpg.de

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organism may contain multiple types of transpos able elements. Most of them may be inactive because they have been mutated or suppressed by the host. Highly mutated transposable elements prob ably are the source of much of the noncoding repetitive DNA. There are numerous types of transposable elements in insects. The ubiquity of transposable elements in the genomes of organi sms has raised a number of unanswered questions about their evolutionary effects. Examples are still being discovered in which new transposable ele ments are in the process of invading and spread ing within insect populations.

Symbionts of Arthropods As noted above, mitochondria are derived from a microbial intracellular symbiont that became dependent upon its host cell early in the evolution of eukaryotes (organisms with a defined nucleus and cytoplasm). The relationship between mito chondria and the eukaryotic cell is now mutualistic and obligatory. Other organisms (viruses, bacteria, rickettsia, spirochaetes) also may have long evolu tionary relationships with arthropods. Some are gut symbionts, while others are associated with the salivary glands and reproductive tracts. Some rela tionships are obligatory, others are not. For additional details about the relationship between microbial genomes (contained within symbionts) and the insect genome.  Symbionts of Arthropods

References Hoy MA (2003) Insect molecular genetics, 2nd edn. Academic Press, San Diego, CA Gray MW, Burger G, Lang BF (1999) Mitochondrial evolu tion. Science 283:1476–1481 Henikoff S (2000) Heterochromatin function in complex genomes. Biochimica et Biophysica Acta 1470:1–8 Mount DW (2001) Bioinformatics. Sequence and genome analysis. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437 Wagner RP, Maguire MP, Stallings RL (1993) Chromosomes: A synthesis. Wiley-Liss, New York, NY White MJD (1973) Animal cytology and evolution, 3rd edn. Cambridge University Press, Cambridge, UK

Genomics The study of genome data. The complete DNA sequences of organisms such as the human, mouse, rat, zebrafish, D. melanogaster, C. elegans and Arabidopsis thaliana can provide a plethora of infor mation on entire families of genes and pathways of interacting proteins.  Proteomics  Structural Genomics  Functional Genomics

Genotype The genetic makeup of an individual (contrast with phenotype).

Genus (pl. genera) The principal subdivision of a family. A group of species that are similar in appearance and appear to have a common ancestry.

Geographic Information System (GIS) A management system for data associated with precise locations.

Geological Time john l. capinera University of Florida, Gainesville, FL, USA The time line that describes the history of the earth has been divided into large blocks of time, but

Geological Time

each large block is normally subdivided, and sub divided again, for convenience (Fig. 16). The gen erally accepted divisions are eon, era, period, epoch, and age. The names given the block of time often have historical significance, and may be associated with occurrence of different fossils. For example, the Phanerozoic eon also consists of three major divisions: the Cenozoic, the Mesozoic, and the Paleozoic eras. The “zoic” part of the word comes from the root “zoo,” meaning animal. “Cen” means recent, “Meso” means middle, and “Paleo” means ancient. These divisions reflect major changes in the composition of ancient faunas, with

each era associated with domination by a particu lar group of animals. The Cenozoic has sometimes been called the “Age of Mammals,” the Mesozoic, the “Age of Dinosaurs,” and the Paleozoic the “Age of Fishes.” This is not entirely accurate, though there is some basis for these designations. Also, unlike most time lines, the time is expressed not only by date, but from the present. Thus, periods or events are commonly described in millions of years ago (mya). Different spans of time on the geological time scale are usually delimited by major geological or paleontological events, such as mass extinctions. For example, the end of the

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Geological Time, Figure 16 A graphical depiction of the geological history of earth (adapted from the Geological Society of America).

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Geological Time

Cretaceous period of the Mesozoic era is marked by the demise of the dinosaurs and of many marine species. The oldest known meteorites and lunar rocks are about 4.5 billion years old, but the oldest portions of Earth currently known are 3.8 billion years old. Sometime during the first 800 million or so years of its history, the surface of the Earth changed from liquid to solid. Once solid rock formed on the Earth, its geological history began. This most likely happened to 3.8–4 billion years ago, but firm evidence is lack ing. The oldest time period, the Hadean eon, is not a geological period per se. No rocks on the Earth are this old, except for meteorites. During the Hadean time, the Solar System was forming, probably within a large cloud of gas and dust around the sun. The Archean eon was marked by formation of land masses as the earth’s crust cooled and plates began to form. The atmosphere was hostile to life as we know it today, consisting mostly of methane, ammonia, and other toxic gases. The only life known from this early period are bacteria and bacteria-like archaea, com mencing about 3.5 billion years ago. Things got interesting only in the Proterozoic eon, when life became more plentiful and the first more advanced life (eukaryotic) forms began to appear and oxygen began to accumulate. Eukaryotic life forms, including some animals, began to appear perhaps as long ago as one billion years ago, but certainly by 500 mya. The Paleozoic era was interesting because well-preserved fossils document this period. The seas were dominated by trilobites, brachiopods, corals, echinoderms, mollusks, and others, and toward the end of this period life appeared on land. On land, the cycads, primitive conifers, and ferns were abundant. The Mesozoic saw the radia tion and disappearance of dinosaurs, mammals appeared, while more advanced land plants such as ginkgos, ferns, more modern conifers, and even tually the angiosperms began to appear. The Cenozoic, the most recent era, is divided into two main sub-divisions: the quaternary and

the tertiary periods. Most of the Cenozoic is the Tertiary, from 65 million years ago to 1.8 million years ago. The Quaternary includes only the last 1.8 million years. The Cenozoic is particularly interesting to biologists because most of the life forms we see today developed in this period. It has been called the “age of insects” due to the development of great diversity, but could also be known as the age of flowering plants, birds, etc.; most of the flora and fauna we see today evolved during this period. The last 10,000 years (the Holocene) is sometimes known as the “age of man” and is also the time period since the last major ice age. The time period before the Holo cene, the Pleistocene, is interesting because though much of the recent flora and fauna is the same as today, some interesting and now extinct megafauna were present, including mastodons, mammoths, saber-toothed cats, and giant ground sloths. The human species, Homo sapiens, also expanded during this time period, and as men tioned previously, there was a significant ice age period. From an entomological perspective, the Phanerozoic eon (Table 4) was an exciting time. Arthropods ventured onto land during the Paleo zoic, perhaps 400 mya, though the Silurian ento mofauna consisted of primitive myriapods and arachnids. Fossil hexapods have been recovered from the Devonian, most notably springtails from chert. Insects proliferated rapidly during the remainder of the Paleozoic and thereafter. Interest ingly, during the Mississippian (also called the Early Carboniferous) we have no fossil evidence of insects, whereas in the Pennsylvanian (also called late Carboniferous) we have numerous records of early (mostly now extinct) insect groups (e.g., prot odonata and protorthopterans from deposits in France). At the close of the Paleozoic, the Permian period, the environment of earth was undergoing significant change, most notably a less tropical climate. Numerous insects from many deposits around the world document over a dozen orders of insects, including the occurrence of “giant” insects.

Geological Time

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Geological Time, Table 4 Important time periods of the Phanerozoic eon (543 million years ago to present) Cenozoic era

Quaternary period (1.8 mya to today)

(65 mya to today)

Holocene Epoch (10,000 years to today) Pleistocene Epoch (1.8 mya to 10,000 yrs) Tertiary Period (65 to 1.8 mya) Pliocene Epoch (5.3 to 1.8 mya) Miocene Epoch (23.8 to 5.3 mya) Oligocene Epoch (33.7 to 23.8 mya) Eocene Epoch (54.8 to 33.7 mya) Paleocene Epoch (65 to 54.8 mya)

Mesozoic Era

Cretaceous Period (144 to 65 mya)

(248 to 65 mya)

Jurassic Period (206 to 144 mya) Triassic Period (248 to 206 mya)

Paleozoic Era

Permian Period (290 to 248 mya)

(543 to 248 mya)

Carboniferous Period (354 to 290 mya) Pennsylvanian Epoch (323 to 290 mya) Mississippian Epoch (354 to 323 mya) Devonian Period (417 to 354 mya) Silurian Period (443 to 417 mya) Ordovician Period (490 to 443 mya) Cambrian Period (543 to 490 mya) Tommotian Epoch (530 to 527 mya)

The Triassic period of the Mesozoic era saw a warming of the earth, and fossil deposits docu ment the occurrence of early insects such as Blat taria and some Orthoptera, Coleoptera, Odonata, Plecoptera, Neuroptera and Grylloblattodea. Tran sition into the Jurassic was not abrupt for insects, and the fossil record documents few marked changes, but increased radiation. The Cretaceous period is notable for the radiation of angiosperms that took place. Because many insects are intimately associated with plants through phytophagy and pollination, they were profoundly affected by the availability of these new resources. Many of the modern taxa became established during this period, though more modern taxa such as some Diptera and Lepi doptera radiated later, in the Cenozoic. One very noteworthy feature of the Cretaceous is the great

availability of amber. The spread of resin-pro ducing trees through this period and into the Tertiary provided an excellent preservation medium for insects. Thousands of species and perhaps 30 orders have been recovered from amber deposits around the world. As insects transitioned from the Cretaceous to the Ceno zoic era, the earth witnessed the appearance of “modern” insect groups such as termites, scale insects, fleas, lice, batbugs, flies, bees, and ants.  Fossil Record of Insects  Amber Insects: DNA Preserved?

Reference Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge, United Kingdom. 755 pp

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Geometer Moths (Lepidoptera: Geometridae)

Geometer Moths (Lepidoptera: Geometridae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Geometer moths, family Geometridae, also called inch worms, are the second largest family of Lepi doptea, with about 21,150 described species from all faunal regions; the actual fauna probably exceeds 26,500 species. The major biodiversity is in the Neotropics, with over 6,500 species described, and the Indo-Australian region with about 6,670 species. The family is in the superfam ily Geometroidea, in the section Cossina, subsec tion Bombycina, of the division Ditrysia. The family is divided into eight subfamilies (recent past classifications mainly used only 6 subfami lies): Archiearinae, Oenochrominae, Orthostixi nae, Ennominae, Desmobathrinae, Geometrinae, Sterrhinae, and Larentiinae. There are a very large number of tribal names used and much study and consolidation of overlapping groups is still needed in order to sort out all the valid tribes among the different faunal regions. Adults small to large

(8–120 mm) (most range 20–45 mm), with head scaling normal; haustellum naked; labial palpi upcurved; maxillary palpi small, 1 to 2-segmented; antennae various but mostly filiform (males usu ally with thicker antennae then females). Wings triangular, usually with somewhat pointed fore wings (sometimes rounded), but sometimes emar ginate or with falcate apex; hindwings more rounded in most species (rarely tailed); a number of genera have brachypterous or apterous females (Fig. 17). Body usually slender and delicate, but robust in some genera. Maculation extremely var ied, but most species with somber hues of brown or gray; occasionally green (especially among Geometrinae) or very colorful among many tropi cal genera (especially in Ennominae). Adults mostly nocturnal, but also some crepuscular and diurnal groups. Larvae mostly leaf feeders, typi cally moving in looping fashion due to reductions in proleg numbers, and many remain motionless when disturbed and resemble small sticks or twigs. Some larvae deposit debris on their bodies to cam ouflage even further (Geometrinae); also known are attacking predaceous larvae (Semiothisa sp.) in Hawaii. Host plants include most all plant families. Some major defoliating pests are known in this family.

Geometer Moths (Lepidoptera: Geometridae), Figure 17 Examples of geometer moths ( Geometridae): top left, (subfamily Ennominae), Macaria monticolaria (Leech) from Taiwan; top right, Nacophora quernaria (J. E. Smith) from Florida, USA; bottom row left, Palyas auriferaria (Hulst) from Florida, USA; bottom row right (subfamily Oenochrominae), Sarcinodes aequilinearis (Walker) from Taiwan.

Germar, Ernst Friedrich

References Hausmann A (2001) The geometrid moths of Europe, vol 1. Introduction: Archiearinae, Orthostixinae, Desmobath rinae, Alsophilinae, Geometrinae. Apollo Books, Sten strup, p 282 (8 pl) Holloway JD (1993–1997) Geometridae. In: The moths of Bor neo. Pt 9–11. Malayan Nature Society, Kuala Lumpur, (Malayan Nature Journal 45:1–309, 85 + 19 pl. (1993); 49:147–326, 26 + 12 pl. (1996); 51:1–242, 90 + 12 pl (1997)) Janse AJT (1932) Family Geometridae. In: The moths of South Africa, Transvaal Museum, Pretoria, 1:90–376, pl. 15 McGuffin WC, Bolte KB (1967–1990) Guide to the Geometri dae of Canada (Lepidoptera). Mem Ent Soc Can 50:1–67 (1967); 86:1–159 (1972); 101:1–191 (1977); 117:1–153 (1981); 138:1–182 (1987); 151:1–252 [Bolte] (1990) Scoble MJ (1999) Geometrid moths of the world: a catalogue. CSIRO, Collingwood, 1400 pp Seitz A (ed) (1912–1954) Familie: Geometridae. In: Die GrossSchmetterlinge der Erde, Kernen, Stuttgart, 4:1–479, pl. 1–25 (1912–1916); 4(suppl.):1–766, pl. 1–53 (1934–1954); 12:1–356, pl. 1–50 (1920–41); 12:1–144, pl. 1–17 (1932–38); 16:1–160, pl. 1–18 (1930–38) Wang H-Y (1997–1998) Geometer moths of Taiwan and its allied species from the neighboring countries, 2 vol. Taiwan Museum, Taipei Xue D, Zhu H, Chu H (1999) Fauna Sinica. 15. Lepidoptera: Geometridae, Larentiinae. Science Press, Beijing, 1063 pp, pl. 25

Geometridae A family of moths (order Lepidoptera). They com monly are known as measuring worm moths or geometer moths.  Geometer Moths  Butterflies and Moths

Geophilous This term, which literally means “ground-loving” is applied to organisms that live on the soil, or favor this habitat.

Georeference Reference to the location on the earth’ s surface based on latitude and longitude coordinates.

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Geotaxis Taxis response with respect to gravity.

Geotrupidae A family of beetles (order Coleoptera). They com monly are known as earth- boring dung beetles.  Beetles

Geridae A family of bugs (order Hemiptera). They some times are called water striders.  Bugs

German Cockroach, Blattella germanica (Linnaeus) (Blattodea: Blattelidae) Blattella germanica is one of the most important nuisance species of cockroaches.  Cockroaches  Urban IPM  School IPM

Germar, Ernst Friedrich Ernst Germar was born in Germany on November 3, 1786. At 21 he moved to Leipzig and bought Hübner’ s insect collection. In 1810 he obtained a doctorate in philosophy from Universität Halle. That was the year when the first part of his (1810– 1812) work “Dissertatio sistens Bombycum spe cies…” was published. In 1911, he traveled to Dalmatia, resulting in a (1817) book “Reise nach Dalmatien.” In 1813 he founded an entomological journal “Magazin der Entomologie” which ran for six years, was interrupted, and resumed publication in 1839–1845, at which time it was merged into “Linnaea Entomologica.” He married

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Germarium

ilhelmine Keferstein in 1815. In 1817, he was W appointed (at first without tenure) professor of mineralogy in Universität Halle. His other great entomological works were (1817–1847) “Fauna insectorum europae” and (1824) “Insectorum spe cies novae…” He died in July 1853.

Reference Newman E (1854) The president’ s address. Trans Entomol Soc London (2) 2:149–150

Germarium An area at the tip of the ovarioles (in females) or sperm follicles (in males) where egg or sperm for mation is initiated.

Germ Band During the blastoderm stage of embryogenesis a region of thickened cells called the germ band forms on the ventral side and elongates. Eventually in differentiates and invaginates.  Embryogenesis

Ghilarov, Mercury Sergeevich bella r. striganova A.N. Severtsov Institute of Ecology and Evolu tion, Moscow, Russia M.S. Ghilarov was born on February 22, 1912, in Kiev (Russian Empire, now the capital of the Ukraine). He was educated at the State University of Kiev (1929–1933) where he specialized in entomology. After graduation from the University, he worked as an entomologist in the Ukrainian Station of Plant Protection. In 1936 he accepted the position of the senior scientific worker in the

State Research Institute of Rubber-bearing Plants in Moscow. He studied ecology of soil insects and influence of soil conditions on the fauna of pests in arable soils. In 1938 he obtained a Ph.D. degree. His further scientific interests turned into studies of general problems of insect adaptations to soil environment. In 1944 he moved to the Institute of Evolutionary Morphology, USSR Academy of Sci ences (now the Institute of Ecology and Evolution, Russian Academy of Sciences) in Moscow where he remained until the end of his life. In the 1940s he developed the concept of the evolutionary role of soil as an intermediate environment in the course of transition of animals from the aquatic to terrestrial life. For this work he gained the degree of Doctor of Biological Sciences. His monograph “The specificity of soil as insect habitat and its role in insect evolution” (1949) served as the theoreti cal basis of soil zoology, the modern branch of soil natural history. In 1956 he founded the Labora tory of Soil Zoology in the Institute, and in the 1950–1960s he organized the broad comparative study of soil entomofauna in different regions of the Northern Palearctic. He found that the ranges of a number of soil-dwelling insects coincide with the particular types of the soil (“Zoological method of the soil diagnostics,” 1965). He headed the taxo nomic study of soil insects and mites which were resulted in “Key of soil-dwelling insect larvae” (1964), and “Key of soil-dwelling mites” (Sarcopti formes, 1975; Mesostigmata, 1977; Trombidi formes, 1978). He published more than 500 scientific papers devoted to various aspects of entomology. From 1973 he was the President of the USSR Entomological Society. In 1974 he was elected as a member of the USSR Academy of Sciences and in 1975 he was appointed the Academician-Secretary of the Division of General Biology of the Academy. Beginning in 1978 he also headed the Department of Invertebrate Zoology in the State University of Moscow. He was engaged in a broad range of international activities. He was a member (starting in 1956) and the Vicepresident (1967) of the Permanent Committee of International Entomological Congresses, and

Ghost Moths (Lepidoptera: Hepialidae)

from 1976–1982 he was the vice-president of the International Union of Biological Sciences. His scientific awards include three USSR State Prizes (1951, 1967, 1980), the Philippo Sylvestry Golden Medal (1965), the Gustav Kraatz Medal of the German Agricultural Academy (1966), a medal of the International Committee on the entomofauna of Middle Europe (1975), a medal of the Zoological Society of France (1976), a medal of the German Academy “Leopoldina” (1977), the I. Mechnikov Golden Medal of the USSR Academy of Sciences (1978) and honorary memberships in entomological societies and acad emies of sciences of a number of countries. He passed away in Moscow, USSR, on March 6, 1985.

Reference Polyakova NB, Orlova TA (1990) Mercury Sergeevich Ghila rov. Bibliography of the USSR Scientists. Ser. Biological, Zoology, 1. Moscow, “Nauka” (in Russian).

Ghost Moths (Lepidoptera: Hepialidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Ghost moths (sometimes also called swifts), family Hepialidae, comprise about 496 species and occur in all faunal regions, although most species are in the ancient refugia regions of Australia, South Africa and Chile. The family is the main component of the superfamily Hepialoidea, in the infraorder Exoporia. Adults small to very large (20–250 mm wingspan), with head roughened; haustellum absent or vestigial and no mandibles are evident; labial palpi small and 2- or 3-segmented; maxillary palpi are minute and 1 to 5-segmented; antennae are very short. Maculation is usually dull with light (Fig. 18) spotting, but can include some green or gold irides cent markings or other light spots or bands. The

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Ghost Moths (Lepidoptera: Hepialidae), Figure 18 Example of ghost moths (Hepialidae), Zelotypia stacyi Scott from Australia.

hindwings tend to be large and overall the adults have large bodies. Adults are typically crepuscular or nocturnal, but a few are diurnally active. Larvae feed as borers on roots, trunks or under bark of trees, various bushes, or grasses, or even leaf litter. A few species are considered pests in Europe, Asia and Australia. This family has the record for egg deposi tion by a single female, of about 50,000 eggs, which are scattered over potential Host plants during flight. A few are economic. The largest species are the Australian Zelotypia stacyi Scott and the Amazonian Trichophassus giganteus (Herrich– Schäffer).

References Buser H, Huber W, Joos R (2000) Hepialidae – Wurzelbohrer. In: Schmetterlinge und ihre Lebensräume: Arten – Gefährdung – Schutz. Schweiz und angrenzenden Gebi ete, 3:61–96, pl. 1–2. Pro Natura-Schweizerische Bund fuer Naturschutz, Basel Dugdale JS (1994) Hepialidae. In: Fauna of New Zealand 30:1–161 Nielsen ES, Robinson GS (1983) Ghost moths of southern South America (Lepidoptera: Hepialidae). Ento monographia 4:1–192 Nielsen ES, Robinson GS, Wagner DL (2000) Ghost-moths of the world: a global inventory and bibliography of the Exoporia (Mnesarchaeoidea and Hepialoidea) (Lepi doptera). J Nat Hist 34:823–878 Tindale NB (1932–1958) Revision of the ghost moths (Lepi doptera Homoneura, Family Hepialidae). Records of the South Australian Museum (Adelaide), 4:497–536 (1932); 5:13–43 (1933); 5:275–332 (1935); 7:15–46, pl. 5–7 (1941); 7:151–168, pl. 9–11 (1942); 11:307–344, pl. 26–32 (1955); 13:157–197, pl. 16–23 (1958)

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Giant Axons

Giant Axons Very large neurons running through the abdomi nal ganglia of insects, and connecting by electrical rather than chemical synapses. Giant axons pro mote the rapid transmission of impulses.

Giant Coccids Some members of the family Margarodidae, super family Coccoidae (order Hemiptera).  Bugs

Giant Butterfly Moths (Lepidoptera: Castniidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Giant butterfly moths, family Castniidae, total 170 known species, mostly Neotropical but with some species also in the Indo-Australian region; likely world total may exceed 180 species. Three subfam lies are known, with the more unusual groups being from Australia and Southeast Asia: Syn emoninae, Neocastniinae, and Castniinae. The family is its own monobasic superfamily, Cast nioidea, in the section Cossina, subsection Cos sina, of the division Ditrysia. Adults medium to large size (24–190 mm wingspan), with head smooth scaled and eyes large; haustellum naked (rarely vestigial); labial palpi often with distal seg ment erect; maxillary palpi 2 to 4-segmented; antennae clubbed. Body robust. Wings quadratic and broad (Fig. 19); hindwings rounded. Macula tion variable but often dark browns with lighter bands or other markings; often colorful with vari ously colored patches and markings, especially on the hindwings. Adults diurnal or crepuscular. Lar vae are borers of monocot plants, including grasses (Gramineae), Cyperaceae, Bromeliaceae, Maran taceae, Musaceae, and Palmae, among others.

Giant Butterfly Moths (Lepidoptera: Castniidae), Figure 19 Example of giant butterfly moths (Castniidae), Castnia licus Fabricius from Peru.

A few are economic on banana plants, various palms, and sugarcane. One palm pest from Argentina has become established in southern Spain in recent years.

References Dalla Torre KW von (1913) Castniidae: subfamily Castniinae, Neocastniinae, Pemphigostolinae. In: Lepidopterorum catalogus, 15:1–28. W. Junk, Berlin Houlbert C (1918) Révision monographique de la sous- famille des Castniinae. In: études de Lépidoptèrologie comparée, 15:5–730, pl. 587–612. C. Oberthür, Rennes Miller JY (1972–1980) Studies in the Castniidae. Bull Allyn Mus 6:1–13 (1972); 60:1–15 (1980) Seitz A (ed) (1911–1926) Familie: Castniidae. In Die GrossSchmetterlinge der Erde. Teil 10. Die indo-australischen Spinner und Schwärmer, 6:5–19, pl. 1–8 (1913); 10:1–4, pl. 1, 9 (1911); 14:15–18, pl. 1 (1926). A. Kernen, Stutt gart: [also English and French editions] Westwood JO (1877) A monograph of the lepidopterous genus Castnia and some allied genera. Trans Linn Soc Lon 2-Zool 1:155–207, pl. 28–33

Giant Hooktip Moths (Lepidoptera: Cyclidiidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Giant hooktip moths, family Cyclidiidae, are a small family of 14 described species, all Oriental plus one species in the southern Palearctic. The family is in

Giant Lappet Moths (Lepidoptera: Eupterotidae)

the superfamily Drepanoidea, in the section Cos sina, subsection Bombycina, of the division Ditry sia. Adults medium to large size (56–85 mm wingspan), with head scaling normal; maxillary palpi small, 3-segmented; antennae serrate or fili form; body slender. Wings broad and triangular, with somewhat acute forewing apex; hindwings rounded (Fig. 20). Maculation mostly pale with gray striae or other markings; dark spot on hindwings in some species, otherwise similar to forewings. Adults are nocturnal. Larvae are leaf feeders. Host plants recorded so far only in Alangiaceae.

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Giant Lappet Moths (Lepidoptera: Eupterotidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA

Members of the family Polystoechotidae (order Neuroptera).  Lacewings, Antlions, and Mantidflies

Giant lappet moths, family Eupterotidae, total 325 species worldwide (except the Nearctic), but most are Oriental (238 sp.); only four species are recorded in the Neotropics. Three subfamilies are recognized: Janinae (in Africa), Eupterotinae, and Panacelinae (in Australia). Some specialists now include Hibrildinae (plus Tissanginae) in Eupterotidae. The family is in the superfamily Bombycoidea (series Bombyciformes), in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults small to large (23–140 mm wingspan), with head scaling roughened; haustellum (Fig. 21) absent (rarely vestigial); maxillary palpi absent; antennae bipecti nate (sometimes tripectinate or serrate); body robust. Wings mostly broad and rounded. Macula tion varies but mostly shades of brown or gray with few markings. Adults are nocturnal. Larvae are leaf feeders, usually with many secondary setae. Host plants among numerous different plants, including Acanthaceae, Boraginaceae, Gramineae, Legumi nosae, Myrtaceae, Pinaceae, and Rubiaceae, among others. Few species are economic (e.g., rice or forest pests).

Giant Hooktip Moths (Lepidoptera: Cyclidiidae), Figure 20 Example of giant hooktip moths (Cyclidiidae), Cyclidia substigmaria (Hübner) from Taiwan.

Giant Lappet Moths (Lepidoptera: E upterotidae), Figure 21 Example of giant lappet moths (Eupterotidae), Palirisa cervina (Moore) from Taiwan.

References Holloway JD (1998) Subfamily Cyclidiinae. In: The moths of Borneo. Malayan Nature Society, Kuala Lumpur, (Malayan Nature Journal 52), 8:70–72, pl. 6 Inoue H (1962) Lepidoptera: Cyclidiidae, Drepanidae. In: Insecta Japonica. Hokuryukan, Tokyo (2)1:1–54, pl. 3 Warren W (1922) Subfamilie: Cyclidiinae. In: Seitz A (ed) Die Gross-Schmetter linge der Erde. 10. Die indo- australischen Spinner und Schwärmerpl 48. Kernen, Stuttgart, Germany, pp 444–446

Giant Lacewings

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Giant Leaf Katydids

References Aurivillius POC (1901) On the Ethiopian genera of the family Striphnopterygidae. Kongliga Svenska VetenskapsAkademiens Handlingar (4) 27 (7):1–33, 5 pl Griveaud P (1961) Insectes. Lépidoptères Eupterotidae et Attacidae. In: Faune de Madagascar, 14:1–64, 12 pl. Tananarive-Tsimbazaza: Tananarive Inst. Sci Holloway JD (1987) Family Eupterotidae. In: The moths of Borneo. Malayan Nature Society, Kaula Lumpur, (Malayan Nature Journal, 41), 3:61–73, pl. 7–8 Seitz A (ed) (1911–1928) Familie: Eupterotidae. In Die GrossSchmetterlinge der Erde 2:185–188, pl. 29–30 (1911); 6: 629, pl. 86 (1928); 10: 417–432, pl. 31, 37, 56–57 (1922); 14: 293–311, pl. 42–47 (1927). Kernen, Stuttgart, Germany

Giant Leaf Katydids A subfamily of katydids (Phyllophorinae) in the order Orthoptera: Tettigoniidae.  Grasshoppers, Katydids and Crickets  Katydids

Giant Stoneflies Members of the stonefly family Pteronarcidae (order Plecoptera).  Stoneflies

Giant Water Bugs (Hemiptera: Prosorrhyncha Belostomatidae) marta goula Universitat de Barcelona, Barcelona, Spain These aquatic insects are also known as giant fish killers, electric light bugs, and toe biters. They are predators of insects and other small organisms up to the size of tadpoles, small water birds or even fish, and occasionally are known to inflict injury to humans. In humans, a belostomatid bite produces a painful burning sensation that lasts several hours.

Morphology Giant Mealybugs Members of the family Putoidae, superfamily Coc coidae (order Hemiptera).  Bugs  Scale Insects and Mealybugs

Giant Northern Australia Termite A termite species, and family of termites called Mastotermitidae.  Termites

Giant Silkworm Moths Some members of the family Saturniidae (order Lepidoptera).  Emperor Moths  Butterflies and Moths

Belostomatidae are large-sized (up to about 110 mm), ovoid to elongate aquatic bugs. They are brownish, dorsoventrally flattened while ventrally convex. The head extends triangularly in front of the large eyes. They have a stout syringe-like ros trum or beak, which is the result of the pair of man dibles and the two pairs of maxillae evolved in long piercing stylets. The beak is three segmented. A pair of short, 4-segmented antennae are concealed in grooves beneath the head. Segments 2 and 3 have lateral projections. Belostomatidae possess a pair of large compound eyes, but lack ocelli. The head does not overlap the pronotum. The front wings are in the form of hemelytra, with a sclerotized basal region (corium) and a membranous apical region (membrane) with reticulate venation. The hind wings are completely membranous. The front legs usually are raptorial. They are at least dexterous, as in the genus Limnogeton, but in most cases they act as a vice-like grip. Very dense short setae on the under surface of most front leg

Giant Water Bugs (Hemiptera: Prosorrhyncha Belostomatidae)

segments help the insect grasp. Front femora are expanded to contain a powerful musculature that allows the tibia and tarsi to seize the prey. Except in the case of Limnogeton, the middle and hind legs are paddle-shaped, and well suited for swim ming. They are flattened and broadened, and doubled-fringed with long, fine setae that increase the effective swimming surface. The tarsi may be 2-, 3- or more rarely 1-segmented. There may be a single claw, slightly or greatly reduced, or paired claws, like in the front legs of Horvathiniinae. A metathoracic scent gland system (MSGS) has been reported only in Lethocerinae. In nymphs, the dorsal abdominal scent glands are not functional. In the apex of the abdomen (tergum 8), the Belostomatidae have a pair of retractable, straplike appendages that allow snorkeling while the insect is under water. These special respiratory structures are the most distinctive feature of the group. Belostomatidae also are provided with static sense organs, associated with spiracles 2–7.

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Taxonomy

Giant Water Bugs (Hemiptera: Prosorrhyncha Belostomatidae), Figure 22 Adult giant waterbug, Lethocerus sp. (photo courtesy of Dave Almquist, University of Florida).

Belostomatidae, as Belostomida, were recognized as a group by Leach in 1815. This family presently is arranged in three subfamilies: Lethocerinae, Horvathiniinae and Belostomatinae. Currently, 11 genera and approximately 150 species are recog nized. The antennal and spiracular characteristics are most often used to identify subfamilies. The Lethocerinae are 37–150 mm in length. Formerly it contained a single genus, Lethocerus, that was recently divided into three genera: Benacus, with a single species B. griseus; Kirkaldyia also with a single species K. deyrolli; and Lethocerus with the remaining 22 species. Lethocerus maximus (Fig. 22) is the largest true bug and is among the largest insects. Males of Lethocerinae perform emergent-brooding, attending clutches glued to vegetation at the shore. The Belostomatinae are between 9 and 70 mm in length. They are found worldwide, and contain most of the genera of Belostomatidae, and about a

hundred species. Belostoma, with approximately 60 species, is the most species-rich genus. Other quite species-rich genera are Diplonychus (approx imately 6 species), Abedus (10 species) and Apassus (17 species), while Sphaerodema, Hydrocyrius and Limnogeton, among others, comprise very few species each. Limnogeton, with its unspecialized legs and its diet restricted to water-snails, is the most primitive genus. Poissonia and Weberiella, two monospecific genera, are poorly known. Belostomatinae males perform back-brooding. Horvathiniinae, which measure 25–30 mm in length, are the least known belostomatid subfam ily. In the unique genus Horvathinia, nine species were described, but recent revision (2005) left only two species: H. pelocoroides and H. lenti. Generally, only specimens attracted to light are known. How ever, recently two adults were collected for the first time in their natural habitat, but nymphs have never been observed. The real position of

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Horvathiniinae is uncertain. Egg color is as in Lethocerinae, and the eggs are buried as in Nepi dae (water scorpions), but those eggs lack the respiratory horn-like structures typically found in water scorpions.

Biology Giant water bugs live in many freshwater environ ments. In Japan, rice fields have been reported to function as alternative wetlands for many aquatic insects, including belostomatids. Overwintering occurs in the mud at the bottom of the rice field. Giant water bugs in the subfamily Lethocerinae inhabit ponds, lakes and slow waters of streams and rivers. Belostomatinae prefer lentic waters, from small puddles to margins of large lakes. Horvathinia pelocoroides (Horvathiniinae) has been captured in the province of Corrientes, Argentina, in a perma nent shallow pond of about 1 ha surface and 2.1 m depth; during the rainy season, the water level is high enough to drain into a stream. The pond was densely filled with floating hydrophytes dominated by water hyacinth, Eicchornia crassipes, and water lettuce, Pistia stratiotes. Other belostomatids shared the habitat with H. pelocorides. Other fauna, including tadpoles and snails were reported to live in the area. Belos tomatids are quite easily reared, so their biology has been extensively studied in laboratory trials. Belostomatids are good flyers, and this ability is needed to escape (migrate) from drying ponds or streams, or due to shortage of prey. Migration may be related to the lunar cycle, as is the case in Diplonychus rusticus or Lethocerus sp. (in the latter case, during the full moon). Heavy rains also induce flight activity (called “rainfall response behavior”), primarily as an adaptation to migrate to breeding sites. However, the rainfall response behavior also ameliorates the risk of extinction due to flash floods. For Abedus aberti, there is a report that a torrential rainfall threshold of 8.0 min caused one-third of the adults to abandon a rapidly flowing stream; immatures respond more slowly to the flooding cue, usually requiring about

30 min of torrential rainfall. In this species, flash flood mortality normally causes less than 15% mortality because they can perceive danger through rainfall rate, while for most freshwater invertebrates exposed to such flooding the mor tality may be more than 90%. Belostomatids are good swimmers, but in the case of Limnogeton and in Horvathiniinae, they are less efficient than the rest of the group. Positive phototropism (attrac tion to light, especially to mercury vapor lamps) of giant water bugs is the basis for their common name “electric light bugs.” Such lights interfere with their normal nighttime navigation as they normally navigate using star light. Giant water bugs are carnivorous, and either ambush or actively pursue and capture the prey (foraging). They attack moving prey, but not still or immobile objects. Once grasped by the front legs with lightning speed, the prey is pierced with the robust rostrum. The bug then injects venom ous saliva containing proteases, hyaluronidases, phospholipases, hemolythic enzymes and heartstopping neurotoxins. This mixture, similar to that in snake venom, easily subdues (paralyzes and kills) the prey. As a result, the prey’s tissues are liquefied by external digestion, and the bug sucks out that liquid using a cybarial pump. Once grasped, the prey is never released, however it struggles to escape from the predator. The size of prey tends to match that of the predatory bug. The smallest belostomatids prey on water snails, which seems to be an ancient trait of the group. Increasing size allows them to prey on crusta ceans, dragonfly nymphs, vertebrate larvae, small fish, and even frogs, salamanders, water-birds, larger fish, and snakes. Except for Limnogeton, a specialist in water-snails, the rest of the Belos tomatidae have a diversified diet, always includ ing vertebrates. It is hypothesized that the ancestral snail consumption, which requires quite precise movements and tight grasping, is a pre adaptive trait (a trait evolved for one function but later co-opted for another) that allows the insect to handle more demanding prey such as vertebrates. Some species catch more prey than


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they can eat, a hoarding behavior. Cannibalism is sometimes reported. Although living in water, belostomatids need to breath air. Breathing is mediated by the special abdominal airstraps, which are protruded to the surface while lying motionless in the water. They transmit the air to the subhemelytral airstore by a channel, formed by the setae, which converge mesioventrally. Air finally passes to the tracheal system mainly through the dorsal first abdominal spiracle. In nymphs, respiration occurs from the airstore on the ventral surface of the abdomen, and cuticular breathing also plays a key role. Defensive behavior is well developed in this group. The first reaction to a threat is the motion of the front legs as if to grasp the aggressor. Also, a foul-smelling liquid may be ejected from the anus for more than a meter. In Lethocerinae, the metathoracic scent gland does not play any defen sive role, but seems to be essential in marking the trail to the clutch laid on the shore vegetation. The odor of the metathoracic gland does not prevent Lethocerus specimens from being eaten by humans in several parts of Asia. Reproductive behavior of giant water bugs is unique among insects, as paternal care is the rule in most of them. Lethocerinae are emergent-brooders, while Belostomatinae are back-brooders. Only Horvathiniinae seem not to perform brood-caring, and eggs are half-buried in small groups in the wet sand of the shore. When paternal care occurs, a reversal of the typ ical sexual competition occurs, as the females fight for mates. Most probably, the big size of Belostomatidae, a primary trait, promoted ancil lary selection of paternal care. Hatching occurs one or two weeks after egg laying, and nymphal development occurs in one or two months, requiring five molts.

of Kirkaldyia are preyed upon by the water scorpi ons Laccotrephes, Notonecta, and Ranatra, the giant water bug Appasus, and dragonflies of the family Aeschnidae. Belostomatids such as Belostoma (Fig. 23) may serve as hosts of ectosymbiont platyhelm inths such as Temnocephala. Also, Bodo kineto plastid flagellates were isolated from the hindgut of Lethocerus indicus. Some belostomatid species have been reported as intermediate hosts for meta cercariae of digenetic trematodes; this is the case for several Belostoma spp. that are parasitized by the trematode Stomylotrema in Brazil and Argentina. Trematode metacercariae lodge in the abdominal cavity of both male and female bugs.

Natural Enemies

Giant Water Bugs (Hemiptera: Prosorrhyncha Belostomatidae), Figure 23 Male giant waterbug, Belastoma sp., bearing eggs and young (photo courtesy of Doug Tallamy, University of Delaware).

Predation of eggs of Belostoma by water scorpions, Notonecta, has been reported. Also, young nymphs

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Distribution Although distributed worldwide, Belostomatidae are most diverse in the tropics. Lethocerinae have a pantropical distribution, with a few temperate representatives. Benachus lives in North America and the Caribbean regions, Kirkaldyia is distrib uted in East and Southeast Asia, and Lethocerus is a cosmopolitan genus. Belostomatinae genera dif fer in their distribution. For example, Belostoma is known from the Americas, while Abedus is restricted to the southwestern USA and to Central America. Diplonychus lives in Asia, India, China, and probably Malaysia. Appasus lives in Africa and Asia, Hydrocyrius is present in Saudi Arabia, Africa and Madagascar, and Limnogeton is found exclusively in Africa. Horvathiniinae have been recorded in Central and South America (north eastern Argentina, Uruguay, Paraguay, Bolivia and southeastern Brazil).

Ecological and Economic Significance Belostomatids play a key role in freshwater ecosys tems, where they perform as intermediate-stage predators in the food chain. Their control over invertebrate populations is greater in the absence of fish. Belostoma and Lethocerus species, among others, may be efficient controllers of freshwater snail populations. As a consequence, they may play a useful role in preventing human and veterinary schistosomiasis, as snails are an intermediate host. Lethocerus may be of concern in fisheries, as it may prey on specimens up to 20 cm long. Mosquito and/or chironomid larvae and/or pupae are actively preyed upon, and controlled to some extent, by Belostoma, Diplonychus, Spherodema and Lethocerus species. However, pesticide treatments targeted at mosquito larvae, or other biocide treat ments for agricultural purposes, may poison water and prove harmful to giant water bugs. Kirkaldyia deyrolli is reported to be a threatened-vulnerable

species in the Read Data Book of Japan, most prob ably due to water pollution. Interestingly, Bacillus sp. spread to control larval mosquitoes may remain in belotomatid feces and dead bodies, acting as a mosquito-killing microbe repository. Relative to humans, the main role of these insects is as a food source in several Asian coun tries where adults of Lethocerus are considered a delicacy, and are eaten both fresh and cooked. In Southeast Asia, some species are highly valued for extraction of a very expensive essence from the essence-producing glands. The “essence” is a sexpheromone, and is produced by males to attract females. It is used by humans in cooking (dipping sauce). Belostomatids may also be a nuisance because they are attracted to lights, especially when attracted to lighted pools where they might bite swimmers. The role of some giant water bugs as second intermediate hosts of digenetic trema todes may result in medical importance of giant water bugs in some regions. Thus, like many insects, belostomatids display several behaviors that could result in them being classified as either useful or harmful insects.

Evolution In past times, giant water bugs likely took advan tage of shallow waters teeming with small verte brates or invertebrate larvae, an empty niche unavailable to large predatory fish, which need deeper water. The individuals best adapted to feed on larger prey succeeded over the predators taking smaller prey, in a feed-back cycle whose only limit was egg size and embryo nutrition. Thus, it appears that large body size, a primary trait under natural selection because it allows feeding on bigger prey, has shifted the evolution of Belostomatidae to their current large body size.  Parental Care in Heteroptera  Bugs (Hemiptera)

Glabrous

References Ichikawa N (1988) Male brooding behaviour of the giant water bug Lethocerus deyrolli Vuillefroy (Hemiptera: Belostomatidae). J Ethol 6:121–127 Lauck DR, Menke A (1961) The higher classification of Belostomatidae (Hemiptera). Ann Entomol Soc Am 54:644–657 McGavin GC (1993) Bugs of the world. Blandford, London, UK, 192 pp Miller NCE (1971) The biology of the Heteroptera, 2nd edn. E.W. Classey, Hampton, UK, 106 pp Perez Goodwyn PJ (2006) Taxonomic revision of the subfam ily Lethocerinae (Heteroptera: Belostomatidae). Sutt garter Beitrage fuer Naturkiunde A695:1–71 Schaefer CW, Panizzi AR (Eds) (2000) Heteroptera of eco nomic importance. CRC Press, Boca Raton, FL, 828 pp Schnack JA, Estévez AL (2005) On the taxonomic status of the genus Horvathinia Montandon (Hemiptera: Belso tomatidae). Zootaxa 1016:21–27 Schnack JA, Estévez AL, Armúa de Reyes C (2006) Laguna Don Blanco, Argentina: first record of Horvathinia (Hemiptera: Belostomatidae) as a wetland dweller. Ento mol News 117:197–202 Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Heteroptera). Classification and natural history. Cornell University Press, Ithaca, NY Smith RL (2004) Evolution of paternal care in the giant water bugs (Heteroptera: Belostomatidae). In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, NY, pp 116–149

Gill A respiratory structure found in immature aquatic insects, through which they obtain dissolved oxy gen. Gills take various forms, and are found at various locations.

Girault, Alexandre Arsène Alexandre Girault was born in the state of Maryland, USA, on January 9, 1884. He earned a B.S. degree from Virginia Polytechnic Institute in 1903, and then in 1904 became employed by the U.S. Depart ment of Agriculture. During that employment he worked as an applied entomologist on the plum curculio, Colorado potato beetle, and lesser peach

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borer. In 1908 he moved to Illinois as assistant to the State entomologist and then as assistant in entomology at the University of Illinois. There he worked on insects of stored products, the Colorado potato beetle, and Cimex bed bugs. In 1911, he moved to Australia, as entomologist to the Bureau of Sugar Experiment Stations in Queensland. There, he worked on taxonomy of “parasitic” Hymenoptera. He also studied thrips. Three years later, he returned to the USA to work again for the U.S. Department of Agriculture, but this time in Washington, DC, on the classification of Chalci doidea. He moved back to Australia in 1917, this time as assistant entomologist to the Queensland Department of Agriculture and Stock. His major work was a monograph (1912–1915) “Australian Hymenoptera Chalcidoidea” of over 900 pages. Many others of his over 300 papers were small notes, some of them badly printed on a small press of his own, and distributed to few institutions and hymenopterists, thus not readily available. He died in Brisbane, Australia, on May 2, 1941.

References Mallis A (1971) Alexandre Arsene Girault, In: American ento mologists. Rutgers University Press, New Brunswick, New Jersey, pp 376–377 Muesebeck CFW (1942) Alexander Arsene Girault. Ann Entomol Soc Am 35:122–123

Gizzard This term is rarely used in entomology, but applies to a pouch-like structure at the juncture of the crop and stomach. This organ is used for filtering and grinding of food and usually is called the proventriculus.  Alimentary Canal and Digestion

Glabrous  Smooth and without hairs

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Gladiators (Mantophasmatodea)

Gladiators (Mantophasmatodea) In 2002, German researchers announced the dis covery of a new insect order, Mantophasmatodea. The order name is based on the names of their close relatives, the Mantodea (praying mantids) and the Phasmatodea (walking sticks). This was a significant find because a new order had not been discovered since 1915. Indeed, it remains to be seen whether the entomological community accepts the report that this is a new order. It has been a contro versial topic since the initial discovery. Some have argued that Mantophasmatodea is a sister group of Grylloblattodea, and that they should be treated as suborders in the order Notoptera. Further, two of the three families were relegated to subfamily status in this system, and the insects were named “rock crawlers,” whereas the members of the sister taxon, were called “ice crawlers.”

Characteristics Mantophasmatodea was first found in the Brandenberg Mountains of Namibia in southwest ern Africa (since then they have been found widely in the western regions of South Africa, and in Tanzania). They were found at the base of grass clumps growing in rock crevices. In most respects these insects resemble stick insects (Phasmatodea), but have characteristics of praying mantids (Manto dea), and some unique attributes. Superficially, they resemble immature mantids, which are wingless like gladiators, but the gladiators lack the well-developed raptorial front legs of mantids. They differ from stick insects in that the head is hypognathous (pointing downward), the first thoracic segment is the largest, the first and second pairs of legs are raptorial, and the insects are carnivorous. Unlike mantids, the sec ond pair of legs is used in feeding. The thorax appears to be armored, hence the name “gladiators.” They are also known as “heelwalkers” because they tend to elevate their tarsi when walking. Gladiator insects are hemimetabolous, like other orthopteroids. The antennae are long and

filiform, the head hypognathous. The thoracic seg ments decrease in size from anterior to posterior. The femora of the first and second pairs of legs are broadened and armed with spines. The tarsi have five segments. There is slight sexual dimorphism. In males, the subgenital plate has a median projec tion. The cerci are one-segmented, prominent and clasping. In females, the ovipositor projects mark edly beyond the short subgenital lobe. The female abdomen is widest in the middle, whereas in the male it is widest apically. Males are smaller than females. All insects are apterous. They generally are under one cm in length. They are brown or green, and may be uniform or mottled in color, often with a dorsal stripe or stripes. Polymorphism is common.

Biology The eggs of gladiators hatch after the seasonal rains commence, with the nymphs developing during the wet months and the adults maturing at the end of the rainy season. The adults mate, lay eggs and die within two weeks. Mating can be pro tracted, lasting for 1–3 days. The eggs persist through the arid period in an egg pod in the soil. The pod is composed of sand granules glued together with an exudate. Each pod contains about 12 eggs, and females (Fig. 24) produce several pods. Gladiators feed on small insects such as flies and bark lice. They may be nocturnal or diurnal. They frequent low vegetation such as tufts of grass. Apparently they communicate vibrationally, as they have been observed taping their abdomen on the substrate.

Taxonomy The order presently consists of three or more fami lies, several genera (some have yet to be placed in families) and perhaps 12 species. One genus, Raptophasma, is known from Baltic amber, dating back

Glassy-Winged Sharpshooter, Homalodisca vitripennis (Hemiptera: Cicadellidae)

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Klass KD, Zomporo O, Kristensen NP, Adis J (2002) Manto phasmatodea: a new insect order with extant members in the Afrotropics. Science 296:1456–1459 Klass KD, Picker MD, Damgaard J, van Noort S, Tojo K (2003) The taxonomy, genitalic morphology, and phylogenetic relationships of southern African Mantophasmatodea (Insecta). Entomologische Abhandlungen 61:3–67

Glaphyridae A family of beetles (order Coleoptera). They com monly are known as glaphyrid scarab beetles.  Beetles

Glaresid Beetles Members of the family Glaresidae (order Coleoptera).  Beetles

Glaresidae A family of beetles (order Coleoptera). They com monly are known as glaresid beetles.  Beetles Gladiators (Mantophasmatodea), Figure 24 Female Austrophasma sp. (Mantophasmatodea: Austrophasmatidae) (adapted from Klass et al. 2003).

about 45 million years. These extinct insects differ from the modern forms in lacking the spines on the femora and tibiae of the first and second sets of legs. Order Mantophasmatodea Family Tanzaniophasmatidae Family Mantophasmatidae Family Austrophasmatidae

References Arillo A, Engel MS (2006) Rock crawlers in Baltic amber (Notoptera: Mantophasmatodea). Am Mus Novit 3539:1–10

Glassy-Winged Sharpshooter, Homalodisca vitripennis (Hemiptera: Cicadellidae) tobin d. northfield, russell f. mizell iii University of Florida, Quincy, FL, USA The glassy-winged sharpshooter, Homalodisca vitripennis (Germar) feeds on xylem fluid and is damaging to crops and ornamentals through the transmission of Xylella fastidiosa, a bacterium that causes phony peach disease, Pierce’s disease in grapes, and leaf scorch in almond, plum, elm and oak. In Brazil, a strain of X. fastidiosa causes citrus variegated chlorosis, but the current geographic range of the strain does not overlap that of

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H. vitripennis. Homalodisca vitripennis is native to the southeastern United States, and in the late 1980s or early 1990s spread from Texas to south ern California, where Pierce’s disease caused $30 million in damage to California vineyards from 1994 to 2000. In California, H. vitripennis is a more important vector than the native species because it spreads the disease further into vineyards from surrounding vegetation. Furthermore, in the southeastern United States only muscadine grapes are grown successfully, because only the musca dine varieties are resistant to Pierce’s disease. The range of H. vitripennis is restricted to areas with mild winters. However, H. vitripennis has been accidentally introduced to Hawaii, Tahiti, and Easter Island, Chile. Also, climatological models predict that H. vitripennis and X. fastidiosa could become established in Central and South America, southern Europe and Asia, Africa, Australia, and northern California. The “sharpshooter” name refers to leafhop pers in the tribes Proconiini and Cicadellini (Hemiptera: Cicadellidae), and the name has two possible derivations. One reason for the name sharpshooter is the tiny “bullet holes” in branches and stems that are caused by the piercing-sucking behavior. In addition, adults and nymphs quickly move to the opposite side of a branch when star tled, and this behavior is similar to the way a mili tary sniper moves to the far side of a tree to avoid detection. The Proconiini tribe comprises 350 spe cies in 56 genera, including H. vitripennis, and the

range of the tribe includes the Americas and Tahiti. Homalodisca vitripennis adults (Fig. 25) are generally light brown with black and red wings, and are 11–13 mm in length. Adults usually align head to tail with their heads facing down when feeding, and feed on a wide range of host plants (>100 species), including hardwoods, softwoods, fruit trees, herbaceous crops, and grasses. Some preferred hosts include plum, holly, crape myrtle, citrus, grape and sunflower. Feeding on xylem may limit the number of competitive interactions H. vitripennis encounters, as few insects feed on xylem fluid and there is little or no degradation of xylem quality with insect feeding. In addition, xylem fluid has little or no chemical defensive compounds, which may enable H. vitripennis to feed on such a broad host range. However, there are some disadvantages associated with xylem feeding, and H. vitripennis has devel oped some important adaptations to feeding on xylem fluid. To overcome the strong negative pres sure associated with xylem tissue, H. vitripennis uses a large cibarial pump in the anterior portion of the head to extract the xylem fluid. Further more, xylem fluid is approximately 99% water, so a portion of the gut and the Malpighian tubules form a filter chamber that is designed to extract most of the water from the ingested xylem fluid. This process allows nutrients to be absorbed from a more concentrated solution. In addition, H. vitripennis feeds for long periods in order to

Glassy-Winged Sharpshooter, Homalodisca vitripennis (Hemiptera: Cicadellidae), Figure 25 Adult of glassy-winged sharpshooter, Homalodisca vitripennis (Germar).


gain adequate nutrients. Hourly consumption of xylem is often 10–100 times greater than the dry body weight of the individual, so they must pro duce large amounts of waste. Homalodisca vitripennis has become a pest to the tourist industry in Tahiti due to the dense populations of adults and nymphs and the “rain” they excrete that falls on tourists. Homalodisca vitripennis excreta consist of a dilute mixture of water and ammonia, which is much less physiologically expensive than urea or uric acid. Most animals do not use ammonia as a waste product, due to the chemical’s toxic nature, but H. vitripennis waste products are too dilute to cause ammonia poisoning. Glassy-winged sharpshooters have adapted high assimilation efficiency (about 99%) of amino acids, organic acids and sugars. This assimilation may be due in part to two species of endosymbi otic bacteria that live in the cytosol of H. vitripennis cells and aid in attaining the adequate nutritional requirements. Each species of bacteria complements the nutritional advantages of the other and is passed by females to offspring from generation to generation. One species, Baumania cicadellinicola, is related to endosymbionts of aphids, tsetse flies, and ants, but is a more primi tive species and synthesizes most vitamins and cofactors. The other species, Sulcia muelleri, pro duces many of the essential amino acids that are not abundant in xylem fluid. Adults often fly from plant to plant, sampling xylem fluid to find optimal hosts and adjust feed ing rates to correlate with xylem nutrition. Flight behavior usually consists of short flights from plant to plant and H. vitripennis generally flies 2–3 m high, depending on the height of the sur rounding vegetation. Dispersal rates vary with available host plants and seasonal conditions, but a single H. vitripennis can travel up to 100 m in a matter of minutes. Daily foraging usually occurs between 10 am and 2 pm, during peak xylem flow and this behavior allows adults to attain the best sample of a host in order to make a decision to stay and feed or move on. In addition, H. vitripennis may feed on different plants at different times

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of the day to correlate feeding with maximum xylem flow in the plants. Foraging adults and nymphs are attracted to the color yellow, which may resemble new growth occurring in host plants. Homalodisca vitripennis also uses plant volatiles to locate host plants, but olfactory cues appear to be secondary to visual stimuli. Adults do not appear to use phero mones as aggregation cues or to locate mates. When mating occurs, females line up head to tail on branches, while males fly from branch to branch looking for aggregations of females. Once the male selects a branch to land on, it walks down the branch in a spiral formation and looks for an accepting mate. If the female is not ready to mate, she will stick her legs and abdomen in the air and block off any potential suitors. Mating occurs in the morning or evening, and females deposit eggs at night. Eggs are inserted under the leaf epider mis on the underside of the leaf in groups of 3–28, although eggs are occasionally deposited in fruits or herbaceous stems. A single female can lay up to 1,000 eggs, and eggs hatch approximately 7 days after oviposition. Nymphs are gray and develop through five instars, usually lasting about two months. Nymphs have different nutritional prefer ences than adults. Adults prefer to feed on xylem fluid that is high in amides (glutamine and aspar agine), and nymphs prefer to feed on xylem fluid with a more balanced spectrum of amino acids. In addition, adults can feed on stems with thicker epidermis than nymphs, due to the adult’s thicker proboscis. Pubescent leaves and stems also deter nymphs from feeding, as first and second instars often feed on xylem in leaf veins, and have diffi culty reaching the plant through the trichomes. Often eggs are laid on hosts that are acceptable to adults but do not support the development of nymphs, so the nymphs must disperse to find new hosts. However, nymphs have developed excellent dispersal abilities, and third and fifth instars can jump up to 68 and 79 cm, respectively. In addition, nymphs can traverse up to 10 m across a grassy field in three days, and neonates survive an aver age of 84 h without a host plant.

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Nymphs and adults cover themselves in a light coating of lipid-protein molecules called bro chosomes, which are produced by special cells in the Malpighian tubules. Homalodisca vitripennis secrete brochosomes from the hindgut after each molt and spread them over the integument with their hind legs. In addition, adult females often have conspicuous, white spots of brochosomes on their wings. Females cover their egg masses with these brochosomes by using their hind legs to brush the powdery substance from the forewing patch to the egg mass. All Cicadellidae species cover their integument with brochosomes, but only Proconiini species cover egg masses as well. The structure of brochosomes varies between spe cies, and brochosomes that cover egg masses are structurally different than those that cover the integument. Brochosomes have repellant proper ties and probably aid adults, nymphs and eggs in the repellency of water and sticky substances, as well as protect against infections. In addition, bro chosomes on egg masses may inhibit parasitism by egg parasitoids. Brochosomes may also protect against desiccation and UV light in some instances, as well as aid in thermoregulation. In northern Florida and southern Georgia there are one or two generations per year. The first generation emerges from eggs laid by overwintered adults in forest edges, and migrates as adults to summer hosts and cropping systems in late May. The second generation migrates back to the forest in August and September, where they spend the winter in reproductive diapause and feed only dur ing warm spells. There are two or three generations per year in California, with the highest oviposition periods in early spring and mid to late summer. During winter months in California adults actively feed on citrus, but do not reproduce. The close proximity of vineyards to these citrus orchards often increases the ease of movement between win ter and spring hosts, and can increase the spread of H. vitripennis and Pierce’s disease into vineyards. Late in the summer in their native range most H. vitripennis eggs are parasitized by mymarid (Hymenoptera: Mymaridae) parasitoids. These

parasitoids include Anagrus stethynioides and sev eral Gonatocerus species, most of which have been evaluated and/or used as biological control agents in California as part of a Pierce’s disease manage ment program. The most common parasitoids in the native range are G. ashmeadi, G. triguttatus, G. morrilli, and G. fasciatus. Eggs are susceptible to the different parasitoid species at different stages, but generally eggs older than 6 days are not suscep tible. Once parasitized, eggs turn black as the para sitoid develops, and eventually the parasitoid chews a distinctive, circular exit hole and emerges. Para sitism often reaches close to 100% in the southeast ern United States, but in California parasitism rates rarely exceed 19%. In addition to high mortality from parasitism, H. vitripennis populations suffer predation from several generalist predators, includ ing spiders, anoles, dragonflies, and birds. An entomopathogenic fungus, Hirsutella homalodiscae, often infects nymphs and adults, and is most common in mid to late summer. Infected H. vitripennis can be recognized by the fuzzy, white fungus growing on the exoskeleton. The generalist fungus Beauveria bassiana also infects H. vitripennis, but infection rates vary by strain and are generally low. Strains from natural populations in the southeastern United States and Texas are more efficient than commercially avail able strains. In addition, there are several chemical controls available that have strong effects on H. vitripennis nymphs and adults, but low effects on associated egg parasitoids. The main focus in the control of H. vitripennis populations is on limiting the geographic spread of H. vitripennis. If H. vitripennis populations spread to the north from southern California, the damage to central California vineyards could be devastating. In addition, limiting the international spread is very important to the economic stability of vineyards in Europe and Australia and to the control of citrus variegated chlorosis in South America. The most important method to contain H. vitripennis is through the monitoring of horticul tural shipments. This is a daunting task, due to the wide range of food and oviposition hosts used by

Glory Moths (Lepidoptera: Endromidae)

H. vitripennis. However, if this monitoring is not conducted there could be worldwide consequences.  Bugs (Hemiptera)  Leafhoppers (Hemiptera: Cicadellidae)  Transmission of Xylella fastidiosa Bacteria by Xylem-Feeding Insects  Management of Insect-Vectored Pathogens of Plants  Transmission of Plant Diseases by Insects  Citrus Pests and Their Management  Small Fruit Pests and Their Management

References Purcell AH, Hopkins DL (1996) Fastidious xylem-limited bacterial plant pathogens. Annu Rev Phytopathol 34:131–151 Redak RA, Purcell AH, Lopes JRS, Blua MJ, Mizell RF, Ander sen PC (2004) The biology of xylem fluid-feeding insect vectors of Xylella fastidiosa and their relation to disease epidemiology. Annu Rev Entomol 49:243–270 Turner WF, Pollard HN (1959) Life histories and behavior of five insect vectors of phony peach disease. USDA Tech Bull 1188:1–27

Glial Cell A cell surrounding the axon, soma, and other por tions of a neuron. Glial cells provide structural and nutritive support, and protect the nerve cell from outside chemical and ionic influences.  Nervous System

Global Positioning System (GPS) Georeferences based on transmission received from a network of satellites.

Globular Springtails A family of springtails (Sminthuridae) in the order Collembola.  Springtails

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Glory Moths (Lepidoptera: Endromidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Glory moths, family Endromidae, are a monobasic family of four species, with Endromis (one sp.) from Europe, Dalailama (one sp.) from Tibet, and Mirina (two sp.) from Central Asia. There are two subfamilies: Endrominae and Mirininae. The fam ily is in the superfamily Bombycoidea (series Sat urniiformes), in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults medium size (29–74 mm wingspan), with head vertex rough-scaled; haustellum absent (or vesti gial); labial palpi short,dropping (2 to 3-segmented); maxillary palpi vestigial; antennae bipectinate; body robust with very long hair-like setae. Wings broadly rounded with somewhat acute apex; hind wings rounded. Maculation dark orange brown, with various white spots and darker striae, or lighter and spotted (Fig. 26). Adult males are diur nal but females are nocturnal. Larvae are leaf feeders. Host plants recorded in Betulaceae, Capri foliaceae, Salicaceae, Tiliaceae, and Ulmaceae.

References Freina J, de J, Witt TJ (1987) Familie Endromidae Boisduval 1828. In: Die Bombyces und Sphinges der Westpalaearktis, Forschung & Wissenschaft Verlag, Munich, 1:328–329, pl. 24 Jost B, Schmid J, Wymann H-P (2000) Endromidae – Früh lingsspinner. In: Schmetterlinge und ihre Lebensräume: Arten – Gefährdung – Schutz. Schweiz und angren zenden Gebiete, Pro Natura-Schweizerische Bund fuer Naturschutz, Basel, 3:362–366, pl. 19 Rougeot PC (1971) Endromidae. In: Les Bombycoides (Lepidoptera – Bombycoidea) de ʹ Europe et du Basin Méditerranéen. In: Faune de lʹ Europe et du Basin Médi terranéen, Masson, Paris, 5:131–140 Seitz A (1911) Familie: Endromidae. In: Seitz A (ed) Die Gross-Schmetterlinge der Erde. 2. Die palaearktischen Spinner und Schwärmer, pl. 35. A. Kernen, Stuttgart, pp 193–194

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Glossa (pl. glossae)

Zolotuhin VV, Witt TJ (2000) The Mirinidae of Vietnam (Lepidoptera). Entomofauna 11 (suppl.):13–24

Glossa (pl. glossae) The median lobes on the labium.  Mouthparts of Hexapods

Glossinidae A family of flies (order Diptera). They commonly are known as tsetse flies.  Flies

Glossosomatidae A family of caddisflies (order Trichoptera). They commonly are known as saddle-case makers.  Caddisflies

Glossy Said of a surface having the ability to reflect light. A measurable quality. The antonym is matte. Con trast with LUMINESCENT. Many authors fail to distinguish between these conditions, and errone ously write “shining” or “shiny.”

Glory Moths (Lepidoptera: Endromidae), Figure 26 Example of glory moths (Endromidae), Endromis versicolora (Linnaeus) from Germany.

Glover Scale, Lepidosaphes gloveri (Packard) (Hemiptera: Diaspidae) Lepidosaphes gloveri is an important pest of trees and shrubs.  Citrus Pests and their Management  Scale Insects and Mealybugs

Glover, Townend Townend Glover was born in Rio de Janeiro on February 20, 1813. His parents were English, and it to was Leeds, England, that Townend was sent on his mother’s death when he was only six weeks old. He became interested in natural history and enjoyed drawing. He was left an inheritance by his father, and this became available to him at the age of 21. He traveled to visit Munich, studied paint ing, and visited other European cities before returning to Leeds. His paintings, perhaps because he was shortsighted, were meticulous in detail. In 1836 he sailed for the USA to visit relatives, and traveled widely, especially in the South. In 1838 he moved to the state of New York, married in 1840, spent his time on natural history in the widest sense, and in 1846 bought his father-in-law’s coun try estate. In 1854 he joined the “Bureau of Agri culture” which had just been established in the U.S. Patent Office; his job was to collect information about insects. In 1856–1857 he was sent to British Guiana and Venezuela to collect new planting stock of sugarcane for Louisiana. Next, he worked on insect pests of citrus in Florida. He also stud ied plant diseases, soils, birds, mammals, reptiles, Indian mounds, and even human nature. In 1859 he resigned from the Patent Office and joined the faculty of the Maryland Agricultural College. In 1862 a new U.S. Department of Agriculture was established, independent of the Patent Office, and Glover was appointed United States Ento mologist to it. He became a one-man Depart ment of Agriculture, occupied with projects far

Glowworms

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Glowworms

Glover, Townend, F igure 27 Townend Glover.

broader than entomology. He recommended fumigation of insect-infested shipments from abroad, a clairvoyant policy which has never been followed totally and adequately. He also was occupied with the biological collections of the (Fig. 27) Department of Agriculture. Ill and with failed vision, he resigned in 1878 and went to live in Baltimore with his adopted daughter. The copper plates that he assembled (273 of them) of his drawings of insects were never used to illustrate a major text on entomology but eventually, after his retirement, were bought by the U.S. Government Committee of Agriculture. He was succeeded as U.S. Entomologist by Charles Riley, another Englishman. He died in Baltimore on September 7, 1883, survived by his wife and adopted daughter.

Reference Mallis A (1971) Townend Glover. In: American entomolo gists. Rutgers University Press, New Brunswick, New Jersey, pp 61–69

Although this term is sometimes applied to any insect that produces light, it is more correctly applied to Arachnocampa spp. (Diptera: Keroplati dae). These insects live in New Zealand and Australia, often in caves or other dark shelters. The best known are A. luminosa of New Zealand, and A. richardsae, A. flava and A. tasmaniensis of Australia. The larvae have organs that produce blue-green light. The light is used to attract prey, which are then ensnared in vertical silk threads coated with sticky mucous material that the larvae dangle from the ceiling of the cave or shelter. They are most frequent along streams, and suffer if exposed to low humidity. Elsewhere, other light-producing flies include Keroplates sesioides in Sweden, K. testaceus in Germany, K. nipponicus in Japan, and Orelia fultoni in the Appalachian Mountains of the USA. Several relatives of these insects pro duce long sticky threads for prey capture but are not luminescent. Fireflies or lightningbugs (Coleoptera: Lampyridae) are sometimes called glowworms, but it is best not to apply this term to lampyrids. Glowworms produce about 130 spherical eggs that measure about 0.75 mm in diameter. They hatch in 1–3 weeks depending on tempera ture. The larvae construct a hollow, tubular nest of silk and mucus, release sticky threads and begin light production. There are five instars, with the larva attaining a length of about 30–40 cm in about nine months. This is the only stage that feeds. The pupa is suspended by two silk strands, and in some species the pupal stage is lumines cent. Pupation requires about two weeks. Upon emergence, the adults are quite different in appear ance, the female being much larger and heavier. The adults live briefly, not more than one week, and the adult males are more active fliers. The adult females of some species luminance inter mittently. Mating occurs upon emergence and females mate only once. Females, being poor fliers, tend to lay their eggs near where they emerged.

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Glowworms are not selective in their feeding behavior, taking anything that is captured on their sticky threads.

References Baker CH, Merritt DJ (2003) Life cycle of an Australian glow-worm Arachnocampa flava Harrison (Diptera: Keroplatidae: Arachnocampinae). Aust Entomol 30:45–55 Meyer-Rochow VB (2007) Glowworms: a review of Arachnocampa spp. and kin. Luminescence 22:251–265

Glycogen A polysaccharide found in insects that is one of the two most common carbohydrate stored reserves (the other is trehalose) for insect flight. It occurs principally in the glycogen, fat body, and gut tissues. Glucose is released for metabolism from glycogen. Glucose usually is transported by the hemolymph as trehalose.

GLP An acronym for “Good Laboratory Practice,” representing internationally recognized, sound standards of conduct and procedures. The objec tive of GLP is to ensure the generation of high quality and reliable test data. In entomology, GLP is usually reference to the context of pesticide assessment, but has broad application to laboratory-based science, and has a corre sponding protocol for field research, “Good Field Practice” (GFP).

Glyphipterigidae A family of moths (order Lepidoptera). They com monly are known as sedge moths.  Sedge Moths

 Butterflies  Moths

Gmelin, Johann Friedrich Johann Gmelin was born in Tübingen, Germany, in 1748, the son of a professor of medicine. In 1768, at the age of 20, he took a three-year journey through Holland, England, and Austria. In 1771, he became an untenured professor of medicine at Universität Tübingen, and three years later a tenured professor at Universität Göttingen. His (1787) treatise “Abhan dlung über die Wurmtroknis,” which described effects of Ips typographus, was a major contribution for forest entomology. He contributed pages 1517– 2224 to the 13th edition (1790) of Linné’ s “Systema naturae…” He died in 1804 at the age of 56.

Reference Schwertfeger F (1973)Forest entomology. In: Smith RF, Mittler TE, Smith CN (eds) History of Entomology. Annual Reviews Inc, Palo Alto, CA, pp 361–386

Gnat Bugs Members of the family Enicocephalidae (order Hemiptera).  Bugs

Gnotobiotic Culture Culture of insects when all the species (usually of microorganisms) are known.

Goat Moths Some members of the family Cossidae (order Lepidoptera).  Carpenterworm Moths  Butterflies and Moths

Gold Moths (Lepidoptera: Axiidae)

Goblet Cells Goblet-shaped cells found in the midgut of some insects. They house a proton ATPase pump that pumps hydrogen into the goblet cavity. Potassium is exchanged for hydrogen in the goblet cells, a process that creates transmembrane voltages, cre ates a high midgut pH, and aids in absorption of amino acids released in digestion.

Goblets Small, round structures located on the spiracular plate of ticks.

Gobryidae A family of flies (order Diptera).  Flies

Goeldi, Emil (Emilio) August Emil Goeldi was born in Ennetbühl im Obertoggenburg, Switzerland, on August 28, 1859. His schooling was in Switzerland until in 1882 he entered Universität Jena in Germany and studied zoology and anatomy. After he was awarded a doc toral degree, he was offered three job possibilities overseas, and of these he chose to become a pro fessor in Rio de Janeiro. There, he worked in the Museu Nacional under the auspices of Brazil’s emperor, Dom Pedro II. When a republic was pro claimed in 1889, he lost his job and went to live in the montane Colonia Alpina of Serra dos Órgãos. Later, the new Brazilian government offered him the job of founding a new museum at the mouth of the Amazon, so in 1894 he traveled to Belém, and in a few years had built a large institution, the Museu Paraense. He began two scientific journals, the Boletím and the Memórias of that museum which became known, even in his lifetime, as Museu Goeldi. His first name is usually written in Brazil as Emilio, in keeping with Portuguese

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spelling. He collected extensively and published numerous papers on various animal groups. Some of those works were on insects, including Coleoptera and Diptera (a major work on the mosquitoes of the state of Pará). In 1907 he returned to Switzerland to teach at Universität Bern. He published (1913) a book on medical zoology, “Die sanitarischpathologische Bedeutung der Insekten und Verwandten Gliedertiere, namen tlich als Krankheits-Erreger und Krankheits Uber trager” drawing upon his experiences in Brazil. He died in Zurich on July 5, 1917.

References Anon. (2002) Emil August Goeldi. Available at http://www. macalester.edu/environmentalstudies/ARLab/; Hypo geanFishes/biogoeldi.hrm. Accessed August 2002 Papavero N (1973) Emil Goeldi. In: Essays on the history of Neotropical dipterology, with special reference to col lectors (1750–1905). vol 2, Museu de Zoologia, São Paulo. pp 374

Gold Moths (Lepidoptera: Axiidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Gold moths, family Axiidae, are a very small family of only six Palearctic species in the Mediterranean region, mostly in the genus Axia. The family is in the superfamily Drepanoidea, in the section Cos sina, subsection Bombycina, of the division Ditry sia. Adults medium size (23–30 mm wingspan), with head scaling normal; labial palpi slightly por rect but very short; maxillary palpi vestigial; anten nae bipectinate. Wings elongated and triangular, with relatively acute forewing apex; hindwings tri angular and rounded (Fig. 28). Maculation mostly shades of brown to pink, but with at least one bright iridescent mark (often golden color); hind wings unicolorous. Adults nocturnal. Larvae are leaf feeders. Host plants all are in Euphorbiaceae.

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Gomphidae

Gondwanaland Moths (Lepidoptera: Palaephatidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Gold Moths (Lepidoptera: Axiidae), Figure 28 Example of gold moths (Axiidae), Axia theresiae schelhornae Amsel from Iran.

References Chrétien P (1916) Observations sur la Cimelia margarita, Hb. In: études de Lépidoptèrologie Comparée, 12:37–65, pl. A–D, 502 Freina, JJ de, Witt TJ (1987) Familie Axiidae Rebel 1919. In: Die Bombyces und Sphinges der Westpalaearktis, Forsc hung & Wissenschaft Verlag, Munich, 1:298–302, pl. 23 Marten W (1937–1938) Zur Kenntnis der Axiidae. Entomolo gische Rundschau 54:306–308, 408–412, 493–497, 511– 515, 534–536, 543–548, 576–579 (1937); 55:15–17, 21–23, 46–48, 61–66 (1938) Rebel H (1923) Axia (Cimelia) margarita Hb. und eine neue Lepidopterenfamilie: Axiidae. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 69 (Lepid.):111–114 Reisser H (1933–1934) Beitrag zur Kenntnis der Axiidae (Lep. Heteroc.). Die Biologie der Axia (Cimelia) napoleona Schaw. nebst übersetzung der Chrétienschen Arbe1it über Cimelia margarita Hbn. Internationalen Entomol ogische Zeitschrift, 27:357–364, 381–387 (1933), 433– 437, 473–479, 485–489, pl. 1–4 (1934)

Gondwanaland moths, family Palaephatidae, total only 31 known species, with 28 from Chile and Argentina and three from Australia. The fam ily forms a monobasic superfamily, Palaepha toidea, in the section Nepticulina, of the division Monotrysia, infraorder Heteroneura. Adults small to medium (8–36 mm wingspan), with head roughened; haustellum is average length and naked (unscaled); labial palpi short and porrect, and 3-segmented; maxillary palpi 5-segmented (rarely 4-segmented and short), long and folded; antennae rather short. Wing venation is heteroneurous, with frenulate wing coupling, and usually with somewhat falcate fore wing tips. Maculation is variable, usually with various spots; without large fringes (Fig. 29). Adults are thought to be diurnally active. Biolo gies are little known and the single known species has larvae that tie twigs together on its host plants (Verbenaceae and Proteaceae).

Gomphidae A family of dragonflies (order Odonata). They commonly are known as clubtails.  Dragonflies and Damselflies

Gonad The basic component of the reproductive system, possessed by both males (testes) and females (ovaries).

Gondwanaland Moths (Lepidoptera: Palaephatidae), Figure 29 Example of Gondwanaland moths (Palaephatidae), A zaleodes micronipha Turner from Australia.

Gorgas, William Crawford

References Davis DR (1986) A new family of Monotrysian moths from Austral South America (Lepidoptera: Palaephatidae), with a phylogenetic review of the Monotrysia. Smithso nian Contrib Zool 434:1–202 Nielsen ES (1987) The recently discovered primitive (nonditrysian) family Palaephatidae (Lepidoptera) in Aus tralia. Invertebr Taxonomy 1:201–229 Parra LE, Ibarra-Vidal H (1994) Descripcion de los estados inmaduros y notas biologicos sobre Metaphatus ochraceus (Lepidoptera: Palaephatidae), defoliador del notro (Embothrium coccineum). Revista Chilena de Entomo logia 21:77–84

Gonopod An appendage of the genital segment modified for copulation, insemination or oviposition.

Gonopore The external opening of the ejaculatory duct (in males) or oviduct (in females).

Gorgas, William Crawford William Gorgas was born on October 3, 1854, near Mobile, Alabama. The son of General Josiah Gor gas, William graduated from the University of the South in 1875. General Josiah Gorgas was an offi cer in the Confederacy during the American Civil War, so it is perhaps not surprising that William was denied entrance to the premier American mil itary college, the United States Military Academy at West Point, New York. William was determined to have a military career, a prestigious career in earlier days, so he entered the military by way of a medical degree. In 1880 he entered the U.S. Army Medical Corps as an assistant surgeon. William Gorgas’ life was fairly average for about two decades after entering the military. However, he was stricken by yellow fever early in his career, and thereafter he was immune, so was

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frequently drafted for service wherever yellow fever was a problem. Yellow fever was an enigma at that time, and its appearance, impact, and the inability to control the disease were quite puzzling. Gorgas was dispatched to Cuba during the Spanish-American War, in 1898, when yellow fever was seriously affecting American troops. The pre vailing approach for the management of the dis ease at that time was fire, and the village and hospital to which Gorgas was assigned were torched in September of that year. In 1898, Gorgas was made chief surgeon of Havana, Cuba, and he followed the generally accepted methods of yellow fever management, relying primarily on sanitation and isolation. However, it was not until the Cuban doctor Carlos Finlay, the English scientist Ronald Ross, and the U.S. Army doctor Major Walter Reed identified the Aedes aegypti mosquito as the vector of yellow fever that truly effective practices of management could be implemented. Prior to this time, yellow fever was thought to be transmitted from person to person via personal belongings or merchandise on which the organism was carried, and attempts to prove that mosquitoes could transmit the dis ease had been futile. Indeed, the earliest attempts to clean up Havana were unsuccessful because although the sanitation efforts cleaned up the water and debris, the relevant vector was favored by clean water and so prospered. However, once all mosquito breeding sites in the city of Havana were eliminated by either preventing mosquitoes from accessing water, or by oiling the surface of water where mosquitoes were likely to breed, yellow fever was effectively suppressed. Thus, Gorgas came to believe that environmental sani tation, and particularly mosquito management, could be used to reduce or eliminate yellow fever. At the turn of the century, the development of the Panama Canal was in progress. The French were stymied in their efforts to complete the project due to yellow fever and malaria, losing 20,000 lives in an eight year effort to construct the canal. Ironically, the U.S. government seemed

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similarly inclined to ignore taking adequate measures to prevent workers from contracting the disease. The Canal Commission considered health measures to be extravagant expenditures, but as disease extracted a lethal toll on workers, Gorgas’ ideas on sanitation received a better reception. He promoted the draining of swamps in Panama, thereby mitigating malaria and yellow fever and greatly prolonging the life of workers involved in the construction project. Even after conditions improved, Gorgas’ enemies were quite effective in discrediting him and his mosquito control policies, and it took the intervention of President Theodore Roosevelt to assure that his procedures would be implemented. Even then, the U.S. military attacked Gorgas’ sanitary ser vice. Gorgas prevailed, however, and made the Panamanian cities of Panama and Colon as safe as any city in the United States. In 1914, based on his successes in Panama, Gorgas was appointed Surgeon General in the U.S. Army. He retired in 1918, but was commis sioned to investigate the yellow fever situation in western Africa. Unfortunately, he experienced a stroke in 1920, and died a month later in London on July 4, 1920. William Gorgas is remembered as the person whose sanitation skills allowed construction of the Panama Canal, a monumental achievement. His achievements at managing yellow fever in Havana are overshadowed by the Panamanian successes, but even the Cuban successes would accord him considerable recognition.  History and Insects  Yellow Fever  Malaria  Reed, Walter

References Gibson JM (1950) Physician to the world: the life of General William C. Gorgas. Duke University Press, Durham, NC, 315 pp Litsios S (2001) William Crawford Gorgas (1954–1920). Persp Biol Med 44:368–378

Gossamer-Winged Butterflies (Lepidoptera: Lycaenidae) john b. heppner Florida State Collection of Arthropods, Gainesville, FL, USA Gossamer-winged butterflies, family Lycaenidae (including blues, coppers, elfins, hairstreaks, and harvesters), total about 5,955 species worldwide; the actual fauna probably exceeds 7,000 species. About 1,125 species are Neotropical. The family is in the superfamily Papilionoidea (series Papilioni formes), in the section Cossina, subsection Bom bycina, of the division Ditrysia. Most of the relictual groups are Southeast Asian and African, such as the subfamilies Lipteninae, Poritiinae, Liphyrinae, Miletinae, and Curetinae. The family has eight subfamilies: those just noted, plus Lycaeninae, Theclinae, and Polyommatinae. North temperate species are only found in the latter three subfamilies. Some specialists include Riodinidae as another lycaenid subfamily, and also reduce the subfamily number to five (including the Riodini nae), thus the classification is still in flux. Adults small to medium size (6 to 92 mm wingspan) (most average 20 to 39 mm), with body usually slender (rarely robust). Wings mostly rounded, but some with acute forewing apex; hindwings some times with tails (usually very narrow tails) (Fig. 30). Maculation varied but often with blues, greens or other bright colors, and with iridescence or lus trous shine, and often without many dorsal spots (more spotting usually on ventral sides of both wings); hindwings often with color spots near tails at the tornal corner of the wing margin (so-called “false heads”); and fringes short but often white or lustrous. Adults diurnal, but a few of the relict gen era possibly crepuscular or only in dark forests. Larvae mostly somewhat slug-like, with tubercles and short setae; head usually retractable into tho rax. Larvae feed as leaf feeders (some on other plant parts), but many are myrmecophilous and some even are carnivorous on ant larvae or hemipterans (especially Liphyrinae and Miletinae).

Graham, Marcus William Robert De Vere

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Gracillariidae A family of moths (order Lepidoptera). They com monly are known as leafminer moths or leaf blotch miners.  Leafminer Moths  Butterflies and Moths

Gossamer-Winged Butterflies (Lepidoptera: Lycaenidae), Figure 30 Example of gossamer-winged butterflies (Lycaenidae), Hypaurotis crysalus (W. H. Edwards) from New Mexico, USA.

Some of the relict groups feed on lichens (Lipteni nae). Host plants are in a wide variety of plant families, particularly Fagaceae and Leguminosae. A few economic species are known.

References Clark GC, Dickson CGC (1971) Life histories of the South African lycaenid butterflies. Capetown. 272 pp, pl. 125 Eliot JN (1973) The higher classification of the Lycaenidae (Lepidoptera): a tentative arrangement. Bull Br Mus Nat Hist Entomol 28:371–505, pl. 6 Huang SMY (1943) The Chinese Lycaenidae. Notes Entomo logicae Chinois 10:67–213 New TR (1993) Conservation biology of Lycaenidae (Butter flies). IUCN, Gland, S173 pp Pleisch E, Sonderegger P (eds) (1987) Lycaenidae – Bläulinge. In Schmetterlinge und ihre Lebensräume: Arten – Gefährdung – Schutz. Schweiz und angrenzenden Gebi ete, Pro Natura-Schweizerische Bund fuer Naturschutz., Basel, 1:319–402, pl. 21–25 Seitz A (ed) (1908–1931) Familie: Lycaenidae. In: Die GrossSchmetterlinge der Erde A. Kernen, Stuttgart, 1:257–328, pl. 72–83 (1908–1909); 1(suppl.):239–306, 351–353, 817–832, pl. 15–16 (1930–1931); 5:739–832, 1043–1046, pl. 144–159 (1919–1924); 13:297–504, pl. 63–74 (1914–25) Stempffer H (1967) The genera of the African Lycaenidae (Lepidoptera: Rhopalocera). Bull Br Mus Nat Hist Entomol Suppl 10:1–322, pl 1

Gradual Metamorphosis This is a type of incomplete metamorphosis (hemimetabolous development) found in some aquatic insects (Odonata, Ephemeroptera, Ple coptera). Unlike insects displaying the typical form of incomplete metamorphosis, in which the immature and adult stages are substantially the same in body form (differing principally in the presence of fully formed wings among the adults), immature and adult stages of these aquatic insects differ slightly to significantly in appear ance as compared to their adults. However, they lack a pupal stage, which is characteristic of insects with complete metamorphosis (holome tabolous development). Because these insects depart from the typical pattern of hemimetabo lous development, they sometimes are said to have gradual metamorphosis or paurometabolous development. Consistent with this differentiation, the immature are sometimes called naiads rather than nymphs (contrast with incomplete meta morphosis, complete metamorphosis).  Metamorphosis

Graham, Marcus William Robert De Vere Marcus Graham was born in the county of Durham, England, on March 25, 1915. As a boy, he became intrigued with natural history. At the start of World War II, he enlisted in the British army, and served in India from 1942 to the end of

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Grain Beetles

1945. But he had begun to publish entomological papers in 1941. At the end of 1945, he entered Trinity College, Dublin, and graduated in 1950 with a B.A. degree and a B.Sc. degree. In Dublin, he studied the taxonomy of Braconidae, then turned to Chalcidoidea. He was soon appointed to the post of curator of the insect collections of the Hope Department of Entomology, Oxford University. He married in 1953. In 1955, he was awarded the degree of D.Phil. from Oxford University. He taught, took part in administra tion, and conducted taxonomic research on Hymenoptera until his retirement in 1981. His research was meticulous, he solved many puzzles resulting from inadequate descriptions by early taxonomists of Hymenoptera, and became the foremost authority on European Chalcidoidea. He produced major contributions on the Euro pean Pteromalidae, Tetrastichinae (Eulophidae), Encyrtidae, and Myrmaridae. He described 60 genera and 475 species of Hymenoptera. Apart from insect taxonomy and botany, he was inter ested in Romance languages and medieval litera ture, painting, and naval history. After retirement, he continued to work (his total production was some 200 papers) and was working on a revision of the genus Torymus (Torymidae) when he died, on March 27, 1995. He was survived by his wife, Nora, and son.

Reference Bouček Z, Noyes JS (1997) Marcus William Robert de Vere Graham (1915–1995) [with a bibliography]. Entomol Mon Mag 133:83–93

Grain Beetles Several beetles are important pests of stored grain.  Stored Grain and Flour Insects

Grain Borers Several beetles in the family Bostrichidae are important grain pests.  Stored Grain and Flour Insects

Grain Weevils Several weevils are serious pests of stored grain.  Stored Grain and Flour Insects

Gramineous Lepidopteran Stem Borders in Africa rami kfir ARC-Plant Protection Research Institute, Pretoria, South Africa Cereals, especially maize and sorghum, are the most important field crops grown in Africa by commercial and small-scale farmers. Sugar cane is also an important cash crop in many countries on the continent. Although maize and sorghum are grown primarily for human consumption, sur pluses are used as fodder for livestock. Among the insect pests found attacking these crops in Africa, lepidopteran stem borers are by far the most injurious. Given their great economic importance, an enormous amount of literature has accumu lated during the past century. The aim of the following sections is to briefly summarize the current state of knowledge on these stem borer pests of cereals. Special attention is given to Busseola fusca and Chilo partellus, which are the principal borer pests of maize and grain sorghum in Africa, and to Chilo sacchariphagus, a serious pest of sugar cane on the Indian Ocean islands, which has recently invaded Mozambique.

