Handbook of Biological Control: Principles and Applications of Biological Control

Biological

c-0n t v* 1

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Biolosical Principles and Applications of Biological Control

Editors: Thomas S. Bellows

T. W. Fisher

University of California Riverside, California

University of California Riverside, California

Associate Editors:

L. E. Cahgirone

D. L. Dahlsten

University of California Berkeley, California

University of California Berkeley, California

C. Gordh Agricultural Research Service Kika de la Garza Subtropical Agricultural Research Center

C. B. Huffaker University of California Berkeley, California

ACADEMIC PRESS A Harcourt Science and Technology Company

San Diego San Francisco New York London Sydney Tokyo

Boston

This book is printed on acid-free paper. @ Copyright 0 1999by ACADEMIC PRESS All Rights Reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in writing from the publisher.

Academic Press a division of Harcourt Brace & Company 525 B Street, Suite 1900, San Diego, California 92101-4495, USA http:/lwww.apnet.com

Academic Press

24-28 Oval Road, London NWl 7DX, UK http:l/www.hbuk.co.uWap/ Library of Congress Catalog Card Number: 98-89454 International Standard Book Number: 0-12-257305-6 PRINTED IN THE UNITED STATES OF AMERICA 99 00 01 02 03 0 4 E B 9 8 7 6 5

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To s.c.c. j. m a y youv light nevel* fail.

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Contents

Contributors xix Preface and Acknowledgments xxi

Chapter 27 Chapter 28 Chapter 29 Chapter 30 Chapter 31 Chapter 33 Chapter 34 Chapter 35 Chapter 36 Chapter 37 Chapter 38 Chapter 39 Chapter 40 Chapter41

P A R T

INTRODUCTION 1. Scope a n d Significance of Biological Control C. B. HUFFACKER AND D. L. DAHLSTEN

Introduction 1 Principles and Processes Chapter 2 Chapter 3 Chapter 4 Chapter 5 Chapter 6 Chapter 7 Chapter 8 Chapter 9 Chapter 10 Chapter 11 Chapter 12 Chapter 13 Chapter 14

4

References

4 5 5 6 6 6 7 7 8 8

15

2. Theories a n d Mechanisms of Natural Population Regulation T. 5. BELLOWS, Jr. AND M. P. HASSELL

Introduction 17 Single-Species Populations

17

Homogeneous Environments Patchy Environments 19

Interspecific Competition

8

17

20

Homogeneous Environments Patchy Environments 22

9 9

21

Host-Parasitoid Systems 23

Agents, Biology, and Methods 9 Chapter 15 9 Chapter 16 9 Chapter 17 (and Chapter 34) Chapters 18 and 21 10 Chapter 19 10 Chapter 20 10 Chapter 22 1 1 Chapter 23 11 Chapter 24 1 1 Chapter 25 1 1

12 12 12 13 13 13 13 14 14 14 15 15 15 15

Host Density Dependence 24 Spatial Patterns of Parasitism 25 Age-Structured Systems 29 Spatial Complexity and Asynchrony in Metapopulations Generalist Natural Enemies 33

10

Host-Pathogen Systems 33 Multispecies Systems 36 Competing Natural Enemies 37 Generalist and Specialist Natural Enemies 37 Parasitoid-Pathogen-Host Systems 38 Competing Herbivores and Natural Enemies 39

Applications 12 Chapters 26 and 32 12

References

vii

40

3I

viii

Contents Considerations on Geographic Origin of Pest 87 Securing Natural Enemies in the Native Range 90 Searching Outside the Native Range 90 Summary Concerning Search Locations 91

P A R T

PRINCIPLES AND PROCESSES 3. Taxonomy a n d Biological Control GORDON GORDH AND JOHNW. BEARDSLEY

Introduction 45 Taxonomy: The Historical Perspective 45 The Importance of Taxonomy to Biological Control 46

Contributions of Biological Control to Taxonomy 48 Zoogeographical Data 48 Biological Data 49 Behavioral Data 49 Ecological Data 49 Hybridization Studies 49

Risk Assessment and Evaluation of Natural Enemy Potential 91 Terrestrial Vertebrates 92 Phytophagous Arthropods and Phytopathogens 92 Terrestrial Scavengers 92 Aquatic Vertebrates and Invertebrates 93 Parasitic and Predaceous Arthropods and Arthropod Pathogens 93 Assessing Natural Enemy Potential 94

Planning, Preparation, and Execution of a Foreign Collecting Trip 95 Planning and Preparation 95 Conducting the Exploration 96

References 98

Sources of Taxonomic Expertise 49 Literature, Reference Collections, and Voucher Specimens 50 Specimens in Biological Control Research

50

Modern Systematic Tools and Techniques 52 Preparation of Specimens 52 Point Mounts 53 CardMounts 53 Minuten Nadelns 53 Alcohol as a Preservative 53 Transmittal of Specimens 53 Additional Technologies 54 Distinguishing Similar Species 54

References 54

4. Molecular Methods in Classical Biological Control THOMAS R UNRUH AND JAMES B. WOOLLEY

Introduction and Rationale 57 Molecular Markers 58 The Genetic Material 58 Molecular Variation 58 Enzyme Polymorphism 59 Techniques for Studying DNA

6 . Quarantine T. W. FISHER AND L. A. ANDRb

Introduction 103 Establishing Quarantine Facilities

Quarantine Procedures

59

Systematics 64 Population Biology 72 Population Structure, Gene Flow, and Mating Systems 72

Conclusions 76 References 76

5. Exploration for Natural Enemies

110

Introduction 110 Federal Regulations 110 Permits 111 Packaging and Shipping of Biological Control Agents 113 Coordination with Collectors I14 Removal of Unwanted Parasites, Hyperparasites, and Pathogens 115 Identification I15 Culture of Hosts and Natural Enemies 116 Testing and Screening of Biological Control Agents 1 18 Disposal 118 Voucher Specimens 119 Records and Reports 119 Quarantine Procedural Problems 120

Personnel

Applications in Biological Control 64

104

Location and Utilities 104 Structural Design 106 Equipment and Amenities 107

121

Biological Control and Biological Relationships of Natural Enemies 121 Computer Skills 121 Communication Skills 121 Physical Plant 121 Sanitation, Visitors, and Emergencies 12 1

References

122

7. Culture a n d Colonization L. K. ETZEL AND E. F. LEGNER

E. F. LEGNER AND T. S. BELLOWS

Culture of Hosts for Entomophagous Arthropods Introduction 87 Areas for Search 87

Host Food 125 Host Production 127

125

ix

Contents

Culture of Entomophagous Arthropods

140

Contamination 140 Genetic Changes 142 Causes of Genetic Change 144 Retaining Genetic Diversity 146 Culture and Synthetic Diet 148 Interactions between Entomophages, Hosts, and Host Food 150 Food for Adult Entornophages 152 Factitious Hosts for Entomophages 152 Dead Hosts for Entomophages 153 Diapause 155 Environmental Conditions 156 Mating 156 Sex-Ratio Changes 157 Rearing Density and Entomophage to Host Ratios 158 Behavior 159 Special Techniques and Considerations 160 Quality 164

Colonization of Entomophagous Arthropods

165

9. Evaluation of Biological Control with Experimental Methods ROBERT F. LUCK, B. MERLE SHEPARD, AND PETER E. KENMORE

Introduction 225 Evaluation Techniques .226 Introduction and Augmentation of Natural Enemies

226

Exclusion or Inclusion Techniques 227 Cages and Other Baniers 227 Insecticide Removal 230 Hand Removal 231 Outplants or Prey Enrichment 231

Assay Techniques 232 Serological Methods 232 Electrophoretic and Isoelectric Focusing Methods Prey Marking 235 Visual Counts 236

234

Summary 236 References 237

Liberation Procedures 165 Collection and Dissemination 166 Principal Factors Influencing Establishment or Effectiveness 167

Addendum References

175 176

10. Evaluation of Results A. P. GUTIERREZ, L. E. CALTAGIRONE, A N D W. MEIKLE

8. Life Table Construction a n d Analysis for Evaluating Biological Control Agents T. S. BELLOWS A N D R G. VAN DRlESCHE

Introduction 243 Naturally Occurring Biological Control 244 Estimating the Benefits and Costs of Classical Biological Control 244 Justifying the Need for Biological Control 248 Biological Control as an Alternative to Pesticide Use 248

Introduction 199 Definitions and Data Collection

Perceived Risk 249 Conclusion 250 References 250

199

Types of Life Tables 199 Types of Data Used in Life Table Construction 200 Applications to Biological Control Systems 201 Determining Total Numbers Entering Stages 201 Additional Sources of Mortality Caused by Parasitoid Impact of Sample Design 205

203

Assessing Quantitative Impact of Natural Enemies 206 Parameters in the Life Table 206 Interpreting Life Tables 208

GARY W. ELZEN AND EDGAR G. KING

Determining Ecological Roles of Natural Enemies 21 1 Role Questions and Density Relatedness Ecological Roles and Hypotheses 21 1 Analytical Techniques 212

21 1

Experimental Designs for Life Table Studies 215 Applications to Categories of Natural Enemies Other Than Parasitoids 217 Pathogens of Arthropods 218 Predators 2 18 Beneficial Herbivores and Plant Pathogens Augmentation 2 18

Conclusions 219 References 220

1 1. Periodic Release and Manipulation of Natural Enemies

21 8

Introduction 253 Augmentation 253 Trichogramma spp. 253 Evaluating Natural Enemies as Candidates for Augmentation 257 Field Evaluations and Assessment 259

Conservation 260 Monitoring 26 1 Rearing 262 In Vitro Rearing 263 Conclusions 263 References 264

Contents

X

12. Genetic Improvement a n d Other Genetic Considerations for Improving t h e Efficacy and Success Rate of Biological Control M . J. WHllTEN AND M. J. HOY

Introduction 27 1 Category 1: Biological Control by Restoring a Natural Balance 273 Category 2: Biological Control of Secondary Pests 274 Category 3: Biological Control of Weeds and Pests in Novel or Disturbed Environments 274 Genetic Considerations for Improved Success Rates in Biological Control 276 Limited Opportunity for Genetic Improvement in Category 1 Cases of Biological Control 276 Relevance of Genetic Variability in Category 1 Weeds to Their Suitability for Biological Control 278 Improving Efficacy of Natural Enemies for Category 1 Weeds 280 Genetic Improvement of Natural Enemies of Secondary Pests (Category 2) 282 Genetic Improvement Opportunities Where the Natural Enemy Is Confronted with One or More Novel Conditions in the Environment (Category 3) 286 The Scope of Molecular Biology and Genetic Engineering for Improving the Success Rate of Biological Control 288 References 290

13. Enhanced Biological Control through Pesticide Selectivity MARSHALL W. JOHNSONAND BRUCE E. TABASHNIK

Introduction 297 Effects of Pesticides on Natural Enemies 297 Direct Effects 297 Indirect Effects 299

Consequences of Disrupting Biological Control 302 Resurgences 302 Secondary Pest Outbreaks

Vegetation Management 324 Mechanical Crop Management Chemical Inputs to the System

Techniques to Reduce the Negative Impact of Chemicals on Natural Enemies 304 304

Conclusions 3 11 References 3 12

14. Environmental Management to Enhance Biological Control in Agroecosystems

Mechanisms of Enemy Enhancements 335 Theoretical Aspects of Environmental Management 339 Enemy-Free Space 339 Island Biogeographic Theory 339 Consumer Dynamics 341 Effects of Vegetational Diversity 342 Optimal Foraging 342

Conclusions 343 References 344 P A R T

AGENTS, BIOLOGY, AND METHODS 15. Biology of Parasitic Hymenoptera G. GORDH, E. F. LEGNER AND L. E. CALTAGIRONE

Introduction 355 Definitions 355 Important Anatomical Features of Parasitic Hymenoptera 356

Parasitic Hymenoptera Important in Biological Control 357 The Parasitica 357 Aculeata 360

Principal Aspects of Parasitoid Biology 360 Developmental Stages 360 Oogenesis-Ovisorption-Spermatogenesis 363 Oviposition Strategy and Progeny Number 364 Sex Regulation 364 Host Feeding 366 Diapause in Parasitoids 367 Genetics 367 Selective Breeding 368 Habitat Location 368 Host Location 369 Host Acceptance 369 Parasitoid Attack and Host Defenses Host Suitability 370

370

Summary 370 References 37 1

16. Terrestrial Arthropod Predators of Insect a n d Mite Pests K. 5. HAGEN, N. J. MILLS, G. GORDH, AND J. A. MCMURTRY

D. K. LETOURNEAU AND M . A. ALTIERI

Introduction 3 19 Classification of Agroecosystems 320

329 332

Ecology of Parasitic Hymenoptera 368

303

Crop Monitoring and Economic Thresholds Pesticide Selectivity 306

Modes of Environmental Management 324

Introduction 383 Subphylum Chelicerata 384 Class Arachnida

384

xi

Contents

Subphylum Uniramia Class Hexapoda

391

Nematodes 539

392

Biological Properties in Relation to Insect Control Nematodes as Biological Control Agents 539

Conclusions 460 References 46 1

539

Discussion and Conclusions 541 Classical Biological Control 542 Mass Production and Cost-Effectiveness 542 Future Utility of Different Pathogen Types 543

17. Arthropods and Vertebrates in Biological Control of Plants

References 545

T. S. BELLOWS AND D. H. HEADRICK

Introduction 505 Effects of Herbivory on Weedy Plants

19. Cross-Protection a n d Systemic Acquired Resistance for Control of Plant Diseases

505

J. ALLAN DODDS

Reduced Reproduction or Recruitment to the Plant Population 506 Direct Mortality of Plants 506 Indirect Mortality of Plants 506 Interactions with Other Stresses 507

Introduction 549 Comparison of Cross-Protection and Systemic Acquired Resistance 549 Systemic Acquired Resistance 550 Cross-Protection 550

Taxa Used in Biological Control 507 Invertebrates 508 Vertebrates 5 12

Mechanisms of Cross-Protection 551 Practical Application and Biological Control

Attributes and Safety of Control Agents 5 12 Host Specificity 5 13 Other Attributes 514

55 1

Conclusions 554 References 554

Agent Selection 514 References 5 15

20. Genetic Mechanisms for Engineering Host Resistance to Plant Viruses

18. A Perspective o n Pathogens as Biological Control Agents for Insect Pests 8. A. FEDERlCl

Introduction 5 17 Historical Background 5 18 Current Usage in Perspective

5 18

521

Viruses

Biological Properties Related to Insect Control 521 Use of Viruses as Insect Control Agents 523 Use of Recombinant DNA Technology to Improve Nuclear Polyhedrosis Viruses 527

Bacteria 528 Biological Properties in Relation to Insect Control 528 Bacillus thuringiensis 528 Biology and Use of Bacillus popilliae for Scarab Control 529 Biology and Use of Bacillus sphaericus for Mosquito Control 530 Biology and Use of Serratia entomophila for Scarab Control 530

Fungi

BRET COOPER

Introduction 557 Engineered Viral Resistance Strategies 557 CP-Mediated Protection 558 RNA-Mediated Protection 559 Replicase-Mediated Protection 560 Defective Movement Protein-Mediated Protection Other Viral Genes Tested 563 Antisense RNA 563 Defective Interfering RNNSatellite RNA 564 R Genes 564 Pathogenesis-Related Proteins 565 Antiviral Agents 565

561

Transgenic Plant Performance 565 Virus Transmission 566 Field Trials 566 Effects of Engineered Resistance Genes on Plants

567

Regulation and Risk Assessment 567 Prospects 569 References 570

530

Biological Properties in Relation to Insect Control Fungi as Insect Control Agents 531

Protozoa

530

536

Biological Properties in Relation to Insect Control General Biology of Microsporidia 537 Microsporidia as Biological Control Agents 538

21. Bacilhs thuringiensis in Biological Control 8. A. FEDERICI

536

Introduction 575 General Biology of Bacillus thuringiensis

575

xii

Contents

Bacillus thuringiensis as a Bacterial Species 576 Molecular Systematics of B. thuringiensis 578

Feeding and Nutrition of Adult Entomophagous Species 603

Insecticidal Proteins of Bacillus thuringiensis 579 Cry and Cyt Protein Nomenclature 579 Mode of Action and Structure of Cry Proteins 580 Mode of Action and Structure of Cyt Proteins 582

Major B.t. Pathotypes 583 Parasporal Body Shape, Complexity, and Pathotype

584

Commercial Products Based on Bacillus thuringiensis 584 Products Based on Natural Isolates of B. thuringiensis 584 Bacillus thuringiensis subsp. morrisoni (H8a8b), Isolate DSM 2803 585 Bacillus thuringiensis subsp. kurstaki (H3a3b), Isolates HD1 andNRD12 585 Bacillus thuringiensis subsp. aizawai (H7) 586 Bacillus thuringiensis subsp. israelensis (H14), Isolate ONR60A 587 Products Based on Transconjugate or Recombinant Bacteria 588

Resistance to Bacillus thuringiensis Insecticides 589 Transgenic Bacillus thuringiensis Crops 589 Resistance Development Concerns 589 Bacillus thuringiensis Resistance Management in Transgenic Crops 590 Other Concerns about Bacillus thuringiensis Crops 59 1

References 591

Supplemental Foods and Performance 603 Plant Foods 604 Host Feeding by Hymenopteran Parasitoids 605 Proovigenic and Synovigenic Parasitoids 605 Patterns of Host Feeding by Hymenopteran Parasitoids 606 Models of Host Feeding by Hymenopteran Parasitoids 606 Host Feeding by Dipteran Parasitoids 608 Honeydew Feeding by Adult Entomophagous Species 608 Nutritional Requirements of Adult Entomophagous Species 608

In Vitro Culture of Parasitoids 612 Physiological Factors of Importance to Successful Development of Parasitoids 6 12 Artificial Diets in vitro Culture of Dipteran Parasitoids 612 Artificial Diets and in vitro Culture of Hymenopteran Parasitoids 620 In vitro Culture of Koinobiontic Endoparasitoids 62 1 In vitro Culture of Trichogramma 622 Role of Hormones in the in vitro Culture of Parasitoids 623 Role of Teratocytes in the Nutrition of Parasitoids 624 Importance of Dietary Osmotic Pressure to Successful in vitro Culture of Parasitoids 624

In vitro Culture of Predators 625 In In In In

vitro Culture vitro Culture vitro Culture vitro Culture

of of of of

Coccinellids 625 Chrysopa and Chrysoperla Hemipterans 628 Predaceous Mites 63 1

628

Continuous Artificial Mass Culture 63 1

22. Nutrition of Entomophagous Insects and Other Arthropods S. N. THOMPSON AND K. 5. HAGEN

Introduction 594 Host Effects on the Biological Attributes of Parasitoids 594 Host and Parasitoid Size and the Effects of Parasitoid Size on Fitness 594 Effects of Host Nutrition on Parasitoid Attributes 596 Host Nutrition and Parasitoid Behavior 597 Effects of Prey Species on the Biological Attributes of Predators 597

Food Utilization 597

Behavior and in vitro Culture 631 Chemical Cues Influencing the Behavior of Entomophagous Species 632 Continuous in vitro Culture of Trichogramma 632 Performance of in vitro-Cultured Entomophagous Insects 634