Gramineous Lepidopteran Stem Borders in Africa

Distribution of Major Stem Borers of Maize, Sorghum, Rice and Pearl Millet william A. overholt ARC-Plant Protection Research Institute, Pretoria, South Africa Lepidopteran cereal stem borers in Africa typically occur as complexes of species, with notable regional variation in their distributions. The noctuids Busseola fusca Fuller and Sesamia calamistis Hampson, and the pyralid Eldana saccharina (Walker), are present throughout most of sub-Saharan Africa, but there are important regional differences in the ecozones they inhabit, and their pest status. In east ern and southern Africa, B. fusca is a major pest of maize and sorghum at medium and high elevations (greater than 1,000 m), while in West Africa, it is considered to be important from sea level to 2,000 m. Sesamia calamistis generally is not a major pest in eastern and southern Africa, whereas in West Africa, this species is one of the most damaging to maize, sorghum and rice. Eldana saccharina is pri marily a pest of sugar cane in South Africa, while in West Africa, E. saccharina is a major pest of maize, and attacks sugar cane to a lesser degree. In some areas of East Africa, E. saccharina attacks maize, but tends to arrive late in the season when the crop is less susceptible to yield loss. Other important stem borers have more lim ited distributions. Coniesta ignefusalis (Hampson) (Crambidae) is the dominant stem borer of pearl millet in the Sahelian region of West Africa, but only a minor pest in other crops and other regions. It also has been recorded from Sudan, Ethiopia and Angola, and thus probably has a fairly wide distribution. Chilo orichalcociliellus (Strand) occurs in eastern Africa, mainly in lowland coastal zones, where it once was considered to be a major pest of maize and sorghum. However, recent studies suggest that den sities of C. orichalcociliellus have decreased due to competition with Chilo partellus, an invasive Asian borer. Chilo partellus is thought to have arrived in eastern Africa in the early part of the twentieth

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c entury, and has since spread to all countries in the eastern and southern parts of the continent. It seems likely that its distribution will continue to expand westward. C. partellus is generally the most damag ing stem borer of maize and sorghum at elevations below about 1,000 m in eastern and southern Africa. Sesamia cretica Lederer, which occurs in Somalia, Sudan, Egypt, and Ethiopia, and S. nonagrioides botanephaga Lefebvre, which is found in both East and West Africa, are both important locally. Chilo aleniellus (Strand) has been reported as an impor tant pest of maize in Ivory Coast. In addition to stem borers, there are several lepidopteran cob borers in Africa, one of which, Mussidia nigrivenella Ragonot (Pyralidae), is an important pest in West Africa. This species is discussed in a later section. The important stem borers of maize, sorghum and millet are listed below (Table 5), along with an approximation of their relative importance in different regions. Information on rice stem borers is primarily from West Africa, and the Indian Ocean Islands, as these are the areas where rice is an important food crop. Chilo zacconius Bleszynski is considered to be the most important stem borer of rice through out West Africa. Maliarpha separatella and S. calamistis also are of economic importance in the region. M. separatella is the only rice borer that has a widespread distribution in sub-Saharan Africa, and also occurs in the Comoro Islands and Madagascar. Other stem borers in rice in West Africa include Scirpophaga spp., Chilo diffusilineus (de Joannis), and S. nonagrioïdes botanephaga Lefebvre. Additionally, Chilo aleniellus (Strand) is mentioned as a rice stem borer in Ivory Coast.

Distribution and Pest Status of African Sugarcane Stem Borers des E. Conlong SASA Experiment Station, Mount Edgecomb, South Africa Many subsistence farmers throughout tropical and subtropical Africa grow sugar cane for chewing

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Gramineous Lepidopteran Stem Borders in Africa, Table 5 Important stem borers of maize, sorghum and millet in sub-Saharan Africa Area of Africa Family/species

South

East

West

Central

Noctuidae

Busseola fusca

+++

+++

++

+++

Sesamia calamistis

+

+

+++

++

Sesamia cretica

+++

Sesamia nonagrioides botanephaga

++

Crambidae

Chilo partellus

+++

+++

Chilo orichalcociliellus

++

Chilo aleniellus

+

Coniesta ignefusalis

+++(millet only)

Pyralidae

Eldana saccharina

(only sugar cane)

+

+++

++

a

b

c

d

Only in Northeast Africa (Sudan, Somalia, Eygpt) Only reported as important in Ghana c Only in coastal East Africa d Only in Ghana, Ivory Coast a

b

purposes. Commercial sugar cane production, however, has an interesting history in Africa. Many countries had very strong industries in the early 1900s, which collapsed during various civil wars and for other reasons through the years. Some of these countries now are rehabilitating their industries. A few still have very strong industries, which have withstood the vagaries of time. This section deals only with the commercial sugar industries known to occur in Africa, as it is only from reports and papers emanating from these that pest records are known. Also, for the purposes of this section, Africa is divided into southern, eastern, northern and west ern regions. The countries known to have, or have had, viable sugar cane industries in southern Africa include South Africa, Swaziland, Zimbabwe, Malawi, Mozambique and Zambia. In east Africa, they are Tanzania, Kenya, Uganda and Ethiopia. In north Africa, these are limited to Egypt, the Sudan and possibly Libya. West African countries producing, or

known to have produced, sugar on a commercial scale include Sierra Leone, Ivory Coast, Burkino Faso, Ghana, Nigeria, Cameroon, Gabon, Mali, Senegal, Guinea Bissau and, more recently, Angola. In Africa, only lepidopteran larvae have been recorded as borers of sugar cane. These can attack the youngest shoots, causing dead hearts, through to the most mature sugar cane stalks. In severe infestations, the rootstock of ratooning sugar cane can harbor developing larvae, which can severely affect the regrowth of the crop. In addition, larvae of some species of Lepidoptera develop in the whole stalk when the cane is mature, others only in the top third, and still others in the bottom third. In differ ent parts of Africa, the same species may develop in the bottom third of mature sugar cane plants, while in other parts, they may develop in the top third of the stalk. Oviposition by different species of Lepi doptera attacking sugar cane also may vary. Some


species prefer to oviposit on the green leaves of sugar cane, either on the abaxial and/or adaxial surfaces of leaf blades, and in sugar cane from one month old to maturity, which may be up to 24 or 30 months old. Other species oviposit in cryptic positions, in older sugar cane behind dead leaf sheaths, in folded dead leaf blades, or even in decaying dead leaf material around the bases of mature sugar cane stalks. Until 1992, fourteen species of Lepidoptera had been recorded as attacking sugar cane in Africa. The majority of these are indigenous to the African continent. In 1999, a fifteenth species, Chilo sacchariphagus (Bojer) (Pyralidae), was con firmed as attacking sugar cane in Mozambique. This is the first record of an exotic lepidopteran establishing on sugar cane in economic propor tions in Africa. Prior to this, the only other exotic reported to occasionally attack African sugar cane has been Chilo partellus (Swinhoe) (Crambidae). Most of the boring lepidopteran pests of sugar cane belong to the families Crambidae, Pyralidae, and Noctuidae, and a ranking, in 1994, of these species (using the number of citations in Review of Applied Entomology, 1972 to 1992 to each on sugar cane) has revealed that only four are regarded as major pests in Africa. These are Eldana saccharina Walker (Pyralidae), Chilo agamemnon Bleszynski (Crambidae), Sesamia cretica Lederer and S. calamistis Hampson (both Noctuidae) (Table 6). More recently, Busseola fusca (Fuller) has been recorded occasionally from sugar cane

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in West Africa. The following table outlines the distribution of the stem borers regarded as major pests in African sugar cane, and their severity in south, east, north and west Africa. Eldana saccharina is by far the most injurious stalk boring pest in Africa. It is also one of the few attacking mature (or older) sugar cane stalks. In southern Africa is has been the subject of much research in plant resistance, biological control, insecticide and cultural means in attempts to con trol it. In southern and coastal eastern Africa, it attacks the lower portion of sugar cane stalks. However, in the Kenyan and Ugandan industries around Lakes Victoria and Albert, respectively, and in West Africa, it attacks the upper third of mature stalks. In many of the more tropical countries, sugar cane is cut at too early a stage for E. saccharina to become a pest, although if the cane is not harvested at this early age for some reason, then this borer can affect it seriously. Chilo agamemnon has received much atten tion in Egypt, where it is classed as an internode borer, thus attacking the more mature cane stalks. However, it also attacks young plants, causing dead hearts. Researchers in Egypt are working on plant resistance, as well as inoculative biological control using egg parasitoids. The Sesamia species are generally pests of young cane, causing dead hearts. By the time the sugar cane is mature though, these borers have been brought under control by parasitoids, and thus do not become major pests.

Gramineous Lepidopteran Stem Borders in Africa, Table 6 The distribution of stem borers regarded as the major pests of sugar cane in Africa, and a rating of their pest status (+++ = Major Pest; ++ =Occasionally a Pest; + = Present in Low Numbers) Area of Africa Species

South

Eldana saccharina

+++ Generally +

Sesamia cretica

b

North

West

++ Generally +

+

+

++

b

Chilo agamemnon

+

++

Sesamia calamistis

+

+

+

Only in South Africa and Zimbabwe Only in Western Uganda

a

East a

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Pest Status of Mussidia nigrivenella Ragonot, a Cob-borer of Maize in Western Africa mamoudou sÉtamou Texas A&M Research Center, Texas, USA and fritz schulthess IITA, Cotonou, Republic of Benin, In West Africa, five borer species are commonly found feeding in maize cobs, but Mussidia nigrivenella Ragonot (Lepidoptera: Pyralidae) is by far the most important across all zones. Grain yield losses are relatively low and range from 2 to 25%. Percentage of grain infected by the toxic fungus Aspergillus flavus as well as mean aflatoxin con tent of samples, however, increases exponentially with grain damage. Cob damage by M. nigrivenella also promotes the infestation of storage bee tles such as Sitophilus zeamais Motschulsky, Carpophilus spp. and Cathartus quadricollis Guérin. Furthermore, damaged cobs cannot be sold as green maize, an important source of cash in the vicinity of centers of population. Thus, in addition to the direct damage, M. nigrivenella induces indirect qualitative and quantitative losses in the field and store. Mussidia nigrivenella is highly polyphagous, and is found on 20 plant species from 11 different plant families, among them cotton, Phaseolus bean and cover-crops such as the velvet and Jack bean. In West Africa, no parasitoids were ever obtained from annual crops, and most alternate host plants. The solitary chalcidid pupal parasi toid, Antrocephalus crassipes Masi, was the pre dominant species with highest and stable parasitism on Gardenia spp. Mussidia nigrivenella has never been described from annual crops in eastern Africa, but according to some anecdotal reports is found on wild host plants. This opens the opportunity of the novel association biological control or expanding the geographic range of a natural enemy species.

Displacement of Native Stem Borers by Chilo partellus william A. overholt ARC-Plant Protection Research Institute, Pretoria, South Africa The invasive stem borer, Chilo partellus, has proved to be a highly competitive colonizer in many of the areas it has invaded in eastern and southern Africa, often becoming the most injurious stem borer, and displacing native species. In coastal Kenya, there is evidence that C. partellus has partially displaced the indigenous borer, Chilo orichalcociliellus. Whether the displacement of C. orichalcociliellus will proceed toward complete extirpation in the southern coastal area of Kenya seems unlikely. Recent sampling has shown that C. orichalcociliellus continues to persist, and laboratory studies have found that C. orichalcociliellus was able to complete development in two native grasses in which C. partellus could not develop. This difference in niche breadths of the two species may account for the continued occurrence of the native species. Addi tionally, a parasitoid of C. partellus from Asia, Cotesia flavipes (Cameron), has been introduced and established in several countries in Africa. Evidence from coastal Kenya suggests that the introduction of C. flavipes has resulted in a marked population decrease of C. partellus, but that populations of two native borers, C. orichalcociliellus and Sesamia calamistis, have slightly increased. In addition to the work in coastal Kenya, there is evidence of displacement of native stem borers in two other areas in Africa. In the Eastern Province of Kenya, work conducted in the 1980s found that C. partellus was present, but less abundant than Busseola fusca. However, in the same area in the late 1990s, B. fusca was rare and C. partellus was domi nant. Similarly, in the Highveld region of South Africa, C. partellus has partially displaced B. fusca. Several factors may be responsible for the competitive superiority of C. partellus over the native stem borers. Various studies have shown that C. partellus completes a generation in less time


than C. orichalcociliellus. As fecundities of both species are similar, the shorter generation time is likely to lead to higher population levels, which may give the alien species a numerical advantage. A more rapid diapause termination compared to both C. orichalcociliellus and B. fusca has also been shown, which may allow C. partellus females to colonize host plants before the two native species, which would be particularly important if the native species avoid previously infested plants.

Damage and Pest Status rami kfir ARC-Plant Protection Research Institute, Pretoria, South Africa Feeding and tunneling by stem borers can result in serious damage and crop losses. Damage is caused by the larvae, which at first feed on the young leaf funnels at the growing point and then later by tun neling into the stems. Apart from leaf damage, growing points may be killed, leading to stunting and deadhearts or to early senescence of plants. Stem tunneling may cause lodging, but also second ary and insidious effects, such as interference with translocation of metabolites and nutrients, result ing in malformation and loss of grain. There can also be a sharp increase in the incidence of stalk rot. Feeding in ears has been associated with fungal infection and elevated levels of mycotoxins.

Busseola Fusca In South Africa, crop loss assessments in cereal crops from B. fusca attack ranged from 10 to 100%. Although much of this was due to leaf damage in maize, the most severe loss was from stem-boring activity. In Lesotho, seasonal v ariation in maize yields due to B. fusca ranged from 0.4 to 37%. In Tanzania, 40–100% of the sorghum crop can become infested with B. fusca. Together with

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Kenya, loss of about 12% maize yield for every 10% of plants infested with B. fusca has been d ocumented. In Ethiopia, movement of B. fusca larvae into the base of the sorghum panicle resulted in undersized panicles and a 15% yield reduction. In Burundi, using insecticides and exclusion cages, 30–50% of the maize harvest was shown to be lost to B. fusca. In the Northern Guinea savanna of Nigeria, where B. fusca is the dominant stem borer, 49% loss of sorghum was reported. Comparative yields on 22 farmers’ sorghum fields in Nigeria, sprayed and unsprayed with insecticide, showed a 21% mean loss in yield due to this borer. Losses to B. fusca in sorghum crops in Nigeria are very much dependent on the time of initial infestation. Thus, sorghum infested prior to the booting stage suffered the greatest yield losses. The proportion of internodes bored in the lower part of the stalks had a more consistent negative correlation with harvested grain than did the proportion of stalks tunneled. A recent study in Cameroon showed that stem borers, pri marily B. fusca, were responsible for a 9 g loss in sorghum yield per plant per borer. There was also an 11% crop loss through deadheart.

Chilo Spp The estimated yield losses in maize and sorghum in South Africa due to C. partellus exceeded 50%. A negative correlation between the level of C. partellus infestation and yield has been demonstrated. Comparative trials in separate and mixed stem borer populations, using artificial infestation tech niques, indicated that C. partellus was more injuri ous to sorghum than B. fusca. More damage also was caused by C. partellus to long-season sorghum cultivars, mainly due to their longer exposure to stem borer attack while in the susceptible preflowering stage. In Mozambique, the third generation of C. partellus, the most important stem borer occur ring in the country, was reported to infest 87% of cobs of late planted maize and to cause 70% loss of grain. Infestations of up to 100% of the crop, with

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considerable yield losses, were recorded in the Maputo and Gaza Provinces and in the Limpopo Valley, in southern Mozambique. In Zimbabwe, C. partellus caused sorghum yields to drop by 50–60%, while in maize up to 70% damage was reported from the fields of resource-poor farmers. However, in the commer cial farming areas, where insecticides are routinely applied, maize damage was less than 30%. In Kenya, 18% loss of maize was attributed to C. partellus and C. orichalcociliellus, while 88% loss of sorghum crop to C. partellus was reported. Heavy stalk damage to maize, and up to 80% of the sorghum harvest, was lost to the latter borer on 20-day-old crops. Chilo partellus infestations caused insignificant crop loss when 60-day-old plants became infested. Similar observations were reported from Uganda.

Sesamia spp In Ghana, a positive relationship between the number of Sesamia sp. larvae and the extent of damage to maize stalks, and a negative relation ship between damage to maize stems and maize yields were demonstrated. The calculated losses caused by Sesamia sp. to maize in the rain forest, coastal, derived and Guinea ecological zones were 27, 15, 18 and 14%, respectively. Chemical control of stem borers in sorghum in the Southern Guinea savanna of Nigeria, where S. calamistis predomi nates, increased yields by 16–19%.

Eldana Saccharina In West Africa, natural infestations by E. saccharina decreased maize yields by 16, 15 and 28%, respectively, in the dry season and the first and second rainy seasons. Infested maize plots had significantly lower grain weight, indicating that E. saccharina damage to the stems affected grain filling. In Burundi, insecticides and exclusion cage trials indicated diminished maize yields of 12–15%

by E. saccharina. Curiously, in southern Africa, E. saccharina is not known as a pest of either maize or sorghum, but is a serious pest of sugar cane.

Stem Borer–Fungal Interactions kitty f. cardwell USDA, CSREES, Washington, DC, USA and fritz schulthess IITA, Cotonou, Republic of Benin Both fungi and insects possess chitin-based exteri ors. Also, both are heterotrophic, i.e., acquire nutri ents by feeding on other organisms. It is at this nutritional interface where fungi and insects often intersect, giving rise to many different types of insectfungus relationships, which can be neutral, mutually beneficial, exploitative, or antagonistic. Some rela tionships are merely opportunistic, while others are co-evolved and have become obligatory. Direct mycophagy, or fungivory, occurs when insects pref erentially select fungi as a food source. Alternatively, many fungi require insects as a food source and become pathogens. Insects that feed on plants often encounter fungi that either live within the plant as endophytes or in association with plant tissues, resulting in an indirect effect on insect fitness. Often, insects are the vehicle by which fungi gain ingress into a plant or disperse throughout a habitat. Fusarium verticillioides is an endophyte of wild and cultivated grasses. It produces mycotoxins such as fumonisin, which promotes esophageal cancer in humans and leucoencephalomalacia in horses. The fungus may attack at all growth stages of the plant and move from seed to stem into the cob. Similarly, variants of F. moniliforme have been found to pro duce the compound beauvericin, which was originally isolated from the entomopathogenic fun gus Beauveria bassiana. In a survey in southern Benin, F. verticillioides was the most common endo phytic fungus inhabiting maize stalks. Incidence was higher in plants damaged by insect pests, and was cultured from stems of 71–80% of plants damaged by stem borers. It was found that ovipositing adult


lepidopteran stem and cob borers such as E. saccharina, S. calamistis and Mussidia nigrivenella not only preferred infected plants, but that offspring had higher survival and fecundity. This relationship is completely mutualistic because the insects feeding on infected plants may also vector the fungus from soil to plant and from plant to plant. Furthermore, lepidopteran pests feeding in the ear produce exit holes before pupating, which then are used as entry holes by storage beetles, which may be grain or fun gal feeders. They, in turn, vector the mycotoxic fun gus Aspergillus flavus, which has been shown to be suppressive to S. calamistis, E. saccharina and C. partellus; M. nigrivenella, on the other hand, was not sensitive to aflatoxin or A. flavus in the diet, which makes it a perfect vector; thus, aflatoxin content in grain increase exponentially with grain damage caused by M. nigrivenella or resulting increased bee tle infestations. Control programs at the Interna tional Institute of Tropical Agriculture in Nigeria aim at both the fungi and the insects, and include biological control (e.g., Trichoderma sp.) and seed treatment against F. verticillioides, cultural control (sorting of infected ears), host plant resistance, com petitive niche displacement (the use of atoxigenic, competitive races) against A. flavus, and host plant resistance, biological control and habitat manage ment against stem and ear borers.

Larval Diapause rami kfir ARC-Plant Protection Research Institute, Pretoria, South Africa Many cereal stem borers undergo a resting period toward the end of the cropping season in response to cold and/or dry conditions. The resting period is spent as mature larvae within dry crop residues and stubble in the fields. In the elevated regions of southern Africa, B. fusca and C. partellus pass winter (May to September), which is the cold dry season, in diapause in the lower portions of the dry stalks of their host plants, where they are well protected

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from adverse climatic conditions. In West Africa, B. fusca also enters a prolonged diapause during the dry season, which takes up to six months to complete. With the start of the rains, the larvae pupate within the stems and 10–12 days later emerge as adult moths. While B. fusca diapauses throughout its dis tribution range in Africa, the larvae of C. partellus do not undergo diapause in the warmer low-lying South African provinces of Kwazulu-Natal and Mpumalanga, Swaziland and southern Mozam bique. Likewise, while C. partellus is known to dia pause in the dry season in India and on several islands off the coast of Africa, non-diapausing larval populations occur along the coast of Kenya. In periods between cropping seasons, some C. partellus larvae enter diapause within maize stubble, whereas other larvae remain actively feed ing on alternative host plants, such as Napier grass growing in the proximity of the cultivated areas. Thus, in coastal regions where there is an abundance of host plants and where the climate remains favorable, C. partellus normally exhibits continuous development. Whereas inland, on the upland plateau, which experiences a long dry or cold season, larvae enter a diapause. Similarly, C. ignefusalis in West Africa exhibits a facultative diapause within dry millet stems. In the interior of Kenya, the larvae of C. partellus and C. orichalcociliellus, together with S. calamistis, enter diapause for several months in the dry season. However, S. calamistis was reported not to enter diapause in Uganda nor in Nigeria. An increase in carbohydrates and a decrease in protein and water content of the host plant are the principal factors inducing diapause in B. fusca. Drying out of the host plant, and a gen eral deterioration in the nutritive environment, were found to induce diapause in C. partellus lar vae, even when climatic conditions remained favorable for development. Diapause also could be “artificially” induced in non-diapausing larvae by introducing them into aging maize stems. During diapause, larvae of B. fusca and C. partellus both showed a progressive decrease in weight and an increase of up to seven additional molts. The

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longer the larvae remained in diapause, the smaller the resultant moths became. Such female moths showed impaired ovarian development with fewer oocytes, and also laid fewer eggs. After eight months in diapause, the emerging moths weighed about half as much and produced half as many eggs as those moths emerging from non-diapausing larvae. Diapausing larvae of B. fusca collected in South Africa in the field during winter emerged as moths in mid-October, regardless of the date of collection and the length of time they were kept at 21°C and 60% RH in the laboratory. However, larvae of C. partellus collected during April to June from the field emerged in November, while those collected in July emerged as moths in October. Those collected in August emerged in September. Regardless of collec tion date, C. partellus started to emerge from dia pause earlier and the emergence period of the moths was up to twice as long as that found for B. fusca. In the field, C. partellus moths emerged from diapause in the second half of August and continued doing so until the first week of November, emergence thus lasting a total of 12 weeks. In contrast, B. fusca only pupated d uring October to November. B. fusca hence had an obligatory larval dia pause, whereas C. partellus had a facultative dia pause. These differences in the pattern of moth emergence following diapause explain the distinct annual generations occurring in B. fusca and the continuous overlapping generations of C. partellus observed in South Africa. Conditions of continuous moisture during the long rainy season in Kenya played a significant role in the termination of diapause in B. fusca. However, rainfall alone did not appear to be the main cause. Contact with free water was of more significance in breaking diapause than water uptake. In Ethiopia, as well as in the Ivory Coast, provision of water played an important role in promoting pupation during post-diapause dormancy of B. fusca. Any delay in wetting of larvae after diapause, and access to water early in diapause, had an adverse effect on the larvae. The key factor enabling diapausing B. fusca larvae to survive adverse conditions appears to be efficient water conservation.

A combination of temperature and photope riod also played an important role in termination of diapause of B. fusca in South Africa. Water was important in stimulating morphogenesis follow ing larval diapause. Long days accelerated termi nation of diapause in C. partellus, but under a 16 h daylight regime, termination of diapause was faster than under constant illumination. In con trast, temperature, relative humidity and day length did not affect diapause of C. partellus and C. orichalcociliellus larvae in Kenya. It appears that C. partellus larvae collected in South Africa at 25°38ʹ latitude are more affected by day length than Kenyan borer populations located near the equator. It has been suggested that the right combination of day length and temperature could be used for breaking diapause in order to rear large numbers of larvae for experimental use in plant resistance trials. Simpler and cheaper facilities could hence be used for maintaining continuous labora tory cultures of these stem borers.

Pest Management Use of Synthetic Sex Pheromones Pheromone-baited traps are useful devices for monitoring stem borer moth populations. Trap catches of male moths provide useful information for quantifying moth abundance and for alerting and timing of spray applications. From the advances made in the identification and the use of sex phero mones in stem borer monitoring, it was concluded that trapping alone was unlikely to provide effective control; mating disruption was a more likely control option. Synthetic pheromone blends for Chilo suppressalis, C. sacchariphagus, C. indicus, C. auricilius and C. zacconius have been shown to be attractive to male moths in the field. Sex pheromones for B. fusca, C. partellus, S. calamistis, S. cretica, S. nonagrioides and Coniesta ignefusalis have been identified and are now commercially available. Several years of monitoring B. fusca moths in South Africa with the aid of sex pheromone


traps have revealed that the first flight of moths, emerging from overwintering larvae, peaked about mid-November. A second, larger flight then occurred in the latter half of February, while a third flight peaked around mid-April. No moths were trapped during winter (June to September). In the field, larval peaks of B. fusca lagged from 4 to 6 weeks behind the corresponding moth flight peaks. Omni-directional traps were found to be superior to delta traps for quantitative and quali tative estimation of B. fusca moth populations. More research into trap design and the correla tion between trap catches and subsequent field infestations are required before trapping of C. partellus moths can be used in predicting economic threshold levels. A slow-release pheromone formulation pro duced high levels of mating disruption in B. fusca when applied at 40 g a.i. per hectare at 250–500 release points per hectare. This effect persisted for at least 18 weeks and, based on release rate studies, was predicted to last for six months. In field trials in Kenya, some reduction in damage levels was observed, suggesting that mating disruption had indeed occurred.

Cultural Control Cultural control is probably still the most relevant and economical method of stem borer control available to farmers in Africa. Other control meth ods are less practical. For example, pesticides often are unavailable or are too expensive for resourcepoor farmers. Resistant cultivars are likewise not easily available, nor can biological control of stem borers be completely relied upon. Cultural control is amongst the oldest, tradi tional, farming practice known. It is considered the first line of defense against stem borer pests and includes methods such as removal and destruction of old crop residues, intercropping, crop rotation, manipulation of planting dates and use of different tillage methods. The latter three cultural practices are of particular importance and

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can directly benefit crop yields. Though many of these cultural practices are very labor intensive, they do have the advantage of having minimal environmental impact and also can be readily implemented without extra capital investment. However, adequate knowledge of stem borer biology and phenology, together with a close working relationship with the crop through all its growth stages, are essential for the development of efficient cultural control strategies. The differences found in the behavior of E. saccharina in South Africa and in East Africa affords an example of the importance of pest knowledge in making the right control decision. In South Africa, larvae of E. saccharina mainly infest the lower part of sugar cane stalks and farmers therefore cut off the tops of the cane, which are simply left lying as crop residues in cane fields. In contrast, the same larvae in East Africa largely occur in the upper cane, and any tops of plants left as residues would therefore pro vide a further source of infection and exacerbate the carry-over of the pest population. Although cultural control options for stem borer management appear promising and offer relief, many African farmers have not adopted them. Cultural control is still severely constrained by a lack of management capability of farmers, especially in areas where agricultural extension services are inadequate.

Managing Crop Residues Crop residues are especially important for the carry-over of stem borer larval populations from one growing season to the next. In Nigeria, larvae of B. fusca, E. saccharina and S. calamistis were found in crop residues below the soil surface, and higher incidences of these borers always occurred in no-tillage plots. In Kenya, C. orichalcociliellus, C. partellus, E. saccharina and S. calamistis were observed in stalks after harvest. In Ethiopia, a con siderable proportion of B. fusca larvae survived in the stubble. In Uganda, untreated crop residues often were used to mulch the next crop. Under

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these conditions, moths emerging from the previ ous crop constantly reinfest newly planted crops. An effective control option would thus be to reduce the first generation moth populations by destroying the bulk of the mature larvae overwin tering in the old stalks. Plowing, in order to bury the maize stubble, proved an effective measure for controlling B. fusca infestations as far back as the 1920s in South Africa. In Zimbabwe, it was observed that B. fusca moths experienced difficulty in emerging through 5 cm of soil and that deep burial under 10–15 cm of soil could totally prevent moth emergence. Deep plowing tillage in South Africa, where large areas are under maize or sorghum and where den sities of up to 226,000 borer larvae per hectare have been estimated, is thus a viable control option for B. fusca and C. partellus. Slashing of maize and sorghum stubble to expose overwintering larvae to the elements and natural enemies destroyed 70% of C. partellus and B. fusca populations, while additional plowing and disking destroyed a further 24% of the pest population in sorghum and 19% in maize. However, for these cultural control measures to be really effective, the close cooperation of all farmers in a particular region is required because moths emerging from untreated fields will readily infest neighboring crops. Currently, this cultural control strategy is no longer so widely practiced in South Africa, owing to the advent of minimum tillage and to the importance of providing winter grazing on old maize fields for beef cattle. In rural Africa, farmers often use the dry stalks of maize, sorghum and millet as building construc tion material in their houses and fences, in contour terracing and for use as stakes. Stalks also are kept for fuel and for use as bedding for livestock. Farm ers often stack the dry stalks in the field, where they are kept until the start of the rainy season, thus cre ating ideal reservoirs of stem borer infection. To solve this problem, early cutting of stalks and hori zontal placement on the soil surface have been rec ommended. This was found to cause 97% mortality of stem borers in maize and 100% in sorghum in

Ethiopia. This practice also has reduced the resid ual population of borers in uncut millet stems from 16% to 3%. The high levels of mortality of C. partellus, C. orichalcociliellus and S. calamistis larvae observed in horizontally placed stalks was ascribed to the combined effects of radiant heating and high temperatures on the thermal tolerance of borer lar vae. On the other hand, in Nigeria, the control of S. calamistis, B. fusca, C. ignefusalis and E. saccharina, through removal of maize stalks and stubble after harvest, did not reduce stem-borer populations sig nificantly, apparently because of immigration of moths into the crop. Control of B. fusca and C. partellus by burning old stalks and other crop residues after harvest also has been recommended. For example, almost com plete eradication of C. partellus was achieved on maize and sorghum in Tanzania after setting fire to old crop residues. However, in Nigeria where the majority of farmers make use of their old sorghum stalks and do not normally burn them after har vest, a partial burn when the leaves were dry and the stalks still green gave up to 95% control of C. partellus larvae. The heat generated from burn ing the leaves apparently killed the larvae inside their tunnels. At the same time this cured the stalks, which not only improved their strength for build ing purposes, but also made them more resistant to termite attack. On the other hand, crop residues are the only organic matter that is added to the soil on many small scale cultivations in Africa. Burning of old crop residues can thus deprive the soil of organic matter and also result in increased soil degradation due to wind and water erosion.

Manipulation of Sowing Dates and Plant Densities Planting crops when the pest is least abundant ensures that the more susceptible early growth stages escape becoming infested. In Kenya, an attempt to legislate this principle was made for controlling B. fusca on maize during the 1920s and 1930s. The aim was to restrict maize plantings to


the February to May period, a time when moth infestations were normally low. Unfortunately, there is no available information on the efficacy of these measures, and the last attempt at implementing such legislation was in 1937–1938, after which it fell into disuse. In West and Central Africa, early planting has been found to reduce B. fusca and S. calamistis infestations. Reports of increased stem borer dam age to late maize plantings, as compared to early plantings, have come from Benin, Cameroon, Ghana, Nigeria, Burundi and Zaire. In some areas of West Africa, farmers also do not plant maize during the second rainy season because of the risk of severe infestation. This also influenced the borer populations found in the rain forest zone, where alternative wild host plants in the dry season are scarce. Early planting of cereals also is practiced in the semi-arid tropics, where rainfall is variable and unpredictable. Late sowing, however, is also unpopular because of poor yields, even in the absence of stem borer damage. On the Highveld region of South Africa, the second generation of B. fusca in mid-summer is larger and causes more damage than the first spring generation. The best control strategy is hence to plant early in the season. Similar condi tions apply to Lesotho, Zimbabwe and Ethiopia, where second generation larvae caused crop losses of 23–100% as compared to 0–23% by first genera tion larvae. At lower elevations in South Africa, it is rec ommended that sorghum be planted after midOctober to avoid infestation from the first moth peak of C. partellus. In Tanzania, it was shown that maize planted early in the season was more liable to severe infestation by B. fusca than later maize plantings. In Malawi, planting date also influenced pest levels of B. fusca and C. partellus on sorghum. However, the choice of optimum sowing date also depended on the sorghum cultivar planted. In contrast, in the Sahelian region, manipulating the planting dates of millet was not an effective option against infestation by C. ignefusalis.

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Sowing density may also affect crop growth and thereby influence pest population levels. The behavior of the pest in its search for food or for oviposition sites may well be adversely affected by plant density. Young C. partellus larvae need to migrate from their hatching site to the leaf funnels or to reach adjacent plants within their immediate vicinity. During this critical migration period, up to 100% mortality of the first instar larvae may occur. The lowest incidence of deadheart was caused by B. fusca at low plant densities of sor ghum in South Africa and from maize in Nigeria. Conversely, a reduction in row width increased the number of stem borer larvae infesting adjacent crop rows through migration, and this in turn resulted in greater crop damage. B. fusca larvae can migrate up to a distance of 2.4 m from their eclosion site. At the standard 90 cm inter-row planting distance used in commercial maize pro duction in South Africa, lateral transmission over ±4 rows of maize is thus possible. Rather than reducing plant densities within individual rows, wider row spacings also have been used in the Ivory Coast in an attempt to reduce B. fusca and E. saccharina damage to maize. However, studies on C. partellus in maize and on C. ignefusalis in millet, planted at different crop densities, showed no significant differences in stem borer incidence. In subsistence farming systems in Africa, where farmers normally intercrop cereals with other crops, and where lack of water is an overrid ing constraint, manipulation of sowing dates and plant densities is not always possible. Farmers gen erally must plow and plant after the first rains have fallen, rendering some of these cultural control alternatives impractical.

Fertilizers Providing fertilizer to cereal crops has been shown to increase stem borer infestation and sur vival of borer larvae. For example, damage to rice by Maliarpha separatella in Nigeria increased with

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fertilizer application, while sorghum plants with no fertilizer supplied were less preferred for ovi position by C. partellus moths in South Africa. However, no such differences were observed in similar oviposition behavior trials with B. fusca. However, in South Africa, where E. saccharina is a problem on sugar cane, a reduction in nitrogen fertilizer rates from 50 kg to 30 kg per hectare proved beneficial. Increased survival of S. calamistis larvae and accelerated larval development occur with increased nitrogen content of maize resulting from fertilizer treatment. It also was suggested that addition of fertilizer might stimulate additional annual generations of stem borers. Although nitrogen fertilizer enhanced borer development, it also had a positive effect of increasing host plant tolerance to borer attack. Yield losses decreased linearly from 20% with no fertilizer, to 11% with 120 kg nitrogen added per hectare. It also has been reported that timing of nitrogen fertilizer application influenced the inci dence of C. ignefusalis on millet. The suggestion has been made that by manipulating the timing and quantity of nitrogen fertilizer, a compromise between using low fertilizer levels to dampen stem borer infestation, and high fertilizer levels to stim ulate better yields, might be achievable.

Intercropping and Habitat Management zeyaur R. khan ICIPE, Nairobi, Kenya Small-scale farmers in Africa practice intercropping or mixed cropping to reduce risk of crop failure, attain higher yields, and improve soil fertility. Although no studies have shown that farmers grow specific intercrops to reduce insect pests, some of these practices also lead to suppression of cereal stem borer populations. Studies in Kenya have con centrated both on the practice of intercropping cow pea with maize and sorghum, and on the ways in which these systems could be adopted by small-scale

farmers in the region. Most studies on intercropping have shown a reduction in the incidence of stem borers. Maize/cassava intercropping systems in Nigeria were found to reduce by half larval numbers of stem borer populations. Unfortunately, many of these intercropping studies did not seek to deter mine the underlying mechanisms behind the effect of intercropping on stem borer populations. Inter cropping maize with cowpea was an effective way of reducing damage caused by C. partellus, because 30% of C. partellus oviposition was on cowpea. Planting an outer encircling row of a highly preferred host to act as a trap plant is a useful diver sionary tactic to control stem borers. Napier grass, Pennisetum purpureum, and Sudan grass, Sorghum vulgare sudanense, common fodder plants in Africa, are reported to provide natural control of stem borers by acting as trap plants. Although the stem bor ers oviposit heavily on the attractive Napier grass, only very few larvae are able to complete their life cycles. In on-farm trials in Kenya, planting Napier grass around maize fields has been shown to signifi cantly increase crop yields by reducing the stem borer population in maize. Sudan grass provided natural control of stem borers by acting as a trap plant, and as a reservoir for its natural enemies. A recent study from Kenya has reported the effectiveness of intercropping maize with a non-host grass, Melinis minutiflora. In field trials, M. minutiflora showed no colonization by stem borers, and when used as an intercrop with maize, significantly reduced stem borer infestation in the main crop. A significant increase in parasitism of stem borers by the larval parasitoid Cotesia sesamiae was also observed. Volatile agents produced by M. minutiflora repelled stem borers but attracted C. sesamiae. Female C. sesamiae were attracted to (E)-4,8-dimethyl-1,3,7-nonatriene, one of the vol atile components released by intact molasses grass. While serving as an effective cover crop, M. minutiflora at the same time provides good fodder for livestock. The grass is now being tested in on-farm trials in Kenya to control stem borers on maize. For the control of stem borers in resourcepoor maize farming systems in eastern Africa, “push-pull” or stimulo-deterrent diversionary


t actics have been developed. These strategies involve combined intercropping and trap crops. Stem borers are trapped on highly susceptible trap plants (pull) and are driven away from the maize crop by repellent intercrops (push). The plants that are used as trap or repellent plants in a push-pull strategy are Napier grass, Sudan grass, M. minutiflora and silverleaf desmodium, Desmodium uncinatum. Napier grass and Sudan grass are used as trap plants, whereas M. minutiflora and silverleaf desmodium repel ovipositing stem borers. All four plants are of economic importance to farmers in eastern Africa as livestock fodder. Before making decisions on the use of inter crops and trap plants for stem borer control, it would be important to assess economic impact as well as the biological effects. The economic gain from the use of intercrops usually depends on the balance between a lowered cost of stem borers control and the increased cost of maintaining an intercropped field, along with any decrease in yield of the main crop from greater plant competition. Net profit can be increased if the intercrop favorably changes the balance between income and costs.

Host Plant Resistance Host plant resistance as an approach to pest man agement in gramineous crops confers many advan tages. Resistant crop varieties provide an inherent control that involves no environmental problems, and are generally compatible with other insect con trol methods. Major emphasis on the host plant resistance work in Africa has been on screening maize and sorghum crops against Chilo partellus and Busseola fusca. Attempts have been made to understand the nature of C. partellus and B. fusca resistance in maize and sorghum. A general associa tion between plant phenology and resistance to stem borers has been established. A wide range of mechanisms are involved in C. partellus and B. fusca resistance in maize and sorghum, including nonpreference for oviposition, reduced larval settling, reduced larval feeding and food utilization, and reduced larval survival and development. The cause

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of ovipositional antixenosis mechanism in maize against C. partellus was found to be a high number of trichomes on the lower leaf surface. Information on the mode of inheritance and the number of genes involved in the resistance of plants to particular insect species, although not essential for breeding plants, has great practical significance for identifying donors for resistance, developing isogenic lines, and breeding broadbased resistant varieties. In maize and sorghum, resistance to C. partellus, measured in terms of leaf-feeding, deadhearts and stem-tunneling, is polygenic. Polygenic resistance is moderate, but more stable and longer lasting than monogenic or oligogenic resistance. In sorghum, an additive gene effect was important in the inheritance of C. partellus resistance. Efforts are underway in Africa to identify sources of stem borer resistance in cereal crops, but high levels of resistance have not been found. Crop varieties resistant to one stem borer species are not necessarily resistant to others. Therefore, it is important that sources with multiple resistance to stem borers are selected for breeding for dura ble resistance. During the last two decades, several national and international programs have been attempting to incorporate resistance to C. partellus into a good agronomic background of maize and sorghum, and many genotypes are already in national yield trials. Resistant lines/hybrids with good general combining ability have been identi fied. Several hybrid sorghums bred in South Africa exhibited tolerance to stem borer damage, and therefore suffered low yield losses.

Introduction of Biological Control of Chilo partellus in Africa william A. overholt ARC-Plant Protection Research Institute, Pretoria, South Africa Because C. partellus is an exotic stem borer in Africa, there have been several attempts to intro duce exotic parasitoids for its control. The first was

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in East Africa, where eight species of parasitoids, mostly from India, were released from 1968 to 1972 by the Commonwealth Institute of Biological Control. There were no reports of establishment. In South Africa, there were a series of introduc tions of 11 parasitoids from various locations from 1980 to 1993, but again, none established. In 1993, a program was initiated in Kenya to introduce the gregarious larval endoparasitoid, Cotesia flavipes, from Pakistan for biological control of C. partellus. Releases were made in 1993 at three locations in the southern coastal area of Kenya, and the parasitoid was recovered during the season of release from C. partellus and two native stem borers, C. orichalcociliellus and S. calamistis. Cotesia flavipes was released at a fourth site in coastal Kenya during the non-cropping season of 1994 in an area where the vegetation was dominated by a wild grass, Sorghum arundinaceum (Desv.) Stapf. Recoveries in the wild habitat, and in a nearby maize field during the following cropping season, indicated that the parasitoid could sustain its population during the dry season in wild grasses and then colonize maize fields during cropping seasons. Other than recoveries at the wild sorghum site, only one stem borer parasitized by C. flavipes was found in 1994, despite intensive sampling. In 1995 and 1996, a few recoveries were made, but parasitism was low. In 1997, the number of recov eries increased dramatically and parasitism at 30 sites averaged about 6%. Parasitism continued to increase during the next two years with average parasitism of about 13% at 67 sites in 1999. Surveys in other maize growing areas of Kenya in the mid to late 1990s showed that C. flavipes was present in the Eastern Province and in the area bor dering Lake Victoria in western Kenya. In the East ern Province, which borders the Coast Province, C. flavipes was found in low densities in 1996 and then released at three sites in 1997. Parasitism during the season following the releases was about 14%. Para sitism in western Kenya did not increase to the lev els observed in coastal Kenya or the Eastern Province, which may be due to the composition of the stem borer complex. In western Kenya, four

stem borers are common: C. partellus, S. calamistis, B. fusca and E. saccharina. All of these are attractive and acceptable hosts for C. flavipes, but two of them, B. fusca and E. saccharina, are not suitable for its development. The presence of acceptable, but unsuitable, hosts in an area appears to act as a sink which depresses population growth of C. flavipes. The impact of C. flavipes on stem borer populations in coastal Kenya was recently investigated. A host-parasitoid model was used to estimate the stem borer density with and without the parasitoid. A reduction of 1.1 to 1.6 stem borers/ plant, equivalent to a 32–55% decrease in the stem borer density, was shown. As there is not yet any evi dence that the C. flavipes density has reached an equilibrium, it may continue to increase and provide greater suppression of stem borers in the future. In addition to the work in Kenya, C. flavipes was found in northwestern Tanzania in 1995. Based on surveys conducted prior to 1994, and on electrophoretic evidence, it was concluded that the most likely explanation was that C. flavipes moved into Tanzania from Kenya. Likewise, surveys in 1999 and 2000 revealed that C. flavipes had moved into Ethiopia. Releases of C. flavipes have now been made in several other countries including Mozambique, Uganda, Somalia, Malawi, Zambia, Zanzibar and Zimbabwe. Establishment has been confirmed in Mozambique, Uganda, Malawi and Zanzibar. In Uganda, C. flavipes was found to be the most com mon larval parasitoid of stem borers one year after its release.

Biological Control of Chilo sacchariphagus on the Indian Ocean Islands and Africa rÉgis goebel CIRAD-CA, SASEX, Mount Edgecomb, South Africa Over 150 years ago, C. sacchariphagus was intro duced from Java to the Indian Ocean islands of


Mauritius, Réunion and Madagascar in cane cut tings. The biology of this insect is similar to that of other sugarcane borers like Eldana saccharina in Africa or Diatraea saccharalis in the Americas. Damage is caused by the larvae, which penetrate into the stalk internodes where they feed until pupation. In terms of economic losses, damage results in a significant lowering of cane tonnage and, to a lesser extent, in a loss of sugar due to the inversion of saccharose, and to impurities in the juice. On a susceptible variety, the loss in cane weight is estimated to range from 10 to 30 tons per hectare, depending on the growing conditions. This pest has been increasing in some cane producing areas of the island due to the adoption of new varieties, and since 1994 it has been the subject of research to devise an integrated control program. Recent results from field experiments suggest new strategies for minimizing borer attack using predators, parasitoids and varietal resistance.

Biological Control Attempts: Lessons from the Past In the Indian Ocean islands, attempts to control C. sacchariphagus with exotic parasitoids started in the 1940s. However, variable results were obtained. In Mauritius and Réunion, introduc tion and large scale releases of parasitoids, mainly originating from India, did not control C. sacchariphagus, despite the successful estab lishment of species like Trichogramma chilonis Ishii and Cotesia flavipes in sugar cane fields. In Réunion, several attempts at biological control in the 1970s by introducing and releasing tachinid flies also failed to control the pest. Paradoxically, during the years of mass- releases, there were few ecological studies on C. sacchariphagus and its indigenous parasitoids and predators. Moreover, no accurate informa tion was available concerning the parasitization rate of borer eggs by Trichogramma spp. and other egg parasitoids. However, in Réunion,

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Mauritius and Madagascar, natural parasitism of C. sacchariphagus eggs was generally high and ranged from 80 to 90%.

The Imoprtance of Predation by Ants Predation of C. sacchariphagus eggs in Réunion was assessed on sugar cane fields in 1996–1997 by placing fresh eggs on the top leaves through the cane cycle. In two experiments conducted at dif ferent localities, 70–100% of the eggs were attacked by ants when sugar cane was six months old. The level of predation remained very high until the harvesting period (12 months). Trap catches and regular observations in the plots revealed that Pheidole megacephala F. (Hymenoptera: Formici dae) was the major predatory species. However, predation by ants on eggs interfered with a major parasitoid, Trichogramma sp. Obser vations of parasitized eggs in clutches spared by the ants indicated that the ants destroyed the eggs whether they were parasitized or not. Despite this, natural control of the stem borer is a reality in sugar cane fields, and efforts should be focused on conserving natural enemies. This can be done by ceasing certain cultural practices such as burning at harvest, which is totally incompatible with the conservation of predatory insects.

Revised Biological Control with the Use of Trichogramma sp A new biological control program using Trichogramma spp. is currently being implemented in Réunion Island. This program encompasses different steps, from field and lab research to technology trans fer. It includes the choice of suitable species and the selection of strains to improve field performance (higher fecundity, survivorship and more efficient parasitism). One of the most important steps was to identify the Trichogramma strains and set up differ ent studies on biology and population dynamics. Morphological and molecular characterization of

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numerous strains collected form different sites around the island led to the identification of Trichogramma chilonis Ishii. This species, previously named T. australicum, probably originated from Southeast Asia, the native home of C. sacchariphagus. All bio types identified were evaluated for parasitism and the most suitable one will be mass-reared for inunda tive releases in the field. Further studies on popula tion dynamics of T. chilonis are currently being conducted on a susceptible cane variety. The main objective of this study is to investigate the response of T. chilonis to different densities of C. sacchariphagus eggs. This information is essential to determine the ability of T. chilonis to control the borer in the field. The technology for mass rearing of Galleria moths to produce high quality Trichogramma has been transferred to an organization in Réunion, which has many contacts with farmers. The method will be improved for eventual mass- releases. Nevertheless, small scale production of Trichogramma will allow the testing of different factors linked to the methods of release, quantity of Trichogramma per hectare, time of releases, packaging of the parasitoids, and indicators to assess efficacy of the releases. These practical stud ies will be conducted in partnership with farmers. Predation by ants, as mentioned previously, also should be considered in the timing of Trichogramma releases. Therefore, to ensure the highest efficiency, these releases should be conducted dur ing the period when predation is low and sporadic, which is also the egg laying period for C. sacchariphagus. After this period and until maturity of the cane, predation should assure the destruction of most of the borer eggs.

C. sacchapriphagus in Mozambique: a Threat to the South African Sugar Industry In 1998, the presence of C. sacchariphagus in sugar cane in Mozambique was confirmed. Prior to that, its presence was suspected and was mentioned in various unpublished reports as early as the 1970s.

Subsequent to its positive identification, a biologi cal control program has been initiated with the collaboration of the sugar estate management. An ichneumonid pupal parasitoid, Xanthopimpla stemmator, which is a parasitoid of C. sacchariphagus in Sri Lanka, and which had been introduced and established in Mauritius and Réunion, was chosen as the first biocontrol candidate. Methods to detect the presence of C. sacchariphagus in the South African sugar industry are already organized. During the last two years, a series of insect pheromones traps have been in operation in strategic locations along the border of South Africa with Mozambique. However, traps cannot detect the presence of borers in sugar cane stalks transported across the border. It is suspected that the first introduction of this pest into the Indian Ocean islands and Mozambique was made in this way. Presently, the risk of invasion of C. sacchariphagus is high for countries that have a common border with Mozambique (particularly Zimbabwe and Tanza nia). Continued vigilance along the common bor ders will minimize the possibility of the importation of infested sugar cane stalks. Appropriate control measures can be applied immediately should an infestation in sugar cane farms be detected.

References Goebel FR, Fernandez E, Bègue JM, Tibère R, Alauzet C (2000) Predation and varietal resistance as important components of integrated protection of sugarcane stem borer Chilo sacchariphagus (Bojer) (Lepidoptera: Pyra lidae) in Réunion. In: Allsopp PG, Suasa-ard W (eds) Sugarcane pest management in the new millennium. International Society of Sugar Cane Technologists, Brisbane, Australia, pp 51–56 Kfir R, Overholt WA, Khan ZR, Polaszek A (2002) Biology and management of economically important lepi dopteran cereal stem borers in Africa. Annu Rev Ento mol 47:701–731 Polaszek A (1998) African cereal stem borers: economic importance, taxonomy, natural enemies and control. CABI, Wallingford, UK, 530 pp Schulthess F, Cardwell KF, Gounou S (2002) The effect of endophytic Fusarium verticillioides on infestation of two maize varieties by lepidopterous stemborers and coleopteran grain feeders. Phytopathology 92:120–128

Granulovirus

Sétamou M, Schulthess F, Poehling H-M, Borgemeister C (2000) Monitoring and modeling of field infestation and damage by the maize ear borer Mussidia nigrivenella Ragonot (Lepidoptera Pyralidae) in Benin, West Africa. J Econ Entomol 93:650–657 Williams JR, Metcalfe JR, Mungomery RW, Mathes R (1969) Pests of sugar cane. Elsevier Publishing Company, Amsterdam, The Netherlands

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though animals that feed on grass seeds can be said to be both granivorous and graminivorous.  Food Habits of Insects  Phytophagy  Herbivory

Granular Formulation Graminivory Eating or feeding on grasses (the plant family Graminae or Poaceae). Arthropods that feed on grasses are said to be graminivorous or gramini vores. Grasses are sometimes said not to be par ticularly well defended biochemically against insect feeding, depending instead on silicification, lignification, trichomes, and a basal meristem for defense against herbivory. However, secondary plant compounds are also abundant in grasses.

A dry formulation of pesticides that is substan tially larger and heavier than dust, and applied with a granule applicator, not a duster.

Granule The individual particles that are used in a granular formulation of pesticide.

Granulocyte References Redak RA (1987) Forage quality: secondary chemistry of grasses. In: Capinera JL (ed) Integrated pest manage ment on rangeland. A shortgrass prairie perspective. Westview Press, Boulder, CO, pp 38–55 Rittenhouse LR, Roath LR (1987) Forage quality: primary chemistry of grasses. In: Capinera JL (ed) Integrated pest management on rangeland. A shortgrass prairie perspective. Westview Press, Boulder, CO, pp 25–37

Granary Weevil, Sitophilus granarius (Linnaeus) (Coleoptera: Curculionidae) This is an important pest of Stored grain.  Stored Grain and Flour Insects

Granivory Seed feeding. Such arthropods are said to be granivorous or granivores. This is distinct from graminivorous (graminivores), or grass feeding,

A type of hemocyte that is important in encapsu lation of foreign objects found in the hemolymph.  Hemocytes of Insects: their Morphology and Function

Granulosis A disease of certain insects caused by granulosis virus (granulovirus) and characterized by the pres ence of minute granular inclusions in infected cells.  Granulovirus

Granulovirus kia rashidan1, claude guertin2, jean cabana2 1 INRS-Institut Armand-Frappier (INRS-IAF), Laval, Qc, Canada 2 AFA Environment Inc., Montreal, PQ, Canada There are an increasing number of problems associated with the use of chemical pesticides, including emergence of resistant insects,

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e limination of non-target insects, and environ mental contamination. Thus, the need for alternative biological insecticides that are costeffective and environmentally safe is greater than ever. As a result, interest in microbial insecticides is increasing. Microbiological pathogens include various species of bacteria, fungi, nematodes, and viruses. The best-known example of a micro biological insecticide, which is used in large scale against agriculture and forest pests, is the bacte rium, Bacillus thuringiensis (commercially known as Bt). Viruses comprise another important class of insect pathogens that are being considered as good alternative biological insecticides due to their specificity for insect hosts. At least eight families of insect viruses are known, but the viruses most commonly used as viral bioinsecticides are those from Baculoviridae family. Baculoviruses are a group of viruses that are specific to arthropods. Unlike other insect viruses, no morphologically similar counterpart to bacu loviruses has been detected in vertebrates. Baculo viruses are characterized by the presence of a large protein matrix or occlusion body which encase the viral particles. Baculoviruses are classified in two genera: the nucleopolyhedroviruses (NPVs), and the granuloviruses (GVs). Safety testing of non-target organisms including mammals, fish, and birds has shown baculoviruses to have a very limited host range and to be safe to non-target organisms. Of the insect viruses, only baculovi ruses have been recommended for field use. Although baculoviruses have been isolated from different orders of insects, they have been used mostly to control pest species from the orders Lepidoptera, Hymenoptera, and Coleoptera. Overall, the most successful examples of baculovirus usage can be found in forestry. For instance, in the U.S.A. and Canada, baculoviruses have been used successfully in large-scale against the Douglas fir tussock moth (Orgyia pseudosugata), pine sawfly (Neodiprion sertifer), red headed sawfly (Neodiprion lecontei) and gypsy moth (Lymantria dispar).

Granulovirus Infection (Granulosis) Granulovirus (GV) infection, known as granulo sis, was first detected by Paillot, in 1926, in the larvae of Pieris brassicae (the large white butter fly). At that time he called this disease pseudogras serie. Later he described a similar disease in Agrotis segetum (a cutworm). In 1947, Steinhaus rediscov ered the disease in Peridroma saucia (variegated cutworm), and he called the disease granulosis because he observed some tiny granules in affected tissues when observed with light microscopy. In 1948, a similar disease in Choristoneura muriana (pine shoot roller) was described by Bergold. Bergold was the first to demonstrate the viral nature of granulosis with electron microscopy; he described the virus as rod-shaped particles. Infection begins when larvae ingest the occlusion body. Several days after infection, lar vae begin to display unusual characteristics such as sluggishness, loss of appetite, followed by color change from the light brown to pink or white. For example, Choristoneura fumiferana (spruce budworm) and Pieris rapae larvae become pink, and Cydia pomonella (codling moth) larvae become white in very late stages of infection. The organ of the insect that is princi pally affected is the fat body, but virus also repli cates in other tissues such as the epidermis, hemocytes, tracheal matrix cells, and Malpighian tubules. The high pathogenicity of GVs toward dif ferent insect pests of agricultural crops and for ests make this group of viruses a very attractive candidate to be used as biological insecticides. Since the 1950s, different GVs have been used as a biological insecticide in different parts of the world. One of the first countries to use GVs against Hadena sordida and Trichoplusia ni was the former Soviet Union. In Canada, GVs are mostly used in forestry against spruce budworm (C. fumiferana), and fir budworm (C. muriana). In the U.S.A., GVs have been used against Cydia pomonella (codling moth) and Plodia interpunctella (Indian meal moth).

Granulovirus

General Aspects of Granulovirus GVs are rod-shaped enveloped virions that con tain one molecule of circular (super coiled) double stranded DNA. Nucleocapsids, which consist of proteinaceous capsid and DNA-protein core, are relatively large, 200–450 nm long and 30–100 nm in diameter. Nucleocapsids are cylindrical struc tures in which subunits of capsid are assembled in rings stacked one on top of another. Each turn of the helix consist of 12 copies of the capsid protein. The two ends of the nucleocapsid are different in shape and have been described as “nipple and claw.” One end (nipple end) has the appearance of stacked rings of decreasing diameter. GVs produce two different phenotypes, termed budded virions and occlusion-derived virions. Dis tinct viral structures are visible in thin sections of infected tissue. These two phenotypes are produced at different times and locations in the infected lar vae. Budded virions are produced in the late phase of the infection cycle, when nucleocapsids bud from the surface of infected cells. Occlusion-de rived virions, on the other hand, are produced very late in infection; they become enveloped and sub sequently occluded within an occlusion body within the infected cell. Enveloped nucleocapsids are individually encased in occlusion bodies. Occlusion body is a protein matrix, termed granu lin, which protect the viral DNA against the UV radiation of sunlight. Each phenotype has different functional roles. Occlusion-derived virion is the phenotype that is released in the environment after the death of the infected insect, it has a great infec tious potential toward other susceptible insects.

Molecular Biology of Granulovirus Genome Granuloviruses have large genomes (80–180 kbp) that have the potential to encode about 100 genes. On the contrary, other viruses with big genomes like poxvirus that carry an extensive array of enzyme

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which are essential for early gene transcription, granuloviruses (like other baculoviruses) carry no virion-associated proteins that are essential for virus early gene transcription on their genome. The genome of granuloviruses is composed almost entirely of unique DNA sequence, though several small repeated sequences known as homologous regions are known in the DNA. The homologous regions have roles as enhancers for early genes, and also as origin of DNA replication. The activation property of an early gene known as ie-1 is enhanced when the genes are linked to homologous region sequences. Open reading frames (ORFs) are located on either strand of the DNA. Most ORFs are separated by 2–200 bps of DNA rich in A + T. There are also some overlapping ORFs in granulovirus genome, usually termination codon UAA overlaps with the primary polyadenylation signal AAUAAA. Some promoters are located within the neighboring ORFs. Frequently, transcripts of one gene initiate within, into, or through neighboring ORFs. Beside partial clustering of genes which have assigned roles in early gene regulation (e.g., ie-1, ie-2, and pe-38), genes in the genome of granulovirus, like other baculoviruses, do not appear to be clustered. Genes encoding structural proteins are distributed throughout the genome with no obvious pattern to the location.

Structural Proteins Granulin is the major protein in SDS- polyacrylamide gel electrophoresis (SDS-PAGE). Studies on alkaline solubilized granulin of differ ent GVs show that matrix protein of GVs has a molecular weight equal to approximately 30 kDa. Analysis of the nucleotide and amino acid compo sition of granulin in different GVs show a high degree of similarity. Amino acid sequence analysis of granulin in different granuloviruses showed conserved amino acid residues, which is likely due to “evolutionary memory,” which maintains the secondary structure of granulin in all GVs.

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The presence of 12–20 proteins has been shown in enveloped nucleocapsids of different GVs by SDS-PAGE analysis. Molecular weight of these polypeptides ranges from 12 to 160 kDa.

Cycle of GV Infection in Susceptible Insects The infection cycle of granulovirus has two dis tinct phases: primary and secondary cycle.

Primary Cycle of Infection The primary phase of infection is initiated by inges tion of virus by larvae, followed by dissolution of granulin (matrix protein of occlusion body) in the midgut of the insect, and liberation of the envel oped nucleocapsids. Granulin dissolved due to the alkaline environment of the insect’ s midgut. Occlu sion-derived virion infectivity is boosted by a pro tein present in occlusion body, termed Enhancin, which is a proteolytic compound with structural and functional characteristics of metaloproteases. Enhancin seems to have a direct effect on degrada tion of the peritrophic membrane in insect midgut. Enveloped nucleocapsids attach to the surface of microvilli of columnar cells, and nucleocapsids enter the cytoplasm of cells following fusion of the viral envelope with plasma membrane. Nucleo capsids move toward the nucleus of the cell by polymerizing the actin filaments and release their DNA into the nucleus. Replication and transcription of viral DNA take place in the nucleus of infected cells, and progeny nucleocapsids are formed in the nucleus of columnar cells. Nucleocapsids acquire their envelope by budding through the modified plasma membrane. This modification is due to the trans portation of virus-made proteins into the plasma membrane of the infected cells. The primary phase of infection terminates when these enveloped nucleocapsids, known as budded virion pheno type, are released from infected cells. Budded

v irions are potentially infectious for tissues within the hemocoel. The mechanism by which the bud ded virion traverses the basal lamina of the midgut epithelium is not completely known. Some researchers suggest this possibility that budded virions may directly traverse the basal lamina of the midgut epithelium during budding. There is also another possibility that budded virions may use the tracheal system as a conduit to cross the basal lamina of the midgut epithelium.

Secondary Cycle of Infection The secondary phase of granulovirus infection is different from the primary phase in several ways: (i) budded virions enter these cells by a receptormediated endocytosis in contrast to the occlusionderived virion, which enter by fusion, (ii) more cells are infected, (iii) the yield of progeny virus per cell is much higher, (iv) progeny nucleocapsid acquire envelope inside the cell (instead of budding through the plasma membrane), (v) enveloped nucleocapsids encased inside the proteinaceous matrix, and (vi) the occluded progeny (termed occlusion-derived virion phenotype)are released upon cell lysis. Viral entry by endocytosis is a process that usually consist of six steps: (i) virion attachment to a receptor on the surface of host cell, (ii) invagina tion of host plasma membrane in the viral attach ment site, (iii) formation of a vesicle containing the enveloped virion (endosom), (iv) acidification of the endosom, (v) fusion of the viral envelope and endosomal membrane, and (vi) release of the nucleocapsid into the cytoplasm. Following the release of nucleocapsid into the cytoplasm, they are transported toward the nucleus. Studies that concentrate on the mecha nism of the transportation in NPVs showed that actin cables might play a major role in this move ment. These studies also suggest that a structural protein in the nucleocapsid triggers the polymer ization of actin cables. After nucleocapsid reach the nucleus, viral DNA is directly released into the

Granulovirus

nucleus through the nuclear pores. It seems that a phosporylated capsid protein (P78/83), which is localized at one end of the nucleocapsid, plays a role in the interaction of nucleocapsid and nuclear pores. The mechanism of uncoating of DNA in another baculovirus genus, NPVs, is different than GVs. Nucleocapsids of NPVs enter host cell nuclei and uncoat within the nucleus. Upon uncoating of granulovirus DNA in the nucleus, early genes are transcribed by a host RNA polymerase. Early viral products are mostly regulatory proteins that activate transcription from other early genes. The transition from early to late phase is characterized by inhibition of host transcription and replication of viral DNA. Replication of viral DNA seems to be a crucial step prior to late phase transcription. Late genes are transcribed by a viral RNA polymerase. At least 18 baculovirus genes have been shown to control the late gene expression; these genes are identified as late expression factors genes (lef genes). All struc tural proteins are expressed in late and very late gene expression. Nucleocapsid assembly begins after synthesis of late proteins. Electron microscopy studies demonstrate that initially a virogenic stroma appears within nuclei, and empty capsids assemble within this stroma. These capsids then fill with DNA. A basic DNA binding protein in the capsid (P7/12) may play a role in packaging of viral DNA. This protein has similarity to cellular protamines, the basic proteins that substitute for histones in the packaging of DNA within the sperm of many species. Both proteins (i) are rich in arginine resi dues which lead to a high basic charge, (ii) have the ability bind zinc (Zn+2), and (iii) are a substrate for kinase activity. After the process of packaging viral DNA, nucleocapsids are ready for envelopment fol lowed by occlusion. The mechanism for envelop ment is not known, but some researchers suggest that budding through the nuclear membrane fragments is a possible way for envelopment. The very late phase of infection starts by hyper- expression of very late genes such as granulin

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(the occlusion body protein). Granulin crystal lizes around the enveloped nucleocapsids and encases the virions. Following the occlusion pro cess, an envelope-like structure (calyx) covers the occlusion body. At the final stage of granulovirus infection, cells become packed with occluded virions that cause cell lysis and liberation of virus into the hemocoelum followed by death of the insect.

Use of Baculovirus against Lepidoptera Baculoviruses have been used to control different lepidopterous pests in agriculture and forestry. Historically, the first attempt to use viruses as a bio insecticide date back to 1892. In this year, a baculo virus was used to control Lymantria monacha population in pine forests in Germany. The United States was the first country in North America to use a baculovirus against Lymantria dispar. There is no record of large scale use of bacu loviruses in agriculture in United States before the late 1940s. In this year, aerial application of NPV against C. eurytheme (alfalfa caterpillar) were attempted in California. The use of Helicoverpa zea NPV in the 1970s showed promising results in soybean and maize agriculture. Between 1975 and 1980, over one million hectares were treated by HzNPV. Introduction of synthetic pyrethroids in the early 1980s decrease the use of HzNPV, but the emergence of a worldwide resistance against pyrethroids during the 1990s promoted the use of the HzNPV. In 1996, HzNPVwere again used in large scale in the cotton industry in the United States. Currently, China is one of the countries that use HzNPV and H. armigera NPV in cotton indus try. Annually, 100,000 ha of cotton fields in China is treated by HaNPV. Thailand and Vietnam are two other countries, among others, that use HaNPV on a large scale. One of the best examples of using baculovirus in fruit crops is the use of a granulovirus against Cydia pomonella (codling moth: a pest of apples,

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pears and walnuts). Cydia pomonella granulovirus (CpGV) demonstrates a high pathogenicity against the larva and kills the insect very quickly. Field tests with CpGV in North America demonstrated that CpGV is a highly virulent and selective con trol agent against codling moth. CpGV is currently in use in different European countries. France, Switzerland, Germany, and Russia are the major consumers. Records of using baculoviruses in forestry show that the following insects were the most important Lepidopera that were subjected to applications of baculoviruses: C. fumiferana (spruce budworm), C. occidentalis (western spruce budworm), C. pinus (jackpine budworm), L. dispar (gypsy moth) and O. pseudotsugata (Douglasfir tussock moth). A NPV for O. pseudotsugata was registered and used in United States in 1976. This virus has been used during the last three decades in different parts of the United States and Canada. Lymantria dispar NPV is another baculovirus that has been used widely since its registration in 1978. The first baculovirus used against spruce bud worm was CfMNPV. The most important problem related to CfMNPV is its low pathogenicity. The other baculovirus that has a great potential to be used as a microbiological insecticide against spruce budworm is C. fumiferana granulovirus (ChfuGV).

A Case Study: Use of Choristoneura fumiferana Granulovirus (ChfuGV) in Canada In eastern North America, spruce budworm is con sidered the most destructive insect of coniferous trees. The spruce budworm is a huge economic threat to vast forest areas (60 million ha) in Canada and eastern United States. The Maritime Provinces (New Brunswick, Nova Scotia, Newfoundland), Quebec, Ontario, and the Great Lake states are the areas that are affected by spruce budworm outbreaks most extensively. Spruce budworm larvae feed on a number

of conifers, but balsam fir (Abies balsamea [L.] Mill.), and white spruce (Picea glauca [Moench] Voss) are the major hosts in eastern North America. Species occasionally attacked include black spruce (Picea mariana [Mill.] B.S.P.), red spruce (Picea rubens Sarg.), eastern hemlock (Tsuga canadensis [L.] Carr.), tamarack (Larixlaricina [Du Roi] K. Koch), and white pine (Pinus strobus L.). In Quebec, Canada the outbreak of C. fumiferana usually affects huge forest areas. For example, the infested area in 1999 was estimated more than 23,000 hectares. This figure was twice as large as the infested area in 1998. Defoliation, inhibition of seed production, cone mortality, root mortality and tree mortality are the most important impacts of spruce budworm on trees. Defoliation caused by spruce budworm decreases the growth rates of trees; this decline can last several years. When out breaks occur, the affected trees usually die after three to four years of heavy defoliation, and most of the trees die between six and ten years after the first attack. Even when the spruce budworm popu lation returns to its endemic level, the damaged trees continue to die. Chemical insecticides were the most com mon method of protecting spruce-fir forests from spruce budworm from 1927 up to the 1970s. DDT and Phosphophamidon were used mostly during the period from 1944 to 1970. In the 1970s and 1980s organophosphates and carbamates replaced DDT. Most of these compounds are toxic to humans and other warm-blooded animals. The concern about finding an alternative for chemicals started during the 1960s and among the candi dates were biological insecticides. Also, as insects continue to gain resistance to chemical pesticides, industrial interest in commercial development of biological pesticides increases. Natural predators, parasites, competitors and pathogenic microorganisms like fungi, bacteria and viruses have been used as biological agents. In eastern Canada Bacillus thuringiensis var. kurstaki (Btk) is used in insect control programs against spruce budworm. No major resistance against Btk in natural population of spruce budworm has been

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reported. However, laboratory results demon strated that several insect species are able to develop resistance against the Btk toxin. The risk of appearance of resistance against Btk obligates the researchers to quest for new alternatives. ChfuGV has been isolated from infected spruce budworm in several part of eastern Can ada. This virus is considered a very attractive and powerful candidate to be used instead of, or along with, Btk in the case of the emergence of resistant spruce budworm larvae. Laboratory bioassays with ChfuGV demon strated its high pathogenicity for spruce budworm population (LD50 = 5.72 × 105 viruses/larvae). The development and implementation of ChfuGV as a microbial insecticide were carried out during a pilot project on 100 ha of forests in Quebec, Canada. The results of these field experiments demonstrated that two weeks after treatment with ChfuGV a considerable reduction (40%) of defoli ation was observed in treated areas as compared to control areas. Also, the number of C. fumiferana larvae was reduced by over 35% in treated areas. One of the most interesting results, from an eco nomical perspective, is that when ChfuGV was used in a lower rate volume applied per ha, the same level of protection was observed.

Production of Granulovirus-based Insecticides Currently, most granuloviruses are produced in vivo. The reason is due either to the absence of cell lines for some granuloviruses, or low yield of virus production for the others. One of the most important drawbacks concerning the in vitro production is that the viruses often lose infectiv ity after several passages through cell culture. The most important aspect of the virus production process is: (i) choice of the host. (ii) rearing con ditions. (iii) virus purification. (iv) formulation. Usually, a natural virus host is the best choice in virus production, but in the cases that the natu ral host is not suitable for laboratory rearing, and

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alternative hosts must be considered. The following cases are examples of unsuitable hosts: (i) when the natural host has a special dietary requirement, or (ii) when long obligatory diapause is required. Temperature and humidity are the most important aspects in insect rearing. The other key factor for in vivo virus production is the number of larvae per each diet container and the size of con tainer. The use of large containers is not recom mended for species with a cannibalistic nature. Formulation of granulovirus-based insecti cides is a very important part in production. For large-scale applications, different aspects such as storage stability and UV protection must be con sidered in order to have a stable and high quality product. The formulation also must provide good residual activity in field. The formulation must not contain any additive with negative effects on virus activity.

Standardization and Quantification of Granulovirus-based Insecticides One of the most important requirements for the production and use of GVs is the availability of bioassays. With bioassays, GV producers can deter mine the potency and virulence of an industrial product or preparation. On the other hand, bioas says can be also used: (i) to determine the biologi cal activity of GVs for different insect species, (ii) to determine the relative biological activity of several viruses against one or more insect hosts. Bioassays ensure the activity of the product prior to field use. In each bioassay there are some facts that should be respected to ensure the quality of the bioassay: (i) the purity of the virus prepara tion should be established by electron microscopy or other analytical procedures, (ii) presence of con taminating micro organisms such as bacteria and mycets should be checked, (iii) the assay must be reproducible for the same strain of insect species under similar conditions. Different methods of bioassays, such as bioassays by injection, bioassay

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Grape Berry Moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae)

by contaminated leaf disks, and finally bioassays by contaminated artificial diet have been suggested by different workers. Injection methods have been used for estab lishment of activity of non-occluded virus obtained from alkaline-dissolved granules (granule: a com plete granuloviral particle contain nucleocapsid, envelope and occlusion body). This method is very tedious and time consuming, but the primary advantages of this type of assay are (i) the amount of inoculums per insect is known, and (ii) the time of the beginning of infection is known. Another time consuming method of bioassay is using leaf disks contaminated by with known quantities of GV preparation. Bioassays using con taminated artificial diets are the most commonly used assays for many insect viruses including GVs. In this method, known quantities of GVs are incorporated into, or layered on, the surface of artificial diets, which allows the evaluation of the LC50. There are two very important advantages related to this method: (i) early stages of insect larvae, which are generally the most susceptible to viral infection, can be used in large numbers, (ii) insect handling is minimized since the stay in the same container throughout the bioassay. The disadvantage of this method is that the dose of the virus ingested by each insect is not known. There are always problems that could arise in different types of bioassays, but these problems can be avoided if certain precautions are taken.

Methods of Application of Granuloviruss-based Insecticides An effective application should distribute virus to the insect’ s feeding sites in a way that the probability of acquiring a lethal dose of virus is maximized. Granuloviruses, like most other bac uloviruses, are applied by spraying the viral product to the target site. Ground application is mostly used for agricultural crops, but aerial application is the common method in forestry. There also are other application techniques that

have been demonstrated, such as release of infected insects, though these have some limitations.

The Future of Granulovirus Baculoviruses and among them granulovirus, can be considered to be major elements in biological control programs in the next 10 years. On the other hand, considering the fact that a great deal of effort has been directed toward the develop ment of recombinant baculoviruses, it also is probable that recombinant viral insecticides will be used on a large scale against insects pests of for ests and crops in near future. The most important issue concerning the use of genetically modified baculoviruses is the safety issue. Therefore, to be safe, it is important to prepare comprehensive risk assessment protocols for genetically modified baculoviruses.

References Tanada Y, Hess RT (1991) Baculoviridae, granulosis viruses. In: Adams JR, Bonami JR (eds) Atlas of invertebrate viruses. CRC Press, Inc., Boca Raton, FL, pp 227–257 Summers MD (1977) Baculoviruses. In: Maramorosch K (ed) The atlas of insect and plant viruses. Academic Press, New York, NY, pp 3–28 Bonning BC, Hammock BD (1996) Development of recombi nant baculoviruses for insect control. Annu Rev Entomol 41:191–210 Cory JS, Hails RS (1997) The ecology and biosafety of baculo viruses. Curr Opin Biotechnol 8:323–327 Miller LK (1996) Insect viruses. In: Fields BN (eds) Fields virology, vol 1, 3rd edn. Lippincott-Raven Publishers New York, NY, pp 533–585

Grape Berry Moth, Endopiza viteana Clemens (Lepidoptera: Tortricidae) Endopiza viteana is an important grape pest.  Small Fruit Pests and their Management

Grape Phylloxera, Daktulosphaira vitifoliae (Fitch) (Hemiptera: Aphidoidea: Phylloxeridae)

Grape Leafhopper, Erythroneura sp. (Hemiptera: Cicadellidae) Several species of Erythroneura are pests of grapes.  Small Fruit Pests and their Management

Grape Phylloxera, Daktulosphaira vitifoliae (Fitch) (Hemiptera: Aphidoidea: Phylloxeridae) doug downie Rhodes University, Grahamstown, South Africa Grape phylloxera is a primitive aphid that feeds and develops on grapevines (Vitis species). It is notorious for the damage it caused to viticulture first in France, then globally as it was introduced and spread into vineyards in nearly every grapegrowing region of the world in the middle to latter part of the nineteenth century. Its native range is North America east of the Rocky Mountains, the southwestern USA, and well into Mexico and Cen tral America to as far south as Venezuela. Grape phylloxera has had a checkered nomenclatural his tory, and the genus names Pemphigus, Rhizaphis, Peritymbia, Viteus, and Daktulosphaira as well as Phylloxera have been applied to it. For many years, Phylloxera was the most commonly applied name so the common name and Latin genus name were one and the same. This name was subsiding from use after 1952, however, and Russell cleared up the nomenclatural mess more than thirty years ago. However, there is no phylogenetic hypothesis for the Phylloxeridae so nothing is known about the relationship of D. vitifoliae to the approximately 41 described species of Phylloxera and it may still turn out, once such a hypothesis is in hand, that erecting a new genus for grape phylloxera was unjustified. There is an unfortunate prevalence in both entomological and viticultural circles to use the name phylloxera as the common name. Because a large number of other species in the family have this as their Latin name, it is desirable to specify “grape” phylloxera when discussing this insect.

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Life Cycle and Biology Grape phylloxera is a gall forming insect (as are the majority of species in the Phylloxeridae) causing galls on leaves and young roots on native vines and on hardened roots of susceptible culti vars. It has been stated that grape phylloxera may form galls on vine tendrils, but this is not true under natural conditions. Its host range appears to be restricted to about six to eight (depending on taxonomic concepts) of the some 20 or so Vitis species in the Americas and a number of cultivars, most notably the wine grape V. vinifera L. The distribution of grape phylloxera in Mexico and Central America is uncertain at this time. On leaves, pouch galls are formed that completely enclose the gall-former and her eggs. Galls on young roots (typically called nodosities) have a characteristic hook shape as cells distal to the insect feeding site become hypertrophied. The gall-former may be partially hidden in the elbow of the hook, but is otherwise exposed. Galls on hardened roots (tuberosities) appear as bumps on the surface of the root, with the gall-former and her eggs exposed on the surface. There is currently no evidence to suggest that the mecha nism of gall induction differs on the three differ ent plant organs or tissue types attacked; the different morphology is due to the different sub strates galled (i.e., a pouch gall cannot form on a cylindrical and hardened root). The life cycle differs in the native range and under most vineyard conditions and these will be discussed separately:

Native Range As with the majority of Aphidoidea, grape phyl loxera is a cyclic parthenogen in its native range. That is, one to multiple generations pass by apomictic parthenogenesis followed by a single generation of sexual reproduction each year. Sexually produced eggs are cold-resistant and are the overwintering stage. Individuals hatching

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Grape Phylloxera, Daktulosphaira vitifoliae (Fitch) (Hemiptera: Aphidoidea: Phylloxeridae)

in the spring from these zygotic eggs are called fundatrices. As first instar crawlers, fundatrices initiate galls on newly forming leaves in which they will mature in 2–3 weeks, laying upwards of 300 eggs as adults. Galls can only form on the newly expanding leaves. Fundatrices and all sub sequent gall mothers (gallicolae) generally do not leave their gall after gall initiation. As eggs hatch, the crawlers leave the galls and move up the shoots to newly forming leaves where they in turn make their galls. A variable number of gen erations may pass this way. New leaf growth tends to slow or cease as summer progresses, meaning there is no longer any leaf resource for grape phylloxera. In the southwestern USA, and perhaps Mexico and Central America, it appears that this is when sexual forms (sexuales) are induced and overwintering eggs produced, end ing the life cycle. There is evidence that gallico lae will sometimes secondarily occupy already-formed galls. There are no winged forms (alatae). In eastern North America the life cycle is prolonged by crawlers moving to the roots where they (called radicicolae) form galls on new, unhardened rootlets. Analogous to host alternation in aphids, it is here that alatae are produced that ascend into the canopy to lay a small number of male and female eggs. Induc tion of alatae may be influenced by density dependence, deterioration of the resource, or temperature. The neotenic sexual morphs have no mouthparts and live only a few days. Follow ing mating these females lay a single zygotic egg each. It is often said that the overwintering eggs are laid in crevices in the bark on the trunks of vines but there have been too few observa tions to convincingly say how these eggs are distributed.

Vineyards Vineyards in the eastern part of North America appear to be attacked by the local populations of grape phylloxera, and the life cycle on these

cultivated vines does not differ. Elsewhere, except in cases where rootstocks are allowed to sucker or grow from cut down vines, the life cycle has been modified by elimination of the leaf galling phase, and with it production of sexual forms. Overwin tering occurs as first or second instars. There is now good evidence that most populations of grape phylloxera, in vineyards of Australia and California at least, reproduce only asexually. Alate individuals are common, however, and have been observed at various times of the year. Apparently they are either infertile, their eggs are inviable, or sexuales do not survive to adulthood. Both nodos ities and tuberosities are formed, with some culti vars resistant to tuberosity formation but susceptible to nodosity formation. Dispersal of grape phylloxera occurs by flight of alatae and by blowing of crawlers by wind, and may also occur by windblown or water-carried galled leaves that harbor eggs or live individuals. In vineyards, all stages could be moved by agricul tural equipment and activities.

Damage and Management There are no data directly relevant to how dam aging grape phylloxera is to wild grapevines and what effect on fitness, if any, is incurred. It has commonly been assumed that these vines are tol erant, but this is not likely to be strictly true because extensive galling must divert resources away from seed production. More study of this plant-insect interaction on wild grapevines is needed and would aid in understanding the evo lution of resistance in grapevines. In vineyards, damage is most severe when tuberosities are formed, vines being able to with stand the damage from nodosity formation. Tuberosities tend to occlude the vascular system, and a heavy infestation high up in the root system will effectively remove a substantial pro portion of the translocation to and from the root system. This effect is exacerbated significantly by entrance of fungal pathogens through the

Grape Root Borer, Vitacea polistiformes (Harris) (Lepidoptera: Sesiidae)

cracked surface of the galled portion of the roots, resulting in necrosis and loss of root area. Ulti mately, attacked vines die. Management tactics have varied over the years and have included spraying of copper bisulphide in the early days to more modern insecticides (especially against leaf galling forms), and even flooding vineyards. The cryptic and protected habi tat of root galling individuals makes use of conven tional insecticides problematic.Systemic insecticides have found some use, but have not been widely applied. The use of natural enemies has not been thoroughly explored. Because fungal pathogens play an important role in damage, efforts are under way to control these. Finally, grape phylloxera has been effectively excluded from some wine regions in Australia by enforcing strict quarantine measures. The only effective and durable management tactic has been the development and use of host plant resistance. Resistant cultivars have been developed directly from vine collections from the native range or, more often, from breeding pro grams, often leading to complex hybrids. The dom inant Vitis species that have been used in these breeding programs have been V. riparia, V. rupestris, and V. berlandieri. Once developed, these cultivars are used as rootstocks for scions of the wine grape, V. vinifera L. The mechanisms of resistance are not well understood but there is evidence for antixeno sis (insect avoidance), antibiosis (death or poor development of the insect) as well as tolerance (plant can suffer large numbers of herbivores with out succumbing). Phenolic compounds may play a role in inhibiting development, and a hardened periderm beneath the feeding site has been observed, which would inhibit gall formation and isolate the insect from its nourishment. Host plant resistance has been an effective strategy for managing grape phylloxera since it was introduced in the late 1800s, with only a few examples of failure. A notable example of a fail ure of what was previously considered to be a resistant rootstock is that of the rootstock AXR#1 in California in the 1980s. This rootstock was widely planted in California vineyards in the

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1960s and 1970s but began declining under grape phylloxera attack in the 1980s, leading to large scale replanting to other rootstocks and massive economic outlays. It is likely, however, that this rootstock was never sufficiently resis tant to grape phylloxera under California condi tions, and the failure of resistance in this case may be more a failure of implementation than a failure of resistance.

References Corrie AM, Crozier RH, Van Heeswijck R, Hoffmann AA (2002) Clonal reproduction and population genetic structure of grape phylloxera, Daktulosphaira vitifoliae in Australia. Heredity 88:203–211 Downie DA (2002) Locating the sources of an invasive pest using a mtDNA gene genealogy. Mol Ecol 11:2013–2026 Downie DA, Granett J, Fisher JR (2000) Distribution and abundance of leaf galling grape phylloxera and Vitis species in the central and eastern United States. Environ Entomol 29:979–986 Granett J, Walker MA, Kocsis L, Omer AD (2001) Biology and management of grape phylloxera. Annu Rev Entomol 46:387–412 Moore MO (1991) Classification and systematics of eastern North American Vitis north of Mexico. Sida 14:339–367 Lin H, Walker MA, Hu R, Granett J (2006) New simple sequence repeat loci for the study of grape phylloxera (Daktulosphaira vitifoliae) genetics and host adaptation. Am J Enol Vitic 57:33–40 Omer AD, Granett J, De Benedictis JA, Walker MA (1995) Effects of fungal root infections on the vigor of grape vines infested by root-feeding grape phylloxera. Vitis 34:165–170 Russell L (1974) Daktulosphaira vitifoliae, the correct name for the grape phylloxeran (Hemiptera: Homoptera: Phylloxeridae). J Wash Acad Sci 64:303–308

Grape Root Borer, Vitacea polistiformes (Harris) (Lepidoptera: Sesiidae) Vitacea polistiformes is one of the most important grape pests in eastern North America.  Small Fruit Pests and their Management

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Grapevine Leafhopper Complex (Hemiptera: Cicadellidae) in Cyprus

Grapevine Leafhopper Complex (Hemiptera: Cicadellidae) in Cyprus george m. orphanides Agricultural Research Institute, Nicosia, Cyprus Various species of leafhoppers attack grapevines throughout the world. In Cyprus, the grapevine leafhopper complex consists of three species that have been identified by C.A.B. International Institute of Entomology (London) as Zygina rhamni (Ferrari), Jacobiasca lybica (Bergevin & Zanon), and Asymmetrasca decedens (Paoli). Assessment of population density through D-vac samples and insect counts directly on the plants showed an overall prevalence of Zygina over the other two. Zygina and Jacobiasca prevailed in areas with drier microclimatic conditions (Avdhimou and Pakhna) where the overall rele vant populations were 52% and 45%, respec tively. At Phassouri, though, a much less drier area, 45% of the leafhopper population was Asymmetrasca. This pest prevailed from April to early August and then its populations dropped significantly as it moved to other host-plants. Minor differences have so far been found in the within-plant distribution of the two principal species. At low population levels, these cicadel lids had the tendency to live on different leaves, but at higher populations they could also be found on a same leaf, almost exclusively on the lower leaf surface. More insects were found on the basal than on the apical half of the vines. The adult females lay their eggs singly in the epidermal tissue of the leaves and appear like tiny bean-shaped blisters. The young leafhoppers that emerge (nymphs), and the adults, are found almost exclusively on the lower leaf surface. They feed by sucking out the sap from the leaf cells or veins causing discoloration, deformation and in cases of heavy infestation, drying and shedding of leaves. Although Zygina is more widespread, it is not so harmful to the plants because it sucks the sap from the leaf cells, causing only leaf discoloration. The

other two leafhopper species are more harmful because they suck the sap from the leaf veins, caus ing leaf deformation and drying. Yellow sticky trap catches showed increased populations of Zygina only from the end of July to the end of November, while those of Jacobiasca followed the same trend with about a three-week delay. Considering this population behavior, and the insect count on the grapevine leaves that were much lower than those reported as economically significant elsewhere, the pest status of the leafhopper complex was questionable. Adults of Z. rhamni overwinter on Rubus sp. and Sarcopoterium spinosum (L.) Spach. They present a reddish pigmentation on their head and front wings, which in grapevines with poor growth starts appearing gradually from midAugust onwards, while in those with rich and tender growth, 15 days later. This gradual change of adult pigmentation is completed generally by mid-November. Adult migration to the winter quarters may start as early as September with a gradual infestation of Rubus, which is an ever green bush. Sarcopoterium is available for infes tation from around mid-November. This cicadellid develops (Fig. 31) one generation on these plants in early spring, and then it moves to grapevines where it stays for as long as there are green leaves, developing a maximum of 4 more generations. Jacobiasca lybica overwinters as adult on Rubus, and then it develops only on grapevines, completing a maximum of six generations per year. Asymmetrasca decedens overwinters on cit rus and on several weeds without interrupting its development, although it slows down because of the lower temperatures. In spring it moves to sev eral vegetables and to grapevines where it prevails until the end of July. It then develops on various vegetables until winter, completing a maximum of eight generations per year. Aphelopus orphanidesi Olmi (Hymenoptera Dryinidae), a new species, was the only parasite of Z. rhamni found so far in Cyprus. Adult females oviposit in the body of the leafhopper nymphs

Grass

a

b

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becomes shining black. It then becomes white after the larva abandons it. On adults reared in the laboratory at 25°C and in the field during the summer, the sac remains white throughout the entire larval development. Upon completion of its development, the parasitic larva leaves its moribund host, and drops to the soil where it becomes pupa and then adult. The parasitoid completes five generations in one year. Emergence of adult parasitoids from the overwintering generation occurs in March and coincides with the appearance of first generation host nymphs, which are available for parasitiza tion. Adults of the following parasitoid genera tions appear in May, July, August, and September. Parasitization rates are relatively high (75%) only on the overwintering leafhopper generation. In this generation, oviposition starts from September, but parasitized leafhoppers are noticed by the unaided eye from January onwards.

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Grapevine Leafhopper Complex (Hemiptera: Cicadellidae) in Cyprus, Figure 31 Zygina rhamni: (a) adult of summer generations, (b) adult of overwintering g eneration, (c) adult female parasitized by A phelopus orphanidesi.

only and larval development extends in the adult stage of the host. The older nymphal stages seem to be preferred. Adult leafhoppers exposed to parasitoid females have never been attacked. The parasitoid female grasps the cicadellid nymph with her mandibles, holds it in position with her legs, and oviposits in its body. Parasitized leaf hoppers, noticed by the unaided eye only at the adult stage, bear a sac on either side of the fore parts of the cicadellid gaster in a dorso-lateral position under the wings that contains the para sitoid larva. No leafhopper nymphs have been found to carry any larval sac of the parasitoid. On the overwintering leafhoppers, the sac darkens gradually as the parasitoid larva grows, and

References Jensen FL, Flaherty DL (1982) Grape leafhopper. In: Grape pest management. Division of Agricultural Sciences, Publication No. 4105. University of California, Davis, CA, pp 98–110 Olmi M, Orphanides GM (1994) A new species of the genus Aphelopus from Cyprus (Hymenoptera Dryini dae). Bolletino del Museo Regionale di Scienze Natu rali di Torino 12:407–412 Orphanides G (1995) Bioecology and biological control of the leafhopper complex on grapevines. In review for 1994, Agricultural Research Institute, Ministry of Agri culture. Natural Resources and the Environment, Nicosia, Cyprus, pp 33 Orphanides G (1996) Biological control of the grapevine leafhopper, Zygina rhamni (Ferrari). In review for 1995, Agricultural Research Institute, Natural Resources and the Environment, Nicosia, Cyprus, pp 37

Grass A plant with narrow leaves containing parallel veins. A monocotyledonous plant. A common

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Grass Flies

name for plants in the family Graminae (contrast with broadleaf plant).

Grass Flies Members of the family Chloropidae (order Diptera).  Flies

Grasshopper and Locust Pests in Africa john l. capinera University of Florida, Gainesville, Florida, USA Africa has an exceedingly rich fauna of Orthoptera, including several families and well over 1,000 spe cies, that could be considered to be grasshoppers or locusts. In Africa (also in Asia, Australia, and South and Central America), some grasshoppers are called “locusts.” This term is applied to species of grasshoppers that display phase polymorphism. Phase polymorphism is largely a behavioral change between different states: gregarious and solitary forms, with intermediate forms called “transiens.” During the gregarious phase, which is induced by high densities, locusts tend to disperse long distances in groups (during the nymphal stage the groups are called bands, during the adult stage they are called swarms). These same species are not very dispersive, nor gregarious, during the solitary phase. Physical changes in appearance may also occur during the change in phase, and of course physiological changes underlie the behav ioral and morphological shifts. Transition between the solitary and gregarious phase takes more than one generation. In contrast, grasshoppers tend not to disperse long distances, tend not to aggregate during dispersal, and their appearance remains about the same regardless of density conditions. Thus, “grasshoppers” do not display phase change. Africa suffers from both grasshopper and locust

infestations, but is best known for locust problems. The Arabic phrase for locusts translates to “teeth of the wind,” providing some indication of the severity of the problem. As is the case elsewhere in the world, most of the orthopteran pests are in the family Acrididae, but other families of the order Orthoptera, particularly Pyrgomorphidae, are present as pests. Locusts and grasshoppers sometimes, but not always, conform to the “typical” phase pattern sug gested by the common name of these insects. As expected, when comparing the gregarious and solitary phases of desert locust, Schistocerca gregaria (Forskål), and migratory locust, Locusta migratoria migratorioides (Reiche & Fairmaire), the different phases can be quite distinctive. The behavior, coloration and size differ markedly between the gregarious and solitary phases. A common measure of the gregarious phase is the ratio of wing length to the width of the head; the gregarious phase has relatively longer wings. How ever, in some other species such as the Moroccan locust, Dociastaurus maroccanus (Thunberg), there is little or no change in color, though the relative size of body parts does change. The Senegalese grasshopper, despite not being called a locust, displays some morphological differences between the swarming and non-swarming populations, including longer wings. Thus, it is a good idea not to dwell on the common name of orthopterans, but to look critically at the biology of species indi vidually. Other species are more typically grass hopper-like. Africa has a few spectacular species of “locusts” that command most of the attention and notoriety (as is largely the case in Australia), but some regions also suffer from a large assem blage of grasshoppers (as is largely the case in North America). Some of the more important spe cies are shown in Table 7 and Fig. 32. In Africa, and generally elsewhere in the world, grasshopper and locust populations in arid regions tend to grow in response to increased rainfall, and increased availability of host plants brought about by the precipitation. Annually, favorable habitats result from the belt of rain that

Grasshopper and Locust Pests in Africa

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Grasshopper and Locust Pests in Africa, Table 7 Examples of serious and less serious locust and grasshopper pests in Africa, and regions of Africa where they are abundant Pest status

Scientific name

Common name

Region

Serious

Schistocera gregaria (Forskål)

Desert locust

N, E, W

Locusta migratoria migratorioides (Reiche & Fairmaire)

Migratory locust

N, S, W

Nomadacris septemfasciata (Serville)

Red locust

S, E, W

Locustana pardalina (Walker)

Brown locust

S

Dociostaurus maroccanus (Thunberg)

Moroccan locust

N

Anacridium melanorhodon Walker

Tree locust

E

Oedaleus senegalensis (Krauss)

Senegalese grasshopper

N, W

Aiolopus simulatrix (Walker)

Sudan plague locust

E, W

Zonocerus variegatus (Linnaeus)

Variegated grasshopper

W

Less serious

Hieroglyphus daganensis Krauss

Rice grasshopper

E, W

Kraussaria angulifera (Krauss)

N, E, W

Cataloipus fuscocoeruleipes Sjöstedt

E, W

Cataloipus cymbiferus (Krauss)

N, S, W

Kraussella amabile (Krauss)

Diabolocatantopx axillaris (Thunberg)

N, W

Ornithacris turbida cavroisi (Finot)

Bird locust

W

Pyrgomorpha spp.

Acorypha glaucopsis (Walker)

E, W

Acanthacris ruficornis (Fabricius)

W

Zonocerus elegans (Thunberg)

S

Catanops spp.

Eyprepocnemis plorans (Charpentier)

Bersim grasshopper

N, E, W

N, S, E, and W indicate northern, southern, eastern and western Africa, respectively

follows the movement of the intertropical conver gence, the pattern of prevailing winds that sweeps southward toward the equator from the northern hemisphere, and northward to the equator from the southern hemisphere. Higher than normal

levels of precipitation in the arid regions tends to result in population upsurges, but population decrease can be brought about by losses due to dispersal, competition for food, reduction in food due to decrease in precipitation, and the actions of

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African tree locust

Inhabited area

Migratory locust

Outbreak area

Brown locust

Outbreak area

Recession areas

Invasion area

Invasion area

Moroccan locust

Inhabited area

Red locust

Outbreak area

Inhabited area

Invasion area

Invasion area

Senegalese grasshopper

Desert locust

Sudan plague locust

Inhabited area

Variegated grasshopper

Inhabited area

Grasshopper and Locust Pests in Africa, Figure 32 The distribution of some important grasshoppers and locusts in Africa. The regularly inhabited areas are dark-shaded. For the dispersive species, the areas inhabited occasionally (during periods of outbreak) are shown as cross-hatched.

natural enemies. However, as is often the case in biology, not always does this simple pattern of sea sonal rainfall leading to population increase occur. This is due partly to the vagaries of weather, which

are quite complex, and regionally and temporally subject to variation. Also, the different grasshop per and locust species have evolved different sur vival strategies. Species like the desert locust,


especially when in the gregarious phase, are capa ble of long distance dispersal, and contrary to expectations, may seemingly disperse against the prevailing winds or disperse to areas where rainfall has not recently occurred. Temperature is as important as rainfall and food in governing grasshopper and locust popu lations. Temperature affects nearly all biological activities, and when grasshoppers are outside their relatively narrow optimal temperature zone, they do not thrive. Optimal body temperature for most species is 35–42°C. To some degree, grass hoppers can modify their internal temperatures by changing their behavior, a process called ther moregulation. By basking in the sun, they can raise their body temperature by several degrees, and by moving into the shade or elevating them selves away from the hot soil surface, they can reduce their temperature. However, they remain substantially at the mercy of ambient weather conditions. In northernmost and southernmost Africa, weather is predictably limiting during the cool periods of the year. However, even in the warmer regions, temperature can be limiting, and grasshoppers engage in basking behavior and suffer metabolically during periods of heavy cloud cover or rain.

Desert Locust, Schistocera gregaria (Forskål) Not only is desert locust a devastating pest in Africa, but worldwide it is the most dangerous locust species. It has the capacity to produce very large, long-lasting, and dispersive swarms. This insect is graminivorous, but during outbreaks it feeds on a large number of plants, including all the important grain crops, cotton, and fruit of the region. It occurs in a persistent form within a large area of northern Africa, Saudi Arabia, and east to India. Only small areas of this area of persistence, called a recession area, typically produce the locusts leading to swarms that spread more widely, to regions called invasion areas. Even portions of

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Europe and the former Soviet Union are invaded on occasion, and invasion of over 60 nations in the area has been recorded. Within the recession area are sites where locusts feed, breed and become gregarious; these can be called outbreak areas. These outbreak areas are characterized by having sandy or silty soils and being in arid or semi-arid regions. They are not always the same sites, how ever, because rainfall and vegetation are prerequi sites to population increase. Rainfall is required for oviposition, and females produce 20–100 eggs per pod, and two to three pods per female. On average, the solitary form produces about 95 eggs in the first pod, the gregarious form about 75. Subsequent pods have fewer eggs. The eggs complete their development in 11–75 days, fastest at about 32–34°C. The ensu ing nymphs develop in about 38 days (range of 20–66 days), undergoing five instars. The molt to the adult is called fledging, and the young adult a fledgling. The adults require weeks to months to mature reproductively, but once mature persist for only about 30 days. Once they are ready to oviposit, they have only a few days to find a suitable site. Eggs do not undergo diapause. One to three generations are completed per year, depending on conditions. Crowding for more than one generation is required for development of fully gregarious characteristics. Reduction in plant material within the outbreak sites sometimes forces the insects into closer proximity and stimulates gre garization. Alternately, repeated rains can pro duce several generations in the same area, allowing population increase and crowding. Sometimes partially gregarized populations move to another site that fosters further gre garization. Hoppers spend most of the day marching, and then roost at night on vegetation. Much of the feeding occurs while roosting. Once hoppers reach the adult stage, they are soon capable of flight, but do not always do so. Soli tary locusts fly at night, gregarious locusts dur ing the day. During swarms, locusts can fly for up to 17 hr per day, and travel for 5,000 km

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uring their lifetime. Breeding can occur in the d winter months in the Somali peninsula and along the Red Sea, some of the Saharan summer breed ing areas and southeast Africa, and some of Pak istan and India.

Migratory Locust, Locusta migratoria migratorioides (Reiche & Fairmaire) There are several named subspecies of migratory locust found in the eastern hemisphere. In Africa, the migratorioides subspecies is by far the domi nant race. Migratory locust traditionally has been more of an issue in the southern half of Africa. It occurs in varied habitats, including dunes with open tussock vegetation, man-made habitat including fallow fields, and flooded areas. Its areas of outbreak normally are limited to small areas just south of the Sahara Desert where grass plains flood during summer rains, providing ample food. In more recent times, migratory locust has bene fited from the expansion of irrigated agriculture in the Sahara region, and northern Africa is now realizing migratory locust problems. It is gramini vorous. Migratory locust has two to four genera tions per year, and females produce one to five egg pods with up to 65 eggs per pod. Eggs normally hatch in 10–50 days, but sometimes persist for up to 100 days. There are five to seven instars, requir ing a total of 21–40 days. The adults remain imma ture for 10–14 days, but persist for up to 70 days. Unlike most locusts and grasshoppers, migratory locust lacks a stage that can tolerate long periods in unfavorable conditions. They must breed continuously or they die out. On the other hand, favorable conditions allow them to increase in number rapidly. The locusts migrate from the flood plains to the surrounding Sahe lian areas where they oviposit, but then migrate back to the flood plain and reproduce further. The offspring of this generation again migrate to the Sahel, and return, as did their parents, to the flood plains.

Red Locust, Nomadacris septemfasciata (Serville) Red locust occurs widely in southern Africa during periods of swarming, but the areas of outbreak are limited to several small regions along the Rift Valley in eastern Africa. Outbreak areas are wet lowland regions dominated by grasses and characterized by extreme conditions of flooding and drought. The outbreak areas comprise only 1/1,000 of the invasion area. This locust has only one generation per year, and eggs complete their development in 30 days. The female deposits about 100 eggs in each pod (more in the solitary form), with up to five pods produced per female at 10–15 day intervals. Six to seven instars are completed in about 60–70 days. The pre-reproductive adults persist through the dry season in regions called reten tion areas; these are principally in eastern Z imbabwe, southern Malawi, southwest Uganda, and northern Tanzania. They persist in this stage for over eight to nine months, and then at the start of the rainy season they mature and lay eggs, but adults live for only about a month. Eggs are deposited in areas of bare soil or sparse vegetation. Young hoppers initially remain clumped in family groups, then disperse and re-group in about the second or third instar. The tendency to concentrate is highest in dense vegetation. About the third instar, nymphs begin to form into hop per bands. They shelter at night beneath vegeta tion and then climb upward to bask in the sun in the morning. As ambient temperatures reach 23°C the nymphs commence feeding and dis perse, only to reassemble into bands for evening roosting. This species is graminivorous, and there always seems to be plenty of grass in the outbreak areas, so formation of swarms cannot be ascribed to lack of food. Swarms persist for long periods within their favored habitats, but when they disperse to other areas that are less favorable for reproduction the population declines.


Brown Locust, Locustana pardalina (Walker) Brown locust occurs only in southern Africa, and its outbreak area is found in the southern most part of the continent. Like most locusts, its preferred habitat is semi-arid and desert. It is graminivorous, feeding on grain crops and pas tures. There are two to four generations per year. The female deposits four to five egg pods with about 40 eggs per pod at 7–8 day intervals. Ovi position occurs in dry soil but eggs require mois ture to hatch. They can persist for up to 15 months without rain. These locusts tend to ovi posit communally. Some eggs display delayed hatch of 1–3 months, even though they may be in the same pod as eggs hatching quickly. The rapidly developing eggs require only about 10 days to develop, and hatch when 10 mm or more of precipitation occurs. The nymphal stage has 4–5 instars, and requires 20–40 days to develop. Solitary hoppers complete development in as few as 20 days whereas gregarious hoppers tend to require 40 days, and transient forms intermediate in development time. The adults are short-lived, persisting for 2–3 weeks in the pre-reproductive stage and then 1–2 months in the reproductive stage.

Moroccan Locust, Dociostaurus maroccanus (Thunberg) Moroccan locust occurs throughout the Mediter ranean region on semi-arid steppe and semi-arid desert with grasses, particularly Poa bulbosa. It is found in northern Africa in Morocco, Algeria, and Tunisia, but is also found in southern Europe and east to Iran and central Asia in a discontinu ous pattern. Formerly a minor pest, it has assumed greater importance due to destruction of forests and overgrazing, which provide additional habi tat for this insect. This graminivorous species thrives in regions with winter rains and untilled soil for oviposition. Tilled soil is unsuitable, but

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fallow or abandoned crop land becomes suitable again. Moroccan locust has only one generation per year, and persists during the dry season, about nine months, in the egg stage. The female pro duces 2–5 pods, each containing 20–30 eggs. Pods tend to be grouped in clusters of 5–6 pods with several such clusters in a one meter square area. The nymphs have fives instars, and develop in 30–45 days. They form narrow bands when marching, often only 2 m deep, but a single band may extend for several km. Bands usually march during the day, but sometimes extend into the night. The adult persists for 2–4 months. The adult is gregarious, but not migratory.

Tree Locust, Anacridium melanorhodon (Walker) Tree locust generally is considered to be inconse quential except in Sudan, where it defoliates Acacia senegal, the tree used to produce gum arabic. It feeds preferentially on trees, and is found in the Sahelian region, south of the Sahara desert, from coast to coast. Despite this preference for Acacia, there are reports of it attacking fruit trees, cotton, tobacco, and millet. Outbreaks occur in semi-arid areas, within natural thickets of Acacia spp. Nor mally, a single generation occurs annually, some times a second. Egg pods contain about 150 eggs per pod, and the eggs require 1–2 months before hatching. The nymphs undergo 5–8 instars and complete their development in 2–3 months. Imma tures are found throughout the dry season, and adulthood is attained with the onset of rains (usu ally May-June). Oviposition begins in June-July, and young hoppers appear in August-October. Despite numerous attempts to differentiate between swarming and non-swarming popula tions on the basis of morphometrics, there is little difference to be found. Swarms and bands, when they occur, are relatively small. Both adults and immature forms tend to roost high in trees during the day, descending and feeding at night or early in the morning. They also fly at night.

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Senegalese Grasshopper, Oedaleus senegalensis (Krauss) The Senegalese grasshopper is graminivorous, and is associated with sandy soils and open steppe veg etation, predominately grasses. Found mostly in Sahelian central Africa, its distribution also extends to North Africa, the Arabian peninsula, and beyond into southwest Asia. It occurs principally in lightly wooded or open savanna, and steppe or ephemeral prairies with sandy soil. It often is associated with Aristada pallida, a perennial tussock grass, and Cenchrus biflorus, an annual grass. This species has 2–4 generations per year, and the female produces 1–2 pods with only 20–30 eggs. Eggs are deposited in moist, sandy soil. The eggs resist desiccation, and enter a period of quiescence if adequate moisture is not available. Eggs laid after late August enter obligatory diapause, which can continue for two or more years if adequate moisture is not available. The young hoppers develop quickly, progressing through fives instars in 17–20 days. The interval between hatch and first oviposition is about 35 days. The adults can live for 1–4 months. Like some other grasshoppers, this species shows some of the characteristics of locusts, displaying changes in morphology, marching by hoppers, limited swarm ing by adults, and long distance migration. Flight occurs mostly at night.

Sudan Plague Locust, Aiolopus simulatrix (Walker) Sudan plague locust occurs in a broad band across Central Africa, and also in Asia. It is most abun dant, and damaging, in the Nile Valley of Sudan. It is graminivorous and has two generations per year. Breeding begins soon after the start of rains. The female produces 2–3 pods containing 20–30 eggs per pod, which require less than a month for devel opment. The nymphs undergo five instars, and complete their development in less than a month. The adults are long-lived, persisting for 6–9 months. Adults disperse when they are unable to

find suitable breeding sites, which are normally the clay soils of flood plains. The first generation adults migrate north, where the second generation is produced. In turn, the adults from the second generation migrate southward. Flight occurs at night. Second genera tion adults survive the dry season hidden deeply within the cracks in the parched soil. As tempera tures and humidity rise, signaling the beginning of the rainy season, the adults emerge from the soil cracks, but return during the heat of the day. The populations inhabiting the Nile Valley, which is oriented north and south, generally have higher densities than other inhabited areas, which are smaller and not so oriented. The north-south ori entation of the Nile Valley allows the locusts to remain within suitable habitat during their migra tions, resulting in lower mortality.

Variegated Grasshopper, Zonocerus variegatus (Linnaeus) Variegated grasshopper is found in west-central Africa. Unlike most African grasshopper and locust pests, it is found in humid and sub-humid area, inhabiting openings in the forest zone. It occupies both natural clearings and deforested, cultivated areas. This species has only one genera tion per year. In the mid-March to May period, females produce 2–3 pods, each containing 50–60 eggs. Egg pods tend to be clustered, often in groups of hundreds or thousands. The eggs enter diapause, and require 6–7 months for development. Hatch occurs in October or November. The nymphs require a fairly long time, 75–90 days, to undergo 5–6 instars. The nymphs tend to remain clustered into dense groups, and emit foul-smelling liquids from the first abdominal segment. They disperse relative short distances. The adults emerge in February and persist for 60–90 days. They are dimorphic for wing length, and the long-winged forms are capable of short flights. This species is also unusual in that it prefers broadleaf plants rather than grasses.


It damages herbs, flowers, citrus, and coffee. To a lesser extent it feeds on banana, cassava, and cotton. They are most abundant, and damaging, in the dry season.

Damage Most of the African grasshopper and locust pests feed on grasses, and it is the cultivated grasses, the grain crops, that are most damaged. The grain seedlings and immature seed heads are most sus ceptible to damage. Although rangeland grasses are injured, they usually recover quickly, unlike crops. However, many rangelands, particularly in the Sahel region, are being overgrazed by livestock. The additional loss of forage to locusts on such rangelands can have long-term implications for the health of this ecosystem. Damage to both crops and rangeland is often greatest along the margins of deserts. However, when locusts swarm they can affect crops nearly anywhere. Insect damage, when taken on a regional or national basis, often seems relatively insignifi cant, or difficult to justify when compared to the costs of pest suppression. However, to an individual farmer or pastoralist, the losses can be devastating, and sometimes fairly large regions suffer severe losses simultaneously. Particularly in Africa, the losses caused by grasshoppers and locusts are not easily rectified due to poor infrastructure for reallocation of food, poor communication, or political turmoil. Thus, locust and grasshopper problems can have surprisingly severe conse quences, and suppression programs can provide significant benefit. The severity of the issue in Africa can be seen by examining Table 8, which shows the frequency and distribution of locust and grasshopper prob lems in northern Africa and adjacent areas of the Middle East for the 20-year period of 1963–1982. This example shows only countries experiencing large-scale problems that resulted in organized suppression campaigns, not smaller or localized problems. Nevertheless, the scale of the problem is

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apparent, and in each year there was need for orga nized suppression in at least one country. Also, it is apparent that some countries experienced locust or grasshopper problems almost annually, whereas for others it was an infrequent issue. Lastly, an ele ment of area-wide population increase and decrease is evident, with many countries experi encing problems nearly simultaneously, and then release from locust and grasshopper problems at about the same time.

Management Technologies for population assessment have improved, eliminating some of the element of sur prise from locust and grasshopper outbreaks. Weather monitoring and modeling are often very useful for forecasting the potential for problems, and vegetation can be assessed with remote sens ing technology. However, insect populations are normally confirmed by ground survey personnel via site visits, although swarming populations are sometimes monitored by observers in aircraft. The most important benefit of newer (remote) assess ment technologies is that ground survey personnel are able to focus their visits and insect sampling to areas and times where they are likely to detect the pests. This improved efficiency translates into con siderable financial savings. The locust outbreak areas are often targeted for more intensive monitoring and control efforts because costs are greatly reduced by treating pests while they are confined to these relatively small areas. Although it is possible to recommend cultural and physical management techniques to help sup press grasshoppers and locusts, implementation is often difficult. Over the last 50 years, chemical insecticides have proven to be the management technique of choice, and a considerable amount of effort has been dedicated to improving the appli cation techniques or otherwise affecting the killing power of the insecticides. Generally, application of liquid, residual insecticides to plants, by use of both ground application equipment and aircraft,

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Kuwait

Jordan

Nigeria

Niger

Mali

Chad

Mauritania

Western

1

Algeria

Libya

No. of

any year

control in

doing

countries

Morocco

Sahara

Oman

U.A.E.

Egypt

• •

• • •

•

•

•

•

•

4

3

7

•

11

16

•

• 11

•

•

• •

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

•

• •

•

•

•

•

1969

1968

1967

•

PDR Yemen

•

•

Yemen AR

•

Sudan

Saudi Arabia

•

•

Ethiopia

1966

Somalia

1965

Djibouti

1964

1963

6

•

•

•

•

•

•

1970

7

•

•

•

•

•

•

•

1971

7

•

•

•

•

•

•

•

1972

9

•

•

•

•

•

•

•

•

•

1973

10

•

•

•

•

•

•

•

•

•

•

1974

9

•

•

•

•

•

•

•

•

•

1975

13

•

•

•

•

•

8

•

•

•

•

•

• •

•

•

•

•

1977

•

•

•

•

•

1976

9

•

•

•

•

•

•

•

•

•

1978

4

•

•

•

•

1979

6

•

•

•

•

•

•

1980

7

•

•

•

•

•

•

•

1981

7

•

•

•

•

•

•

•

1982

12

8

6

2

8

2

11

11

1

1

1

3

1

6

11

13

17

17

13

4

7

No. years

G

COUNTRY

s uppression occurred during the 20 year period of 1963–1982 and the total number of years the suppression programs were instituted

Grasshopper and Locust Pests in Africa, Table 8 North African and Middle Eastern countries in which large-scale locust/grasshopper

1674 Grasshopper and Locust Pests in Africa

Grasshopper and Locust Pests in Australia

has been effective. On a much more restricted scale, poison bait applications have been used, especially for the treatment of bands of the gre garious, wingless stages of locusts. More recently, flying swarms have been sprayed with insecticides, or even better, swarms that have alighted. For both ground and air application of liquid insecticides, ultra low volume (ULV) techniques are preferred because mixing and dilution with water is unnec essary, and applicators can spray more land area with each load of insecticide. Bioinsecticides have recently been developed as an alternative to chemical insecticides. In par ticular, identification of a relatively fast-acting fun gal pathogen, Metarhizium anisopliae var. acridum (formerly known as M. flavoviridae), and the for mulation of this in oil, have greatly improved the ability to implement non-chemical suppression. Other bioinsecticides, such as Beauveria bassiana and Nosema locustae, have proven to be less effica cious, as has the botanical insecticide neem. Insect growth regulators have been shown to disrupt the development of grasshoppers, but this requires that the product be applied to the immature stages, and will not protect against winged swarms.  Grasshoppers, Katydids and Crickets (Orthoptera)  Diseases of Grasshoppers  Grasshoppers and Locusts as Agricultural Pests  Grasshopper and Locust Pests in Australia  Grasshopper Pests in North America  Grasshoppers of the Argentine Pampas  Desert Locust Plagues

References Anon (1982) The locust and grasshopper agricultural manual. Center for Overseas Pest Research, London, UK, 690 pp Farrow RA (1990) Flight and migration in acridoids. In: Chapman RF, Joern A (eds) Biology of grasshoppers. Wiley, New York, NY, pp 227–314 Goettel MS, Johnson DL (1997) Microbial control of grass hoppers and locusts. Mem Ent Soc Can 171, 400 pp Lecoq M, Welp H, Zelazny B (2005) Locust literature. ISPICIRAD. Available at http://ispi-lit.cirad.fr Accessed August 2007

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Lomer CJ, Prior C (1992) Biological control of locusts and grasshoppers. CAB International, Wallingford, UK, 394 pp

Grasshopper and Locust Pests in Australia john l. capinera University of Florida, Gainesville, FL, USA In Australia (also in Asia, Africa, and South and Central America), some grasshoppers (Orthoptera: Acrididae) are called “locusts.” This designation is applied to species of grasshoppers that display phase change. Phase change is largely a behavioral change between different states, gregarious and solitary forms. During the gregarious phase, which is induced by high densities, locusts tend to disperse long distances as groups (during the nymphal stage, the aggregations are called bands, during the adult stage, they are called swarms). These same species are not very dispersive or gregarious during the solitary phase. Physical changes in appearance may also occur during the change in phase, and of course physiological changes underlie the behavioral and morphological shifts. Transition between the soli tary and gregarious phase takes more than one gen eration. In contrast, grasshoppers tend not to disperse long distances, tend not to aggregate dur ing dispersal, and their appearance remains about the same regardless of density conditions. Thus, “grasshoppers” do not display phase change. The distinction between grasshoppers and locusts is not clear-cut. At low densities, locusts are not gregarious, nor highly dispersive, but they are still called locusts. Some species that occasionally form aggregations, even forming bands, are called grasshoppers, not locusts, because they do not dis perse long distances. In Australia, migratory locusts have all the features associated with phase change: change in body shape and color, and formation of dense swarms during dispersal. The Australian plague locust displays a tendency to become gregarious and to swarm, but lacks a change in

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appearance during the transition between phases. The spur-throated locust rarely forms bands, though it does form swarms. The small plague grasshopper forms aggregations, but does not undergo long distance dispersal in swarms. So the “locusts” of Australia display a wide range of behaviors, from very locust-like to not so typically locust-like. Australia is known for frequent and severe problems with locusts, but grasshoppers also are implicated. The severity of the problem is due principally to the fact that Australia is largely an arid country (about 80% is arid or semi-arid), and in this environment not only do grasshoppers tend to thrive, but the effects of their herbivory are amplified by the sparse grass and other herbage available to livestock in this climate. During peri ods of drought, forage plants are especially valu able, and vital for livestock grazing; thus, conflict with humans is inevitable. However, the relation ship of grasshoppers with moisture is not simple. In the more arid, ephemeral grasslands, high levels of summer moisture provide an abundance of food, allowing grasshoppers to maximize their reproductive potential and build to high numbers, usually over three to four generations. As the veg etation dries, the grasshoppers disperse (migrate) until they find areas with green vegetation. In regions with more rainfall during the sum mer breeding season (formerly forested but cleared by humans for grazing or crops), however, biotic factors that suppress grasshopper numbers are more effective during wet seasons, so population outbreaks are associated with drought. In some areas, clearing of forest, expansion of improved pasture, and the introduction of irrigation have created environments conducive to grasshopper outbreaks. In these areas, species not formerly caus ing problems have emerged as pests.

Pest Species of Grasshoppers in Australia Despite that fact that about 275 species of grass hoppers are known from Australia, only a few are

serious pests, and most are indigenous to Australia. However, most of the damage is caused by only four species: Australian plague locust, Chortoicetes terminifera (Walker); spur-throated locust, Austracris guttulosa (Walker); migratory locust, Locusta migratoria migratorioides (Reiche & Fair maire), and wingless grasshopper, Phaulacridium vittatum (Sjöstedt), and of these, two are rather widespread in Southeast Asia (Fig. 33). The impor tant species are given in (Table 9). Spur-throated locust and migratory locusts sometimes cause severe damage on a localized basis, but the frequency of this is low. Wingless grass hopper has emerged as a chronic pest of improved pastures in southeastern Australia. Small plague grasshopper was formerly a serious pest in Australia during the 1930s and 1940s on cereal crops grown in southern and western Australia, but has dimin ished in importance. Giant grasshopper is pestifer ous only occasionally, and this species is limited to northern and eastern Australia. Yellow-winged locust feeds only on grasses, and though irregularly important, seems to be favored by drought.

Australian Plague Locust, Chortoicetes terminifera (Walker) The Australian plague locust is the most important grasshopper pest in Australia due to the high frequency of outbreaks and the widespread nature of the problem. For example, during the period of 1976–2001, Australian plague locust required con trol in eastern Australia in 18 of the 27 years. The number of generations ranges from one per year in arid, interior regions, to three per year in the more favorable regions of eastern Australia. Outbreaks normally originate in the arid zone of southeastern Australia, and to a lesser degree southwestern Australia, but they can disperse into adjacent but much larger areas during periods of outbreak. Australian plague locust normally inhabits areas containing Mitchell grass, Astrebla spp., species that remain green for several months after rain, thus providing a relatively constant


Migratory locust

Plague locust

Persistent

Persistent

Intermittent

Intermittent

Spur-throated locust

Persistent

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Persistent

Intermittent

Grasshopper and Locust Pests in Australia, Figure 33 The distribution of some important grasshoppers and locusts in Australia. The regularly inhabited areas are dark-shaded. For the dispersive species, the areas inhabited occasionally (during periods of outbreak) are shown as cross-hatched.

food supply. If multiple rainfall events occur, populations build rapidly, and migrate if rain does not continue. The direction of dispersal is determined by the pattern of weather; in eastern Australia, those moving in southerly or easterly

directions pose a serious threat to crops. Longdistance dispersal occurs when nighttime tem peratures (above 25°C) are warm, and strong winds are present at high altitudes. These locusts typically remain airborne for 8–9 h, descending

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Grasshopper and Locust Pests in Australia, Table 9 The most important grasshopper pests in Australia Scientific name

Common name

Occurrence

Chortoicetes terminifera (Walker)

Australian plague locust

Semi-arid interior of Australia

Austracris guttulosa (Walker)

Spur-throated locust

Northern and northeastern Australia, and elsewhere in Southeast Asia; adapted to seasonally dry regions

Locusta migratoria migratorioides (Reiche & Fairmaire)

Migratory locust

Adapted to continuous moist tropical and subtropical conditions, especially coastal regions of northern and eastern Australia, but widespread in the Pacific Region

Phaulacridium vittatum (Sjöstedt)


Moist uplands of temperate regions of Australia

Austroicetes cruciata (Saussure)

Small plague grasshopper

Limited to southern fringe of arid zone in Australia

Gastrimargus musicus (Fabricius)

Yellow-winged locust

Moist subcoastal regions of Australia

Valanga irregularis (Walker)

Giant grasshopper

Eastern Australia

Oedaleus australis Saussure

Eastern plague locust

Eastern interior Australia

Aiolopus thalassinus Fabricius

Clearwinged grasshopper

Coastal and subcoastal eastern Australia

Praxibulus spp.

Yellow-bellied grasshoppers

Southeastern Australia

Fipurga crassa Sjöstedt

Dimorphic grasshopper

Southeastern Australia

Urnesia guttulosa Walker

Salt and pepper grasshopper

Semi-arid interior of Australia

at daybreak. Emigrants may breed successfully and continue the outbreak, but Australian plague locust outbreaks typically dissipate within a few generations. Thus, its notoriety is based more on the frequency of occurrence than the length of the plague. Sometimes migration proves to be deadly for locusts, as their dispersal is largely determined by strong winds associated with weather fronts or low pressure systems. Low pres sure is often indicative of rain, which works to the advantage of insects requiring green grass for breeding, but sometimes locusts are deposited in lakes or the ocean, causing massive mortality. Also, though it is less evident, the progeny of some migratory locusts return from the invaded areas to their regions of persistence, helping to re-establish the potential for new outbreaks.

In the south, the cool winters inhibit develop ment and no egg laying occurs for about three months. Egg deposition typically occurs in hard, packed soil or stony areas. In the warmer north, the interruption in reproduction is shorter. Irrespective of location, however, at the start of the spring the majority of the population is usually in the egg stage, and some diapause occurs. This locust has five or six nymphal instars after hatching, which requires (in total) 3–5 weeks. Males of Australian plague locust measure about 25–30 mm long, females 30–42 mm. Adults of this species are distin guished from other common locusts by the pres ence of a dark spot at the tip of the hind wing. The adult requires only about 2 weeks to mature, and then deposit eggs. Eggs are deposited in the soil at a depth of 6–8 cm. If the weather is favorable and no


diapause occurs, eggs can hatch in as little as 2 weeks. Females deposit two to three egg pods, each containing about 50 eggs. Often females lay large numbers of pods in the same area (egg beds), prob ably because soil moisture conditions are appropri ate. If the rainfall is concentrated into a brief period (typically summer, but winter in some locations) the population is limited to a single generation, but if rainfall continues (e.g., spring and autumn), up to four generations may occur. It is these multiple gen erations per year that can result in rapid population increase and development of a plague.

Spur-Throated Locust, Austracris guttulosa (Walker) This tropical species occurs widely in Australia and nearby islands, north to the Philippines. Unlike most of Australia’s locust and grasshop pers, which survive the inclement periods in the egg stage, this species undergoes reproductive diapause. Thus, it fails to reproduce during the dry season, but commences egg production with the onset of the monsoons in the spring. Additional rain is needed for good egg and nymph survival. As noted previously, the egg stage does not undergo diapause and requires warm conditions in order to develop. A period of quiescence is possible, however, and egg hatch can be delayed for a month if moisture is absent. This species is distinguished by the presence of a large spine between the front legs, and its large size. Males are 55–65 mm in length, females 70–80 mm long. This species lays up to 160 eggs in a pod, and up to five pods within its life span. It does not favor oviposition in egg beds, though barren areas are favored. Areas along roadways and irrigation ditches often are favored oviposi tion sites. Eggs require 18–30 days to hatch. Nymphs can be found at high densities, but they do not form marching bands. Duration of the nymphal stage is 1–2 months. There are 6–8 instars. The adults mature at the end of summer. Only one generation develops per year.

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Outbreaks of spur-throated locust are infre quent, and initially are quite confined in area. Pop ulation dynamics are not well understood, but abnormally high summer rainfall is thought to precede population increases. If vegetation becomes dry, adults are more likely to migrate. After spending the dry winter months in a rather sedentary manner, roosting in trees or other tall vegetation, the adults become active in the spring and may disperse and expand the outbreaks. The populations cannot thrive without wet conditions, however, so except during outbreaks it is largely confined to the wet northern regions. Grasses are the principal host during the early instars. As sum mer habitats dry up, swarms disperse to winter habitats, which are woodlands and cultivated crops. Because the adult stage persists through the winter until mid summer, it can easily damage a wide range of winter crops (wheat, barley, millet) and summer crops (sunflower, soybean, cotton, sorghum), and others. The adults tend to feed dur ing the day, and roost in trees at night. Control of this species is directed at the adult stage, which is sedentary in winter and therefore easy to assess and treat with insecticides. Once the adults disperse, egg laying is scattered, so treat ment of nymphs is difficult.

Migratory Locust, Locusta migratoria migratorioides (Reiche & Fairmaire) Widely distributed in the Australasian region, this is a diapause-free insect that inhabits the mild, mostly coastal and subcoastal regions of Australia, and cannot survive the colder regions of southern Australia. Two (in temperate areas) to four (in tropical areas) generations are produced per year. They are primarily grass feeders, attacking grass pastures and grass crops such as sugarcane, sorghum, maize, and wheat. This large, heavy-bodied species measures about 45–55 mm in length for males, and 55–65 mm for females. Females commonly oviposit in groups,

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resulting in “egg beds” that contain numerous egg pods. A pod contains about 50–60 eggs, with females producing 3–5 pods. Eggs require 11–15 days to hatch. There are about six instars, and this insect requires approximately 30 days to attain maturity. Changes in weather precipitate outbreaks of this species, resulting in gregarization. Increases in winter rainfall and decreases in summer rain are the normal triggers. However, forest removal and pasture improvement has fostered winter breeding in some areas, and provided good sites for oviposition. It was not until the extensive clearing of native vegetation of the central high lands of Queensland that migratory locust became a pest, as pastures and crops have become impor tant food resources. Migratory locust is less dispersive than many other locusts, and nighttime flights are lacking, so development of outbreaks proceeds slowly. The swarms are unusually cohesive, however, and characterized by a low, tumbling or rolling pro gression. Once the swarms leave habitat suitable for breeding, they collapse. Duration of outbreaks is 10–20 generations over 4–5 years, which is lon ger than some other locusts but shorter than exhibited by the same species in Africa and the Philippines (7–13 years). A wide range of crops are damaged by migratory locust, and damage can be quite severe, but due to the limited dispersiveness it tends to be a regional concern rather than a national problem. Control of migratory locust is feasible if prop erly timed because, during the period of gregariza tion, the populations are confined to relatively small areas. If detected during the period of gre garization, suppression with chemical insecticides, using aerial or ground application technology, is quite efficient and economical.

Wingless Grasshopper, Phaulacridium vittatum (Sjöstedt) Wingless grasshopper is actually a species com plex, consisting of Phaulacridium crassum Key

(though much less important and confined to southwestern Australia) in addition to P. vittatum, though the presence of P. crassum is often over looked. It is found in the cooler, temperate areas of Australia. Wingless grasshopper has only one gen eration per year. Eggs are deposited in the fall, undergo diapause and hatch in the spring. Egg pods contain only about 12 eggs per pod, consid erably less than the aforementioned locusts, which usually produce pods of 50 or more eggs. How ever, they may produce 12–16 pods. There are five instars during the summer months. Males of wingless grasshopper are about 8–12 mm in length; females are 12–18 long. Despite the name given these grasshoppers, wingless grass hopper is short-winged under most pasture condi tions and often long-winged in woodland and garden conditions. Wingless grasshopper problems were not known in Australia until about 1935, and were not recorded as a severe problem until 1979, but are increasing in severity. This grasshopper nor mally feeds on broadleaf plants in woodlands and pastures, and though present, is not com mon in natural woodlands, probably due to shortage of suitable food. With European settle ment came land clearing and introduction of grazing animals that depleted the native grasses. Accidentally introduced and deliberately intro duced broadleaf plants soon replaced native grasses; the broadleaf plants proved to be very suitable food for wingless grasshoppers. How ever, it was not until about 1945, when subterra nean clover (a winter-active plant) was planted into pastureland, and fertilized, that wingless grasshopper became a regular problem. Addi tion of other legumes (perennial clover in south eastern Australia and alfalfa [lucerne] in southwestern Australia) during the summer exacerbated the grasshopper problem by provid ing a continuous suitable food supply. It also attacks crops such as sunflowers, sweet corn, potatoes, grapes, ornamentals, and trees. Move ment of these grasshoppers is unlike that of most locusts. The dispersing assemblages are described


as streaming, and as formation of loose bands. They occur when food is depleted, which often is associated with hot weather. The continuous availability of food predis poses improved pastures to wingless grasshopper problems, but outbreaks also involve drought, overgrazing, and insect parasitic nematodes. When droughts occur, the carrying capacity of pastures is exceeded, and overgrazing occurs. Overgrazing, and opening of the canopy, initially favors grass hopper survival, and drought inhibits mermithid nematodes (Amphimermis acridiorum, Agamermis catadecaudata, Mermis quirindiensis, Hexamermis spp.) from parasitizing wingless grasshoppers. When rainfall again increases, the activity of the nematodes increases correspondingly, resulting in grasshopper suppression. Wingless grasshoppers can be managed if continuous vegetative cover is maintained, partic ularly an increase in grasses at the expense of legumes. Natural enemies, particularly mermithid nematodes, are important and favored by good vegetative cover and high moisture. Reforestation, especially of ridge lines where grasshopper survival is favored, will reduce grasshopper numbers. Over grazing should be avoided.

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waste areas and not immediately threatening. This is a departure from past practices, when popula tions were treated primarily when they moved into crop or pasture areas. The reasoning behind not treating locusts until the threat was imminent was that many swarms would collapse due to changes in weather without ever doing damage to crops. However, to allow the populations to develop unimpeded meant that the resultant populations could be quite large and difficult to control. Locust and grasshoppers are treated with liquid insecti cides by air and ground; poison baits also are used, especially for wingless grasshopper. As noted above, some species become problems following changes in land management, mostly land clearing for crops or replacing grasses with more suscepti ble plants. Thus, some problems can be alleviated by wise land use.  Grasshoppers, Katydids and Crickets (Orthoptera)  Diseases of Grasshoppers  Grasshoppers and Locusts as Agricultural Pests  Grasshopper and Locust Pests in Africa  Grasshopper Pests in North America  Grasshoppers of the Argentine Pampas

References Management Strategies Many of Australia’s locust problems result from changes in precipitation, and there is little to be done about weather other than careful weather monitoring. However, it is imperative to under stand how different species respond to precipita tion, and to be alert for impending problems. Population monitoring can be difficult when deal ing with swarming insects, as it is easy to overlook mobile swarms until they move to cultivated areas. Once increasing populations are detected, it is advisable to decrease the threat of economic loss from migrating swarms by eliminating the prob lem before it fully develops. This usually requires decreasing the pest population by 50% in each generation, even when the pests are limited to

Anon (1982) The locust and grasshopper agricultural manual. Center for Overseas Pest Research, London, UK, 690 pp Baker GL (1993) Locusts and grasshoppers of the Australian region. The field guides to the most serious locust and grasshopper pests of the world. D9E. The Orthopterists’ Society, 66 pp Deveson ED, Walker PW (2005) Not a one-way trip: historical distribution data for Australian plague locusts support frequent seasonal exchange migrations. J Orthoptera Res 14:91–105 Hunter DM, Strong K, Spurgin PA (1998) Management of populations of the spurthroated locusts, Austracris guttulosa (Walker) and migratory locust, Locusta migratoria (L.) (Orthoptera: Acrididae), in eastern Australia during 1996 and 1997. J Orthoptera Res 7:173–178 Hunter DM, Walker PW, Elder RJ (2001) Adaptations of locusts and grasshoppers to the low and variable rainfall of Australia. J Orthoptera Res 10:347–351 Rentz DCF, Lewis RC, Su YN, Upton MS (2003) A guide to Australian grasshoppers and locusts. Natural History Publications, Sabah, Malaysia, 419 pp

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Grasshopper Pests in North America

Grasshopper Pests in North America John L. Capinera University of Florida, Gainesville, FL, USA In North America, there is not much effort to label grasshopper species as “locusts,” as is done else where in the world, though the Central American locust, Schistocerca piceifrons (Walker), occurring in Mexico and southward into South America, is a notable exception. At least one additional species (Melanoplus sanguinipes [Fabricius]), perhaps oth ers, would qualify as locusts using the standards of orthopterists elsewhere (see “Grasshopper and locust pests in Australia” for discussion of this topic). Also, the crop-damaging shieldback katy dids or long-horned grasshoppers (Orthoptera: Tettigoniidae) are often called crickets, but func tionally affect crops and rangeland like grasshop pers, or maybe even locusts, so they are mentioned below even though they are technically neither grasshoppers nor crickets. With few exceptions, North American grasshoppers considered to be pests are in the order Orthoptera and family Acridi dae; the exceptions are lubber grasshoppers (Roma leidae) and the aforementioned tettigoniids. Grasshoppers attack nearly all grain, forage, field, fruit, and vegetable crops. Ornamental plant crops are also damaged in both nurseries and the landscape when grasshoppers are especially abundant, but less often than other crops due to their common location in or near urban and subur ban areas, away from habitats conducive to grass hopper outbreaks. Rangeland is the natural habitat of an immense assemblage of grasshoppers, and more than any cultivated crop, it is affected by grass hoppers. Sometimes the grasshoppers cause injury when the plants are quite small and easily defoli ated, or stressed by lack of precipitation. However, mature or nearly mature crops are commonly dam aged when grasshoppers enter crops along the field margins, feeding on the foliar or reproductive struc tures. Unhindered, they may eventually spread over the entire field. On rangeland, grasshoppers are

often found throughout the environment, though the elements of the species assemblage vary accord ing to topographic and host plant characteristics. Ragged leaf tissue or complete defoliation of plants along field margins is suggestive of grass hopper problems. Normally the grasshoppers are readily visible, though the adults of some species sometimes disperse to distant areas with good cover, re-invading the crop daily.

Identity of Crop-Feeding Grasshoppers (Families Acrididae, Romaleidae, Tettigoniidae) Melanoplus spp. (family Acrididae) grasshoppers are the most important grasshopper pests of crops in North America. The principal pests in North America are two-striped grasshopper, Melanoplus bivittatus (Say); differential grasshopper, M. differentialis (Thomas); red-legged grasshopper, M. femurrubrum (De Geer); and migratory grasshop per, M. sanguinipes (Fabricius) (Fig. 34). In north ernmost states of the United States and the Prairie Provinces of Canada, Packard’s grasshopper, M. packardi Scudder, can be locally important, as can other species including some band-winged species, particularly the clear-winged grasshopper, Camnula pellucida (Scudder). In southeastern North America, eastern lubber grasshopper, Romalea microptera (Beauvois) (family Romaleidae) and American grasshopper, Schistocerca americana (Drury) (Acrididae) are locally important. In Mexico and Central America, the Central Ameri can locust, Schistocerca piceifrons Walker displays locust-like behavior. Overall, migratory grasshop per is the most damaging species, and though not usually called a “locust,” nonetheless it is a strong flier and has gregarious tendencies. Other species can surpass the abundance of M. sanguinipes locally, and others display gregarious and disper sive tendencies, but none compare on a regional basis to this widespread grasshopper. In the moun tain and intermountain areas of western North America, certain shieldbacked katydids (family


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Grasshopper Pests in North America, Figure 34 Some common crop-feeding grasshoppers: upper left – red-legged grasshopper, M. femurrubrum (De Geer); upper right – two-striped grasshopper, M. bivittatus (Say); center left – migratory grasshopper, Melanoplus sanguinipes (Fabricius); center right – differential grasshopper, M. differentialis (Thomas); lower left – American grasshopper, Schistocerca americana Drury; lower right, clear-winged grasshopper, Camnula pellucida (Scudder) (photos by J.L. Capinera).

Tettigoniidae) are grasshopper- or locust-like, though flightless. The most important is Mormon cricket, Anabrus simplex H aldeman, but sometimes coulee cricket, Peranabrus scabricolis (Thomas) is abundant enough to be damaging to crops.

Life Cycle of Crop-Feeding Grasshoppers Most grasshoppers pass the winter in the egg stage and have a single generation per year, but in

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southern areas M. sanguinipes and S. americana may have additional generations, and S. piceifrons has two generations. Grasshoppers typically hatch from eggs in the spring or early summer. The species dif fer slightly in the timing of their hatch, and the hatching is not synchronous, so different stages may be found throughout the summer. Grasshoppers usually molt five or six times and require about 5–6 weeks to reach maturity. About two weeks later they commence egg laying, and c ontinue to deposit eggs, in clusters called pods, containing 20–100 eggs per pod until they are killed by cold weather. Eggs, which are deposited in the soil, are not normally affected by weather, but are susceptible to damage by tillage and certain predatory insects. When the young grass hoppers hatch in the spring they are susceptible to inclement weather (low temperatures and rainfall). Throughout their lives, grasshoppers are attacked by parasitic insects, diseases, and insect and vertebrate predators. These natural enemies can suppress grass hoppers locally, but often only after the grasshoppers attain very high and damaging densities. Plants dif fer greatly in suitability for grasshopper survival and growth. In general, these pests prefer broad-leaf plants, not grasses, but the cultivated grains, especially wheat and corn, are highly attractive and suitable for grasshopper survival.

Management of Crop-Feeding Grasshoppers The need for management is most directly related to grasshopper density. As a general rule, when grasshopper densities are 15 or more per square yard (18 per square meter) within a grain field or more than 40 per square yard (48 per square meter) along field borders, economic damage will ensue. With densities of 8–14 per square yard (10–17 per square meter) within a field, or 20–40 per square yard (24–48 per square meter) along field borders, the crop is at risk. These lower densities can prove damaging when the grasshoppers are more mature (larger), the crop is young, or the crop is stressed by lack of soil moisture. Thus, for winter wheat culture

(the crop is planted in the late summer, becomes dormant in the winter, and completes its growth in the spring), the lower thresholds for treatment are used because the grasshoppers are mature in the autumn when the wheat is young. Grasshopper problems most often originate outside the crop field (though planting into wheat stubble or fields that were previously weedy can be exceptions), so treatment of weedy or waste areas (sometimes rangeland) surrounding a field with an insecticide can be an effective approach to pre vent invasion of the crop (Fig. 36). Liquid formula tions of contact insecticides are usually used for this approach. Alternatively, treatment of the crop margin (about 150 feet [47 m] of the border areas) will kill most grasshoppers as they disperse into a crop. Fast-acting contact insecticides applied to foliage or soil, contact insecticides applied to wheat bran bait, and systemic insecticides applied to the foliage or seed are some approaches used to deliver toxicants to grasshoppers. In some areas, farmers commonly plant higher densities of grains along the field margins if they anticipate grasshopper problems, to allow for some crop loss.

Identity of Rangeland Grasshoppers Rangeland occurs mostly in arid and semi-arid regions, which corresponds roughly with the western half of the United States and Canada. This habitat consists of grasses and broadleaf plants (forbs), and sometimes shrubs, but not usually trees. The North American grasshoppers affecting rangeland sometimes are the same as those affect ing crops, particularly Melanoplus sanguinipes, and to a lesser degree Camnula pellucida and Anabus simplex, which can be abundant and damaging in both environments. Most often, however, the abundant species on rangeland are not the same as those affecting crops (Fig. 35), even when irrigated crops are surrounded by rangeland, providing good opportunity for rangeland species to dis perse into crops. Often when the crop-feeding


Grasshopper Pests in North America, Figure 35 Some common rangeland grasshoppers: upper left – Phoetaliotes nebrascensis Thomas; upper right – Amphitornus c oloradus Thomas; second row, left – Aulocara elliotti Thomas; second row, right – Mermiria bivittata Serville; third row, left – Cordillacris occipitalis Thomas; third row, right – Ageneotettix deorum Scudder; bottom left – Aeropedellus clavatus (Thomas); bottom right – Opeia obscura Thomas (photos by J.L. Capinera).

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Grasshopper Pests in North America, Figure 36 Damage to the edge of a winter wheat field caused by grasshoppers. Grasshoppers dispersed from the residue of a previous weedy wheat crop ( designated “a”), to the margin of a young wheat crop, where they destroyed the seedlings (location “b”). The undamaged wheat is in the foreground (location “c”).

species are present on rangeland, it is due to dis turbance and growth of weedy vegetation instead of native grasses or forbs. Floral disturbance can occur following overgrazing, excessive trampling of the soil (a common occurrence around live stock water tanks), or other factors such as out breaks of white grubs (Coleoptera: Scarabaeidae) which kill the grasses, allowing weeds to invade. The species most commonly associated with rangeland damage are listed in the table. North America has a surprisingly rich fauna on rangeland, with a large number of species con tributing to “grasshopper” population outbreaks (Table 10). About 375 species of grasshoppers are found inhabiting North American rangeland. About a third are considered to be pests, but nearly all the rest are innocuous, either due to their dietary habits or their lack of abundance. Most outbreaks on rangeland consist of an assemblage of species, with the species varying from place to place, and some peaking early in the outbreak cycle, and others later. Another interesting aspect of rangeland grasshop per problems is that some species have proven to be destructive at one time or another, only to fade into oblivion for many years (e.g., high plains grasshop per, Dissosteira longipennis Thomas). Interestingly, not all rangeland-dwelling grasshoppers are pests. Many species do not feed on grasses or other important livestock food (the “grass” hopper designation, like many common

names, is not entirely accurate). More importantly, some species feed selectively on rangeland plants that are considered to be toxic to livestock (e.g., Hesperotettix viridis [Scudder] on snakeweed, Gutierrezia sarothrae and microcephala) or com petitors for moisture or light with more nutritious species (e.g., Hypochlora alba Dodge on sagebrush, Artemisia spp.). Even Anabrus simplex, long viewed as a scourge of farmers and ranchers in the Rocky Mountain region, has been shown to be relatively innocuous on rangeland under normal conditions. It avoids grasses, except for seed heads, preferring to feed on flowers and foliage of low-value broad leaf weeds. Only under severe drought conditions, when there is almost no forage available for live stock, is this insect a pest of rangeland.

Life Cycle of Rangeland Grasshoppers The biology of rangeland grasshoppers and cropfeeding grasshoppers is, in most cases, about the same. However, a few rangeland species overwin ter as nymphs, and in southernmost areas adults are sometimes found in the winter. Natural ene mies are more important in the survival of range land grasshoppers because insecticides are rarely used, and therefore beneficial insects are more abundant. Tillage is not normally practiced on


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Grasshopper Pests in North America, Table 10 Grasshoppers commonly damaging to rangeland in North America Family

Subfamily

Scientific name

Acrididae

Melanoplinae

Melanoplus sanguinipes Fabricius

Melanoplus infantilis Scudder

Melanoplus devastator Scudder

Melanoplus occidentalis Thomas

Oedaleonotus enigma Scudder

Phoetaliotes nebrascensis Thomas

Gomphocerinae

Aulocara elliotti Thomas

Aulocara femoratum Scudder

Ageneotettix deorum Scudder

Aeropedellus clavatus (Thomas)

Amphitornus coloradus Thomas

Phlibostroma quadrimaculatum Thomas

Opeia obscura Thomas

Cordillacris occipitalis Thomas

Mermiria bivittata Serville

Chorthippus curtipennis Harris

Psoelessa delicatula Scudder

Eritettix simplex Scudder

Oedopodinae

Camnula pellucida Scudder

Trachyrhachys kiowa Thomas

Dissosteira longipennis Thomas

Dissosteira spurcata Saussure

Encoptolophus costalis (Scudder)

Metator pardalinus Saussure

Trimerotropis pallidipennis Burmeister

Tettigoniidae

Tettigoniinae

Anabrus simplex Haldeman

rangeland, so there is less soil disturbance that might result in destruction of egg pods. In con trast to crop environments, egg pods in rangeland are less likely to be concentrated along field mar gins, as often occurs with crops that have weedy margins along fences and irrigation ditches, which are favored by grasshoppers for oviposition. A notable aspect of rangeland grasshopper biology is the relatively synchronous increase or decrease in abundance of different species in the grasshopper species assemblage. Population cycles

are related to weather, host plant abundance, and natural enemy abundance. Generally, hot and dry weather are responsible for increase in population density in northern areas, where grasshoppers are limited by inadequate daily warmth during the summer days, or a short summer season. In south ern regions, however, warmth is not so limiting, and the lack of abundant nutritious vegetation is more constraining, so rainfall during the spring (which determines the availability of host plants) is a controlling variable.

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Grasshoppers need to control their body temperature if they are to feed, develop, and reproduce optimally. Patches of bare soil allow grasshoppers a site to elevate their body temper atures by basking in the sunshine, and so many species thrive where the vegetation density is low enough to allow basking. However, if there is too much vegetation-free space they cannot meet their nutritional needs. Thus, there are trade-offs between not enough and too much vegetation, and this is made more complex by the differing dietary needs (different host prefer ences and amount of vegetation required) of dif ferent species of grasshoppers. Competition for the most suitable food resources is more fre quent and important than generally acknowl edged. Many observers fail to recognize that grasshopper populations can be under nutri tional stress when there is still relatively abun dant vegetation on rangeland because it may be difficult to discern that the most favored plant species have already been consumed. Rangeland differs greatly in suitability for plants and grasshoppers. Precipitation is the major determinant of plant species occurrence and in plant size, but temperature effects, due both to altitude and latitude, are important. The dominant species of grasses, and their biomass, change with location. For example, the dominant grasses are various Adropogon, Agropyron, Stipa, Panicum, and Calamovilfa spp. in the eastern areas of the Great Plains of North America, but are replaced by Bouteloua and Stipa spp., Koleria scoparius, and Agropyron smithii centrally, and Bouteloua gracilis, Agropyron smithii, and Buchloe dactyloides in more western regions. There is also a general decrease in the average height of vege tation as one moves from east to west in the Plains region, so these regions are denoted as tallgrass, mixedgrass and shortgrass regions, respectively. In the intermountain region, bunch grasses such as Agropyron spicatum and Bromus spp. predominate. As noted in the table, spe cies from three subfamilies, Melanoplinae, Gomphocerinae, and Oedopodinae, are important

rangeland grasshoppers. Generally, members of each subfamily occur together, but the propor tion in each subfamily is not constant among dif ferent localities. Though tallgrass and mixedgrass environments are dominated by grasshoppers in the subfamily Melanoplinae (spurthroated grass hoppers), shortgrass sites are dominated by grasshoppers in the subfamily Gomphocerinae (stridulating slantfaced grasshoppers).

Management of Rangeland Grasshoppers The principal challenges confronting rangeland grasshopper management are the extensive areas to be managed, and the low value of the forage. Both factors limit the amount of money that can be expended per unit area, and preclude using anything but the most economic pest suppression measures in most instances. Insecticides are generally used for suppres sion of grasshoppers, and usually area-wide cam paigns are instituted with the help of government agencies because when a problem develops, it nor mally occurs over a large geographic area. Large, specially equipped aircraft often are used to treat large land areas with liquid insecticide, and some times ultra low volume (ULV) insecticides are applied because they are applied undiluted and at very low application rates, which means that more land area can be treated between refills of the spray tanks. This reduces time and labor costs consider ably. A common alternative to liquid insecticide application is to apply insecticide-treated bran bait using aircraft. This has the advantage of being more selective, because although many species of grasshoppers will feed on bait and perish, many other insects are unaffected. When initiating grasshopper suppression on rangeland, the common biological considerations are the grasshopper species involved, their den sity, and the stage of development. Not all grass hoppers are damaging, and some are quite a lot more damaging than others. A density of 10–15

Grasshoppers

grasshoppers per square yard (12–18 per square meter) is normally needed to justify treatment (hopefully adjusted for the species involved). Not all grasshoppers hatch synchronously, and appli cations are timed to allow for all, or at least most, of the hoppers to hatch and thus come into con tact with the insecticide. Waiting too long, how ever, is counterproductive because they will have already consumed a significant amount of live stock forage. Grasshopper suppression operational con siderations are as important as biological consid erations in determining the feasibility of area-wide grasshopper suppression. Operational consider ations usually involve population sampling to delineate areas that need treatment over an exten sive area, including areas that are “sensitive” and cannot be treated; obtaining and scheduling the aircraft and toxicants; organizing ranchers to obtain funds and permission for treatment; and establishing a mechanism of effective mapping, communication, and rancher and public informa tion, including news releases. Livestock grazing pressure is often suggested as an element that affects grasshopper abundance. Historically, overgrazing by livestock disrupted the native flora, especially in the eastern regions of the Great Plains, allowing invasion of weeds more suitable for grasshoppers. Also, grazing can result in more barren soil, which is attractive to grasshoppers for thermoregulation and oviposi tion. Thus, grasshopper problems are sometimes attributed to overstocking of livestock. While overgrazing should be avoided for several reasons, including the ability to cause grasshopper prob lems under certain conditions, some rangeland can tolerate quite a lot of grazing pressure, and even benefit from grazing by livestock. Extensive research has demonstrated a positive correlation between vegetation abundance and grasshopper abundance in the arid regions of the Great Plains where vegetation is shorter or less abundant, and grasshoppers tend to be food-limited. As noted previously, these areas are dominated by gom phocerine species, whereas other areas have

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roportionally more melanoplines and oedo p podines. Where gomphocerine grasshoppers pre dominate, moderate or heavy grazing can reduce the abundance of grasshoppers relative to ungrazed or lightly grazed areas.  Grasshoppers, Katydids and Crickets (Orthoptera)  Diseases of Grasshoppers  Grasshoppers and Locusts as Agricultural Pests  Grasshopper and Locust Pests in Africa  Grasshopper and Locust Pests in Australia  Grasshoppers of the Argentine Pampas  Migratory Grasshopper  Red-Legged Grasshopper  Two-Striped Grasshopper  Differential Grasshopper  American Grasshopper  Mormon Cricket

References Capinera JL (ed) (1987) Integrated pest management on rangeland; a shortgrass prairie perspective. Westview Press, Boulder, CO, 426 pp Capinera JL, Scott RD, Walker TJ (2004) Field guide to grass hoppers, katydids, and crickets of the United States. Cornell University Press, Ithaca, NY, 249 pp Cunningham GL, Sampson MW (1996) Grasshopper inte grated pest management user handbook. USDA, APHIS Tech Bull 1809 Gangwere SK, Muralirangan MC, Muralirangan M (eds) (1997) The bionomics of grasshoppers, katydids and their kin. CAB International, Wallingford, UK, 529 pp Pfadt RE (2002) Field guide to western grasshoppers, 3rd edn. Wyoming Agricultural Experiment Station Bulletin 912. University of Wyoming, Agricultural Experiment Station, Laramie, WY, 288 pp Vickery VR, Kevan DKMcE (1985) The insects and arach nids of Canada. Part 14. The grasshoppers, crickets and related insects of Canada and adjacent regions. Agriculture Canada Biosystematics Research Institute Publication 1777, 918 pp

Grasshoppers The suborder Caelifera of the order Orthoptera.  Grasshoppers, Katydids and Crickets

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Grasshoppers and Locusts as Agricultural Pests

Grasshoppers and Locusts as Agricultural Pests Steven Arthurs Texas A&M University, College Station, TX, USA Orthoptera represent a large insect order with a worldwide distribution. Taxa in the superfamily Acridoidea are commonly either called grasshop pers or locusts. This division separates insects that readily aggregate in persistent bands or swarms in response to increases in intra-specific density (“locusts”) from those that show no such change in behavior (“grasshoppers”). Economically, socially and historically, locusts and grasshoppers are one of the most destructive pests. This century alone, there have been eight major plagues of the desert locust Schistocerca gregaria Forskål. Agricultural production across 29 million km2 in Africa and south-western Asia is threatened during plague periods. Although the desert locust is probably the most infamous of all acridoid pests, a suite of other locust and grasshopper species and species assemblages cause more frequent and cumulatively far more significant damage (Fig. 37) throughout Africa,

ustralia, the middle East and parts of Asia and A North and South America. In Southern Africa, the Brown Locust, Locustana pardalina Walker, has necessitated frequent widespread control measures over the last 45 years. In central and southern Africa, the Red locust, Nomadacris septemfasciata Serville; in Sudan, the tree locust, Anacridium melanorhodon Walker; in Madagascar, the migratory locust, Locusta migratoria migratoriodes Reiche and Fairmaire; and in semi-arid territories around the Mediterranean, the Moroccan locust, Dociostaurus maroccanus Thunburg, all require regular control measures to prevent the formation of migratory swarms. Although less mobile, grasshoppers such as Melanoplus sanguinipes Fabricius within North America, and Phaulacridium vittatumeastern SjÖstedt within Australian grasslands also require frequent control measures. Grasshopper complexes within the semiarid African Sahelian belt such as Aiolopus simulatrix Walker, Kraussaria angulifera Krauss, Acrotylus spp. and Oedaleus senegalensis Krauss, as well as those from the more humid West Africa zone, nota bly Hieroglyphus daganensis Krauss and Zonocerus variegatus L., represent a continuing threat to the food security of many rural communities. Even today, locusts and grasshopper outbreaks cause problems in every major continent of the world.

Outbreak Area Invasion Area

Grasshoppers and Locusts as Agricultural Pests, Figure 37 Outbreak and invasion areas of some A frican locusts. The locusts tend to persist in the outbreak areas, and when conditions for r eproduction are favorable the locusts multiply and spread to invasion areas. Desert locust, S chistocerca gregaria (left map), has a relatively large area of persistent habitation, consisting of most of northern Africa and the Arabian Peninsula, whereas African migratory locust, Locusta migratoria migratorioides (center map), and red locust, Nomadacris septemfasciata (right map) have small areas of origin in northwest and south central Africa, respectively.


Grasshopper and Locust Control The task of combating locust and grasshopper plagues usually falls to the national crop protection services in cooperation with regional control orga nizations such as the Desert Locust Control Organ isation for Eastern Africa (DLCO-EA). In recent years, this challenge has largely relied on the appli cation of synthetic chemical insecticides applied as baits or dusts, and more recently and more com monly, sprayed as ultra low volume (ULV) oil for mulations. The adoption of recent environmental monitoring technologies means the breeding habi tats of some migratory locusts and grasshoppers can be monitored using satellite imagery as well as aerial and ground surveys. Prevention of upsurges by early intervention is now normally the preferred approach. Modeling and recent improvements in forecasting have helped some governments, donors, researchers and locust officers predict potential outbreak periods and contain the problem of outbreaks at the source level. For example, the goal of the FAO’s Emergency Prevention System (EMPRES) for Transboundary Animals and Plant Pests and Diseases is to minimize the risk of locust plagues emanating from the central region of the desert locust distribution area through timely, environmentally sound interventions. However, in many rural areas, such as the Sahel, where access to pesticides is limited, traditional methods such as using smoke to repel arriving swarms or driving migrating hopper bands (immature locusts) into steep-sided ditches from which they cannot escape continue to be employed.

Chemical Control Locust and grasshopper control has evolved since the middle of the twentieth century. Until the 1970s, most control operations used persistent organo chlorine insecticides, with dieldrin favored for des ert locust control due to its effectiveness at low doses and in barrier sprays. There is circumstantial evidence supporting the effectiveness of such

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insecticides in suppressing plagues, with the period 1930 to 1960 representing the longest known interplague period for the desert locust. Dieldrin, how ever, is now banned in most countries due to environmental damage, negative effects on human and animal health and legislation originating in the USA concerning the stockpiling of toxic wastes. The use of carbamate and organophosphorous such as bendiocarb, malathion and fenitrothion began in the 80s, and more recently pyrethroid insecticide compounds such as deltamethrin have been used. However, although these products have a lower mammalian toxicity (most insecticides currently used for locust control are classified as “moderately hazardous” to human health based on acute oral and dermal toxicity studies in rats) their reduced persistence makes them less effective than dieldrin, and repeated applications are often necessary to achieve the same level of control. This is of particu lar importance in recession (permanent sites of locust breeding) areas where the requirements for repeat applications have resulted in increased con trol costs and amounts of pesticides used. Most recently, the phenylpyrazole compound fipronil has been promoted as a significant break-through in locust control, since it is effective and persistent at low doses. Fipronil was largely used in the half-million hectares treated against migratory locusts in Madagascar in recent years. The most recent desert locust upsurge (1986– 1989) and a simultaneous grasshopper outbreak in the West African Sahel triggered a massive emer gency response from the international community. The problem was again countered by large-scale spraying of swarms as well as feeding and breeding sites. Nearly 14 million hectares in Africa alone were sprayed for locusts while additional millions of hectares were sprayed in the Sahel for grasshop per control. Total donor assistance was approxi mately $250 million (U.S. dollars) and total costs including contributions from afflicted countries exceeded $295 million (U.S. dollars). However, the value of recent desert locust control campaigns has been called into question. While crop losses caused by swarms during plague conditions may be high

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(national pre-harvest losses due to grasshoppers in the Sahel have been estimated at 30% or more), overall yields may not be affected, as plague years are normally rainy and thus associated with better than average harvests. As well as concerns over economic viability, the environmental and human health conse quences of large-scale control campaigns using synthetic broad-spectrum insecticides in sensitive ecological areas (often representing breeding sources for many migratory acridid pests) has come under increasing scrutiny. For example, at the recommended rates for locusts and grasshoppers, fenitrothion is near the thresh old where it can cause immediate death among birds. Chlorpyriphos and pyrethroids may reduce the biodiversity of honeybees, spiders and aquatic insects. Fipronil is highly toxic to certain birds, fish, terrestrial and freshwater invertebrates. Human exposure to pesticides during control operations can present problems during handling, or as a result of spray drift from operations, especially where protective clothing is not available or there is an unwillingness to wear it under hot field conditions. Local resi dents and nomadic pastoralists may also be affected directly through spray drift or through contamination of livestock, water or foodstocks.

Biological Control There are numerous reports of natural enemies of grasshoppers and locusts. The principle groups consist of vertebrate and invertebrate predators which attack eggs, nymphs and adult insect, as well as insect parasitoids, parasitic nematodes and pathogens. In addition to natural control, recent research has led to the development of biopesti cides based on entomopathogenic fungi. Most locusts and grasshopper predators are generalists, and will attack a range of species, rather than any single host. Both nymphs and adults are attacked by various arthropods such as scorpions, spiders and solifugids and predaceous

insects like asilid flies, sphecid wasps, ants, mantids and ant lions, and also by many species of lizards, snakes and birds. Eggs are also attacked by larvae of bombyliid flies and various Coleoptera, chiefly tenebrionid larvae. Additionally, a number of naturally occurring diseases also suppress locust and grasshopper populations worldwide, includ ing descriptions of spectacular epizootics by the Entomophaga grylli complex of fungal pathogens. There are, however, relatively few in-depth studies on the impact of grasshopper and locust natural enemies, especially for tropical species. Although they merit conservation, indige nous natural enemies are often killed by non- selective chemical insecticides. This aspect, plus the concerns over the human health consequences of large-scale applications of chemical pesticides during recent locust campaigns, has led to recom mendations by the World Bank and others to place locust and grasshopper control within the context of integrated pest management (IPM) programs. This has increased pressures to intro duce biological control. Although arthropod predators and parasitoids may hasten the end of plagues, apart from possibly controlling static grasshopper populations they cannot be manipulated, and migratory pests such as the desert locust are poor targets for classical biological control. However, pathogens can be manipulated for use as biological pesticides. Many locusts and grasshoppers are migratory pests and have characteristics amenable for control with microbial agents, (i) feeding and breeding take place outside the crop, often in conservation areas where high natural mortality can be expected to occur; (ii) as there is often public funding for con trol, high environmental values are involved in the purchasing decisions. The major pathogen groups that have received interest as biological control agents of locusts and grasshoppers are bacteria, protozoa, entomopox viruses and fungi. The characteristics needed for a good agent include cheap and easy production, tox icological safety, host specificity and (given the exis tence of highly developed application technology)


the ability to be formulated and applied using cur rently available equipment. Commercial formula tions of entomophilic nematodes are available, but their high cost and water requirements during application and infection restrict their use in most regions against locusts and grasshoppers. The use of entomopathogenic bacteria against locusts and grasshoppers has received some atten tion. The non-sporeforming Serratia marcescens Bizio and Pseudomonas aeruginosa (Schroeter) Migula have high pathogenicity in laboratory cultures. However, disappointing field results and concerns over mammalian safety have precluded further investigation. Though it has a well-devel oped production technology, efforts to find strains of Bacillus thuringiensis that produce endotoxins with pathogenicity against locusts or grasshoppers have not yet been successful. Various protozoa are known to infect locusts or grasshoppers. Among the Microsporidia (Phylum Microspora), Nosema locusta Canning has received the most attention, possibly due to its easy and efficient in vivo pro duction characteristics. N. locusta has been the subject of a number of inundative field trials against grasshoppers where its spores are typically incorporated into bait carriers. However, the release of such pathogens generally only causes modest reductions. Nevertheless, because N. locusta may reduce the rates of host development, fecundity and feeding, it is considered by some to be a candidate for long-term population suppres sion and low impact maintenance in IPM strate gies. N. locusta is registered for grasshopper control within conservation rangeland areas in the USA. The use of entomopox viruses (EPVs) against locusts and grasshoppers is also receiving attention. The most extensively studied is the rangeland grasshopper Melanoplus sanguinipes (Fig. 38) virus (MsEPV), which is considered to have some potential as a biocontrol agent on Canadian rangelands. However, field studies dem onstrating effective control are limited and restric tions to their production in vitro and ability to be formulated in spray carriers suggest that using EPVs against locusts and grasshoppers currently

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Grasshoppers and Locusts as Agricultural Pests, Figure 38 Migratory grasshopper, Melanoplus sanguinipes (Fabricius), an American g rasshopper with locust-like dispersive behavior. (artwork, J. Mottern)

remains unlikely. Further investigations into the infectivity of the baculoviruses, such as the nuclear polyhedrosis viruses (NPVs), which have better production characteristics, may open up new opportunities. Among pathogens, the entomopathogenic fungi are the easiest to be manipulated as biopesti cides. They have the advantage over other patho gens because they are able to infect through the insect cuticle, thus avoiding the necessity of pro viding bait. Spores (conidia) of fungal pathogens are also lipophilic, favoring their formulation in the oil-based carriers that are typically applied as a low volume spray in locust and grasshopper con trol campaigns. Over 700 species of fungi from approximately 90 genera are pathogenic to insects; however, only the deuteromycetes Metarhizium spp. and Beauveria spp. (class Hyphomycetes) currently fulfill the criteria required for a successful inundative biological control agent. The entomophthoralean fungi, in particular members of the Entomophaga grylli (Fres.) Batko species complex, represent a group of obligate pathogens found in most areas of the world that have frequently been recorded decimating populations following epizootics. Although species in the E. grylli complex have been used successfully in some classical biocon trol introductions in the USA, difficulties with host specificity and in vitro mass production limit their application for inundative release. Recent research programs have developed the fungal pathogen Metarhizium anisopliae var. acridum for the control of locusts and grasshop pers in Africa and Australia, and Beauveria bassiana

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Grasshoppers, Katydids and Crickets (Orthoptera)

for grasshopper control in Canada. Currently the development of microbial-based pesticides follows the same procedures of testing and registration as the chemical ones. Ongoing technological research in these programs has resulted in significant advances in the in vitro production, storage and formulation characteristics of such pathogens and recently has been the focus of commercial scale efforts to produce available mycopesticide prod ucts. Accordingly, applied using conventional spraying equipment at rates of 0.5–5 l per hectare, mycopesticides have proven at least as effective as chemical insecticides against locusts and grasshop pers in a variety of ecological zones.  Grasshoppers, Katydids and Crickets  Diseases of Grasshoppers and Locusts  Desert Locust Plagues

References Carruthers RI, Onsager JA (1993) Perspective on the use of exotic natural enemies for biological control of pest grasshoppers (Orthoptera: Acrididae). Environ Ento mol 22:885–903 Chapman RF, Joern A (1990) Biology of grasshoppers. Wiley, New York, NY Goettel MS, Johnson DL (eds) (1997) Microbial control of grasshoppers and locusts. Mem Ent Soc Can 171, 400 pp Joern A, Gaines SB (1990) Population dynamics and regula tion in grasshoppers. pp. 415–460 in Chapman RF, Joern A (eds) Biology of grasshoppers. Wiley, New York, NY Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas MB (2001) Biological control of locusts and grasshoppers. Annu Rev Entomol 46:667–702

Grasshoppers, Katydids and Crickets (Orthoptera) John L. Capinera University of Florida, Gainesville, FL, USA Members of the order Orthoptera are found at nearly all latitudes, though they are primarily trop ical insects as judged by species diversity, which is greatest in warm areas. Most are known for their

well-developed hind legs and jumping abilities, but many are noteworthy because they “sing,” particu larly at night. Orthopterans, or at least the grass hoppers and locusts, are often considered synonymous with “plagues” due to the devastating damage they inflict during periods of abundance. Orthopterans are usually medium-sized to large insects. Not surprising for a large taxon, the wing condition varies considerably. They may be apterous (wingless), micropterous (short-winged and incapable of flight), or macropterous (longwinged and capable of flight). When bearing wings, which is the usual condition, they usually bear two pairs, and sometimes are capable of very strong flight. The name Orthoptera means “straightwinged” and refers to the thickened front wings or tegmina. The front wings bear numerous veins, and function more for protection than as an aid for flight. The front wings often are pigmented with a color or pattern that provides camouflage. Sometimes the front wings are quite broad and modified to resemble leaves. The hind wings usu ally are broader, folded like a fan, and though sometimes brightly colored, often are unpig mented. The wings, even if short, are often involved in sound production. Species inhabiting open des ert and grasslands tend to be strong fliers, those inhabiting woodlands, islands and mountaintops tend to be flightless. In a few taxa, the second pair of wings is absent. In several groups, including many crickets, katydids and pygmy grasshoppers, the front wings are shorter than the hind wings. Orthopterans possess chewing mouthparts. Their eyes are large, and ocelli are usually present and three in number. The antennae usually are narrow, but vary in length: short in suborder Cae lifera and long in suborder Ensifera. The thorax is large, and the saddle-shaped pronotum bears large lateral lobes that serve as the sides of the thorax. The legs are long. The hind legs are most often enlarged, especially the hind femora, and allow the insects to jump when alarmed. The tarsi have 1–4 segments and normally end with a pair of claws. Contrary to popular belief, normal locomotion is by walking, not jumping. Sometimes the front legs


are enlarged, either for digging or for prey capture. The abdomen consists of about 11 segments and usually is free of notable structures other than the cerci and the ovipositor. Tympana, or hearing organs, are commonly present in these insects. In the suborder Caelifera, they are located on the side of the first abdominal segment. In the suborder Ensifera, they are found on the front tibiae. Orthopterans display gradual metamorpho sis. After hatching from the egg, the immature stage (nymph) feeds and grows, molting four or more times before reaching the adult stage. The number of molts varies considerably among taxa, and is commonly 4 or 5 in grasshoppers, but gen erally more than 10 in crickets. As in all exoptery gote (wings developing externally) insects, the nymphs greatly resemble the adults, both in appearance and in mode of life. There is an excep tion, however. Grasshoppers and katydids hatch ing in the soil actually have a pronymphal stage preceding the first instar. This initial form is called the vermiform (worm-like) larva, and consists of the young nymph encased in a cuticular covering. The vermiform larva wriggles through the soil to the surface, and then the nymph escapes the cov ering, beginning its above-ground existence as a young hopper. The vermiform stage is not counted in the instar numbering system because it is just the first instar within a sheath. Nymphs and adults can be difficult to distin guish (Fig. 39). The principal differences in appear ance are the imperfectly developed wings and genitalia of nymphs. Nymphs have external wings pads that enlarge with each molt. Their shape is useful for determining the instar. In Acrididae, Tettigoniidae and Gryllidae, the wing pads initially point downward, but part-way through nymphal development, the orientation switches and the wing pads point upward or backward. With wingless or short-winged species, distinguishing the instar is more difficult. At maturity, the males court the females (rarely the roles are reversed) and copulate. In the suborder Caelifera, the male deposits the sperm internally. In the suborder Ensifera, the males of some taxa attach a

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s permatophore (packet containing sperm) exter nally at the female’ s genital opening, whereas oth ers display the internal sperm deposition system. In both cases, the female stores sperm until ovipo sition (egg deposition), when fertilization occurs. Insects with gradual metamorphosis have the ability to regenerate lost limbs. If a grasshopper loses an antenna or leg as a young nymph, the miss ing appendage is regrown, in part, at the next molt. If the damage occurs early enough in the develop ment of the insect, the lost appendages may be completely regenerated. These insects also shed limbs readily, a process called autonomy. If a leg is grasped by a predator or caught in a spider web, the leg may be shed, allowing the insect to escape. The order Orthoptera is usually divided into two suborders: Caelifera and Ensifera. The suborder Caelifera consists of the grasshoppers and locusts (including the deceptively named pygmy

Grasshoppers, Katydids and Crickets (Orthoptera), Figure 39 Typical nymphal and adult stages of a grasshopper, Schistocerca americana (Thomas). Note that they are similar in body form, with the primary distinguishing factor the abbreviated wings of the nymph (top). Shown is the sixth instar, which bears the largest wings prior to the molt to the adult. Unfortunately, many grasshopper species possess such abbreviated wings as adults, making age determination difficult. Some possess both short-winged and long-winged forms. A few species show no development of wings. (images from United States Department of Agriculture).

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mole “crickets,” which are now recognized to be derived from grasshoppers, not crickets). The sub order Ensifera consists of the katydids and crickets (including the true crickets, mole crickets, camel crickets and Jerusalem crickets). There are many easily-recognizable groups within the order, and there is little dispute about most of these divisions and their phylogenetic relationships. However, there is considerable disagreement over the placement of the groups within the taxonomic hierarchy, i.e., whether or not they should be regarded as super families, families or subfamilies. There are more than 25,000 species of Orthoptera in the world and, depending on the author of the classification sys tem, up to about 35 families within the order.

Suborder Caelifera The Caelifera usually have enlarged hind femora, short antennae, and tarsi with three or fewer seg ments. The antennae are normally threadlike, some times flattened, and occasionally enlarged at the tip. Tympana are often present, and are located on the sides of the first abdominal segment. Wing length is variable, but the cerci and the ovipositor are always short. Most species are diurnal, and phytophagous. Some primitive caeliferans, such as Eumastacidae, Tetrigidae and Tridactylidae, feed on more primi tive plants, such as ferns and algae. Some Caelifera species inhabit areas of bare soil, many are associ ated specifically with grasses or broadleaf plants, while others dwell in trees. Visual and acoustic dis plays are part of the mating ritual of many species, and one or both sexes may produce sound. Sound production usually results from rubbing the hind legs against the front wings (called stridulation), although some groups stridulate by rubbing the front wings against the hind wings. Wing snapping in flight (called crepitation) also can occur. Eggs are normally deposited in the soil in clusters, and usu ally within a protective foamy structure called an egg pod. Univoltine and multivoltine species occur, with a tendency for greater multivoltinism in the warmer latitudes.

Following is one possible classification system for Caelifera, which basically follows Otte’ s Orthoptera Species File. Subfamilies are not given in the following list except in the case of Acrididae, the largest and most important family. Suborder: Caelifera Superfamily: Acridoidea Family: Acrididae Subfamily: Acridinae Subfamily: Calliptaminae Subfamily: Catantopinae Subfamily: Conophyminae Subfamily: Coptacridinae Subfamily: Cyrtacanthacridinae Subfamily: Dericorythinae Subfamily: Egnatiinae Subfamily: Eremogryllinae Subfamily: Euryphyminae Subfamily: Eyprepocnemidinae Subfamily: Gomphocerinae Subfamily: Hemiacridinae Subfamily: Illapeliinae Subfamily: Lithidiinae Subfamily: Melanoplinae Subfamily: Oedopodinae Subfamily: Ommatolampinae Subfamily: Oxyinae Subfamily: Podisminae Subfamily: Proctolabinae Subfamily: Rhytidochrotinae Subfamily: Spathosterninae Subfamily: Teratodinae Subfamily: Tropidopolinae Subfamily: Trybliophorinae Family: Charilaidae Family: Lathiceridae Family: Lentulidae Family: Ommexechidae Family: Pamphagidae Family: Pauliniidae Family: Pyrgomorphidae Family: Romaleidae Family: Tristiridae Superfamily: Eumastacoidea Family: Eumastacidae


Family: Proscopiidae Superfamily: Pneumoroidea Family: Pneumoridae Family: Tanaoceridae Family: Xyronotidae Superfamily: Trigonopterygoidea Family: Trigonopterygidae Superfamily: Tetrigoidea Family: Tetrigidae Superfamily: Tridactyloidea Family: Cylindrachetidae Family: Regiatidae Family: Ripipterygidae Family: Tridactylidae

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Subfamily Acridinae (Silent Slantfaced Grasshoppers) Grasshoppers in this subfamily have a slanted face and flattened, sword-shaped antennae (Fig. 40). Acridines lack a spine (the prosternal spine) between the front legs. The hind wings are colorless or nearly so. Acridinae are very similar in appearance to the

Following is information on some of the important families and subfamilies within the suborder Caelifera:

Family Acrididae This is the largest family of the Orthoptera, and consists of the “true” grasshoppers and locusts. It is not uncommon to see other approaches to the classification of this family. The acridids are small to large in size, and stout to slender in general appear ance. Their color is variable, but green and brown are common. The antennae and the pronotum are elongate and distinct. The legs are long, the hind legs are especially long and the femora is stout. The wings are variable in length, but often long. Acridids possess tympana, and sometimes produce sound. They are found in nearly all habitats. They are gen erally phytophagous, but vary in specificity. Eggs are deposited within pods in the soil; pods may contain three to 200 eggs, depending on the species. Some subfamilies, such as Catantopinae, Gomphocerinae, Melanoplinae and Oedopodinae, are large and contain 500 or more species. Other subfamilies possess as few as one to five species. Some subfamilies are quite limited geographically and are found only on a single continent. Other taxa are found across Africa, Europe, Asia and Australia, or even more broadly (though they are absent from Antarctica).

Grasshoppers, Katydids and Crickets (Orthoptera), Figure 40 Representative grasshoppers in the family Acrididae (top to bottom): a birdwing grasshopper, Schistocerca nitens Thunberg (subfamily Cyrtacanthacridinae); stridulating slantfaced grasshoppers, Opeia obscura ( Thomas), Psoloessa texana (Scudder), and Achurum sumichrasti Saussure (subfamily G omphocerinae); a New World spurthroated grasshopper, Melanoplus differentialis Thomas (subfamily Melanoplinae). (images from Arizona Agricultural Experiment Station).

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stridulating slantfaced grasshoppers (subfamily Gomphocerinae), but as the common name sug gests, members of this subfamily lack stridulatory pegs on the hind femora of males and thus do not produce sound. This subfamily is most abundant in Africa and Eurasia, though it occurs widely. Over 400 species are known.