Current Applications 634 Conclusions and Future Directions 635 Nutrition and Dietetics 635 Dependence of Parasitoid Development on Host Physiology 636 Nutritional Ecology of Entomophagous Species 636 Genetic Basis and Modification of Nutrition 636 Genetic Engineering of Entomophagous Species 637

References 637

Food Utilization by Parasitoids 597 Food Utilization by Predators 598

Developmental Nutritional Requirements 599 General Nutritional Requirements of Insects 599 Requirements for Development of Hymenopteran Parasitoids 599 Requirements for Development of Dipteran Parasitoids 601 Requirements for Development of Predators 601 Evaluation of Developmental Nutritional Requirements 60 1 Developmental Nutrition, Environmental Conditions and Biological Characteristics of Parasitoids 602 Importance of Nonnutritional Factors in Feeding and Nutrition 603

23. Sex Ratio and Quality in t h e Culturing of Parasitic Hymenoptera: A Genetic and Evolutionary Perspective R F. LUCK, L. NUNNEY, AND R STOUTHAMER

Introduction 653 Sex Determination 653 Sex-Ratio Distorting Factors 656 Sex Ratio in Heteronomous Parasitoids 658 Postcopulation Fertilization Lags 659

xiii

Contents

Multiple Copulations 659 Temperature and Photoperiod 659 Sex Allocation 660 Sex Ratio and Variation in Fitness 663 Local Parental Control and Variation in Fitness-Host Size Interactions 664 Clutch Size and Sex Ratio 664 Sex Ratio of Polyembryonic Wasps 665 Summary 666 References 666

Microbial and Habitat Characteristics 701 Pathogens and Antagonists 701 Soil and the Rhizosphere 702

Control of Soil Borne Plant Pathogens 702 Conservation 703 Augmentation 705 Induced Resistance 708

Developing and Using Beneficial Species 709 References 7 10

27. Biological Control in Subtropical and Tropical Crops

24. Evolution of Pesticide Resistance in Natural Enemies BRUCE E. TABASHNIK AND MARSHALL W. JOHNSON

Introduction 673 Hypotheses and Evidence 673 Bias in Documentation 673 Differential Preadaptation 675 Population Ecology 683 Perversity of Nature 686

Summary and Implications 686 References 687

C. E. KENNElT, 1. A. MCMURTRY, AND J. W. BEARDSLEY

Introduction 7 13 Citrus 713 Armored Scales: Diaspididae 7 13 Unarmored or Soft Scales: Coccidae Fluted Scales: Margarodidae 720 Mealybugs: Pseudococcidae 720 Whiteflies: Aleyrodidae 722 Psyllids: Psyllidae 724 Mites 725 Snails 726

Olive 727 Olive Pests

Avocado

25. Hypovirulence to Control Fungal Pathogenesis DENNIS W. FULBRICHT

Introduction 691 Searching for the Cause of Hypovirulence 693 Hypoviruses 694 Biological Control 694 Treating Chestnut Trees with Hypovirulent Strains 695 References 696

717

727

728

Avocado Pests 728

Tea 731 Coffee 732 Coconut 732 Important Pests 732 Lepidopterous Pests 734

Banana 734 Banana Pests 734

References 735

28. Biological Control in Deciduous Fruit Crops P A R 1

M. T. ALlNlAZEE AND B. A. CROFT

Introduction 743 Biological Control of Secondary Pests 743

APPLICATIONS 26. Controlling Soil-Borne Plant Pathogens T. 5. BELLOWS

Management of Endemic Natural Enemies of Secondary Pests 744 Introductions of Biological Control Agents 750

Biological Control of Direct, Primary, and Sporadic Pests 750 Management of Endemic Natural Enemies

750

Introduction of Exotic Biological Control Agents Introduction 699 Root Pathogens and Their Biological Control Agents 699 Microbial Pathogens and Antagonists 699 Plant-Parasitic Nematodes

700

Codling Moth 752 Apple Maggot (Rhagoletis pornonella) 753 Other Fruit Fly Species 754 Other Insects 754

752

xiv

Contents

Summary of Status of Biological Control of Deciduous Fruit Pest Species 755 References 756

Ostrinia nubilalis (Hubner) (Pyralidae), the European Corn Borer 797 Phenacoccus manihoti Matile-Ferrero (Pseudococcidae), the Cassava Mealybug 798 Mononychellus tanajoa (Bondar) (Tetranychidae), the Cassava Green Mite 801

Inundative and Augmentative Releases 802

29. Biological Control of Forest Insects D. L. DAHLSTEN AND N. j. MILLS

Introduction 761 Ecological Attributes of Forest Ecosystems 761 Influence of Forests on Biological Control 762 Biological Control Strategies in Forestry 762

Importation of Natural Enemies 763 Introduced Pests 763 Native Pests 764

Augmentation of Natural Enemies 766 Conservation of Natural Enemies 768 Biological Control Organizations in Forestry 769 Australia 770 United States 770 Canada 770 International Institute of Biological Control

Use of Trichograrnrna spp. to Control Lepidopterous Pests of Annual Crops 802 Biological Control of Spider Mites on Transient Crops 806 Control of the Mexican Bean Beetle, Epilachna varivestis Mulsant (Coccinelidae), by Inoculative Releases of an Imported Parasitoid 807 Use of Microbial Pesticides 808

Interactions of Biological Control with Other IPM Tactics 810 Impact of Cultural Practices on Natural Enemies 810 Effect of Plant Resistance on Biological Control 810 Impact of Pesticides on Natural Enemies 81 1

Conclusion 8 11 References 8 11

77 1

Case Histories 771 Lepidoptera 771 Hymenoptera: Symphyta 777 Coleoptera 78 1

References 782

MICHAEL P. PARRELLA, LlSE STENGARD HANSEN, AND JOOPVAN LENTEREN

30. Enhancement of Biological Control in Annual Agricultural Environments M. KOGAN, D. GERLING, AND J. V. MADDOX

Introduction 789 Ecological Characteristics and Faunal Colonization Patterns 789 Dynamics of Transient Crop Development 789 Colonization of Transient Crops by Herbivores and Natural Enemies 790 Recruitment of Crop Colonizers 791

Natural Control in Transient Crops 791 Predators 792 Parasitoids 792 Entomopathogens

3 1 . Glasshouse Environments

792

Classical Biological Control 794 Nezara viridula (Linnaeus) (Pentatomidae), the Southern Green Stink Bug or Green Vegetable Bug 794 Dacus cucurbitae Coquillet (Tephritidae), the Melon Fly 795 Oulerna melanopus (Linnaeus) (Chrysomelidae), the Cereal Leaf Beetle 795 Hypera postica (Gyllenhal) (Curculionidae), the Alfalfa Weevil 796

Introduction 8 19 Vegetable Crops 819 Factors Conducive to the Use of Biological Control in Vegetables 820 Control of the Two-Spotted Spider Mite Tetranychus urticae with Pytoseiulus persimilis 821 Introduction Methods

822

Control of Greenhouse Whitefly, Trialeurodes vaporariorum, Using Encarsia formosa 823 Biological Characteristics 823 Introduction Methods 824

Control of Leafminers Using Parasites 825 Control of Aphids with Parasitoids and Predators 826 Control of Onion Thrips, Thrips tabaci, and Western Flower Thrips, Frankliniella occidentalis, Using Predators 827 Ornamental Crops 828 Chrysanthemums 829 IPM for Chrysanthemums 832 IPM for Roses 833 New Developments to Ensure Successful Application of Biological Control 833

Summary 834 References 835

xv

Contents

32.Foliar, Flower, a n d Fruit Pathogens T. S. BELLOWS

Introduction 84 1 Pathogens and Their Biological Control Agents 841 Stems 841 Leaves 842 Flowers and Fruits

842

Habitat and Agent Characteristics 843 Pathogens and Antagonists 843 Phyllosphere Habitat Characteristics

Case Histories of Recent Successes in North America and Other Parts of the World 880 Alligatorweed, Alternanthera phylloxeroides, in the Southeastern United States and Australia 880 Puncturevine, Tribulus terrestris, in the Southwestern United States, Hawaii, and St. Kitts 881 Water Hyacinth, Eichorniu crussipes, in the Southeastern United States 882 Three Recent Successes Outside of North America 884

Future Direction of Biological Control of Weeds References 886

843

886

Biological Control of Plant Pathogens 844 Conservation 844 Augmentation 845 Induced Resistance 848 Hypovirulence 849 Parasitism of Pathogens 850

35.U s e of Plant Pathogens in Weed Control

Developing and Using Beneficial Species 850 References 8.51

33. Biological Control of Insects and Mites o n Grapes D. L. FLAHERlY AND L. T. WILSON

Introduction 853 Biological Control of Insect and Mite Pests

853

Homoptera 853 Lepidoptera 859 Coleoptera 86 1 Thysanoptera 861 Acari 862

E. N. ROSSKOPF, R CHARUDATTAN, AND J. B. KADlR

Introduction 891 Biological Control Strategies 89 1 Successful Examples Using the Classical Approach 892 Commercialization and the Bioherbicide Approach 893 Deleterious Rhizobacteria and Weed Control 897 Developmental Testing of Mycoherbicides 900 Field Assessment 901 Formulation of Biological Control Agents 901 Bioherbicides and Integrated Weed Management 904 Biotechnology and Biological Control 905 Laws Governing Biological Control Agents 907 Production of Bioherbicide Agents 910 References 9 11

Conclusion 86.5 References 866

36. Biological Control of Insects in Urban Environments 34. Biological Control of W e e d s in Terrestrial and Aquatic Environments R D. GOEDEN AND L. A. ANDR&

Introduction 871 What Is Biological Control of Weeds?