Subfamily Calliptamine These small to medium-sized grasshoppers are fairly typical in most respects, but the males are distinguished by their large, forceps-like cerci. The antennae are threadlike. The face is vertical or curved, but not strongly angled. The wing length is variable. Tympana are present, though sound pro duction is limited to mandibular stridulation. They occur in Europe, Africa and Southeast Asia. About 100 species are known.

Subfamily Catantopinae (Old World Spurthroated Grasshoppers) These typical-appearing grasshoppers vary con siderably in size, and in wing structure. Their antennae are threadlike. The tympana generally are present though sound production is unknown. A prosternal spine is present. They greatly resem ble Melanoplinae, and are separated mostly on the basis of geography. Cantantopines occur in Europe, Asia and Africa. Over 1,000 species are known.

num). The antennae usually are threadlike. The head is not especially large in size, and these grass hoppers do not appear to be especially heavy- bodied. In most genera, the head has a vertical orientation. These grasshoppers generally have long wings. The genus Schistocerca contains espe cially long-winged, strong fliers. Cyrtacanthacri dine grasshoppers do not make sounds during flight; nor do they stridulate. The habitat preferences of these grasshoppers are highly variable. Dietary habits also vary, but generally these insects are polyphagous. This group contains many important pests. Many of the grass hoppers are called “locusts” because of the swarming behavior found in this group. These grasshoppers are found throughout the world, but the greatest diversity occurs in Africa. In Schistocerca, however, the greatest diversity is in Central and South America.

Subfamily Eyprepocnemidinae These insects are fairly typical in appearance, and variable in size. The antennal shape also varies. They possess a prosternal spine. The wing length is variable. The typana are present, though sound production is limited to mandibular stridulation. These insects are found principally in Africa, but also in southern Europe and Southeast Asia. About 175 species are known.

Subfamily Cyrtacanthacridinae

Subfamily Gomphocerinae (Stridulating Slantfaced Grasshoppers)

The treatment of this subfamily varies greatly among authors. Sometimes the subfamily name Cyrtacanthacridinae is used to include a great number of genera and species. Here, it is restricted to about 75 genera, the most important of which is Schistocerca, the birdwing grasshoppers. These grasshoppers bear a prosternal spine ventrally between the front legs (on the proster

Grasshoppers in this subfamily tend to have slender bodies and long, slender legs. Their heads are elongate and often cone-shaped, usually with a highly slanted face. The hindwings are not color ful. Gomphocerines often have relatively short wings, rendering them incapable of sustained flight. When disturbed, these grasshoppers leap and use their wings, but their wings often do little


more than increase the distance jumped. They do not make sounds during flight. This does not mean that these grasshoppers are silent. They can stridu late by rubbing the inner surface of the hind femur on the edges of the forewing while resting. Because the males of this subfamily usually have a row of stridulatory pegs on the inner surface of the hind femora, they are also known as toothlegged grasshoppers. The habitat of gomphocerines tends to be tall grasses in open fields. The form and color of many species allows them to blend in with stems and blades of grass, making them difficult to detect until they move. Most species feed predominantly on grasses. They are found throughout the world, and species number nearly 1,000.

Subfamily Melanoplinae (New World Spurthroated Grasshoppers) These grasshoppers bear a prosternal spine, the basis for their common name. For this reason, they are often grouped into the Cyrtacanthacrid inae. The antennae usually are threadlike. The head is not especially large, and they do not appear to be especially heavy-bodied. In most genera, the head has a vertical orientation. The wing length is variable. Melanoplines do not make sounds during flight; nor do they stridu late. The habitat of these grasshoppers is highly variable. Thus, their dietary habits vary. This group contains many important crop and pasture pests. During periods of drought, they often attain high densities and cause considerable damage. They are found in North, Central and South America. Over 600 species are known.

Subfamily Oedipodinae (Bandwinged Grasshoppers) The bandwinged grasshoppers are usually heavy bodied, and bear enlarged hind legs. The head of these grasshoppers often appears enlarged and

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broadly rounded. The orientation of the face is nearly vertical. Bandwinged grasshoppers lack a spine between the front legs. The bandwinged grasshoppers tend to be gray or brown in color, and often are mottled with darker spots. The fore wings frequently bear distinct or indistinct trans verse bands. The bandwinged grasshoppers usually bear bright colors, but this may not be obvious. The hindwings are often yellow, orange, or reddish basally, with a broad black band crossing near the center of the wing. The colorful hindwings are hidden by the front wings except when in flight. The males produce sound in flight. The oedipodine grasshoppers normally are associated with open, sunny areas, and particularly with bare soil where their coloration provides excellent camouflage. About 800 species are known throughout the world.

Subfamily Oxyinae These are small to medium-sized grasshoppers, and their body has a smooth integument. They do not stridulate, and they lack tympana. The wing length is variable. The antennae are threadlike. An interesting characteristic of these grasshoppers is that the hind tibiae usually are expanded distally, which is thought to be an adaptation for swim ming. The female’ s ovipositor valves are serrate or spined. Oxyinids are found in Africa, Europe, Southeast Asia and Australia, but are most abun dant in humid, tropical habitats, especially wet environments. About 175 species are known.

Family Eumastacidae This is one of the more primitive forms of grass hoppers, and they are sometimes referred to as monkey grasshoppers. The common name is derived from their agility when moving through vegetation. They tend to be small to medium in size. These insects lack tympana. They may bear wings, or be wingless. The legs, when the insect is

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at rest, are often held away from the body. The tarsi are three-segmented. The antennae usually are variable in shape, unusually short, and often bear a small tubercle on an apical segment, called the antennal organ. They lack a prosternal spine. These are tropical insects, and are absent from Europe and northern Asia. In North America, they are found only in the warm-weather Southwest. They feed on ferns, algae and gymnosperms. Most of the approximately 750 known species occur in the Old World.

Family Pamphagidae

Family Romaleidae This group, also known as lubber grasshoppers, is sometimes considered to be a subfamily of Acridi dae. It is distinguished, in part, by having a spine on both the inner and outer surface at the tip of the hind tibiae. Other grasshoppers (Fig. 41) may have moveable spurs, which resemble spines, but lubbers also have immovable spines at this location. Lubber grasshoppers also bear a prosternal spine. Lubber grasshoppers often are large, robust, colorful and usually bear short wings. The name “lubber” is derived from the heavy-bodied appearance and clumsy behavior of these insects. The shape of the

Generally medium or large in size, these grasshop pers possess a prosternal spine or elevated process. The pronotum is often elevated, sometimes form ing a distinct crest. The wing development is vari able. The tympana are either present or absent, and stridulation occurs. These grasshoppers often are cryptically colored, allowing them to blend with rocky soil and sand. These grasshoppers are found in Africa, southern Europe and Asia. Over 300 species are known.

Family Pyrgomorphidae These insects have a conical head, usually with a very slanted face. They have a relatively soft body and weak integument. The antennae are threadlike or flattened. A prosternal spine or elevated process on the prosternum is present. Often brightly col ored, they also excrete body fluids from between the first and second abdominal segments that pro vides a form of chemical protection that is vari ously repellent or poisonous. Wing length varies in this group. These grasshoppers usually are asso ciated with grass vegetation in tropical and sub tropical areas. They are known mostly from eastern Africa, Southeast Asia, Australia, and Central and northern South America – basically everywhere except North America. Over 400 species are known in this family.

Grasshoppers, Katydids and Crickets (Orthoptera), Figure 41 Representative grasshoppers in the family Acrididae (top to bottom): bandwinged grasshopper, Tropidolophus formosus (Say) and Xanthippus corallipes Haldeman ( subfamily Oedipodinae). Representative grasshopper in the family Romaleidae: a lubber grasshopper, Brachystola magna Girard. (images from Arizona Agricultural Experiment Station).


head, though variable, is usually broadly rounded. The hind femora are enlarged. When disturbed, lubber grasshoppers may hiss and spread their wings. The males also may use their wings to stridu late. The forewings and hindwings sometimes are brightly colored. The lubber grasshoppers are found in North, Central and South America, with their abundance greater in the southern latitudes. About 500 species of R omaleidae are known.

Family Tanoceridae These grasshoppers, known also as desert longhorned grasshoppers, are medium in size and wingless. The threadlike antennae are relatively long in males and shorter in females. They are nocturnal, and are not often found by collectors. They are known only in the southwestern region of North America. Only four species from this family have been described thus far.

Family Tetrigidae The pygmy grasshoppers (Fig. 42) are also known as groundhoppers and grouse grasshoppers. They are distinguished by their small size, usually 6–16 mm in length; their dull, cryptic coloration, usu ally brownish gray, gray, or black or mottled, but never green; their prominent eyes; and especially their greatly elongated pronotum, which often extends backward to the tip of the abdomen and ends in a sharp point. The antennae are relatively short. They may be long- or short-winged, or

Grasshoppers, Katydids and Crickets (Orthoptera), Figure 42 Representative of the family Tetrigidae: (top) a pygmy grasshopper, Tetrix subulata (Linnaeus).

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ingless. Like other grasshoppers, their hind w femora are enlarged. Both sexes stridulate, and mating is a very brief process. They apparently feed on algae and possibly other organic matter in the soil. They often are found in marshy areas and at the margins of water, or in moss covered habitats. Some can descend into water, carrying an air bub ble with them. They deposit loose clusters of eggs in wet soil. They tend to live in small groups in a more or less gregarious condition. They are diffi cult to collect unless special effort is made to sweep close to the soil. In some environments, they may be common. Tetrigids are found throughout the world, but they are most abundant in Southeast Asia. About 1,200 species are known.

Family Tridactylidae These very small insects, usually measuring only 4–10 mm in length, are grasshoppers despite their common name: pygmy mole crickets. The antennae are relatively short, as with acridid grasshoppers. However, they possess some unusual features that differentiate them from other grasshoppers. They resemble mole crickets because they have front legs that are adapted for digging in soil and an arched pronotum. The tip of the abdomen bears a set of bristly appendages that resemble cerci, so they appear to have two sets of cerci. The hind tarsi possess plates that help them move on water, an important feature because they frequent the sandy edges of streams and ponds. They are quite good at walking on the water surface. Their diet consists mostly of organic material such as algae, possibly fungi, nematodes and bacteria, often ingested along with sand particles. Tridactylids are found through out the world, but seem to flourish in tropical and subtropical locations. Nearly 200 species are known.

Suborder Ensifera The ensiferans, like the caeliferans, are jumping insects. However, their legs tend to be longer, and the

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hind femora less enlarged, than the caeliferans. Their most distinctive feature is their long, threadlike antennae, which normally exceed the length of the body. The tarsi are three or four-segmented. The tympana, when present, are located on the front tib iae. Stridulation is common, and normally is caused by rubbing one front wing against the other. Some times the wings are slightly elevated when singing, but this behavior varies among taxa. Females bear a long sword-shaped or cylindrical ovipositor. The wing length is variable, but often even the longwinged species are weak fliers. Most species are noc turnal, and dietary habits vary from carnivory to phytophagy, but omnivory is common. Ensiferans often are associated with thick vegetation, and are most common in mesic areas. The superfamily Tet tigonioidae, in particular, frequent vegetation almost exclusively. The Gryllacridoidea and Grylloidea, in contrast, often seek shelter in crevices, tunnels beneath the soil, or tree holes. Acoustic displays are an important part of the mating ritual of many spe cies. Eggs are deposited singly, though several may be laid at the same location. Unlike grasshoppers, katydids and crickets do not produce egg pods. Some crickets and katydids deposit eggs on or in vegetation, others in soil. Following is one possible classification system for Ensifera, based on that found in Otte’ s Orthoptera Species File. Subfamilies are not given, except in the case of the Tettigoniidae and Gryllidae, the most important groups. Suborder: Ensifera Superfamily: Tettigonioidea Family: Haglidae Family: Tettigoniidae Subfamily: Austrosaginae Subfamily: Bradyporinae Subfamily: Conocephalinae Subfamily: Hetrodinae Subfamily: Lipotactinae Subfamily: Listroscelidinae Subfamily: Meconematinae Subfamily: Microtettigoniinae Subfamily: Phaneropterinae Subfamily: Phasmodinae

Subfamily: Phyllophorinae Subfamily: Pseudophyllinae Subfamily: Saginae Subfamily: Tettigoniinae Subfamily: Tympanophrinae Subfamily: Zaprochilinae Family: Prophalangopsidae Superfamily: Gryllacridoidea Family: Gryllacrididae Family: Cooloolidae Family: Anostostomatidae Family: Stenopelmatidae Family: Schizodactylidae Family: Rhaphidophoridae Superfamily: Grylloidea Family: Gryllidae Subfamily: Brachytrupinae Subfamily: Cachoplistinae Subfamily: Eneopterinae Subfamily: Euscyrtinae Subfamily: Gryllinae Subfamily: Gryllomiminae Subfamily: Itarinae Subfamily: Malgasiinae Subfamily: Nemobiinae Subfamily: Oecanthinae Subfamily: Pentacentrinae Subfamily: Podoscirtinae Subfamily: Pteroplistinae Subfamily: Sclerogryllinae Subfamily: Trigonidiinae Family: Gryllotalpidae Family: Mogoplistidae Family: Myrmecophilidae

Following is information on some of the important families and subfamilies within the suborder Ensifera.

Family Anostostomatidae This unusual group is known as king crickets and wetas. They are large, stout, and have oversized heads. Nearly all are wingless, but a few have fully formed wings. The mandibles and hind legs are


sometimes enlarged. they are nocturnal. King crickets seem to be omnivores, though wetas are herbivores. To deter avian and reptilian predation, wetas raise their hind legs, exposing long spines. However, hiding below-ground is the principal defense. Wetas possess large tympana on their front legs. wetas and king crickets stridulate, though their sound production is a relatively primitive, intermediate stage in the evolution of acoustic signaling. They also transmit vibratory signals through their substrate. Tree wetas, but not king crickets, maintain harems of females and possess enormous mandibles that they use for fighting with competing males, whereas giant weta males freely compete for females without aggression. The king crickets and wetas occur in a variety of habitats. About 40 king crickets are known from southern africa, and 60 from australia and New Zealand. Wetas occur in Australia and New Zealand. Wetas are at risk of extinction because they are relatively defenseless against imported animals such as rats.

Family Cooloolidae The cooloolids are called cooloola monsters due to their unusual appearance. These insects, though considered to be ensiferans, have short (10-seg mented) antennae. They possess a large abdomen, and relatively short legs and with a muscular, hump-backed appearance. They resemble king crickets and wetas (Anastostomatidae) and to a lesser degree Jerusalem crickets (Stenopelmati dae). These are not leaping insects. Also, they do not tunnel, rather, living below ground where they “swim” through sandy soil. This very small (three species) and unusual family is known only in Australia.

Family Gryllacrididae Some gryllacridids are known as leaf-rolling crick ets, but not all species exhibit this behavior. They produce silk from glands in their mouthparts, and

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use it to tie leaves. The leaf rolls provide daytime shelters, but some species inhabit burrows in soil. The common name raspy crickets has also been suggested. This name stems from a raspy sound produced during defense. These are robust crick ets, and can be fairly large, attaining 15 cm in length. They may be winged or wingless. The antennae are as long as or longer than the body. They are distinguished by the lateral lobes of the tarsi, and the presence of pegs on the inner surface of the hind femora that rub against the abdomen. They are not as long-legged as the cave and camel crickets (Rhaphidophoridae), and are soft bodied as compared to the king crickets and wetas (Anas tostomatidae). This group is not well known, but all are thought to be nocturnal. They occupy varied habitats, and their dietary habits include herbivory, omnivory and carnivory. They are found widely in southern Africa, southwestern Asia, Australia, the Pacific region and South America. Few species are known from the northern hemisphere. Over 600 species are known around the world.

Family Gryllidae Most crickets are compact and large-headed insects. Their antennae are long, usually reaching the tip of the abdomen or beyond. The forewings, when fully formed, are relatively broad, and flat tened over the abdomen. Many species are wing less or short-winged. The front wings may be shorter than the hind wings, and in males, may function principally as acoustic devices. Many species can only be recognized by their calling behavior. Some species are mute. Tympana are found on the front tibiae. The ovipositor is long, thin and tubular. The body color is dull, usually pale, brownish or black. Long cerci are found near the tip of the abdomen and are similar in both sexes. Gryllids are often considered to be omnivorous, which is largely true, though indi vidual species vary from herbivorous to nearly carnivorous. About 3,000 species occur in this large family.

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Subfamily Eneopterinae (Bush Crickets) The bush crickets are medium sized and slender. The body usually has a fine covering of hairs. They frequent vegetation rather than soil. About 200 species are known from this subfamily.

wing length varies considerably. They can call dur ing the day and night, and tend to dwell belowground. Many species are similar morphologically and are distinguished by their calling behavior. They are omnivorous. About 500 species are known and are distributed widely in the world. A few species are considered to be crop pests.

Subfamily Gryllinae (Field Crickets)

Subfamily Nemobiinae (Ground Crickets)

These common crickets (Fig. 43) are similar to the ground crickets (Nemobiinae), but usually are medium in size rather than small. They tend to be heavy-bodied and brown or black in color. Their

The ground crickets tend to be small, and often bear a sparse covering of hairs. Tympana are present on the front tibiae. The wing length is variable. They often are uniformly brown, which

Grasshoppers, Katydids and Crickets (Orthoptera), Figure 43 Representative of the family Anostostomatidae (top) a weta, Hemideina crassidens (Blanchard) (image from Larry Field); the family Gryllidae: (bottom left) a field cricket, Gryllus veletis (Alexander and Bigelow) (subfamily Gryllinae); and (bottom right) a ground cricket, Allonemobius griseus E.M. Walker (subfamily Nemobiinae) ( images from Lyman Entomological Museum).


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allows them to blend in well with their terrestrial environment. These insects can be quite numerous in pastures and woodlands, and can be active during the daylight hours. They are omnivorous. About 200 species are known around the world.

Subfamily Oecanthinae (Tree Crickets) The tree crickets (Fig. 44) are slender and pale col ored, often greenish or whitish. The males tend to have broad front wings. Most are quite vocal. They inhabit trees, shrubs and weedy fields. Some cause injury to trees and shrubs by depositing their eggs within twigs. Tree crickets tend to be predatory. They are found throughout the world, but are most numerous in Africa and South America. About 175 species occur in this subfamily.

Subfamily Trigoniinae (Sword-Tail Crickets) These insects tend to be small, and pale in color. The wing length is variable, though the wings can be quite long when present. Tympana are present. Sword-tail crickets often are found in vegetation adjacent to water, and do not normally frequent the soil surface. About 275 species are known throughout the world.

Family Gryllotalpidae Among the most easily distinguished orthopterans, the mole crickets bear wide forelegs modified for digging. Both the femora and tibiae are flattened, with the tibiae bearing enlarged teeth or “dactyls.” The hind legs are not markedly enlarged. The antennae are shorter and thicker than in many ensiferans. The oval pronotum is disproportionately large and sturdy. They are often, but not always, long-winged. The ovipositor is not apparent. These insects dwell below-ground during the day, often

Grasshoppers, Katydids and Crickets (Orthoptera), Figure 44 Representative of the family Gryllidae, (top left) a tree cricket, Oecanthus nigricornis (subfamily Oecanthinae); the family Gryllotalpidae, (top right) a mole cricket, Scapteriscus sp.; and (bottom) a mole cricket, Neocurtilla hexadactyla (images Lyman Entomological Musuem except Scapteriscus from Florida Division of Plant Industry).

emerging in the evening to sing or eat. They sing from specially constructed acoustical chambers, constructed in the soil, that expand as they open to the outside like the end of a trumpet. This design serves to amplify their call. Some species are mute. Mole crickets create deep permanent burrows, but also superficial foraging tunnels. The eggs are deposited in special egg chambers within the bur rows. Their dietary habits range from carnivorous to phytophagous, but some are important vegetable and pasture pests. Three species of Scapteriscus from South America were accidentally introduced into southeastern North America and have caused

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considerable damage. Less than 100 species are known from this family.

Family Mogopistinae These insects are called scaly crickets. Resembling silverfish, these small crickets tend to be shortwinged, flat and slender. Their name is derived from the presence of translucent scales covering most of their body. They are mostly tropical in dis tribution and seem to favor areas near water. Over 350 species are known.

Family Myrmecophilidae This is a small family of very small, wingless, oval and flattened crickets that inhabit ant nests. They cannot live independently from the ants. The eyes are reduced, though the cerci are pronounced. The tympana are lacking. The ovipositor is shortened and stout. The hind femora are broad. These unusual insects feed on secretions produced by ants. Apparently, they are taken to be ants by their hosts. Some species are parthenogenetic. Only about 50 species are known.

Family Rhaphidophoridae The camel crickets (Fig. 45) are similar to the Tettigoniidae, but wingless. They bear long, threadlike antennae, usually longer than in Tettigoniidae. Their legs also are quite long. The pronotum is smoothly rounded and lacks ridges. Unlike most of their close relatives, they do not have a hearing organ on the front tibia. They are not usually considered to be singers, though some are capable of making some sounds, and some species have stridulatory pegs. Because they lack wings, it is dif ficult to distinguish adults from nymphs except by the developing ovipositor, or fully developed male genitalia. They are dull colored insects, usually some shade of brown or gray. Camel crickets are

Grasshoppers, Katydids and Crickets ( Orthoptera), Figure 45 Representatives of the family Myrmecophilidae, (top) an ant nest-inhabiting cricket, Myrmecophilus oregonensis Bruner; the family Rhaphidophoridae, (center) a camel cricket, Tachycines asynamorus Adelung; and the family Stenopelmatidae, (bottom) a Jerusalem cricket, Stenopelmatus fuscus Haldeman (images from Lyman Entomological Museum).

nocturnal. About 250 species are known around the world.

Family Stenopelmatidae This group consists of cricket-like insects known as Jerusalem crickets. They are flightless, noctur nal and infrequently encountered. Thus, they are poorly known. Jerusalem crickets are large,


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somewhat hump-backed, with large heads resembling anastostomatids. Their legs bear stout spines. They have large mandibles and bite readily. When disturbed, Jerusalem crickets will flip onto their backs, exposing their mandibles in a defensive p osture. They seem to be omni vores, and they benefit from animal protein. Most occupy arid western North America, often resting below-ground or beneath objects, but surfacing at night to feed. In Central America, however, some inhabit rotting logs and stumps. Jerusalem crickets can be large, some species weighing as much as 8 g, but others weigh less than 1 g. They transmit vibratory signals through the substrate. The males are sometimes eaten by the females after copulating. At least 80 species are known to occur in North America, but most are undescribed.

Family Tettigoniidae This is a large and important family that is variously known as katydids in North America and Australia, or bush crickets in other Englishspeaking areas. These species tend to be mediumsized or large in size, often 35–50 mm in length. The antennae are longer than the body. These insects bear tympana on the front tibiae. The pronotum only rarely bears a ridge. A large, sword-shaped ovipositor is usually present in the females. Although some katydids oviposit in soil, they also deposit eggs in leaf tissue, stem tis sue and even bark crevices. Some oviposit flat tened, overlapping eggs like roof shingles on leaf and stem tissue. A small number construct “nests” of chewed plant material and mud. Katy dids (Fig. 46) are usually green or brown in color, and though some species are active during the day, most are largely nocturnal. The males strid ulate freely, and in many environments, these insects are an important element of night-time sounds. They are largely phytophagous, but are also omnivorous and a few feed on other insects. They prefer proteinaceous food, and even the

Grasshoppers, Katydids and Crickets ( Orthoptera), Figure 46 Representatives of the f amily Tettigoniidae: (top) a coneheaded katydid, Neoconocephalus ensiger (Harris) ( subfamily Conocephalinae); (center) a false katydid, Amblycorypha oblongifolia (De Geer) (subfamily Phanopterinae); and (bottom) a shield-backed katydid, Atlanticus monticola Davis (subfamily Tettigoniinae) (images from Lyman Entomological Museum).

phytophagous species often select blossoms and fruit for their higher protein content. The males tend to produce a large edible spermatophylax, a structure containing the spermatophore. The spermatophylax is passed on to the female as a nuptial gift, and is also a means of providing a protein supplement to the female when she is producing eggs. Tettigoniids are found through out the world, and number nearly 400 species.

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Subfamily Conocephalinae (Meadow and Coneheaded Katydids)

Subfamily Pseudophyllinae (True Katydids)

These katydids are small to medium in size. They are long, thin insects and some have a conical head. The ovipositor may be long and swordshaped. The antennae are long. They are green or brown, blending well with vegetation. The pre ferred habitat is short or tall grasses and broadleaf plants, normally in fields and swamps, but some times in forests. They sing mostly at night, and are found throughout most of the world. Nearly 1,000 species are known. One tribe, the copiphorini, is sometimes treated as a subfamily.

These are broad-winged insects that commonly inhabit trees and shrubs. The subfamily is quite diverse in the tropics of both the New World and the Old World, and different species often mimic different natural elements of their habitat such as leaves and bark. About 1,000 species are known.

Subfamily Meconematinae (QuietCalling Katydids) These are small, diurnal insects. They are found in Africa, Europe and northern Asia. Over 400 spe cies are known in the subfamily.

Subfamily Phaneropterinae (False Katydids) This group of katydids is distinguished by the absence of spines on the prosternum and by the wing length; the hind wings are longer than the front wings. These insects are noted songsters, and they vocalize late in the day and during the evening. They normally are brown, but pink forms are known. About 2,000 species are known.

Subfamily Phyllophorinae (Giant Leaf Katydids) These leaf feeders are the largest of the tettigoni ids. Their wing spans attain 25 cm. They bear a very heavy pronotum, and the males have lost the ability to stridulate using the tegmina. There are about 70 known species, all from Australia and nearby areas.

Subfamily Saginae (Stick Katydids) These flightless insects occur in Africa, Europe and Asia. One species, of European origin, has established in North America. This flightless spe cies, Saga pedo, reproduces parthenogenetically, a rare occurrence among katydids. Sagines are pred ators, and quite aggressive about grasping prey with their spined forelegs. About 50 species are known.

Subfamily Tettigoniinae (Shield-Backed Katydids) Many large, ground-dwelling, flightless species are found in this subfamily. They tend to be shortwinged, and are sometimes dark in color, often brown or black. Other species in this same subfamily are long-winged and good fliers. They occupy a diversity of habitats. Some, such as the Mormon cricket, Anabrus simplex Haldeman, are crop pests in western North America. Omnivory and carnivory are common in this group. Nearly 900 species are known from this group. They are found throughout the world.

Evolution of Orthoptera The evolution of Orthoptera can be traced back to the Protorthoptera of the Upper CarboniferousPermian period some 300 million years ago. The


Protorthoptera gave rise to several primitive groups that eventually gave rise to the ancestors of the most recent orthopteroid orders. The order Orthoptera probably underwent an early split to give rise to the two major lines of evolution now recognized as Caelifera and Ensifera. Ensifera is considered to be more primitive than Caelifera. The orthopterans are closely related to the mantids, walkingsticks, cockroaches and rock crawlers. They are less closely related to earwigs, webspinners and termites. Collectively, these taxa are referred to as the orthopteroid orders. All are thought to be descended from a common neopteran ancestor that predated the Protorthoptera. Not everyone agrees with this interpretation, however. It is also possible that Caelifera and Ensifera evolved independently from different pro torthoperan ancestors. It has even been suggested that the Orthoptera could be an artificial group (Caelifera plus Ensifera) that appears united mostly because they have enlarged hind legs for leaping. Consider that although the orthopterans produce sound, the two suborders differ in how they pro duce and hear sound. However, most available evidence, and most orthopterists, support the idea of a single order.

Natural Enemies of Orthoptera There are numerous natural enemies of orthopter ans, and the same types of natural enemies gen erally affect the several taxa of Orthoptera. However, the relative importance of the natural enemies varies among orthopterans, among dif ferent periods of the orthopteran population cycle, in different regions of the world, according to the weather and according to the soil type. Natural enemies of orthopterans include predators (which kill and eat their prey), parasi toids (parasitic insects that develop in or on the host orthopteran and kill the host only when the parasite reaches maturity), and pathogens (micro bial diseases that kill the host after the host’ s nutrients are exhausted).

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Important egg predators include bee flies ( Diptera: Bombyliidae), ground beetles (Coleoptera: Carabidae) and blister beetles (Coleoptera: Meloi dae). Nymphs and adults are captured and eaten by spiders, birds, small mammals and rodents, ants (Hymenoptera: Formicidae), sphecids (Hy menoptera: Sphecidae) and robber flies (Diptera: Assilidae). Among the important parasitoids of nymphs and adults are blow flies (Diptera: Calli phoridae), sarcophagids (Diptera: Sarcophagidae), nemestrinids (Diptera: Nemestrinidae) and tachin ids (Diptera: Tachinidae). Mites (Acari) are com monly found clinging to orthopterans, and some feed on the blood of their host. Although mites weaken their host, they are not thought to be impor tant mortality agents. Pathogens affect all stages of orthopteran development, and among the most important are nematodes, fungi, viruses and microsporidians. Nematodes and fungi are readily affected by soil and weather conditions, so their occurrence is inconsistent. However, these patho gens can have dramatic effects on orthopteran pop ulations when conditions favor their virulence. Viruses and microsproridians are found widely, though they often are not especially virulent. The impact of pathogens is often overlooked relative to predators and parasitoids because their effect may be expressed as a shortening of the life span or as a reduction in reproduction, rather than in direct mortality. The importance of natural enemies is difficult to measure, and the action of these beneficial organisms may come too late in a population out break to prevent damage. Sometimes they may interfere with one another, as when robber flies capture insect parasitoids as well as grasshoppers, or when fungal diseases kill a host insect prema turely, causing the death of the parasitoid con tained in the host orthopteran. Nevertheless, there are many striking examples of natural enemies suppressing orthopteran populations. Examples of natural enemy effects include: parasitism of grass hoppers by the nematode Mermis nigrescens killed 71% of Melanoplus femurrubrum grasshoppers in Michigan, USA; mermithids infected 69% of

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Locusta migratoria in wet areas of Papua New Guinea, but only 15% in dry areas; 30–70% of field crickets were infected with microsporidians in Michigan, USA; grasshoppers comprised 94% of the diet of the robber fly Proctacanthus milbertii, a generalist predator, in studies conducted in Montana, USA, and this fly consumed about 25% of all hoppers present; birds ate about 27% of adult grasshoppers during the summer in Nebraska, USA; over 200 species of birds in Nebraska feed on grasshoppers, and during the summer months, the average bird’s stomach contains at least 25 grasshoppers at any time; parasitism of Zonocerus locusts exceeded 40% by a calliphorid in Africa; and the combined effects of natural enemies accounted for about 50% mortality in desert locust, Schistocerca gregaria, populations in Africa.

Importance of Orthoptera to Humans Grasshoppers, katydids, crickets and other orthopterans vary considerably in their impor tance to humans. In some societies, grasshoppers are a minor source of food, and katydids and crickets are kept as pets for their acoustical abili ties. However, these beneficial aspects are minor compared to their destructive attributes. Grass hoppers are widely recognized to be serious pests of arid-land or prairie agriculture, and to a lesser degree, in mesic areas. Katydids, crickets and allied insects usually have minor effects on agri culture, though a few species are quite damaging. Grasshoppers, katydids and sometimes other orthopterans consume considerable amounts of foliage during their nymphal development, and also as adults. Occasionally, other insect activities such as tunneling (by mole crickets) or oviposi tion (by tree crickets) may be the basis for injury. Pasture, forage, grain, vegetable, and even fruit and ornamental crops can be affected. Histori cally, grasshoppers and locusts have been very disruptive to civilizations in Africa, the Middle East, India, China and North America. However,

Australia, Europe and South America also have witnessed serious problems, so, virtually no area of the globe is immune to attack by grasshoppers. However, except in areas where access to tech nology and funds are limited, the tools are now available to manage these pests and to prevent them from excessive destruction. Abnormally high densities of grasshoppers are called outbreaks or plagues. Regardless of the terminology applied, the phenomenon occurs throughout the world, and its origin is invariably related to food and weather. Grasshoppers that tend to attain high densities periodically, especially those that tend to become gregarious and move together as groups or swarms, are sometimes called locusts. Locusts do not really differ from grasshoppers, other than displaying a greater degree of gregarious behavior. Even species known as locusts periodically experience periods when they are not numerous, not gregarious, and do not cause much injury. Grasshoppers require warm and sunny con ditions for optimal growth and reproduction. Warmth alone seems to be inadequate, and grass hoppers often bask in the sun to raise their body temperatures. Thus, drought stimulates grasshop per population increase, apparently because there is less rainfall and cloudy weather to interfere with grasshopper activity. A single season of such weather is not adequate to stimulate massive population increase; rather, 2–3 years of drought usually precede grasshopper plagues. Warm winter temperatures also seem to be beneficial, because less mortality occurs by overwintering nymphs and adults. This scenario explains outbreaks that occur in temperate climates, where food is not limited, but heat may be inadequate. However, it does not explain all grasshopper outbreaks. Food is a necessary prerequisite for grasshop per success, and optimal weather alone, in the absence of adequate food supply, will prove insuf ficient for rapid grasshopper population growth. For outbreaks or plagues to occur, both requisites must be satisfied. Thus, some precipitation must be present at the appropriate time to stimulate plant


growth, but an over-abundance results in too much cloud cover. In tropical or subtropical climates, especially warm but arid regions, precipitation is an important stimulus that increases grasshopper breeding and causes outbreaks to develop.

Management of Orthoptera Pests The ideal way to manage orthopteran pests is to manage the environment to prevent them from attaining pest status. One example of how this can be accomplished is with weed management in fallow fields, and along roadsides and irriga tion ditches. Luxurious growth of weedy vegeta tion often favors the survival of grasshoppers, which then can spread to adjacent crops. If this land is instead tilled or planted with short grass, fewer grasshoppers will breed there and the dam age potential is greatly reduced. Unfortunately, many environments cannot be manipulated eas ily, and when weather or other factors favor pop ulation increase, a suppressive action must be initiated. Another example of how problems can be prevented is by introducing natural enemies of grasshoppers that have invaded a new area, and have therefore left their natural enemies behind. The introduction of a parasitic fly, Ormia depleta, and an entomopathogenic nematode, Steinernema scapterisci, for the suppression of Scapteriscus mole crickets in Florida, illustrates how this method can be applied effectively to invaders. However, most orthopteran pests are native, and there is little opportunity to identify natural enemies from elsewhere. Biological suppression of orthopteran popula tions is difficult to achieve once they have attained damaging levels. Natural enemies sometimes even tually build to high enough levels to help decrease pest abundance. For example, wild birds will some times switch their feeding to take advantage of an abundance of grasshoppers, but this is effective only on a local scale, not a regional scale. Domestic fowl, especially turkeys, readily consume vast quantities of grasshoppers, and can be used for small-scale

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suppression. There also are grasshopper disease agents that are under investigation, and even some that are sold commercially, but so far, none has been shown to provide adequate suppression. Entomo pathogenic nematodes are used for mole cricket suppression in some environments. Biological con trol remains a promising area for research, and the search continues for more effective products, but thus far, there are few practical options. For some people, neem products are attractive. Neem prod ucts are botanical derivatives that, when applied to plants, act as a feeding deterrent, reducing damage. Also, if applied to grasshopper nymphs, neem can act as a growth regulator, disrupting the normal growth and development, and sometimes resulting in the death or sterilization of grasshoppers. Although neem products are chemicals, many peo ple take comfort in knowing that they are derived from plants, and are therefore somewhat “natural.” Like many natural controls, effectiveness is not always consistent. In some situations, physical barriers can pro vide some protection from damage. It is possible to screen or cover valuable plants with netting, floating row cover, or similar material to deny grasshoppers access to susceptible plants. This is suitable for small gardens, and is even applied commercially for orna mental plant production, wherein shade houses are sealed tightly to deny access to orthopterans. The potential for this approach is limited in scale due to the cost. For flightless species such as lubber grass hoppers or Mormon crickets, physical barriers such as a ditch with steep sides, or a short metal or plastic “wall,” can prove to be effective impediments to grasshopper dispersal. If such a wall is contemplated, however, consider that orthopterans have sharp claws and can ascend vertical surfaces with amazing agility, so the top of a barrier should end in a 45 degree angle, forcing the insects to fall back. As mentioned above, cultural management of crop- and pasture-land can sometimes be used to manipulate orthopteran abundance. The habitats most favorable for grasshopper population growth and survival are open, sunny habitats containing mixed, early to mid-successional plants. Land with

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Grasshoppers of the Argentine Pampas

trees providing moderate to deep shade rarely pro duce large numbers of grasshoppers. Also, land that is kept mowed, either mechanically or by livestock grazing, tends not to produce grasshoppers unless grass pasture-land is damaged by overgrazing and broadleaf weeds invade. If natural enemies and cultural manipula tions have failed to keep orthopteran pests in check, chemical insecticides are most often used to prevent excessive damage. Chemical insecti cides can be applied in liquid form, by application directly to the grasshoppers, or to the plants they will walk or feed upon. Insecticides can also be applied to food bait, usually bran flakes, and dis tributed in the pest’s environment. If insecticides are to be used, it is advisable to apply the chemi cals when the pests are young. Small insects are much easier to kill than large ones, and grasshop pers and crickets are notoriously difficult to kill under any conditions. Also, because the grasshop pers usually develop in surrounding vegetation, it is usually best to take the “battle” there, and apply insecticides to the young grasshoppers before they disperse into crops and cause damage.  Grasshoppers of the Argentine Pampas  African Pine-Feeding Grasshopper  Diseases of Grasshoppers and Locusts  Grasshoppers and Locusts as Agricultural Pests  Desert Locust Plagues  Rhammatocercus schistocercoides  Weta  Katydids  Jerusalem Crickets

References Chapman RF, Joem A (eds) (1990) Biology of grasshoppers. Wiley, New York, NY Field LH (ed) (2001) The biology of wetas, king crickets, and their allies. CABI Publishing, Wallingford, UK Gwynne DT (2001) Katydids and bush-crickets. Reproduc tive behavior and evolution of the Tettigoniidae. Cornell University Press, Ithaca, NY Huber F, Moore TE, Loher W (eds) (1989) Cricket behavior and neurobiology. Cornell University Press, Ithaca, NY Otte D (1981/1984) The North American grasshoppers, vol 1, 2. Harvard University Press, Cambridge, MA

Otte D (1995) Orthoptera species file, vol 1–7. The Academy of Natural Sciences of Philadelphia, Philadelphia, PA. Available at http://viceroy.eeb.uconn.edu/Orthoptera Uvarov B (1966/1977) Grasshoppers and locusts. A handbook of general acridology, vol 1, 2. Cambridge University Press, London, UK

Grasshoppers of the Argentine Pampas Norma E. Sánchez, María. L. de Wysiecki Universidad Nacional de La Plata, La Plata, Argentina The Pampas, which occupies the Province of Buenos Aires and parts of the Provinces of Entre Ríos, Santa Fe, Córdoba, La Pampa and San Luis, are temperate subhumid grasslands. Mesother mic grasses dominate in this region of mild climate with mean annual temperature ranging from 10 to 20°C, and annual rainfall between 400 and 1600 mm. There is a general decrease south westward in annual precipitation, soil organic matter and grassland productivity. The landscape has been altered markedly dur ing the last century due to agricultural and grazing activities, and pristine grasslands have been drasti cally modified. Most of the land has been converted to cropland, mainly soybean, corn, sunflower and wheat. Among the most important native herbivores are grasshoppers, which are a recurrent pest of the agro ecosystems of this area. These insects may cause, in some years, forage and crop losses of con siderable magnitude. The Pampas and the Great Plains of North America have some ecological similarities in grasshopper fauna. However, species richness and diversity are higher in the US grasslands, while the Pampas have a greater diversity of higher acridid taxa, three families (Acrididae, Romalei dae and Ommexechidae) and nine subfamilies (Melanoplinae, Gomphocerinae, Copiocerinae, Leptysminae, Cyrtacanthacridinae, Acridinae, Romaleinae, Ommexechinae and Aucacrinae)

Grasshoppers of the Argentine Pampas

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Grasshoppers of the Argentine Pampas, Table 11 Grasshopper species composition of the argentine pampas Acrididae

Romaleidae

Acridinae

Melanoplinae

Romaleinae

Allotruxalis strigata (Bruner)

Atrachelacris gramineus G.Tos

Diponthus argentinus Pictet & Saus

Covasacris albitarsis Liebermann

Baeacris punctulatus (Thumberg)

Elaeochlora viridicata Serville

Laplatacris dispar Rehn

Baeacris pseudopunctulatus Ronderos

Xyleus laevipes Stål

Parorphula graminea Bruner

Dichroplus conspersus Bruner

Zoniopoda omnicolor Bruner

Copiocerinae

Dichroplus elongatus (G.Tos)

Zoniopoda tarsata Serville

Aleuas linneatus Stål

Dichroplus maculipennis (Blanchard)

Aleuas viticolis Stål

Dichroplus obscurus Bruner

Leptysminae

Dichroplus patruelis Stål

Leptysma argentina Bruner

Dichroplus pratensis Bruner

Gomphocerinae

Dichroplus schulzi Bruner

Amblytropidia australis Bruner

Dichroplus vittatus Bruner

Borellia brunneri (Rehn)

Leiotettix pulcher (Rehn)

Euplectrotettix ferrugineus Bruner

Neopedies brunneri G.Tos

Orphulella punctata De Geer

Ronderosia bergii (Stål)

Rhammatocerus pictus Bruner

Ronderosia forcipatus (Rehn)

Scyllina signatipennis Blanchard

Scotussa cliens Stål

Scyllina variabilis Bruner

Scotussa daguerrei Liebermann

Sinipta dalmani Stål

Scotussa lemniscata (Stål)

Staurorhectus longicornis G.Tos

v ersus two families (Acrididae and Romaleidae) and six subfamilies (Oedipodinae, Melanoplinae, Gomphocerinae, Acridinae, Cyrtacanthacridinae and Romaleinae). The Melanoplinae is the main subfamily in both regions and the genus Melanoplus of North American is considered to be the ecological equivalent to the South American genus Dichroplus (Table 11). There exists a large-scale association between grasshopper and plant communities along the Pampas. Indeed, assemblages may differ in density, dominance, and species composition because of differences in vegetation and climatic conditions. Total species richness is thirty nine, ranging from four to sixteen at different sites. Dichroplus pratensis and D. elongatus (Fig. 47) are clearly the most common and widely distributed species in this region. Both are polyphagous species, eating grasses

and forbs. Eggs hatch in November and, after pass ing through 5 nymphal instars, reach the adult stage in January. They have an obligatory embry onic diapause and one generation a year.

Grasshoppers of the Argentine Pampas, Figure 47 Dichroplus elongatus G. Tos. Another species of this genus, D. maculipennis, one of the most harmful species of this area thirty years ago, has exhibited very low populations during the last decade.

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Grassi, Giovanni Battista

In relation to damage, a population of D. pratensis with a peak of 22.19 individual/m2 may cause a forage loss of approximately 274.32 kg/ha. Another species of this genus, D. maculipennis, one of the most harmful species of this area thirty years ago, has exhibited very low popula tions duringthe last decade. Other common species are Laplatacris dispar, Amblytropidia australis, and Scotussa lemniscata in the humid northeastern grasslands. The central grasslands are dominated by D. pratensis, D. elongates, Staurorhectus longicornis, Leiotettix pulcher and D. vittatus. Borellia brunneri, Covasacris albitarsis and S. lemniscata are common in the southeastern habitats. Grasshopper assemblages of the xeric west ern grasslands are dominated by D. pratensis and Neopedies brunneri, and among common species are Rhammatocerus pictus, S. longicornis, D. vittatus and the Romaleidae Zoniopoda tarsata. Most species in the Pampas are rare. Some are registered every year from most sites, but in low numbers (e.g., Baeacris punctulatus), whereas oth ers are found in many years but only in some sites (e.g., Xyleus laevipes and Z. omnicolor). At present, the only control measure against these insects is the use of chemical pesticides. The microsporidian pathogen Nosema locustae Can ning was introduced between 1978 and 1982 to control pest grasshoppers, and became established in some areas. However, no surveys to evaluate the effectiveness as a biological control agent has been conducted. Only one native microsporidian pathogen, Perezia dichroplusae Lange, is currently known in argentine grasshoppers. Other patho gens, like the amoeba Malameba locustae King & Taylor (Protozoa: Rhizopoda), the virus Entomopox (Poxviridae: Entomopoxvirinae) and the fungus Entomophaga grylli (Fresenius) (Zygomy cetes: Entomophtorales) also are recorded.

References Cigliano MM, de Wysiecki ML, Lange C (2000) Grasshopper (Orthoptera, Acrididae) species diversity in the Pampas, Argentina. Diver Distrib 6:81–91

de Wysiecki ML, Sánchez NE (1992) Dieta y remoción de forraje de Dichroplus pratensis (Orthoptera: Acrididae) en un pastizal natural de la provincia de La Pampa, Argentina. Ecología Austral 2:19–27 Lange CE (1998) Patógenos asociados a tucuras (Orthoptera: Acrididoideae) en las provincias de Buenos Aires y La Pampa. Monografía 16. Comisión de Investigaciones Científicas de la provincia de Buenos Aires Sánchez NE, de Wysiecki ML (1990) Quantitative evaluation of feeding activity of the grasshopper Dichroplus pratensis Bruner (Orthoptera: Acrididae) in a natural grassland of La Pampa, Argentina. Environ Entomol 19:1392–1395 Soriano A (1992) Río de La Plata Grasslands. In: Coupland RT (ed) Natural grasslands. Introduction and western hemisphere. Ecosystems of the World, 8. Elsevier, Amsterdam, The Netherlands, pp. 367–407

Grassi, Giovanni Battista Giovanni Grassi (Fig. 48) was born in the province of Como, Italy, on March 27, 1854. He was educated at the u niversities of Pavia and Messina (Italy) and Heidelberg and Würzburg (Germany). In 1883 he was appointed professor of zoology, anatomy, and comparative zoology at Università di Catania, and in 1895 he was appointed to a similar position at Università di Roma. His works began on intestinal worms, proceeded to Protozoa (especially of termites), continued with flies (1883, “Malefizi delle mosche”) as vectors of eggs of nematodes and spores of fungi, on embryology of the honey bee, morphology and phylogeny of arthropods, the biology of termites, the transmission of malaria by Anopheles mosquitoes, the life history of Phlebotomus, on the grapevine pest Phylloxera, and on chaetognaths, marine eels, and development of the vertebral column. In 1908 he was made a member of the Italian senate. In 1884–1889 he studied Thysanura, Scolopendrella, and Koenema mirabilis, the last being an arachnid that he discovered. For his collaborative work with Sandias on termites, and for his studies of muraenoid eels, he was awarded the Darwin gold medal of The Royal Society. In 1898–1900, he concentrated on malaria, finding that all Italian species of Anopheles can transmit Plasmodium, and that Plasmodium is the same parasite that Ross described under the name

Grass Moths

Grassi, Giovanni Battista, Figure 48 Giovanni Batista.

Proteosoma (1900, Studi di uno zoologo sulla malaria). He continued his studies of malaria in 1917, continued to publish, but died on May 5, 1925.

Reference Wyatt AK (1926) Obituary. Entomological News 37:126–128

Grass Miner Moths (Lepidoptera: Elachistidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Grass miner moths, family Elachistidae, comprise about 723 species worldwide, but most are Palearctic (472 sp.), and many are in the genus Elachista. Two subfamilies are used, or only tribes: Perittiinae and Elachistinae. The family is part of the super family Gelechioidea in the section Tineina, subsec tion Tineina, of the division Ditrysia. Adults small (5–23 mm wingspan), with head smooth-scaled; haustellum scaled; labial palpi upcurved but some times porrect; maxillary palpi minute, 1 to 2-seg mented. Wings narrow and lanceolate, with reduced venation, but with large hindwing fringes (Fig. 49). Maculation often white with various markings or

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Grass Miner Moths (Lepidoptera: E lachistidae), Figure 49 Example of grass miner moths (Elachistidae), Biselachista cucullata (Braun) from Florida, USA.

bands, or darker, sometimes with iridescence. Adults are often crespuscular or nocturnal, but some are diur nal. Larvae are leafminers (sometimes gregarious) or stem miners, especially on grasses (Gramineae) and related plant groups like Juncaceae and Cyperaceae, but other plant families are also utilized.

References Braun AF (1948) Elachistidae of North America (Microlepi doptera). Mem Am Entomol Soc 13:1–110, pl. 26 Kaila L (1996–1999) A revision of the Nearctic Elachistidae s.l. (Lepidoptera, Elachistidae). Entomologica Scandi navica 27:217–238 (1996); Acta Zoologica Fennica 206:1–93 (1997), 211:1–235 (1999) Keila L (1999) Phylogeny and classification of the Elachisti dae s.s. (Lepidoptera: Gelechioidea). Syst Entomol 24:139–169 Traugott-Olsen E (1995–1996) Phylogeny of the Elachistinae s.str. (Lepidoptera, Elachistidae). SHILAP Revista de Lepidopterologia 23:153–180, 257–290, 417–449 (1995); 24:129–149 (1996) Traugott-Olsen E, Nielsen ES (1977) The Elachistidae (Lepi doptera) of Fennoscandia and Denmark. In: Fauna Entomologica Scandinavica, 6:1–299. Scandinavian Science Press, Klampenborg

Grass Moths Some members of the family Pyralidae (order Lepidoptera) also known as snout moths.  Snout Moths  Butterflies and Moths

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Gravenhorst, Johan Ludwig Christian

Gravenhorst, Johan Ludwig Christian Johan Ludwig Gravenhorst was born in Braun schweig [Brunswick], Germany, on November 14, 1777. He was educated at the Katharinen Gymnasium in Braunschweig. Despite an early interest in natural history, he decided on a career in law, and entered Universität Helmstadt to study law. However, in 1790 he entered Univer sität Göttingen to study zoology, mineralogy, and botany. In 1801 he returned to Helmstadt and defended his dissertation “Conspectus his toriae entomologiae” and was awarded the title of “Doctor philosophiae et magister liberalium artium.” Then he returned to Braunschweig and spent all his time on entomology. His first major publication (1802) was “Coleoptera Microptera Brunsvicensia,” after which he journeyed to Paris to study insect collections, and meet entomolo gists. On return to Braunschweig, he bought entomological collections, became a “Privatdo cent” at Universität Göttingen, and published (1906) “Monographia Coleopterorum Micropter orum,” which expanded his recognition among entomologists. He worked on an expanded edi tion of this work until Erichson’ s (1840) “Gen era et species Staphylinorum” made it redundant. In 1810 he accepted a position of professor of natural history and second director of the botan ical garden at Frankfurt an der Oder. In 1811, this university was transferred to Breslau (now Wroclaw in Poland), and Gravenhorst followed. In 1814 he sold his insect collection to the uni versity in return for a guaranteed annual income transferable to his widow, and he founded the zoological museum there. He began to work on Ichneumonidae (Hymenoptera) on which he published intensively to 1829. In 1830 he trav elled to Prague, Vienna, and Trieste to study marine animals, on which he published. He was a member of at least 21 natural history societies in Germany, France, Italy and England. He died in Breslau on January 17, 1857, after a very lengthy illness.

Reference Herman LH (2001) Gravenhorst, Johan Ludwig Christian. Bull Am Mus Nat Hist 265:70–71

Gravid This refers to a female that is full of eggs, or is ready to deposit her eggs.

Gray Mold of Grapes This is a serious fungal disease of grape.  Transmission of Plant Diseases by Insects

Graybacks A family of dragonflies in the order Odonata: Petaluridae.  Dragonflies and Damselflies

Greater Date Moth, Arenipses sabella Hmps. (Lepidoptera: Pyralidae) Yousif Aldryhim King Saud University Riyadh, Saudi Arabia The importance of the greater date moth as a date pest seems to be increasing. It is known from India, Iran, Iraq, Saudi Arabia, Oman, Egypt and Algeria.

Description The adult greater date moth is 18–22 mm long, with a wing span of 33–35 mm in males and 40–42 mm in females. They are light brown to yellowish. The head and thorax are light brown and the abdo men is silvery white, the front wings are brownish to yellowish with black scales and the hind wings

Greater Date Moth, Arenipses sabella Hmps. (Lepidoptera: Pyralidae)

are light brown. The eggs generally are laid singly, but also have been observed in clusters. They are creamy-white in color and spherical in shape. The larvae of the greater date moth are 28–35 mm in length and are dark pink in color. The pupae are elongated, about 18 mm in length, and are light brown.

Behavior The adult greater date moths are nocturnal, but attracted to artificial light. They hide in the inner side of the bases of the palm petioles during the daytime. The larvae are also nocturnal at high tem peratures, but have been seen active during the daytime at moderate temperatures. The hiding places of the larvae are at the inner bases of the split spathes, between the base of strands, in the inner base of the palm petioles. The larvae are quite mobile and can hide easily when threatened.

Biology and Damage The biology of this pest is not well understood. The adults are active most of the year in warm areas and are not seen in the winter months in cold areas. The pest spends the winter in the larval stage in coccons under the fibers of the tree cab bage (head of the tree). The number of generations per year is uncertain, but there are at least two generations per year. In February in warm areas, larvae feed on the inner base of the petioles. The females lay eggs on the external tips of the unopened spathes, on strands and on fruit clus ters. Hatched larvae feed on the tips of unopened spathes, which become black because of the clus tering of black frass and silken threads. The larvae penetrate the sheath of the unopened spathes and feed on the strand mainly on tips. The tips of the strands become light gray to silver in color and devoid of flowers. When the spathes open, the lar vae may remove the flowers and young fruits from the strands. The larvae also feed on the base of the

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main axis of the fruit cluster and make longitudi nal tunnels and holes, both filled with black frass, coarse silks and plant fragments. The larvae feed in September on the ripened fruits. The infested dates become filled with black frass tied by silks. The infested dates may be inadvertently harvested and transferred to stores where consumers unfor tunately encounter the larvae and adults.

Control No definitive studies have been done to control this pest. The adult greater date moths were observed to be attracted to light traps with high rates of attracting from March to May. Pruning of the palm fronds may eliminate the hiding places of the larvae and adults. The current gen eral practices to control this pest are dusting the cabbage of the tree with organophosphorus or pyrethriod insecticides in the autumn after har vesting, and dusting the strands and the bases of the fruit clusters with an insecticide at the time of pollination. If the problem persists, sprays also should be applied on the young fruits. No active and promising natural enemies have been recorded for this pest. The pheromone of this pest has not yet been identified, therefore, it is important that new research focus on this aspect.

References Talhouk N (1984) The most common agricultural pests in Saudi Arabia. Ministry of Agriculture and Water, Riyadh, Saudi Arabia, 121 pp (In Arabic) Hussain A (1974) Pests of date palm trees and dates in Iraq. University of Bagdad, Ministry of Higher Education and Scientific Reasearch, Iraq, 190 pp. (In Arabic) Talhouk A (1969) Insects and mites injurious to crop in Middle Eastern countries. Verlag Paul Parey Hamburch, 239 pp Hammad SM, Kadous AA (1989) Studies on the biology and ecology of date palm pests in the eastern province. Research Grants Program, Technical Report No. 25. KACST, Riyadh, Saudi Arabia, 142 pp

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Greater Fritillaries or Silverspots, Speyeria [=Argynnis] (Lepidoptera: Nymphalidae)

Greater Fritillaries or Silverspots, Speyeria [=Argynnis] (Lepidoptera: Nymphalidae) James C. Dunford, Kelly R. Sims University of Florida, Gainesville, FL, USA Speyeria scudder (Nymphalidae: Heliconiinae: Argynnini), commonly known as greater fritillaries or silverspots, are medium to large butterflies (wing spans of 40–90 mm) that represent conspicuous members of North American Lepidoptera. The genus was named in honor of a German entomolo gist, Adolph Speyer, who specialized in butterfly studies. The origin of the common name “fritillaries” is obscure, and one explanation is that these butter flies resemble the lily genus Fritillaria. Typically orange and black or brown in color, most are recog nized by distinctive black spots and bars on the dorsal wing surface and silvery or cream-colored spots located on the ventral surface of the hind wings. Speyeria fritillaries are restricted to North America (absent in southeastern regions of the United States and all but northern Mexico), although morphologically similar genera exist in other temperate parts of the world and together may be considered the temperate-zone counter part to tropical Heliconiini (i.e., passion-vine butterflies). Long included in the Old World genus Argynnis Fabricius, they differ from their Eurasian relatives primarily in genitalic structure and were thus considered generically distinct from Argynnis by dos Passos and Grey; all North American taxa named since that time have been described within Speyeria. Recent workers, however, have treated Speyeria as a subgenus of the primarily Palearctic Argynnis fritillaries. Speyeria species and associated geographical forms have been collected and examined in great detail in the past and continue to be a target for professional and amateur butterfly enthusiasts. The early works on Speyeria listed over 100 “spe cies” names, but subsequent workers realized that most of these “species” were no more than geo graphical forms or races associated with a few

polytypic species. Since then, several additional subspecies have been described, three subspecies have been elevated to full species status, and some taxon names have been declared synonyms. Speyeria is presently comprised of 16 spe cies Table 12), and according to some authors, over 100 subspecific, geographical forms. Speyeria cybele (Fabricius), S. aphrodite (Fabricius), S. idalia (Drury), and S. atlantis (Edwards) occur east of the Mississippi River, each with distributions or sub species occurring in western North America, while S. diana (Cramer) is restricted to the eastern United States (in Appalachian and Ozark Mountain ecosys tems). The remaining species occur in the western regions of North America, some as far north as Alaska. All but three Speyeria species are extremely variable [exceptions include S. diana, S. idalia, and S. edwardsii (Reakirt)], with the western North Ameri can species, in particular, fragmenting into numer ous geographic forms that are often clinally joined with considerable intergradation occurring. Species and subspecies determinations are made primarily using wing patterns, wing color ation, and geographical location; because of this, specific and subspecific identification is difficult in many taxa due to subtle pattern (Fig. 50) and color variations. Generally, adult morphological varia tion between species and subspecies is based on overall size, varying degrees of sexual dimorphism, and the wings. Important wing characteristics found dorsally are ground color, intensity of black markings, degree of dark basal suffusion, promi nence of marginal band, and thickness of veins on the wings. Ventrally the important characteristics are the general ground color of the discal area on the hindwings, the size, shape, color and position of spots on the hindwings, and color and width of the submarginal band between the two outer rows of spots on the hindwings (Fig. 52).

Life History Adults frequent open fields, moist meadows, and open woodlands near streams, or are restricted


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Greater Fritillaries or Silverspots, Speyeria [=Argynnis] (Lepidoptera: Nymphalidae), Table 12 The known species of Fritillary butterflies Speyeria species and associated common names Speyeria diana (Cramer) – Diana Fritillary, Great Smokies Fritillary Speyeria cybele (Fabricius) – Cybele Fritillary, Great Spangled Fritillary Speyeria aphrodite (Fabricius) – Aphrodite Fritillary Speyeria idalia (Drury) – Regal Fritillary, Eastern Regal Fritillary, Prairie Regal Fritillary Speyeria nokomis (Edwards) – Nokomis Fritillary, Western Seep Fritillary Speyeria edwardsii (Reakirt) – Edward‘s Fritillary Speyeria coronis (Behr) – Coronis Fritillary Speyeria carolae (dos Passos and Grey) – Carol‘s Fritillary Speyeria zerene (Boisduval) – Zerene Fritillary Speyeria callippe (Boisduval) – Callippe Fritillary Speyeria egleis (Behr) – Egleis Fritillary, Great Basin Fritillary Speyeria adiaste (Edwards) – Unsilvered Fritillary Speyeria atlantis (Edwards) – Atlantis Fritillary Speyeria hesperis (Edwards) – Hesperis Fritillary, Western Fritillary Speyeria hydaspe (Boisduval) – Hydaspe Fritillary Speyeria mormonia (Boisduval) – Mormon Fritillary

to coastal dunes, tallgrass prairies, or mountains. During the summer months they may be abundant in forest clearings, by roadsides, and along flower rich slopes and meadows in mountainous regions. Speyeria often prefer tall nectar sources such as thistles, wild asters, sunflowers, penstemons, mint, and dogbane. Males are often found congregating in large numbers at seeps and roadside puddles. Adults are strong fliers and can fly many kms, especially in late summer. They are rather long lived (several weeks to 2–3 months from May-September) and all members of the genus are univoltine. Adult males typically emerge a week before females and patrol for potential mates. Courtship is rather elaborate, and pheromone cues from both sexes may be a reproductive barrier between species. Speyeria adults (Fig. 51) bear scent scales that lie along the veins on the upper side of the wings. Males pursue females, draw their forewings forward, and flick the closed wings slightly open in quick bursts. Each burst of two to five flicks lasts less than a sec ond, wafting pheromones up to the female’s anten nae. The tips of the abdomens of male Argynnini

(including Speyeria) contain paired glands nor mally hidden in the abdomen that aid in courtship. Courting males keep their forewings in a forward position and open and close them near the resting female to waft pheromones. Unreceptive females will flutter their wings to reject males. Fritillaries are fecund butterflies, with some species laying over 2,000 eggs. Females delay egglaying until late summer and usually oviposit rather haphazardly near their host plants rather than care fully placing them on the plant as most butterflies do. They are known to deposit eggs on twigs, leaves, stones and other debris. Eggs bear a tannish, cam ouflage coloration and are slightly rounded, taper ing toward the apex. They are highly sculptured and likely adapted to withstand considerable envi ronmental pressures including submergence, frost, and ground dwelling predators and microbes. Larvae usually pass through six instars, over wintering as first instars and breaking diapause to complete development the following season. They are generally secretive and feed primarily at night, returning to hiding places under host leaves or

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Greater Fritillaries or Silverspots, Speyeria [=Argynnis] (Lepidoptera: Nymphalidae), Figure 50 Dorsal (left) and ventral (right) wing patterning of some Speyeria species: (a) Speyeria hesperis (New Mexico); (b) Speyeria callippe (Nevada); (c) Speyeria mormonia (Nevada); (d) Speyeria zerene (Nevada) (images by James C. Dunford).

nearby vegetation during the day. Most species are black with lighter markings and bear three rows of branching spines on either side of the body. Some species exhibit spots of red/orange or other colors. Larvae feed on various violet species (Viola), and in laboratory conditions they are known to feed on every American violet species tested. Viola species range widely across temperate habitats of the Northern Hemisphere and into higher elevations of mountain systems towards the equator. Speyeria pupae are generally tan or brown with a few mark ings and hang freely from the cremastral end. Speyeria individuals likely gain protection from potential predators in a variety of ways. Speyeria diana females (Fig. 52) are sexually dimor phic from S. diana males and, unlike the typical orange and black patterning of most Speyeria spe cies, have been implicated in a Batesian mimicry complex with the distasteful, similarly colored pipevine swallowtail butterfly. In some Speyeria species, an eversible gland, capable of producing an unpleasant odor, is located on the dorsum of the

female abdomen. Larvae also bear a gland located ventrally just behind the head that is likely used for defense against predators. Other avoidance mea sures during the larval stages include taking refuge under leaves during the day and feeding at night. First instars will also often hibernate inside grass stems. Eggs in some species may also contain phytochemicals used to deter potential predators.

Conservation A few Speyeria species have been declining over the past 200 years and have been listed as either federally/state endangered or threatened [e.g., S. idalia, S. diana, S. zerene hippolyta (Edwards)]. Speyeria and their larval host plants (Viola) are among the best indicator organisms of native, undisturbed ecological communities in North America. They are also among the first organisms to be eliminated from such communities as a result of human-caused disturbances.


Marginal band

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Basal suffusion Discal area

a

Submarginal band

b

c e

d

f

Greater Fritillaries or Silverspots, Speyeria [=Argynnis] (Lepidoptera: Nymphalidae), Figure 51 Speyeria (a) general wing features; (b) Speyeria idalia egg; (c) Speyeria idalia larva; (d) Speyeria aphrodite larva; (e) Speyeria idalia pupa; (f) Speyeria idalia (Regal Fritillary) nectaring on butterflyweed (Wisconsin) (images b-e by David L. Wagner; images a and f by James C. Dunford).

Speyeria idalia populations have been extir pated in much of the northeastern United States and have declined precipitously in other parts of its range. They inhabit native tallgrass prairies in the Midwest, an ecosystem that is shrinking due to development and agricultural activities. Speyeria diana disappeared from southeastern Virginia in about 1951 and is considered uncommon or extir pated in many other parts of its range. Historical populations in the Midwest and the Virginia

iedmont were extirpated in the 1800s, and most P occurrence records (except in the Appalachians and Ozarks) are more than 50 years old. Coastal subspecies, such as the Oregon Silverspot (S. z. hippolyta), have been federally listed and depend on vanishing salt-spray meadows along the Ore gon coast. Research on Speyeria butterflies continues to focus on various conservation and management measures required to maintain and protect threatened or endangered species.

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Greenbottle Flies

Opler PA, Warren AD (2005) Lepidoptera of North America. 4. Scientific Names List for Butterfly Species of North America, North of Mexico. Contributions of the C.P. Gillette Museum of Arthropod Diversity, Colorado State University, Fort Collins, Colorado. 83 pp Scott JA (1986)The butterflies of North America: a natural history and field guide. Stanford University Press, Stanford, CA. Simonsen TJ (2006) Fritillary phylogeny, classification, and larval hostplants: reconstructed mainly on the basis of male and female genitalic morphology (Lepidoptera: Nymphalidae: Argynnini). Biol J Linn Soc 89:627–673

Greenbottle Flies Members of the family Calliphoridae (order Diptera).  Flies

Greenbug, Schizaphis graminum (Rondoni) (Hempitera: Aphididae) Greater Fritillaries or Silverspots, Speyeria [=Argynnis] (Lepidoptera: Nymphalidae), Figure 52 Speyeria diana (a) male and (b) female (Tennessee). In each image, the left side is the dorsal wing surfaces and right side is the ventral wing surfaces (images by James C. Dunford).

References Dos Passos CF, Grey LP (1945) A genitalic survey of Argyn ninae (Lepidoptera, Nymphalidae). Am Mus Novit 1296:1–29 Ferris CD (1989) Supplement to: a catalogue/checklist of the butterflies of America north of Mexico. Mem Lep Soc No 3, 103 pp Hammond PC, McCorkle DV (1984) The decline and extinc tion of Speyeria populations resulting from human environmental disturbances (Nymphalidae: Argynni nae). J Res Lepidoptera 22:217–224 Holland WJ (1931) The butterfly book. Doubleday, Doran and Co., Garden City, NY, 382 pp Moeck AH (1957) Geographic variability in Speyeria: Com ments, records and description of a new subspecies (Nymphalidae). Milwaukee Entomological Society Special Publication, 48 pp

Greenbug is an important aphid pest of grass crops.  Wheat Pests and their Management

Green-Eyed Skimmers A family of dragonflies in the order Odonata: Corduliidae.  Dragonflies and Damselflies

Green Flies Members of the family Aphididae (order Hemiptera).  Bugs

Greenheads Some members of the family Tabanidae (order Diptera).  Flies

Greenhouse Whitefly, Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae)

Greenhouse Whitefly, Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) John L. Capinera University of Florida, Gainesville, FL, USA Greenhouse whitefly is found widely around the world, including most of the temperate and sub tropical regions of North America, South Amer ica, Europe, Central Asia and India, northern and eastern Africa, New Zealand and southern Aus tralia. It does not thrive in most tropical loca tions, and occurs in colder regions only by virtue of its ability to survive winter in greenhouses. It often overwinters only in such protected loca tions, but in mild-winter areas it survives out doors throughout the year. The origin of this species is not certain, but is thought to be Mexico or the southwestern United States.

Life History The development period from egg to adult requires about 25–30 days at 21°C, and 22–25 days at 24°C. Thus, because the preoviposition period of adults also is short, less than two days above 20°C, a complete life cycle is possible within a month. Greenhouse whitefly can live for months, and o viposition time can exceed the development time of immatures; this results in overlapping generations. Optimal relative humidity is 75–80%. The developmental threshold for all stages is about 8.5°C. Eggs are oval in shape, and suspended from the leaf by a short, narrow stalk. The eggs initially are green in color and dusted with white powdery wax, but turn brown or black as they mature. The eggs are about 0.24 mm long and 0.07 mm wide. Eggs are deposited on the youngest plant tissue, usually on the underside of leaves in an incom plete circular pattern. Up to 15 eggs may be depos ited in a circle measuring about 1.5 mm in diameter. This pattern results from the female

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moving in a circle while she remains with her mouthparts inserted into the plant. This pattern is less likely on plants with a high density of trichomes because plant hairs interfere with the oviposition behavior. Duration of the eggs stage is often 10–12 days, but eggs may persist for over 100 days under cool conditions. When cultured at 18, 22.5, and 27°C, egg development requires an average of 15, 9.8, and 7.6 days, respectively. Maximum fecundity varies according to temperature; optimal tempera ture is 20–25°C regardless of host plant. When feeding on eggplant, greenhouse whitefly produces over 500 eggs, on cucumber and tomato about 175–200 eggs. The newly hatched whitefly nymph is flat tened, oval in outline, and bears functional legs and antennae. The perimeter is equipped with waxy filaments. The first instar measures about 0.3 mm in length. It is translucent, usually appear ing to be pale green in color but with red eyes. After crawling one cm or so from the egg, it settles to feed and molt. Development in the first instar requires 6.5, 4.2, and 2.9 days, respectively, when cultured at 18, 22.5, and 27°C. The second and

Greenhouse Whitefly, Trialeurodes v aporariorum (Westwood) (Hemiptera: Aleyrodidae), Figure 53 Adult of greenhouse whitefly, Trialeurodes vaporariorum (Westwood).

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third nymphal stages are similar in form and larger in size, though the legs and antennae become reduced and nonfunctional. They measure about 0.38 and 0.52 mm in length, respectively. Duration of the second instar requires about 4.3, 3.2, and 1.9 days whereas third instars require 4.5, 3.2, and 2.5 days, respectively, when cultured at 18, 22.5, and 27°C. The fourth nymphal stage, which is usually called the “pupa,” differs in appearance from the preceding stages. The fourth instar measures about 0.75 mm in length, is thicker and more opaque in appearance, and is equipped with long waxy fila ments. The pupal stage actually consists of the fourth nymphal instar period, which is a period of feeding, plus the period of pupation, which is a time of transformation to the adult stage. Thus, pupation occurs within the cuticle of the fourth instar. Duration of the fourth instar period and pupal period are 8.7 and 5.9, 5.9 and 4.0, and 4.5 and 2.8 days, respectively, at 18, 22.5, and 27°C. The form of the pupa is used to distinguish among whitefly species (Fig. 54), and can be used to separate greenhouse whitefly from the similar-

Greenhouse Whitefly, Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae), Figure 54 Pupa of greenhouse whitefly, Trialeurodes vaporariorum (Westwood).

appearing Bemisia spp. Greenhouse whitefly is straight-sided when viewed laterally, ovoid, and lacks a distinct groove near the anal end of the body. In contrast, the Bemisia spp. are obliquesided, irregularly oval, and possess a distinct groove in the anal region. Individuals of greenhouse whitefly which develop on lightly or moderately pubescent leaves tend to be relatively large and to have four pairs of well developed dorsal waxy filaments. In contrast, whiteflies developing on densely pubescent leaves tend to be smaller, and to bear more that four pairs of dorsal filaments. These morphological varia tions are not entirely consistent, and have led to considerable taxonomic confusion. Adults (Fig. 53), are small, measuring 1.0–2.0 mm long. They are white in color, with the color derived from the presence of white waxy or mealy material, and have reddish eyes. They bear four wings, with the hind wings nearly as long as the forewings. The antennae are evident. In general form, viewed from above, this insect is triangular in shape because the distal portions of the wings are wider than the basal sections. The wings are held horizontally when at rest; this characteristic is useful for distinguishing this species from the similar-appearing Bemisia spp. whiteflies, which hold their wings angled or roof-like when at rest. Mating may occur repeatedly, though females can also produce eggs without mating. This species has a very wide host range, with over 300 species recorded as hosts. However, some hosts are more suitable. Vegetable plants often serv ing as good hosts are bean, cantaloupe, cucumber, lettuce, squash, tomato, eggplant, and occasionally cabbage, sweet potato, pepper, and potato. Among greenhouse-grown vegetables, the most common hosts are tomato, eggplant, and cucumber. Many ornamental plants serve as good hosts, including ageratum, aster, chrysanthemum, coleus, gardenia, gerbera, lantana, poinsettia, salvia, verbena, zinnia and many others. Natural enemies of greenhouse whitefly are numerous,but few are consistently effective,especially under greenhouse conditions. Greenhouse whitefly


is attacked by the common predators of small insects, including minute pirate bugs (Hemiptera: Anthocoridae), some plant bugs (Hemiptera: Mir idae), green lacewings (Neuroptera: Chrysopidae), brown lacewings (Neuroptera: Hemerobiidae), and ladybirds (Coleoptera: Coccinellidae). Para sitic wasps attacking greenhouse whitefly are largely confined to the family Aphelinidae, but many species are involved and they vary region ally. Some of the important parasitoids are Encarsia formosa Gahan, Aleurodophilus pergandiella (Howard), Eretmocerus haldemani Howard, Prospaltella transvena Timberlake, and Aphidencyrtus aphidivorus (Mayr). Although these agents exer cise considerable control on whitefly populations in weedy areas or on crops where insecticide use is minimal or absent, they do not survive well in the presence of most insecticides. Encarsia formosa has been used successfully under greenhouse con ditions, and to a lesser extent field conditions, to affect biological suppression. The pathogens of greenhouse whitefly are principally fungi, particularly Aschersonia aleyrodis, Paecilomyces fumosoroseus, and Verticillium lecanii. All occur naturally and can cause epizootics in greenhouses and fields, and also have been pro moted for use in greenhouses as bioinsecticides. Aschersonia is specific to whiteflies, Verticillium has a moderately wide host range, and Paecilomyces has a broad host range. For optimal development of disease, high humidity is required. Aschersonia is spread principally by rainfall, so often fares poorly in greenhouse environments.

Damage Adult and nymphal whiteflies use their piercingsucking mouthparts to feed on the phloem of host plants. This results in direct damage, resulting in localized spotting, yellowing, or leaf drop. Under heavy feeding pressure, wilting and severe growth reduction may occur. Whiteflies also secrete large amounts of sugary honeydew, which coats the plants with sticky material, and must be removed

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from fruit before it is marketed. The honeydew also provides a substrate for growth of sooty mold, a black fungus that interferes with the photosyn thesis and transpiration of plants. Greenhouse whitefly is, as the common name suggests, primarily a pest in greenhouses, and is a serious limitation to the production of vegetables grown in such structures. However, it can also be a field pest, often in warmer climates but also in cool climates when seedlings contaminated with white flies are transplanted into the field. Greenhouse whitefly is capable of transmitting viruses to plants, but is not considered to be a serious vector, particularly relative to the Bemisia spp. However, greenhouse whitefly transmits beet pseudo-yellow virus to cucumber in greenhouse culture.

Management Although whitefly nymphs and adults can be detected readily by visual examination of foliage, most monitoring systems take advantage of the attraction of adults to yellow, and use yellow sticky traps to capture flying insects. Sticky cards or ribbons are suspended at about the height of the crop for optimal monitoring. Traps must be placed close to plants or close to the ground or population densities will be underestimated. Traps should be dispersed widely because white fly distribution is not uniform within a crop. Whitefly flight peaks at about noon, but under greenhouse conditions is independent of tem perature if the basal flight temperature of 16–17°C is exceeded. Applications of insecticides are often made to minimize the effects of whitefly feeding on crops in greenhouses. Greenhouse whitefly feeds on the lower surface of foliage and is sessile throughout most of its life, habits that minimize contact with insecticides, and resulting in fre quent applications and effectiveness mostly against the adult stage. In greenhouse culture, application intervals of only 4–5 days are common,

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Green June Beetle, Cotnius nitida (Linnaeus) (Coleoptera: Scarabaeidae)

and systemic insecticides are often used to increase the likelihood of insect contact with toxins. Thus, whitefly resistance to nearly all classes of insecticides is known, and rotation of insecticide classes is encouraged. Mixtures of insecticides are often used, which is indicative of high levels of resistance among whiteflies to insecticides. Field populations of greenhouse whitefly invariably are derived from greenhouse populations, and possess similar resistance to many insecticides. Applications of petroleum oils and biological control agents help to avoid diffi culties with insecticide resistance. Some insecticidal materials can be integrated into biologically based whitefly management sys tems. Selective materials that affect only adult and nymphal whiteflies, insect growth regulators, and insecticidal soaps are somewhat compatible with parasitoids and can be used when parasitoids are failing. Few cultural practices are available, but dis ruption of the whitefly population with host-free periods is important. Continuous culture of plants allows whiteflies to move from older to younger plants. Similarly, weeds may allow whiteflies to bridge crop-free periods, and should be elimi nated. Culture of plants over white reflective mulch also reduces whitefly densities. Yellow sticky traps can be hung in greenhouses to capture adult whiteflies, thereby reducing whitefly density. Seasonal inoculative release of the parasitoid Encarsia formosa Gahan into crops infested with greenhouse whitefly has been used extensively for suppression of whiteflies on greenhousegrown vegetable crops. Excellent suppression of whiteflies is attainable, but on host plants such as cucumber and eggplant, which are very favorable for whitefly reproduction and have hairy leaves that interfere with parasitoid searching, frequent releases must be made. Alternatively, cucumber varieties with reduced trichome density have been developed, and which favor parasitism. Another critical factor is temperature, because low greenhouse temperatures are more suitable for whitefly activity than parasitoid activity.

aytime temperatures of about 24°C seem to be D optimal; temperatures of 18°C or less suppress parasitoid searching. A cold-tolerant Encarsia strain that is active at 13–17°C has also been used to overcome this temperature problem. Interfer ence from pesticides can markedly affect parasi toid survival, so other pests such as mites must be managed biologically also. Lastly, release rates are important because if too many parasitoids are released the host whiteflies are driven nearly to extinction, leading to disappearance of the para sitoids; this is most likely to occur in small green houses. Alternatively, parasitoid releases can be made throughout the season, irrespective of whitefly presence. Although the protocols and technologies for whitefly management using E. formosa have been perfected for use in green houses, management under outdoor conditions awaits further research. The fungus Verticillium lecanii is sometimes used commercially in Europe for whitefly and thrips suppression in greenhouses, though its success is strongly affected by humidity. Where humidity can be raised to a high level, epizootics can be induced in 1–2 weeks. Both young and adult stages are susceptible to infection.

References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, CA, 729 pp van Roermund HJW, van Lenteren JC (1992) The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae) XXXIV. Life history parameters of the greenhouse whitefly, Trialeurodes vaporariorum as a function of host plant and temperature. Wageningen Agricultural University Papers 92–93,Wageningen, The Natherlands, 147 pp

Green June Beetle, Cotnius nitida (Linnaeus) (Coleoptera: Scarabaeidae)  Turfgrass Insects and their Management

Green Peach Aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae)

Green Lacewings Members of the family Chrysopidae (order Neuroptera).  Lacewings, Antlions, and Mantidflies

Green Muscardine A mycosis of various larval, pupal, and adult insects, caused by the fungus Metarrhizium.  Muscardine

Green Peach Aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) John L. Capinera University of Florida, Gainesville, FL, USA Green peach aphid is found throughout the world, including both tropics and temperate latitudes. It is considered to be a pest nearly everywhere, often due to its ability to transmit plant viruses. In addition to attacking plants in the field, green peach aphid read ily infests vegetables and ornamental plants grown in greenhouses. This allows high levels of survival in areas with inclement weather, and favors ready transport on plant material. When young plants are infested in the greenhouse and then transplanted into the field, fields will not only be inoculated with aphids but insecticide resistance may be introduced. These aphids are also reported to be transported long distances by wind and storms.

Life History The life cycle varies considerably, depending on the presence of cold winters. Development can be rapid, often 10–12 days for a complete generation, and with over 20 annual generations reported in mild climates. Where suitable host plants cannot

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persist, the aphid overwinters in the egg stage. In the spring, soon after the plant breaks dormancy and begins to grow, the eggs hatch and the nymphs feed on flowers, young foliage, and stems. After several generation on Prunus spp., dispersants from overwintering hosts deposit nymphs on summer hosts. In cold climates, adults return to Prunus spp. in the autumn, where mating occurs, and eggs are deposited. All generations except the autumn generation culminating in egg production are parthenogenetic. Eggs are deposited on Prunus spp. trees. The eggs measure about 0.6 mm long and 0.3 mm wide, and are elliptical in shape. Eggs initially are yellow or green, but soon turn black. Mortality in the egg stage sometimes is quite high. Nymphs initially are greenish, but soon turn yellowish, greatly resembling viviparous adults. There may be four instars in this aphid, with the duration of each averaging 2.0, 2.1, 2.3, and 2.0 days, respectively. Alternatively, five instars also have been reported, with a mean development time of 2.4, 1.8, 2.0, 2.1, and 0.7 days, respectively. Parthenogenetic females give birth to offspring 6–17 days after birth, with an average age of 10.8 days at first birth. The length of reproduction var ies considerably, but averages 14.8 days. The aver age length of life is about 23 days under caged conditions where predators are excluded. The daily rate of reproduction averages 1.6 nymphs per female, with about 75 offspring produced. The maximum number of generations occurring annu ally is 20–21, depending on the year. Up to eight generations may occur on Prunus, but as aphid densities increase winged forms are produced, which then disperse to summer hosts. Winged (alate) aphids have a black head and thorax, and a yellowish green abdomen with a large dark patch dorsally. They measure 1.8–2.1 mm in length. Winged green peach aphids seem ingly attempt to colonize nearly all plants avail able. They often deposit a few young and then again take flight. This highly dispersive nature contributes significantly to their effectiveness as vectors of plant viruses.

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The offspring of the dispersants from the overwintering hosts are wingless, and each pro duce 30–80 young. The wingless (apterous) aphids are yellowish or greenish in color. They measure about 1.7–2.0 mm in long. A medial and lateral green stripes may be present. The cornicles are moderately long, unevenly swollen along their length, and match the body in color. The append ages are pale. The rate of reproduction is positively correlated with temperature, with the develop mental threshold estimated to be about 4.3°C. As aphid densities increase or plant condition deteri orates, winged forms are again produced to aid dispersal. The nymphs that give rise to winged females may be pinkish. The dispersants typically produce about 20 offspring, which are always wingless. This cycle is repeated throughout the period of favorable weather. In the autumn, in response to change in day length or temperature, winged male and female aphids are produced which disperse in search of Prunus (Fig. 55). Timing is important, as foliage on the Prunus hosts is physiologically optimal as leaves begin to senesce. Females arrive first, and give birth to wingless (apterous) egg-laying forms (oviparae). Males are attracted to oviparae by a pheromone, capable of mating with several females, and eggs are produced. The oviparous female deposits 4–13 eggs, usually in crevices in and near buds of Prunus spp. The oviparous female is 1.5–2.0 mm long, and pinkish.

Parthenogenic reproduction is favored in the many parts of the world where continuous production of crops provides suitable host plants throughout the year, or where weather allows sur vival on natural (noncrop) hosts. The average temperature necessary for survival of active forms of green peach aphid is estimated at 4–10°C. Plants in the families Cruciferae and Chenopodiaceae, both crops and weeds, readily support aphids through the winter months. Green peach aphid feeds on hundreds of host plants in over 40 plant families. However, it is only the viviparous summer stages that feed so widely; the oviparous winter stages are much more restric tive in their diet choice. In temperate latitudes the primary or overwintering hosts are trees of the genus Prunus, particularly peach and peach hybrids, but also apricot and plum. During the summer months the aphids abandon their woody hosts for secondary or herbaceous hosts, including orna mental, vegetable and field crops. Crops differ in their susceptibility to green peach aphid, but it is actively growing plants, or the youngest plant tissue, that most often harbors large aphid populations. In warmer climates the aphids do not seek out over wintering hosts, but persist as active nymphs and adults on hardy crops and weeds. Broadleaf weeds can be very suitable host plants for green peach aphid, thereby creating pest problems in nearby crops. Common and wide spread weeds such as field bindweed, Convolvulus arvensis; lambsquarters, Chenopodium album; and redroot pigweed, Amaranthus retroflexus, are often cited as important aphid hosts, and plant viruses may be acquired from these hosts.

Natural Enemies

Green Peach Aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), Figure 55 Adult of green peach aphid, Myzus persicae (Sulzer).

Hundreds of natural enemies have been recorded, principally ladybirds (Coleoptera: Coccinellidae), flower flies (Diptera: Syrphidae), lacewings (Neu roptera: mainly Chrysopidae), parasitic wasps (Hymenoptera: Braconidae), and entomopatho genic fungi (mainly Entomophthorales). Most are


general predators, moving freely among green peach aphid, other aphids, and even other insects. Quantitative data generally are lacking for the influence of most natural enemies. Weather also reportedly contributes to significant change in aphid numbers, including direct mortality, but this also is poorly documented. The ephemeral nature of aphid infestation in many crops is believed to prevent the benefi cial organisms from consistently locating the aphids and reproducing in a timely manner. Nevertheless, anyone who has frequently observed green peach aphid at high densities probably has observed sudden population decreases following the appearance of ladybirds, wasp parasitoids, or entomopathogenic fungi such as Erynia neoaphidis. Unfortunately, the disease epizootic often occurs too late to keep aphids from attaining high numbers. Various studies that selectively excluded or killed benefi cial organisms have demonstrated the explosive reproductive potential of these aphids in the absence of biological control agents, thus dem onstrating their value in reducing damage poten tial. In greenhouse crops, where environmental conditions and predator, parasitoid, and patho gen densities can be manipulated, biological suppression can be effective and consistent.

Damage Green peach aphids can attain very high densities on young plant tissue, causing water stress, wilt ing, and reduced growth rate of the plant. Pro longed aphid infestation can cause appreciable reduction in yield of root crops and foliage crops. Contamination of harvestable plant material with aphids, or with aphid honeydew, also causes loss. Where mild winters allow good overwintering survival of green peach aphid on spinach, crop value is affected by insect presence. Blemishes to the plant tissue, usually in the form of yellow spots, may result from aphid feeding. Leaf distor tions are not common except on the primary host.

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Contamination of vegetables by aphids some times presents quarantine problems and fumiga tion techniques have been developed that kill the insects without causing harm to the vegetables. The major damage caused by green peach aphid is through transmission of plant viruses. Indeed, this aphid is considered by many to be the most important vector of plant viruses throughout the world. Nymphs and adults are equally capable of virus transmission, but adults, by virtue of being so mobile, probably have greater opportunity for transmission. Both persistent viruses, which move through the feeding secretions of the aphid, and non-persistent viruses, which are only temporary contaminants of aphid mouthparts, are effectively transmitted. Over 100 viruses are transmitted by this species. Some of the particularly damaging diseases include potato leafroll virus and potato virus Y to Solanaceae, beet western yellows and beet yellows viruses to Chenopodiaceae, lettuce mosaic virus to Compositae, cauliflower mosaic and turnip mosaic viruses to Cruciferae, and cucumber mosaic and watermelon mosaic viruses to Cucurbitaceae. A discoloration in potato tubers, called net necrosis, occurs in some potato varieties following transmission of potato leafroll.

Management Day-degree models using a developmental thresh old of 4°C can be used to predict various pheno logical events such as egg hatch and immigration of alate aphids. Yellow traps, particularly water pan traps, are commonly used for population monitoring. Despite the numerous options potentially available, many crop producers are dependent on insecticides for suppression of green peach aphid abundance. Systemic insecticide applications are especially popular at planting time, most of which provide long-lasting protection against aphid pop ulation buildup during the critical and susceptible early stages of plant growth, and some of which provide protection for months.

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Green Stoneflies

Green peach aphid is able to develop at lower temperatures than its parasitoids, so the wasps are beneficial only in benign climates or where tem perature can be controlled, as in some greenhouses. Indeed, there has been considerable success using parasitoids, the entomopathogenic fungus Verticillium lecanii, and the predatory midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae) for greenhouse-grown vegetables in Europe. The overwintering behavior of green peach aphid, which in many areas is restricted to Prunus or other relatively restricted sites, has fostered research on techniques to reduce aphid abundance and disease transmission to other crops, by either removing the overwintering site or by eliminating the aphids before they disperse. Destruction of peach and apricot trees, and treatment of trees with dormant oil and insecticide, have been used effectively to disrupt aphid population increase. Similarly, vegetable and flower plants grown in greenhouses during the winter months have been shown to be an excellent source of infestation dur ing the following spring, and incidence of leafroll in potatoes can be directly related to the abun dance of aphids in home gardens. Inspection of garden centers and treatment of seedlings found infested with aphids can be important elements of the overall potato leafroll reduction effort. As is usually the case with aphids, green peach aphid populations tend to be higher when plants are fertilized liberally with nitrogen fertilizers. Because some of the virus diseases transmitted by green peach aphid are persistent viruses, which typically require considerable time for acquisition and transmission, insecticides can be effective in preventing disease spread in some crops. For exam ple, potato leafroll virus is transmitted within the potato crop principally by wingless aphids moving from plant to plant. Infected seed potatoes are the principal source of leafroll in most potato crops, so planting disease-free seed is obviously an important step in minimizing the incidence of the disease. Insecticides may not keep winged aphids from alighting in a crop and quickly transmitting non persistent virus, but they can certainly prevent the

secondary spread of virus within a crop by coloniz ing aphids. However, insecticide resistance is a severe problem in many areas. Application of min eral oil and use of aluminum or white plastic mulch reduces virus transmission. Aphids that are not effectively repelled by reflective mulch seem to thrive on mulched crops and exhibit high rates of reproduction. Therefore, even in mulched crops some aphid control is necessary.

References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, CA, 729 pp van Emden HF (1966) Studies on the relations of insect and host plant. III. A comparison of the reproduction of Brevicoryne brassicae and Myzus persicae (Hemiptera: Aphididae) on Brussels sprout plants supplied with dif ferent rates of nitrogen and potassium. Entomologia Experimentalis et Applicata 9:444–460 van Emden HF, Eastop VF, Hughes RD, Way MJ (1969) The ecology of Myzus persicae. Annu Rev Entomol 14:197–270

Green Stoneflies Members of the stonefly family Chloroperlidae (order Plecoptera).  Stoneflies

Green Vegetable Bug This is Nezara viridula (Linnaeus) (Hemiptera: Pen tatomidae), and is also known as southern green stink bug. The latter name is based on its distribution in the USA, but it now occurs on most continents.  Southern Green Stink Bug

Gregarines of Insects The subclass Gregarinasina currently encompasses about 220 genera and 1,500 named species. The modern day gregarines are a monophyletic group associated with invertebrates, including various

Gregarines of Insects

polychaetes (marine worms), oligochaetes (earth worms), and arthropods. The majority of the gregarines have been described from insect hosts, including a wide variety of aquatic insects and many coleopterans. Normally, these organisms are capable of infecting a certain group of hosts without the involvement of a vector or secondary host. It is likely that the current list of gregarine species represents only a small percentage of the gregarines existing in nature. Gregarines display a high degree of host specificity, and may be restricted to a particular tissue (or site) of a specific life stage of a single insect species. However, certain neogregarines (Mattesia spp.) have been experimentally transmitted to insects of different orders. In many cases, insects may harbor a gregarine complex. Gregarines, lack ing the virulence of other insect disease agents and not possessing a vertebrate counterpart, have not received much attention from pathologists during the past several decades. Morphologically, the gregarines produce mature gamonts which have the conoid structure modified into an epimerite or mucron. The epimerite, often containing attachment hooks, mediates gregarine attachment to the host cell. This anucleated segment, separated from the main cell by a septum, often is lost when the gamont detaches from the host cell. The mucron, unlike the epimerite, lacks the septal structure. Gregarines are divided into four major groups: the Archigre garines, Blastogregarines, septate Eugregarines, and Neogregarines. The primitive archigregarines and blastogregarines are parasites of the digestive tracts of marine worms and annelids. The life cycle of these latter gregarines includes three schizogo nies: merogony, gametogony, and sporogony. The Eugregarine group, believed to arise from an ancestral archigregarine, contains the vast major ity of the described gregarines (1,300 species). Most eugregarines that are detrimental to the host insect are found within the genus Ascogregarina. The life cycle of the eugregarines, unlike the archigregarines or neogregarines, lacks the merogony phase. Host insects ingest the dormant oocyst stage that is activated to release infectious sporozoites that exit through the

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polar canals. Excystation is a pH-sensitive event and, therefore, may be regulated by the pH gradi ent existing in the insect’s digestive tract. Excysted sporozoites (4–8 per oocyst) migrate to the midgut epithelium and undergo both intracellular and extracellular growth phases. Upon attaching to the midgut epithelia, sporozoites differentiate and pro duce either epimerite (septate gregarine) or mucron (aseptate gregarines) attachment structures. These cells, referred to as trophozoites or gamonts (Fig. 56), may penetrate the midgut or remain attached to the microvillar surface. Individual gamonts undergo extensive growth, reaching a size that may be measured in millimeters. Normally, the fully mature detached gamont is the stage that is detected in infected insects. Mature gamonts detach them selves from the midgut and pair off in the lumen, forming a prenuptial association known as syzygy. A membrane is formed around the paired gamonts, forming the gametocysts that are expelled in feces. Within the gametocyst one of the gamonts pro duces microgametes and the second gamont devel ops macrogametes. Alternatively, both gamonts may produce isogametes. The gametes fuse, pro ducing a diploid zygote that undergoes successive meiotic and mitotic divisions, resulting in a thickwalled oocyst filled with haploid sporozoites.

Gregarines of Insects, Figure 56 Light micrograph of septate gamonts of Gregarina blatteria attached to cockroach midgut surface.

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Gregarines of Insects

Eugregarines lacking the merogonic cycle are unable to multiply and spread within host insects. The number of gamonts found in the host is a direct reflection of the number of sporozoites released from the ingested oocysts. The impact of gregarines inhabiting the digestive tract is often negligible; damaged host cells are replaced with out a noticeable impact on the host insect. For example, the mealworm Tenebrio molitor is host to Gregarina polymorpha, and can harbor up to 6,000 gamonts in its digestive tract without any pathological effect. In certain cases, these organ isms are considered commensals. However, in other cases, the presence of these gregarines results in a measurable impact on the host. Large numbers of gregarines often damage the gut bar rier and allow opportunistic microbes to invade and kill the host. This is especially true for the coelomic gregarines that penetrate the midgut and develop in the hemocoel. Normally, the impact of these organisms is subtle and cannot be measured simply in terms of insect mortality. For example, Ascogregarina barretti does not kill infected Aedes triseriatus, but results in the pro duction of short winged adults. Similarly, under appropriate environmental conditions, infection by the aseptate gregarine Ascogregarina culicis alters the developmental kinetics and reduces the survival fitness of the host mosquito Aedes aegypti. A second aseptate gregarine, Ascogregarina chagasi, has been reported to cause popu lation declines in laboratory colonies of the dipteran Lutzomyia longipalpus. The order Neogregarinida includes the neogregarines characterized by their additional merogonic life stage. Neogregarines are found commonly in members in the orders Lepidoptera, Coleoptera, Hemiptera, Diptera, and Orthoptera and include the well-studied genus Mattesia. Neogregarines are transmitted orally and display a high level of host specificity. These gregarines usu ally are smaller than the eugregarines and possess a nonsegmented body plan. The oocyst stage of neogregarines is ingested and the digestive fluids act on polar caps (plugs), allowing for the release

of the infectious sporozoites. The sporozoite penetrates the midgut and invades the fat body. Within this tissue, the sporozoites develop and give rise to micronucleate meronts. These meronts grow, producing multinucleate cells that measure 20–30 µm in length, and contain 30–200 nuclei. The nuclei move to the peripheral region and bud from the meront, releasing motile, elongate mero zoites. These motile merozoites, released from infected cells, infect other healthy cells, spreading the infection through the target tissue(s). The merozoites, after undergoing one or more cycles, eventually undergo macronuclear merogony. The exocellular budded macronuclear merozoites round up and transform into gamonts, thus initi ating the sexual phase. The gametocytes form pairs that synthesize an envelope and transform into the gametocyst. The gamonts within the cyst each produce a set of gametes that fuse to form the zygote. The zygotes develop a spore wall forming the oocyst. The zygote undergoes division, produc ing a set of sporozoites within the oocyst or spore. The best-studied genus of insect neogregarines is Mattesia. The species M. grandis, pathogenic to the cotton boll weevil, Anthonomous grandis, has been examined as a microbial control agent. Under insectary conditions, M. grandis was found to cause epizootics and to decimate laboratory colonies. In the mid-1960s, this pathogen was mass-produced in host weevils. Spores harvested from infected adults were bait formulated and tested against wee vil populations. Field-cage experiments demon strated that spores delivered as baits could infect weevils. The high cost of production and erratic field performance has limited subsequent interest in this pathogen.

References Cook TJP, Janovy J Jr, Clopton RE (2001) Epimerite-host epi thelium relationships among eugregarines parasitizing the damselflies Enallagma civile and Ischnura verticalis. J Parasitol 87:988–996 Levine ND (1988) The protozoan phylum Apicomplexa, vol 1. CRC Press, Boca Raton, FL.

Gregarious Behavior in Insects

Schrevel J, Caigneaux E, Gros D, Philippe M (1983) The three cortical membranes of the gregarines. I. Ultrastructural organization of Gregarina blaberae. J Cell Sci 61:151–174 Siegel JP, Novak RJ, Maddox J (1992) Effects of Ascogregarina barretti (Engregarinida: Lecudinidae) infection on Aedes triseriatus (Diptera: Culicidae) in Illinois. J Med Entomol 6:968–973 Sulaiman I (1992) Infectivity and pathogenicity of Ascogregarina culicis (Eugregarinida: Lecudinidae) to Aedes aegypti (Diptera: Culicidae). J Med Entomol 29:1–4

Gregarious Behavior The tendency of organisms to stay in groups.

Gregarious Behavior in Insects Gregory A. Sword University of Sydney, Sydney, NSW, Australia Many insects spend time in a group of conspecifics at some point during their lives. Insect groups can form passively, for example, through the common use of feeding, mating, oviposition, basking or shel ter sites. Alternatively, insect aggregations may arise through the detection and active movement toward conspecifics or their associated cues. Cues used to detect the presence of conspecifics can be tactile, visual, auditory, olfactory or pheromonal, and may act alone or in combination. Gregarious behavior is commonly associated with social insects that live in communal colo nies (see Sociality of Insects), but it is also wide spread among the non-social insects considered here. In these cases, insect groups of various sizes form under a myriad of conditions and are often interchangeably referred to as aggregations, asso ciations, clumps and other such terms. Impor tantly, gregariousness is not limited solely to insects, but rather is widespread throughout the animal kingdom (e.g., fish schools and bird flocks). As such, the study of group living and its population level consequences are active areas of behavioral, ecological and evolutionary research.

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Entomological studies have played important roles in all of these disciplines. In general terms, insect groups are considered as associations among multiple conspecifics at some point in space and time. Although a precise definition of groups and their respective sizes that might be appropriate for all non-social insects is lacking, this omission is largely irrelevant to the study of gregariousness. The conditions under which insects aggregate, the developmental stages during which aggregation occurs, as well as the physiological and behavioral mechanisms that underlie their formation have all been found to vary among and even within species (Fig. 57). The evolution and maintenance of gregari ousness necessarily requires the benefits of group formation to outweigh the corresponding costs in terms of individual fitness consequences. Empirical and theoretical studies investigating the benefits of grouping have historically out numbered those concerned with measuring its costs. Even more rare are integrative empirical studies that have attempted to examine both the costs and benefits of gregariousness within sin gle species. Comparative phylogenetic analyses that seek to examine the evolutionary relation ships between gregariousness and other ecologi cal, morphological and behavioral traits are similarly rare, but have provided important insights and will likely increase as phylogenetic frameworks become available for a variety of different insect lineages. Some of the many examples of the costs and benefits of gregariousness in insects are provided below. When considering these examples, it is important to keep in mind that they are by no means mutually exclusive. Multiple benefits, as well as costs, may be at play and those benefits that initially favor the evolution of gregariousness need not be the same ones responsible for its mainte nance. Indeed, a broad consensus has emerged that no single factor likely serves as a general explanation for the evolution and maintenance of gregarious behavior, or the lack thereof, among insect species.

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Gregarious Behavior in Insects, Figure 57 A dense aggregation of Doratifera casta caterpillars. Doratifera casta expresses ontogenetic variation in gregariousness. Larvae are gregarious during the early instars, but become solitary in later stages. Gregariousness confers at least two advantages during early stages of development, facilitation of feeding and functioning as part of an aposematic anti-predator strategy. Their subsequent switch to a solitary lifestyle suggests that these advantages disappear or are outweighed by costs associated with intraspecific competition during the final instars. (Photo by Dieter Hochuli.)

Benefits of Gregarious Behavior Mate Finding Many insects that are otherwise solitary-living form groups during the process of finding a mate. In acoustically signalling insects such as crickets and some grasshoppers, males can be attracted to the calls of conspecific males, resulting in local aggregations. Males in these groups often have a higher probability of securing a mate than their solitary counterparts. Among desert clicker grass hoppers, Ligurotettix coquilletti, which tend to aggregate in this manner, males selectively chose the highest quality food plants from which to call. Thus, a male’s call may also serve as an indicator of host plant quality to females. Insects in a variety of orders also form leks in which males aggregate

and display to attract mates. Females visit these sites only to mate and typically gain no other resources. The advantage to females afforded by leks appears to be the choice of a large number of potential mates and the opportunity to simultane ously assess the quality of multiple males. The advantage to males of participating in leks is less clear, but is likely related to the prediction that the rates of female visiting and mating should increase with lek size, thereby increasing the average num ber of matings per male participant in the lek.

Facilitation of Feeding Gregarious insects are often able to obtain food resources that they would otherwise be unable to consume as solitary individuals. Nymphs of the


two-spotted stinkbug, Perillus bioculatus, feed together on caterpillars and beetle larvae. Older and larger nymphs are better able to overcome prey defenses than are the smaller and younger nymphs that often join them in feeding. Older nymphs likely benefit from the assistance provided by younger nymphs in subduing larger prey, whereas the younger nymphs gain access to other wise unobtainable prey items. Among herbivorous insects, there are many examples in which individuals in larger groups develop at an increased rate compared to smaller groups or lone individuals. Grouped larvae of the neotropical nymphalid Chlosyne janais achieve this benefit either by inducing a nutrient sink in the damaged leaf or by overcoming an induced defen sive response on the part of their host plant. In the eucalyptus-feeding beetle Chrysophtharta agricola, neonate survivorship increases with group size because feeding sites on tough leaves initiated by larvae with larger mandibles provide smaller individuals with access to feeding sites. Milkweed bugs, Oncopeltus fasciata, feed on seedpods and also survive better in larger groups. In this case, the joint secretion of lytic enzymes by multiple individuals facilitates the ingestion of nutrients from the seeds within the pod.

Microhabitat Modification Insect aggregations can serve to buffer group members from harsh environmental conditions. Aggregations of Blattella germanica cockroach nymphs enable group members to better survive under dry conditions. The diffusion fields of water vapor overlap among group members and reduce individual evaporative water loss to the air. Anti-desiccant effects have also been observed in aggregations of other insects such as woodlice, stinkbugs and beetles. Clustering of eggs by ovipositing females similarly functions to prevent water loss by reducing the amount of exposed surface area. Importantly, this strategy of egg clustering may serve as one of the principle

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echanisms underlying the initial formation of m many larval insect groups. Grouping has also been shown to play an important role in thermoregulation. Higher body temperatures in grouped versus solitary caterpil lars have been observed in a number of different lepidopterans. These higher temperatures result in faster growth rates and reduced development times that in turn can reduce the risk of exposure to predators, parasitoids or pathogens, and possi bly allow the insects to outpace a decline in host plant quality. Some gregarious insects even build structures within which their microhabitat is modified. For example, temperatures inside the tent shelters constructed by eastern tent caterpil lars, Malacosoma americanum, have been shown to be higher than outside air temperatures.

Protection from Natural Enemies By far the most commonly invoked benefit of gre garious behavior is protection from natural ene mies such as predators and parasitoids. The notion that individual attack risk declines as group size increases has been widely referred to as the “selfish herd” effect. In other words, the reduction in attack risk provides individuals with a selfish motive to join a group. However, a number of different underlying mechanisms, both passive and active, may be responsible for conferring protection to individual group members. Similarly, as evidenced by the other benefits described above, instances in which the improved survivorship of insects in groups was assumed to be due to protection from natural enemies may actually have been due to other unrecognized benefits of group living. The simplest scenario for protection in a group is a dilution effect in which the risk of attack to an individual group member is inversely pro portional to the size of the group. However, few if any insects rely solely on a dilution effect for pro tection. They often also have some means of active defense such as early detection, evasion, chemical defense and warning coloration (aposematism).

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Groups of sea-skaters, Halobates robustus, detect and respond to predators from a greater distance than do solitary individuals. Once a predator attack has been initiated, insects in dense groups will often flee in erratic patterns that are assumed to either startle or confuse predators, or reduce the predictability of prey locations. Given that individual predators have an upper limit to the number of prey they can con sume, sufficiently high numbers of insects in aggregations may effectively swamp or satiate local predators and confer the benefit of reduced predation on surviving group members. Preda tor swamping has been proposed for mass emerging insects such as mayflies and periodi cal cicadas, and likely operates during outbreak periods in insects such as locusts (e.g., Schistocerca spp.) and Mormon crickets (Anabrus simplex) that exhibit widely fluctuating local population dynamics. Many gregarious insects are also aposematic. These insects utilize conspicuous warning color ation as a signal to potential predators that they are deterrent or unpalatable by virtue of possess ing some form of defense, usually chemical. The relationship between insect gregariousness and the evolution of both unpalatability and warning coloration has been the source of long running debate. Theoretical and empirical evidence suggest that grouping can facilitate the evolution of chem ical defenses, as well as enhance predator learning of warning coloration. Based on this, it has been hypothesized that gregariousness initially pro motes the evolution of unpalatability, followed by the evolution of conspicuous warning coloration. Despite the seeming logic behind this argument, a series of phylogenetic analyses using lepidopteran larvae suggest a different polarity for the evolution of these traits. These analyses indicate that gregari ousness has repeatedly evolved after, rather than before, unpalatability and warning coloration. Thus, although it seems likely that defenses have evolved prior to warning coloration and gregari ousness, the precise polarity of events could feasibly vary among taxa depending on the specific

ecological circumstances. Additional phylogenetic analyses in other insect lineages will be critical in resolving this issue.

Costs of Gregarious Behavior Intraspecific Competition One of the most obvious and widely documented costs of gregariousness is intraspecific competi tion. As more individuals share a limited resource, the amount available per individual decreases. Food, mates, and sites for shelter, basking or ovi position can all be limiting resources. Some insects such as bark beetle larvae may deplete their food sources and die before reaching the more mobile adult stage. In others such as aphids, the effects of competition may be less severe but still result in restricted access to nutrients, smaller adult size and reduced fecundity. Perhaps the most extreme form of intraspecific competition is cannibalism, the threat of which can be particularly severe among larval forms of insects that feed in enclosed environments such seeds, fruit, stems, and stored products. Cannibalism can also serve as an impor tant mechanism by which individual insects redress nutritional imbalances brought on by increased competition for resources at high popu lation densities.

Pathogen Transmission Another clear cost of living in a group is the increased risk of becoming infected with a patho gen or parasite. An increased probability of fungal pathogen infection among group members has been shown in a variety of insects such as aphids, cicadas, caterpillars, and beetle larvae. Both patho gens and parasites can be spread by direct contact with infected individuals as well as their excre ment and saliva. Alternatively, propagules from infected individuals may be rapidly dispersed locally among group members through the air or


across the substrate surface where they can be sec ondarily encountered. Some insects have evolved an elegant solution to the increased risk of patho gen infection in crowds by incurring the metabolic cost associated with pathogen resistance only under high population density conditions. This form of density-dependent pathogen resistance or prophylaxis has been demonstrated across insect orders in taxa such as Tenebrio molitor beetles, Spodoptera exempta caterpillars, and Schistocerca gregaria locusts.

Increased Conspicuousness to Predators A group of insects should simultaneously be more apparent to predators and more worthwhile as a source of potential food than solitary prey. The cost of increased conspicuousness in a group should be even greater for aposematic insects that are themselves conspicuously colored. That so many gregarious insects exist in the first place sug gests that this cost is routinely surmounted by at least one of the benefits described above. In addi tion to providing a larger visual stimulus to preda tors, aggregations may also result in the local concentration of other cues used by natural ene mies to find insect prey. Predators and parasitoids can locate their prey directly by orientation toward cues such as aggregation pheromones or the sound of calling males, as well as indirectly through cues such as volatile compounds emanating from frass or plant tissues exposed by feeding damage.

Physiological Costs Among insects that use aggregation pheromones for group formation, pheromone production necessarily involves a metabolic cost. For example, these costs may range from minimal when pheromones are by-products of existing metabolic pathways and structures as they appear to be in Phylotretta cruciferae flea beetles, to more substantial when pheromone production requires the development

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and maintenance of specialized glands or organs as in the triatomine bugs. Furthermore, aggregation pheromone production has been shown in some beetles to be regulated and can be reduced under crowded conditions. However, it is not yet known if this facultative response serves to reduce metabolic costs or is perhaps an adaptation that reduces some other cost associated with crowding.

Population Level Consequences of Gregarious Behavior Gregariousness not only affects the performance and survivorship of individual insects, but can also have important population level consequences. The expression of gregarious behavior can interact with other ecological processes to influence a species’ population dynamics, dispersal or migra tion, and spatial distribution patterns. Gregarious behavior in insects can sometimes lead to devastat ing consequences for humans, as evidenced by its central role in the biology of two major pest spe cies, the desert locust, Schistocerca gregaria, and the Mormon cricket, Anabrus simplex.

The Desert Locust Under outbreak conditions, locusts form huge groups in which millions of insects can travel en masse on the ground in migratory bands as juveniles and in the air as characteristic swarms of flying adults. Unlike other grasshoppers, locusts can express an extreme form of density-dependent phenotypic plasticity known as “phase polyphenism.” Individuals reared under low population densities (the harmless, non-migratory “solitarious” phase) differ markedly in behavior, physiology, color and morphology from locusts reared under crowded conditions during outbreaks (the migratory swarming “gregarious” phase) (Fig. 58). A shift to the expression of gregarious behavior at high pop ulation density is central to the process of locust phase change. This form of behavioral phenotypic

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Gregarious Behavior in Insects, Figure 58 Gregarious behavior in locusts is environmentally determined and mediated by changes in local population density. Examples of the alternative density-dependent phenotypes of final instar desert locust nymphs, Schistocerca gregaria, are pictured. The non-migratory and cryptic “solitarious” phase produced at low population density is on the left. The migratory and aposematic “gregarious” phase induced by high population density is on the right. (Photo by Greg Sword.)

plasticity suggests that natural selection has favored, within the same individual, the ability to lead a solitary lifestyle when it is advantageous at low population densities, as well as the ability to take advantage of gregariousness under high popula tion density conditions. At the heart of locust swarm formation and migration is the shift from the shy, cryptic behavior of solitarious phase locusts, which are relatively sedentary and avoid one another, to the highly active behavior and tendency to aggregate typical of gre garious phase insects. Nymphs of the desert locust, Schistocerca gregaria, can become behaviorally gregarious after just 1 h of crowding. This behavioral transition to gregariousness is soon followed by changes in other traits. One such change is a shift in feeding behavior in which the newly crowded insects become willing to feed on noxious plants that cause the locusts to be toxic to their predators. In turn, these behavioral changes are followed at the next

nymphal molt by a density-dependent change in coloration from crypsis to warning coloration that enables the nymphs to advertise their recently acquired unpalatability to predators. Predator learning and subsequent avoidance of aposematic gregarious phase locust nymphs can reduce the per capita pre dation risk and facilitate additional population growth. In addition to functioning as part of an apos ematic anti-predator strategy, gregariousness in desert locusts also interacts with local habitat structure resulting in some habitats being more likely than others to generate locust swarms. Individual locusts are more likely to come in contact with each other and change into the migra tory gregarious phase when the resources they utilize, such as host plants or roosting sites, are dis tributed in an aggregated as opposed to dispersed manner. As more and more locusts become gregarious, they also become locally concentrated,


and once a critical population density is reached, mass migration is triggered. Recent evidence suggests that mass movement among juvenile locusts in migratory bands is mechanistically linked to the risk of cannibalism in high-density groups, a process first identified in Mormon crick ets and described below.

The Mormon Cricket Mormon crickets are flightless tettigoniids from western North America that also form huge migratory bands during outbreaks. Although Mormon cricket and locust migratory bands share many similar characteristics, Mormon crickets do not appear to express the densitydependent phase changes in gregariousness or other traits as do locusts. Thus, the phenomenon of migratory band formation (Fig. 59) and move ment appears to have convergently evolved in

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these two groups via different underlying behav ioral mechanisms. Mormon crickets constitute a unique model system in which understanding the costs and benefits of gregariousness has provided a unifying framework that explains both how and why interindividual interactions can lead to landscape- scale mass movement. In terms of benefits, a radiotelemetry-based mark recapture study revealed that migratory bands form as part of an anti-predator strategy. Individual band members are much less likely to be killed by predators than are insects that have been separated from the group. As predicted, once migratory bands have formed, individual band members are subject to increased intraspecifc competition for nutritional resources. Individual crickets within migratory bands have been shown to be deprived of specific nutritional resources, namely protein and salt. When provided with augmented dietary protein, individual crick ets spent less time walking, a response that was not

Gregarious Behavior in Insects, Figure 59 A migratory band of Mormon crickets, Anabrus simplex, crossing a dirt road in NE Utah, USA. Migratory bands can contain millions of insects that walk up to 2 km/day. Gregariousness confers protection from predators. However, band members suffer from intraspecific competition and must keep moving to encounter new nutritional resources as well as to avoid being cannibalized by other hungry insects in the band. (Photo by Greg Sword.)

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Gregarious Parasitoid

found when crickets had ample carbohydrate. Thus, group movement results in part from loco motion induced by protein deprivation and should act to increase the probability that individual band members will encounter new resources and redress their nutritional imbalances. An additional cost of group formation is that Mormon crickets are notoriously cannibalistic. Their propensity to cannibalize is a function of the extent to which they are nutritionally deprived. Given that Mormon crickets are walking pack ages of protein and salt, the insects themselves are often the most abundant source of these nutrients in the habitat. As a result, individuals within the band that fail to move risk being attacked and cannibalized by nutritionally deprived insects approaching from the rear. Thus, the mass movement of individuals in migratory bands is a forced march driven by cannibalism due to individuals responding to their endoge nous nutritional state. The fact that migratory bands are maintained as cohesive groups despite these conditions suggests that the risk of preda tion upon leaving the band must outweigh the combined costs of intraspecific competition for resources and cannibalism.  Cycloalexy  Sociality of Insects  Aposematism  Phase Polymorphism in Locusts  Phase Polyphenism in Insects  Juvenile Hormone

References Hunter AF (2000) Gregariousness and repellent defenses in the survival of phytophagous insects. Oikos 91:213–224 Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford, UK Prokopy RJ, Roitberg BD (2001) Joining and avoidance behavior in nonsocial insects. Annu Rev Entomol 46:631–665 Reader T, Hochuli DF (2003) Understanding gregarious ness in a larval Lepidopteran: the roles of host plant, predation, and microclimate. Ecol Entomol 28:729–737

Ruxton G, Sherratt T (2006) Aggregation, defense and warn ing signals: the evolutionary relationship. Proc R Soc London B Biol Sci 273:2417–2424 Simpson SJ, Sword GA (2007) Phase polyphenism in locusts: mechanisms, population consequences, adaptive signifi cance and evolution. In: Whitman D, Ananthakrishnan T (eds) Phenotypic plasticity of insects: mechanisms and consequences Science Publishers, Inc., Plymouth, pp 93-135 Simpson SJ, Sword GA, Lorch PD, Couzin ID (2006) Cannibal crickets on a forced march for protein and salt. Proc Natl Acad Sci USA 103:4152–4156 Vulinec K (1990) Collective security: aggregation by insects as a defense. In: Evans DL, Schmidt JO (eds) Insect defenses: adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany, NY, pp 251–288 Wertheim B, Van Baalen EJA, Dicke M, Vet LEM (2005) Pheromone-mediated aggregation in nonsocial arthro pods: an evolutionary ecological perspective. Annu Rev Entomol 50:321–346

Gregarious Parasitoid Parasitoids than can co-exist with others of the same species within the body of a host insect.

Gressitt, Judson Linsley Judson Linsley Gressitt was born in Tokyo in 1914 to an American family. He grew up in Tokyo and was educated at an American school. On finishing school, he traveled alone at age 18 to Taiwan and collected insects in much of the island, including the highest mountains. His first degrees were in entomology at the University of California, after which he accepted a position at Lingnan University in Guangzhou, China. He continued fieldwork, and he married Margaret Kriete. The family was interned in 1941–1943 by Japanese forces in China. After the war, Lin returned to Berkeley and earned a doctor ate in entomology. Then he returned to Lingnan University as Associate Professor until 1951. In 1949 the family was interned again, this time by Chinese forces as the Chinese revolution raged and the Korean War was imminent. His involvement with Pacific entomology and especially with the Bernice

Grote, Augustus Radcliffe

P. Bishop Museum in Honolulu followed. In 1955, he began an association with New Guinea, which led in 1961 to establishment of what is now the Wau Ecology Institute. His research interests covered biogeographic and ecological questions in plants, vertebrates, and invertebrates. His particular taxo nomic interests were in the beetle families Ceram bycidae and Chrysomelidae. But his work included many other projects such as insect disease carriers, Antarctic entomology, transoceanic dispersal, and insect conservation. He was editor of four serial publications. He and his wife, Margaret, died in an air crash in China on April 26, 1982.

Reference Holloway JD (1982) Dr J Linsley Gressitt, 1914–1982. Antenna 6: 285

Grid Mapping Mapping the locations of pests in a field using coordinates.

farm in New York when he was seven. As a schoolboy he spent much time collecting insects. His hopes of attending Harvard University were dashed when his father’s investments failed and the family was left in straitened circumstances. He did, however, receive an A.M. degree from Lafayette College, Pennsylvania, after studies in Europe. In Alabama in the early 1870s, he stud ied the cottonworm, Alabama argillacea, eventu ally publishing five papers on it. On the death of his wife in 1873, he moved to Buffalo, New York, and worked as museum director. He was pub lisher of the Bulletin of the Buffalo Society of Natural History and of a short-lived journal called “The North American Entomologist.” He wrote many articles on Lepidoptera, and pro duced with Coleman Robinson “A synonymical catalog of North American Sphingidae, with notes and descriptions” and a “List of the Lepi doptera of North America.” In 1884 he moved to Germany, first to Bremen and then to Hildesheim, but continued writing for North American journals. For the last nine years of his life, he was honorary assistant at the Roemer Museum in Hildesheim, in which city he died on September 12, 1903. His large insect collection was offered

Gripopterygidae A family of stoneflies (order Plecoptera).  Stoneflies

Grooming Cleaning of the body using the mouthparts or legs. In solitary insects, it is a self-cleaning process, but in social insects individuals groom one another.

Grote, Augustus Radcliffe Augustus Grote (Fig. 60) was born in Liverpool, England on February 7, 1841, of a Welsh mother and German father who moved with him to a

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Grote, Augustus Radcliffe, Figure 60 Augustus Grote.

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Ground Beetle (Coleoptera: Carabidae) Feeding Ecology

for sale in the USA, but when there were no buy ers it was sold to the British Museum (Natural History).

Reference Mallis A (1971) Augustus Radcliffe Grote. pp. 304–308 in American entomologists. Rutgers University Press, New Brunswick, New Jersey. 549 pp.

Ground Beetle (Coleoptera: Carabidae) Feeding Ecology Eric W. Riddick U.S. Department of Agriculture, Agricultural Research Service, MS, USA The Carabidae, or ground beetles, represent approx imately 40,000 described species found throughout the world, with most species present in the tropics. There are nearly 2,700 described species in Europe and over 2,000 species in North America. Detailed biological descriptions are available for fewer than 100 species (mostly western European species). Many carabids are easily recognized at the family level. Adults are well-proportioned beetles with pronounced mandibles and palps, long slender legs, striate elytra, and sets of punctures with tactile setae. Many possess an antenna-cleaning organ and mostly pubescent antennae. Many are dark colored, shiny or dull. Some have bright or metallic colors and some are pubescent. Although carabids possess an easy-to-recognize general body form, they have undergone morpho logical adaptations to suit the habitat in which they are found. Such modifications have permitted running, burrowing in soil and sand, living under tree bark, climbing plants, and swimming in water. Consequently, some species are found in very unique places. For example, some inhabit the edges of ice glaciers, others live in caves, others along stream banks. Others are found in woodlands, or are found in deserts. Most species reside on the

ground (epigeic), but some species are plant-dwelling (arboreal) during the adult stage. Others live in self-constructed tunnels in sand or fine soil. Based upon research in Britain (in Europe), carabid genera are found typically in certain habitats: species of Bembidion are common amongst vegetation alongside rivers and lakes; species of Acupalpus, Agonum, Stenolophus, and smaller-sized Pterostichus are present in litter on the soil surface in marshy (fresh water) habitats. The genera Dicheirotrichus, Dyschirius, and Pogonus are found in salt marshes. Larger-bodied genera such as Calathus, Carabus, Harpalus, Nebria, or Pterostichus can be found in rough grass, or in gardens. In drier habitats, especially exposed to sun, Amara, Badister, some Harpalus and Notiophilus can be found. The location of the preferred habitat (and microhabitat) can be influenced by season, temperature and humidity extremes, life history pattern, competitors, and food availability.

General Feeding Ecology Feeding Preferences Carabid beetles can be categorized as carnivores, herbivores, or omnivores. A recent survey of 1,290 literature references indicated that 775 species were partially or exclusively carnivorous, 85 species were exclusively herbivorous, and 206 species were omniv orous. Some carnivorous species opportunistically feed on a diversity of prey. For example, the diet of numerous species in the genera Agonum, Calathus, Chlaenius, Poecilus, or Pterostichus is most often dependent on the season and availability of specific prey. Other carnivorous species are more selective. Some oligophagous species such as those in the genera Cychrus and Scaphinotus are predators of snails and slugs. Others in the genus Calosoma prey upon caterpillars. Species of Loricera and Notiophilus are predators of springtails (Collembola). Species in the genus Promecognathus specialize upon milli pedes. Some species are parasitoids in the larval stage,


but are predators in the adult stage. For example, the larvae of Lebia spp. are ectoparasitoids of pupae of leaf beetles (Chrysomelidae), whereas the adults attack egg and larval stages. The larvae of Brachinus spp. (bombardier beetles) are ectoparasitoids of pupae of water scavenger beetles (Hydrophilidae) and whirligig beetles (Gyrinidae). Herbivorous carabids may consume plant seeds, ripe fruit, and foliage. Zabrus adults and larvae consume ripe grains and sprouting leaves of cereal plants. Many Harpalus and Amara adults feed on germinating weed seeds. The diet of the larvae, however, is unknown for the majority of species. Several Harpalus species collect and cache seeds of grasses in burrows. Omnivorous carabids are apparently opportunists that feed upon the food items most readily available in their immediate habitat. Many carabid species are likely omnivorous. In fact, predominantly carnivorous species probably consume pollen, fungi, and other plant materials during periods of prey shortage to avoid starvation.

Searching for Food Carabid beetles are known to search actively for food by means of random search, vision, or chemical cues. Most adults rely on random search, in which the beetle contacts the prey with its mouthparts, antennae, or setae on some body part or appendage. This strategy is common to nocturnal species. Very little is known about the searching behavior of cara bid larvae. Presumably, the larvae of most nocturnal species rely on random search and then physical contact with prey. Some carabid larvae do not actively search for prey. Instead, they deploy an ambush strategy. They remain concealed inside burrows or tunnels and only attack prey that come too close to their burrows. This strategy is typical of tiger beetle larvae (tribe Cicindelini; e.g., Amblycheila, Cicindela, Megacephala, and Omus). Diurnal species rely upon short-range vision to locate prey. For example, Notiophilus biguttatus adults and larvae feed extensively on springtails

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(Collembola). Adults are aided by their large compound eyes to hunt their prey. This predator may intensify its search for prey in relation to light intensity. Greater light intensity usually results in an increased search rate. The N. biguttatus larvae rely more on physical contact for detection of prey. Several carabids respond to the odor of their prey to facilitate detection. Adults of Pterostichus melanarius and Harpalus rufipes were attracted to an aphid alarm substance released by aphids under attack by predators, such as ladybird beetles. In contrast, Nebria brevicollis adults were attracted to the odor of live springtails, but not to aphid alarm substance. Note that P. melanarius was also attracted to the odor of live aphids, but the other two species were not. Larvae of N. biguttatus are guided by chemical cues to the aggregation sites of springtails. Reliance upon chemical cues from prey (or hosts in the case of parasitoids searching for concealed prey) is probably more widespread than currently reported. Although most carabids search for prey on the ground, some species seek prey on plants. Calleida, Cymindis, Dromius, Lebia, Parena, Pinacodera, and Plochionus adults have been found foraging on plants during the day. More than 30% of tropical carabid species (e.g., Agra, Lebia) forage on plants. Adults of a few species of Agonum, Amara, Chlaenius, Harpalus, and Pterostichus are occasionally found foraging on plants. Both adults and larvae of Calosoma sycophanta (and other species of Calosoma) forage for prey on the trunks of forest trees.

Prey Capture Once prey is located, some species lunge toward it with their mandibles agape. Most adult carabids use their well-developed mandibles to subdue and kill prey. Morphological and behavioral adaptations can be involved in capturing prey, particularly for the species with specialized feeding habits. Cychrus caraboides and Carabus violaceous successfully subdue slugs (gastropods) by biting them at specific

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locations on the body, which may paralyze prey. This could prevent the production and secretion of mucus by the slugs, a mechanism of defense against predation. Species that specialize on snails are not deterred by the shell. Some Cychrus and Scaphinotus adults readily capture and consume large-sized snails by inserting their slender, elongate head and prothorax into the opening, then proceed to kill and consume the prey. Cychrus larvae crawl inside the shell and feed, in spite of the mucus secretions of the prey. Some generalists such as Pterostichus species can crush shells with their mandibles. Shell thickness could influence the vulnerability of snails to attack from generalist carabids. Prey capture behavior has been described for several species that hunt springtails. Adults and larvae of N. biguttatus rely on vision to capture elusive springtails. Prey capture occurs when the predator rapidly lunges toward the springtail and grasps it within the mandibles. Adults of Loricera pilicornis capture springtails at night. Physical contact, rather than sight, is a prerequisite to prey capture. Adults lunge toward prey during the attack and bring their antennae together to entrap the springtail. Long, strong setae on the antennae enclose the prey and draw it toward the gaping man dibles. The prey capture behavior of L. pilicornis larvae differs from that of adults. Although prey are located by physical contact, the larvae do not lunge toward prey. Instead, larvae turn in the direction of contact while opening their mouthparts. The setae on the maxillae and an adhesive secretion coating the proximal end of each maxilla function to entrap the prey. The springtail is ultimately grasped by the mandibles.

Digestion The adults of most carabids ingest and digest prey fragments, after mastication, with little or no extraintestinal (i.e., pre-oral) digestion. The mandibles are used for crushing or tearing off fragments of food, which then are ingested. Enzymes involved

in digestion are copious once food enters the foregut. In contrast, the adults of other species, particularly in tribes Carabini (e.g., Calosoma, Carabus), Cicindelini (e.g., Cicindela, Omus), and Cychrini (e.g., Cychrus, Scaphinotus, Sphaeroderus) masticate their prey only to lubricate it and extract the fluid contents from it. Extra-intestinal diges tion commences after adults discharge a fluid from their buccal cavity (mouth) onto the prey or prey fragments. This fluid contains enzymes (proteases, carboxylases, amylases, etc.) that liquefy tissues. These enzymes are synthesized in the midgut, but are stored in the crop, from whence they are regur gitated onto the food prior to feeding. Only very fine particles and liquefied remains of prey are ingested. Digestion proceeds within the foregut, including the crop. Absorption of nutrients occurs primarily in the midgut. As far as is known, cara bid larvae digest their food extra-intestinally. Once liquified food is ingested, the digestion process continues in the foregut, with absorption occur ring primarily in the midgut. Carabid larvae that are ectoparasitoids (e.g., Brachinus, Graphipterus, Lebia) may rely almost exclusively on extraintestinal digestion of host tissues.

Applied Feeding Ecology Predation of Aphids and Leafhoppers In sugar beet fields, carabid adults (especially Pterostichus dorsalis) were capable of reducing aphid (Aphis fabae) population densities in field cages. Carabids, even when at relatively low densities, were able to locate low density populations of aphids. The impact of carabids and wolf spiders (Class Arachnida, Order Araneae, Lycosidae) on leafhopper (Cicadellidae) and aphid populations was assessed in maize fields. The abundance of both predator groups was manipulated by remov ing or adding individuals within field enclosures during mid-season and end-of-season. Although the impact of carabid predation could not be dif ferentiated from spider predation, the combined


action of both predator groups reduced popula tions of leafhoppers. In addition, the combined predators were capable of reducing aphid popula tions during mid-season. Research in cereal fields indicated that the rate at which aphids (Sitobion avenae) dropped from plants to escape predators on the plants was critical to the efficacy of carabid predation on the ground. Carabids intercepted many aphids before they could climb back up on the plants. The effect of generalist predators functioning in-concert to impact aphid populations was investigated in experiments deploying carabids and lady beetles (Coccinellidae) in alfalfa fields. Positive predatorpredator interactions occurred between the lady beetle Coccinella septempunctata, and the carabid Harpalus pensylvanicus. In laboratory arenas and in field cages, both predators fed on pea aphids, Acyrthosiphon pisum. Predation rates were greater than expected for the combined action of both predators. Thus, synergism occurred as C. septempunctata foraged on plants and H. pensylvanicus foraged at the base of the plants.

Predation of Flies Predation of gall midge (Cecidomyiidae) larvae on the soil surface was found to be considerable, since polyphagous predators were responsible for 43–58% reduction of wheat gall midges (Contarinia tritici). Predation caused an 81% decrease in adult emer gence of the midge Sitodiplosis mossellana. Feeding bioassays in the laboratory indicated that the carabids P. melanarius and Platynus dorsalis were primarily responsible for the decline of S. mossellana populations. Carabid predation of the cabbage root fly (Delia radicum) and other anthomyiid species has been examined. Carabids (especially Bembidion lampros and Trechus quadristriatus) caused approximately 30% mortality of D. radicum by predation of eggs and first instar larvae in the soil. In a greenhouse experiment, a predator density of two Bembidion tetracolum adults per plant

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revented an infestation of D. radicum in the p spring season. Carabid predation caused an 82% reduction of the pest population, when D. radicum eggs were exposed on the soil surface. But, other carabid species (B. tetracolum) had difficulty locat ing eggs that were buried just beneath the surface. Bembidion quadrimaculatum adults located onion maggot (Delia antiqua) eggs that were buried 1 cm deep in the soil. Up to 25 eggs were consumed daily under laboratory conditions and onion maggot numbers were reduced by up to 57% in field cages. Another study investigated the impact of predation on D. antiqua pupae exposed on the soil surface in corn fields. Carabid beetle abundance was manipulated so that the rate of removal of pupae from field exclosures (exclud ing vertebrates but not invertebrates) was deter mined during the growing season. Significantly more onion maggot pupae were removed from the cages that excluded vertebrates than from the cages that excluded both vertebrates and inverte brates. Carabid abundance correlated positively with predation rates. Feeding trials in the labora tory indicated that the four most abundant carabids (Pterostichus and Poecilus species) in corn fields readily consumed D. antiqua pupae.

Predation of Beetles Carabids can be significant predators of the Colorado potato beetle Leptinotarsa decemlineata (Chrysomelidae), a pest of cultivated potato. In Bavaria (Germany), predation of larvae by Carabus spp. reduced the yield damage from this pest by approximately 33% in experimental plots compared to infested control plots that did not contain Carabus adults. Carabus consumed from 8 to 10 L. decemlineata larvae (third and fourth instars) per day in the laboratory. In the United States, Lebia grandis larvae are confirmed ectoparasitoids and adults are special ist predators of L. decemlineata on cultivated potato. In the late 1930s, several years after the inadvertent introduction of L. decemlineata into

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France, L. grandis was imported from the United States and a mass rearing program was initiated. The rearing technique was capable of generating large quantities of L. grandis, but was too labor intensive. Released adults had little demonstrable impact on L. decemlineata populations and failed to become established in France. Carabid predation of weevils (Curculioni dae) was documented. One study revealed that 28% of Sitona hispidulus eggs were removed by carabids when placed in experimental cages in alfalfa fields. Of the carabid species tested, Amara aenea was the most efficient predator. Carabid predation resulted in greater than 30% reduction of larvae and overwintering adults of Sitona lineatus in field beans. Bembidion properans adults consumed S. lineatus eggs and young larvae. Predation of the rape blossom beetle, Meligethes aeneus (Nitidulidae) by the carabid Clivina fossor was documented. In a two-week period C. fossor adults consumed 65% of M. aeneus larvae and pupae that had been introduced into an arena containing soil at a depth of 6–7 cm. Another investigation indicated that M. aeneus experienced a 39% population decline, perhaps, during the time that mature larvae had left the crop plants (rape) and wandered on the soil surface, prior to pupation. Predation by polyphagous predators was thought to be responsible for the decline of the pest population. Research is ongoing to deter mine the contribution of different species to the mortality of Meligethes spp.

Predation of Moths In the early 1900s, Calosoma sycophanta was introduced into northeastern United States to control the gypsy moth Lymantria dispar (Lyman triidae), an inadvertently introduced pest of forest and shade trees. The beetle is well-established in most areas where gypsy moth is distributed, and is an important arthropod natural enemy of larval and pupal stages. Adult C. sycophanta are long-lived

(2–4 yr) and even a low density of beetles can have considerable impact on L. dispar popula tions. A single C. sycophanta larva can kill more than 50 late instar L. dispar larvae during a two-week time span, whereas, an adult can kill an average of 150 late instar larvae. Unfortunately, this carabid has a slow numerical response to pest population densities and has not been able to pre vent gypsy moth outbreaks. In apple orchards, carabids are important predators of codling moth, Cydia pomonella (Tortricidae), a worldwide pest of pome fruit, including apple. Carabids can forage on the ground during the season when mature larvae are wandering on the soil surface before pupation in leaf litter or under loose tree bark. Several carabid species from an apple orchard in Canada gave positive serological reactions to antiserum against C. pomonella larvae. Pterosticus species consumed C. pomonella mature larvae in experi mental arenas in the laboratory. In the field, tethered mature larvae were located and then killed by carabids; 60% predation by carabids per night was estimated during the first generation of codling moth in the spring in an apple orchard in northern California, USA. Pterostichus californicus, Pterostichus cursitor, and Pterostichus lustrans dominated the carabid assemblage in an unsprayed orchard in northern California. Maize plants suffered significantly less dam age from armyworms Pseudaletia unipuncta (Noctuidae) when ground-foraging predators were included in experimental arenas rather than excluded from arenas. Carabid predation of armyworms was thought to be responsible for the reduction. Pterostichus chalcites, Pterostichus lucublandus, and Scarites subterraneus adults readily consumed second and fourth instar P. unipuncta larvae in the laboratory. A laboratory and field investigation assessed the impact of carabid predation on diamondback moth Plutella xylostella (Yponomeutidae) larvae on seedling cabbage plants in Japan. The highest consumption rate (of 24 carabid species tested) was 23 larvae (fourth instars) per day by Chlaenius

Ground Beetle (Coleoptera: Carabidae) Taxonomy

posticalis adults. Note that C. posticalis and Chlaenius micans larvae consumed approximately 92 and 191 early fourth instar P. xylostella larvae, respectively.

Conclusion Despite their generally accepted role as natural enemies, detailed information on the feeding ecology of carabids is not available for many species. More research is needed to clarify the trophic relations of carabid larvae. Carabids appear to affect the populations of some crop pests. Carabids may have their greatest impact when operating in concurrence with other natu ral enemies.

References Chaboussou F (1939) Contribution à l’ étude biologique de Lebia grandis Hentz, prédateur américain du Dory phore. Annales des épiphyties et de Phytogénétique 5:387–433 Digweed SC (1993) Selection of terrestrial gastropod prey by Cychrine and Pterostichine ground beetles (Coleoptera: Carabidae). Can Entomol 125:463–472 Hagen KS, Mills NJ, Gordh G, McMurtry JA (1999) Terres trial arthropod predators of insect and mite pests. In: Bellows TS, Fisher TW (eds) Handbook of biological control: principles and applications of biological con trol. Academic Press, San Diego, CA, pp 383–503 Hengeveld R (1980) Polyphagy, oligophagy and food special ization in ground beetles (Coleoptera, Carabidae). Neth J Zool 30:564–584 Kromp B (1999) Carabid beetles in sustainable agriculture: a review on pest control efficacy, cultivation impacts and enhancement. Agric Ecosyst Environ 74:187–228 Lang A, Filser J, Henschel JR (1999) Predation by ground beetles and wolf spiders on herbivorous insects in a maize crop. Agric, Ecosyst Environ 72:189–199 Larochelle A (1990) The food of carabid beetles (Coleoptera: Carabidae, incl. Cicindelinae). Association des Ento mologistes Amateurs du Québec. Fabreries, Suppl 5:1–132 Losey JE, Denno RF (1998) Positive predator-predator inter actions: enhanced predation rates and synergistic sup pression of aphid populations. Ecology 79:2143–2152 Lovei GL, Sunderland KD (1996) Ecology and behavior of ground beetles. Annu Rev Entomol 41:231–256

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Luff ML (1991) Carabidae. In: Cooter J (ed) A coleopterist’ s handbook, 3rd edn. The Amateur Entomologist’ s Soci ety, Middlesex, UK, pp 69–72 Menalled FD, Lee JC, Landis DA (1999) Manipulating carabid beetle abundance alters prey removal rates in corn fields. BioControl 43:441–456 Stork NE (ed) (1990) The role of ground beetles in ecological and environmental studies. Intercept, Andover, UK Suenega H, Hamamura T (1998) Laboratory evaluation of carabid beetles (Coleoptera: Carabidae) as predators of diamondback moth (Lepidoptera: Plutellidae) larvae. Environ Entomol 27:767–772 Thiele HU (1977) Carabid beetles in their environments: a study on habitat selection by adaptations in physiology and behaviour. Springer-Verlag, Berlin, Germany

Ground Beetle (Coleoptera: Carabidae) Taxonomy Paul M. Choate University of Florida, Gainesville, FL, USA There are approximately 110 families of beetles found worldwide. The order Coleoptera is subdi vided into two major sub-orders, Adephaga and Polyphaga. Polyphaga contains most beetle species. Ground beetles are placed in the sub-order Adephaga. This sub-order contains relatively few families of beetles, most families belonging to the much larger sub-order Polyphaga. As now defined, Adephaga contains the families Gyrinidae, Halipli dae, Trachypachidae, Noteridae, Amphizoidae, Dytiscidae, Hygrobiidae, and Carabidae. Adult Adephaga are separated from all other beetle fami lies by the presence of a visible notopleural suture on the prothorax; six visible abdominal sterna; with the first 3 segments fused and divided by hind coxae (Figs. 61–64). Many species are capable of flight and possess fully developed flight wings. Ground beetles range in size from less than 1 mm to more than 60 mm in length. Most ground beetles are uniformly dark in color, but some species are brightly colored (especially tropical species). Carabids occur throughout the world, and may be found from sea level to altitudes of above 5,000 m in the Himalayas. Although there is diversity of form among carabid tribes (Figs. 65–74), the large number of species in

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Maxillary palpus

Notopleural suture

Antennae Labial palpus Mandible

Maxilla

Tarsus

sm Eye

Gula Pepl

Proepisternum ps

1

cc

2

Femur Prosternal Epimeron Mesepisternum Mesosternal epimeron Mesepisternum

psp ms

3

cc

4 5

Metasternum acp c c

6

Tibia

Gena

epi

Mesotarsus

t

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 61 Ventral view of adult ground beetle.

Mesotibia metasternal epimeron

Metatibia Mandible

ss

Labrum

Metatarsus

Clypeus Clypeal suture

Scape

Occiput

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 62 Hind coxa (shaded) fused to and dividing sternite 1.

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 63 Dorsal view of ground beetle adult, showing exposed flight wing.

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 64 Ventral view of a ground beetle showing major sclerites, followed by dorsal view of head. Abbreviations: ps = prosternum; psp = prosternal process; cc = coxal c avity; c = coxa; t = trochanter; epl = epipleuron; pepl = proepipleuron; ss = supraorbital setae; acp = anterior coxal process.

some genera makes separation of specimens diffi cult at the species level. In spite of the abundant number of species, the tribal classification is fairly well established. Because there are no rules for assignment of categories above the species level, grouping of taxa above tribes is very much unset tled, and vary according to author and region. What follows here is a current arrangement of the higher taxa of ground beetles with representative illustra tions of adults of several tribes.


Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 65 Representative figures of ground beetle tribes: tiger beetles, (left) Cicindelini, Cicindela; (right) Megacephalini (Megacephala).

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 66 Representative figures of ground beetle tribes: (left) Bembidiini, Bembidion; (middle) Carabini, Calosoma; (right) Elaphrini, Elaphrus.

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 67 Representative figures of ground beetle tribes: (left) Brachinini, Brachinus; (middle) Lebiini, Plochionus; (right) Pogonini, Diplochaetus.

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Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 68 Representative figures of ground beetle tribes: (left) Dyschirini, Dyschirius; (middle) Scaritini, Pasimachus; (right) Cychrini, Scaphinotus.

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 69 Representative figures of ground beetle tribes: (left) Lachnophorini, Calybe; (right) Lachnophorini, Euphorticus.

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 70 Representative figures of ground beetle tribes: (left) Helluonini, H elluomorphoides; (middle) Ctenodactylini, Leptotrachelus; (right) Nebriini, Nebria.

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Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 71 Representative figures of ground beetle tribes: (left) Notiophilini, N otiophilus; (middle) Omophronini, Omophron; (right) Rhysodini, Omoglymmius.

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 72 Representative figures of ground beetle tribes: (left) Cyclosomini, T etragonoderus; (middle) Psydrini, Nomius; (right) Chlaeniini, Chlaenius.

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 73 Representative figures of ground beetle tribes: (left) Platynini, Olisthopus; (middle) Panagaeini, Panagaeus; (right) Pentagonicini, Pentagonica.

Ground Beetle (Coleoptera: Carabidae) Taxonomy, Figure 74 Representative figures of ground beetle tribes: (left) Harpalini, S tenomorphus; (right) Zuphiini, Zuphium.

Identification of ground beetles includes analysis of external morphological characters, and frequently comparison of genitalic structures. The latter requires dissection of specimens and is used less commonly than external morphological char acters. Species definitions for ground beetles are varied, dependent upon the group and diagnostic characters defined by that group’ s expert. Literature dealing with the identification of ground beetle species is voluminous. Maddison (1995) listed the world higher classification of ground beetles. His classification differed some what from Ball and Bousquet (2001), who pre sented a comprehensive outline of higher classification of the Nearctic ground beetles based on the classification scheme of Lawrence and Newton (1995). In their classification scheme the wrinkled bark beetles are treated as the fam ily Rhysodidae. Madison (1995) cited disagree ment over placement of several Adephaga families, namely the tiger beetles (family Cicin delidae or supertribe Cicindelitae) and the wrin kled bark beetles (family Rhysodidae or tribe Rhysodini). I follow the classification scheme of Lawrence and Newton (1995) here. Tribes are listed in phylogenetic order (according to degree


of relatedness) beginning with what are considered the most primitive groups. The following abbreviations are used in the listing of ground beetle taxa (f = family; s.f. = subfamily; t = tribe; ** = with representatives in North America). Approximate distributions are listed for those taxa that are sufficiently well known and defined. Family: Carabidae Subfamily: Paussinae Tribe: Metriini ** – 2 species restricted to western North America Tribe: Ozaenini ** – Pantropical, occurring in Ori ental, Afrotropical, Australian, and Neotropi cal regions Tribe: Paussini – myrmecophilous, restricted to tropics in southern Hemisphere Subfamily: Gehringiinae Tribe: Gehringiini** – a single Pacific Northwest species in North America Subfamily: Nebriinae Tribe: Notiophilini** – Palearctic, Oriental, Nearc tic, Neotropical regions Tribe: Notiokasini – Neotropical Tribe: Pelophilini** – Arctic and subarctic regions Tribe: Opisthini** – Nearctic and China, India, Bhutan, Nepal, and Taiwan Tribe: Nebriini** – Holarctic and north Oriental Subfamily: Carabinae – Tribe: Carabini** – worldwide distribution Tribe: Ceroglossini – Chile Tribe: Pamborini – Australia Tribe: Cychrini** – Holarctic, and China, Tibet, and Sikkim, Himalaya Subfamily: Cicindelinae (tiger beetles) Tribe: Omini** – western US Tribe: Collyridini – Pantropical Tribe: Megacephalini** – Nearctic, Palearctic Tribe: Ctenostomatini – Neotropical Tribe: Manticorini – South Africa Tribe: Cicindelini** – worldwide Subfamily: Loricerinae – Tribe: Loricerini** – Holarctic – Oriental regions Subfamily: Omophroninae – found in all major zoo geographical regions except Australia Tribe: Omophronini**

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Subfamily: Elaphrini – Holarctic Tribe: Cicindini – Kuwait Tribe: Elaphrini** – Holarctic Tribe: Migadopini – Chile Tribe: Amarotypini – distribution uncertain Subfamily: Promecognathinae – Tribe: Promecognathini** – Nearctic and South Africa Subfamily: Scaritini – all major zoogeographical regions Tribe: Siagonini – Palearctic Tribe: Hiletini – Peru, tropical Africa, Southeast Asia, Indonesia Tribe: Clivinini** – all major zoogeographical regions Tribe: Scaritini** – all major zoogeographical regions Subfamily: Rhysodinae – worldwide Tribe: Rhysodini** – wrinkled bark beetles, some times placed in family Rhysodidae Subfamily: Trechinae – worldwide, mostly in temper ate regions Tribe: Psydrini** – Holarctic and Australia Tribe: Melaenini – South India Tribe: Cymbionotini – South India Tribe: Broscini** – temperature portions of all major zoogeographical regions Tribe: Apotomini – South India Tribe: Trechini** – worldwide distribution Tribe: Zolini – Chile Tribe: Pogonini** – all zoogeographical regions Tribe: Bembidiini** – all zoogeographical regions Tribe: Patrobini** – Oriental, Palearctic, and Nearctic regions Tribe: Amblytelini – Australia Subfamily: Harpalinae Tribe: Pterostichini** – all major regions Tribe: Morionini** – Nearctic and pantropical regions Tribe: Cnemalobini – Argentina Tribe: Catapieseini – Neotropics Tribe: Platynini** – all major zoogeographical regions Tribe: Zabrini** – Holarctic, Oriental, Ethiopian, and Neotropical regions Tribe: Bascanini – sub-Saharan Africa

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Ground Beetles

Tribe: Peleciini – Neotropics, Oriental, Africotro pical regions Tribe: Cuneipectini – western Australia Tribe: Chaetogenyini – distribution uncertain Tribe: Licinini** – all major zoogeographical regions Tribe: Oodini** – all major zoogeographical regions Tribe: Panagaeini** – Nearctic, Neotropics Tribe: Chlaeniini** – worldwide Tribe: Harpalini** – all major zoogeographical regions Tribe: Dryptini** – all major zoogeographical regions Tribe: Zuphiini** – all major zoogeographical regions Tribe: Galeritini** – Pantropical, Holarctic Tribe: Physocrotaphini – distribution uncertain Tribe: Anthiini – eastern Hemisphere tropics Tribe: Helluonini** – most zoogeographic region Tribe: Idiomorphini – India Tribe: Orthogoniini – eastern Hemisphere Tribe: Hexagoniini – Afrotropical, Oriental regions Tribe: Ctenodactylini** – Neotropical Tribe: Amorphomerini – distribution uncertain Tribe: Lachnophorini** – Western hemisphere Tribe: Pentagonicini** – all major zoogeographical regions Tribe: Odacanthini** – all major zoogeographical regions Tribe: Calophaenini – distribution uncertain Tribe: Perigonini** – Pantropical Tribe: Graphipterini – Afrotropical Tribe: Cyclosomini** – primarily tropical, Orien tal, Afrotropical, Neotropical Tribe: Masoreini – Afrotropical Tribe: Lebiini** – all major zoogeographical regions Subfamily: Pseudomorphinae Tribe: Pseudomorphini** – Nearctic, Neotropical, and Australian regions Subfamily: Brachininae (bombardier beetles) – all major zoogeographical regions Tribe: Crepidogastrini – eastern Hemisphere Tribe: Brachinini** – all major zoogeographical regions, largely tropical

References Ball GE, Bousquet Y (2001) 6. Carabidae Latreille, 1810. In: Arnett RH Jr, Thomas MC (eds) American beetles, vol 1. Archostemata, Myxophaga, Adephaga, Polyphaga: Staphyliniformia. CRC Press, Boca Raton, FL, pp 32–132 Ball GE, Casale A, Vigna Taglianti A (eds) (1998) Phylogeny and classification of Caraboidea (Coleoptera: Adephaga). Torino, Italy. Atti Museo Regionale di Scienze Naturali, 543 pp Erwin TL, Ball GE, Whitehead DR, Halpern AL (eds) (1979) Carabid beetles: their evolution, natural history, and classification. Dr. W. Junk, The Hague, The Netherlands, 644 pp Lawrence JF, Newton AF Jr (1995) Families and subfamilies of Coleoptera (with selected genera, notes, references and data on family-group names). In: Pakaluk J, Slipinski SA (eds) Biology, phylogeny, and classification of Coleoptera: Papers celebrating the 80th birthday of Roy A. Crowson. Museum I Instytut Zoologii PAN, Warsaw, Poland, pp 779–1006 Maddison DR (1995) Carabidae. Ground beetles and tiger bee tles. Available at http://www.tolweb.org/Carabidae/8895

Ground Beetles Members of the family Carabidae (order Coleoptera).  Ground Beetle Taxonomy  Ground Beetle Feeding Ecology  Beetles

Ground Crickets A subfamily of crickets (Nemobiinae) in the order Orthoptera: Gryllidae.  Grasshoppers, Katydids and Crickets

Ground Pearls Some members of the family Margarodidae, super family Coccoidae (order Hemiptera).  Bugs  Turfgrass Insects and their Management

Guenée, Achille

Group Predation Hunting and retrieving of prey by groups of coop erating individuals. Among insects, this is well developed in ants.

Group Selection An evolutionary process functioning through the effects of different numbers of descendents left by groups rather than by individuals.

Grouse Locusts A family of grasshoppers Tetrigidae) in the order Orthoptera.  Grasshoppers, Katydids and Crickets

Grub A thick-bodied larva with well-developed head and thoracic legs, but without abdominal prolegs. At rest, the body is curved, and often is described as C-shaped. A scarabaeiform larva (Scarabaei dae). This term also is sometimes applied to larval wasps (Hymenoptera).  Beetles  Scarab Beetles  Hymenoptera

Gryllacrididae A family of crickets (order Orthoptera). They commonly are known as leaf-rolling crickets.  Grasshoppers, Katydids and Crickets

Gryllacridoids Certain members (suborder Ensifera, superfamily Gryllacridoidae) of the order Orthoptera.  Grasshoppers, Katydids and Crickets

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Gryllidae A family of crickets (order Orthoptera). They commonly are known as crickets.  Grasshoppers, Katydids and Crickets

Grylloblattodea An order of insects. They commonly are known as rock crawlers.  Rock Crawlers

Gryllotalpidae A family of crickets (order Orthoptera). They commonly are known as mole crickets.  Grasshoppers, Katydids and Crickets

Gryropidae A family of chewing lice (order Phthiraptera). They sometimes are called guinea pig lice.  Chewing and Sucking Lice

Guenée, Achille Achille Guenée was born in Chartres, France, on January 1, 1809. He began to study Lepidoptera as a boy. His first university education was at Chartres, and then he studied law in Paris. Of a wealthy family, he married and had a son and two daughters, of whom the son died young. He lived at his country residence at Châteaudun for the remainder of his life and contributed 63 papers on Lepidoptera. A major contribution was his six volumes in the series “Suites à Buffon” [a supplement to Buffon’s series on “Histoire naturelle”], “Spécies général des lepidoptères” (1852–1857). Another was “Essai sur une nouvelle classification des microlepidoptères” (1845), a major classificatory work. He died at Châteaudun on December 30, 1880.

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Guérin-Méneville, Félix Edouard

Reference Essig EO (1931) Guenée, Achille. In: A history of entomology. The Macmillan Company, New York, NY, pp 640–642

Guérin-Méneville, Félix Edouard Félix Guérin-Méneville was born in Toulon, France, on October 12, 1799, named Félix Edouard Guérin. He produced taxonomic works on most orders of insects, but later wrote on applied entomology, including sericulture and pests of grapevines. In 1836 he changed his surname to Guérin-Méneville. In 1831 he founded and edited “Magasin de Zoologie,” and when it was merged with “Revue Zoologique” in 1849 as “Revue et Magasin de Zoologie,” he contin ued as editor until 1873. His own output of publi cations was over 400, of which his encyclopedic “Iconographie de règne animal de G. Cuvier” in seven volumes brought him the most recognition. France’s “Legion d’Honneur” was the most prestigious of his many awards. He died in Paris on January 26, 1874.

Reference Herman LH (2001) Guérin-[Méneville], Félix Edouard. Bul letin of the American Museum of Natural History 265:72–73.

Guest Among social insects, this term is used to indicate a social symbiont.

Guild A group of species that exploits the same resource in a similar manner. Examples of a guild are the various insects that are responsible for decompo sition of cow dung, or the various insects that attack the flower head of sunflower.

Guinea Pig Lice Members of the family Gryropidae (order Phthiraptera).  Chewing and Sucking Lice

Gula A sclerite found centrally beneath the head, in the position of the “throat.” It also is called the gular plate.

Gundlach, Johannes (Juan) Christopher Johannes Gundlach was born in Marburg, Germany, on July 17, 1810. His father, a university professor there, died young, leaving his widow and their five children with inadequate income. Johannes became interested in natural history, and began to collect birds by shooting them in prepa ration for taxidermy. An early accident with a gun left him with an injured palate and nose, and loss of his senses of smell and taste. His mother wanted him to study religion, and he began to do so, but he obtained a job as conservator of the university museum and put aside his religious training to study zoology. He obtained free tuition as son of a faculty member, a master of arts degree in 1837, and a doctorate in philosophy in 1838. He was offered accommodation in Surinam by a friend who was a military doctor there, and began to seek funding for his trip, the funds to be repaid by the sale of specimens collected. While organizing this funding, he spent six months studying specimens in the zoological museum at Frankfurt am Main, southern Germany. His sea voyage to Surinam took him first to Cuba, where he spent from Christmas 1838 through early January 1839 col lecting before learning that his friend in Surinam had died. Johannes decided to remain in Cuba and to repay his loan with specimens collected in Cuba. He received much hospitality in Cuba from

Gyllenhal, Leonhard

landowners, even to the extent in 1846 of estab lishing a museum of his collections at a farm called “El Refugio” near to Cárdenas. This museum received thousands of visitors. In 1864 the collec tion was moved to a building on the farm of the Cárdenas family. He collected in all parts of Cuba with enthusiasts and sponsors or alone. The Cuban insurrection against Spanish rule began in 1868 and made fieldwork dangerous because of roving bands of rebels and Spanish soldiers, so Johannes collected intensively on the Cárdenas farm and made three visits to Puerto Rico, in 1873, 1875–1876, and 1881. His hosts, the Cárdenas family, had meanwhile encountered great financial difficulty. In 1892, after approval from Spain, Johannes sold his collections to the Instituto de Segunda Ense ñanza de la Habana (“Institute of Havana”), and gave all the proceeds to the Cárdenas family. How ever, the transaction also allowed a small salary as curator to Johannes. The collections were installed in Havana in 1895, and Johannes (known in Cuba as Juan) died on March 17, 1896. He published on numerous aspects of Cuban and Puerto Rican zoology. His major works on insects were (1881, 1886, 1891) “Contribución a la entomología cubana” in three volumes, and (1887, 1891, 1893) “Apuntes para la fauna puerto-riqueña” (a series published in Anales de la Sociedad Española de Historia Natural, of which the parts in volumes 16, 20 and 22 of that journal concern insects). He never married, lived very frugally, and dedicated his life to Cuban zoology.

Reference Ramsden CT (1915) Juan Gundlach [with bibliography]. Entomol News 26:241–260

Gustatory This is used to describe features related to the sense of taste such as gustatory sensilla or gusta tory behavior.

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Gut pH The pH of the insect gut is variable, and has significant influence on the actions of enzymes secreted in the midgut, and solubility of the food. Different enzymes function optimally at different pH levels. Though the gut tends to be slightly acidic in most species (about pH 4–6), the gut pH is related to host plant chemistry. Insects that feed on trees, which typically pos sess high levels of t annins, have higher pH lev els, around 8.6, apparently because this reduces the effects of ingested tannins. The hindgut regions of insects ingesting cellulose, such as termites and crickets, tend to be acidic due to anaerobic fermentation of glucose derived from cellulose digestion.  Alimentary Canal and Digestion

Gyllenhal, Leonhard Leonhard Gyllenhal was born in Algusthorp, Sweden, on December 3, 1752. At the age of 17 he entered the University of Uppsala, and studied natural history with Linnaeus, being influenced by the latter to specialize in entomology. However, after three years he entered the Swedish army and served for 27 years. Upon retirement as a major from the army, he met Gustav Paykull and helped the latter with his “Fauna svecica” (1798–1800), and collaborated with Carl Johann Schönherr in production of the latter’ s “Synonymia insectorum” (1806, 1808). Only then did he start his own work, “Insecta Svecica,” of which four volumes were published (1810–1827) on Coleoptera. In the 1830s he also contributed heavily to Schönherr’s “Genera et species curculionidum” He died on May 13, 1840, in Hoeberg, Sweden.

Reference Herman LH (2001) Gyllenhal, Leonhard. Bull Am Mus Nat Hist 265:73–74

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Gynandromorph

Gynandromorph An individual that contains structural characte ristics of both sexes, often with one sex on one side and the other sex on the other side. This is an abnor mal condition in insects, occurring infrequently.

Gyne A female of the reproductive caste in social Hymenoptera. It is applied to potential or actual queens of ants, bees and wasps.

Gynopara (pl. gynoparae) In aphids, viviparous females that are produced on the secondary host in the autumn, and then fly to the primary host to produce new females that mate and deposit eggs.  Aphids

Gypsy Moth, Lymantria dispar Linnaeus (Lepidoptera: Lymantriidae) Wayne Brewer Auburn University, Auburn, AL, USA

Gypsy Moth, Lymantria dispar Linnaeus (Lepidoptera: Lymantriidae), Figure 75 Etienne Leopold Trouvelot, a French naturalist who accidentally introduced gypsy moth into the field at Medford, Massachusetts, in 1869 (courtesy of USDA).

The gypsy moth, Lymantria dispar L., is recognized as one of the most serious insect defoliators of North American forests and urban landscapes. Since its introduction, the gypsy moth has spread to all or part of 17 states and the District of Columbia. Yearly defoliation often reaches into the millions of acres, and the costs of damage and control run into tens of millions of dollars. The moth is a native of Europe and Asia where it is a sporadic pest. It was introduced into the U.S. in 1869 by a French natu ralist, Etienne Leopold Trouvelot (Fig. 75), who brought the moths to his home in Medford, Massachusetts. He apparently intended to cross them with other moths to create a prolific and hardy

strain of silkworms. The experiment failed, the moths escaped and spread to the surrounding area. The first outbreaks of the gypsy moth began in Trouvelot’ s neighborhood about 10 years after their introduction and, in 1890, the State and Federal Government began attempts to eradicate the moth. These efforts ultimately failed and the gypsy moth has continued to spread since that time. Currently established populations occur throughout the northeastern U.S. and the moth is spreading south and west across the U.S. The moth often “hitchhikes” to new areas on the camper trailers and motor homes of northern residents vacationing in unin fested areas. The result is that every year isolated

Gypsy Moth, Lymantria dispar Linnaeus (Lepidoptera: Lymantriidae)

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populations are discovered beyond the contiguous range of the gypsy moth, but these are usually erad icated or disappear without intervention. However, it is inevitable that the gypsy moth will continue to expand its range in the future.

Biology The gypsy moth (Fig. 76) has one generation per year. The adults emerge in midsummer, usually in July but variations occur depending on local or regional conditions. Although winged, the females cannot fly and usually remain near the pupal case from which they emerged. Soon after emerging, the females release a sex pheromone that attracts the males, which do fly; they mate and she begins to lay eggs. The females normally produce one egg mass in which the number of eggs may range from fewer than 100 to over 1,000. The eggs are covered by a dense coating of hairs that are sloughed from the abdomen of the female as she oviposits. It is thought that these hairs provide a form of insulation that helps protect them from low temperatures. Gypsy moths overwinter in the egg stage which lasts 8–9 months. The following spring, the eggs hatch and the larvae emerge. The date of larval emergence is strongly influenced by temperature. Larval feeding continues through four instars with the last instar doing most of the damage to foliage. It has been esti mated that a single larva consumes about one square meter of foliage during its development. Pupation occurs about eight weeks after egg hatch. The pupae are usually located in cryptic locations such as cracks or crevices of the bark, in the leaf litter, or in other protected places. This stage lasts about two weeks and then adults emerge to continue the cycle.

Dispersal The newly hatched, small and hairy larvae move to the tops of trees and feed on new foliage. Some may be blown by the wind to new locations. The long larval hairs of the early instars and the strands

Gypsy Moth, Lymantria dispar Linnaeus (Lepidoptera: Lymantriidae), Figure 76 Some stages of the gypsy moth life cycle: top, a mature larva; center, female moths (adults) with egg masses protruding from beneath; bottom, a male moth (adult photos courtesy of John Ghent, U.S. Forest Service).

of silk they produce from special glands in their heads are conducive to this type of transport. This “ballooning” is a major means of natural dispersal. However, most long distance spread to new loca tions occurs as result of the transport of infested items by humans. The larvae may pupate, or females may lay egg masses, on almost any object left outside. These include campers, mobile homes, packing crates, pallets and other items. If infested

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Gypsy Moth, Lymantria dispar Linnaeus (Lepidoptera: Lymantriidae)

items are moved to a new location, a new infesta tion may become established.

Nuisance Factors

The gypsy moth is known to feed on the f oliage of over 300 species of trees and shrubs with species of oaks ranked among the most preferred hosts. Oaks are common in much of the forested and urban areas of the U.S. and their wide distribution will be a major factor in the ultimate distribution of the moth. Where oaks are less common, how ever, the gypsy moth has maintained populations on other tree species including aspen and other hardwoods. A few species, including tulip poplar and dogwood, appear to be immune to feeding and other species, especially conifers, are not acceptable to very young gypsy moth larvae, but older instars feed readily on them.

At low population levels, gypsy moth larvae remain inactive and secluded in resting places during the day, but when populations are high, their behavior changes dramatically. Larvae in dense populations become hyperactive during the day. Infested areas are literally crawling with larvae as they move inces santly up and down trees and travel along the ground. These larvae are attracted to and climb any object in their path including trees, telephone poles, cars and people. They are not harmful, but the presence and activity of such large numbers of these larvae create a nuisance. In addition, when outbreaks occur, many larvae die from various mortality factors. The unpleasant odor of decaying larvae is often evident throughout the defoliated area. Outdoor activities, such as picnics and barbeques, are often disrupted by larvae, or their frass (excrement) dropping from infested trees onto patios, decks and picnic tables.

Damage

Natural Enemies

When the gypsy moth first moves into a new area, tree mortality is often extensive. Species of oaks, especially white and chestnut oaks, appear to be most susceptible with mortality often exceeding 50 %. The effects of repeated defoliation can be very serious. Coniferous trees often die after a single defoliation. Deciduous trees can withstand one or two defoliations but the mortality level rises sharply after the third. Other stresses, such as drought or poor site conditions, may increase the risk of mor tality. Much tree mortality is actually caused by pathogens or insects, such as wood borers that attack and kill weakened trees. In areas where the gypsy moth has existed for some time, such as New England, the moth is more notorious as a nuisance rather than for killing large numbers of trees. This may be a result of gypsy moth populations eventu ally coming under control by natural enemies, or the change in forest composition due to favored hosts being killed and the remaining trees being less suitable as sources of nutrition.

Various biological control agents have been collected from Asia and Europe and introduced into infested areas of the U.S. over the last 100 years. These include over 20 insect parasitoids and predators that are nat ural enemies of the gypsy moth. Small mammals, like the white-footed mouse, and other rodents such as shrews, are perhaps the most important gypsy moth predators, especially at low population densi ties. Birds are also known to prey on gypsy moths, but do not seem to cause any substantial reduction in moth populations. A nucleopolyhedrosis virus usually causes the collapse of outbreak populations, and recently an entomopathogenic fungus species has caused considerable mortality of gypsy moth populations in North America.

Hosts

Control In addition to the introduction of natural enemies, several million acres of forest land have been aerially

Gyropidae

sprayed with pesticides over the last 20 years to sup press gypsy moth populations. Though some areas are treated by private companies under contract with land owners, most areas are sprayed under joint programs of state governments and the USDA For est Service. The USDA, state and local governments also jointly participate in programs to identify and eradicate new gypsy moth populations in currently uninfested areas. These survey programs involve the use of small triangular-shaped traps baited with a synthesized female sex pheromone. In addition, the USDA Forest Service, working with state and federal cooperators, began a Gypsy Moth Slow the Spread (STS) project in 1999. The project covers the 1,200 mile gypsy moth frontier from North Carolina through the Upper Peninsula of Michigan. The proj ect goal is to use novel integrated pest management strategies to reduce the rate of moth spread.

References Campbell RW (1975) The gypsy moth and its natural enemies. U.S. Department of Agriculture, Washington, DC, Agriculture Information Bulletin 381

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Doane CC, McManus ML (1981) The gypsy moth: research toward integrated pest management. U.S. Department of Agriculture, Washington, DC, Forest Service Bulletin 1584 McManus ML, Zerillo RT (1979) The gypsy moth: an illus trated biography. U.S. Department of Agriculture, Wash ington, DC, Home and Garden Bulletin 225 Smith HR, Lautenschlager RA (1978) Predators of the gypsy moth. U.S. Department of Agriculture, Washington, DC, Agriculture Handbook 434 Talerico RL (1978) Major hardwood defoliators of the eastern United States. U.S. Department of Agricul ture, Washington, DC, Home and Garden Bulletins 223 and 224

Gyrinidae A family of beetles (order Coleoptera). They com monly are known as whirligig beetles.  Beetles

Gyropidae A family of chewing lice (order Mallophaga). They sometimes are called guinea pig lice.  Chewing Lice

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Habitat The place where an organism dwells. This is a less inclusive term than “niche.”

Habitat Diversity The range of habitats present in an area. Because insects often have preferred habitats, there usually is a strong correlation between habitat and insect diversity.

Habituation Failure to elicit normal response after repeated stimuli. Often the organism gradually decreases it response to the stimulus, and the organism may not respond even after the stimulus is discontinued for a protracted period. All insects are thought to be capable of habituation to some stimuli, and it is considered to be the simplest form of learning.  Associative Learning  Latent Learning  Insight Learning  Learning in Insects

Haddow, Alexander John Alex Haddow was born in Scotland in December 1912, and as a boy showed intense interest in insects. His first degree was in zoology, from Glasgow

niversity in 1934. He took another 4 years to comU plete an M.D. degree. Next, he studied at the London School of Tropical Medicine for a diploma in tropical medicine. In 1941 he traveled to Kenya and studied biting cycles of mosquitoes under conditions of a 24-h continuous catch, developing and standardizing methods for collecting and analyzing the data. Other work in Africa was on the epidemiology of yellow fever, and it involved collecting and sampling from monkeys. After 24 years in Africa, he returned to Britain in 1965, to become Administrative Dean of the Faculty of Medicine at Glasgow University. His honors include election to the fellowship of The Royal Society as well as the Royal Society of Edinburgh. He died in Glasgow on December 26, 1978, survived by his wife, Peggy, and two sons.

Reference Gillett JD (1979) Alexander John Haddow 1912–1978. Antenna 3:54

Haematomyzidae A family of chewing lice (order Phthiraptera).  Chewing and Sucking Lice

Haematopinidae A family of sucking lice (order Phthiraptera). They sometimes are called ungulate lice.  Chewing and Sucking Lice

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Hagen, Hermann August

Hagen, Hermann August Hermann Hagen (Fig. 1) was born in Königsberg (now Kaliningrad), then in German East Prussia (now in Russia), on May 30, 1817. He was educated at Universität Königsberg, and became a physician in that city. He studied extant insects (Odonata, Neuroptera, Isoptera, Psocoptera, Plecoptera, and Trichoptera) and fossil insects. Some of his major works were “Monographie der Termiten” (1855–1860) and “Bibliotheca Entomologica” (1862–1863) [for a subsequent bibliography of the world’s entomological literature, see: Horn, Walther]. In 1867 he was invited to the USA to take charge of the entomological section of the Museum of Comparative Zoology at Harvard University in Massachusetts. He accepted, organized and built that collection, and greatly influenced taxonomic entomologists in the USA. In 1890–1891 he was afflicted with paralysis and influenza, and died in Massachusetts in 1893.

References Essig EO (1931) Hagen, Hermann August. In: A history of entomology. Macmillan, New York, NY, pp 643–646 Mallis A (1971) Hermann August Hagen. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 119–126

Hagen, Kenneth Sverre Ken Hagen was born in the state of California, USA, on November 26, 1919. He displayed an early interest in insects and formed a collection. He earned a B.S. degree from the University of California at Berkeley in 1943. After service in the U.S. navy in World War II (landings at Normandy and Okinawa), he returned to the graduate school of the same institution, earning degrees of M.S. in 1948 and Ph.D. in 1952. While he was a graduate student he worked as a technician, but after his Ph.D. he was hired as junior

Hagen, Hermann August, Figure 1 Hermann Hagen.

entomologist in the Division of Biological Control, of the University of California’s Agricultural Experiment Station at Albany. He became entomologist in 1965 and professor of entomology in 1969. His areas of research interest included the behavior of coccinellids, highlighted in a (1970) article in National Geographic called “The highflying ladybug.” He was the leader of projects that resulted in introduction of 25 species of biocontrol agents against 17 economically important pests. He had a pioneering role in the nutrition of biocontrol agents, with proof in the field that manipulative techniques using artificial nutrition could work. He authored more than 160 scientific publications and received numerous awards. He was also a gifted teacher. He died on January 10, 1997, survived by his wife, Maxine, and one son.

References Caltagirone LE, Dahlsten DL, Garcia R (1997) Kenneth Sverre Hagen, Entomological sciences: Berkeley. Available at http://sunsite.berkeley.edu:2020/dynaweb/teiproj/uchist/ inmemoriam/inmemoriam1997. Accessed Aug 2002

Hale Carpenter, Geoffrey Douglas

Hahn, Carl Wilhelm Carl Hahn was born on December 16, 1786, and lived mainly in Nürnberg (Nuremberg), Germany. He studied the spiders of his country, which he described and illustrated in two major works, “Monographie der Spinnen” and “Die Arachniden”. His premature death in 1836 interrupted publication of the latter, of which he completed only two volumes. It was then completed, in a further 14 volumes, by C. L. Koch between 1836 and 1849.

Reference

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Hairy Chinch Bug, Blissus leucopterus hirtus Montandon (Hempitera: Lygaeidae) Hairy chinch bug is an increasingly important pest of turfgrass.  Turfgrass Insects and their Management

Hairy Fungus Beetles Members of the family Mycetophagidae (order Coleoptera).  Beetles

Bonnet P (1945) Bibliographia Araneorum 1:32

Hair Pencil Clusters of long setae on the body of certain insect (particularly male Lepidoptera and some Neuroptera). They occur on various parts of the body, but usually on the abdomen. They are associated with exocrine glands, and usually used during courtship to disperse sex pheromones. This term is synonymous with “brush organ.”

Hair Plate A sensor structure found at the leg joints and at other limb articulations. They respond to touch, bending and joint flexing by emitting nervous stimuli, and adapt slowly. They allow the insect to know the orientation of the head and appendages. A more complex version of the hair plate is the chordotonal sensillum.

Hairstreaks Some members of the family Lycaenidae (order Lepidoptera).  Gossamer Winged Butterflies  Butterflies and Moths

Hale Carpenter, Geoffrey Douglas Geoffrey Hale Carpenter was born in Eton College, England, on October 26, 1882. His undergraduate studies were at Oxford University, and then in 1908 he qualified in medicine and took a D.M. degree in 1913. But by 1911, interested in tropical medicine and natural history, he was studying the bionomics of Glossina palpalis and its relation to sleeping sickness in Uganda. His research was published in reports of The Royal Society in 1912, 1913, and 1919. In Uganda, too, he studied mimicry in butterflies, and through rearing experiments solved problems of relationships. He viewed mimicry among butterflies as a result of natural selection by predatory birds, mammals, and reptiles. His butterfly studies are published mainly in journals of the Royal Entomological Society. In 1933 he was appointed Hope Professor at Oxford University, succeeding Sir Edward Poulton. He retired in 1948 and died in Oxford on January 30, 1953.

Reference Riley ND, Hale Carpenter GD (1953) Entomologist 86:155–156

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Half Life

Half Life The period of time required for a pesticide to lose half of its original effectiveness or toxicity.

Halictidae A family of bees (order Hymenoptera, superfamily Apoidae).  Wasps, Ants, Bees and Sawflies

Halictophagidae A family of insects in the order Strepsiptera.  Stylopids

Haliday, Alexander Henry Alexander Haliday (Fig. 2) was born in Belfast in 1807. At the age of 15, he entered Trinity College, Dublin, remaining there 5 years and obtaining an M.A. degree. Next, he studied law, and apparently was successful, although it is not clear that he ever practiced this profession. Returning to the north of Ireland, he devoted his time to the study of literature and natural history. He was appointed High Sheriff of the county of Antrim in 1843, a political

position rather than one in law-enforcement. Beginning in 1828, he published a long series of papers on the Irish insect fauna, especially Diptera. He also published extensively on Chalcidoidea and other “parasitic” Hymenoptera, and on Thysanoptera. Due to poor health, he emigrated to Lucca, Italy, about 1860. There, he continued collecting insects and helped to found the Società Entomologica Italiana. He died on July 12, 1870.

Reference Anonymous (1870) Alexander Henry Haliday. Entomologist’s Monthly Magazine 7:91

Halimococcidae A family of insects in the superfamily Coccoidae (order Hemiptera).  Bugs

Haliplidae A family of beetles (order Coleoptera). They commonly are known as crawling water beetles. Beetles

Haltere (pl., halteres) The vestigial, modified hind wings of Diptera that function as balancing organs.

Hamophthiriidae A family of sucking lice (order Phthiraptera).  Chewing and Sucking Lice

Hamulus

Haliday, Alexander Henry, Figure 2 Alexander Haliday.

(pl., hamuli) Hook-shaped hairs on the leading edge of the hind wing in Hymenoptera that unite the fore- and hind wings.  Wings of Insects

Haploid

Handling Time

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Hangingflies

The time a predator spends pursuing, subduing, and consuming prey (a meal).