871

Definition 87 1 Methodology 87 1

History of Biological Control of Weeds 873 Scope of Biological Control of Weeds 877 Target Weeds 877 Insect Agents Used 878 Phytopathogenic Agents Used Other Agents Used 878 Countries 879 Agencies 879

878

D. L. DAHLSTEN AND R W. HALL

Introduction 9 19 Ecological Attributes of Urban Outdoor Environments 920 Potential for Urban Biological Control 920 Biological Control Case Histories 921 Blattaria: Blattidae and Blattellidae (Cockroaches) 92 1 Dermaptera: European Earwig (Forjicula auriculuria Linnaeus) 923 Thysanoptera: Cuban Laurel Thrips (Gynaikothrips jicorum Marchal) 924 Homoptera 923 Coleoptera 929 Lepidoptera 930 Diptera 930

References 930

mi

Contents

37. Biological Control of Medical and Veterinary Pests R GARCIA AND E. F. LEGNER

Introduction 935 Mosquitoes 936

Chile 978 Colombia 979 Cuba 979 Mexico 979 Peru 979 Other Programs 986

Three Contemporary Case Studies 986

Fish 936 Arthropods 939 Fungi 941 Nematodes 942 Bacteria 943 Protozoa 943 Viruses 943

Biological Control of Cereal Aphids in Chile and in Brazil 986 Biological Control of Sugarcane Borer in Brazil 987 Biological Control of Alfalfa Aphids in Argentina 987

Synanthropic Diptera 943

Centers of Biological Control in Latin America 987 Possibilities for Further Work and Conclusions 988 References 989

Endophilic Flies 943 Exophilic Flies 944

Snails 945 Predators 945 Antagonists 946

P A R T

V

References 946

38. Biological Control of Vertebrate Pests MARK S . HODDLE

Introduction 955 Factors That Facilitate Vertebrate Establishment 956 Community Characteristics 956 Species Characteristics 956 Relocation of Vertebrates and Human Assistance in Establishment 957

Vertebrate Pest Management 957 Predators as Biological Control Agents 958 Parasites as Biological Control Agents 959 Pathogens as Biological Control Agents 962

New Avenues for Biological Control of Vertebrates 966 Immunocontraception for Control of Vertebrate Pests 966

Regulating Vertebrate Introductions 969 Biological Control of Exotic Pests as an Evolutionarily Stable Control Strategy 970 References 970

39. Classical Biological Control in Latin America: Past, Present, and Future M. A. ALTlERI AND C. I. NICHOLLS

Introduction 975 Historical Overview 975 Pesticide Use in Latin America and Implied Environmental and Health Impacts 976 Brief Country Profile on Classical Biological Control 978 Argentina 978 Brazil 978

RESEARCH AND THE FUTURE 40. Social and Economic Factors Affecting

Research and Implementation of Biological Control JOHN H. PERKINS AND RICHARD GARCIA

Introduction 993 The Political Economic Framework for Biological Control 993 Definition of Biological Control 994 Problems in Measuring Biological Control 995 Allocation of Resources to Biological Control Research 997 Magnitude of the Research Effort 997 Biological Control within the Pest Control Sciences 997 Organization of Biological Control Research 998 New Areas of Study 999 Factors Affecting Biological Control Research 1000 Research Needs on the Political Economy of Biological Control Research 1002

Socioeconomics of Biological Control

1002

Biological Control as an Investment 1002 Classical Biological Control 1003 Augmentative Biological Control 1003 Conservatory Biological Control 1003

Summary of Factors Affecting Biological Control Social 1005 Economic 1005 Political 1005 Philosophical 1006

Recommendation 1006 References 1008

1005

xvii

Contents

41. Whither Hence, Prometheus? The Future of Biological Control T. S. BELLOWS

A Gift of Fire 1011 Whither Hence? 1012 Combating Adventive and Native Pests 1012 Microbial Agents as Biological Pesticides 1012 Protection of Natural Ecosystems 1013

Nontraditional Settings 1013 Gene Use and Modification 1013 Experts and Institutions 1014 Training Future Scientists and Practitioners

Toward the Light 1014 References 1015

Subject Index 1017 Taxonomic Index 1031

1014

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Contributors

Numbers in parentheses indicate the pages on which the authors' contributions begin.

B. A. Federici (517, 575) Department of Entomology, University of California, Riverside, CA 92521

M. T. AliNiazee (743) Department of Entomology, Oregon State University, Corvallis, OR 97331

T. W. Fisher (103) Department of Entomology, University of California, Riverside, CA 92521

Miguel A. Altieri (319, 975) Division of Insect Biology, University of California, Berkeley, CA 94720

D. L. Flaherty (853) Cooperative Extension, Agricultural Guidling, County Civic Center, Visalia, CA 93291

L. A. Andrrs (103, 871) USDA-ARS, Western Research Center, 800 Buchanan Street, Albany CA 94710

Dennis W. Fulbright (691) Department of Botany and Plant Pathology, Michigan State University, East Lansing, MI 48824

J. W. Beardsley (45, 713) Department of Entomology, University of Hawaii at Manoa, Honolulu, HI 96822

R. Garcia (935, 993) Division of Biological Control, University of California, Albany, CA 94706

T. S. Bellows, Jr. (17, 87, 199, 505, 699, 841, 1011) Department of Entomology, University of California, Riverside, CA 92521

Dan Gerling (789) Department of Zoology, Tel Aviv University, Ramat Aviv, Israel

L. E. Caltagirone (243, 355) Division of Biological Control, University of California, Berkeley, CA 94720

R. D. Goeden (871) Department of Entomology, University of California, Riverside, CA 92521

R. Charudattan (891) Plant Pathology Department, University of Florida, Gainesville, FL 32611

G. Gordh (45, 355, 383) USDA, Agricultural Research Service, Kika de la Garza Subtropical Agricultural Research Center, Weslaco, TX 78596

Bret Cooper (557) Division of Plant Biology, Department of Cell Biology, The Scripps Research Institute, La Jolla, CA 92037

A. P. Gutierrez (243) Center for Biological Control, University of California, Berkeley, CA 94720

B. A. Croft (743) Department of Entomology, Oregon State University, Corvallis, OR 97331

K. S. Hagen (383, 593) Division of Biological Control, University of California, Berkeley, Albany, CA 94706

D. L. Dahlsten (1,761,919) Division of Biological Control, University of California, Berkeley, CA 94720

R. W. Hall (919) Department of Entomology, Ohio State University, Columbus, OH 43210

J. Allan Dodds (549) Department of Plant Pathology, University of California, Riverside, CA 92521

Lise Steng~rd Hansen (819) Danish Pest Infestation Laboratory, Ministry of Foods, Agriculture, and Fisheries, Lyngby, Denmark

Gary W. Elzen (253) Subtropical Agricultural Research Center, U.S. Department of Agriculture, Agricultural Research Sevice, Weslaco, TX 78596

M. P. Hassell (17) Department of Biology, Imperial College, Silwood Park, Ascot, Berkshire, SL5 7PY, United Kingdom

L. K. Etzel (125) Center for Biological Control, University of California, Berkeley, CA 94720

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XX

Contributors

D. H. l-leadrick (505) Department of Crop Science, California Polytechnic State University, San Luis Obispo, CA 93407 Mark S. Hoddle (955) Department of Entomology, University of California, Riverside, CA 92521 Majorie A. l-loy (271) Department of Entomology and Nematology, University of Florida, Gainesville, FL 32611

W. Meikle (243) Center for Biological Control, University of California, Berkeley, CA 94720 N. J. Mills (383, 761) Division of Biological Control, University of California, Berkeley, CA 94720 J. A. McMurtry (383, 713) Department of Entomology, University of California, Riverside, CA 92521 Clara I. Nicholls (975) Department of Entomology, University of California, Davis, CA

C. B. Huffaker (1) Center for Biological Control, University of California, Berkeley, CA 94720

L. Nunney (653) Department of Biology, University of California, Riverside, CA 92521

Marshall W. Johnson (673, 297) Department of Entomology, University of Hawaii, Honolulu, HI 96822

Michael P. Parrella (819) Department of Entomology, University of California, Davis, CA 95616

J. B. Kadir (891) Department of Plant Protection, Faculty of Agriculture, Universiti Putra Malaysia, Selangor, Malaysia

John H. Perkins (993) The Evergreen State College, Olympia, WA 98505

Peter E. Kenmore (225) Inter-Country IPC (Rice) Programme, Manila, The Philippines C. E. Kennett (713) Division of Biological Control, University of California, Albany, CA 94706 Edgar G. King (253) Subtropical Agricultural Research Center, U.S. Department of Agriculture, Agricultural Research Sevice, Weslaco, TX 78596 Marcos Kogan (789) Integrated Plant Protection Center, Oregon State University, Corvallis, OR 97331

E. N. Rosskopf (891) USDA-ARS, Fort Pierce, FL 34945 B. Merle Shepard (225) International Rice Research Institute, Manila, The Philippines R. Stouthamer (653) Department of Entomology, Agricultural University, Wageningen, The Netherlands Bruce E. Tabashnik (673, 297) Department of Entomology, University of Arizona, Tucson, AZ 85721 S. N. Thompson (593) Division of Biological Control, University of California, Riverside, CA 92521

E. F. Legner (87, 125, 355, 935) Department of Entomology, University of California, Riverside, CA 92521

Thomas R. Unruh (57) Yakima Agricultural Rsearch Laboratory, USDA Agricultural Research Service, Wapato, WA 98951

Joop Van Lenteren (819) Department of Entomology, Agricultural University, Wageningen, The Netherlands

R. G. Van Driesche (199) Department of Entomology, University of Massachusetts, Amherst, MA 01003

D. K. Letourneau (319) Department of Environmental Studies, University of California, Santa Cruz, CA 95064

M. J. Whitten (271) FAO Intercountry Programme on IPM in South and Southeast Asia, Makati City, The Philippines

R. F. Luck (225, 653) Department of Entomology, University of California, Riverside, CA 92521 Joseph V. Maddox (789) Center of Agricultural Entomology, Illinois Natural History Survey, Champaign, IL 61820

L. T. Wilson (853) Department of Entomology, Texas A&M University, College Station, TX 77843 James B. Woolley (57) Department of Entomology, Texas A&M University, College Station, TX 77843

Preface and Acknowledgments

At a meeting of 22 biological control workers from the Berkeley and Riverside campuses of the University of California in January 1986, a new biological control-oriented reference text was conceived, and collectively there was agreement to contribute to the task of preparing such a volume. The end product was not perceived as a revision of Biological Control of Insect Pests and Weeds, edited by DeBach (1964), which was "California School" classical biological control oriented and had a strong technique, or application, bias. We initially hoped that the present volume would be made available for the Vedalia Centennial Symposium on Biological Control held at Riverside in April, 1989. However, further consideration of the project, and of the greatly expanded scope of biological control in the last thirty years, indicated that a much larger work than was at first envisaged would be necessary to cover the field. The project was refined and reshaped, additional authors were recruited to add chapters suited to the scope of the field, and the volume grew in both breadth and depth. The intent was to cover, as much as possible, the great breadth of biological control science and application as is practiced in so many fields today. The result is the volume before you. Reported in this volume are certain aspects of the science derived from biological control research (Principles and Processes), detailed discussion of many of the agents and practices that form the operational characteristics of biological control (Agents, Biology, and Methods), and detailed reports on its use in many field programs (Applications). Of the 62 authors involved in the present volume, 21 received advanced degrees from U.C. departments of entomology or biological control. Three--Fisher, Hagen and Huffakermalso participated in the writing of Biological Control of Insect Pests and Weeds which, because of the mass of information it contains, continues to be viewed as an important classic general biological control reference. We hope that a reprinting will be forthcoming as a companion to the present book.

The intentional use of natural enemies to control pests of agriculture and forestry was practiced well before biological control, per se, became part of entomological and agricultural curricula. Formal course presentation in the U.S. was first offered in 1900 at Massachusetts Agricultural College (Sweetman 1958). In 1947 a course titled "Biological Control" which emphasized population dynamics and applied biological control entered the curriculum at the University of California, Berkeley (then the teaching campus), under the guidance and participation of Professor Harry S. Smith, who founded the biological control research unit at the University of California Citrus Experiment Station, Riverside, in 1923. Lecture and laboratory courses were taught at UC Berkeley by H. S. Smith, S. E. Flanders, J. K. Holloway (USDA) and R. L. Doutt. "Insect Pathology" under E. A. Steinhaus also became a formal and continuing component of the entomological curriculum at UCB. In 1962 similar courses were added to the entomological curriculum at UCR (P. DeBach and I. M. Hall, instructors). Between the two campuses (UCB 1940-1997, UCR 19641997) approximately 90 M.S. and 210 Ph.D. biological control-oriented degrees have been awarded. Approximately 54% were to foreign students. Many of the students and postdoctoral associates who worked at the two campuses subsequently were employed by universities or industry in the U.S. or abroad. Others were employed by their respective country's or state's agricultural agencies. Those who became involved in their own teaching and/or research programs, and their students, further extended an ecological, if not strictly classical, biological control perception. From this cadre and their students, the more sophisticated academic approaches (population and systems modeling, genetics, biotechnology, etc.) aimed at better understanding of ecological mechanisms and their interrelatedness, have greatly broadened the understanding of many crop ecosystems. Beginning in 1964, a regional research program, titled

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Preface and Acknowledgments

Project W-84, was funded by the USDA for the purpose of developing effective biological control procedures and incorporating them into pest management programs. Scientists, mostly entomologists, from agricultural experiment stations in nine western states and the USDA, participated in that project. The practical applied results of this project for the years 1964-1969 were published by Davis et al. [eds.] (1979), and the results of the years 1970-1990 are presented in another text, Nechols et al. [eds.] 1992. From 1971-1979, funding by the U.S. National Science Foundation and the Environmental Protection Agency (NSF/ EPA) permitted expansion, refinement and deepening of this type of research, and included personnel from 19 universities across the U.S. Popularly known as "the Huffaker Project" (after its director, C. B. Huffaker), the formal title was "Integrated Pest Management: The principles, strategies and tactics of pest population regulation and control in major crop ecosystems"; the results of the research conducted in this project were published in many papers and books, and were broadly treated by Huffaker (1980). The W-84 program (now continued with a new number, W-! 85) and the "Huffaker Project" served to fix irrevocably ecological awareness in the thinking of pest control management practices in the U.S. and have served as models and catalysts for similar studies on other crop systems in the U.S. and other countries. The term "biological control" connotes a broad variety of meanings and concepts depending on the age, perspective (or bias) and training of those who use the term. In the literal, applied sense, classical biological control, as wellstated by Waterhouse & Norris (1987), means "the importation and permanent establishment of exotic natural enemies" (and the consequences therefrom-- [eds.] ), and they list over 50 species of introduced weed and arthropod pests as being worthy of further study in the south and western Pacific regions. Recent publications which further emphasize the importance of continuing study, importation, and use of naturally occurring biological control organisms are those by Rosen (1990) and Andrews and Quezada (1989). DeBach and Rosen (1991) put forth several compelling reasons in support of strengthening research in classical biological control. Baker and Dunn (1990) and Maramorosch and Starkey (1992) include information on a wide miscellany of entomophagous microorganisms and present a broader view of "biological control" as perceived by many current workers who hold a strong bio-technological perspective of the subject. Largely from that perspective, two journals were inaugurated in 1991, "Biological control: theory and application in pest management," Academic Press, San Diego, CA, U.S.A., and "Biocontrol science and technology," Carfax Publ. Co., Abingdon, Oxfordshire, U.K. Other current articles on biological control are published by Intercept, Andover, Hampshire, U.K. In 1992 the Entomological Society of America began publishing a spe-

cialty journal titled "Biological Control." The text "Biological Control" by Van Driesche and Bellows (1996) focuses on both underlying principles and their practical application in employing biological control to solve real-world problems. Improved biological control of pests is widely considered the cornerstone of "sustainable agriculture," today's buzzword which implies incorporation of all known components in food and fiber production programs--plant breeding, soil fertility, pest control, socio-economics, and so o n - - w i t h safer human, animal, and environmental health being the main objective. Prospects presented by genetic engineering toward enhancement of pest control along several avenues (including beneficial organisms) offer much to ponder and conjecture about, but their application, much less their effectiveness over time in the field, has a very short track record. Biological control explorers continually search for presumed biotypes, which genetically may be more effective as natural enemies than those previously introduced. Possibly, this activity could eclipse the need for genetic engineering of natural enemies. Ironically, increased interest in biological control in the U.S. as currently expressed by federal (USDA, EPA) and state departments of agriculture parallels a deemphasis, i.e., reduced support, of classical biological control programs, especially in universities where most of the pioneering research and development in this field has occurred. This is a trend we hope to see reversed! Royalties from the previous Biological Control of Insect Pests and Weeds volume and from this present one accrue to the Harry Scott Smith Memorial Fund, a UC Regents endowment fund which is used at the University of California, Riverside to bring guest lecturers to UC and to assist students in their biological control training program through travel grants or modest stipends, and at UC Berkeley, to provide stipends for outstanding high school students to conduct biological control research in a laboratory setting. The editorial committee has tried to accomplish a meaningful presentation of the subject matter as submitted by the authors who wrote from their individual perspectives and subspecialties in the broader field of biological control. As an unavoidable consequence, certain of the biological control programs and the natural enemies or hosts involved are treated in more than one chapter. Our original intent was to list only currently accepted scientific names (from a U.S. perspective) in the index, but to include recently used synonyms in the text when appropriate. Names shown only as binomens are the responsibility of the chapter author(s) who used them. We wish to acknowledge with gratitude the assistance of our associate editors. As the chapters came in, a division of editorial labor evolved. Editors at Berkeley (L. E. Caltagirone, D. L. Dahlsten and C. B. Huffaker) reviewed and commented on the manuscripts and returned them to Riv-

Preface and Acknowledgments erside, where the heavily time consuming task of technical editing was performed, mainly by G. Gordh and T. S. Bellows. T. W. Fisher and T. S. Bellows managed the collative technical editing and management of the development of the project. The critique of outside reviewers has been carefully considered and is gratefully acknowledged. Further appreciation is extended to the secretarial staff at the authors' respective institutions for their skill and patience in producing initial drafts for most of the chapters. Special thanks are due to Pam Hoatson (Administrative Assistant, UCR), who prepared numerous revisions of chapters as they developed. Her professional expertise, dedication, and good natured handling of the task are indeed greatly appreciated. C. Meisenbacher and S. Kokel assisted greatly during the proof stage, especially in tracking down missing references. During the gestation of this project, a few of our colleagues have retired from institutions were they long advanced the field of biological control. Among these are L. Andres, J. Beardsley, L. Caltagirone, T. Fisher, D. Flaherty, R. Garcia, K. Hagen, C. Huffaker, C. Kennett, E. F. Legner, J. Maddox, J. McMurtry, and M. Whitten; C. Huffaker and K. Hagen are now deceased. We have enjoyed the privilege of working with these individuals during this project. When we consider the years of experience in the field of biological control represented by the authors who contributed to this Handbook, we recognize more than 1500 scientistyears of expertise, gathered here between two covers. Our thanks to each of them for their patience, endurance, and contribution. And to the reader, our best wishes as you delve into a most rewarding and fascinating field. T. W. Fisher T. S. Bellows, Jr.