Handlirsch, Anton

Members of the family Bittacidae (order Mecoptera).  Scorpionflies

Hansen, Viktor

Anton Handlirsch was born in Vienna on January 20, 1865. He studied pharmacy, and in 1883 received a master’s degree in that subject. Then, he became scientific helper, assistant (1892), adjunct custodian (1899), second-class custodian (1906), first-class custodian (1918) and director (1922) of the Naturhistorisches Hofmuseum of Vienna. His earliest entomological work was on Hymenoptera, reaching a climax (1887– 1894) with a monograph of wasps related to Bembex and Nysson. He took charge of Hemiptera at the museum, purchased the Signoret collection for it, and wrote a monograph on Phymatidae (1897). Next, he turned his attention to fossil insects. His (1906–1908) book “Die fossilen Insekten und die Phylogenie der rezenten Formen” enumerated or described all known fossil insects. It included a new classification with discussion. In his contributions to Schroeder’s (1925) “Handbuch der Entomologie” and Kükenthal’s (1926–1935) “Handbuch der Zoologie,” he modified the classification. He also published about 100 other titles. He died in Vienna on August 28, 1935.

Viktor Hansen was born in Copenhagen on August 29, 1889. In 1907 he entered the Metropolitanskolen and in 1913 obtained his law degree. He worked in the Justitsministeriet from 1915, became a superior judge in 1941, and worked in that capacity until he retired in 1959. However, he began to collect beetles as a teenager, and in 1905 joined the Entomologisk Forening [entomological society]. His first paper was published in 1907 in Entomologiske Mededelser. His lifetime total was more than 100 papers on the Danish beetle fauna. His major production was 23 volumes on beetles in the series Danmarks Fauna. For this, he was awarded an honorary doctoral degree from Københavns Universitet in 1950, and medals from entomological societies in Denmark and Sweden, and from a natural history society in Denmark. He died on March 6, 1974.

Reference Herman LH (2001) Hansen, Viktor. Bull Am Mus Nat Hist 265:75

Haplodiploidy Reference Calvert PP (1936) 47:168–169

Obituary.

Entomological

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Handsome Fungus Beetles Members of the family Endomychidae (order Coleoptera).  Beetles

A type of parthenogenetic reproduction in which males are produced from unfertilized eggs and are haploid, while the females are diploid. In Hymenoptera, females can control the release of sperm, and regulate the sex ratio of offspring.

Haploid Cells or organisms that contain a single copy of each chromosome.

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Hardy-Weinberg Equilibrium

Hardy-Weinberg Equilibrium An equilibrium of genotypes achieved in populations of infinite size in which there is no migration, selection, or mutation after at least one generation of panmictic mating. With two alleles, A and a, of frequency p and q, the Hardy-Weinberg equilibrium frequencies of the genotypes AA, Aa and aa are p2, 2pq and q2, respectively.

Harlequin Bug  Crucifer Pests and their management

Harlequin Bug, Murgantia histrionica (Hahn) (Hemiptera: Pentatomidae) john l. capinera University of Florida, Gainesville, FL, USA Indigenous to Mexico and Central America, harlequin bug has dispersed north into the United States. Its appearance in Texas, USA, in 1864 coincided with the occurrence of Union troops during the American Civil War, and in parts of the South earned it the name “Sherman-bug” after the northern General Sherman, and “Lincolnite” after President Abraham Lincoln. It rapidly spread throughout the southern states, and eventually reached northern locales such as Colorado, Iowa, southern Michigan, Pennsylvania, and Massachusetts. It is considered to be a serious pest only in southern states, however, and is not regarded as a problem in California. It has also dispersed to the Hawaiian Islands.

Life History Harlequin bug breeds continuously in the southern portions of its range. During mild winters all stages have been observed as far north as Virginia.

In colder climates only the adults survive the winter in sheltered locations. They seek shelter in and near fields, among overwintering crop plants, and in other organic debris such as dead leaves and bunches of grass. Two or three generations per year seem to be normal, but there appears to be four generations in south Texas. Adults begin depositing eggs about 2 weeks after becoming active in the spring. Eggs are deposited beneath leaves, usually in clusters of 12 arranged in two rows of six, at intervals of 5–6 days. As the female nears the end of her life, the egg batches get slightly smaller and the egg arrangement less regular. The eggs are barrel-shaped, and measure about 1.30–1.38 mm long and 0.90–0.92 mm in diameter. They are light gray or pale yellow in color, and generally are circled by two black bands. They may also bear small black dots or spots, and the top has a semicircular black marking. The average number of eggs is reported to be 115 per female. Egg deposition may occur over a period of 40–80 days. Eggs hatch in about 4–5 days during warm weather, while 15–20 days may be required during cool weather. Upon hatching, young nymphs stay clustered near the old eggs for 1 or 2 days. The newly hatched nymphs are pale green with black markings, but soon become brightly colored: black or blue, with red and yellow or orange markings. Reportedly there are six instars in Texas, and nymphal development can be completed in as little as 30 days. There, average development times are 3.4, 3.2, 4.7, 4.7, 7.0, and 4.3 days, respectively, for the six instars developing under summer conditions. Under spring conditions, development times were increased by about 30%. Studies in Virginia suggest only five instars, however, and a development time requirement of 40–60 days during the summer, and slightly longer, perhaps 70 days, during cool weather. The adults usually live about 60 days, but may live considerably longer during the winter. They measure about 8.0–11.5 mm in length. The adults are brightly colored, similar to the large nymphs, principally black and yellow or black and red. The color pattern varies (Figs. 3 and 4), with the spring and summer bugs being more brightly colored

Harlequin Bug, Murgantia histrionica (Hahn) (Hemiptera: Pentatomidae)

Harlequin Bug, Murgantia histrionica (Hahn) (Hemiptera: Pentatomidae), Figure 3 Adult of harlequin bug, Murgantia histrionica (Hahn).

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horseradish. In the southernmost states, crucifers do not thrive during the summer months, and the bugs are forced onto other plants. Thus, they are sometimes found feeding on asparagus, beans, okra, squash, tomato and many other vegetables, but this is usually due to lack of normal food. Harlequin bug feeds readily on cruciferous weeds such as wild mustard, Brassica spp.; shepherds purse, Capsella bursa-pastoris; and pepperweed, Lepidium spp.; and related mustard oil-containing plants such as members of the family Capparaceae. Other weeds common in crops, such as pigweed, Amaranthus spp., and lambsquarter, Chenopodium album, are also fed upon, and reproduction occurs on these plants. Harlequin bug appears to be relatively free of natural enemies, other than for egg parasites and general predators. The egg parasitoids are Oencyryus johnsoni (Howard) (Hymenoptera: Encyrtidae), Trissolcus murgantiae Ashmead, and T. podisi Ashmead (both Hymenoptera: Scelionidae). The species that is best known is O. johnsoni, which has been reported frequently from harlequin bug eggs, and has caused up to 50% mortality during a harlequin bug outbreak in Virginia. This parasite is widely distributed, and apparently has other hosts. It attacks eggs in all stages of embryonic development, and prevents the eggs from hatching. However, O. johnsoni is not the only effective parasite, as T. murgantiae was observed to parasitize 45% of harlequin bug eggs in North Carolina, at locations where O. johnsoni parasitized only 30% of eggs. Because of its effectiveness, T. murgantiae was introduced into California.

Harlequin Bug, Murgantia histrionica (Hahn) (Hemiptera: Pentatomidae), Figure 4 Third instar of harlequin bug, Murgantia histrionica (Hahn).

Damage

than the overwintering insects. As with many stink bugs, harlequin bugs produce a disagreeable odor if disturbed, and birds avoid eating them. Harlequin bug is principally a pest of crucifers, attacking broccoli, Brussels sprout, cabbage, cauliflower, Chinese cabbage, collard, kale, kohlrabi, mustard, radish, rutabaga, turnip, and watercress. Harlequin bug is reported to be especially fond of

The piercing-sucking feeding behavior of this insect results in white blotches at the site of feeding. Wilting, deformity, and plant death may occur if insects are abundant. Mild winters are said to favor survival, and subsequent damage. Once considered the most serious crucifer pest in the south, this insect has been relegated to minor status in commercial production and persists mostly as a home-garden pest.

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Harris, Thaddeus William

Management Insecticides are applied to the foliage for suppression of harlequin bug. Harlequin bug can be difficult to control with insecticides; targeting the young bugs and thorough coverage are recommended. Soap applied alone or in combination with rotenone has provided good control. Trap crops, usually consisting of early-planted mustard, rape, or kale are sometimes recommended to divert the overwintering bugs from the principal crop. Such trap crops must be sprayed or destroyed, however, or the adults will soon move to the main crop. Destruction of crop residues, on which the insect may overwinter in the north or oversummer in the south, is an important cultural practice to alleviate harlequin bug damage. Susceptibility to damage varies among crucifer crops. Mustard and Chinese cabbage are quite susceptible; turnip, kale, rutabaga, and some radishes are intermediate; and cauliflower, cabbage, broccoli, collard, Brussels sprout, kohlrabi, and most radish varieties are fairly resistant. Cabbages are the most resistant crop, but considerable variation among cultivars is evident.  Crucifer Pests and their Management  Vegetable Pests and their Management, Stink Bugs (Hemiptera: Pentatomidae) Emphasizing Economic Importance

medicine and married. In 1823 he published his first entomological paper. In 1831 he published a catalogue of insects and became librarian at Harvard University. Teaching of courses in natural history and entomology followed. His 1841 “Report on insects injurious to vegetation” became a classic and was reprinted several times. He also published some descriptions of new species of insects that were of economic importance. He died in Massachusetts on January 16, 1856.

References Essig EO (1931) Harris, Thaddeus William. In: A history of entomology. Macmillan, New York, NY, pp 651–653 Mallis A (1971) Thaddeus William Harris. In: American entomologists. Rutgers University Press, New Brunswick, NJ, pp 25–33

Harvester Ants Ant species that store seeds in their nests. This behavior occurs in many ant taxa, including some that are not closely related.  Harvester Ants, Pogonomyrmex

References Capinera JL (2001) Handbook of vegetable pests. Academic Press, San Diego, 729 pp White WH, Brannon LW (1939) The harlequin bug and its control. USDA Farmer’s Bulletin 1712, 10 pp

Harris, Thaddeus William Thaddeus Harris (Fig. 5) was born in Massachusetts on November 12, 1795. He obtained a first degree from Harvard University in 1815 and then a medical degree in 1820, after which he practiced

Harris, Thaddeus William, Figure 5 Thaddeus Harris.

Harvester Ants, Pogonomyrmex Mayr (Hymenoptera: Formicidae)

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Harvester Ants, Pogonomyrmex Mayr (Hymenoptera: Formicidae) thomas o. crist Miami University, Oxford, OH, USA Harvester ants are so named because they collect and store seeds in their nests for later consumption. The seed-harvesting habits of ants are noted in several historical accounts and are the subject of numerous scientific studies. Over 150 species of seed-harvesting ants occur worldwide. In the New World, harvester ants comprise 60 species belonging to two closely related genera, Pogonomyrmex Mayr (“bearded ant”) and Ephebomyrmex Wheeler (“youthful ant”). The beard, or psammophore, refers to the tuft of hairs that extend below the head on the workers of nearly all 45 species of Pogonomyrmex. This distinctive trait corresponds to the ground-nesting habits of harvester ants because the psammophore is used to move particles of soil. Some harvester ants build large mounds or craters of soil and gravel on the soil surface while others have more inconspicuous nests under rocks. Most Pogonomyrmex occur in deserts and grasslands where seeds are abundant, but a few species are found in forest and montane environments. Harvester ants (Fig. 6) range throughout South America, portions of Central America and the Caribbean, and virtually all of western North America and the southeastern Coastal Plain. The geographic ranges of most species, however, are found within southwestern North America and northern South America, the latter of which is likely the evolutionary origin of Pogonomyrmex. The mating behavior and life cycle is generally similar among Pogonomyrmex species. During spring or summer, ant colonies produce numerous winged males and females (“alates”) that are reproductively viable and larger than the sterile workers. Alate flight activity is synchronous among colonies, usually occurring in the late morning on 2 or 3 days following a significant rainfall. Mating flights can occur several times a year, but are usually restricted to a 2 or 3-week period. After leaving the nest, alates

Harvester Ants, Pogonomyrmex Mayr (Hymenoptera: Formicidae), Figure 6 A worker harvester ant. The genus Pogonomyrmex is named after the prominent beard (the psammophore) on the lower side of the head. Drawing is by Ruth Ann DeNicola, published in Cole, A. C., Jr. (1968) Pogonomyrmex harvester ants: a study of the genus in North America. Reproduced with permission from The University of Tennessee Press, Knoxville, Tennessee.

aggregate on hills or cliffs and in the uppermost portions of shrubs, trees, or structures such as fence posts, windmills, or buildings. Males often “lek” (form mating aggregations) together in groups of 5–20 individuals, and females are attracted to male aggregations by a pheromone. Females typically mate with several males, a behavior that results in genetically variable workers after the queen begins reproduction. In some species, such as P. badius (the Florida harvester ant), lekking does not occur and males fly to another nest to mate with females, or mating might take place between males and females of the same colony, which can result in inbreeding and a loss of genetic variability over time. After mating, the fertilized female sheds her wings and begins excavating a nest in the soil. Most “foundress queens” die before successfully establishing a colony. The queen must carry out all of the worker tasks – foraging, nest maintenance, and brood care – for 2 or 3 weeks until her first brood matures into adult workers. The mortality of young colonies continues to be high until the next year when the size of the worker population may increase substantially. Pogonomyrmex colonies have variable

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Harvester Ants, Pogonomyrmex Mayr (Hymenoptera: Formicidae)

numbers of workers: P. laticeps and P. magnacanthus have only 50–250, whereas P. rugosus (the rough harvester ant) and P. barbatus (the red harvester ant) may boast up to 15,000. Most species have a worker force of 500–5,000 ants. Two species, the slavemaking P. anergismus and P. colei, have no workers at all; instead, they live in the nests of P. rugosus or P. barbatus and enslave workers to raise reproductive males and females for them. It appears that all Pogonomyrmex species are monogynous (have one queen) during the life of a colony, which may persist for 10–50 years in some species such as P. occidentalis (the western harvester ant) and P. owyheei [salinus] (the Owyhee harvester ant). Workers perform a variety of tasks. Nest workers take care of the queen and developing larvae and pupae. They also create and maintain a variety of nest chambers for seed storage, brood development and discarded refuse. Storage chambers are connected by networks of tunnels, which may extend 2–3 m vertically below ground in some species. The queen and workers usually overwinter more than a meter below ground in colder climates. Worker tasks vary according to the age of the worker and the needs of the colony. After emerging from pupae, ants work mostly within the nest. Then, as workers get older, they shift to exterior maintenance of the nest, and finally to patrolling, scouting, or foraging, which may entail venturing up to 20 m from the nest in some species. Workers also switch tasks according to the needs of the colony. For example, if a nest is damaged by heavy rain, foraging workers might switch to nest maintenance. Similarly, a nest intruder may elicit an alarm pheromone that rapidly employs a substantial number of workers to defend the nest. Harvester ants are well-equipped for nest defense, as the workers of many species will deliver a painful sting. A number of scientific studies have examined the foraging and seed-harvesting behavior of Pogonomyrmex ants. Foraging workers search for seeds in an individualistic manner, specializing on particular seed species or locations near the nest. Although this is the primary foraging strategy in some species (e.g., P. desertorum, P. maricopa, and P. californicus,

the California harvester ant), several harvester ants also show group foraging tactics. These involve the use of permanent pathways (trunk trails) that orient workers to different foraging areas, and pheromone trails that chemically recruit workers to areas of high-food density (e.g., P. rugosus, P. barbatus, and P. occidentalis). Recruitment pheromones are volatile compounds that dissipate rapidly if workers do not reinforce them by laying additional pheromones along the recruitment trail. Ants usually harvest 85% and is capable of transmitting sunlight. The chemical and physical properties plus the availability of engineered kaolin particles that were heat treated, shaped and sized made this mineral an ideal candidate for study. The term “particle film technology” was coined by the group for the research that led to the development of a multi functional mineral product capable of control ling many insects pests, certain diseases and improved plant health. Particle film technology was originally based on kaolin particles made hydrophobic by a sili cone coating. Hydrophobic kaolin, M-96–018, (BASF, Research Triangle Park, North Carolina, USA; formerly Engelhard Corporation, Iselin, New Jersey, USA) was initially applied as a dust using various hand-operated dusters or modified sand-blasters for large scale studies because the hydrophobic material could not be mixed and delivered in water. However, the drift associated with dusting operations, plus lack of adhesion to the plant, made M-96–018 dust applications impractical. In 1998, the first particle film formu lations were registered with the U.S. Environmental Protection Agency (EPA) under the names M-96–018 and M-97–009 Kaolin. M-96–018 was soon formulated by using a methanol (MEOH)-water system where M-96–018 could be pre-slurried with

Kaolin-Based Particle Films for Arthropod Control

99% MEOH (11.3 kg or 25 lbs M-96–018 + 18.0 L or 4 gal MEOH premixed then added to 436 L or 96 gal water) and delivered as a spray to trees. During field tests, it was determined that this for mulation was too expensive for practical use, and handling and transportation of 99% MEOH pre sented logistical and safety problems. Laboratory and field studies determined that formulations based on hydrophilic kaolin particles (M-97–009) plus a spreader sticker were just as effective as M-96–018 hydrophobic kaolin dusts or aqueous sprays in controlling insects and diseases. As a result, the development of M-96–018 was dropped in favor of M-97–009. Advantages to using hydrophilic M-97–009 kaolin formulations were (i) ease of mixing, (ii) more economical, (iii) compatible with other materials for tank-mixes, and (iv) formulation flexibility to alter spreading and rain fastness. M-97–009 + M03 became commercially available in 1999 under the name Surround® (BASF, Research Triangle Park, North Carolina; formerly Engelhard Corporation, Iselin, New Jersey) and in most cases was applied at 25 lbs kaolin plus 1 pt spreader-sticker in 96 gal water. In 1999, a new formulation of M-97–009 was registered with the U.S. EPA under the name Sur roundTM WP that had the spreader-sticker system incorporated into the particles as a single packaged system that could be added directly to water. This formulation became available in 2000 and is the main formulation currently in use. The historical safety record of kaolin in the paint and plastics industry, including a series of health and toxicity tests for EPA registrations, has been used to support the approval of SurroundTM products for organic crop production.

Action of Particle Films on Arthropods Two basic actions of mineral particles against insects have been well addressed in the literature. Minerals (diatomaceous earth, fumed silica) that are abrasive or absorptive to the insect’s cuticular

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waxes can be used for control of insects, mainly stored grain pests. Minerals that were white and reflective to sunlight (calcium carbonate) could potentially be applied as whitewashes to the soil as reflective mulches to repel aphid pests. Although these concepts were sound, these materials had little impact on the arthropod pest control indus try, although calcium carbonates have been widely used for sunburn protection in fruit production. Particle film technology diverged from all other mineral-based insecticides in concept where the effects on insect behavior and on plant health were recognized. A major advancement in this technology was in formulation chemistry that enabled kaolin particles to be mixed with water, applied through conventional pesticide sprayers, forming a porous film, and producing a film that could resist rain and wind, yet be easily removed after harvest. Particle films act on the insect’s processes of locating and accepting plants as hosts for feeding and reproduction which are dictated through the senses of touch, taste, sight, and smell. During the process of locating and accepting hosts, the four senses interact to produce both positive and nega tive cues, the sum of which provokes a positive or negative behavior in insects. Plant tissues coated with white particle films are altered visually and tactilely to insects. Particle films also may alter the taste or smell of the host plant. Choice and no-choice laboratory bioassays on various insects revealed that the primary mechanism of action was repellence of adults from treated foliage, resulting in reduced feeding and oviposition. Repellency is only used tentatively as a mecha nism since it has not yet been demonstrated if insects orient away from particle films before film contact (repellence) versus after film contact, which is more appropriately termed a deterrent. Other mechanisms include (i) reduced survival of adults or immature insects (larvae) when born into the particle film coated leaf environment, (ii) reduced mating success of adult Lepidoptera exposed to particle films, (iii) impeded move ment/host finding ability within plant canopies,

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(iv) camouflage of the host by turning the plant foliage white with the particle film, and (v) imped ance of the insect’s ability to grasp the plant. Most of the effects particle films have on insects result from particle attachment to the insect’s various body parts (Fig. 1). The underlying mechanisms of this technology make it unlikely that insects would develop resistance.

Particle Film Applications for Arthropod Pest Control Applications of particle films, M-96–018, M-97–009, SurroundTM and SurroundTM WP for pest control are typically made at 3–6% solids in water (w:w). Particle film solutions can be applied by any type of boom, orchard blast, or hand sprayers and can be applied aerially. Research on

film weather ability and functionality on insects have concluded that 3% are as effective as 6% solu tions under most circumstances. There are usually at least three applications made 7–14 days apart for control of foliar pests. In certain circumstances, such as dormant applications, only 1–2 applica tions of 6% solutions are needed for pear psylla control in pear. Applications are typically made to near “run-off ” or “drip,” and are considered a “dilute application” where 200 gallons/acre (1850 L/ha) are applied to mature fruit trees 8 m in height. The principal use for particle films is for con trol of pear psylla, Cacopsylla pyricola Foerster, in pear in the USA and (Fig. 2) Europe. Dormant applications of SurroundTM WP and SurroundTM CF have been used on nearly 100% of the pear acreage in northern Washington over the past several years. Particle films are effective against many key orders of arthropod pests affecting crops

Kaolin-Based Particle Films for Arthropod Control, Figure 1 SEM of a two-spotted spider mite, Tetranychus urticae Koch., that was exposed to a M-96–018 particle film treated apple leaf for 10 minutes. Inset is a 10 μm diameter circle to indicate scale of particle coverage.


Kaolin-Based Particle Films for Arthropod Control, Figure 2 Particle film, Surround WP, dormant timing application to pear to prevent infestations of pear psylla near Wenatchee, Washington, USA.

including hemipterans, coleopterans, lepidopter ans, dipterans, rust mites, and eriophyid mites. Examples of other uses are for leafhoppers and sharpshooter control in grapes, plum curculio, Conotrachelus nenuphar (Herbst), in apple and plum, and olive fruit fly, Bactrocera oleae L., in olive. Particle films are not effective against tetranychid mites and San Jose scale, Quadraspidiotur perniciosus (Comstock), in tree fruits. These pests are generally controlled by natural predators and parasites and the particle film is thought to reduce the efficacy of these beneficial organisms. Research continues to expand, with over 25 research papers on the effects of particle films on insects on various crops. Most of the research focuses on crops where particle film residues are either not a concern and are processed with the fruit (e.g., wine grapes, fruits for juices) or are removed in pack house operations where fruits are washed, brushed, waxed and bagged (e.g., apples, pears, citrus) for the fresh fruit and vegetable market.

Multi-Functionality of Particle Films Initial studies into particle film technology discovered that plants directly benefited from the film’s properties, including film porosity,

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which allowed gas exchange between the leaf and atmosphere, and the ability of the film to transmit photosynthetically active radiation (PAR) yet exclude ultraviolet (UV) and infrared (IR) radiation to a significant degree. Whole-tree photosynthesis, water use efficiency, yield, size, and quality of apples were compared for the kaolin, SurroundTM WP, and calcium carbonate. Only the kaolin formulation increased photosynthesis over the untreated control although water use efficiency was reduced through increases in stomatal conductance associated with reduced leaf temperature. Calcium carbonate, despite its white color, produced none of these effects and reflected more PAR from the tree canopy than processed kaolin. Increases in plant photosynthesis from kaolin-based particle film treatments can lead to favorable effects on plant productivity. Yield and fruit size increases have been noted in apple, pear, cotton, and citrus. In addition, cooling of the tree canopy through the reflectance of IR can improve fruit color in apple and pear, but these results are variety dependent. Numerous studies throughout the world have supported the consistent ability of a kaolin particle film to reduce sunburn. Reflectance of IR and UV in conjunction with significant reductions in plant surface temperatures reduce solar injury. The impact of particle film technology as a sunburn prevention agent in agriculture is essentially equal to the pesticidal uses of particle film. SurroundTM WP is currently used to prevent sunburn and heat stress in apple, pear, citrus, walnut, banana, canta loupe, and tomato. Particle films have many other applications where the properties of the films can be altered by particle physics and formulation chemistry. These potential uses include sprayable reflective mulches, herbicides, frost prevention, and in pesticide delivery.  Visual Attractants and Repellents in Ipm  Host Plant Selection by Insects  Diatomaceous Earth  Pear Psylla

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References Glenn DM, Puterka GJ, Van der Zwet T, Byers RE, Feldhake C (1999) Hydrophobic particle films: a new paradigm for suppression of arthropod pests and plant diseases. J Econ Entomol 92:759–771 Glenn DM, Puterka GJ (2005) Particle film technology: A new tool for agriculture. Hortic Rev 31:1–45 Puterka GJ, Glenn DM, Pluta RC (2005) Action of particle films on the biology and behavior of pear psylla (Homoptera: Psyllidae). J Econ Entomol 98:2079–2088 Puterka GJ, Glenn DM, Sekutowski DG (2000) Method for protecting surfaces from arthropod infestation, U.S. Patent No. 6,027,740 Puterka GJ, Glenn DM, Sekutowski DG, Unruh TR, Jones SK (2000) Progress toward liquid formulations of particle films for insect and disease control in pear. Environ Entomol 29:329–339 Puterka GJ, Reinke M, Luvisi D, Ciomperik MA, Bartels D, Wendel L, Glenn DM (2003) Particle film, Surround WP, effects on glassy-winged sharpshooter behavior and its utility as a barrier to sharpshooter infestations in grape. Online. Plant Health Progress doi:10.1094/PHP2003–0321–01-RS

Kaszab, Zoltán George Hangay Narrabeen, NSW, Australia Zoltán Kaszab was born on the September 23, 1915 at Farmos, in Pest- Pilis- Solt- Kiskun Shire in Hungary. Even as a child, he was deeply inter ested in animals, especially insects. He completed his tertiary education at the University of Science in Budapest, where he was awarded a doctoral degree in zoology, geology and mineralogy. After university he gained employment with Professor Endre Dudich in the Institut of Zoological Taxonomy and eventually joined the staff at the Hungarian Natural History Museum in Budapest. In 1955 he became the chief curator of the zoo logical collections and from 1970 until 1985 he was the principal director of the museum. Kaszab was an extremely hard worker, totally committed to entomology, specifically to the Tenebrionidae and Meloidae (Coleoptera). He researched the tenebrionid beetles of Bíró’s vast New Guinean

collection and published the results. In a relatively short time he became a world expert of these aforementioned beetle families. From 1963 until 1968 he dedicated most of his time and energy to the zoological exploration of Mongolia. During this period he undertook six collecting expedi tions, mostly on his own, and collected 486,342 specimens, mainly insects. More than 200 workers from the international scientific community participated in the research of this singular collec tion. By the mid 1980s nearly 500 papers (approx imately 7,000 pages in total) were produced, including 60 new genera and 1,600 new species. Zoltán Kaszab appeared to be physically strong, yet he had a weak heart. In 1963, just before his first Mongolian expedition, he overcame a very serious illness and survived a major heart opera tion. His health improved somewhat and he could work harder than anyone around him. In the mideighties his health declined and he had to resign from his directorial post in order to devote him self completely to his beetle studies. On the April 4, 1986 he passed away. Zoltán Kaszab’s achieve ments in entomology are unparalleled amongst the Hungarian entomologists. He described 2,800 new species and published 397 scientific papers, totalling approximately 10,000 pages.

References Matskási I (1987) In memoriam Dr. Zoltán Kaszab (1915–1986). Annales Historico-Naturales Nationalis Hungarici, Tomus 79. Budapest, Hungary Papp CS (1986) In memoriam Zoltán Kaszab (1915–1986). Entomography, vol 4

Katydids (Orthoptera: Tettigoniidae) Darryl Gwynne University of Toronto, Toronto, ON, Canada Katydids belong to a family of ensiferan orthopter ans with over 6, 000 described species and found

Katydids (Orthoptera: Tettigoniidae)

in a variety of habitats on all continents except Antarctica. Most taxonomic schemes recognize katydids (called bush-crickets in Europe) as a family, Tettigoniidae. Katydids are typically large insects of several centimeters in length. They share with most other Ensifera – a suborder that includes Grylloidea, the true crickets, Rhaphidophoridae, the camel crickets, and Anostostomatidae, the weta – nocturnal activity, long antennae, a long blade-like ovipositor, tibial tympana, and a com plex spermatophore that has a spermatophylax serving as a food gift for the female. There are about 17 subfamilies although this scheme is likely to be revised with further phylogenetic study. A formal phylogenetic analysis of the family is cur rently lacking. The earliest fossil tettigoniids are Permian. Katydids are best known for the distinct male sounds produced by tegminal (forewing) stridula tion and used to attract mates. In many species the tegmina are leaf-like, allowing daytime crypsis in the vegetation habitat. Other species have short tegmina, a robust cricket-like appearance, and inhabit low vegetation, occasionally moving over the ground. The use of vegetation as a retreat during daylight contrasts with most other ensifer ans that use burrows or crevices. Features that distinguish katydids from other ensiferans, and indicate that the family is a natural (monophyl etic) group, include: four tarsal segments, leftover right tegminal stridulation, and certain DNA sequences. Grylloidea, the second most diverse ensiferan subgroup, also show tegminal stridula tion but with the opposite tegminal overlap to that of katydids. Also, in contrast to other ensiferan subgroups, most species of true crickets and katydids have an egg-to-adult life cycle that is completed within one year. As in other Ensifera, many katydids lay their eggs in soil. However, many others oviposit into leaves, bark and other plant parts, or paste their flattened eggs like overlapped shingles onto leaves. There is a diversity of development patterns typi cally involving diapause, the temporary cessation of development during favorable conditions in

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order to survive future severe periods such as winter. Eggs of some species diapause through just one winter, whereas in others several winters may be required to continue development to the adult stage. Depending on the species, there are four to nine instars. A few tropical species show an unusual change during development. For example, the small larvae of Macroxiphus sumatranus (Cono cephalinae) mimic ants both in structure and movement whereas the adult insect is brightly colored and aposematic. Some katydids are herbivorous, others car nivorous, but most species are omnivores. A few species have specialized diets such as pollen (the Australian Zaprochilinae). The list of natural enemies of tettigoniids includes predators such as bats that orient to the calls of males. Sphecid wasps (some of which are katydid specialists) use paralyzed katydids as food provisions for their fossorial larvae. Katydid killers also include parasitoids such as ormiine flies (Tachinidae) that larviposit on males after being attracted to their calls, and the thread-like horsehair worms (phy lum Nematomorpha) and mermithid nematodes that can virtually fill the body cavity of their hosts. Important parasites include endoparasitic microsporidians and gregarine protozoans. Ectopar asites include mites, stick ticks (ceratopogonid flies) and strepsipterans. Katydid defenses against natural enemies include camouflage with some tropical katydids showing remarkable mimicry to leaves. A few species have chemical defenses including reflex bleeding in which blood squirts can be aimed at predators. Although most katydids live a mainly soli tary existence, a few show gregarious habits which can lead to economic damage. For example aggregations of ovipositing false-leaf katydids (Pseudophyllinae: Pterophylla) can damage forest trees. A few species at very high densities show coordinated group behavior. This is best known in the locust-like swarms of flying cone-headed katydids (Conocephalinae: Ruspolia) in Africa and, in particular, the massive migrations of bands of North American Mormon crickets, a

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Katydids (Orthoptera: Tettigoniidae)

flightless shield-backed katydid (Tettigoniinae: Anabrus simplex). Band-forming populations contrast with other populations of Mormon crickets that are quite solitary in their behavior. Bands form in the early instars and by the adult stage can form huge aggregations several hundred meters wide and kilometers long that show highly directed migrations. Such bands can devastate agricultural crops. Individuals in bands experi ence a much reduced risk of predation but need to move continuously to avoid cannibalism by conspecifics. Cannibalism reflects intense compe tition within the band for protein and salt. Male katydids stridulate by moving a scraper on the top of the right tegmen over a file on the underside of the left tegmen. Stridulatory calling is found in virtually all species and functions mainly to attract females. Calling song can mediate female choice of males and in a few species can serve as a barrier to matings between species. In most species the male song is a series of noisy (broad spectrum of sound frequencies) buzzes, zips or clicks. More musical (narrow spectrum) sounds are produced by many neo tropical species, some of which are ultrasonic. Although pairing in most species is accom plished when the female is attracted to the male call, in a few species, including many Phanerop terinae, females answer males with their own call and males move to these sounds. Individuals hear sounds using a complex system of foretibial tympana connected to specialized thoracic tracheae and paired thoracic spiracles. The acoustical systems of katydids have been studied extensively and have been model systems for neurophysiological, behavioral and evolutionary studies. Copulation typically follows the female mounting the male and the mated pair assuming a position in which the male is curled behind the female. The end of the spermatophore is inserted into the female’s genital chamber. The exterior sperm ampullae and attached spermatophylax of the spermatophore comprise up to 40% of the male’s weight (Fig. 3).

Katydids (Orthoptera: Tettigoniidae), Figure 3 Photograph: Mormon crickets, the shield-backed katydid Anabrus simplex. The female in the foreground has just mated and has a spermatophylax meal attached to her abdomen. The male is in the background. His short singing wings protrude from beneath the pronotal shield.

The need for protein in katydids in band-forming Mormon crickets, and katydids in which food supplies can be limited, underlies extreme varia tion in sexual selection and mating behavior observed in these species. Starvation decreases male mating (spermatophore producing) fre quency but increases the propensity of hungry females to mate as they seek spermatophore meals. This leads to sexual competition among females that is not seen in populations with adequate food. Experimental manipulations of proteinaceous food in these species have supported a central tenet of sexual selection theory that relative investment of the sexes in offspring controls sexual differences in both mate choice and sexual competition.  Grasshoppers, Katydids, and Crickets (Orthoptera)  Mormon Cricket  Cannibalism  Gregarious Behavior in Insects  Sexual Selection  Acoustic Communication in Insects

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References Bailey WJ, Rentz DCF (eds) (1990) The Tettigoniidae: biology, systematics and evolution. Crawford House, Bathurst, Australia, 395 pp Capinera JL, Scott RD, Walker TJ (2004) Field guide to grass hoppers, katydids, and crickets of the United States. Cornell University Press, Ithaca, NY, 280 pp Gwynne DT (2001) Katydids and bush-crickets: reproductive behavior and evolution of the Tettigoniidae. Cornell University Press, Ithaca, NY, 400 pp Ragge DR, Reynolds WJ (1998) The songs of the grasshoppers and crickets of western Europe. Harley Books, Colchester, UK, 600 pp

Kaufmann Effect The developmental response of insects to temper ature is usually determined by exposing different groups of them to various constant temperatures. The relationship between environmental tempera ture and insect development rate over most of the range between the highest and lowest tolerable temperatures is usually linear, with higher tem peratures promoting (up to a point) higher rates of development. However, some nonoptimal tem peratures may cause either a retardation or accel eration of development rates; this deviation from what is expected (non-linearity) shows up when insects are exposed to alternating temperatures. The difference between development predicted by linear models, and the development observed under variable temperature conditions (or pre dicted by nonlinear models) was first observed by O. Kaufmann in 1932, and so is called the “Kaufmann effect” or the “rate summation effect.”  Phenology Models for Pest Management

References Petavy G, David JR, Gilbert P, Moreteau B (2001) Viability and rate of development at different temperatures in Drosophila: a comparison of constant and alternating thermal regimes. J Therm Biol 26:29–39 Worner SP (1992) Performance of phenological models under variable temperature regimes: consequences of the Kaufmann or rate summation effect. Environ Entomol 21:689–699

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Kauri Moths (Lepidoptera: Agathiphagidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Kauri moths, family Agathiphagidae, have only two known species, one each from Queensland and Fiji. The family comprises the monobasic superfamily Agathiphagoidea and the only representative of the suborder Aglossata. Adults small (9–14 mm wing span), with head vertex rough-scaled; with rudi mentary chewing mouthparts (haustellum absent); short labial palpi, 3-segmented; maxillary palpi 5-segmented and folded. Maculation somewhat similar to Micropterigidae but mostly gray with fine speckling spots. Adults are diurnally active. Larvae are seed-borers of kauri pines (Agathis, Araucari aceae) of the South Pacific and are modified for this kind of feeding. Thus, they appear much more elon gated and different from larvae of Micropterigidae.

References Common IFB (1973) A new family of Dacnonypha (Lepi doptera) based on three new species from southern Australia, with notes on the Agathiphagidae. J Aust Entomol Soc 12:11–23 Dumbleton LF (1952) A new genus of seed-infesting microp terygid moths. Pac Sci 6:17–29 Kristensen NP (1967) Erection of a new family in the lepi dopterous suborder Dacnonypha. Entomlogiske Med delelser 35:341–345 Kristensen NP (1984) The male genitalia of Agathiphaga (Lepidoptera, Agathiphagidae) and the lepidopteran ground plan. Entomologica Scandinavica 15:151–178 Upton MS (1997) A twelve-year larval diapause in the Queen sland kauri moth, Agathiphaga queenslandensis Dumb leton (Lepidoptera: Agathiphagidae). Entomologist 116:142–143

Ked A louse fly; a member of the fly family Hippoboscidae.  Flies

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Keel

Keel The crest or raised ridge running along the dorsal midline of cockroach oothecae; the median carina (a dorsal raised ridge) on the pronotum of a grasshopper.

Kellogg, Vernon Lyman Vernon Kellogg was born December 1, 1867, in Emporia, Kansas, USA. He received his B.S. and M.S. degrees from the University of Kansas in 1889 and 1892, respectively. He also was awarded the LL.D. degree from the University of California in 1919 and from Brown University in 1920. He was awarded a Sc.D. from Oberlin College in 1922. Kellogg worked at the University of Kansas as an assistant professor of entomology, and then at Stanford university as an assistant professor, associate professor, and professor. He was a suc cessful teacher of entomology. His areas of expertise were morphology, genetics, and behav ior. Kellogg authored several general zoology and evolution texts, and also an economic ento mology and zoology book (co-authored with R.W. Doane). Despite a successful career as an educator, Kellogg is best known for his humani tarian work. During World War I, he worked U.S. Food Administration and other relief groups in Europe in the aftermath of the war. He was deco rated by several European governments for his humanitarian efforts. He was also instrumental in forming the National Research Council in the USA, an agency that links government and science. He died August 8, 1937.

Kennedy, John S John Kennedy was born May 15, 1912, in Pennsylvania, USA, but spent most of his early life in London, England. He attended University College, London and then attained a M.S. with G. S. Frankel followed by a Ph.D. in 1938 at the Imperial Institute of Entomology in Birmingham. He studied locusts and mosquito behavior before joining V. B. Wigglesworth at the Unit of Insect Physiology in Cambridge. The unit was dissolved in 1967 but Kennedy moved to Imperial College and started a new physiology research unit. Kennedy was known for his research on many facets of insect behavior, including animal orientation, insect migration, and insect flight. He was a leader in separating behavioral research from anthropo morphic interpretation, an unfortunate result of the influence of Konrad Lorenz and research on “higher” animals. This crusade won him few friends initially, but his disciplined, clear-thinking approach won out and he eventually received con siderable acclaim, honors and awards. He died on February 4, 1993, at Oxford, England.

Reference Brady J (1993) Professor J. S. Kennedy, F.R.S., (1912–1993). Antenna 17:105–107

Kermesidae A family of insects in the superfamily Coccoidae (order Hemiptera). They sometimes are called gall-like coccids.  Bugs  Scale Insects and Mealybugs

References Essig EO (1931) A history of entomology. The Macmillan Company, New York, NY, 1029 pp Mallis A (1971) American entomologists. Rutgers University Press, New Brunswick, NJ, 549 pp

Keroplatidae A family of flies (order Diptera).  Flies

Kershaw, John Crampton Wilkinson

Kershaw, John Crampton Wilkinson Emmett R. Easton University of Hawaii at Manoa, Honolulu, HI, USA John Kershaw was born in Broughton, Notting hamshire, England, in 1871, and was known as a scholar as early as age 10. His father, George S. Kershaw, was Vicar of Broughton in Nottingham. Very little is known of John’s early life but his two younger brothers were also interested in entomol ogy. Colonel Sidney H. Kershaw collected butter flies and moths wherever he was stationed and G. Bertram Kershaw collected them in England, so the family was interested in Lepidoptera. John grew up during the latter part of the nineteenth century when the need of a college education was not an absolute necessity to work in natural history; however, his lack of it may have influenced success in later life. The coleop terist David Sharp, who was most liberal in giv ing assistance and encouragement to young persons planning to visit other countries, may have influenced him, as many entomologists as well as zoologists went to Sharp at the Cambridge museum in search of information about suitable equipment and the most profitable method of work. He was surely influenced by Edward B. Poulton, Hope professor of Zoology at the University of Oxford, who collected a wide vari ety of natural history objects. Kershaw’s robber flies collected in Macao are listed in Poulton’s pioneering work on Predaceous insects and their prey (Transactions of the Entomological Society of London, 1906) and Kershaw and Frederick Muir are listed in several of the Hope Reports (Oxford University) for their contributions in entomology in Macao, South China, over several years. He was certainly influenced by his longlived friend, Dr. Robert C. L. Perkins, with whom he collected Odynerus vespid wasps in Hawaii later in 1912.

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In 1898, at the age of 28, John Kershaw was in China where he studied natural history. He met the ornithologist and Englishman Frederick W. Styan (a tea merchant in Shanghai) who influenced him to study birds. Kershaw observed and collected them along the South China coast before Hong Kong became established. At that time, the Portuguese enclave of Macao was occupied by the English and other Europeans exploring or doing business in China. John Kershaw occupied one of the beautiful colonial type residences at 19 Praie Grande in Macao on the outer harbor as early as 1900, and used the rooftop of his home to rear the insects he studied. When the exploratory entomologist Frederick A. G. Muir came to China via Macao in 1906–1907, they collaborated in Hawaiian Sugar Planter Asso ciation activities. Kershaw had recently published, and was becoming well known for his book on the Butterflies of Hong Kong (1906), the first to be pub lished on South China Lepidoptera. Kershaw probably gained insight on insect parasitoids from his friend, as Muir was looking for biological control agents that could be introduced into Hawaii to control a leafhopper. Biological control had been criticized by economic entomologists, and Muir set out to prove that it would work in Hawaii. The sugar cane weevil, Rhabdocnemis obscura (Boisduval), was also affecting sugar pro duction in the islands and Muir was looking for a biological control agent to control it. John Kershaw possessed local experience collecting insects that was not found among others in Macao. He had collected Hemiptera that were sent to G. W. Kirkaldy in Honolulu. This had resulted in several papers they published together until Kirkaldy’s untimely death in 1900. Kirkaldy had named a cicada after Kershaw that the latter found in Macao; it remains known as Balinta kershawi Kirkaldy. John Kershaw also traveled with Muir to the How-lik Monastery area in the Guangdong province of China, collecting insects that were housed in the former Hawaiian Sugar Planters insect collection (currently in the Bernice P. Bishop Museum, Honolulu).

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Kershaw, John Crampton Wilkinson

After collecting in the How-lik area among fine forest trees in virgin forest (in what is now known as the Dinghushan Biosphere Reserve) in search of cane leafhopper parasites, they began to search in other areas of Southeast Asia. In November 1908, they both traveled to Indonesia to look for parasites of the sugar cane weevil in west Ceram (The Moluccas). Although unable to locate para sitized cane borers, their time was still profitable with the discovery of a new velvet worm (Ony chophora), a species of Peripatus known today as Paraperipatus ceramensis (Muir and Kershaw). This invertebrate was earlier believed to be a “miss ing link” between the Annelids and the arthropods, and they worked out the developmental biology in this animal. In a later trip to Papua New Guinea in 1909, Muir discovered a tachinid fly, Lixophaga sphenophori (Villeneuve) that was affecting populations of the sugar cane weevil and he tried to import it into Hawaii, but failed to bring in enough live material for propagation and release in the fields. John Kershaw was sought from Macao to help him in this endeavor. John had developed exceptional skill in keeping insects alive. For example, he had reared several species of butterfly including the rare lycaenid Miletus chinensis C. Felder, and the ant-attended larva of the long-banded silverline, Spindasis lohita (Horsfield), in preparation for his book on Hong Kong butterflies. He was also suc cessful in culturing an asilid fly (Promachus sp.), the pentatomids Erthesina fullo (Thunberg) and Chrysocoris stollii (Wolff), a predaceous pyrrhoc orid bug Dindymus sanquineus (Fabricius), the fulgorid Fulgora candeleria (L.), and even a rare primitive grasshopper of the genus Eumastax, now known as Erianthus versicolor Brunner van Wattenwyl in the family Eumastacidae. In 1910 Kershaw left Macao and traveled to Mossman in Queensland of northern Australia to establish a rearing colony of L. sphenophori at the Mossman central sugar mill. The flies had been collected originally in lowland Papua New Guinea, and work at the mill was pre-arranged by Muir. Kershaw then approximated the natural conditions

of the fly by designing very large cages over 2 m in height (screen covered and topped with leafy materials to supply shade during sun-lit periods of the day) and he filled them with sugar cane stalks and placed the cages a foot above the ground on posts to avoid predation by ants. The smaller sized cages used earlier had evidently lacked enough space to allow the pre-nuptial flight nec essary for mating behavior in the tachinid flies because although the smaller cages only produced 10 parasitoid puparia, the new large cages pro duced 300 puparia. Using a relay station in the Fiji islands, Muir brought live larvae and pupae in sugar cane stalks into the state during the latter part of 1910, and Kershaw arrived later with addi tional stock. Their actions insured that enough parasitoids reached Hawaii’s plantations to save the sugar industry from appreciable loss. Without Kershaw’s mass rearing skills, this fly would not have been successfully reared and the cane-beetle effectively controlled in Hawaii. Kershaw was a member of the Hawaiian Entomological Society, a Fellow of the Entomolog ical Society of London, a fellow of the Zoological Society of London, and also a Fellow of the Ento mological Society of Belgium. He resigned as assis tant entomologist with the Hawaiian Sugar Planters Association in 1912 taking a position in Trinidad, West Indies, working on economic control of the froghopper Tomaspis sp. (Hemiptera) of sugar cane. After completing this contract, he returned to England and, following the war, wrote a natural history book with the local historian Charles G. Harper on the Downs and the Sea, wildlife and scenery in Surrey, Sussex & Kent, published by C. Palmer, London, in 1923. He then retired as an entomologist/zoologist. He passed away in Whiffen’s cottage, Kent County, England, on the August 26, 1959 at age 79. If not acknowledged as the father of natural history in South China, Kershaw should at least be remembered as the “Father of Entomology in Macao.” In addition to the aforementioned accomplishments and abilities, he was skilled in insect embryology, writing on egg development in

Key Factor

Siphanta acuta (Walker), a flatid hemipteran (common at higher elevations in Hawaii), and on Pristhesancus papuensis, a New Guinea reduviid. Also, he was an early pioneer in the study of webspinning Embioptera, and one of the first persons to study egg development in Antipaluria urichi (de Saussure) in Trinidad. A skilled craftsman, he was an excellent illustrator in all of his publications. This is particularly apparent in his excellent draw ings on the anatomy of the fulgorid homopteran, F. candeleria, once believed to possess a snout with luminous qualities and commonly found on trunks of lychee and longan trees in South China.

References Easton ER (1999) John Kershaw – Something old and some thing rare: the work of one of South China’s earliest naturalists. Porcupine, Newsletter of Ecology and Biodi versity, University of Hong Kong, vol 20, p 28 Kershaw JC, Kirkaldy GW (1910) A memoir on the anatomy and life history of the homopteran insect, Pyrops candeleria (or candle-fly). Zoologische Jahrbücher. Abteilung für Systematik, Geographic and Biologie 29:108–124 Kershaw JC (1907) The life history of Spindasis lohita Horst. Trans Entomol Soc Lon 55:245–248 Kershaw JC (1914) Development of an Embiid. J R Microsc Soc 34:24–27 Muir F, Kershaw JC (1909) Peripatus ceramensis n. sp. Q J Microsc Sci 53:737–740 Muir F, Kershaw JC (1912) Development of the mouthparts in the homoptera with observations on the embryo of Siphanta. Psyche 19:77–89 Steinheimer FD, Easton ER, Lewthwaite RW (2003) Redis covery of John Crampton W. Kershaw’s birds from Macau including his record of small Niltava. Bull Br Ornithol Club123:220–227

Kerriidae A family of insects in the superfamily Coccoidea (order Hemiptera). They sometimes are called lac insects or lac scales.  Bugs  Scale Insects and Mealybugs  Shellac  Costs and Benefits of Insects

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Kevan, Douglas Keith Mcewan Keith Kevan was born at Helsinki, Finland, in 1920, but spent most of his early years near Edinburgh, Scotland. He attended Edinburgh University and graduated with first class honors in 1941. He then attended Imperial College, Trinidad for a two-year course in tropical agriculture, and afterwards worked in Kenya with the Kenya Department of Agriculture. He returned to England in 1947 to head the Zoology Section of the University of Nottingham, where he worked on soil fauna but also developed a strong interest in orthopteroids. Kevan relocated to Canada in 1957 to head the Entomology Department at McGill University in Quebec, where he served as chairman from 1957 to 1971. Kevan was an accomplished entomologist as well as an effective administrator. He became one of the world’s foremost authorities on grasshoppers, and the undisputed authority on the family Pyrgo morphidae. He also was interested in Neuroptera, and published on cultural entomology and eth noentomology. He authored several books includ ing “Soil animals” (1962), and several monographs on grasshoppers and locusts. In addition, he authored over 400 technical articles. Kevan served as president, and was named a fellow of the Ento mological Society of Canada, as well as receiving many other honors. He also played a key role in ini tiating the biological survey of insects of Canada. Kevan died in 1991.

References Vickery VR (1991) Douglas Keith McEwan Kevan. Am Ento mol 37:253–254 Vickery VR (1992) Douglas Keith McEwan Kevan (1920– 1991). Antenna 16:4–6

Key Factor The factor most responsible for changes in popu lation trends. In life table studies, key factor

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Key Pests

a nalysis is used to identify population regulating mechanisms.  Life Table

Key Pests The pests that have the greatest potential to affect the profitability of the crop.

Keystone Species A species that has a particularly great influence on an ecosystem and, if removed from the system, its loss has a significant effect on the entire eco system, especially its other inhabitants.

Khapra Beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae)

After a short pre-oviposition period, females (Fig. 4) deposit up to100 eggs, but mean fecundity is about 35 eggs. The eggs are cylindrical, with one end rather pointed and bearing spine-like projec tions, but the other end rounded. Normally they measure about 0.7 mm long and 0.25 mm wide. They are translucent white, but yellowish or red dish marks develop on the chorion. The eggs hatch in 3–14 days, depending on temperature. The larvae are yellowish brown or brown, and bear numerous long hairs on the dorsal sur face. Younger larvae bear a “brush” of long hair on the ninth abdominal segment that projects like a “tail,” and although this look tends to dimin ish as the larvae grow older, the tuft of hairs remains prominent. The larval period can be completed in 15 days, but when faced with star vation the larvae can persist for 13 months, and with limited food can survive for up to six years! Males typically undergo four instars, females five, though this varies considerably. Larvae attain a length of about 5 mm. Young larvae feed on cracked grain kernels as such food is not protected

John L. Capinera University of Florida, Gainesville, FL, USA A very serious pest of stored grain, khapra beetle has been the target of many successful eradica tion efforts in regions of the world where it does not naturally occur. Generally, it thrives in warm dry regions. It is found in northern and central Africa, the Middle East, and east through India to Myanmar. It is generally absent from Europe, though there are a few localized infestations. Pres ently it is absent from the western hemisphere, Australia, and New Zealand. The life cycle can be as short as 35 days at about 34°C, but is nearly 150 days long when reared at 10°C. As many as 12 generations are reported annually in India. The adults are short-lived, seldom living more that 10–12 days. Mating occurs immediately at high tempera tures but may require several days at cooler temperatures.

Khapra Beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae), Figure 4 Adult Khapra beetle, Trogoderma granarium.

Khapra Beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae)

by a seed coat, but larger larvae attack the intact kernel. Larvae (Fig. 5) are usually found feeding on the surface of infested material, but can pen etrate several centimeters in search of food. Cast skins also are commonly found on the surface of grain containing infestations. Some larvae are able to undergo diapause when exposed to unfa vorable temperature, humidity and crowding, but others lack the capacity for diapause. When they are ready to pupate, larvae crawl into crevices. Pupation occurs within the last lar val exuvium, and typically lasts 3–5 days. Pupae measure about 5 mm long, and are light brown, and bear a medial ridge of long hairs dorsally.

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The emerging adults are small, only 1.8–3.8 mm long. They are oblong-oval in shape, and females are larger than males. They are yellowish brown to reddish brown, with the pronotum u sually darker than the elytra, and indistinct reddish brown marks on the elytra. The males are distinguished from other male Trogoderma by an antennal club of five or fewer segments; females by an antennal club of three or fewer segments. The adults can produce eggs without having to drink or eat after emerging. Adults reportedly do not fly. Several natural enemies are known, includ ing predatory Hemiptera and mites, parasitic wasps, and diseases. Biological suppression is not practiced.

Damage This species attacks such vital staples as wheat, barley, rice, millet, sesame, corn (maize), sor ghum, and peanut. Feeding reduces grain to a powdery mass, reducing weight and grade of the grain. The larvae chew through grain sacks as well, weakening the fibers and resulting in tears. They are favored by hot, dry conditions and can not compete with other species under moist conditions.

Management

Khapra Beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae), Figure 5 Larva of Khapra beetle, Trogoderma granarium.

Hygiene is an important element of management, and it is useful to remove old grain, avoid spillage, and fill cracks and crevices. Treatment of grain storage facilities with residual contact insecticides deters infestation, and fumigants are used to dis infest grain. The diapausing larvae are fairly resis tant to fumigants, so protracted fumigation is advised. On-farm grain storage in India often used neem seed powder mixed in with the grain. Heat treatment also can be effective. Traps for detecting infestation use both food and sex pher omones as bait.  Stored Grain and Flour Insects

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Kiesenwetter, Ernst August Hellmuth Von

References Banks HJ (1977) Distribution and establishment of Trogoderma granarium Everts (Coleoptera: Dermestidae): climatic and other influences. J Stored Prod Res 13:183–202 CABI and EPPO (1997) Trogoderma graminarium. In: Quar antine pests for Europe, 2nd edn. CABI International, Wallingford, UK, pp 554–559 Hadaway AB (1956) The biology of the dermestid beetles Trogoderma granarium Everts and Trogoderma versicolor Creutz. Bull Entomol Res 46:781–796

Kiesenwetter, Ernst August Hellmuth Von The noted Saxon entomologist E. A. H. von Kiesenwetter was born at Dresden, Germany, on November 5, 1820. He studied law at the Univer sity of Leipzig until 1843, and rose to promi nence in the Ministry of the Interior. He began taking collecting trips, and publishing entomo logical articles, in the 1840s. Though known principally as a coleopterist, Kiesenwetter also published on other orders. His principal contri bution, other than the numerous papers he authored, was to author much of the Coleoptera section of the “Naturgeschichte der Insecten Deutschlands.” He died on March 18, 1880, at Dresden, Germany.

References Anon (1880) Obituaries, E. A. Hellmuth von Kiesenwetter. Entomol Mon Mag 16:280 Herman LH (2001) Kiesenwetter, Ernst August Hellmuth von. Bull Am Mus Nat Hist 265:85–86

King Crickets and Wetas A family of crickets (Anostostomatidae) in the order Orthoptera.  Grasshoppers, Katydids and Crickets  Weta

Kinnaridae A family of insects in the superfamily Fulgoroidae (order Hemiptera). They sometimes are called planthoppers.  Bugs

Kin Selection A theory put forth by W. D. Hamilton (1964) that states that an altruistic act by close relatives is favored because it increases the inclusive fitness of the individual performing the social act. Inclusive fitness is the fitness of the individual as well as his effects on the fitness of any genetically related neighbors. The theory is that alleles change in frequency in a population due to the effects on the reproduction of relatives of the individual in which the trait is expressed rather than on the reproduc tive success of the individual. A mutation that affects the behavior of a sterile worker bee, even though detrimental to her, could increase the fit ness of the worker if her behavior increased the likelihood that a close relative would reproduce. Kin selection could explain the evolution of soci ality, which appears to have developed as many as eleven times in the order Hymenoptera.

Kinesis (pl., kineses) A class of orientation behavior characterized by undirected movements in which the frequency of turning (klinokinesis) or speed of movement (orthokinesis) is related to the intensity of the stimulation. A change in the rate of movement in response to an environmental condition, with the direction of the movement random and unrelated to the stimulus. Often, if conditions are favorable, organisms remain quiescent, mov ing to another location if conditions are not favorable. Types of kineses include: chemokine sis, stereokinesis, photokinesis, and hygrokinesis (contrast with taxis).

Kissing Bugs (Hemiptera: Reduviidae: Triatominae)

Kirby, William William Kirby was born in September 1759 at Witnesham Hall, Suffolk, England. Kirby is known as the “father of British entomology.” He was educated for the clergy, and graduated from Caius College, Cambridge, in 1781. Kirby successfully conducted his ministry, but also studied insects. His first publication was a monograph on British bees, published in 1802. He also established the Order Strepsiptera. He was a fellow and honorary member of numerous scientific societies. Kirby met William Spence when he was 48 years old, and co-authored, with Spence, the first popular ento mology work on insects published in English: “An introduction to entomology,” which was published in four volumes between 1816 and 1826. It remained the most important work on insects published in English for over 100 years, and was published in seven editions. The significance of his work is easy to underestimate because we now take for granted that entomology is a legitimate pursuit, whereas until Kirby and Smith authored their book, the common notion was that anyone inter ested in insects was not entirely sane. He died at Barham, near Ipswich, England, on July 4, 1850.

References Essig EO (1931) A history of entomology. The Macmillan Company, New York, NY, 1029 pp Morris FJA (1915) The centenary of Kirby and Spence’s “An introduction to entomology.” Can Entomol 47:384–386

Kissing Bugs (Hemiptera: Reduviidae: Triatominae) Eugene J. Gerberg University of Florida, Gainesville, FL, USA Kissing bugs of this subfamily are also known as conenoses, Mexican bed bug (Fig. 6), barbeiro, chipo, vichua, pito and other names in Latin

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America. The head of triatomine bugs is more or less cone-shaped, the sturdy proboscis can be thrust forward or repose beneath the head, and the prothorax is well developed. The antennae are four or five-segmented. They fly readily. These insects are obligate blood feeders. Many species are vectors of the trypanosome Trypanosoma cruzi, the etiologic agent of Chagas disease, or American trypanosomiasis. Kissing bugs become infective by imbibing blood from an infected ver tebrate host. The parasite develops in the gut of the triatomine and the infective trypomastigotes pass out in the feces. When the infective feces are rubbed into the bite site, skin, or mucous mem branes, transmission occurs. Another mode of transmission is through blood transfusion. In ver tebrates other than humans, infection may occur by ingestion of the infected bug. The bite of kissing bugs is often painless, a useful adaptation for feed ing on vertebrates, but some are capable of inflict ing a painful bite. Humans vary in their sensitivity to bites. Some bitten individuals are hypersensitive and may suffer an anaphylactic reaction. Kissing bugs are chiefly nocturnal, and on humans they prefer to feed on exposed skin, such as the face, particularly the upper lip, arms and legs. Many species of kissing bugs transmit Trypanosoma cruzi, but Triatoma infestans (Klug), T. maculata (Erichson), T. dimidiata (Latreille), Panstongylus megisus (Burmeister) and Rhodnius prolixus (Stål) are common vectors. Humans suffering from infection often exhibit a swelling of the eyelid and face, a symptom known as “the sign of Romaña.” Infection can last many years, and affect the heart. Some species principally inhabit the soil surface, though others frequent trees or other habitats. Natural hosts are generally woodrats or other animals; humans are accidental. The wood rat builds nest of available plant materials, and these nests are favored by triatomes. Kissing bugs will also feed on domestic pets and wild animals that may occur near human habitation. The development of the kissing bug requires five to eight nymphal instars, which may last

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a fringed cap. They are deposited singly or in small clusters, and deposited in the same habi tats as occupied by adults. The eggs hatch in 8–30 days. In addition to transmission of Chagas disease, bugs can also cause anaphylactic reactions. Hyper sensitivity follows repeated bites. Patients develop nausea and diarrhea, welts and rashes, edema, and itching.  Chagas Disease or American Trypanosomiasis  Assassin Bugs  Kissing Bugs and Others (Hempitera: Reduviidae)  Chagas  Carlos Justiniano Ribeiro

References

Kissing Bugs (Hemiptera: Reduviidae: Triatominae), Figure 6 A representative kissing bug, Triatoma sanguisuga (LeConte), also known as the “Mexican bed bug.”

from three months to a few years. The length of the nymphal instars depends upon the quantity of the blood meals. The nymphs and adults require blood meals usually of vertebrate ani mals. The amount of blood ingested varies from approximately 6 mg to over 275 mg. Females are ready to mate shortly after the final molt. The female may oviposit 1–3 weeks after copulation. There is considerable variation in the number of eggs deposited. The eggs are shiny and smooth. Eggs, which are often barrel-shaped, may possess

Ryckman RE (1979) Host reactions to bug bites (Hemiptera, Homoptera): a literature review and annotated bibliog raphy, pt 1. Calif Vector Views 26:1–24 Ryckman RE, Bentley DG (1979) Host reactions to bug bites (Hemiptera, Homoptera): a literature review and anno tated bibliography, pt 2. Calif Vector Views 26:25–49 Ryckman RE, Casdin MA (1976) The Triatominae of western North America, a checklist and bibliography. Calif Vec tor Views 23:35–52 Tonn RJ (1988) Review of recent publications on the ecology, biology and control of vectors of Chagas’ Disease. Revista Argentina de Microbiologia 20:4–24 Usinger RL (1944) The Triatominae of North and Central America and the West Indies and their public health sig nificance. Public Health Bull 288:1–81

Klee, Waldemar G. Waldemar Klee was born in 1853 in Copen hagen, Denmark. He was educated in agriculture in Denmark, but moved to the USA at the age of 19 and worked for the University of California. For many years he studied the biology and man agement of fruit pests, and was appointed Inspec tor of Fruit Pests by the California State Board of Horticulture in 1886. Klee received parasitoids of cottony cushion scale from Australia and

Koebele, Albert

l iberated them in San Mateo County in 1888, initiating the first biological control effort directed at this serious pest. He died in 1891 in Santa Cruz, California, USA.

Reference Essig EO 1931. A history of entomology. The Macmillan Company, New York, NY, 1029 pp

Knipling, Edward Fred Edward Knipling was born at Port Lavaca, Texas, USA on March 20, 1909. He graduated from Texas A&M University (B.S. 1930) and Iowa State University (Ph.D. 1947) before joining the United States Department of Agriculture for a 43-year career with that agency. He led the Orlando, Florida, laboratory that developed DDT and other insecticides and repellents to protect American troops during World War II from disease- spreading insects. He also led the Insects Affecting Livestock, Man, Households, and Stored Products Division in Washington, DC, and led the Entomology Division. Knipling is credited with developing the sterile insect technique, and also the use of mathematical models for pest suppression based on the sterile insect technique. This technique has been used successfully to eradicate screwworm fly, Medi terranean fruit fly, tsetse fly, melon fly, and other pests throughout the world. He published over 225 technical articles during his career, includ ing an insightful but oft-overlooked book “Prin ciples of insect parasitism analyzed from new perspectives: practical implications for regulat ing insect populations by biological means” (1992). He was a member of the prestigious National Academy of Sciences and received numerous honors and awards. He died on March 17, 2000 in Arlington, Virginia.  Sterile Insect Technique

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Reference Suszikiw J (2000) Edward F. Knipling. Am Entomol 46:269–270

Knockdown Incapacitation of an insect following exposure to a sublethal dose. Following such exposure, insects may recover due to metabolic detoxification of the pesticide, or perish. In assessing the response of insects to insecticides, knockdown is usually assessed separately (at about 1 h post-treatment) from mortality (often at 24 h post-treatment).

Koch’s Postulates Criteria proposed by Koch that are commonly used for establishing the pathogenicity of a micro organism: the microorganism must by consistently associated with the disease; the microorganism can be isolated and grown in culture; and when the microorganism is injected into a healthy host, disease is expressed.

Koinobiont Parasitoids that do not immediately impair their hosts upon oviposition, and host development continues. These are typically endoparasitoids.

Koebele, Albert Albert Koebele was born in 1852 at Waldkirch, Germany. When he moved to the United States is not certain, but he became a citizen in 1880. His abilities so impressed C. V. Riley that Riley appointed him to the US Department of Agricul ture in 1881 and assigned him to work on cotton pests in Florida and Georgia. In 1885 he trans ferred to California to work on fruit pests. He

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was sent to Australia in 1888, where he sent a parasitic fly, Cryptochetum iceryae (Williston), and a ladybird beetle, Rodolia cardinalis (Mul sant), to California. The ladybeetle was a very successful biological control agent, gaining him recognition for saving the citrus industry from cottony cushion scale. On a later trip to the region he also traveled to New Zealand where he intro duced some ladybirds from California into New Zealand, and several additional ladybirds into California. His success earned him the ire of some collaborators who were jealous of his rec ognition, and he resigned from USDA in 1893 to (Fig. 7) join the Hawaii Board of Agriculture and Forestry. There, he continued introductions from Southeast Asia, Australia, Japan, and Mexico. In 1903 he joined the staff of the Experiment Station of the Hawaiian Sugar Planters Association. Koe bele suffered from illness (probably malaria) contracted while living in the tropics, and he returned to Germany in 1908 to recuperate. Dur ing World War I he suffered considerable hard ship and attempts were made to move him back to California. However, Koebele never regained his health, despite his move to Germany, and he was found to be too feeble to be transported. He died in Waldkirch, Germany, his home town, on December 28, 1924.

References Essig EO (1931) A history of entomology. The Macmillan Company, New York, NY, 1,029 pp Mallis A (1971) American entomologists. Rutgers University Press, New Brunswick, NJ, USA, 549 pp

Kraatz, Ernst Gustav Ernst Kraatz was born in Berlin, Germany, on March 13, 1831. He began collecting insects at an early age, and published his first paper at the age of 18. From 1850 to 1853 Kraatz studied law at the Universities of Heidelberg and Bonn, but had no real interest in this field, so he moved to the University of Berlin and obtained a Ph.D. in 1856. He was active in German entomological societies, and founded the Deutsche Entomolo gische Gesellschaft, and served as its president for 25 years. He also was the primary force behind establishment of the Deutsche Entomol ogisches Nationalmuseum. Kraatz was a very prominent coleopterist, and published nearly 1400 papers. He described hundreds of species. Late in life he lost his eyesight. Kraatz died in Berlin on November 2, 1909.

Reference Herman LH (2001) Kraatz, Ernst Gustav. Bull Am Mus Nat Hist 265:90–92

Kring, James Burton

Koebele, Albert, Figure 7 Albert Koebele.

Jim Kring was born on May 25, 1921, at Monett, Missouri. He graduated from Rockhurst College and received both the M.S. and Ph.D. degrees from Kansas State University. After serving in the military during World War II, Kring became an instructor at Kansas State, then moved to the Connecticut Agri cultural Experiment Station, where he worked from 1951 to 1977. In 1977, he became head of the

Kyasanur Forest Disease

Department of Entomology at the University of Massachusetts, and later acting Dean of the College of Food and Natural Resources. He retired in 1981 and moved to Florida, but continued to conduct research in conjunction with the University of Flor ida’s Gulf Coast Research and Education Center at Bradenton, Florida. Kring had diverse interests of both basic and applied nature, but he is remem bered for his pioneering work in aphid ecology. Kring, along with V. Moericke of Germany and J. S. Kennedy of England, elucidated the changing host selection behaviors of dispersing aphids, namely a positive response to sunlight when dis persing, and a negative response to sunlight and a positive response to plant pigments when alighting. He was the first to demonstrate that aphids could be managed through visual disruption of their hostseeking behavior, which he accomplished by appli cation of reflective mulch to the soil surrounding plants. Subsequently, this practice has been shown to be both effective for reducing aphid and whitefly infestation rates and plant virus infection, and eco nomic for high-value crops such as vegetables. Thus, the practice has been widely adopted in some pro duction areas. An author of over 100 papers, Kring was also very involved in professional society affairs. He served as president of the Connecticut Entomo logical Society, the president of the eastern branch

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of the Entomological Society of America, and presi dent of the Entomological Society of America. He received several other honors from this society. He died at Anna Maria, Florida, on October 29, 1990.

Reference Cardé R, Prokopy R, Doane C (1991) James B. Kring. Am Entomol 37:59

K-Strategists Species with life history characteristics making them well suited for population stability and stable envi ronments (“K” is an expression of carrying capacity of the environment). K-selected species represent an extreme on a continuum of life history characteris tics, with r-selected species at the other end of the continuum. K-selected species can also be said to conform to the “competitive strategy” (Table 1).

Kyasanur Forest Disease This tick-borne virus disease is found in southern Asia.  Ticks

K-Strategists, Table 1 A comparison of the characteristics of r-selected and K-selected species

r-selected

K-selected

Habitat type

Unstable, not permanent

More stable

Reproduction

Rapid under favorable conditions; many offspring produced

Usually slower; fewer offspring produced

Development

Rapid; often multivoltine

Slower; often univoltine

Mortality

Often density independent and catastrophic

Often density dependent and more gradual

Population size

Extremely variable in time

Less variable in time

Dispersal capacity & mode

High and random

Lower and oriented

Brood care

Absent

Sometimes present

Body size

Often quite small

Often larger

Competition

Variable, but often low

Often very keen

Ultimate effect

High productivity

Efficient use of resources

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Labellum The mouth of certain Diptera, consisting of a ridged lip at the end of the proboscis. This term also is used to describe the extension of the labrum covering the base of the rostrum in Coleoptera and Hemiptera, and a lobe at the apex of the glossa in honey bees.  Mouthparts of Hexapods

Labial Glands Glands opening at the base of the labium that secrete saliva to aid digestion. Sometimes they also produce silk.

Labial Palpi Short (one- to four-segmented) sensory appendages on the insect labium.  Mouthparts of Hexapods

Labiduridae A family of earwigs (order Dermaptera). They sometimes are called striped earwigs.  Earwigs

Labium A structure that forms the floor of the mouth. The lower lip (Fig. 1).  Mouthparts of Hexapods

Laboubeniales The Laboubeniomycetes (Ascomycota) contains the order Laboubeniales with the greatest number of ectoparasitic species (more than 1,300). However, in some instances, parasitization by selected numbers of the Laboubeniales may result in pathological symptoms in host insects. These fungi most commonly infect Coleoptera but can be

submentum

palpiger mentum glossa paraglossa palpus

Labiidae A family of earwigs (order Dermaptera). They sometimes are called little earwigs.  Earwigs

Labium, Figure 1 External aspect of the labium in an adult grasshopper, showing some major elements.

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Labrum

found among other insect orders, usually on the adult stage, and also in mites and millipedes. They may attack only one sex of an insect and may even be site-specific, developing only on certain areas of the cuticle. Their association with arthropod hosts is obligate (essential) for completion of a life cycle. The Laboubeniales may appear as hair-like structures on the cuticle surface. Careful examination of these structures reveals a thallus, consisting of a receptacle and its appendages. The thallus, as recently described for Hesperomyces virescens, arises from ascospores that contact and attach to the host (ladybird beetle) cuticle. The receptacle is attached to the host cuticle by a basal cell called the foot. Antheridia (male gametangia) arising from the receptacle produce non-motile spermatia. Trichogynes (the female receptive hyphae) are borne on young perithecia also located on receptacles. There are no known anamorphs so that infection and thallus development on the cuticle must originate from the sexually produced ascospores. In a few cases, haustoria may grow from the foot and penetrate the cuticle and the underlying

hemocoel, as reported for H. virescens, to obtain nutrients. Narrow branches of these invasive haustoria (rhizomycelia) may destroy fat body and muscle, thus causing symptoms of severe disease. Premature death may result or basic functions such as egg production and feeding may be affected.

References Tavares II (1979) The laboubeniales and their arthropod hosts. In: Batra LR (ed) Insect-fungus symbiosis: nutrition, mutualism, and commensalism. Allanheld, Osmum, Montclair, NJ, pp 229–258 Weir A, Beakes GW (1996) Correlative light- and scanning electron microscope studies on the developmental morphology of Hesperomyces virescens. Mycologia 88:677–693

Labrum A structure that forms the roof of the mouth. The upper lip (Fig. 2).  Mouthparts of Hexapods

flagellum vertex

antenna pedicel frons

scape median ocellus

face anterior tentorior pit

basimandibular sclerite frontoclypeal suture

mandible clypeus clypeolabral suture

labrum maxillary palpus

maxilla labial palpus

Labrum, Figure 2 Front view of the head of an adult grasshopper, showing some major elements.

Lace Bugs (Hemiptera: Tingidae)

Lace Bugs (Hemiptera: Tingidae) Laura T. Miller West Virginia Department of Agriculture, Charleston, WV, USA Tingids are commonly called lace bugs because the pronotum and forewings have delicate and intricate reticulations resembling lace. Lace bugs can be confused with the Piesmatidae or ash-gray lace bugs, which also have forewings that are somewhat lace-like or reticulated. However, the lack of ocelli in the Tingidae distinguishes them from the Piesmatidae. All tingids are phytophagous and generally are host specific. Some species can be very destructive to plants, some of economic importance. The Tingidae are distributed worldwide. The family is comprised of approximately 2,000 species placed in three subfamilies. The Cantacaderinae occur mainly in the Southern Hemisphere, the Tinginae are represented throughout the tropical and temperate zones, and the Vianaidinae are a small Neotropical group. The Tinginae comprise the majority of the lace bugs within the family, including some 220 genera out of approximately 250 genera. The higher level classification is:

Dorsally, they look like fancy lace, the pronotum and forewings having a network of multiple cells or areolae (Figs. 3–7). Many species have very wide wings and their head can be concealed or partially obscured under a hood-like projection from the pronotum. Many others have very narrow wings and very small pronotal hoods or no hoods at all. The pronotum can have extremely diverse structures, from low carinae to globose hoods, bump-like projections, and foliaceous overgrowths. Lace bugs have no ocelli. The antennae are four- segmented, with the third antennomere being the longest. The head can possess spine-like, finger-like, or tubercle-like projections, or it can be completely devoid of such projections. The hemelytra, which are the first pair of wings, are translucent or transparent in many species. Some species have brachypterous forms, meaning that the wings are reduced in some degree, sometimes exposing one or two posterior abdominal segments. The rostrum or beak is elongate with four segments. In repose, it rests in a rostral groove, which has margins that are delimited by foliaceous and areolate carinae. Their legs are generally thin and elongate with the tarsi divided to form two tarsomeres.

Order: Hemiptera Suborder: Heteroptera Superfamily: Tingoidea Family: Tingidae Subfamily: Cantacaderinae Subfamily: Tinginae Subfamily: Vianaidinae

Diagnosis Tingids are very small insects, approximately 2–10 mm in length. Their coloration is generally cryptic, ranging from white or yellowish to brown and black. Their general appearance is somewhat flattened dorso-ventrally, and it can vary from quadrate or broadly oval to narrow and slender.

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Lace Bugs (Hemiptera: Tingidae), Figure 3 Corythucha sp. lace bug.

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Lace Bugs (Hemiptera: Tingidae), Figure 4 Calotingis sp. lace bug.

Lace Bugs (Hemiptera: Tingidae), Figure 6 Macrotingis sp. lace bug.

Biology

Lace Bugs (Hemiptera: Tingidae), Figure 5 Phatnoma sp. lace bug.

Most species of lace bugs live on the underside of leaves, but a few can live on the upper and lower parts of stems (Melanorhopala froeschneri Henry and Wheeler, Physatocheila plexa (Say)) or even on the upper parts of roots (Coleopterodes). Species of two Old World genera, Copium and Paracopium are gall-makers on the flowers of their host plants. Adults and nymphs alike feed on the sap of the host plant by piercing the epidermis. Although each tingid species is usually somewhat host specific, lace bugs collectively feed on a diverse array of plants. They complete their whole life cycle on the same host plant species and on the same part of the plant. Most species of lace bugs are gregarious, and some have shown parental care. Tingids generally have one or two generations a year, although some species have multiple generations. Most species of lace bugs over-winter


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Economic importance

Lace Bugs (Hemiptera: Tingidae), Figure 7 Leptoypha sp. lace bug.

as adults, but a few over-winter as eggs (Stephanitis) and some as nymphs (Acalypta). Lace bugs can lay their eggs deeply into the plant tissues or set them on the abaxial surface of a leaf. They are hemimetabolous or, in other words, have incomplete metamorphosis, in which the immature stages (nymphs) are similar to the adult stage, with the exception of smaller size and the absence of fully developed wings and genitalia. Wings appear as small pads in the second or third instar (nymphal stage) and increase in size with each moult. Most species have five instars before reaching the adult stage, although a few species have four instars (for example, Stephanitis rhododendri Horvath). The nymphs’ general appearance can be flat with a great number of needle-like spines covering the dorsal surface, or it can be smooth. In some species, the spines seem to produce secretions that afford protection against predators.

Although not all tingid species are of economic importance, some are serious pests. Lace bugs are capable of causing great damage to their host plants during seasonal outbreaks. The piercing of the plant’s epidermis can cause extensive tissue damage that diminishes photosynthesis. As a result, especially when high numbers of nymphs and adults are present, chlorosis (yellowing of the plant parts) occurs due to chlorophyll reduction, and as a consequence, the plant loses vigor. A good number of tingids are common pests of forest trees, agricultural crops, fruit trees, and ornamentals. Some examples are as follows: Gargaphia tiliae (Walsh), the basswood lace bug, is a common pest of Tilia americana L., a forest and ornamental tree in North America; Corythucha gossypii (Fabricius), the cotton lace bug, is an important pest of beans and cotton from the southern United States to northern South America; C. cydoniae (Fitch), the hawthorn lace bug, attacks many species of wild and ornamental woody rosaceous plants in North America; C. mcelfreshi Drake, the peach lace bug, causes constant defoliation which greatly affects fruit production in some areas of Mexico; C. ciliata (Say), the sycamore lace bug, is a very common lace bug that feeds on Platanus occidentalis L., the common sycamore tree in North America, and on its ornamental hybrid P. x acerifolia Ait., the London plane tree; Stephanitis pyri (Fabricius), a polyphagous pest in Europe and the Middle East, feeds primarily on a variety of trees and shrubs, including rose, elm, oak, poplar, cherry, etc.; Habrochila ghesquierei Schouteden is an important pest of coffee from eastern Africa; and Stephanitis pyrioides (Scott), the azalea lace bug, probably a native of Japan, has become an important pest of ornamental azaleas almost anywhere azaleas are grown. Some species of lace bugs have been considered for the biological control of noxious weeds. The lantana lace bug, Teleonemia scrupulosa Stål, feeds on the invasive weed Lantana spp. Oncochila simplex (Herrich-Schaeffer) is a possible control for leafy spurge (Euphorbia spp.) in the U.S.A. Dictyla

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Lacewings, Antlions and Mantispids (Neuroptera)

echii (Schrank) has been considered for the control of viper’s bugloss, Echium plantagineum L., an invasive weed of pastures.  Bugs (Hemiptera)

References Blatchley WS (1926) Heteroptera or true bugs of eastern North America, with especial references to the faunas of Indiana and Florida. Nature Publishing Co, Indianapolis, IN, 1116 pp Drake CJ, Davis NT (1960) The morphology, phylogeny, and higher classification of the family Tingidae, including the description of a new genus and species of the subfamily Vianaidinae (Hemiptera: Heteroptera). Entomol Am 39 (ns):1–100 Drake CJ, Ruhoff FA (1965) Lacebugs of the world: a catalog (Hemiptera: Tingidae). U.S. National Museum Bulletin 243, 634 pp Schaefer CW, Panizzi AR (2000) Heteroptera of economic importance. CRC Press, Boca Raton, FL, 828 pp Schuh RT, Slater JA (1995) True bugs of the world (Hemiptera: Heteroptera): classification and natural history. Comstock Publishing Associates, A division of Cornell University Press, Ithaca, NY, 336 pp Slater JA, Baranowsky RM (1978) How to know the true bugs (Hemiptera: Heteroptera). Pictured Key Nature Series. Wm. C. Brown Co. Publishers, Dubuque, Iowa, 256 pp

Lacewings, Antlions and Mantispids (Neuroptera) Lionel Stange Florida Department of Consumer and Agricultural Services, Division of Plant Industry, Gainesville, FL, USA This is the largest order of the Neuropterida which also includes snakeflies, alderflies and dobsonflies and contains about 5,000 described species. Until the recent split of the order Neuroptera into three orders, the true Neuroptera were also called Planipennia. Seventeen extant families are recognized which include minute insects with a forewing length of about 2 mm (Coniopterygidae) to very large insects with forewing lengths of 70 mm or more (Myrmeleontidae). Most species

are moderate-sized insects. They are holometabolous insects in which the families have been grouped by the shape of the larval mandibles. They are short and stout in Ithonidae and Polystoechoetidae (which have subterranean larvae), elongate but straight in the Osmylidae, Sisyridae, Nevrorthidae, Dilaridae, Berothidae and Mantispidae, curved without teeth in the Chrysopidae, Nemopteridae and Hemerobiidae and curved with teeth in the Psychopsidae, Nymphidae, Nemopteridae, Ascalaphidae and Myrmeleontidae. The mandibles of the Coniopterygidae appear to be highly modified which contributes to their phylogenetic isolation from other families. The adults are conservative morphologically with chewing mouthparts, five segmented tarsi and two pairs of wings which have dissimilar venation. Venation is usually dense (Fig. 8) and complete but can be very reduced, especially in small species. The larvae are unique in that the mandible is grooved to receive part of the modified maxilla to form a sucking “jaw.” Also, the digestive tube is strange in that the midgut does not empty into the hindgut until the adult emerges from the pupa and deposits a meconium pellet. This is made easier by the fact that food is always taken in liquid form as the larva injects digestive enzymes into the prey to liquefy the tissue. However, they can pass urine. The Malpighian tubules (usually eight in number) are adapted to produce silk which is manipulated by the anal spinneret to construct the silken cocoon. The carnivorous larvae are terrestrial except for the aquatic Sisyridae and some Osmylidae. The Neuroptera were clearly distinct by the Permian, with extant families (Chrysopidae, Coniopterygidae, Nymphidae, Psychopsidae) present in the Triassac Period. Schlüter (1986) recognized an additional 14 families existing in the Mesozoic Era which are now extinct. Although the primitive Neuroptera flourished during the Mesozoic Era, they now appear to be dying out with many families represented by only a few species. Polystoechotidae are now restricted to the Western Hemisphere and are represented by only four species in three genera. The Neurorthidae with about 10 species is


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Lacewings, Antlions and Mantispids (Neuroptera), Figure 8 Some common Neuropterans: top left, brown lacewing (Hemerobiidae); top right, green lacewing (Chrysopidae); second row left, eggs of green lacewings; second row right, larva of green lacewing; third row left, antlion larva (Myrmeleontidae); third row right, mantispid (Mantispidae); bottom left and right, antlion adults (upper photos by Jim Castner, lower photos by Lyle Buss).

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found only in the Old World, the Rapismatidae with 16 species limited to the Oriental Region, the Nymphidae with about 25 species restricted to Australia and New Guinea and the Ithonidae with about 17 species limited to Australia and North America. The Nemopteridae and Osmylidae are now absent from North America but both families are represented in the Florissant shales of Colorado (Miocene). The other 10 families have representatives on all continents but even the most speciose families, Chrysopidae and Myrmeleontidae, have only about 1,700 species each. Coniopterygoidea Coniopterygidae Ithonoidea Ithonidae Rapismatidae Polystoechotidae Osmyloidea Dilaridae Neurorthidae Osmylidae Sisyridae Mantispoidea Berothidae Mantispidae Hemerobioidea Chrysopidae Hemerobiidae Myrmeleontoidea Ascalaphidae Myrmeleontidae Nemopteridae Nymphidae Psychopsidae

The family Coniopterygidae contains the pygmies of the order with the forewing length ranging between 2 and 6 mm and are called dusty wings. Although considered rare for many years because of their size, they often are among the most abundant Neuroptera in many habitats, living on trees and shrubs although the aberrant Brucheiserinae evidently live under stones. The body, wings, and legs often are coated with white or grey wax secreted by hypodermal glands. The antenna has

15–62 segments with the flagellar segments moniliform, often with scale-like hairs in distinct whorls in the males. The wings are held roof-like over the body. The hindwing usually is smaller than the forewing, sometimes greatly reduced, and the venation is highly reduced. There are never more than two basal costal crossveins, the forewing Sc is forked distally and the posterior branch resembles the distal part of R1; radial sector separating from R1 near middle of wing, often forked and the posterior branch sometimes resembling the distal part of medial vein. The tarsus is distinctive in the order although similar to those of the Sialidae in having the fourth segment modified (flattened and bilobed). The abdomen lacks the spiracle on the eighth segment which is apomorphic and distinctive among the Neuroptera. The genera usually are separated by wing venation, whereas examination of the male genitalia usually is required to identify the species. The larvae are active predators, often feeding on mites, but they also feed on other small, soft-bodied insects in their environment. They have a large head but the mouthparts are mostly concealed and consist of a short labial palpus with the apical segment expanded, short, straight and pointed styles. The eyes consist of 4–5 stemmata. There are about 490 described species in about 30 genera in three subfamilies and is the fourth most speciose family in the order. The aberrant Brucheiseridae are found in arid areas of Argentina and Chile and consist only of the genus Brucheiser with several species. These apparently are flightless insects with highly sclerotized, reticulate wing venation. Their biology is unknown. The Aleuropteryginae is mostly cosmopolitan although the genera are not. They possess peculiar and unique structures on the abdomen called plicaturae. These are paired organs which are strongly folded and placed on an oblong, somewhat membranous area. Their function is unknown. Also, the wing venation differs from the other subfamilies in having two radio-medial crossveins in the middle of the wing. The larvae have the mouthparts projecting from beneath the labrum and the antenna is about as long as the


labial palpus. There are about 14 genera classified in three tribes. The most common are Aleuropteryx (Holarctic), Neoconis (Neotropics) and Spiloconis (Australia). The Coniopteryginae have two speciose, cosmopolitan genera, Coniopteryx Curtis and Semidalis Enderlein (except Australia). The members of this subfamily lack plicaturae and have only one radio-medial crossvein. Often the males have scale-like setae on the antennae and a few species have a hook on the frons. This subfamily is the most commonly collected and of great biological control interest since many species live on economic crops such as citrus. The vast majority of coniopterygids fly at dawn or dusk, fluttering slowly between plants where they lay eggs. Many species are specific to certain types of plants like junipers. The family Ithonidae is similar in appearance to the Rapismatidae but are whitish to brownish in coloration and commonly live in arid regions. They hold their wings relatively flat over the back which is unusual in the order and resemble dull hepialid moths both in appearance and in flight, which has led to the common name “moth lacewings” for this family. The forewing ranges from about 15 to 30 mm. Three monotypic genera occur in the southwestern United States (Oliarces Banks), in Mexico (Narodona Navás) and in Honduras (Adamsiana Penny). Elsewhere, they are found only in Australia (about 24 species in Ithone Newman, Megalithone Riek and Varnia Walker). Ngymata (slightly domed, bare areas on the wing) are found in this family and are of unknown function; similar structures are found in other families of Neuroptera, as well as Trichoptera, Megaloptera and Mecoptera. Claims have been made that the subterranean larvae are predacious on Scarabaeidae grubs but this has not been clearly established. Some species of ithonids (Ithone, Megalithone and Oliarces) have been observed swarming in vast numbers for short periods of time. In most cases, the swarming sites have been detected first by the presence of many frenzied birds which have a feast when these fat, hapless insects are swarming. The adults can run fairly quickly and lay their eggs in the sand by means of a “sand plough.”