UC Riverside, March, 1999

xxiii

R e f e r e n c e s Cited Andrews, K. L. & Quezada, J. R. (1989). Manejo entegrado de plagas insectides en la agricultura. Library School of Agriculture Pan-Americana, Apt. Post. 93, Tegucigalpa, Honduras. 623 pp. Baker, R. R. & P. E. Dunn. 1990 (1989). New directions in biological control: alternatives for suppressing agricultural pests and diseases. Proceedings of a UCLA colloquium, Frisco, Colorado, Jan. 20-27, 1989. Alan R. Liss, Inc., New York. 815+ pp. Davis, D. W., S. C. Hoyt, J. A. McMurtry & M. T. AliNiazee [eds.]. 1979. Biological control and insect pest management. University of California, Division of Agricultural Sciences, Bulletin 4096 (reprinted as Bull. 1911). 102 pp. DeBach, P. [ed.]. 1964. Biological control of insect pests and weeds. Chapman & Hall. 844 pp. DeBach, P. & D. Rosen [eds.]. 1991. Biological control by natural enemies, 2nd ed. Cambridge University Press. 440 pp. Huffaker, C. B. [ed.]. 1980. New technology of pest control. John Wiley & Sons. 500 pp. Maramorosch, K. & R. L. Starkey [eds.]. 1992. Biotechnology for biological control of pests and vectors. CRC Press, Inc., Boca Raton, Fla. Nechols, J., Jr., L. A. Andres, J. W. Beardsley, R. D. Goeden & C. G. Jackson [eds.]. 1992. Biological control in the U.S. western region: Accomplishments and benefits of regional research project W-84, 1964-1989. UC Press (D.A.N.R.) Oakland, CA. Rosen, D. led.]. 1990. World crop pests: armored scale insectsm their biology, natural enemies, and control. Elsevier Scientific Publishers, Amsterdam. 2 vols., 800+ pp. Sweetman, H. L. 1958. The principles of biological control. Wm. C. Brown, Co., Dubuque, IA. 560 pp. Van Driesche, R. G. & Bellows, T. S. Jr. (1996). Biological Control. New York: Chapman & Hall. Waterhouse, D. F. & K. R. Norris. 1987. Biological control: Pacific prospects. Australian Centre for Int. Agricultural Research. Inkata Press, Melbourne. 443 + pp.

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1 Scope and Significance of Biological Control C. B. HUFFAKER and D. L. DAHLSTEN Center for Biological Control 201 Wellman Hall University of California Berkeley, California

The amount of food for each species of course gives the extreme limit to which each can increase, but very frequently it is not the obtaining of food, but the serving as prey to other animals, which determines the average numDarwin on the Origin of Species (1859) ber of a species.

Biological control when considered from the ecological viewpoint as a phase of natural control can be defined as the action of parasites, predators or pathogens in maintaining another organism's population density at a lower average than would occur in their absence P. DeBach (1964, p. 6)

INTRODUCTION Biological control has commonly had both pure and applied definitions and connotations. In this book the authors adhere mostly to DeBach's quotation, with the proviso that parasites, predators, and pathogens include "antagonists" of plant pathogens. The significance of biological control is clear in the quotations from both Darwin and DeBach, residing in the roles such natural enemies have in determining the densities of other organisms in nature and thus their impacts on their environments. Huffaker and Rabb (1984) considered, "Nature as a complex of interacting systems is widely accepted, but many questions remain as to how these systems are arranged and to what degree they are interdependent. To what extent are structure and function deterministic or probabilistic? To what degree should we treat elements of the system

Handbookof BiologicalControl

as relatively fixed or subject to [and altered by] evolutionary change?" These are questions various authors in this book have considered and have offered some insights. DeBach's usage of biological control in the antecedent volume to this book (DeBach, 1964a) was "demographic and ecological in context but does not explain the mechanisms of control or regulation." Bellows and Fisher's preface to this book discusses the various concepts of biological control and its implications in practice. This section also details the beginning of curricular biological control at the University of California and discusses the antecedent volume on this subject edited by DeBach (1964b) for its historical relevance. Readers of this chapter should be sure to read that preface as a prelude to this introductory chapter and the rest of the book. There are some rather basic differences among some chapter authors relative to what is meant by biological control, and in other cases the value of different approaches to evaluating the role of natural enemies. For example, Federici in Chapter 21 includes as biological control certain biotechniques not accepted as such by the authors of many of the chapter. Also, the methods of evaluation of natural enemies utilized by certain authors in the book Critical Issues in Biological Control edited by Mackauer, Ehler, and Roland (1990) differ distinctly from those described in Chapter 2 by Bellows and Hassell, in which they consider that theories of interactions "accord well with observed outcomes of experimental populations in both laboratory and natural settings," especially so for simpler systems. DeBach and Rosen (1991) give data on some 164 species of insect pests being permanently controlled by introduced natural enemies (classical biological control): for 75 Copyright 9 1999 by AcademicPress. All rights of reproduction in any form reserved.

2

C.B. Huffaker and D. L. Dahlsten

species "complete," for 74 species "substantial," and for 15 species "partial" control. Because many of these species were also controlled in more than one country, they noted that up to 1988 there had been some "384 successful projects worldwide." They also state: "This is by far the greatest number of successes achieved by any one non-chemical method, with the possible exception of cultural control, which to our knowledge has not been tabulated." All other nonchemical methods combined would add only a few pest species up to now. It was noted that nearly one-third of the species first controlled in a country were again controlled in other countries. Information is drawn from works of DeBach (1964a), Clausen (1978), Laing and Hamai (1976), and Luck (1984); and from BIOCAT information furnished by D. J. Greathead in 1988 and "some additions from their own records." With the preceding records of "4 successes in 10," directed against only 415 pest species, it is an indictment of environmentally interested sponsorship worldwide that none of the others among some 10,000 species of insect pests (95%) have been investigated for possible importations. Moreover, DeBach and Rosen (1991) note that of some "4226 natural enemy species introduced worldwide, 1251 have become established, 2038 failed, and the fate of 932 is still unknown." This gives an establishment rate of "38% of those with known outcome." Yet, clearly it is not the percentage, or number, of species established, but the success of the project that is important. As often happens, a highly effective species may displace or prevent establishment of less effective competing species, and better biological control commonly results (see "competitive displacement," Huffaker & Messenger 1976; also DeBach & Sundby, 1963; Huffaker & Kennett, 1969). Also, Huffaker et al. (1971) present specific cases where competitive displacements have improved biological control, often with reductions in the complex of enemy species in the system. Successes worldwide have been directly related to the effort expended; for this reason only, such areas as Hawaii (31), California (24), the rest of the United States (20), Chile (16), Australia (13), New Zealand (13), Canada (11), Israel (11), France (11), and Mauritius (10) have had corresponding degrees of success. Moreover, DeBach and Rosen (1991) conclude that the costs of biological control importations are very low compared to the costs of developing pesticides, which are offering declining rewards, and that if all countries expended the effort on biological control that "the leading twelve [do now] the number of problems solved would jump enormously." As seen in this volume, classical importations include only a part of modem biological control. Nechols (1995) discusses the accomplishments and benefits of a number of W-84 control projects in the western United States from 1964 to 1989. Rosen and DeBach (1991) discuss the importance foreign exploration plays in classical biological control. DeBach's definition of biological control (cited earlier)

does not describe the discipline of biological control, which is broader and includes what the profession must do (see Chapters 40 and 41). In that same antecedent volume the density-regulating roles of natural enemies and the mechanisms were discussed by Huffaker and Messenger (1964), including interdependencies and deterministic or probabilistic features, for different types of habitats and weather. These ideas are used and modified by various authors in this book. Biological control of other organisms is exemplified far beyond entomology. Its research and practice have been greatly expanded relative to plant and animal diseases and weed control. It was also utilized very early in attempts to control rats, for example, by use of the mongoose. Davis et al. (1976) also dealt with the use of other vertebrates to control vertebrates, and with the use of disease for control of European rabbit hordes in Australia. Since then, biological control has become an increasingly strong component in a broader vital area, that of conserving and promoting a viable, sustainable agriculture, forestry, and biosphere (see Chapters 26, 29, 34, and 36 to 39). To regulate a population, factors (singly or in combination) must act either in a direct density-dependent way (Huffaker et al., 1971; Huffaker et al., 1984) or in an inverse density-dependent way associated with prey patches within a host generation (Hassell, 1986). Huffaker et al. (1984) dealt at length with the functioning of natural control in general, and with the roles of the specific densitydependent regulating performance of various natural enemies or other negative feedback processes. They noted that even while some such natural control factors may be responsible for density regulation in a specific limited time and place frame, evolutionary processes may be operating to alter the case in time (see Chapters 12, 13, 15, and 23). They presented a chart illustrating that intraspecific competition of predators for prey and the linked intraspecific competition of the prey for hiding places or predator-free space can explain the various manifestations of density regulation for specific biotic and abiotic conditions. They also cited several authors who refer to competition for enemy-free space as a means of reducing the species diversity of herbivorous insects on a particular plant species. Yet, most of the authors of chapters in this book dealing with theory of natural-enemy control of prey (or host) species look at it as linked predator,prey population interaction and do not consider it one of prey competing for predatorfree places. We also present here in Fig. 1, Huffaker et al.'s illustrations of various density-related performance functions for insects and other relevant factors. In this volume, considerable general attention is given to the question of evolutionary processes, for example, in Chapters 15 and 23, and to the question of pesticide resistance in Chapters 13 and 24. It is important now to place the forms of biological control in the context of animal and plant protection

Chapter 1

3

S c o p e a n d Significance of Biological Control

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1 rule is in terms of the distribution of searching parasitoids. Such data, however, are rarely available from natural populations; most of the information is in the form of relationships between percentage parasitism and host density per patch (Fig. 12). Pacala and Hassell (1991), however, show that it is possible to estimate values of all the parameters necessary to calculate the CV2 from such data. In particular, they show that CV2 > 1 from this general model may be approximated as: CV 2 = C I C D - 1

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28

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indicating that heterogeneity at this level ought to be sufficient to stabilize the populations. Interestingly, in 14 of these 18 cases heterogeneity in Ct alone was sufficient to make CV2 > 1. Thus, contrary to the popular view, this analysis suggests that density-independent spatial patterns of parasitism (e.g., Fig. 12 d) may be more important in promoting population regulation than density-dependent patterns. The work of Pacala and Hassell shows how relatively simple models of host-parasitoid interactions can be applied to field data on levels of parasitism in a patchy environment. Such heterogeneity has often been regarded as a complicating factor in population studies, and one that rapidly leads to analytical intractability of models. Clearly, this need not necessarily be so. The CVz > 1 rule explains the consequences of heterogeneity for population dynamics in terms of a simple description of the heterogeneity itself. The rule gives a rough prediction of the effects of heterogeneity and also identifies the kinds of heterogeneity that

Chapter 2 Theoriesand Mechanisms of Natural Population Regulation

29

2.5

contribute to population regulation. Taylor (1993) reviews the application of the CV2 rule as an expression of "aggregation of risk" of attack by a parasitoid and discusses further applications to data on parasitism from natural systems.

2

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.A~ DISCRETE

Age-Structured Systems Insects grow through distinct developmental stages, and hence the concepts of age and stage structure are linked (more closely in some systems than in others). Many of the general models described in the previous sections take some account of developmental stages [Eqs. (4), (10), and (11)]. A more detailed treatment of age or stage structure, however, requires different approaches to developing population models and theories of population regulation. One such approach has been to construct more complex models, often called system or simulation models, which incorporate more biological detail at the expense of analytical tractability. Such models can be used to explore not only population dynamics but also other features such as population developmental rate, biomass and nutrient allocation, community structure, and management of ecosystems. In this chapter, we will be concerned only with those features of such systems that bear on population regulation in ways not directly addressable in the simpler analytical frameworks presented earlier.

Synchrony of Parasitoid and Host Development Insect populations in continuously favorable environments (laboratory populations, some tropical environments) may develop continuously overlapping generations. Interestingly, in the presence of parasitism as a major cause of mortality such populations often exhibit more-or-less discrete generations (Tothill, 1930; Taylor, 1937; Van der Vecht, 1954; Utida, 1957; Wood, 1968; Hassell & Huffaker, 1969; White & Huffaker, 1969; Metcalf, 1971; Bigger, 1976; Banerjee, 1979; Perera, 1987). Godfray & Hassell (1987, 1989) and Godfray et al. (1994) have discussed these findings and have developed both a simulation model and a delayed differential equation model in which they consider an insect host population growing in a continuously favorable environment (with no intraspecific density dependence) that passes through both an adult (reproductive) and preimaginal stages. The dynamical behavior of these systems was characterized by either (1) stable populations in which all stages were continuously present in overlapping generations, (2) populations that were stable but occurred in discrete cycles of approximately the generation period of the host, and (3) unstable populations. These dynamics were dependent principally on two parameters, the degree of contagion in parasitoid attacks, k, and the relative lengths of preimaginal

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RATIO OF PARASITOID-TO-HOST DEVELOPMENTAL TIMES

FIGURE 13 Regions of continuous reproduction, discrete generations, and unstable behavior for a system with developmental asynchrony between host and parasitoid. [After Godfray, H. C. J., & Hassell, M. P. (1987). Nature (London), 327, 144-147.]

host and parasitoid developmental time (Fig. 13). Low values of k (strong contagion) promoted continuous, stable generations. Moderate values of k (less strong contagion) were accompanied by continuous generations when the parasitoid had developmental times approximately the same length as the host, approximately twice as long, or very short. When developmental times of the parasitoid were approximately half or 1.5 times that of the host, discrete generations arose. Unstable behavior arose for larger values of k. Asynchrony between host and parasitoid can thus be an important factor affecting the dynamic behavior of continuously breeding populations, particularly for parasitoids that develop faster than their hosts.

Parasitism and Competition in Asynchronous Systems Utida (1950, 1957) described the dynamics of a hostparasitoid system that had unusual dynamic behavior characterized by bounded, but aperiodic, cyclic oscillations that may well prove to be chaotic (Fig. 14 a). The laboratory system consisted of a regularly renewed food source, a phytophagous weevil, and a hymenopteran parasitoid. Salient characteristics of the system were host-parasitoid asynchrony (the parasitoid developed in two-thirds of the weevil developmental time), host density dependence (the weevil adults competed for oviposition sites and larvae for food resources), and age specificity in the parasitoid-host relationship (parasitoids could attack and kill three larval wee-

30

T.S. Bellowsand M. P. Hassell

Invulnerable Age Classes

vii stages and pupae, but could only produce female progeny on the last larval stage and pupae). Bellows and Hassell (1988) describe a model of a similar system that incorporated detailed age-structured host and parasitoid populations, intraspecific competition among host larvae and adults, and age-specific interactions between host and parasitoid. The dynamics of the model (Fig. 14 b) had characteristics similar to those shown by the experimental populations and distinct from those of any simpler model. In particular, asynchrony of host and parasitoid, the attack by the parasitoid of young hosts (on which reproduction was limited to male offspring), and intraspecific competition by the host were all important features contributing to the observed dynamics. The interaction of these three factors caused continual changes in both host density and age-class structure. In generations where parasitoid emergence was synchronized with the presence of late larval hosts, there was substantial host mortality and parasitoid reproduction. This produced a large parasitoid population in the succeeding generation that, when emerging coincident with young host larvae, killed many host larvae but produced few female parasitoids. The reduced host larval population suffered little competition (because of reduced density). This continual change in intensity of competition and parasitism contributed significantly to the cyclic behavior of the system.

The two previous models both incorporated susceptible and unsusceptible stages, ideas that are inherent to any stage-specific modeling construction for insects where the parasitoid attacks a specific stage such as egg, larvae, or pupa. The consequences of invulnerable stages in a population have been considered by Murdoch et al. (1987) in relation to the interaction between California red scale [Aonidiella aurantii (Maskell)] and its external parasitoid, Aphytis melinus DeBach. Their models include both vulnerable and invulnerable host stages, juvenile parasitoids, and adult parasitoids; they also contain no explicit density dependence in any of the vital rates or attack parameters, but did contain time delays in the form of developmental times from juvenile to adult stages of both populations. Murdoch et al. (1987) developed two models, one in which the adult hosts are invulnerable and one in which the juvenile hosts are invulnerable. They found that either model can have stable equilibria (approached either monotonically or via damped oscillations), stable cyclic behavior, or chaotic behavior. The realm of parameter space that permitted stable populations was substantially larger for the model in which the adult was invulnerable than for the model when the juvenile was invulnerable. Whether or not the stabilizing effect on an invulnerable age class was sufficient to overcome the destabilizing influence of parasitoid

500 (a) O B S E R V E D

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GENERATION FIGURE 14 Observed (a, after Utida, 1950) and simulated (b, after Bellows & Hassell, 1988) dynamics for laboratory host-parasitoid systemswith both developmental asynchronyand host competition.

Chapter 2

Theories and Mechanisms of Natural Population Regulation

developmental delay depended on the relative values of several parameters, but short adult parasitoid life span, low host fecundity, and a long adult invulnerable age class all promoted stability. Many insect parasitoids attack only one or few stages of a host population (although predators may be more general), and hence many populations contain potentially unattacked stages. In addition, however, many insect populations are attacked by more than one natural enemy, and general statements concerning the aggregate effect of a complex of natural enemies attacking different stages of a continuously developing host population are not yet possible. Nonetheless, it appears that, at least for the California red scale-A, melinus system, the combination of an invulnerable adult stage and overlapping generations is likely a factor contributing to the observed stability of the system (Reeve & Murdoch, 1985; Murdoch et al., 1987).

Spatial C o m p l e x i t y a n d A s y n c h r o n y in M e t a p o p u l a t i o n s In predator-prey or parasitoid-host systems that occur in a patchy or heterogeneous environment, we may distinguish between dynamics that occur between the species within a patch and dynamics of the regional or global system. Here we distinguish between "local" dynamics (those within a patch) and "global" dynamics (the characteristics of the system as a whole). Such systems where the entire population is distributed in smaller units, or patches, each with its own intrinsic dynamics, are termed "metapopulations." The properties and dynamics of such metapopulations have received considerable attention, and much research is still addressing questions of biological parameters suited to the investigation of such populations and of suitable mathematical frameworks for use in describing them. Considerable attention has been directed at questions of movement between subpopulations (patches) and at how such movement, combined with unequal distributions of individuals among patches, can affect population dynamics. While still interested in such dynamical behavior as stability of an equilibrium, we also seek to understand what features of the system might lead to global persistence (the maintenance of the interacting populations) in the face of unstable dynamical behavior at the local level (see review by Taylor, 1988). One set of theories concerned with the global persistence of predator-prey systems emphasizes the importance of asynchrony of local, within-patch, predatorprey cycles (Den Boer, 1968; Reddingius & Den Boer, 1970; Levin, 1974, 1976; Maynard Smith, 1974; Crowley, 1977, 1978, 1981). In this context, asynchrony between patches implies that, on a regional basis, unstable predatorprey cycles may be occurring in each patch but out of phase with one another (prey populations may be increasing in