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The family Polystoechotidae is another family of robust sized insects and superficially similar to the Ithonidae and Rapismatidae. The forewing ranges from 15 to 40 mm. There are only four species known in three genera. The genus Polystoechotes Burmeister has one species in Chile and another in North America. The genus Platystoechotes Carpenter is limited to the Sierra Nevada of California and Oregon where it may be associated with Libocedrus (incense cedar). The third genus, Fontecilla Navás, lives in arid zones in central Chile. Little is known of the biology of this family although the larva has been described. They are subterranean but claims that they feed on plant roots are unsubstantiated. Polystoechotes punctatus (F.) was once commonly distributed through the northern half of the United States. The reason why this species is now restricted to the southwestern United States south to Central America is unknown. Apparently this species is attracted to smoke and all the species are attracted to light. The family Rapismatidae is found in the Oriental region. These large, sturdy lacewings with complex venation are usually greenish to yellowish in coloration and live in mountainous areas. The forewing ranges from about 20 to 36 mm. There are about 20 species, all in the genus Raspisma McLachlan. These insects are relatively rare in collections and little is known about their biology. The family Osmylidae is a relatively large family of lacewings with about 170 species in about 20 genera. The classification is suspect with eight subfamilies recognized based on simplistic wing venational characters. They are found on most continents except North America. The species are moderate sized insects (forewing 15–30 mm long). Nearly all the species have three ocelli and usually two wing nygmata (sometimes faint) which helps define the family. Also, there is a small stylus at the end of gonapophyses laterales of the female. Most of the species have semi-aquatic larvae which have the jaws elongate and straight or slightly curved. The larvae have long legs and lack gills. The Porisminae is composed of one very brightly colored species from southeastern Australia. Apparently the larvae live under bark of

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Eucalyptus. The adults are distinguished by having numerous subcostal crossveins. The Kempyninae contains some of the largest species and is found in southern temperate South America, New Zealand and Australia. The Spilosmylinae is the largest and most diverse group found only in the Old World. Many species have an embossed forewing spot on the posterior margin. Spilosmylus has 35 species known from New Guinea. The Stenosmylinae is another disjunct group with species in South America and Australia. The Osmylinae is a Palaearctic subfamily with one well known species in Western Europe. The Protosmylinae (Oriental region), Eidoporisminae (one species from Australia) and the enigmatic Gumillinae (two anomalous species with long antennae from Mexico but are probably Mexican Chrysopidae) complete the survey of this family. The family Dilaridae consists of small delicate lacewings (forewing length 4–15 mm) and are easily distinguished in the male by the plumose antenna and in the female by the well developed ovipositor. The known larvae are elongate and live in burrows in wood, probably feeding on beetle larvae. There are 67 described species in two subfamilies which are nearly exclusive geographically. The Dilarinae are found only in the Old World (except Australia), and the Nallachiinae are found only in the New World except for recently discovered species in South Africa and India. The family Sisyridae is a small family with about 30 species in four genera. Sisyra Burmeister is cosmopolitan and the large genus Climacia McLachlan is found only in the Western Hemisphere. Two other genera exist but are of doubtful validity and with few species in the Old World. These are small insects (forewing length 4–10 mm). The female has the terminalia elongated into an ovipositor like structure. The wings have relatively few crossveins and there are small thickenings (trichosors) on the posterior margin of the distal half of the wings. They are most easily confused with the Hemerobiidae. The larvae are aquatic and feed on freshwater sponges and probably Bryozoa. The larval jaws are the longest in the order, apparently

adapted for sucking out the contents of sponges. They are called Spongilla-flies for this reason. They are the only truly aquatic insects in the order with the larvae bearing external gills in the second and third instars. The larvae leave the water to pupate, usually constructing a distinctive double cocoon with a mesh-like covering. The adults are predacious on insect eggs and small insects. The family Neurorthidae used to be included in the Sisyridae until the terrestrial larvae were discovered and found to be greatly different morphologically. This small family of delicate lacewings (forewing length 6–10 mm) consists of only 10 species found in Europe and North Africa (Neurorthus), Asia (Nipponeurothus) and Australia (Austroneurothus). There is some data suggesting that this family is not closely related to other families of the order. The family Berothidae, or beaded lacewings, is another family (about 110 species) of small (forewing length 6–15 mm), delicate lacewings occurring on all continents (except Antarctica). Many species have falcate wings and some species have scale-like setae on the wings and sometimes on the body (Lomamyia Banks). There are trichosors present on the wing margins. The family is difficult to define and usually keys out at the end of the family key on venational characters. There are four distinct subfamilies. The Rhachiberothinae are found only in southern Africa and have the forelegs raptorial. There are two genera. The Cyrenoberothinae contains one monotypic genus from Chile (Cyrenoberotha Adams and MacLeod) and one monotypic genus from southern Africa (Manselliberotha Aspöck and Aspöck). Nothing is known of their biology. The adults have the face elongated below the eyes. The Nosybinae contains but one genus, Nosybus Navás, known only from Africa. The wings are rounded and have small venational differences from the Berothinae. The Berothinae is the largest subfamily with about 24 genera in all continents. The life cycle of the North American genus, Lomamyia Banks, has been described. The larvae live in termite burrows. In one species the first instar waves its abdomen at a termite releasing an


“allomone” which paralyzes the termite in a few minutes. Later instars can produce enough gas to immobilize up to six termites per shot. The family Mantispidae, containing about 350 described species, are easily recognized by having raptorial forelegs and thus can be confused only with the subfamily Rhachiberothinae of the Berothidae in the Neuroptera. The larvae are hypermetamorphic, being very active triungulins in the first instar, and becoming inactive scarabaeiform larvae in subsequent instars. Adults of the same species can vary greatly in size since most species are parasitic on spiders. The forewing can vary between 5 and 30 mm. The pronotum is sometimes many times longer than wide and, in contrast to the snakeflies, the legs originate near the anterior margin. There are four subfamilies. The Drepanicinae is found in Chile and Australia and contains the largest species of the family, Drepanicus gayi, from Chile which is green and somewhat leaf-like. The genera Ditaxis McLachlan and Theristria Gerstaecker are found only in Australia; the latter is the most diverse mantispid genus in Australia. The biology of this subfamily is unknown. The Calomantispinae is a small subfamily with only two genera, Nolima Navás (North America) and Calomantispa Banks (Australia). The larvae of Nolima may be generalist predators. The Symphrasinae is a New World subfamily containing three genera, Anchieta Navás, Plega Navás, and Trichoscelia Westwood. The latter genus has been reared out of larval cells of Polybia (Vespidae). The larvae of Plega appear to be generalist predators with prey records including the pupae of Noctuidae and Scarabaeidae and the cells of a leaf-cutting bee (Megachile). Many of the species of Anchieta resemble bees. This subfamily has a well developed ovipositor and possess other characters which isolate it especially from the largest subfamily, Mantispinae. All of the Mantispidae are “parasites” of spider egg sacs. The triungulins either board the female spider until she makes her egg sac or directly searches for the egg sac without phoretic behavior. This varies between species. Some species of Mantispinae resemble vespoid

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wasps such as Cimaciella Enderlein in North America and Euclimacia Enderlein in the Oriental region. These mantispids show considerable variation in color pattern throughout their ranges probably in relation to the variation of the wasp models. Adults are active predators and usually are found in trees and shrubs. They are attracted to light. The genus Mantispa Illiger was once thought to be widespread but apparently is paraphyletic and absent in the New World and Australia. The present number of genera is about 30 but some other genera appear to be undescribed (Fig. 8). The Chrysopidae is probably the largest family of the Neuroptera with more than 1,300 described species in 75 genera and three extant subfamilies. Although called green lacewings, there are many species which are brownish in coloration, especially species that rest on rocks during the day. Also, the greenish color of museum specimens often fades in a few years. The adults lack microtrichia on the wing membrane found in most families of Neuroptera. Nearly all the species possess a tympanal organ on the ventral base of the radial vein. One function of this auditory organ is to detect bat echo-locating sounds, that once identified, will signal the adults to fold their wings and drop to the ground. This family contains the most significant biological control agents in the order, and species of Chrysoperla Steinmann are sold worldwide for biological control. The larvae are active predators living on plants and feed on diverse, soft-bodied insects, especially aphids. The most plesiomorphic subfamily appears to be the Nothochrysinae with about 20 species in seven genera found in Australia (Dictyochrysa EsbenPetersen, Triplochrysa Kimmins), Europe (Hypochrysa Hagen, Nothochrysa McLachlan), Africa (Kimochrysa Tjeder, Pamochrysa Tjeder), and North America (Nothochrysa McLachlan, Pimachrysa Adams). These are mostly robust and moderate sized insects, often dark brown in color and lack the tympanal organ. They seem to live in forests of ancient trees (such as Gymnosperms). The Apochrysopinae contain the giants of the family (forewing length 18–34 mm) and represent a small

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group with about 25 species in 12 genera. Like the Nothochrysopinae, the genera are limited in distribution such as to Australia (two genera), South America (four genera), Africa (two genera) and Asia (four genera). They appear to prefer the dark areas of dense forests. The Chrysopinae are by far the largest subfamily with more than a 1,000 species in nearly 70 genera. Many genera are now cosmopolitan partly because species of Chrysopa Leach, Ceraeochrysa Adams, and Chrysoperla Steinmann have been released and established in diverse regions of the world. The adults of some of these genera (i.e., Chrysoperla) feed on honeydew and employ extracellular symbiotic yeasts to aid in digestion. Many genera (i.e., Ceraeochrysa, Leucochrysa McLachlan) have trash bearing larvae. Special species communication occurs in the family. Some adults (i.e., Chrysoperla) move the abdomen rapidly, transmitting by way of the legs to the substrate a vibration (tremulation), and in the genus Meleoma Fitch stridulation is accomplished by moving the hind femur against abdominal sternites. The larvae have long, strong, curved mandibles (no teeth) similar to those of the Hemerobiidae and can be distinguished by the presence of the trumpet like empodium between the tarsal claws. Nearly all species lay their eggs on stalks, either separate stalks or stalks stuck together at the base, which may help to keep emerging larvae from eating each other. The Hemerobiidae consists of about 500 species in 28 genera and 10 subfamilies. Nearly all species are yellow to dark brown in color but there are a few green species. The species can be distinguished from those of other families by the presence of at least two apparent radial sectors except for the monotypic genus Adelphohemerobius Oswald from Chile. The family appears most closely related to the Chrysopidae but differs notably from that family in possessing microtrichia on the wing membrane. Many species are relatively small (forewing length 4–10 mm) but a few species attain 18 mm in wing length. The biology of the family seems similar among the different genera and are similar to those of the Chrysopidae. Larvae of Hemerobiidae lack the trumpet-shaped

empodium in instars 2 and 3 but have similar shaped “jaws” which are curved and without teeth. This family is important in biological control with most of the larvae being active predators on mostly soft bodied insects and mites on plants. Several genera are cosmopolitan or very widespread (i.e., Hemerobius L, Micromus Rambur, Notiobiella Banks, Sympherobius Banks, Wesmaelius Krüger) whereas most are restricted to one biogeographical realm (eight genera restricted to South America; five genera to Australia). This family demonstrates an unusual amount of wing reduction with flightless species of Micromus in Hawaii and of Conchopterella on the Juan Fernandez Islands. Psectra diptera Burmeister has forms with only one pair of functional wings. The Psychopsidae, or “silky lacewings” contains 26 species in five genera and two subfamilies. The Zygophlebiinae is restricted to southern Africa and contains three genera (Silveira Navás, Cabralis Navás and Zygophlebius Navás). Balmes Navás (Oriental region) and Psychopsis Handlirsch (Australian) belong to the Psychopsinae. These are moderately large lacewings with broad wings and dense venation (forewing length 10–35 mm). Biology and larval stages are poorly known. Cabralis gloriosus Navás is a mostly white species which flutters around in fairly dense and spiny vegetation. Silveira contains four relatively small species living mostly in arid zones. The Nymphidae are found only in Australia and New Guinea. There are about 25 species in eight genera. The Myiodactylinae contain very broad winged lacewings which lack tibial spurs whereas the Nymphinae contains more narrow winged lacewings with short tibial spurs; Nymphes myrmeleonoides Leach resembles some antlions and owlflies in overall appearance but have filamentous antennae. The larvae have strongly curved mandibles, usually with one tooth. There are two types of larvae known. Those of the Myiodactylinae (Myiodactylus Brauer; Osmylops Banks) are strongly flattened and presumably relatively immobile as in most Ascalaphidae. The larvae of Nymphes are more antlion-like, being narrower and searching for prey among litter and vegetation.


The Myrmeleontidae currently have the most described species (about 1,700) in the order with 188 extant genera, 15 tribes and three subfamilies. They are found on all continents but are most abundant in xeric areas since the larvae live in sand or loose soil. The adults are small to large (forewing 10–75 mm) with characteristic wing venation with an elongate cell under the stigma, and the male of many groups has a special gland at the base of the forewing (“pilula axillaris”). Antlions are closely related to the Ascalaphidae but lack the elongate, clubbed antennae of that family The larvae are distinguished from other Neuroptera larvae in having the hind tarsal claws much larger than those of the other legs which is an adaptation for burrowing. Studies have shown that the larvae have preferred habitats and some live under the protection of rock overhangs or in tree holes or animal burrows, but the majority live in open sand. Some prefer coarser sand than others, and members of the tribe Myrmeleontini construct pitfall traps, whereas most others do not. Exceptions occur in the Brachynemurini (i.e., Scotoleon pallidus), Nesoleontini (Cueta Navás) and Myrmecaelurini (Isoleon Esben-Petersen; Myrmecaelurus Costa); these larvae construct a double structured pitfall trap (funnel shaped pitfall below which is a tubular extension) in hard pan soils. Members of Callistoleon Banks (Myrmeleontini) have side furrows to the pitfall trap. There are three extant subfamilies. Palparinae contains the giants of the family with the fore wing length reaching 75 mm. All live in the Old World (except Australia) except for a small group (Dimarini) in South America. One member of the Dimarini, Millerleon pretiosus Banks, has larvae that live in extreme desert conditions and can survive in the larval stage for more than 5 years and can exist many months without feeding. The palparine larvae have enlarged setae distally called fossoria which enable the bulky larvae to dig more efficiently. They have been observed to capture ground resting grasshoppers. The Stilbopteryginae is a small subfamily of large antlions with short, knobbed antennae (similar to Albardia of the Ascalaphidae) restricted

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to Australia (two genera). The Myrmeleontinae contains more than 90% of the genera and species in about eight tribes. The Nemoleontini is the largest tribe, found on all continents, and most genera have similar biologies. However, a few genera (i.e., Navasoleon Banks) have larvae that live on bare rock surfaces. These larvae can remain motionless for weeks. Species of Gatzara of the tribe Dendroleontini, also live on bare rock surface and cover themselves with green lichens for camouflage. Most known larvae of the Dendroleontini have a debris carrying bunch of setae on the metascutum which apparently lures prey. All larvae of the tribe Myrmeleontini and a few genera of the tribe Acanthaclisini move only backwards. Perhaps the most striking species of antlion, Pseudimares iris Kimmins of the monospecific tribe Pseudimarini is large, with a large eyespot on the hindwing and has been collected only twice from southern Iran. All the larvae and nearly all the adults are predacious on other insects. A few adults apparently feed on pollen. Most adults are nocturnal but there are a few day-flying species, such as the butterflylike species of Pamexis Hagen from South Africa and Maracandula Currie from Mexico. The owlflies, or Ascalaphidae, contain mostly fast flying insects that resemble dragonflies. Adults are moderate to large in size (forewing length 15–60 mm), robust and usually very pilose with huge compound eyes which suggested the common name. There are about 500 species in about 80 genera and three subfamilies on all continents (except Antarctica). They are mostly crepuscular aerial predators and sometimes swarm in flight. Nearly all species have elongate antennae which are clubbed somewhat like butterflies except for the monotypic subfamily Albardiinae with short antennae that exists in Brazil. The Ascalaphinae is the largest group and is unique in having the eyes divided by a transverse sulcus. This subfamily contains the day-flying and colorful Libelloides Schäffer of Europe. The females of the most common New World genus of this subfamily, Ululodes Hagen, lay sterile eggs (repagula) coated with ant repellent material at least on the basal side of a string of eggs for protection. The third

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Lachesillidae

subfamily, Haplogleniinae, is worldwide. The males of some species of this subfamily (i.e., Haploglenius) have an apparent startle display in which a hinged flap covering the pronotum is suddenly lifted to expose a contrasting cream or white patch. The taxonomy of this family is difficult and the only worldwide treatment is by Van der Weele (1908), but much general information is found in Tjeder (1992). The Nemopteridae are among the most distinctive looking of the Neuroptera with the hindwings often extremely narrowed. The larvae have strongly curved mandibles but lack teeth. The Crocinae have the hindwing threadlike whereas the Nemopterinae have the hindwing broadened distally. The head is often greatly prolonged ventrally similar to the Mecoptera and is a modification for feeding in flowers. The family is found in most continents except in North America. Most species are nocturnal but some are diurnal and very colorful, such as in the genus Nemoptera Latreille found in Europe. The Crocinae are mostly nocturnal with species usually very limited in distribution and are often in xeric areas. They flutter around at night and are attracted to white flowers. The crocine larva often has the prothorax greatly lengthened and are among the only Neuroptera to live peacefully together in groups of 30 or more, often in sand and small rocks under rock overhangs. These alert larvae have been seen to escape predators (and a shovel) en masse like a herd. The larvae of Nemopterinae appear more diverse and usually burrow into the sand head first in contrast to the antlions. Some genera (i.e., Stenorrhachus McLachlan) have larvae that live relatively deep under the sand and lack ocelli. In that genus, the females are wingless. Palmipenna Tjeder contains day-flying species in which the hindwing is greatly broadened, evidently reducing attacks by robber flies.

References Brooks SJ, Barnard PC (1990) The green lacewings of the world: a generic review (Neuroptera: Chrysopidae). Bulletin of the British Museum of Natural History (Entomology) 59:117–286

Meinander M (1972) A revision of the family Coniopterygidae (Planipennia). Acta Zoologica Fennica 136:1–357 New TR (1989) Planipennia/lacewings. In: Handbuch der zoologie 4. Gruyter, Berlin, Germany, pp 1–129 Oswald JD (1993) Phylogeny, taxonomy and biogeography of extant silky lacewings (Insecta: Neuroptera: Psychopsidae). Mem Am Entomol Soc 40:1–65 Tjeder B (1992) The ascalaphidae of the afrotropical region (Neuroptera). Entomol Scand (Suppl) 41:3–169 Van der Weele HW (1908) Ascalaphiden. Collections zoologiques du baron edm. De Selys Longchamps. Catalogue systematique et Descriptif. Fascicle:1–326

Lachesillidae A family of psocids (order Psocoptera).  Bark-Lice, Book-Lice and Psocids

Lacinia (pl., laciniae) The inner lobe of the maxilla. It is modified in various ways, and in some flies it forms a flat, blade-like structure for piercing.  Mouthparts of Hexapods

Lackey Moths Some members of the family Lasiocampidae (order Lepidoptera).  Lappet Moths  Butterflies and Moths

Lacquers and Dyes From Insects Charles MacVean Universidad del Valle de Guatemala, Guatemala City, Guatemala The use of wild organisms as sources of decorative and protective substances has ancient origins, with recorded instances dating as far back as 6,000 years ago in the use of indigo dyes from plants (Indigofera tinctoria, Leguminosae) in

Lacquers and Dyes From Insects

China, or pre-Columbian use of scale-insect lacquer (Llaveia axin, Margarodidae) in the Mayan civilization of Mesoamerica. While this article deals primarily with insects, it is important to note that natural lacquers, dyes and various types of varnishes have been obtained from a broad range of organisms. Molluscs, for instance, are the ancient source of royal purple dye (from whelks, Murex brandaris, Muricidae) and the indelible sepia-brown ink obtained from cephalopods (octopuses, squid, etc.) in the genus Sepia. This substance is so durable that extracts from fossil cuttlefish have yielded perfectly viable ink. Plants are the most diverse source of dyes, and also provide raw material for the famous lacquer art of the Orient, which uses sap from a relative of sumac trees (Toxicodendron verniciflua, Anacardiaceae). In the insect world, only a few species, concentrated in the superfamily Coccoidea (Hemiptera) or scale insects, historically have been the source of pigments and artistic and protective finishes. This does not include the use of butterfly wings as decorative materials, or metallic flies, wasps and beetles as ornaments (either dead or as living jewels tethered to a lapel!). Such decorative value stems from structural characteristics in the wing scales or the cuticle which cause various reflection patterns of light, distinct from internal chemical pigments used for dyes. This article deals primarily with pigments and finishes derived from insects, but other sources are mentioned insofar as they are used together, or for the sake of comparing key characteristics. Basic physical and chemical characteristics of dyes and lacquers are discussed in order to provide working definitions and basic concepts.

Some Basic Terminology of Dyes and Finishes The terms dye and pigment are often used interchangeably, though traditionally dyes were considered of plant origin while pigments were derived

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from minerals, earths and ground rocks. Usually, a dye is made up of pigments in solution (often in water) which binds to a substrate, such as cloth or leather, in such a way that the color change in the substrate is permanent and difficult to remove. The chemistry of dyeing is still not completely known, though the presence and arrangement of double bonds, C=C, C=O, C=N, and N=N in the dye molecules are important in the production of color. For example, the pigment in cochineal insects, carminic acid, results from the condensation of three benzene rings and contains several such double bonds. To improve the fastness of the dye, substances called mordants are added to the dye and are known to form chemical bridges between the substrate and the pigment, which remain stable after the solvent has evaporated. Salts of various metals are common mordants. Varnishes and lacquers are also terms used without clear distinctions for liquids or pastes which dry to form durable, protective and decorative semitransparent films when applied to various substrates. A useful distinction is that varnishes produce the desired finish with as little as a single coat, while lacquers are the result of many, sometimes hundreds, of thin coats applied over time to produce the final finish. The process by which the substance converts from a paste or liquid to a dry film also varies, and can include simple evaporation of a solvent, the chemical linking of repeating units into polymers or a combination of the two. Both varnish and plant-derived lacquer consist of resins mixed with essential oils (volatile and fragrant), but varnishes are artificial mixtures while lacquer comes from naturally existing combinations. Resins are substances found as natural polymers, usually dissolved in ethanol for application, and include the sap of Toxicodendron verniciflua used for oriental lacquer, shellac from Indian lac insects (Kerria lacca, Kerriidae) as well as many other plant products like water-absorbing gums. Waxes and drying oils are a final group of substances used in producing lacquer finishes, resulting from the presence of reactive double bonds which take up oxygen when exposed to air, and

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which form extensive polymers linked through the oxygen atoms between the original chains of fatty acids. Linseed oil is a well-known drying oil, which produces a simple but not highly durable finish on furniture, for example.

Production and Use of Insect Dyes and Lacquers Probably the best known colorant from insects is cochineal dye (Figs. 9 and 10), obtained from the body contents of cochineal scales, Dactylopius coccus (Dactylopiidae) which yields a bright red color used in textiles, food, drugs, etc. Pre-Columbian Maya and Aztec cultures used the dye for wood, feathers, cloth and as writing ink for codices. The vermilion pigment is concentrated in the female fat body and is thought to repel ants and parasites. Like all scale insects, cochineal exhibits dramatic sexual dimorphism, with wingless females developing through several nymphal instars on the prickly-pear cactus host plants (Opuntia spp.). CH3

O

OH

C6H11O5

HO

OH

HOOC

OH

O

Lacquers and Dyes From Insects, Figure 9 Structure of carminic acid, an anthraquinone dye obtained from cochineal insects (Dactylopius coccus). CH3

(CH2)4

CH

CH

CH

They are readily recognized on Opuntia by the stringy white wax masses they produce. The males, which are indistinguishable from females in the early instars, form pseudopupae and emerge as two-winged adults resembling small flies. The adult females are brushed off the cactus pads, dried and then stored, traded or processed to obtain pure dye. The crimson color is obtained by “reconstituting” the dry bodies (known as “grana” in Spanish) in boiling water to extract the pigment, then precipitating, filtering and drying to a powder. Cultivated from Mexico to Peru by indigenous cultures since before the Spanish conquest, these insects are generally considered native to Mexico and Central America. However, some evidence suggests that they originated in South America and were then traded northward. The cochineal insects found in Mexico and Central America show a long history of domestication and dependence on human protection, along with propagation of the host plants, while production of dye in Peru by ancient Quechua Indians was based on wild Dactylopius. Cochineal first became a product for export to Spain and other parts of Europe in the sixteenth century (Table 1). Initially, this new dye was rejected by the traditional textile industry which used a different insect, Mediterraneangrown Kermes spp., as a source of dye. But the intense red quality and relative cost advantages of cochineal soon served to expand its market, rendering it an extremely important product in the Spanish colonial economy of the eighteenth and nineteenth centuries. This was particularly so for Central America, which did not enjoy the great wealth of precious metals found in South America or Mexico but was richly endowed in biological resources. The other great agricultural export of CH

CH

(CH2)7

CO2H

CH

CH

(CH2)7

CO2H

O O CH3

(CH2)4

CH

CH

CH

Lacquers and Dyes From Insects, Figure 10 Formation of a lacquer polymer by uptake of oxygen at double-bond sites, crosslinking individual fatty acid chains through a peroxide bridge.


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Lacquers and Dyes From Insects, Table 1 Characteristics of some natural dyes and lacquers from insects, plants and molluscs Common/ scientific name Cochineal insect (Dactylopius coccus; Hemiptera: Coccoidea: Dactylopiidae)

Product obtained Bright red dye from dried bodies of adult females

Kermes insect (Kermes illcis and K. vermillo; Hemiptera: Coccoidea: Kermesidae)

Bright red dye, carmine, from dried bodies of adult females

Indigo plant (Indigofera tinctoria, I. suffruticosa, I. guatimalensis, I. thibaudiana; Fabaceae)

Blue indigo dye from leaves and stems, obtained by fermentation, then drying to a powder; oxidation in contact with air produces indigotin, the blue color.

Mediterranean (Murex brandaris), Central American and Mexican (Purpura patula) mollusc or whelk (Muricidae)

Purple dye from mucous glands, the original “royal” or Tyrian purple of Greek, Roman and Phoenician societies

Lac insect (Kerria lacca, Hemiptera: Coccoidea: Kerriidae)

Chemical nature

Sites and history of production Pre-Columbian Central Applied in solution (often America, major export to water) to impart permaEurope between sixteenth nent color by binding to cloth, leather, wood, etc. To and nineteenth centuries, renewed value today as become fast, most dyes require the use of a chemical natural dyestuff which binds the due to the substrate, called a mordant. Tannins from insect-induced oak galls are a mordant used since antiquity. Salts of several metals, since as tin, aluminum, iron and chromium, are also well known mordants Mediterranean region, the medieval standard red due since 1700 b.c., displaced by cochineal beginning in the sixteenth century Originally from India, I. tinctoria was traded widely as of 450 b.c. I. suffruticosa and others in genus became a major export from colonial Central America; displaced by cochineal in nineteenth century

Costly to produce, “royal purple” was traded in the Mediterranean and associated with high rank and wealth; pre-Columbian use for dying cotton fibers on both coasts of Central America and Mexico Known from India since at Natural shellac Resin flakes commonly secreted as a dissolved in ethanol. Resins least 250 a.d. Non-toxic protective shell by are naturally occurring ter- finish used widely on pene polymers often in female scales, wood furniture and floors, mixtures with essential oils, in pharmaceuticals as a harvested in flakes from a wide variety of insoluble in water, contrast coating for pills, applied as with varnishes which are host plants. a stiffener for hats, as a man-made mixtures of glossy coating for candy resins and boiled oils and fruits, as glue for boding glass and metal, and many other uses

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Lacquers and Dyes From Insects, Table 1 Characteristics of some natural dyes and lacquers from insects, plants and molluscs (Continued) Common/ scientific name

Product obtained

Chemical nature

Sites and history of production

Niij (Guatemala) or Aje (Mexico) insect (Llaveia axin; Hemiptera: Coccoidea: Margarodidae)

Lacquer used on gourds, wood, ceramic, leather, from the fat body of the adult females, harvested prior to egg production; used also as skin ointment

The fat, which resembles a soft wax, is a mixture of triacylglycerols and free fatty acids; when rubbed onto the substrate, with various pigments. It polymerizes into a durable and decorative film

Cultivated and traded in pre-Columbian Mexico and Central America; now produced only in Uruapan, Mexico and Rabinal, Guatemala, but offers potential as a natural finish for new markets

Lacquer or “varnish” tree Japanese and Chinese Natural resin; urushiol is the main component, together (Toxicodendron vernici- lacquer from a milky fluum; Anacardiaceae) tree sap with a gum and glycoprotein, which undergo oxidative polimerization; hundreds of coats are often applied to achieve the finished lacquer

the Central American colonies was indigo dye, which had been the mainstay of the local economy during the 17th and 18th centuries. Cochineal production surpassed indigo in the 1800s, but then the advent of synthetic aniline dyes around 1860 caused the virtual demise of both products. Interestingly, this decline indirectly stimulated the development of the budding coffee industry in Guatemala and other countries. Currently, the demand for non-toxic red dyes has created new markets for cochineal. Peru is now the world’s main producer, and Mexico and Central America are also returning to an ancient ethnoentomological crop. With regard to insects used for lacquer, two species are of particular interest: lac insects, Kerria lacca (Kerriidae), of Asian origin, and the giant margarodid scale insects, Llaveia axin (Margarodidae), native to Mexico and Central America, where they are commonly known as “aje” and “niij,” respectively (Table 1). While most scale insects are only a few millimeters in size, adult niij females reach a

Developed in China before the Christian era; perfected by the Japanese during Ming Dynasty (1368–1644 a.d.). Lacquerware was at one time restricted to high classes and production was regulated by the state. Currently produced as fine finish and art form.

total body length of 2.5 cm and can weigh over 0.5 g (Figs. 11 and 12). The substances produced by these insects and used for lacquer are entirely different, as shellac from K. lacca is an external body secretion which encloses the female insect and her eggs in a resinous mass, whereas niij wax is the internal body fat of the adult females. However, both yield a fine, smooth and durable finish for woodwork, ceramic, metal and many other substrates (Fig. 13). The production of lac insects is an ancient tradition in India, and consists of harvesting the amber-colored resin secretion and eliminating insect and plant remains from the crude “sticklac” to yield clean flakes of shellac. The host plants of lac insects span a wide range of families, including Anacardiaceae, Dipterocarpaceae, Euphorbiaceae, Leguminosae, Moraceae and several others. The purification process is rather complex, and includes dissolving the raw resin or sticklac in a base, such as sodium hydroxide, and bleaching with sodium hypochlorite. Dilute acid is used to precipitate the


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Lacquers and Dyes From Insects, Figure 11 Sexual dimorphism of scale insects, shown here in niij insects (Llaveia axin). Adult females are sac-like and wingless, while males possess a single pair of wings and resemble small flies.

Lacquers and Dyes From Insects, Figure 12 Raw body fat from an adult niij female, normally used for egg production; extracted by artisans to yield a fine lacquering substance.

resin in curds like cottage cheese; these are then dried to form dry flakes which can be stored or dissolved in ethanol for use in finishing wood, etc (Figs. 11–13).

Niij insects, on the other hand, are one of the least known sources of artistic and protective lacquer. Adult females are harvested from the host plants (primarily Jatropha spp., Euphorbiaceae;

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Lacquers and Dyes From Insects, Figure 13 Traditional black lacquer on rattles and piggy banks made from gourds and finished with niij wax combined with fine soot, then etched to reveal natural pale gourd color.

Spondias spp., Anacardiaceae; and Acacia spp., Leguminosae), boiled and then mashed through fine cloth to produce a crude aqueous extract. The product used for lacquering is the body fat, which is found as a thick liquid in the living females and accounts for about 30% of total body weight. After prolonged beating of the extract, fat globules separate from the other components and coalesce into bright yellow globs of a soft, paste-like material. These are washed thoroughly with water, shaped into patties or cylinders roughly 0.5 kg in weight and are then ready to use or store. The soft fat, with physical properties similar to cocoa butter, can be rubbed onto a substrate alone or in combination with powdered pigments to produce a permanent film. Traditional uses in Guatemala combine black (fine powdered soot) with red (paste from the seeds of anatto, Bixa orellana, Bixaceae) on the surface of gourds. Etching into the finished surface to reveal the pale gourd color then produces many intricate patterns and figures. The fat alone provides a durable, satiny finish on pottery, ceramic, leather and metal and is resistant to abrasion, water and heat. In the Uruapan

art of Mexico, various figures are scraped out from the initial lacquer layers on wooden plates or furniture and filled in with a different color to produce highly complex inlays. Niij fat is solid at ambient temperature which makes it similar to many waxes. Chemically, the fatty acid chains that make up its main tryacylglycerol components contain many reactive double bonds. In contact with air, oxygen is taken up at these sites and forms links to neighboring chains, thus forming a polymer film. In this sense, niij “wax” shares the properties of drying oils, such as linseed oil, with which it can be mixed to extend and dilute the insect fat. Chía oil is another plantderived lacquering substance used in the Mexican community of Olinalá in combination with various pigments, but without the use of insect products. Like cochineal, niij insects show an old history of domestication and human protection, which has probably influenced the geographic distribution of the species. Cultivation practices for niij insects involve storing the cottony egg masses in covered gourds during the dry season, which protects them against severe egg predation by

La Crosse Encephalitis

c occinellid beetles. With the beginning of the rainy season, newly hatched insects are set out at the base of the host plants to initiate a new generation which feed in dense aggregations (Fig. 14) on the host plants. Traditionally, insect rearing takes place on fence rows rather than dedicated plots of agricultural land. However, the high value of niij “wax” relative to other agricultural products that share its arid tropical habitat provides an opportunity for a novel type of agroforestry production. Like cochineal, niij lacquer has suffered a decline in production (although it was never as important in economic terms), but offers great promise as a decorative and protective finish to substitute synthetic and often toxic industrial products.

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In conclusion, synthetic products have isplaced many of the original uses of natural d substances, but the current emphasis on non-toxic finishes and dyes, and the premiums often associated with natural products, are providing opportunities to rediscover and improve the production of insect and plant-based compounds. Not only are these of interest for their particular protective or esthetic qualities, but they can also contribute to biodiversity conservation through agroforestry productions systems in native habitats.

References Heil C (1995) The pre-Columbian lacquer of West Mexico. Neara J 30:32–39 (includes descriptions of oriental lacquer as well) Hogue CL (1993) Latin American insects and entomology. University of California Press, Berkeley, CA, 536 pp Jenkins KD (1970) The fat-yielding coccid, Llaveia, a monophlebine of the Margarodidae. Pan-Pac Entomol 46:79–81 Kosztarab M (1987) Everything unique or unusual about scale insects (Homptera: Coccoidea). Bull Entomol Soc Am 33:215–220 Simpson BB, Conner Ogorzaly M (2001) Economic botany, plants in our world, 3rd edn. McGraw-Hill, New York, NY, 529 pp

La Crosse Encephalitis Jorge R. Rey University of Florida, Vero Beach, FL, USA

Lacquers and Dyes From Insects, Figure 14 Dense population of adult niij females on Jatropha curcas host tree. The insects are harvested prior to oviposition in order to extract the body fat.

La Crosse encephalitis is a relatively rare viral disease that is spread by infected mosquitoes. The disease affects the central nervous system and can be serious and even lethal in rare instances. It is named for the city of La Crosse, Wisconsin, where it was first identified in 1963. Since then, La Crosse encephalitis has been identified in several Midwestern and Mid-Atlantic states. On average, 73 cases per year are reported to the Centers for Disease Control (CDC), with the majority being from children under 16 years of age. It is

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La Crosse Encephalitis

suspected that La Crosse encephalitis has a higher incidence and wider distribution in the eastern United States, but is not reported because the virus is often not identified, and because symptoms are often mild and medical attention is not sought. The La Crosse encephalitis organism is an arbovirus (arthropod borne virus) of the family Bunyaviridae. It is normally cycled between the treehole mosquito Ochlerotatus triseriatus and vertebrate hosts (chipmunks and squirrels) in forest habitats throughout the range of the disease. O. triseriatus is a daytime biting mosquito that normally inhabits tree holes, but can also develop in other water-holding containers such as discarded tires, cans, etc. Recently, eggs of the Asian tiger mosquito, Aedes albopictus, infected with the La Crosse encephalitis virus have been collected in North Carolina and Tennessee. The virus can be maintained during the winter by transmission in mosquito eggs. An infected female lays eggs that carry the virus and eventually develop into infected adults. This process, where the virus is passed

from mother to offspring, is called transovarial transmission.

The Virus Transmission Cycle In a normal cycle, the virus is transmitted to the vertebrate host through the bite of an infected mosquito (Fig. 15). In the host, the virus replicates and increases in abundance rapidly (a process known as amplification). When sufficiently abundant, the virus can then be passed on to other mosquitoes when they feed on the infected vertebrate host. Infected chipmunks and squirrels do not show signs or symptoms of disease. Although not part of the normal cycle of the disease, humans can also contract the disease by the bite of an infected mosquito. However, humans are “dead end hosts,” meaning that an infected human cannot transmit the virus to uninfected mosquitoes because sufficient amplification of the virus does not occur in humans.

La Crosse Encephalitis, Figure 15 Transmission cycle of La Crosse encephalitis.

Lac Scales

Additionally, the virus is not transmitted from human to human.

Symptomology and Treatment As the name implies, the disease can cause inflammation of the brain which interferes with brain and spinal cord functions. Initial symptoms of La Crosse encephalitis infection include fever, headache, nausea, vomiting and lethargy. More severe symptoms usually occur in children under 16 and include seizures, coma, paralysis and neurological after effects. The death rate for clinical cases of La Crosse encephalitis is about 1%. Many pediatric cases that present La Crosse encephalitis symptoms are screened for herpes or other viral diseases, but are not specifically tested for presence of the La Crosse encephalitis virus. Many of these cases are reported as “aseptic meningitis” or “unknown viral encephalitis”. Diagnosis of the disease is confirmed by the presence of clinical symptoms and a fourfold rise in serum antibody and specific immunoglobulin M antibody capture in cerebral-spinal fluid (CSF) or serum; and/or by isolation of the virus or detection of the viral antigen in blood, CSF, or brain tissue. Serological test for the virus may be negative early in the course of the infection. New diagnostic techniques such as enzyme-linked immunosorbent assay (ELISA) may now be used soon after infection (they do not require a fourfold increase in titer). The use of monoclonal antibodies has also helped to standardize the testing protocols and have increased our ability to quickly identify viral agents. Viral agents can now also be rapidly identified by polymerase chain reaction techniques, but use of these is still not widespread in clinical settings. There is no specific treatment for La Crosse encephalitis. No anti-viral drugs are available at this time, and antibiotics are not effective against viruses. Patients with the disease are given supportive treatment for the symptoms, particularly headaches, fever and seizures.

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Preventing Infection Risk of contracting La Crosse encephalitis is highest in children younger than 16 years, in people residing in or near woodlands that harbor the treehole mosquito, in people who maintain water-holding containers in their residences, and in those involved in outdoor activities where O. triseriatus is present. Prevention of the disease involves protection against the bite of infected mosquitoes. Personal measures include the use of repellents containing DEET, and the use of protective clothing (long sleeved shirts and long pants) when exposed to mosquitoes. Effective local mosquito control measures can also decrease disease risk by lowering mosquito populations, and thus decreasing the probability of mosquito-human encounters, and possibly, the transmission of the disease among wild populations of mosquitoes and vertebrate hosts. Mosquito control includes the use of appropriate pesticides and cleanup of water-holding containers that may offer breeding sites for O. triseriatus. Some mosquito control agencies also fill tree holes where O. triseriatus may develop with sand or cement.

References McJunkin JE, Khan RR, Tsai TF (1998) California La Crosse encephalitis. Infect Dis Clin North Am 12:83–98 McJunkin JE, de los Reyes EC, Irazuzta JE, Caceres MJ, Khan RR, Minnich LL, Fu KD, Lovett GD, Tsai T, Thompson A (2001) La Crosse encephalitis in children. New Engl J Med 344:801–807 Rust RS, Thompson WH, Matthews CG, Beaty BJ, Chun RW (1999) La Crosse and other forms of California encephalitis. J Child Neurol 14:1–14

Lac Scales Members of the family Kerriidae, superfamily Coccoidae (order Hemiptera).  Scale Insects and Mealybugs  Lacquers and Dyes From Insects  Costs and Benefits Of Insects  Shellac

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Lacturidae

Lacturidae A family of moths (order Lepidoptera). They commonly are known as tropical burnet moths.  Tropical Burnet Moths  Butterflies and Moths

Ladybird Beetles (Coccinellidae: Coleoptera) J. H. Frank1, R. F. Mizell III2 1 University of Florida, Gainesville, FL, USA 2 University of Florida, Quincy, FL, USA “Ladybird” is a name that has been used in England for more than 600 years for the European beetle Coccinella septempunctata L. As knowledge about insects increased, the name ladybird became extended to all its relatives, members of the beetle family Coccinellidae. Of course these insects are not birds, but butterflies are not flies, nor are dragonflies, stoneflies, mayflies, and fireflies, which all are true common names in folklore, not invented names. The lady for whom they were named was “the Virgin Mary,” and common names in other European languages have the same association (the German name Marienkafer translates to “Marybeetle” or ladybeetle). Prose and poetry mention ladybird, perhaps the most familiar in English being the children’s rhyme: “Ladybird, ladybird, fly away home, Your house is on fire, your children all gone…” In the U.S.A., the name ladybird was popularly Americanized to ladybug, although these insects are beetles (Coleoptera), not bugs (Hemiptera). Then, the Entomological Society of America decreed that the official name in the USA should be “ladybird beetle.” Elsewhere in English-speaking countries it is still ladybird. Now the word ladybird applies to a whole family of beetles, Coccinellidae or ladybirds, not just

Coccinella septempunctata. There are many species of ladybirds (almost 6,000 now known worldwide). The number of bird species known worldwide is somewhat more than 9,000. Regrettably, newspaper writers are prone to writing about “the ladybird” and erroneously referring to species of ladybirds as “varieties,” although few or none of them would write about “the bird” and consider that bird species (from auks through eagles to hummingbirds), are “varieties.” Many ladybird species are considered beneficial to humans because they eat phytophagous insects (“pests of plants,” often called “plant pests”), but not all eat pests of plants, and a few are themselves pests.

Classification Coccinellidae are a family of beetles belonging to the superfamily Cucujoidea, which in turn belongs to the series Cucujiformia within the suborder Polyphaga of the beetles (Coleoptera). Their relatives within the Cucujoidea are the Endomychidae (handsome fungus beetles) and Corylophidae (minute fungus beetles). The classification of lady beetles is: Order Coleoptera Suborder Polyphaga Series Cucujiformia Superfamily Cucujoidea Family Coccinellidae

The internal classification of the family into tribes and subfamilies is not settled because there are competing systems, none of them clearly correct. In this article, mention of species is grouped according to the food of adults and larvae, an ecological rather than phylogenetic grouping. When subfamilies and tribes are mentioned, it must be understood that these classifications are not universally accepted. More than 480 species are currently reported to occur in America north of Mexico, just 44 in the British Isles, and 600 in Australia. Most of the

Ladybird Beetles (Coccinellidae: Coleoptera)

480+ in America north of Mexico are considered to be native, and others to be adventive (having arrived from somewhere else and established feral populations). Among the adventive species, some were introduced (introduced deliberately), and others are immigrants (having arrived by any means except deliberate introduction).

Description Ladybird adults are oval, range in length from about 1 mm to over 10 mm depending upon species, and have wings. Females on average are larger than males. Adults of some species are brightly colored. Their mandibles are used for chewing. Adult ladybirds are able to reflex-bleed from the tibio-femoral articulations (leg joints). The blood (hemolymph) is repellent by having a repulsive smell as well as containing (in some species) various alkaloid toxins (adaline, coccinelline, exochomine, hippodamine, etc.). The hemolymph is yellow and its repellency and toxicity are believed to be a defense mechanism against predators. Some people have claimed that the bright (red on black, or black on red) colors of some adult ladybirds are aposematic, which is to say that the colors warn would-be predators that the beetles are distasteful or toxic. The immature stages (eggs, larvae, and pupae) also contain the toxins that their adults have. Toxins are said to be produced by dorsal glands in the larvae. Eggs are elongate-ovoidal, and in just a few species are protected by secretions of the adult female. Cannibalism of eggs, larvae and pupae is common, especially when prey is scarce. Larvae are mobile, and in some species (for example of Scymnus and Cryptolaemus) are protected by waxy secretions. Pupae are unprotected by a cocoon (some other beetles pupate in a cocoon) but larvae may wander some distance from feeding sites (where they may be at risk from cannibalism) before pupating.

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Life Cycle and Behavior Ladybird eggs are laid in clusters by at least most aphid-eating species and singly by at least most scale-insect-eating species. Eggs produce larvae that undergo four instars before pupating, metamorphosing, and giving rise to adults. One scale-eating ladybird is reported to have only three instars. Ladybirds may have one or, more typical of warmer climates, several generations each year, and reproduction is slowed or halted by cooler winter weather, when adults may hibernate. In hot, dry climates, ladybirds may aestivate (become inactive) during the hottest months. Ladybirds that feed on aphids develop faster, age faster, move faster, typically are larger, and lay their eggs in clusters. Those that feed on scale insects develop more slowly, live longer, move more slowly, typically are smaller, and lay their eggs singly.

Food Pest Species – Feeding on Plants Adults and larvae of the subfamily Epilachninae feed on plants. Some 500 species are known worldwide. In America north of Mexico, this subfamily is represented only by Epilachna borealis (Fabricius) and E. varivestis Mulsant. Epilachna borealis, the squash beetle, feeds on members of the squash family (Cucurbitaceae). Epilachna varivestis, the Mexican bean beetle, feeds on members of the bean family (Leguminosae). Mexican bean beetle is native to southern Mexico, but it is an immigrant to the USA, first detected in the west in 1849. Now, its distribution is from Costa Rica north through Mexico to the Rocky Mountain states of the USA, and with a separated eastern population which extends southward to northern Florida. In the eastern USA, it has been controlled efficiently by annual releases of the parasitoid wasp Pediobius foveolatus (Crawford) (Eulophidae). This wasp was initially imported from India, where

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it attacks Henosepilachna sparsa (Herbst), which likewise belongs to Epilachninae. Epilachna philippinensis Dieke, a pest of solanaceous crop plants in the Philippines, has been the object of a biological control program by Pediobius epilachnae (Rohwer), native to parts of the Philippines.

Innocuous Species – Feeding on Mildews Ladybirds of the tribe Halyziini (until recently called Psylloborini, of the subfamily Coccinellinae) feed on fungal growths (mildews, Ascomycetes: Erysiphales) on the leaves of plants. Their greatest species diversity is in the tropics, with only six species in America north of Mexico. One of them is the West Indian Psyllobora nana Mulsant which has invaded the extreme south of Florida. In the neotropics, the coccinellid genus Neocalvia feeds on larvae of Halyziini.

Predatory Species – Feeding on Mites Adults and larvae of the tribe Stethorini (of the subfamily Scymninae) feed on tetranychid mites. The tribe is distributed worldwide, and has only one genus. There are five species in America north of Mexico. An example is Stethorus utilis (Horn), a minute ladybird which is distributed in the coastal plains of the southeastern states from North Carolina south through Florida and west through Texas. Another is S. punctillum Weise, a European species that was reported in 1950 as detected in Ontario and Massachusetts.

Predatory Species – Feeding on Whiteflies Four species in America north of Mexico appear to be more-or-less specialized predators of whiteflies. They are Delphastus catalinae (Horn), D. pallidus (LeConte), and D. pusillus (LeConte) (tribe Serangiini), and Nephaspis oculatus (Blatchley) (tribe

Scymnini). The first and probably the fourth seem to be immigrant species from the Neotropical region. The others (D. pallidus and D. pusillus) are considered to be native. After D. pusillus was found to be a very useful biological control agent against sweetpotato whitefly (Bemisia tabaci (Gennadius)) including the “form” that later was named silverleaf whitefly (Bemisia argentifolii Bellows and Perring), “it” was exported from Florida to California and made available commercially and used in other parts of the USA. Somehow this resulted in commercial biological control companies selling D. catalinae under the name D. pusillus.

Predatory Species – Feeding on Cottonycushion Scale Cottonycushion scale (Icerya purchasi Maskell), native to Australia, belongs to the family Margarodidae (commonly called “ground pearls,” although this name hardly fits this species) in the superfamily Coccoidea (scale insects). It is a major pest of citrus, and an important pest of several other trees and shrubs including Acacia, Casuarina, and Pittosporum. After its arrival in California, presumably as a contaminant of imported plants, it threatened to ruin California’s citrus industry in the late 1800s. It was controlled by importation, release, and establishment (as classical biological control agents) of Rodolia cardinalis (Mulsant) and a parasitoid fly, Cryptochetum iceryae (Williston). When cottonycushion scale became a problem in many other countries, R. cardinalis was the biological control agent of choice, so stock of it has been shipped to other continents and countries.

Predatory Species – Feeding on Mealybugs Mealybugs are the homopterous family Pseudococcidae, which includes some notable pests of plants. Cryptolaemus montrouzieri Mulsant, a ladybird native to Australia, is a notable predator of


mealybugs. It was introduced into California first in 1891, and some time later from California into Florida. It has been marketed commercially as a control agent for mealybugs and is often effective, but has one unfortunate characteristic: its larvae produce waxy filaments making them look to the uninitiated like their mealybug prey. Many owners of plants have sprayed the larvae with chemicals in the mistaken belief that they are pests. This misidentification must be overcome by education. Cryptolaemus montrouzieri does not confine its attentions to mealybugs, and also eats soft scales (Coccidae) and armored scales (Diaspididae). Such a catholic diet is normal for a long list of ladybirds, so that their diet cannot neatly be pigeonholed as armored scales or soft scales or mealybugs – they may eat some prey in all of these families, and a few of the larger ones may even eat an aphid from time to time. For that reason, many genera and species are placed below under “Feeding on Scale Insects.”

Predatory Species – Feeding on Armored Scale Insects Some species appear to feed largely or entirely on armored scale insects (Diaspididae). Examples include Microweisea coccidivora (Ashmead), M. misella (LeConte), and M. ovalis (LeConte) of the tribe Microweiseini, Zilus horni Gordon, Z. eleutherae Casey, and Z. subtropicus (Casey) of the tribe Scymnillini, and Cryptognatha nodiceps Marshall of the tribe Cryptognathini. One of these, Cryptognatha nodiceps, is not native to America north of Mexico, having been imported in the 1930s, released, and established as a classical biological control agent for coconut scale (Aspidiotus destructor Signoret).

Predatory Species – Feeding on Scale Insects A large trophic group has scale insects as its prey, meaning members of the superfamily Coccoidea

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(the scale insects). This superfamily includes various related families, notably Coccidae (soft scales), Diaspididae (armored scales), Pseudococcidae (mealybugs), Dactylopiidae (cochineal scales), Kermesidae (gall-like scales), Eriococcidae (felt scales), Cerococcidae (ornate pit scales), and Asterolecaniidae (pit scales). Examples of ladybird genera belonging to this group are: Decadomius, Diomus, Nephus, and Scymnus (all in tribe Scymnini), Brachiacantha, Hyperaspidius, and Hyperaspis (all in tribe Hyperaspini), Axion, Chilocorus, Curinus, and Exochomus (all in tribe Chilocorini), Rhyzobius (tribe Coccidulini), and Azya (tribe Azyini). It is not yet clear how, or whether, they divide up the scale insects between them, because reliable prey records are too incomplete. However, there is at least some level of prey specialization in these (and the three aforementioned groups) that feed on scale insects, which seems not to be the case for the next-discussed trophic group (those that feed on aphids). Brachiacantha has a curious life history in that its larvae so far as is known feed on scale insects within ant nests. Rhyzobius lophanthae (Blaisdell) was introduced to California from Australia in 1892 to control scale insects, and somehow later made its way to Florida (there is no record of an early introduction into Florida). Chilocorus circumdatus (Schoenherr) [other writers give the author name as Gyllenhal] is native to southeastern Asia and is adventive in Australia; it was imported from Australia to the U.S.A. and was released in Florida in 1996 against citrus snow scale, Unaspis citri, and is established. Azya orbigera Mulsant is an immigrant from the Neotropical region. Decadomius bahamicus (Casey) is an immigrant from the Caribbean or the Bahamas or Bermuda. Diomus roseicollis Mulsant is an immigrant from Cuba.

Predatory Species – Feeding on Aphids Adults and larvae of many species (the tribe Coccinellini) probably feed primarily on aphids. Amomg many others, they include Coccinella

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novemnotata Herbst, C. septempunctata L., Coelophora inaequalis (F.), Coleomegilla maculata DeGeer, Cycloneda munda (Say), Cycloneda sanguinea (L.), Harmonia axyridis Pallas, Harmonia dimidiata (Fabricius), Hippodamia convergens Guérin-Méneville, Mulsantina picta (Randall), Naemia seriata (Melsheimer), Neoharmonia venusta (Melsheimer). Although Olla v-nigrum Casey feeds on some aphid species, it has been shown to be an important predator of psyllids (Figs. 16 and 17). Four of these, C. septempunctata (from Europe), C. inaequalis (from Australia), H. dimidiata (from China), and H. axyridis (from Japan) were introduced into North America, although there is some doubt that the presence of C. septempunctata and H. axyridis is due to introduction; their presence may be due to immigration, albeit as hitchhikers aboard ships. Two of these genera, Coleomegilla and Mulsantina, include adelgids (Adelgidae), which are closely related to aphids, in their diet. Further, Coleomegilla also includes pollen whereas Mulsantina also includes scale insects in the broad sense.

Alternative Food Ladybird larvae and adults may supplement their normal prey in times of scarcity with other types of food. They consume flower nectar, water and honeydew – the sugary excretion of piercingsucking insects such as aphids and whiteflies – or pollen. Many plant species also contain organelles in locations on the plant other than the flower – termed extrafloral nectaries – that produce a nutrient-laden secretion. While it was first thought that extrafloral nectaries were used by the plant for excretion, it is well substantiated that most plants actually use the extrafloral nectaries to attract predators and parasites for protection from their herbivores. Over 2,000 species of plants in 64 families have extrafloral nectaries. Extrafloral nectaries may be located on leaf laminae, petioles,

rachids, bracts, stipules, pedicels, fruit, etc. Ladybirds often use the secretions from extrafloral nectaries in their diet and are just some of the many beneficial insects that use extrafloral nectary secretions.

Natural Enemies All insects have predators, parasites/parasitoids, and/or pathogens. Ladybirds are not exempt. Larvae of Epilachna borealis and E. varivestis are attacked by a North American tachinid fly (Aplomyiopsis epilachnae (Aldrich)) which specializes in the genus Epilachna. Larvae of E. varivestis also are attacked by an introduced eulophid wasp (Pediobius foveolatus, see above). Another native tachinid fly, Hyalmyodes triangulifer (Loew), is less specialized, attacking larvae not only of Epilachna varivestis, but also of Coleomegilla maculata, several weevils, and a pterophorid moth. Perhaps the best known of the parasitoids of ladybirds is the braconid wasp Perilitus coccinellae (Schrank). It attacks adult ladybirds and to a lesser extent larvae and pupae of Coccinella septempunctata, Coleomegilla maculata, and several other species. Microsporidial diseases include Nosema hippodamiae Lipa and Steinhaus, N. tracheophila Cali and Briggs, and N. coccinellae Lipa (Fig. 18).

Use of Ladybirds in Biological Control Most species of ladybirds are considered beneficial because they are predators of Hemiptera: Sternorrhyncha or Acarina, many of which are considered to be pests. These predatory ladybirds contribute to the regulation of populations of their prey, and in some situations contribute a high level of regulation. When ladybirds naturally contribute a high level of control of pests, or in combination with other predators and/or parasitoids and diseases contribute a high level of population regulation of pests, people may benefit. That is to


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Ladybird Beetles (Coccinellidae: Coleoptera), Figure 16 Ladybird beetles: Olla v-nigrum eggs (a), larva (b), prepupa (c, left) and pupa (c, right), and adult (d). This species is dimorphic in the adult stage and also occurs as an orange beetle with small black spots. Vedalia beetle, Rodolia cardinalis: adult (e) and larva (f) feeding on cottony cushion scale. This beetle saved the California citrus industry from destruction by cottony cushion scale.

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Ladybird Beetles (Coccinellidae: Coleoptera), Figure 17 Larvae and adults of some ladybird beetles: Azya orbigera larva (a) and adult (b). This species is typical of those that produce waxy secretions in the larval stage. The multicolored Asian ladybird beetle, Harmonia axyridis, larva (c) and adult (d). This species, though predatory, has become a serious nuisance due to its habit of aggregating in buildings during the winter. Mexican bean beetle, Epilachna varivestis, larva (e) and adult (f). This species is one of only a small number of phytophagous ladybird beetle species.


Ladybird Beetles (Coccinellidae: Coleoptera), Figure 18 Some typical adult ladybird beetles: Curinus coeruleus (a), Coleophora inaequalis (b), Coccinella septempunctata (c), Hippodamia convergens (d), and Cryptolaemus montrouzieri (e).

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say that gardeners, growers and farmers may benefit, at no cost, because they have no or negligible pest problems. Sometimes, gardeners mistake the ladybird larvae for pests and spray chemical pesticides that kill them (this is much less of a problem with growers and farmers because they have more experience). The result is increased problems from real pests. The answer is a constant educational effort to inform people about ladybirds and what their larvae look like. This effort cannot end, because people knowing nothing about ladybird life cycles are born each minute. One type of biological control is thus called manipulative biological control (of which a subset is conservation biological control). The objectives are simply to capitalize on the ladybirds (or other beneficial organisms) that already are present, to make conditions as favorable as possible for them (manipulation), and especially to avoid spraying chemicals (insecticides, fungicides, or herbicides) that will harm them (conservation). A second type of biological control is augmentative biological control. This begins with the recognition that ladybirds in a given pest situation are present but too few to do the job required, and buying more from a commercial producer to release to augment those already present. A risk is that if adult ladybirds are released, many of them may fly away. But, if ladybird larvae are released, they have the option of eating the pest with which they are presented, or starving – they cannot fly away. Obviously, this requires matching the pest to a purchased ladybird species that will eat that pest (see above for species options). The rub here is that the number of purchased ladybirds needed for a given pest situation may not have been worked out in detail – it demands a huge amount of practical experience to tie down the details for at least hundreds of situations. Documentation of this experience is progressing very slowly. A third type of biological control is classical or inoculative biological control. Here, some individuals of a ladybird (or other) species that is not already present are released in the hope that they

will establish a population and eventually control the pest that is of concern. Classical biological control typically applies to a situation in which a new pest has invaded, and researchers (from a university, or a national or state department of agriculture) import and release a ladybird (or other kind of organism) that is believed to control the pest elsewhere. Typically, the imported ladybird (or other organism) becomes established or does not become established; if it becomes established, it may or may not control the pest in this new situation. Typically, the foregoing things are done under the name of “research,” and either are cost-free to gardeners, growers and farmers (especially if done by state or federal departments of agriculture) or, if done by university researchers, then gardeners, growers and farmers are asked to contribute toward a grant that will pay for the cost of importation and research on the biological control agent (but subsequently, after it has become established, there are no further costs). The archetypical example is control of cottonycushion scale of citrus by the introduced ladybird Rodolia cardinalis. Although chemical pesticides of the time were failing to control it, and although it threatened to ruin California’s citrus industry, nobody was willing to invest funds in biological control research. Nevertheless, biological control research was “bootlegged” onto other operations by dedicated researchers, was astoundingly successful, and saved California’s (and later Florida’s) citrus industry from ruin: there was no subsequent need to use chemicals against this pest, thus saving billions of dollars as against a trivial expenditure (about $1,500 at the time, for foreign travel). Glasshouses (greenhouses) provide a habitat for plants and pests and biological control agents that differs from outdoor habitats. Typically, culture begins with initiation of a crop of plants that has no pests (or seems to have none). But then pests somehow show up, and there are no ladybirds (or other organisms) to control them. The situation is very much like that of classical biological control, and ladybirds (and/or other beneficial organisms) released into the greenhouses may


control the pests and eliminate need to use chemical pesticides. Here, the question is not about funding new research into a new pest, but into buying the right numbers of ladybirds (or other organisms) of the appropriate species to control a pest that has already been researched. For many such situations, ladybirds (or other organisms) can be purchased from commercial supply houses to control the pest(s).

Commercial Availability The following is a partial species list of commercially available ladybirds posted on the California Department of Food and Agriculture’s website, which can be accessed to provide information about commercial suppliers in Canada, Mexico and the USA in 1997 (it is not up-to-date). The URL (http://www.cdpr.ca.gov/docs/ipminov/ bensuppl.htm) still works. Coleomegilla maculata – a predator of aphids. Cryptolaemus montrouzieri – a predator of mealybugs. Delphastus pusillus – a predator of whiteflies. Harmonia axyridis – a predator of aphids. Hippodamia convergens – a predator of aphids. Some suppliers do not rear the beetles but collect overwintering adults from the mountains of eastern California; these overwintering adult beetles (i) may be heavily parasitized and many may die, and (ii) may be programmed at the end of the winter to end the hibernation by flying west, which may do you no good if they all take to flight and leave your property. Rhyzobius lophanthae – a predator of scale insects. Rhyzobius ventralis – this name is listed in error, it should be called Rhyzobius forestieri (Mulsant). Stethorus picipes – a predator of tetranychid mites; this name is listed in error, it should be called Stethorus punctum picipes Casey, a subspecies of Stethorus punctum (LeConte).

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Stethorus punctillum – a predator of tetranychid mites. Commercial suppliers of biocontrol agents in Australia are listed by the Association of Beneficial Arthropod Manufacturers (ABA: http://www.gc. goodbugs.org.au), and some of these suppliers sell ladybirds. Commercial suppliers of biocontrol agents in Europe (and some other countries around the world) are listed by the International Biocontrol Manufacturers Association (IBMA: http://www. ibma.ch), and some of the listed companies sell ladybirds. Commercial suppliers belonging to the Association of Natural Biocontrol Producers, a North American Organization, are listed (ANBP http://www.anbp.org). By examining the individual sites of these companies, you may determine what ladybird species are available and, from the websites of some of these companies, some of the characteristics of the species available. There is yet no website listing insect cultures available worldwide for purchase, with a list of suppliers for each species. Insect Production Services, Natural Resources Canada, is beginning to compile such a list (http://www.insect. gflc.cfs.nrcan.gc.ca). However, just because a biocontrol agent such as a ladybird species (or subspecies), is available somewhere in the world for purchase, does not necessarily mean you will be able to obtain it. Your own national (and perhaps provincial or state) department of agriculture (or some other government agency) may regulate importations. It is most probable that you will only be able to import species (and subspecies) that already exist in your area. For example, all shipments of living insects into Florida are required to have permits from the Florida Department of Agriculture and Consumer Services, Division of Plant Industry; in general, a permit will be supplied for importation of species (and subspecies) that already occur in Florida. It is the vendors who are required to obtain the permits for commercial shipments. Furthermore, no reputable producer is likely to ship living ladybirds to you unless there is a rapid commercial shipper. Stated policies of some international shippers

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(e.g., Federal Express, DHL, UPS) say that they will not accept consignments of living animals (including insects) for reasons that they do not explain. The lesson is that you should buy from a local supplier wherever possible. Despite all the difficulties in purchase and shipment, some biocontrol producers can provide you with a good product rapidly. Please see the website of the Belgian producer Biobest (http:// www.Biobest.be), which also has websites in other countries (at least Canada, France, Greece, and Spain) as an example of how it can work. That company provides you an online description of the product and what it can do. Four ladybird species (Coleomegilla maculata, Cryptolaemus montrouzieri, Harmonia axyridis, and Hippodamia convergens) have been reared on purely artificial diets, thus promising to reduce labor costs and thus the price of commercially available ladybirds. Diets for others may now be available or under development.

The Downside of Ladybirds The great success of the imported Rodolia cardinalis in controlling cottonycushion scale in California and then in various countries around the world led to great enthusiasm among growers to attempt importation of additional ladybirds to control a long list of pests of plants. Many of these additional ladybirds failed to establish where they were introduced. Others became established but did not provide the required level of control. Relatively few achieved the required level of control. One of the reasons for success of R. cardinalis was its high level of specialization to cottonycushion scale – it would control that pest effectively, but no others. Growers of many crops encounter pest aphids. Ladybirds that prey on aphids are widely distributed, and native ladybirds are often recruited to aphid infestations on crop plants in North America and elsewhere. Perhaps it was a sense of lack of effectiveness of native ladybirds in rapid and

c omplete control of aphid infestations that led to attempts to import additional aphid-feeding ladybird species into North America. At all events, considerable effort was made by USDA entomologists (in collaboration with state and university entomologists) to import the Eurasian Coccinella septempunctata and the Asian Harmonia axyridis to eat more aphids than were consumed by native ladybirds. Whether those efforts succeeded or whether those two ladybird species arrived as immigrants is unclear, but eventually both species became established and spread widely. They proved to be more successful than native ladybirds at controlling aphids in general, and their populations grew and spread. Perhaps if this had happened in the 19th century the success would have been welcomed. But, by the late twentieth century, it was their side-effects that received publicity – there is some evidence that in some places native ladybird populations have declined because of the efficiency of the introduced ladybirds in killing aphids and thus denying food to the native ladybirds. It is undeniable that adult H. axyridis may hibernate in some places (loosely constructed houses, railway electrical boxes, etc.) where they are not welcome. It matters little that houses and railway electrical boxes should and could have simple physical screens to exclude insects (building codes in the southern U.S.A. require screening of houses against mosquitoes) because the public has become incensed against H. axyridis. The era of importation of generalist biological control agents has ended (even, for example, those that feed on many aphid species but no other prey may no longer be welcome), and only specialists may in future be permitted.

References Dixon AFG (2000) Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, New York, NY Gordon RD (1985) The Coccinellidae (Coleoptera) of America north of Mexico. J New York Entomol Soc 93:352–599

Lagenidium giganteum

Hodek I, Honĕk A (1996) Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, The Netherlands, 464 pp Kuznetsov VN (1997) Lady beetles of the Russian Far East. Center for Systematic Entomology, Gainesville, FL (Memoir No. 1) Vandenberg NJ (2000) Coccinellidae Latreille 1807. In: Arnett RH, Thomas MC, Skelley PE, Frank JH (eds) American beetles, vol 2. CRC Press, Boca Raton, FL, pp 371–389

Laemobothriidae A family of chewing lice (order Phthiraptera). They sometimes are called hawk lice.  Chewing and Sucking Lice

Laemophloeidae A family of beetles (order Coleoptera). They commonly are known as lined flat bark beetles.  Beetles

Lagenidium giganteum Lagenidium giganteum (Lagenidiales) is the bestknown entomopathogen belonging to the class Oomycetes. It has been described as a facultative parasite; it infects and kills available insect hosts, but also is capable of surviving saprophytically. Lagenidium giganteum most often infects young mosquito larvae; only occasionally does it infect older larvae and pupae. In addition, infection also has been reported to occur in certain species of gnats and biting midges. The infective propagules are asexually produced biflagellate zoospores that migrate upward and concentrate at the surface of the water to contact surface-breathing mosquito larvae. Once contact is made, the zoospores recognize and attach to the insect cuticle. Zoospores may attach over the entire larval surface or may concentrate in the head region (e.g., in the buccal cavity). After encystment and attachment, the zoospores (cysts) form delicate germ tubes that

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penetrate the cuticle. Mechanical and enzymatic disruption of the cuticle and underlying tissues produced by apical growth of the fungal germ tube promotes the penetration of L. giganteum into host larvae. Successful infection by L. giganteum is host-specific in terms of the ability of a particular strain of the fungus to bypass the defensive reactions exhibited by challenged host larvae. Mycelia eventually fill the body cavity, and this extensive vegetative growth results in the starvation of the insect. At this time, septation of the mycelia occurs, and the resulting segments may become asexual sporangia or male and female gametangia. Zoosporogenesis takes place in the asexual sporangia. In L. giganteum, the sporangia produce exit tubes that pass through the host cuticle and form bubblelike vesicles. The sporangial protoplast moves through an exit tube into a vesicle; the protoplast then divides into individual zoospores, which are released into the water when the vesicle ruptures. The free-swimming, wall-less zoospores, which do not represent a resistant or resting stage of the fungus, must contact host larvae within several hours in order to initiate another infection cycle. The male and female gametangia (i.e., antheridia and oogonia, respectively) may form from segments of the same mycelium or from segments of contiguous mycelia. The antheridium forms a fertilization tube that attaches to the oogonium, and the contents of the antheridium move into the oogonium. Plasmogamy (fusion of the sex cells) and karyogamy (fusion of the nuclei) occur in the oogonia, and the zygotes resulting from these fusion events form into thick-walled oospores. Oospores represent the dormant, resting spore stage of L. giganteum, and their existence insures survival of the fungus during environmental extremes (drought, cold temperatures). Under proper conditions, oospores germinate, and the fungus may then grow saprophytically, or the germinating oospores may act as zoosporangia, releasing infective zoospores. Lagenidium giganteum is a sterol auxotroph that requires exogenous sterols for both zoosporogenesis and oosporogenesis, but not for

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Lag Phase

vegetative growth. Oospores of L. giganteum are resistant to environmental extremes and can be stored indefinitely at room temperature. In vitro, oospores may be produced in yeast extract-basal media supplemented sterols, unsaturated fatty acids; calcium, and magnesium. Sterols such as cholesterol also regulate the cellular uptake of unsaturated fatty acids. Unsaturated fatty acids increase bilayer fluidity when they become incorporated into plasma membranes and, as in the case of sterols, may affect adenylate cyclase activity by changing membrane fluidity. In addition, there is an increase in oospore viability if the unsaturated fatty acids are added as triacylglycerols, which can function as storage products in dormant cells such as oospores. Calcium is required during all stages of oospore formation from induction to spore maturation. At antheridial induction, calcium interacts with the regulatory cyclic nucleotides, and it may be involved in membrane phase transitions during gametangial fusion.

Lag Phase A phase in the typical growth cycle of a population when there is no growth, typically between the introduction of an organism and the period of exponential growth.

Lamarck, Jean-Baptiste Jean-Baptiste Pierre Antoine de Monet, Chevalier de Lamarck, was born near the village of Bazentinle-Petit on August 1, 1744. After study at a Jesuit seminary, military service, and work as a bank clerk, he began to study medicine and botany. He earned great recognition for his book “Flore Française,” published in 1778. During the French Revolution he called for a reorganization of the Jardin du Roi, where he worked, and when it was implemented he was appointed a professor of the natural history of insects and worms, a subject about

which he knew nothing. This was a period when few naturalists considered invertebrates worthy of study. In fact, the word “invertebrates” did not exist at the time, so Lamarck coined it to describe his responsibilities! Lamarck published a series of books on invertebrate zoology and paleontology. Publication of “Histoire naturelle des animaux sans vertèbres” in 1815 and 1822 greatly advanced the classification of invertebrates. However, his work never became popular, and in particular his theories on evolution brought him considerable criticism. “Lamarckism” is now used in a derogatory sense to refer to the discredited theory that acquired traits can be inherited. However, Lamarck’s beliefs were actually more complex, and not so out of step with what became known as Darwinism. Lamarck believed that environmental change affects organisms so that they change their behavior. Altered behavior leads to greater or lesser use of a structure or organ; use would cause it to be enhanced over several generations; disuse would cause it to disappear. The concept that use or disuse would cause structures to enlarge or shrink was called the “first law” in Lamarck’s book “Philosophie zoologique” published in 1809. His “second law” stated that changes were heritable. The result of his first and second laws is that organisms change and adapt to their environment. So although the mechanism proposed by Lamarck to explain evolution is different than Darwin’s, the outcome is about the same. Thus, Lamarck should be credited with advancing the concept of evolution, though Darwin should be justifiably credited with the stronger mechanistic argument and the stronger set of supporting data. He died on December 28, 1829.

References Jackson RT (1905) Professor Packard’s “Lamarck, his life and work”. Psyche 12:36–38 Waggoner BM (1996) Jean-Baptiste Lamarck (1744–1829). Available at http://www.ucmp.berkeley.edu/history/ lamarck.html. Accessed 4 April 2008

Lappet Moths (Lepidoptera: Lasiocampidae)

Lamella A thin plate or leaf-like process.

Lamellate With flattened, plate-like structures. This is usually used to describe antennae with flattened structures at the tip.  Antennae of Hexapods

Lampyridae A family of beetles (order Coleoptera). They commonly are known as lightningbugs or fireflies.  Beetles

Lanceolate A structure that is spear-shaped, with a pointed tip.  Antennae of Hexapods

Lance-Wing Moths (Lepidoptera: Pterolonchidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Lance-wing moths, family Pterolonchidae, total only 11 species, mostly Mediterranean, with two in South Africa.The family is part of the superfamily Gelechioidea in the section Tineina, subsection Tineina, of the division Ditrysia. Adults small (24–27 mm wingspan), with head smooth-scaled; haustellum absent; labial palpi porrect; maxillary palpi absent. Wings elongated. Maculation mostly light shades of brown or mostly white. Adults may

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be mostly crepuscular. Larvae are root borers as far as is known. Only recorded host plants are in Compositae.

References Campobasso GR, Sobhian L, Knutson AC, Pastorino, Dunn PH (1994) Biology of Pterolonche inspersa (Lep.: Pterolonchidae), a biological control agent for Centaurea diffusa and C. maculosa in the United States. Entomophaga 39:377–384 Heppner JB (1997) Immature stages of the Mediterranean knapweed borer, Pterolonche inspersa (Lepidoptera: Pterolonchidae). Holarctic Lepidoptera 4:63–66 Minet J (1988) Quelques caractères pré-imaginaux permettant de maintenir les Pterolonchidae au sein des Gelechioidea (Lepidoptera: Ditrysia). Annals de la Société Entomologique de France (n.s) 24:375–376 Vives-Moreno A (1984) Pterolonche gozmaniella Vives nov. sp., nueva especie de la familia Pterolonchidae Meyrick, 1918, para la fauna de España. SHILAP Revista de Lepidopterologia 12:195–197

Languriidae A family of beetles (order Coleoptera). They commonly are known as lizard beetles.  Beetles

Lappet Moths (Lepidoptera: Lasiocampidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Lappet moths, family Lasiocampidae (also called tent caterpillars), include 2,130 species worldwide, with the most in Africa (790 sp.). Subfamilies remain unclear and need more study, but five are now recognized: Chondrosteginae (African), Chionopsychinae (African), Poecilocampinae (Palearctic), Macromphalinae (New World), and

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Large Cabbage White Butterfly, Pieris brasicae (Linnaeus) (Lepidoptera: Pieridae)

Lasiocampinae. The family is in the superfamily Bombycoidea (series Bombyciformes), in the section Cossina, subsection Bombycina, of the division Ditrysia. Adults small to very large (19–172 mm wingspan), with head vertex roughscaled; haustellum absent (rarely vestigial); labial palpi short, upcurved or somewhat porrect; maxillary palpi absent (rarely vestigial); antennae bipectinate; body robust and usually with very long hair-like setae. Wings broadly triangular and usually rounded, but sometimes with forewing apex somewhat acute; hindwings rounded; some with micropterous females. Maculation mostly somber browns or grays, with various markings, but can be more colorful with pink spotting or completely bright green or yellow, for example, or white with black spotting. Adults mostly nocturnal but some males are diurnal. Larvae are leaf feeders, sometimes communally in silken tent-like webbings. Larvae typically have many lateral secondary hair-like setae that cover the prolegs when on the host leaf. Host plants are various, with many records in Betulaceae, Compositae, Fagaceae, Gramineae, Lauraceae, Leguminosae, Myrtaceae, Rosaceae, Salicaceae, and Tiliaceae, among others. Some species are economic as tree defoliators (Fig. 19).

References Fitzgerald TD (1995) The tent caterpillars. Cornell University Press, Ithaca, 303 pp, 2 pl Franclemont JG (1973) Lasiocampidae. In: Dominick RB (eds) The moths of America north of Mexico including Greenland, Fasc. 20.1. Bombycoidea. E.W. Classey, London, 86 pp, 11 pl [part] Holloway JD (1987) Family Lasiocampidae. In: The moths of Borneo, Malayan Nature Society (Malayan Nature Journal, 41), Kuala Lumpur, pp 311–361, pl 1–6 Jost B, Schmid J, Wymann HP (2000) Lasiocampidae– Glucken, Wollraupenspinner. In: Schmetterlinge und ihre Lebensräume: Arten–Gefährdung-Schutz. Schweiz und angrenzenden Gebiete 3:263–350, pl 11–15, Basel Seitz A (ed) (1911–1934) Familie: Lasiocampidae. In: Die Gross-Schmetterlinge der Erde, 2:147–180, pl 24–30 (1911); 2(suppl):109–125 (1932), 284–285, pl 9–10 (1934); 6:565–628, pl 75–86 (1927–28); 10:391–415, pl 32–35, 46 (1921–22); 14: 205–281, pl 29–40 (1927). A. Kernen, Stuttgart

Large Cabbage White Butterfly, Pieris brasicae (Linnaeus) (Lepidoptera: Pieridae) John L. Capinera University of Florida, Gainesville, FL, USA This species occurs widely in Europe, east to India and southwestern China, and in North Africa, but is not yet found in North America, unlike the similar cabbageworm or small cabbage white, Pieris rapae (Linnaeus). Large cabbage white was accidentally introduced to Chile, in South America, in 1971, and to South Africa in 1994.

Life history

Lappet Moths (Lepidoptera: Lasiocampidae), Figure 19 Example of lappet moths (Lasiocampidae), Lasiocampa quercus (Linnaeus) from Italy.

The number of generations per year depends on day length. In the northernmost regions it displays only one generation, but four generations are common in central Europe and six generations may occur in northern Africa. It is highly dispersive, regularly migrating from continental Europe to the United Kingdom, often in mixed swarms with

Large Cabbage White Butterfly, Pieris brasicae (Linnaeus) (Lepidoptera: Pieridae)

other pierids such as Pieris rapae (Linnaeus) and P. napi (Linnaeus). Adults lay cone-shaped eggs bearing sharp vertical ridges. They are yellow, about 1.2–1.4 mm high, and resemble the eggs of P. rapae but are laid in groups of 20–50 instead of singly or in pairs as in P. rapae. The eggs may be deposited beneath or on the upper surface of the leaves, but the former position is favored. The eggs hatch in 3–13 days, depending on temperature. Upon hatching, young larvae consume the egg chorion before consuming foliage. The young, pale green larvae remain clustered together, though they soon acquire a mottled blue-green appearance. Larvae remain gregarious until nearing their maturity. Usually there are 3 instars (though up to 5 has been reported), and mature larvae wander considerable distances before pupating. Mature larvae are 25–40 mm long, yellowish brown, with black spots and yellow longitudinal stripes. The larva is densely clothed with hairs. About 30 days are normally required for larval development. Typical pupation sites include crop plants, weeds, fence posts, stone walls and other protected areas above the soil. In preparation for pupation, the larvae attach themselves by a supporting silken girdle and posterior hooks; the anterior end faces upward. The chrysalis is 20–24 mm long, 5–6 mm wide, and gray-green to yellow-brown but marked with small black and yellow spots. It bears lateral ridges and a dorsal ridge, and several blunt spikes on the abdomen. Pupation requires 7–60 days, depending on temperature. The butterfly, after it escapes from the pupal case, climbs and expands its wings to dry. The adult is a white butterfly with a wingspan of about 63 mm in males, and 70 mm in females. The forewings have black tips, and the hindwing has a small amount of black at the front margin. Dorsally, the female, but not the male, also bears two prominent black spots and a black dash on the forewing. The ventral surface of the wings is usually pale yellow. The adults favor sunny areas containing flowers, and are most active in hot weather. Adults

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mate 1–4 days after emergence. The male butterfly of P. brassicae can be distinguished from P. rapae by the presence of one dark spot on the forewing of P. rapae. The natural enemies of cabbage white butterfly are numerous, but perhaps most important are a baculovirus and the parasitoid Cotesia (Apanteles) glomerata (L.) (Hymenoptera: Braconidae). Trichogramma sp. (Hymenoptera: Trichogrammatidae) has been reared from eggs, but normally is not a very important mortality factor. General predators such as ground beetles (Coleoptera: Carabidae) and birds also can be locally important.

Damage This species feeds predominantly on cruciferous species, but adults are attracted to mustard oil glycosides so other plants containing these chemi cals also are attacked. Crops damaged include broccoli, Brussels sprouts, cabbage, cauliflower, horseradish, kohlrabi, mustard, rape, radish, rutabaga, sarson, toria and turnip. Many weeds are affected, including shepherd’s purse, Capsella bursapastoris, flixweed, Descurainia sophia, hoary cress, Cardiaria draba, and many others. It is a defoliator, and because it is a fairly large insect, it can cause impressive levels of defoliation when present. However, damage tends to be limited to margins of fields.

Management Large cabbage white now is much less damaging in Europe than formerly, possibly due to better weed management and better insecticides. The principal concern is that due to its dispersive nature, large numbers of butterflies may suddenly appear in some areas, suddenly triggering the need to control them. Normally, a single application of insecticide to foliage provides season-long protection to vegetables; field crops are usually not treated. The bacterial insecticide Bacillus thuringiensis is effective if applied to young larvae,

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Large Caddisflies

though use generally requires more frequent application. For small-scale cultivation, netting may be used to cover the crop and prevent oviposition.  Cabbageworm  Pieris rapae (Linnaeus) (Lepidoptera: Pieridae)  Vegetable Pests and Their Management

References Feltwell J (1982) Large white butterfly. The biology, biochemistry and physiology of Pieris brassicae (Linnaeus), vol 18. W. Junk, The Hague, The Netherlands Harvey JA (2006) Development of the herbivore Pieris rapae and its endoparasitoid Cotesia rubecula on crucifers of field edges. J Appl Entomol 130(9–10):465–470 Hochberg ME (1991) Intra-host interactions between a braconid endoparasitoid, Apanteles glomeratus, and a baculovirus for larvae of Pieris brassicae. J Anim Ecol 60:51–63 McKinlay RG (1992) Vegetable crop pests. CRC Press, Boca Raton, FL, 406 pp

Large Caddisflies Members of the family Phryganeidae (order Trichoptera).  Caddisflies

Large-Legged Thrips Members of the family Merothripidae (order Thysanoptera).  Thrips

Large Milkweed Bug, Oncopeltus fasciatus (Hemiptera: Lygaeidae) Dorothy Feir St. Louis University, St. Louis, MO, USA The large milkweed bug, scientific name Oncopeltus fasciatus (Dallas), is the most common of the five

known species of this genus in the U.S. There are at least 24 species of Oncopeltus worldwide and these may all be called milkweed bugs because they feed on milkweed plants. Although all the bugs look quite similar, there are some differences in the color patterns. Oncopeltus fasciatus is found from the east coast to California, north to Massachusetts and south to Florida and Texas. Related species are found wherever species of milkweed grow. Asclepiadaceae is the very large family of milkweed species. Oncopeltus fasciatus (Dallas) has also been found on live oak in Florida, on the foliage of willow and flowers of goldenrod in Indiana, on the flowers of avocado in Texas, on oleander in Florida and on Apocynum in Missouri. The reports do not indicate whether the insects were actually feeding on the plants. In the laboratory, the bugs were tested on the following, but none would go through their life cycles on them: black walnuts, English walnuts, pecans, Brazil nuts, almonds, seeds of Helianthus, seeds of Arachis hypogaea, raisins, whole kidney beans, rolled oats, cantaloupe seeds, wheat, bluegrass, parsley, gelatin, cabbage, hamburger, peanut butter, fresh string beans and coconut. The bugs have been successfully reared through their life cycles in the laboratory on watermelon seeds that had the coats cracked, raw or blanched peanuts, sunflower seeds, pumpkin seeds and squash seeds. After several generations, milkweed bug strains became adapted to sunflower seeds, cashews and almonds. Survival and reproduction were poor for several generations until the insects became adapted. The sunflower seeds produced the best results in terms of survival and reproduction, but the results were never on a par with the results obtained from feeding them on milkweed seeds. Even after several years of generations fed on sunflower seeds, the bugs seem to still prefer milkweed seeds in choice tests. The bugs are easy to rear in the lab on milkweed seeds and water. It is quite labor intensive to collect a year’s supply of milkweed seeds in the fall when the seeds are ripe, and a number of attempts have been made to develop a chemically defined diet, but these attempts have not been very successful. Milkweed

Large Milkweed Bug, Oncopeltus fasciatus (Hemiptera: Lygaeidae)

pods and seeds can be kept in a dry condition in a freezer, or at room temperature for years and still be adequate food for rearing the bugs. Although a few laboratory studies have shown that adult milkweed bugs can live for short periods of time under freezing conditions, it is generally agreed that these bugs survive the winter only in warm climates. It is thought that all instars die in the fall in northern areas and that new insects migrate up from the south in the spring or summer because, in some states, they have not been seen until July. The large milkweed bug was found to be a migratory insect principally from laboratory studies using tethered insects to determine how long they could fly. The evidence does seem to be rather strong and there is no other explanation as to why they are never found over-wintering in the midwestern and northern states. The adult female large milkweed bug undergoes a reproductive diapause before it enters its migratory phase. The large milkweed bug is described as a hemimetabolous insect that has five immature stages and the adult stage. The immature stages look very much alike except for size. Wing pads appear in the third instar and increase in size in the fourth and fifth instars. The adults have two pairs of fully developed wings in O. fasciatus. The temperature and the amount of available food affect the rate of growth and the size of the insects, but, in general, the adult female is about threequarters of an inch long and is bigger than the male. At 29.5°C in one experiment, the egg stage lasted 4 days, the five immature stages lasted 5.8, 5.9, 6.1, 4.5 and 6.8 days, respectively. There is considerable variation in the life history of the bugs reported in the literature. There is great variability in the length of the adult stage, but many adults live for 2 months. The longest life span seen in the literature was 24.7 weeks for virgin females. Higher temperatures, longer photoperiods and lower densities of the insect increase their reproduction and also their mortality. As long as there are milkweed seeds available and the temperatures are not very cold, milkweed bugs will go through a series of life

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cycles and all stages of the bug may be seen at the same time on the plants. The preferred food of the milkweed bug in the field seems to be Asclepias syriaca and some of the reasons given for the preference are that this species has a relatively large number of pods and the plants grow in clumps or groups. Some of the clumps can be very large and include hundreds of plants. Because the immature large milkweed bugs cannot fly, the adult female has to lay her eggs where there will be abundant food for the offspring. The eggs are usually laid in clumps of 30 or so on the undersides of the leaves, on the unopened pods, or on the fluff of the opened pod. The sucking mouth parts of O. fasciatus are fairly long compared to the size of the insect, but the mouth parts of the young stages cannot penetrate the seed pod to reach the seeds inside. The young insects can feed on the leaves and green pods, but they seem to prefer the ripe, brown seeds when they are available. When feeding on the ripe, brown, hard seeds, the insects build a short sheath or tube that can be seen on the surface of the seed. Some scientists theorize that this serves as a support or a guide for the stylets (mouth parts). The functional mouth of the milkweed bug and its relatives is made up of a pair of elongated maxillae and a pair of elongated mandibles. The maxillae form the inner members of this stylet bundle, and each maxilla has two deep grooves that are opposite the grooves of the other maxilla, and thus, two canals or tubes are formed. Saliva is pumped down one tube and fluids are sucked up through the other tube. There are barbs on the tips of the mandibles that aid in the penetration of foods. When feeding on ripe seeds, the insects eject their salivary secretions into the seeds and then suck up the digested or dissolved seed material. In this way, they completely remove all edible parts of the seed and leave nothing but the seed coat. A number of species in the milkweed family and the closely related family, Apocynaceae, have been shown to contain cardenolides (digitalis-like, toxic compounds). Cardenolides are specific inhibitors of Na, K-ATPase activity, and, therefore,

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Large Milkweed Bug, Oncopeltus fasciatus (Hemiptera: Lygaeidae)

are toxic to many vertebrates and invertebrates. The milkweed bug (and probably other insects that feed on these two families of plants) sequesters the ingested cardenolides into the dorso-lateral space fluid by an energy-dependent physical process. The Na, K-ATPase activity of the milkweed bug is highly resistant to cardenolides, and the bug can tolerate high doses of cardenolide that would be lethal for vertebrates and many other invertebrates. The presence of the cardenolides in the milkweed bugs protect them from predation by many vertebrates and invertebrates. The predators learn that the milkweed bugs are toxic for them and they do not prey on them. There are many red and black insects (the colors of the milkweed bugs) who benefit from mimicking the colors of the toxic milkweed bugs. The cardenolides cause some birds to vomit, which is a quick way to determine the susceptibility of birds and other animals to cardenolides. Some investigators have shown that milkweed bugs feed preferentially on milkweed species that have higher levels of cardenolides, and that seed cardenolide content was a good parameter for the growth efficiency of O. fasciatus. The large milkweed bug has been used extensively as a research insect because of the ease with which it can be reared. Some of the research has shown that the large milkweed bug is somewhat different from the majority of insects. One of these differences is that makisterone A is the major molting hormone of O. fasciatus. Ecdysone and 20-hydroxyecdysone are the principal molting hormones in most other insects that have been studied. Because insects cannot synthesize cholesterol, they must use precursor molecules to make the molting hormones. Campesterol has been suggested as the precursor for the synthesis of makisterone A. Precocenes are compounds derived from the plant, Ageratum houstonianum, and they have been shown to destroy the corpora allata of insects, principally in the Order Hemiptera. The corpora allata are the site of juvenile hormone synthesis, and the inactivation of the corpora allata in the younger large milkweed bug instars resulted in precocious metamorphosis to a small adult,

inhibition of oogenesis in females and inhibition of long-term (migratory) flight in both males and females. The effects of precocene can be counteracted by an appropriate application of juvenile hormone. The large milkweed bug midgut is made up of four subdivisions, and the residues of nymphal meals seem to be retained in the third region until after the molt to the adult when the residues are voided. The fourth region does not have a complete lumen until the adult ecdysis (molt). The ovaries of Hemiptera are different from other insects. In the Hemiptera, each ovariole has a region of nutritive cells at the anterior end of a string of oocytes. Therefore, there is a nutritive tube that carries nutrients from the nutritive cells to the developing oocytes. This is called a telotrophic ovary. Variations on the typical or normal appearance of O. fasciatus have appeared spontaneously in different laboratory strains around the world. A gynandromorph appeared in Oslo, and a white strain or a partially white strain has appeared in several different labs in the U.S. Interspecific hybridizations of O. fasciatus have been found rather frequently in nature, and, in some cases, hybrid individuals have been collected. The authors concluded that both pre- and post-mating isolating mechanisms work to prevent introgressive hybridization. In general, there is a gradual change in color in captive milkweed bugs, which is much less dramatic than in the preceding examples. However, the gradual change (often a lightening of the orange-red color) should be remembered because it might indicate that other changes occur in the bugs with prolonged cultivation. These changes are different in different laboratories; therefore, it might be wise to obtain insects from various laboratories when doing any type of research on milkweed bugs. l-amino acids are by far the most common amino acids in animals. O. fasciatus has d-alanine in its hemolymph. This isomer must be produced during intermediary metabolism because it is not present in the milkweed plant. An antibacterial agent, active against Staphylococcus aureus and one strain of Bacillus subtilis, has been found in

Larger Grain Borer, Prostephanus truncatus (Coleoptera: Bostrichidae)

the hemolymph of the fifth instar. The formula of this compound was determined to be C13H14O3, and it was suggested to have a three-ring structure. The hemolymph of the fifth instar also contains an agglutinating factor for human erythrocytes. However, its activity was lost after 45 min at room temperature. O. fasciatus is a natural host for three species of trypanosomatids: Leptomonas oncopelti, Phytomonas elmassiani and Crithidia oncopelti. Leptomonas oncopelti has been found in various parts of the digestive tract and in the salivary glands. Binary fission switches to budding in the midgut of the bug. The flagellates do not appear in the rectum until adulthood. The flagellates form a “carpet” attached to the cuticular intima of the rectal glands of adults. Because the milkweed plant dies back every fall, and there is no continuity of latex tubules in the roots, the flagellates have no way of overwintering in the plants and, therefore, the plants have to be reinfected every year. Reinfection is probably done by O. fasciatus. The flagellates pass from bug to bug, probably by fecal contamination. Photoperiod affects several aspects of the large milkweed bug’s life. Mating and feeding activities reached the maximum levels at the end of the light phase. Long photoperiods produced higher levels of mating and feeding than did short photoperiods. Large milkweed bugs have a very characteristic odor, which is readily picked up when handling the bugs. This odor probably comes from the accessory gland of the metathoracic scent apparatus in the adult. The odor is probably not a defensive secretion. The dorsal scent glands of the larvae do not function in the adult.

References Chaplin SJ (1980) An energetic analysis of host plant selection by the large milkweed bug, Oncopeltus fasciatus. Oecologia (Berlin) 46:254–261

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Feir D (1974) Oncopeltus fasciatus: a research animal. Annu Rev Entomol 19:81–96 Jones GL, Mei JV, Yin CM (1986) Meridic diet for Oncopeltus fasciatus (Heteroptera: Lygaeidae) and its utilization in evaluating an insect growth regulator. J Econ Entomol 79:323–328 Masner P, Bowers WS, Kalin M, Muhle T (1979) Effect of precocene II on the regulation of development and reproduction in the bug, Oncopeltus fasciatus. Gen Comp Endocrinol 37:156–166 Scudder GGE, Duffey SS (1972) Cardiac glycosides in the Lygaeinae (Hemiptera: Lygaeidae). Can J Zool 50:35–42

Larger Grain Borer, Prostephanus truncatus (Coleoptera: Bostrichidae) Christian Borgemeister University of Hannover, Hannover, Germany As are most other beetles in the family of Bostrichids, the larger grain borer, Prostephanus truncatus (Horn), is a wood-boring beetle. It is native to Central American and Mexican forests and has long been known to occasionally attack stored commodities such as maize and cassava, sporadically causing serious damage in small-scale farmers’ stores. However, the beetle attracted much greater public and scientific interest after its serendipitous introduction into Africa in the late 1970s and early 1980s. The beetle was first observed by farmers in the Tabora region of Central Tanzania. This new pest caused tremendous damage to their maize harvest, and because of the resemblance of the flattened head of the beetle to commonly used trucks in East Africa, farmers called it “scania beetle.” Later, the pest was identified as P. truncatus, which was probably introduced to Tanzania through maize imports from Mexico that had not been properly fumigated. A second independent introduction of P. truncatus happened around 1984, when the pest was first recorded in the greater Lomé area, the capital of the small west African state of Togo. From these two focal points of introduction, the beetle has spread, to date, to a total number of 17 African countries, thus

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c overing a great part of the maize-producing region of sub-Saharan Africa. In some of these countries, P. truncatus has become the most serious pest of farm-stored maize, sometimes causing losses of up to 30 to 40% of the harvested commodity.

Biology, Ecology and Damage Potential The larger grain borer attacks a whole variety of stored commodities besides the various tree species that are their natural host plants. However, the greatest damage is inflicted to farm-stored maize and cassava, though it is a more serious pest of maize than of cassava. Infestations often commence in the field when the adult beetles bore into the maize cobs prior to harvest. Female P. truncatus usually lay up to eight eggs in clutches in maize grains, and their offspring develop within the grains, feeding on the starchy-rich endosperm of the maize kernels. However, the greatest damage is caused by the tunneling behavior of the adult beetles that often turn the maize into flour. The enormous amount of frass caused by the feeding pattern of the adults is often the first and most conspicuous sign of a P. truncatus infestation. Larger grain borer attacks cause greater damage when the maize is stored on the cobs than as shelled grain, unlike the two other important pests of post-harvest maize in Africa, the maize weevil Sitophilus zeamays Motschulsky (Coleoptera: Curculionidae), and the Angoumois grain moth Sitotroga cerealella (Olivier) (Lepidoptera: Gelechiidae). Moreover, P. truncatus can thrive on maize even when the moisture content of the grain drops below a level of 10%, the threshold for most of the other pests attacking stored maize. In southern Togo, maize losses after an average storage period of 6 months increased from 11% prior to the introduction of P. truncatus, to more than 35%. In areas with high incidence of P. truncatus in Tanzania, up to 34% losses of maize have been observed after three months of on-farm storage. When male P. truncatus locate a suitable breeding substrate like maize

where there are no females present, they produce a pheromone that is highly attractive to individuals of both sexes. Once the females have been guided to these sites, the males cease pheromone production. However, beetles feeding and reproducing on maize or other suitable food substrates are no longer receptive to the pheromone. Thus, the pheromone is of paramount importance for the host-finding behavior of the beetles. In the late 1980s, the chemical composition of the pheromone was identified. The pheromone was subsequently synthesized, and is currently commercially available. It is primarily used for monitoring purposes, particularly to document the spread of infestation of P. truncatus throughout sub-Saharan Africa. Larger grain borer adults are rather poor flyers. Pheromone trap data revealed that the beetles only fly during short periods at dusk and at dawn. Thus, the spread of the beetle in Africa is mainly due to movement of infested commodities, i.e., within and between countries trading maize and cassava.

Conventional Control Strategies After its first detection in Tanzania, campaigns were launched in the early 1980s to eradicate the beetle from the African continent. Prostephanus truncatus is highly susceptible to synthetic pyrethroid insecticides like permethrin and deltamethrin, and also to fumigants like phosphine and methyl bromide, (though the latter is now banned in many African countries). However, since the beetle not only attacks stored commodities, but also breeds in natural forest habitats, these eradication efforts were not successful. Yet, binary insecticide programs, consisting of a synthetic pyrethroid for control of P. truncatus and an organophosphorus insecticide for control of other storage pests like S. cerealella, were successfully implemented in many affected East African countries. However, the adoption rate of such a chemical control strategy was much lower in West Africa, mainly due to socio-economic constraints on behalf of the farmers, and logistical difficulties in the distribution of the insecticides.


Classical Biological Control As an exotic outbreak pest in Africa that caused spectacular damage in its new area of distribution but was of considerably lower economic importance in its area of origin in Mexico and Central America, P. truncatus was considered to be a prime candidate for a classical biological control program. Hence, in the mid 1980s, intensive surveys were carried out in Mexico and several countries of Central America to identify efficient natural enemies of P. truncatus. However, the natural enemy complex of P. truncatus turned out to be rather poor in diversity. Several hymenopteran parasitoids, mainly pteromalids, were found to be associated with P. truncatus. Yet, all of these parasitoids were of cosmopolitan distribution, already existed in Africa, had a very broad host range, and showed no clear host preference for P. truncatus. Therefore, they were not considered for importation into Africa. The only specialized natural enemy that was identified during these surveys was the predator Teretrius (formerly Teretriosoma) nigrescens (Lewis) (Coleoptera: Histeridae). A close association between P. truncatus and T. nigrescens had already been observed prior to the introduction of the larger grain borer into Africa. During the subsequent search for natural enemies of P. truncatus in Mexico and Central America, the predator was always found in grain stores that were infested by the larger grain borer. Moreover, once the synthetic pheromone of P. truncatus became available, consistently high by-catches of T. nigrescens were recorded in pheromone traps located both in areas with agricultural production as well as in forests. Later, studies revealed that the predator uses the pheromone of P. truncatus as a kairomone to locate its prey. Electro-antennograms then showed that T. nigrescens reacts as sensitively to the pheromone as P. truncatus itself. In a large series of laboratory experiments by British and German researchers, T. nigrescens was able to fully suppress P. truncatus populations at a predator:prey ratio of 1:10. Both the adults and the larvae of T. nigrescens feed on the eggs and the larval stages of P. truncatus, though

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the larvae are far more voracious than the adult beetles. Adult T. nigrescens are strong flyers, longlived with a longevity exceeding 20 months, and can survive extended periods of starvation (more than 60 days). Based on these findings, the predator was considered for importation into Africa. However, prior to the release, concerns were expressed about the potential ecological risks associated with a wide spread deployment of T. nigrescens in Africa. Histerids are, in general, oligo- to polyphagous predators. Therefore, prior to the release, the prey behavior of T. nigrescens was investigated in laboratory experiments. Results of these studies showed that T. nigrescens readily preys on other insects, mainly other coleopteran and lepidopteran larvae that occur in the maize storage environment, but it strongly prefers P. truncatus as prey in a choice situation. A post-release prey composition study, using electrophoretic gut content analysis techniques, showed that T. nigrescens clearly prefers P. truncatus as prey. The predator was first released in 1991 in southern Togo, and three years later in Ghana and Kenya. Between 1992 and 1997, a long-term impact assessment study was conducted in southern Togo and the neighboring Republic of Benin. Data from pheromone traps, as well as from large-scale storage experiments and surveys of farmers’ maize stores showed a rapid spread of the predator, with substantially decreased trap catches of P. truncatus, as well as significantly reduced infestation levels and post-harvest losses of maize, particularly in the south of Togo and Benin. In Kenya, where the predator had been released in a bush land region dominated by forests, long-term pheromone trapping revealed a substantial decline in trap catches of P. truncatus. Thus, T. nigrescens is capable of controlling P. truncatus both in the maize store environment, as well as in its native forest habitat. To date, the predator has been released in eight African countries and several impact assessment studies are ongoing. This is the first case where classical biological control has been rather successfully used against a post-harvest pest.  Stored Grain and Flour Insects

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References Borgemeister C, Djossou F, Adda C, Schneider H, Djomamou B, Azoma K, Markham RH (1997) Establishment, spread and impact of Teretriosoma nigrescens Lewis (Coleoptera: Histeridae), an exotic predator of the larger grain borer Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae), in south-western Benin. Environ Entomol 26:1405–1415 Hodges RJ (1994) Recent advances in the biology and control of Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae). In: Highley E, Wright EJ, Banks HJ, Champ BR (eds), pp 929–934, Proceedings of the 6th international working conference on stored-product protection, 17–23 April 1994, Canberra, Australia Markham RH, Wright VF, Rios Ibarra RM (1991) A selective review of research on Prostephanus truncatus (Col.: Bostrichidae) with an annotated and updated bibliography. Ceiba 32:1–90 Rees DP (1985) Life history of Teretriosoma nigrescens Lewis (Coleoptera: Histeridae) and its ability to suppress populations of Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae). J Stored Prod Res 21:115–118 Scholz D, Borgemeister C, Meikle WG, Markham RH, Poehling HM (1997) Infestation of maize by Prostephanus truncatus initiated by male-produced pheromone. Entomol Exp Appl 83:53–61

Larviform Shaped like a larva.

Larviporous A method of reproduction, especially in flies, wherein the eggs hatch within the female’s body, and the larvae are deposited. In some cases the larvae obtain nutrition from the female, and pupate almost immediately upon being deposited.

Lasiocampidae A family of moths (order Lepidoptera). They commonly are known as tent caterpillars, lappet, or lackey moths.  Lappet Moths  Butterflies and Moths

Lasiochilidae Largidae A family of bugs (order Hemiptera).  Bugs

A family of bugs (order Hemiptera).  Bugs

Latent Infection Larva (pl., larvae) The growing stage of an insect (usually an insect with complete metamorphosis). The feeding stage between the egg and pupal stages. The immature stages of mites also are called larvae. Larval insects usually bear little resemblance to the adult stage, and often feed on different items.

Larvicide An insecticide used to control the larvae of insects. This term is often used to describe the insecticides used for suppression of mosquito larvae (contrast with adulticide).

An inapparent infection in which the pathogen is still present in a “dormant” or noninfective phase, and in which a certain pathogen-host equilibrium is established.

Latent Learning This form of learning, also called exploratory learning, involves the ability to recognize and remember landmarks. Social insects use landmarks as a means of finding their way back to their nest after they leave to forage for food.  Habituation  Associative Learning  Insight Learning

Latreille, Pierre André

Lateral Oviduct A tube of the female reproductive system that connects the ovaries to the common oviduct, through which eggs pass prior to fertilization (Fig. 20).

Lathridiidae A family of beetles (order Coleoptera). They commonly are known as minute brown scavenger beetles.  Beetles

Latreille, Pierre André Pierre Latreille was born on November 29, 1762 at Brive, in the province of Limousin, France. An illegitimate child of the baron d’Espargnac, he was abandoned by his mother at a church in Brive. His biological father eventually made financial arrangements for his son’s education,

ovary ovariole calyx lateral oviduct spermatheca accessory gland median oviduct vagina

Lateral Oviduct, Figure 20 Diagram of female reproductive system, as found in Rhagoletis (Diptera) (adapted from Chapman, The insects: structure and function).

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and he was educated at the Collège des Doctrinaires at Brive and the Collège du Cardinal Lemoine at Paris. He also was awarded a Master of Arts from the Paris University in 1780, entered a seminary and was made a Deacon in 1786. He likely was made a priest, though there is no record of this, and he was acting vicar at Lostanges in October 1789. At this time he became interested in entomology, living on the income that his father, the général baron d’Espargnac, had established for him. However, the French Revolution would cause him to be imprisoned, and sentenced to death or deportation. His interest in insects was recognized while he was in prison, and a sympathetic official terminated Latreille’s sentence. He remained in prison until 1794, however, and he gave up the priesthood and became a teacher. In 1796, encouraged by Fabricius, he published the “Précis des caractères génériques des insectes.” This innovative treatise created the concept of insect families. In 1798 he received an appointment at the Muséum, where he worked closely with Lamarck. In 1814 he was named a member of the Académie des Sciences, and he entered a very productive stage of his life, but he remained very poor. He often assisted others in their natural history publications, though he also published his own work. In Cuvier’s “Règne Animal” (1829) Latreille laid down the taxonomy of the entire Arthropoda. Eventually he replaced Lamarck as the dominant scientist of the institute. In 1830 he was awarded a new chair at the Muséum. Thus, he received recognition only late in life, despite a legacy of innovative contributions and decades of toil. Latreille is remembered primarily as a taxonomist, though he made important contributions in other areas. He introduced new methodologies and examined an enormous number of taxa. He believed in basing taxonomic groupings on the natural order: assembling species into genera, then into families, etc. Indeed, he was most interested in establishing genera, and named hundreds of new genera. Latreille also had profound impact on zoological nomenclature, emphasizing the principle of

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Lauxaniid Flies

Lauxaniid Flies Members of the family Lauxaniidae (order Diptera).  Flies

Lauxaniidae A family of flies (order Diptera). They commonly are known as lauxaniid flies.  Flies

LC50 An abbreviation for lethal concentration, with the subscript denoting a proportion of the population tested. LC50 is the concentration of a substance that kills half of the test organisms. Latreille, Pierre André, Figure 21 Pierre Latreille.

LD50 priority, insisting that families be named after an included genus, and emphasizing the concept of type species of a genus. Latreille was interested in morphology, and created several new terms. Interestingly, he considered field work most important, and was particularly interested in behavior. He sometimes incorporated behavioral characteristics into his taxonomic treatments. Though Latreille’s achievements were often overshadowed by better-known scientists of the era, he eventually became known as the foremost entomologist of his time, and has even been called the “prince of entomology.” He died at Paris on February 6, 1833 (Fig. 21).

References Dupuis, Claude (1974) Pierre André Latreille (1762–1833): the foremost entomologist of his time. Annu Rev Entomol 19:1–13 Herman LH (2001) Latreille, Pierre Andre. Bull Am Mus Nat Hist 265:94–96

An abbreviation for lethal dose, with the subscript denoting a proportion of the population tested. LD50 is the dose of a substance that kills half of the test organisms

Lea, Arthur Mills George Hangay Narrabeen, NSW, Australia Arthur Mills Lea was born on August 10, 1868 in Sydney, Australia. He began collecting beetles at an early age. During his frequent visits to the Australian Museum where he was assisted and encouraged by Sir William J. Macleay and George Masters. He enrolled in night school to learn Latin and that was the only supplementary education he received, as his family could not afford to give him more. At the age of 15 he began work with an accountant firm in Sydney and remained in this employment for 6 years, during which he pursued entomology as a hobby,

Leaf Beetles (Coleoptera: Chrysomelidae)

winning prizes for his excellent insect collection and drawings of insects. He also taught himself French and German in order to understand entomological articles published in those languages. In 1891 he was appointed as entomologist’s assistant in the New South Wales Department of Agriculture in Sydney and later became Entomologist in the Western Australian Department of Agriculture. In 1899 he took up the position of Government Entomologist in Tasmania. In little more than ten years Lea has built the largest collection of Tasmanian Coleoptera (most of this collection is now in the South Australian Museum, Adelaide) and established himself as a recognized authority in applied entomology and biological control. In 1910 he became Museum Entomologist in the South Australian Museum. He worked for this museum until his untimely death on February 29, 1932. During his 21 years in the South Australian Museum more than a million specimens were added to its collections. Arthur Lea was undoubtedly the most productive Australian Coleopterist. He described and named 5,432 species new to science and published a staggering number of works. He had an exuberant personality and gave inspiration to many of his colleagues and students.

Reference Zimmermann EC (1993) Australian weevils, vol 3. CSIRO, East Melbourne, pp 622–648

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identification of breeding areas and disruption of incipient locust outbreaks. With the onset of World War II, his area of responsibility was changed to North Africa and he developed desert locust campaigns, based on distribution of BHC-treated bait, to help protect the food supply of the area. Returning to civilian life in 1946, he again tackled the sodium arsenite bait problem because ranchers were increasingly reluctant to use this toxic material, which often killed livestock. He enlisted use of BHC against brown locusts beginning in 1947. Lea was responsible for effective emergency locust suppression campaigns, but he also found time for a disciplined, scientific approach to understanding the locust problem. Throughout his career, he studied locust forecasting, population dynamics, and phase transformation. A principal product of his investigations was “Locust control and research in southern Africa” (1972), and he is widely acknowledged as being one of the eminent locust researchers. Lea was fellow of several scientific societies and served as president of the Entomological Society of Southern Africa, and editor of its journal. He died at Pretoria, South Africa on August 25, 1989.

Reference Brown D (1991) Lea HAF (1907–1989) Antenna 15:61–66

Leaching Lea, H. Arnold Arnold Lea was born on November 13, 1907, and was raised in Transvaal, South Africa. He was educated at the University of Pretoria, and in 1930 joined the Division of Entomology in Pretoria, the start of a 42-year career with the South African Department of Agriculture. South Africa experienced severe plagues of locusts beginning in 1932, and Lea joined a newly organized Locust Research Institute. His first task was to improve insecticidal control of red locusts, using improved bait formulations of sodium arsenite. Later he worked on

The movement of pesticides through the soil, assisted by water.

Leaf Beetles (Coleoptera: Chrysomelidae) R. Wills Flowers Florida A&M University, Tallahassee, Florida, USA The Chrysomelidae, or leaf beetles, are the third largest family in the Coleoptera, with 37,000

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described species and possibly as many as 60,000 when estimates of undescribed species are included. Only the Curculionidae and Staphylinidae are larger families. As the common name implies, Chrysomelidae are intimately associated with plants, although specific associations are known for only a small minority of the species. Chrysomelid adults are small to medium-sized beetles, often brightly colored, boldly patterned, or metallic. Some species are covered with hairs or scales. Most species are ovate or elongate-ovate, but body shape can vary from elongate to almost spherical (Figs. 22–26).

Classification Chrysomelidae belong to the infraorder Phytophaga of suborder Polyphaga within the order Coleoptera Leaf Beetles (Coleoptera: Chrysomelidae, Figure 23 Eumolpinae: Colaspis louisianae (Blake).

Leaf Beetles (Coleoptera: Chrysomelidae, Figure 24 Chrysomelinae: Leptinotarsa decimlineata (Say).

Leaf Beetles (Coleoptera: Chrysomelidae, Figure 22 Criocerinae: Neolema sexpunctata (Olivier).

(beetles). The Phytophaga are characterized by crytopentamerous tarsi, in which the fourth tarsal segment is greatly reduced (sometimes entirely absent) and largely hidden by the third segment. The


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Leaf Beetles (Coleoptera: Chrysomelidae, Figure 26 Cryptocephalinae: Cryptocephalus maccus (White). Leaf Beetles (Coleoptera: Chrysomelidae, Figure 25 Galerucinae: Chaetocnema pulicaria (Melsh).

hytophaga contain the superfamily ChrysomeloP idea, which includes the Chrysomelidae, and the superfamily Curculionoidea (weevils and their allies). The Chrysomelidae are one of two major families in the Chrysomeloidea (the other being the Cerambycidae) and are distinguished by having antennae not partially surrounded by the eyes, and by the presence of a basal hood on the median lobe of the male genitalia. Although the major groups within the Chrysomelidae have been generally recognized, the taxonomic ranks and boundaries of these groups continue to be actively debated. Recent phylogenetic analyses have resulted in the removal of several small problematic groups from the Chrysomelidae to other families, and some realignments and changes of the traditional subfamily classification. In the United States, the following subfamilies occur.

Bruchinae Until recently classified as a separate family, bruchids, or seed beetles, are now regarded as a subfamily of the Chrysomelidae, closely related to the Old World and Neotropical Sagrinae. Seed beetles are distinguished by their robust bodies, elongate heads, and enlarged hind legs. Larvae feed within seeds of legumes and other plants.

Donaciinae Adults in this subfamily somewhat resemble lepturine cerambycids in body shape. The head and pronotum are narrower than the width of the elytra at the base, and the general color is bronze or sometimes dark metallic. The family is aquatic in the larval stage and adults are found on emergent aquatic plants such as waterlilies or arrowheads. The underside of the adult is densely covered with hydrofuge hairs, and the

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hind femora often bear small teeth. This subfamily is world-wide except South America; in the Western Hemisphere representatives occur only as far south as Costa Rica.

Criocerinae Adults of this subfamily are generally brightly colored and all have a characteristic constriction across the pronotum. As in the preceding family, the head and pronotum are narrower than the basal width of the elytra, and the head has deep frontal grooves forming an “X” on the facial area (Fig. 22). Larvae feed openly on plants, covering themselves with their own feces for protection. Native North American species feed for the most part on plants of the families Solanaceae or Commelinaceae and cause little economic harm. However, three introduced species have become pests. One, the cereal leaf beetle (Oulema melanopus (L.)) is a serious pest of grain, and two species of Crioceris feed on asparagus.

Hispinae This subfamily has recently been expanded to include the tortoise beetles (Cassidini). The nominate tribe, Hispini, contains elongate beetles, frequently with the elytra very strongly punctate and costate. Members of the tribe Cassidini, on the other hand, are very broadly ovate to hemispherical, with margins of the pronotum and elytra explanate. In many species the head is concealed under the front margin of the pronotum. Many adult cassidines have striking gold or other metallic colors on the dorsal surface which in some species can be turned on or off by the animal. Becauce these colors reside in the living tissues, they unfortunately disappear in pinned specimens. Although ‘typical’ hispines and cassidines have contrasting shapes, intermediate species occur and are not uncommon in tropical areas. All Hispinae have mouthparts that appear crowded into a constricted

opening in the head capsule, and all have foursegmented tarsi, in which the reduced fourth segment found in the rest of the Chrysomelidae has been completely lost. Larvae of the Hispini are leaf miners or, in a widespread Neotropical tribe, specialists in the unrolling terminal leaf of large monocots such as Heliconia; cassidine larvae are open feeders on many plants and cover their bodies with fecal shields for protection. In some tropical cassidine genera, maternal care of larvae has been observed.

Chrysomelinae The Chrysomelinae include some of the largest species of Chrysomelidae. As adults, most are robust oval to hemispherical beetles. The third tarsal segment is entire or at most weakly bilobed (it is strongly bilobed in some Eumolpinae that resemble chrysomelines), and a membrane between the clypeus and labrum is present. A more subjective but quite reliable method of separating chrysomelines from other robust Chrysomelidae is that, viewed from above, the head capsule of most Chrysomelinae appears rectangular with the eyes set diagonally at the anterior corners. Many chrysomeline adults have striking color patterns or bright metallic colors. Adults of Neotropical Doryphora, Platyphora and Metastyla have a prominent horn arising from the ventral surface between the middle and hind legs. Species of Doryphora are among the largest known Chrysomelidae. Adults of the New Guinea genus Promechus are large, elongate and bear a close resemblance to large Buprestidae. Larvae of Chrysomelinae are open feeders on leaves and many are chemically protected. The Colorado potato beetle, (Leptinotarsa decemlineata (Say)), one of the most destructive insect pests in the world (Fig. 24), belongs to this subfamily.

Galerucinae This subfamily is characterized by antennae set close together between the compound eyes,


antennal calli above the insertions, and the pronotum often narrower than the base of the elytra but without the transverse constriction found in the Criocerinae. This is the largest subfamily in the Chrysomelidae, the more so since the formerly independent Alticini (flea beetles) are now included in this subfamily. Although most species from the two major tribes Galerucini (rootworms) and Alticini can readily be distinguished by the size of the posterior femur (greatly enlarged in the flea beetles), many intermediate forms exist and a recent phylogenetic analysis indicates that the Galerucini is paraphyletic with respect to the Alticini. Adult galerucines display feeding behaviors ranging from narrow oligophagy to polyphagy. Larvae are mostly subterranean root feeders, but some open leaf feeders occur in both the Galerucini and Alticini. While most species are of no economic significance, several Galerucini species in the subtribe Diabroticina are extremely serious pests of corn and beans. Control of the corn rootworms (Diabrotica spp.) is the one of the costliest insect pest problems in North America.

Eumolpinae This group, which reaches its greatest diversity in South America, is the second largest subfamily in the Chrysomelidae. Adults range from large to very small, most are broadly oval with glossy dark or metallic colors. Recent phylogenetic studies have placed the formerly independent Synetini and Megascelidini within the Eumolpinae. Although the body shape found in these tribes (slender and elongate) is not typical for the subfamily, intermediate genera exist and genitalic characters strongly support their inclusion in the Eumolpinae. Larval eumolpines apparently are all root feeders; the biology is known for only a few species. Adults are leaf or pollen feeders and tend to be oligophagous or polyphagous. Some appear to specialize on

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young leaves. In North America, a few species are intermittent pests of strawberries and sweet potatoes, and other species cause occasional short-term damage to corn, grapes, and other crops.

Lamprosomatinae This small subfamily is worldwide with most of its diversity in the American tropics. Only one species, Oomorphus floridanus Horn, occurs in North America and it is limited to the tip of the Florida Peninsula. Adults are small and oval to almost spherical, with legs and antennae that can retract into groves on the lower body surface. The upper surfaces are always smooth and shiny. Adults feed on leaves of various trees and known larvae feed on the young bark of trees, living in cone-shaped cases constructed of fecal matter and wood particles.

Cryptocephalinae Members of this subfamily are characterized by a compact body, the second to fourth abdominal sterna narrowed medially, and the pygidium exposed. The subfamily contains three tribes until recently considered separate subfamilies: Cryptocephalini, Clytrini, and Chlamisini. Larvae of all species are case-bearers. Cryptocephalini larvae are found in leaf litter and detritus, on which they are thought to feed. Many larvae of Clytrini are found in association with ants, although it is not known whether this trait holds true for the majority of the tribe. Larvae of Chlamisini feed on leaves alongside the adults. Adult Chlamisini are noteworthy for the extreme rugosity of their dorsal surfaces, giving many species the appearance of pieces of caterpillar frass. While the effectiveness of this mimicry on birds and lizards has not been tested, there are documented instances of entomologists being fooled by the resemblance.

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Leaf Blotch Miners

Chrysomelidae and Pest Management Relatively little research has been done on natural enemies of pest Chrysomelidae. Before the era of modern pesticides, several natural enemies of the Colorado potato beetle had been identified and their effectiveness as control agents was beginning to be investigated. The introduction of synthetic pesticides following World War II put an end to this line of research, since it was assumed that the new miracle chemicals would eliminate the need for alternate forms of control. Now, after decades of attempts at chemical control, the Colorado potato beetle has evolved a complex, multifaceted spectrum of resistances virtually unmatched in any other insect. Not surprisingly, there are the beginnings of renewed interest in the natural enemies of this pest. While the economic damage inflicted by the corn rootworm complex and the Colorado potato beetle are among the best known effects of the Chrysomelidae, this family also has its positive aspects as a source of biological control agents of weeds. One of the success stories of classical biological control is the use of two species of the chrysomeline genus Chrysolina to control the Klamath weed in the western United States. Another success story has been the importation of the alligator weed flea beetle from Argentina. Alligator weed is an aquatic plant accidentally introduced from South America into the Southeastern United States. The weed was highly invasive in fresh water bodies, and its uncontrolled growth choked lakes and rivers. Once the flea beetle was introduced, its feeding reduced alligator weed to a relatively rare species in the U.S. More recently, Palearctic Apthona flea beetles have been introduced into western rangelands to control leafy spurge, and several European Galerucini have been introduced in an attempt to control purple loosestrife in northeastern United States. Invasion by weeds is a continuing and growing problem (e.g., tropical soda apple in Florida and Melastomataceae in Hawaii), and Chrysomelidae are now routinely

investigated as potential control agents of these emerging weed problems.

References Casagrande RA (1987) The Colorado potato beetle: 125 years of mismanagement. Bull Entomol Soc Ame 33: 142–150 Graham F Jr (1984) The dragon hunters. Dutton, New York, New York. 333 + xii pp Jolivet P (1997) Biologie des Coléoptères Chrysomélides. Sociéte Nouvelle des Éditions Boubée, Paris, France. 279 pp Konstantinov A, Vandenberg N (1996) Handbook of Palearctic Flea Beetles (Coleoptera Chrysomelidae: Alticinae). Cont Entomol Int 1:237–439 Lingafelter SW, Konstantinov AS (1999) The monophyly and relative rank of alticine and galerucine leaf beetles: a cladistic analysis using morphological characters (Coleoptera: Chrysomelidae). Entomologica Scandinavica 30:397–416 Reid CAM (1995) A cladistic analysis of subfamilial relationships in the Chrysomelidae sensu lato (Chrysomeloidea). In: Pakaluk J, Slipinski SA (eds) Biology, phylogeny, and classification of Coleoptera: papers celebrating the 80th birthday of Roy A Crowson. Muzeum i Instytut Zoologiii PAN, Warsaw, Poland pp. 559–631 Riley EG, Clark SM, Flowers RW, Gilbert AJ (2002) Family 124. Chrysomelidae. In Arnett RH, Thomas MC (eds) American Beetles, Vol. 2. CRC Press, Boca Raton, Florida, pp. 617–691

Leaf Blotch Miners Members of the family Gracillariidae (order Lepidoptera).  Leafminer Moths  Butterflies and Moths

Leafcutter Moths (Lepidoptera: Incurvariidae) John B. Heppner Florida State Collection of Arthropods, Gainesville, FL, USA Leafcutter moths, family Incurvariidae, total about 116 species from all regions, but most are

Leaf-Cutting Ants (Formicidae: Myrmicinae: Attini)

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Leaf-Cutting Ants (Formicidae: Myrmicinae: Attini) Klaus Jaffe Universidad Simón Bolívar, Caracas, Venezuela

Leafcutter Moths (Lepidoptera: Incurvariidae), Figure 27 Example of leafcutter moths (Incurvariidae), Incurvaria masculella (Denis and Schiffermüller) from Italy.

Palearctic (64 sp.), divided into two subfamilies, Incurvariinae and Crinopteryginae. The family is in the superfamily Incurvarioidea, in the section Incurvariina, of division Monotrysia, infraorder Heteroneura. Adults small (7–18 mm wingspan), with roughened head; haustellum reduced, scaled; labial palpi upcurved; maxillary palpi 5-segmented and folded. Maculation usually is somber, with large spots or bands and some iridescence. Adults are mostly diurnal in shaded habitats. Larvae are leafminers at first, then switch to leaf skeletonizing on a variety of host plants; some are casebearers or shoot borers (Fig. 27).

References Nielsen ES (1981) A taxonomic revision of the species of Alloclemensia n. gen. (Lepidoptera: Incurvariidae s. str.). Entomol Scand 12:271–294 Nielsen ES (1982) Incurvariidae and Prodoxidae (Lepidoptera: Incurvarioidea) from the Himalayan area. Insecta Matsumurana 26:187–200 Nielsen ES, Davis DR (1981) A revision of the Neotropical Incurvariidae s. str., with the description of two new genera and two new species (Lepidoptera: Incurvariidae). Steenstrupia 7:25–57 Scoble MJ (1980) A new incurvariine leaf-miner from South Africa with comments on structure, life-history, phylogeny, and the binomial system of nomenclature (Lepidoptera: Incurvariidae). J Entomol Soc S Afr 43:77–88 Wojtusiak J (1976) Incurvariidae. In: Klucze do Oznaczania Owadów Polski. 27. Motyle–Lepidoptera 94:1–60. Polskie Towardzystwo Entomologiczne (in Polish)

All ant species in the tribe Attini (Formicidae: Myrmicinae) cultivate a symbiotic fungus (Basidomycete: Lepiotacae) in order to feed their brood. The most conspicuous members of this tribe are undoubtedly the leaf-cutter ants from the genera Atta, Acromyrmex and Trachymyrmex. These ants cut leaves, which they prepare by removing surface waxes that normally harbor fungicides, before feeding their symbiotic fungus with it. The fungus helps to detoxify the leaves by degrading the insecticides which are normally found inside the leaves. The larvae feed basically on the fungus, whereas workers feed also on sugary plant sap flowing from the leaves while they are being cut. These ants build subterranean nests in which they grow their fungus which also needs a symbiotic bacterium in order to prosper. The workers regulate nest conditions so as to maintain humidity, temperature and carbon dioxide concentrations between narrow ranges. Workers avoid contaminations from other fungi and bacteria thanks to antibiotic secretions from their metapleural glands and the action of the symbiotic bacterium. The filamentous bacterium (Actinomycete) of the genus Streptomyces produces antibiotics specifically targeted to suppress the growth of the specialized garden-parasite Escovopsis. The symbiotic fungus is known only to occur in association with Attini ants. The lower Attini, which are not considered to be leaf-cutting ants, feed their fungus flowers, fruit pulp, dead insects, and animal excrements.

The Colony The leaf-cutting ant colony is normally monogynic, that is, it contains a single queen. A few cases of polygynic colonies (2–6 queens) have been reported, but this certainly is not the norm for these ants. The colony is formed by different individuals and each type

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of individuals is called a caste. The leaf-cutting ant colony contains normally only female individuals of at least two different castes, the queen and the workers. Just before the beginning of the tropical rain season, the colony produces winged individuals, fertile males and females which wait inside the nest for their nuptial flight after the first rains. All these types of individuals or castes are found in their different life stages such as eggs, larvae, nymphs and adults in a single colony. The architecture of the subterranean nest is characteristic for each species. Workers also have behavioral castes. Young workers are more often engaged in caring for the fungus whereas older workers forage or engage in dumping rubbish and dead ants. The different components of a typical colony are:

The Queen Most mature leaf-cutting ant colonies have a single fertile queen, i.e., they are monogynic. The queen is the fertile female individual, inseminated during the nuptial flight by various males, in charge of laying eggs. The eggs might have been fertilized by a male spermatozoon or not. In the first case, they will produce females; in the second, they produce males. Depending on the amount of food the larvae of females receive (and may be on hormones provided by the colony), they will become either virgin queens, ready to start a nuptial flight and eventually a new colony, or sterile worker ants.

The Workers Workers are sterile female ants. A single Atta colony has workers of different sizes – they are polymorphic – whereas those from Acromyrmex and Trachymyrmex colonies are monomorphic, i.e., they are all approximately the same size. Polymorphism among workers from Atta species is continuous, that is, sizes of workers vary from just above a millimeter to over 2 cm in length. The smallest workers are found mostly inside the nest, caring for the fungus and larvae, whereas the

igger ones engage in foraging, leaf cutting, and b transport of leaf fragments to the nest. Atta colonies have a special soldier caste, formed by very large workers with strong mandibles, which make them have big heads with small brains.

Winged Sexual Individuals The sexually active individuals are born with transparent wings that allow them to engage in the nuptial flight, at the beginning of the rain season, where they copulate. Males die shortly after a single copulation. Once the winged female is inseminated, she lands on the ground, sheds her wings, looks for an appropriate sandy spot, and starts digging her initial nest. Often winged individuals are found inside the nest. These are virgin males or a queen that failed to swarm or will do so in the future. Virgin females in addition have much smaller gasters compared to their physogastric mothers. Males have much smaller heads than females. Males show little activity and their main role is transferring their sperm to the female’s spermatheca.

The Super-Organism In a given leaf-cutter ant colony we generally find only a single queen and her daughters, the workers. Thus, a colony is a family unit. The coordination between the members of a colony-family is so tight that some authors consider the colony to be a superorganism. That is, each individual acts to optimize the adaptive value of the colony rather than itself. The queen dedicates herself to produce eggs, the gut of the larvae and that of workers works like a communal digestive system, the foragers work as the movable extremities of the colony providing the required food, and the glandular secretions of all individuals mingle so as to produce a characteristic colony odor. Thus, the colony has properties that are known to characterize an organism. This is especially true when we look at the systems regulating the temperature and humidity of the nest.


The Uninvited Guests A leaf-cutting ant colony hosts a number of other animals. They range from invertebrate ectoparasites to vertebrates such as snakes, lizards and birds. They normally feed on the brood and/or use the nest as shelter. Reptiles especially profit from the nice temperature in a leaf-cutting ant nest, which is suitable for their eggs. That is certainly the case with the snake Elapomorphus lemniscatus (family Boidae) which is a frequent visitor of Acromyrmex nests. Once inside the nest, the reptile houses in a fungus chamber, eats the ant’s larvae, and exits the nest only when searching for a mate. Beetles, spiders, isopods, flies, collembolans, mites and other arthropods are known to live inside the ants’ nest. A large number of these ectoparasites live in the refuse chamber where they feed on dead ants and other refuse of the colony.

The Nest Atta Nests The nests of the ants from the genus Atta are among the largest and more complex known among insects. A typical nest may occupy a subterranean space of 20 m in diameter and 5 m in depth. It consists of interconnected galleries leading to chambers where ants cultivate their symbiotic fungi. Other galleries lead to the surface and are used to regulate the flux of fresh air so as to maintain the temperature, carbon dioxide concentration and humidity constantly at the optimum inside the nest. A large chamber is used to dispose of the colony’s waste which consists mainly of dead fungus and dead ants. This chamber produces heat and carbon dioxide that allows for a better regulation of the colony’s climate. Other galleries lead deep into the soil for access to the ground water. Galleries leading to the surface end beneath an earth mound with a crater, allowing the exit and entrance of workers. These mounds work as chimneys, helping to regulating

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the flux of fresh air and stopping running water from flooding the nest after torrential rains. Often workers seal the nest entrances with dry leaves and earth, especially when fighting other colonies. Some underground galleries lead up to 200 m from the nest to the colony’s foraging areas. Each Atta species builds nests with its own characteristics. For example, Atta colombica has no refuse chamber but throws its rubbish outside the nest. The form of the mounds with craters depends on the soil’s texture. The depth of the nest is also dependent on soil conditions; for example, nests are shallower in more humid areas.

The Nests of Acromyrmex and Trachymyrmex Nests of Acromyrmex species have variable architecture, depending on the species that builds it. Acromyrmex landolti builds nests with a single vertical gallery with nest chambers connected on the sides of the gallery. The vertical gallery can go as deep as 3–4 m. Acromyrmex octospinosus builds more superficial subterranean nests with many chambers and galleries connected in all directions. Acromyrmex coronatus sometimes builds superficial nests under accumulated dry leaves. These nests are often found in caves of dead tree trunks. Nests of Trachymyrmex species are less elaborate. They are subterranean but normally close to the surface and rather small compared to those of Acromyrmex and Atta (Figs. 28 and 29).

The Life Cycle Reproduction Leaf-cutting ants reproduce sexually, with copulation occurring during the nuptial flight. Normally a virgin queen mates with several males. Nuptial flight occurs at the beginning of the rainy season. After the first heavy rain, thousands of winged individuals start flying from all affected nests in an area. They fly

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new queen flies to the ground, sheds her wings and starts looking for an appropriate site to excavate a nest. Queens also reproduce asexually; non-fertilized eggs will produce haploid males (as are all hymenoptera, these ants are haplodiploid).

The Birth of a Colony

Leaf-Cutting Ants (Formicidae: Myrmicinae: Attini), Figure 28 Nest of Atta laevigata.

Once the recently fertilized queen has found an adequate site (often next to a small tree), she starts digging using her mandibles to remove earth. She digs a small gallery about 15 cm long leading to a small chamber about 7 cm wide. After digging is completed, she seals the nest entrance. In the chamber she lays some unfertilized eggs upon which she deposits the mycelium of the fungus she has taken from her mother’s nest, stored in a cavity in her mouth. If available, roots are also used as a substrate for the fungus. Then she lays her first fertilized eggs. The first larvae that emerge are fed with special unfertile “trophic” eggs produced by the queen. Eventually small “nanitic” workers emerge. During that period, the queen survives on her fat reserves and by metabolizing her wing muscles, now useless. Once the first nanitic workers emerge, they open the nest entrance and start foraging for leaves, flowers, insect droppings, seeds, etc., to feed the fungus. After this initial phase, larger workers emerge capable of cutting fresh leaves.

The Life Cycle of a Worker

Leaf-Cutting Ants (Formicidae: Myrmicinae: Attini), Figure 29 Acromyrmex landolti (drawing by Eduardo Perez).

normally in the early evening and concentrate in a given space several meters above the ground. As males die shortly after mating, dead bodies of males that have copulated rain to the ground, just under the visible swarm. Once successfully inseminated, the

Leaf-cutting ants have four phases in their life cycle: egg, larvae, nymph and adult. The white larvae feed mainly on the symbiotic fungus. They have very little mobility. After several molts, the larvae initiate its metamorphosis without spinning a cocoon and eventually emerges as an adult worker. The amount of food ingested during the larval stage will determine the final size of the worker, as adult workers stop growing. Young workers have a lightly pigmented soft cuticle, whereas older ones are darker. Adult workers have


different nutritional requirements than larvae do; they feed mainly on plant sap because their protein requirement is less than that of the larvae, which mainly feed on the fungus.

The Life Cycle of a Colony The colony starts with the birth of the first nanitic workers. During the first few years, the colony grows continuously in number of workers and in the space occupied by the nest. During that period, workers forage every day, except when it is raining copiously, and feed their fungus, which occupies ever more chambers which must be prepared by the workers. When the colony reaches maturity (4–6 years after being initiated by the queen for Atta, and less for Acromyrmex and Trachymyrmex), the colony produces winged individuals that accumulate in the nest until the initiation of the next rainy season, when they will leave the nest for their nuptial flight. We know little of how the leaf cutter ant colony produces winged females instead of workers, or how the queen decides to fertilize an egg with sperm, producing female offspring, or lay unfertilized eggs that will produce males. It is likely that these ants use hormones for this purpose, as bees do, but little is known for leaf-cutting ants. After a few nuptial flights, the colony is left without winged individuals and with few workers. The colony then has the whole year to again build its workforce, forage for food to grow its fungus, and eventually produce a new batch of individuals capable of sexual reproduction. This cycle is repeated until the old queen dies, which may take several decades.

Communication Pheromones The most common communication system between workers of leaf-cutting ants consists of volatile chemicals or odors called pheromones. These ants

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produce their pheromones through a series of exocrine glands located in different parts of their body. Each of these glands produces a specific secretion composed of a mix of chemicals which are used to communicate information between workers. These multicomponent pheromones are perceived through the insect’s antennae. Some pheromones are detected only upon contact of the antenna with the substrate containing the pheromone; these are called contact pheromones. For example, larval recognition in leaf-cutting ants seems to be achieved using contact pheromones that are located on the cuticle of the larvae.

Alarm Pheromones Leaf-cutting ant workers produce an alarm pheromone in their mandibular glands. This pheromone is composed of highly volatile compounds that disperse rapidly in the air and alarm nestmates up to distances of 60 cm. This same pheromone helps workers and soldiers to orientate to the source or location that caused the alarm, thus helping to coordinate cooperation in defense. This coordination can be very fast and effective when fighting other ant colonies or when deterring an intruder. The compounds of this pheromone are absorbed on the cuticle of these insects, thanks to the cuticular hydrocarbons that cover the insect’s surface. There, the alarm pheromone serves as an individual recognition signal, helping ants to differentiate between nestmates and intruders.

Recruitment Pheromone Another well studied pheromone is the recruitment or trail pheromone. This pheromone is produced in the poison gland located in the gaster. Workers lay trails using this pheromone when returning from a palatable food source. The less volatile compounds in the pheromone serve as orientation cues, whereas the more volatile ones regulate the amount of new workers recruited to the trail, which in turn will

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depend on the quality and quantity of food to which they are recruited. Some of the compounds of this pheromone, isolated from leaf-cutting ant species, are 4-metyl-2-pyrrol-carboxilate for Atta laevigata, Atta cephalotes, Acromyrmex octospinosus, and 3-ethyl-2,5-dimethyl-pyrazine for Atta sexdens rubropilosa and Acromyrmex niger.

Territorial Pheromones These are used to mark the colony’s territory using a secretion from the Dufour’s gland. Workers on territories marked by their colony are more aggressive and fight longer, whereas workers over territories of a foreign colony try to escape. During ant wars, many small workers swarm outside their nest to mark the surroundings of their nest entrance and the battlefield, whereas larger workers engage in combat. These combats can last weeks if the food source they are defending is especially scarce or attractive. This pheromone helps achieve the harmonious cohabitation of neighboring colonies of similar size, which seems to be the norm in nature.

Individual Recognition Leaf-cutting ant workers recognize their nestmates and differentiate them from foreign ants, even if they are of the same species. They achieve this by detecting odors absorbed on the cuticle. These odors mainly come from the mandibular alarm pheromone. This system allows them to recognize individuals even at a distance, and is also used to recognize nestmates from different parts of the nest.

Other Pheromones Other pheromones are less well known. The queen is recognized as such by pheromones, and so are the larvae. Leaf fragments are marked using the Dufour’s gland, probably to ascertain the colony’s

property and to help detect it when workers drop it from the trees. Other communication systems remain to be discovered.

Visual Communication Although known from other ants, nothing is known for leaf-cutter ants.

Communication by Sound Leaf-cutter ants have a stridulatory apparatus between the gaster and the second petiole. This apparatus consists of a stridulated cuticular surface on the dorsal part of the gaster and a cuticular tooth extruding from the petiole that serves as a bow producing vibrations when gliding over the stridulated surface. The ants produce rhythmic ultrasounds with this apparatus by vibrating and elevating their gaster. The sound is barely perceived by some humans. The ants use this sound to guide workers toward branches on trees that need leaf-cutters. They also stridulate when buried, guiding workers to dig in their direction. The sound is transmitted over solid substrate and is perceived thanks to special receptors at the end of their legs.

Trophalaxis and Antennal Contacts Workers exchange liquids through their mouthparts. They do this after contacting the other ant with their antennae. We do not know what information they are transmitting with these behaviors but they might transmit information about the quality of food.

Foraging Leaf-cutting ants have especially sophisticated foraging behaviors. They use trunk trails that they


maintain free of leaves and obstacles, facilitating their movement from the nest to the foraging areas. From this trunk trail, smaller trails lead to the plants they harvest. Scout ants use the same trail system but eventually leave it to explore new terrain. When finding a palatable food source, they return to the nearest trunk trail, leaving trail pheromone behind. Foragers might cut a leaf fragment and carry it through the trail system to the nest. Alternatively, they might do it in stages; some workers cut the leaves and let them drop from the tree, or just carry the leaves to the nearest junction, where other workers collect the leaf fragments and carry them to the nest entrance, where still other workers remove the superficial waxes from the leaves and carry the clean leaves inside the nest, where other workers cut them into fine pieces to feed the fungus. Very small or minima workers are often seen climbing on leaf fragments that are carried by larger workers. The minima help fend off flies from the family Phoridae and other parasites that attempt to attack the carrying worker or enter the nest via the leaf fragment. Older workers remove dry leaves, dead ants and dry fungus from the nest chambers and drop it in the refuse pile.

The Decision Making System The colony has to coordinate its efforts in order to forage efficiently. Not all ants are required at the same place at the same time. Specifically, in the case of recruitment to food, leaf-cutting ants use a decision making system that is different from that used by all other ants studied and which resembles the system used by termites. It works as follows: a scout discovering food will return to the nest or the trunk trail while laying a pheromone trail. The concentration of pheromone on the trail will depend on the quality of the food. Workers encountering this trail, according to their motivation for food, will follow the new trail. On their way back, they will reinforce the pheromone trail but in such a way that the total concentration of pheromone is roughly constant. They will not just

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add their pheromone onto that of others (as done by Solenopsis geminata, for example), but will restrain from adding pheromone if enough of it is already on the trail. In this way, the concentration of pheromone on the trail will not depend on the amount of ants laying trails or returning from the food source but only on the quality of the food. This system allows leaf-cutters to recruit to various different food sites at the same time.

Orientation Foraging scouts need to find their way back to the nest. They achieve this by integrating various keys or environmental signals when foraging and homing. We know that they can use polarized light, visual cues, spatial memory, olfactory cues and tactile cues. They might possibly also use gravitational cues and the earth’s magnetic field. Each species seems to have its own hierarchy in which these cues are used in actual orientation in the field.

Defense Organisms need to defend themselves against predators and parasites in order to increase their odds for survival. Leaf-cutter ants possess no functional sting but they do secrete a toxic fluid from their anal region which they deposit onto enemy combatant ants. This secretion dries or polymerizes quickly, helping to immobilize the affected worker. It also seems to contain neurotoxic substances and volatiles that attract other ants. Large workers and soldiers also use their mandibles to cut wounds on molesting vertebrates and then add irritant secretions to the wounds. The mandibles can cut appendages from invertebrate enemies or even cut them into pieces. Another form of defense is using cryptic behavior, including cessation of all movement until the danger has passed. This behavior is often used by lone foraging scouts. The thick, hard cuticle and the spines over the thorax help the insect to avoid being eaten by

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predators such as lizards, birds and spiders. In addition, the secretion of the metapleural gland is spread all over the body of these insects, helping to fend off fungi, bacteria and other potential illnesscausing agents. The main predators of these ants are spiders, armadillos and anteaters, which feed copiously on them.

Ecology Leaf-cutting ants are only found in the neotropics. They might have an important effect on plant growth, on occasion achieving pest status. Densities of up to 60 adult Atta nests per hectare, or hundreds to thousands of Acromyrmex nests per hectare, can cause serious harm to plantations and crops. On the other hand, the large accumulation of organic material inside the nest, once the queen and the colony die, makes it a formidable substrate for plant growth. In nutrient poor savannas, old collapsed Atta nests are colonized by trees and shrubs, forming forested islands. It is the occasional status as agricultural and forestry pests that has made leaf-cutters most famous. Leaf-cutters with the highest economic importance as pests are all Atta species and some Acromyrmex species. An adult Atta laevigata colony, for example, may cut an average of 5 kg of plant material each day. They target especially young plant tissue, which can be especially damaging to the plants. Estimates of the economic damage caused in the Americas by these ants are close to a hundred billion US dollars per year (Figs. 30 and 31).

Control of Leaf-Cutting Ants There are three basic methods for reducing the populations of these pest ants: (i) Stopping the ants from accessing the plant. Asphalt or other sticky greases painted at the base of tree trunks, plastic or rubber rings that retard ants from reaching the plants, or water barriers that deter the access of these ants are useful ways of dealing

with this pest. (ii) Direct control, killing the ants with insecticides. For large nests this might be difficult and expensive. Fogging and powder pumps may help to get the insecticide inside a nest. (iii) Indirect control, using poisoned but attractive baits, is the most efficient way known to manage large areas with this pest. Attractants (such as citrus pulp) mixed with slow acting insecticides, allow the foragers to carry the poison into the nest so that it is distributed to all chambers by the workers before it starts killing the insects.

References Cameron R, Currie CR, Scott JA, Summerbell RC, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–704 Cedeño A (1984) La ecología de los bachacos. Fondo Editorial Acta Cientifica Venezolana, Caracas Chapela IH, Rehner SA, Schultz TR, Mueller UG (1994) Evolutionary history of the symbiosis between fungusgrowing ants and their fungi. Science 266:1691–1694 Herman HR (1982) Social insects, vol 4. Academic Press, New York, NY, 385 pp Hernandez JV, Lopez H, Jaffe K (2001) Nestmate recognition signals of the ant Atta laevigata. J Insect Physiol 48:287–295 Jaffe K (1984) Negentropy and the evolution of chemical mass recruitment in ants. J Theor Biol 106:587–604 Jaffe K (1987) The evolution of agonistic communication systems in ants. Exp suppl 54:295–311 Jaffe K, Howse PE (1979) The mass recruitment system of the leaf-cutting ant Atta cephalotes. Anim Behav 27:930–939 Jaffe K, Villegas G, Colmenares O, Puche H, Zabala N, Alvarez M, Navarro JG, Pino E (1985) Two different decision making systems in ants. Behavior 92:9–21 Mayhe A, Jaffe K (1998) On the biogeography of the Attini. Ecotropicos 11:45–54 Vilela E, Jaffe K, Howse PE (1987) Orientation in leaf-cutting ants. Anim Behav 35:1443–1453 Weber N (1972) The gardening ants. American Philosophical Society, Philadelphia, 142 pp Wheeler WM (1965) Ants: their structure, development and behaviour, 4th edn. Columbia University Press, New York, NY, 663 pp Whitehouse M, Jaffe K (1996) The ant wars: combat strategies, territoriality and nest defense in the leaf-cutting ant Atta laevigata. Anim Behav 51:1207–1217 Wilson EO (1971) The insect societies. Belknap Press, Harvard University, Cambridge, MA, 548 pp


Leaf-Cutting Ants (Formicidae: Myrmicinae: Attini), Figure 30 Atta laevigata: (a) male, (b) queen, (c) worker, (d) soldier (drawings by Eduardo Perez).

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Leaf-Cutting Ants (Formicidae: Myrmicinae: Attini), Figure 31 Atta cephalotes transporting vegetation (photo by Scott Bauer, USDA).

Leaf-Footed Bugs Members of the family Coreidae (order Hemiptera).  Bugs

Leafhoppers (Hemiptera: Cicadellidae) Chris H. Dietrich Illinois Natural History Survey, Champaign, IL, USA Leafhopper adults and nymphs are active, jumping insects recognized by their piercing-sucking mouthparts and by the presence of four rows of enlarged, spinelike setae on their hind tibiae. Order: Hemiptera Infraorder: Cicadomorpha Superfamily: Membracoidea Family: Cicadellidae

Cicadellidae, the largest family of hemimetabolous insects and one of the largest families of plant-feeding insects, comprises nearly 25,000 described species and over 3,200 genera. their

great diversity may be due to a combination of their long (ca. 125 million years) evolutionary history, their association with a wide variety of flowering plants, and their success at occupying a broad range of habitats and climates. Their closest living relatives are the treehoppers and related families (Membracidae, Aetalionidae and Melizoderidae), and the relict southern hemisphere family Myerslopiidae. More distant relatives include the other two superfamilies of infraorder Cicadomorpha: Cercopoidea – the spittlebugs or froghoppers; and Cicadoidea – the cidadas. Leafhoppers occur in terrestrial habitats worldwide, wherever vascular plants are found. They are most diverse and abundant in the tropics; however, temperate grasslands, savannas and forests also harbor diverse leafhopper faunas and a few species inhabit high elevations and latitudes. A few generalist species occur worldwide and utilize dozens of plant species as hosts, but most species are associated with particular host plants and/or habitats and have relatively small geographic ranges. The oldest fossil Cicadellidae are known from the lower Cretaceous Period.

External Morphology Adult leafhoppers range from 2 to 30 mm in length and are usually somewhat cylindrical or wedge-shaped. Less commonly, species may be strongly flattened dorso-ventrally, greatly elongated, or globular in appearance. They differ from their close relatives, the treehoppers, because they lack a posteriorly produced pronotum and because (with a few exceptions) the setae of their hind tibia are enlarged and spinelike. Most leafhopper species are brown or green but many, particularly in the subfamilies Cicadellinae and Typhlocybinae, are strikingly marked with various color patterns. As in planthoppers (Fulgoromorpha), the head of leafhoppers is highly variable in shape, ranging from short to elongate,

Leafhoppers (Hemiptera: Cicadellidae)

from round to strongly flattened, and sometimes bears spines or other ornamentation (Fig. 32). The median ocellus is absent and the position of the two lateral ocelli, when present, is also highly variable and is one of the main features used to distinguish subfamilies. Other important differences among the major lineages are found in the wing venation, the arrangement of setae on the legs and the male and female genitalia. Although some leafhopper species are easily recognized by their distinctive shapes and color patterns, many groups contain species that closely resemble one another and are difficult to distinguish. In many genera, the most reliable morphological features for distinguishing species are the male genitalia.

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Life History and Habits Details of the life cycle vary from species to species. In general, the female inserts several eggs into the living tissue of the host plant. The eggs either remain dormant for a period ranging from a month to over a year, or they develop and hatch within a few weeks. The young, known as nymphs, feed on plant sap by inserting their beaks into the vascular or parenchyma tissues of the host plant and go through a series of five molts, reaching the adult stage after a period of several weeks. Adult males and females seek each other out for mating, locating each other through vibrational signals made by sound producing organs at the base of the abdomen called tymbals. Leafhopper songs are

Leafhoppers (Hemiptera: Cicadellidae), Figure 32 Leafhoppers (Cicadellidae): (a) Agalliopsis novella (Say); (b) Oncometopia alpha Fowler (the white patch on the forewing is a deposit of brochosomes); (c) Commelus comma (Van Duzee); (d) Attenuipyga platyrhyncha (Osborn); (e) Jikradia olitoria (Say); (f) Ulopa reticulata (Fabricius). (Photos by C. H. Dietrich.)

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transmitted through the substrate and, in most cases, are too faint to be heard by human ears without special amplifying equipment. As implied by their name, most leafhoppers are strong jumpers as both adults and immatures. The adults of most species are also strong fliers, but many species, particularly in arid environments, have the wings reduced or absent and are incapable of sustained flight. Most species are solitary as nymphs and adults, but a few species are gregarious and ant-mutualistic. Some of these, in turn, exhibit parental care (presocial) behaviorfemales guard their eggs and remain with the nymphs throughout their development. Another interesting aspect of leafhopper behavior is a phenomenon known as anointing, in which the leafhopper collects a special fluid secretion from the anus and spreads this secretion over the body using the legs. When the secretion dries, a residue of minute spherical granules called brochosomes remains and provides a hydrophobic coating to the integument. Brochosomes are produced in a specialized glandular segment of the Malpighian tubules. In the leafhopper tribe Proconiini, females of several genera store large globs of brochosomes on the forewings and use their hind legs to scrape the brochosomes onto their egg masses after oviposition.

Predators and Parasites Leafhoppers are attacked by a wide variety of predators, including birds, lizards, spiders, assassin bugs, robber flies and syrphid flies. Mymarid and trichogrammatid wasps parasitize the eggs; dryinid wasps, pipunculid flies, strepsipterans and epipyropid moths parasitize the nymphs and the adults.

Economic Importance Several leafhopper species are important agricultural pests, injuring plants either directly through

feeding, or indirectly through the transmission of plant pathogens. Among the most important are the aster leafhopper (Macrosteles quadrilineatus (Forbes)), the African maize leafhopper (Cicadulina mbila (Naude)), the potato leafhopper (Empoasca fabae Harris), the beet leafhopper (Neoaliturus tenellus (Baker)), the corn leafhopper (Dalbulus spp.), the green rice leafhopper (Nephotettix spp.), the glassy-winged sharpshooter (Homalodisca coagulata (Say)), and various grape leafhoppers (Erythroneura spp.).

Control Measures Control of injurious leafhopper populations is most often accomplished by using conventional contact insecticides. However, use of resistant plant varieties and cultural control (e.g., removal of crop debris used in overwintering) is effective for some species. The potential for biological control using entomopathogenic fungi or parasitoids is a topic of active research.

References Evans JW (1966) The leafhoppers and froghoppers of Australia and New Zealand (Homoptera: Cicadelloidea and Cercopoidea). Mem Aust Mus 12:1–347 Nault LR, Rodriguez JG (eds) (1985) The leafhoppers and planthoppers. Wiley and Sons, New York, NY, 500 pp Oman PW (1949) The Nearctic leafhoppers-a generic classification and check list. Mem Entomol Soc Wash 3:1–253 Oman PW, Knight WJ, Nielson MW (1990) Leafhoppers (Cicadellidae): a bibliography, generic check-list, and index to the world literature 1956–1985. CAB International, Institute of Entomology, Wallingford, UK

Leaf Insects Members of an order of insects Phasmatodea).  Walkingsticks and Leaf Insects

(order

Leaf-Miner Flies (Diptera: Agromyzidae)

Leafcutting Bees Members of the family Megachilidae (order Hymenoptera, superfamily Apoidae).  Bees  Wasps, Ants, Bees and Sawflies

Leaf-Miner Flies (Diptera: Agromyzidae) Stéphanie Boucher McGill University, Lyman Entomological Museum, Ste-Anne-de-Bellevue, Québec, Canada The Agromyzidae, also known as leaf-miner flies, is a large family of phytophagous flies. The family contains approximately 2,860 described species occurring from the tropics to the high arctic, although the majority of known species live in temperate areas of the Northern Hemisphere. There are still many more species of agromyzids to be discovered; as many as half the actual number of species may not yet be described.

Biology and Economic Importance Larvae of all species of Agromyzidae are internal plant feeders. Although they are best known as leaf-miners, many species feed inside other plant parts such as stems, roots, seeds and flowers, while a few species are gall inducers. There are about a hundred species of particular economic importance that may cause damage to cultivated crops and ornamental plants (see examples in Table 2). The degree of damage inflicted on plants may depend on the part of the plant being attacked, the plant’s growth stage at the time of infestation and more importantly, the size of the agromyzid population on the plant. Under normal conditions, agromyzids are naturally controlled by a large complex of hymenopteran parasitoids, keeping agromyzid populations

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below the economic threshold. Unfortunately, this natural balance has often been disrupted by the use of insecticides. This is because the agromyzids often have higher resistance to chemicals than the parasitoids. When present in large numbers, leaf-miners may affect the general health of the plant by reducing its photosynthetic capacity. They also cause aesthetic damage due to their highly visible feeding traces, reducing the commercial value of ornamental plants. For those commercially grown plants, the presence of only a few agromyzid leaf-mines is often enough to make a plant unmarketable. Stem-borers also cause considerable damage by affecting the vascular system of the plant, disturbing water and nutrient supplies. This is especially injurious when the larval feeding occurs in young plants or seedlings. Although most of the damage to plants is caused by the agromyzid larvae, the adult females may also injure plants by inserting their wellsclerotized ovipositor into the plant tissues (Fig. 33a). This is primarily for egg-laying purposes, but the females use these scars also as feeding sites, sucking plant sap through the punctures. These punctures increase the risk of infection of the plant by fungi and bacteria. Some agromyzid species feed on noxious and invasive plants, and are regularly considered as potential natural control agents for those plants. Unfortunately, many attempts at biological weed control using agromyzids have so far failed or encountered problems (Table 3).

Host Plants Agromyzidae have colonized a wide range of host plants including primitive lineages such as horsetails and ferns, but more importantly, over 160 families of flowering plants, including some economically important ones such as the Poaceae (rice, wheat, corn, barley, etc.), Fabaceae (beans, peas, soybeans, lentils, etc.), Solanaceae (potatoes, tomatoes, pepper, etc.) and Asteraceae

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Leaf-Miner Flies (Diptera: Agromyzidae), Table 2 Examples of some important agromyzid pest species Species

Host plants

Larval habits

Localities

Ophiomyia simplex– Asparagus miner

Asparagus (Asparagus officinalis)

Root and stem miner

Western Europe, North America

Ophiomyia phaseoli– Bean fly

Various species in family Fabaceae including snapbeans (Phaseolus vulgaris), soybeans (Glycine max), cowpeas (Vigna unguiculata), garden pea (Pisum sativum)

First instar larva as leaf-miner. Older larva bores into the stem. May also mine towards the roots in seedlings or highly infested plants

Southern Asia (China, India, Indonesia), Hawaii, Australia, East Africa

Melanagromyza obtusa– Pigeon pea pod fly

Various species in family Fabaceae, especially pigeon peas (Cajanus indicus)

Eggs laid inside pods. Larvae are seed feeders

Southeast Asia, Papua New Guinea. Also recorded in Neotropical region (Guadeloupe)

Agromyza frontella– Alfalfa blotch leafminer

Fabaceae: Alfalfa (Medicago Leaf-miner sativa) other species of Medicago. Also Melilotus spp.

Europe, Afghanistan, Israel, North America

Liriomyza sativae– Vegetable leafminer

Polyphagous. Nine plant Leaf-miner families including Cucurbitaceae (cantaloupe, cucumber, squash), Fabaceae (pigeon pea, alfalfa, lima bean and others), Solanaceae (pepper, tomato, egg-plant, potato), also ornamentals (e.g., Chrysanthemum)

Cosmopolitan

Liriiomyza trifolii– American serpentine leaf miner

Highly polyphagous. Approximately 400 host species known from 25 families. Attack various cultivated crops such as onions, beans, potatoes, tomatoes, celery, ornamentals (e.g., Chrysanthemum)

Leaf-miner

Cosmopolitan. Spread around the world mainly with cut flowers. Restricted to greenhouse in temperate regions

Liriomyza huidobrensis– Pea leafminer

Polyphagous. Known from 14 plant families. Attack various cultivated crops such as beets, peas, beans, lettuce, onions, tomatoes, potatoes. Also some ornamental plants

Primarily leaf-miner. May feed occasionally on outer surface of young pods

Central and South America. Expected in all tropical and subtropical regions of Europe, Asia and Africa. Restricted to greenhouse in temperate regions. So far absent from North America (previous records represent cryptic species Liriomyza langei)


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Leaf-Miner Flies (Diptera: Agromyzidae), Table 2 Examples of some important agromyzid pest species (Continued) Species

Host plants

Larval habits

Localities

Chromatomyia horticola– Garden pea leafminer

Highly polyphagous. Known from 35 plant families, including many cultivated plants (onions, peas, cabbages, alfalfa), and ornamentals

Leaf-miner

Europe, Africa and Asia

(lettuces, artichokes, chrysanthemums, etc.). There are no species of Agromyzidae that are known on mosses and very few species have been reared from gymnosperms: one record is from Tropicomyia atomella, an agromyzid species that forms leaf mines on Gnetum sp. in Malaysia and further records consist of feeding channels in wood of gymnosperms that are possibly caused by agromyzid larvae. The host plants are known for approximately 50% of the described agromyzid species. Most agromyzid species show a high degree of host specificity. These are known to feed on plants from a single genus (monophagous) or from multiple genera in the same family (oligophagous). Only a few species (color>shape. Other pollinators, including bumblebees and butterflies, also show the ability to rapidly learn to associate flower colors and shapes with the presence of food rewards. Among foliage feeding insects (e.g., grasshoppers), learned associations between odors and major essential nutrients, and between particular color/light intensity cues and high-quality food, have been documented. However, there are examples of specialist insects learning, particularly among parasitoids

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and specialist butterflies that require specific hosts for their offspring. For example, Microplitis croceipes, a specialist parasitic wasp, uses plant volatiles released from the plant following feeding by caterpillars, which are hosts of the parasitic wasp. Its response to these volatiles is not, however, innate. Rather, an association of the plant volatile (the CS), as a result of damage to the plant following feeding by its caterpillar host (the US), is learned after a few successful oviposition events. Learned associations between a neutral stimulus and a bad feeding experience are particularly valuable for insects because they provide a reliable and rapid mechanism for avoiding foods that contain toxins or unsuitable nutrients. However, examples of learned aversions to foods by insects are rare. Part of this may be because aversion learning tends to occur only in generalist herbivores, as feeding in specialist insects is driven by innate behavior. Additionally, demonstrating learned aversions in insects in the field can be difficult, so a laboratory approach is often required. Nonetheless, examples of learned aversions in insects do exist, particularly among generalist grasshoppers. For instance, two laboratory experiments have revealed that the generalist grasshopper Schistocerca americana, uses aversion learning to regulate the intake of an unsuitable dietary nutrient that cannot be tasted. In an initial experiment, grasshoppers were allowed to feed on spinach, which contains the unsuitable nutrient. After they finished eating, the unsuitable nutrient, or a closely related suitable one, was injected with a syringe directly into their hemolymph (blood). They were then allowed to take a second meal. Interestingly, those injected with the unsuitable nutrients took significantly shorter second meals on spinach (on average 3 sec) than those receiving the suitable nutrient (on average 90 seconds), suggesting that the unsuitable nutrient was detected post-ingestively, and that learning was occurring centrally rather than peripherally. The second experiment, using artificial foods with manipulated nutrient profiles and added flavors, indicated that the grasshoppers were learning to associate the taste of the food with the presence of the unsuitable

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nutrient. This example, plus others that show grasshoppers develop aversion responses to foods after being injected with various toxins, suggest that aversion learning may have an important role in the maintenance of dietary mixing. In addition to securing food, insects must also find and choose mates. Although it is generally assumed that mate location and acquisition is innate and unresponsive to change through experience, the behavior of male apple maggot flies, Rhagoletis pomonella, seems to suggest otherwise. The males spend time on host fruit (either apples or hawthorns) waiting for females to arrive so they can mate. Research has shown that prior positive experience with females on one of the two host fruits influences the time a male will spend on the two fruits. That male insects may learn to assess the characteristics of females has also been suggested. For example, males of sacrophagous Drosophila learn to distinguish between females in particular physiological states, and the male Lasioglossum bees have been shown to learn characteristics of individual females. Where parental care is practiced, insects also must be able to recognize their offspring and feed them accordingly. For species of digger wasps that provide food to several burrows at once, evaluating food demands on an individual basis can be important because offspring may be at different developmental stages (newly hatched to nearly pupating). To assess food requirements, a mother will visit each burrow before setting off to gather food and, over the course of the day, will provide the appropriate amount of food to each burrow. However, experimental manipulation of the larva belonging to one species of digger wasp showed that there is considerable inflexibility in this system. When the larva in the burrows were exchanged following the female’s morning inspection, the amount of food that the mother provided to each larvae upon returning to each burrow was shown to be based not on the current occupant, but on the individual that had been in the burrow during the morning inspection period. Learning to escape from danger (specifically predators) would also be highly beneficial for insects,

but when danger is sufficiently predictable and can be recognized innately, the use of sign stimuli should be favored over associative learning. Because of this, examples of learning to avoid danger are rare. Some butterfly larvae have an innate response to the sound of hunting wasps, and quite a few moths are able to counteract the echolocation used by bats. Also, in the laboratory, bees have been shown to associate sound with impending shock, but within a more natural situation, no examples of learning to associate sounds with danger are documented. The limited resolution of the insect compound eye greatly hinders visually based learning of danger, and no evidence exists to suggest that shapes associated with danger can be learned. At least one example of olfactory-based learning of danger is known. In a laboratory experiment, Drosophila maggots, using associative conditioning, learned to avoid electrical shocks associated with an odor. Some insects have homes (either localized like a nest, or diffused like a home-range) and learning may aid in navigating to, from and around their homes. Most insects use innate mechanisms when navigating through their home territories, but the role of learning appears to be an important factor in calibrating their movements. Bees, for instance, appear to learn the direction of the sun’s movements (left to right or visa versa) before they begin their foraging, and their memory seems to be irreversible. Learning related to navigation in bees is thought to depend on two alternative systems. If large, unambiguous landmarks are visible, the sun’s course relative to these objects is memorized. If large objects are not available, the sun’s rate of movement over the previous 40 minutes is measured and that value is used to calculate the change in the solar azimuth. Among experienced bees, large and unambiguous landmarks may be used in preference to celestial cues.

When Should Insects Learn? In general, insects should learn in situations where the information necessary for guiding behavior is

Learning in Insects

highly predictable, or too complex for innate responses to handle. That innate responses should be favored over learning makes sense because learned information is not as efficient and as reliable as innate information. It is also true that learning takes time, and mistakes (particularly during the initial stages of learning) are inevitable. Interestingly, learning is most favored in environments that are described as being “predictably unpredictable.” This concept is best understood by viewing predictability along a continuum, with 0 being completely unpredictable and 1 being completely predictable. Using feeding as an example, specialist insects live in a predictable world because they only feed on a single plant species over their lifetime (a predictability value near 1). As a result, they will have no need to learn about their food since it is always the same. Likewise, at the other end of the scale, a generalist insect that feeds on a wide range of foods, but that never encounters the same food twice (a predictability value near 0), would never have the opportunity to learn since its experience would never be repeatable. This latter situation is unlikely to occur, and, for most generalist insects, remembering a bad experience with a toxic plant would be beneficial. However, if the plant on which the bad experience occurs is rare, there is limited opportunity to reinforce the learning experience. Where unsuitable foods occur with regularity, the combination of learning and sampling foods before taking large meals is one way in which highly mobile, generalist insects can increase the speed with which foraging decisions are made. However, learning related to food acquisition is probably only practiced in highly mobile insects that are in the latter stages of larval development or in the adult stage. Among generalist grasshoppers, for instance, learning may not be important during the first few instars because they are likely to spend the majority of their early life feeding on only a small number of plants.

What Constrains Learning? The brain is the central processing center of information for all animals, including insects, and is

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responsible for transmitting signals that coordinate all behaviors (Fig. 39). However, the small size of the insect brain may place a great constraint on learning ability. The brain of an insect is split into three main regions (the protocerebrum, deutocerebrum and tritocerebrum) and it is generally thought that learning abilities in insects are in some way related to the size of a region of cells called the mushroom bodies, or corpora pedunculata. These bodies are given their name based on the shape of the five identifiable cell types. The uppermost region of these bodies consists of a flattened cap of neuropiles, called Kenyon cells. Below it lies the calyx, which has a peduncle running from it that eventually splits into two or three lobes, which are designated α, β and γ. The mushroom bodies, which occur at the sides of the pars intercerebralis in the protocerebrum, are small in the Collembola, Heteroptera, Diptera and Odonata, are largest in the social insects (where most examples of learning are documented), and are of intermediate size in Coleoptera, Orthoptera, Blattodea, Lepidoptera and sawflies. Researchers have shown that changes take place in the mushroom bodies with age and experience, but perhaps more interestingly experiments with Drosophila and Apis indicate that mushroom bodies also increase with experience, and are involved in associative learning (Fig. 39). A second constraint on learning relates to the idea that intelligence is modular and that some associations formed between stimuli are more readily learned than others. For instance, experiments with rats show that illness following a meal is more easily associated with the taste and/or smell of the food that caused the illness than is a burst of light or a loud noise given at the time of the meal. This type of constraint may arise because taste and olfactory systems are intimately intertwined with digestion, whereas hearing and vision are not. That such constraints on learning occur makes sense because, evolutionarily, perceptual systems that respond to the most ecologically relevant stimuli in a rapid and reliable manner should be favored.

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Learning in Insects optic lobe Kenyon cells calyx peduncle α lobe

corpus pedunculatum (mushroom body)

β lobe

Learning in Insects, Figure 39 The insect brain is divided into three main regions: the protocerebrum, deutocerebrum and tritocerebrum. The mushroom bodies, found in the protocerebrum, are thought to be a primary region of the insect brain associated with learning. This body consists of the Kenyon cells, calyx, peduncle and two or three lobes running from the peduncle. It has been suggested that the size of the mushroom bodies (specifically the number of neuropiles found in this region of the brain) is positively correlated with learning abilities.

Can Learning Evolve? If learning is to evolve in insects in an adaptive manner it supposes that genetic-based variation in learning exists, and differences in learning are associated with differences in fitness. Clearly, insect populations show genetic variations, and in Drosophila and Phormia flies, existing genetic variations within strains have been used to analyze the physiology of learning. Variation in learning has also been documented in honeybees and it has been shown to be heritable. In phytophagous insects, however, little information on genetically based variation in learning exists. Since documented cases of variation in learning are rare, it is not surprising that so little is known about the extent to which such differences translate into differences in fitness. One study has suggested that learning in generalist grasshoppers translates into higher growth rates, but this study only explored performance over a single instar. Because evolutionary fitness is defined as the ability of an individual/s offspring to survive and reproduce, there are significant logistical problems associated with demonstrating a fitness enhancement associated with learning. Clearly, more work in this field is needed, and a larger

number of taxa need to be examined before any conclusive judgments can be made on the evolution of insect learning.

Conclusions Learning in insects probably occurs with a greater frequency than is appreciated. Of the two main types of learning normally recognized, associative learning is probably easier to document, but operant learning (e.g., learning to handle food, to negotiate different types of substrates, etc.) probably occurs with greater regularity and is likely to take place over the entire life of an insect. Much remains to be discovered about insect learning, particularly the neural-basis of learning and the extent to which learning in insects evolves, but new technologies and methodologies are generating rapid advances. As model systems to explore learning, insects offer many great advantages, and their potential for contributing to a greater understanding of the mechanisms animals use to aid in learning provides a rich opportunity for future research.  Learning in Insects: Neurochemistry and Localization of Brain Function

Learning in Insects: Neurochemistry and Localization of Brain Function

References Bernays EA (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annu Rev Entomol 46:703–272 Manning A, Dawkins MS (1998) An introduction to animal behaviour. Cambridge University Press, Cambridge, UK Papaj DR, Lewis AC (1993) Insect learning: ecological and evolutionary perspectives. Chapman and Hall, London, UK Papaj DR, Prokopy RJ (1989) Ecological and evolutionary aspects of learning in phytophagous insects. Annu Rev Entomol 34:315–350 Shettleworth SJ (1998) Cognition, evolution and behavior. Oxford University Press, Oxford, UK

Learning in Insects: Neurochemistry and Localization of Brain Function Fred Punzo University of Tampa, Tampa, FL, USA Research studies conducted over the last decade on the cellular and molecular mechanisms associated with learning (behavioral plasticity) have led to several generalizations: (i) learning involves changes in neural pathways that are correlated with alterations in synaptic efficacy; (ii) training procedures result in changes in membrane currents; (iii) learning involves second messenger systems; and (iv) behavioral plasticity is associated with changes in macromolecular synthesis within the central nervous system (CNS). These macromolecules include RNA and protein. Proposed cellular mechanisms for learning include reverberating circuits, modification of dendritic processes and synapses, voltage-dependent membrane channels and use-dependent modification of neural pathways. Although these ideas have been applied to both the vertebrate and invertebrate CNS, invertebrate models are particularly well suited for this type of analysis owing to their relative simplicity in contrast with vertebrate systems. Invertebrates that have been used in studies on the cellular and neurochemical basis of learning and memory include gastropod molluscs, decapod

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crustaceans, theraphosid spiders and insects. Specific neurochemical changes that accompany learning include an increase in RNA and protein synthesis, a decrease in cholinesterase activity and changes in biogenic amines and amino acids. These neurochemical events have also been used to identify specific anatomical loci within the arthropod brain (cerebral ganglion) that have been implicated in the mediation of the learning process. Inhibition of protein synthesis within the CNS was found to impair learning in vertebrates as well as orthopteran and coleopteran insects and theraphosid spiders. It was also found to impair the innate phototactic behavior of tenebrionid and passalid beetles suggesting that even rigid (closed) behavioral programs are dependent upon ongoing neurochemical events. This elucidation of the neurochemical correlates of learning and memory in arthropods has occurred in conjunction with advances in behavioral ecology and neuroethology. The importance of learning in many diverse animal groups has been widely discussed. The ability of an organism to modify its behavioral response to varying environmental conditions is often essential to survival and can increase overall fitness. Learning encompasses adaptive changes in individual behavior that increase survival capacity and occur as the result of previous experience. Insects and other arthropods have traditionally been viewed as creatures of instinct characterized by relatively rigid, stereotyped behavioral patterns. Nevertheless, although the behavioral repertoires of many insects are endowed with a rigidity of structure characteristic of Tinbergen’s concept of Fixed Action Patterns (FAPs), there have been many studies demonstrating behavioral plasticity in insects and other arthropods. Furthermore, environmental parameters can influence the neuroarchitecture of specific brain regions in insects. The number of neuronal fibers in the brain of adult Drosophila melanogaster varies according to age, sex, early experience and olfactory conditioning.

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Traditional categories of learning such as habituation, avoidance learning, trial-and-error learning, association and latent learning, and classical conditioning have been demonstrated in insects. The capacity for correcting behavior, imprinting and olfactory conditioning have been reported as well. More recently, investigators have been primarily concerned with the adaptive significance of learning. The contributions of behavioral ecologists and neuroethologists have made it clear that any analysis concerning the adaptive significance of behavior must take into account: (i) the evolutionary history of the behavior; (ii) processes related to the development and/or modification (learning) of the behavior under present conditions; and (iii) the environmental setting in which the behavior occurs. The ability of an organism to learn can also be used to obtain answers to questions concerning how the organism perceives its world, the role of CNS integration in the learning process (molecular mechanisms of learning), and what specific regions of the CNS are involved in the consolidation and storage of experiential information (localization of brain function). This contribution summarizes some of the recent work concerning the neurochemical correlates of learning and localization of brain function in insects.

Learning and Development: Brain RNA Synthesis and the Retention of Learning Through Metamorphosis in Holometabolous Insects The insect brain (cerebral ganglion) (Fig. 40) is divided into three major anatomical divisions: protocerebrum, deutocerebrum and tritocerebrum. The tritocerebrum innervates the muscles and sensory organs of the mouthparts. The deutocerebrum innervates the antennae which contain a rich array of chemo- and mechano-receptors. The protocerebrum innervates the optic lobes of the compound eyes and the ocellar nerves, and also contains several major ganglionic centers including the protocerebral bridge, central body

onv c

cp med Lob

pb cb a

b

L aL

fnv cc

Learning in Insects: Neurochemistry and Localization of Brain Function, Figure 40 Diagrammatic representation of a frontal view of the insect brain. aL, antennal lobe; a, alpha lobe of corpora pendunculata; b, beta lobe of corpora pedunculata; cb, central body; cp, corpora pedunculata; c, calyx; fnv, frontal nerve; cc, circumesophageal connective; L, lamina of optic lobe; Lob, lobula of optic lobe; med, medulla of optic lobe; onv, ocellar nerve; pb, protocerebral bridge.

and the corpora pedunculata (mushroom bodies) (Fig. 40). Insects exhibiting complete metamorphosis (Holometabola) are characterized by distinct egg, larval, pupal and adult life cycle stages. During pupation, some larval tissues and organ systems undergo an extensive breakdown and are eventually reorganized to form the adult animal. As a result, holometabolous insects provide an excellent model for an analysis of the effects of development and CNS reorganization on learning and memory. The degree to which a behavioral response learned during the larval stage is retained by adults can be used to assess the extent of CNS reorganization during development. The retention of an associative learning task following metamorphosis was reported for the locust (Hemimetabola), Locusta migratoria.


However, the degree of CNS reorganization exhibited by hemimetabolous insects does not compare with that exhibited by the Holometabola. However, because relatively few species of holometabolous insects have been studied, the degree of CNS reorganization during pupation may vary widely between species, depending on specific life history characteristics. Research has been conducted on the retention of learning through metamorphosis in the holometabolous darkling beetles, Tenebrio molitor and Tenebrio obscurus, using a more complex spatial learning task (complex maze). These studies were also interested in studying neurochemical events (brain RNA synthesis) associated with learning. The maze consisted of a start chamber, goal chamber and six blind alleys. Only older larvae (

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