31

some fraction of the environment while they are being driven to extinction by predators in another). Such asynchrony may reduce the likelihood of global extinction and thus promote the persistence of the populations. (This asynchrony in populations among patches is distinct from the developmental asynchrony between host and parasitoid of the three preceding systems.) An example of one such system comes from the model of interacting populations of the spider mite, Tetranychus urticae Koch, and the predatory mite, Phytoseiulus persimilis Athias-Henriot, described by Sabelis and Laane (1986). This is a regional model of a plant-phytophagepredator system that incorporates patches of plant resource that may be colonized by dispersing spider mites; colonies of spider mites may in turn be discovered by dispersing predators. The dynamics of the populations within the patch are unstable (Sabelis, 1981; Sabelis et al., 1983; Sabelis & van der Meer, 1986), with overexploitation of the plant by the spider mite leading to decline of the spider mite population in the absence of predators. When predators are present in a patch, they consume prey at a rate sufficient to cause local extinction of the prey and subsequent extinction of the predator. In contrast to the local dynamics of the system, the regional or global dynamics of the system was characterized by two states. In one, the plant and spider mite coexisted but exhibited stable cycles (driven by the intraspecific depletion of plant resource in each patch and the time delay of plant regeneration). The other state was one in which all three species coexisted. This latter case was also characterized by stable cycles, but these were primarily the result of predator-prey dynamics; the average number of plant patches occupied by mites in the three-species system was less than 0.01 of the average number occupied by spider mites in the absence of predators. The overall system thus persisted despite the unstable dynamics at the patch level (Fig. 15). Principal among the models features that contributed to global persistence was asynchrony of local cycles, making it very unlikely that prey would be eliminated in all patches at the same time. This asynchrony could be disturbed when the predators became so numerous that all prey patches were likely to be simultaneously discovered, thereby leading to global extinction of both prey and predator. These results are broadly in accord with the classic experiments of Huffaker (1958) and Huffaker et al. (1963) (Fig. 16), who found that increasing spatial heterogeneity enhanced population persistence. Three features of these experiments are in accord with the behavior of the model of Sabelis and Laane (1986): (1) overall population numbers did not converge to an equilibrium value but oscillated with a more or less constant period and amplitude; (2) facilitation of prey dispersal relative to predator dispersal enhanced the persistence of the populations (Huffaker,

32

T.S. Bellows and M. P. Hassell 12

Phytophagous mites only system 4

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40 years in northern California with imported natural enemies of Klamath weed, Hypericum perforatum, and a species of Hypericum used for roadside plantings (Andrrs, 1981). The benefits derived from importation of phytophagous arthropods and phytopathogens are so vast when levied against weeds that cannot be controlled effectively, economically, or safely with any other strategy, that biological control will continue to be a major effort. The risk involved has been and should continue to be minimized by the extensive studies required prior to importation. Terrestrial S c a v e n g e r s Terrestrial scavengers include scarab beetles that remove cattle dung accumulated in grazing areas to both improve pastures and control symbovine flies, particularly Haematobia irritans (Linnaeus), Musca autumnalis DeGeer, and M. vetustissima Walker. Although dramatic successes have been achieved in the removal of dung by the importation of several species of exotic scarabs in Australia, Hawaii, California, and Texas (Waterhouse, 1974; Macqueen, 1975; Legner, 1978; Legner & Warkentin, 1983; M. M. Wallace, personal communication), there apparently have been no widespread concurrent reductions of fly densities (Legner, 1986a, 1986b; M. M. Wallace, personal communication). In some instances fly densities may have actually increased temporarily in the presence of established dung-burying scarabs. Although laboratory and field experiments predicted practical fly reductions by the dung-scattering activities of the scarabs, in pastures several forces interplay to thwart experimentally based predictions. Elimination of predatory arthropods and increase of available fly larval breeding habitat could be two of the principal causative factors (Legner & Warkentin, 1983; Legner, 1986a, 1986b). Terrestrial organisms that alter large habitats, such as scarab beetles, are especially risky biological control candidates because their activity may overlap portions of the niche of other beneficial species (e.g., predators) so that potential disruptive side effects among organisms in different guilds exist. The outcome for future symbovine fly control may be limited in that some potentially regulative natural enemies, such as certain predatory arthropods, may be more difficult to establish in the disrupted habitat (Legner, 1986a). In California and Texas, the predatory staphylinid genus Philonthus is severely restrained from colonizing the drier dung habitat created by the activity of the dung beetle Onthophagus gazella Fabricius (Coleoptera:

Chapter 5

93

Exploration for Natural Enemies

Scarabaeidae) (Legner & Warkentin, 1983; Roth et al., 1983; Legner, 1986b). Furthermore, various nongraminaceous weed species often invade California irrigated pastures that sustain large populations of exotic scarab beetles, so that mechanical pasture renovation again is required (Legner, 1986a). Aquatic Vertebrates and Invertebrates Aquatic vertebrates and invertebrates used for biological control include such groups as fish for biological aquatic weed and arthropod control and Turbellaria and Coelenterata for arthropod control. The minnows Gambusia and Poecilia are used worldwide in the biological control of mosquitoes (Legner et al., 1974; Legner & Sjogren, 1984). However, the threat to endemic fish has caused widespread concern so that alternatives in the use of native fish are under consideration (Legner et al., 1975; Waiters & Legner, 1980). Because fish can be manipulated readily, the potential for resident species to increase their effectiveness as natural enemies is greater than that with terrestrial organisms where widespread natural dispersion may have already covered most possibilities. Environmental risks may be minimized when vertebrates such as fish are imported to restricted aquatic ecosystems. Such fish can be studied under natural conditions, but in isolation ponds or in restricted waterways, for adverse effects before being widely disseminated. Yet, there are still possibilities that undesirable unforeseen behavioral and adaptive traits, such as spawn-feeding on other desirable fish species, or an extension of subtropical species into temperate climates (e.g., Gambusia spp.) may be expressed once populations are allowed to establish broadly (Legner and Sjogren, 1984). Careful evaluation of ecological traits of closely related organisms may indicate important differences among candidate natural enemies within these groups. One example is a group of cichlid fish imported from Africa to the southwestern United States for the biological control of mosquitoes, mosquito habitats, and chironomid midges. Tilapia zillii (Gervais), Sarotherodon (= Tilapia) mossambica (Peters), and S. (= Tilapia) hornorum Trewazas were imported to California for the biological control of emergent aquatic vegetation (Scirpus spp., Typha spp., Eleocharus spp., etc.) that provides a habitat for such encephalitis vectors as the mosquito Culex tarsalis Coquillett and, additionally, as predators of mosquitoes and chironomid midges. Studies under natural, but quarantine, areas in California showed that the different fish species each possessed certain attributes for combating the respective target pests (Legner & Medved, 1973). Tilapia zillii was best able to perform both as a habitat reducer (aquatic weed feeder) and as an insect predator. It also had a slightly greater tolerance to low water temperatures, which guaranteed its survival

through the winter months in southern California, while at the same time it did not pose a threat to salmon and other game fisheries in the colder waters of central California. It was the superior game species and was the most desirable for eating. However, the agencies supporting the research (mosquito abatement and county irrigation districts) acquired and prematurely distributed all three species simultaneously throughout thousands of kilometers of irrigation system, storm drainage channels, and recreational lakes. The outcome was the permanent and semipermanent establishment of the two less desirable species, S. mossambica and S. hornorum, over a broader portion of the distribution range. This was achieved apparently by a competitive superiority rendered by an ability to mouth-brood their fry, while T. zillii did not have this attribute strongly developed. It serves as an example of competitive exclusion such as conjectured by Ehler and Hall (1982). In some clearer waters of lakes in coastal and southwestern California, the intense predatory behavior of S. mossambica males on fry of T. zillii could easily be observed, even though adults of the latter species gave a strong effort to fend off these attacks. The outcome was not too serious for chironomid control because the Sarotherodon species were quite capable of permanently suppressing chironomid densities to below annoyance levels (Legner et al., 1980). However, for control of submerged higher aquatic weeds m namely, Potamogeton pectinatus Linnaeus, Myriophyllum spicatum var. exalbescens (Fernald) Jepson, and Hydrilla verticillata R o y l e m and emergent aquatic w e e d s ~ s u c h as Typha s p p . ~ t h e Sarotherodon species showed no capability whatsoever (Legner & Medved, 1973). Thus, competition excluded Tilapia zillii from expressing its maximum potential in the irrigation channels of the lower Sonoran Desert of California and in recreational lakes of southwestern California. Furthermore, because the Sarotherodon species were of a more tropical nature, they died out annually in the colder waters of the irrigation canals and recreational lakes without thermal effluent. Although T. zillii populations could have been restocked, attention was later focused on a potentially more environmentally dangerous species, the white amur Ctenopharyngodon idella (Valenciennes), and other carps. The substitution of T. zillii in storm drainage channels of southwestern California is presently impossible because the Sarotherodon species are permanently established over a broad geographic area.

Parasitic a n d P r e d a c e o u s A r t h r o p o d s a n d Arthropod Pathogens The risk of making wrong choices of parasitic and predatory arthropods and arthropod pathogens, especially hostspecific ones, does not pose obvious environmental threats,

94

E. F Legner and T. S. Bellows

because the outcome of the establishment of an innocuous natural enemy is the pest density remaining at status quo; although there is some theoretical debate on the issue (Turnbull, 1967; May & Hassell, 1981, 1988; Ehler 1982, 1990d). However, arguments have been made that wrong choices could possibly preclude the achievement of maximum biological control (Force, 1970, 1974; Legner, 1986b)malthough theoretical considerations indicate that this would be unlikely (Hassell & May, 1973; Hassell & Comins, 1978)mand add to the list of failures, so that careful decisions are desirable (Franz, 1973a, 1973b, Hughes, 1973). The need for choosing the best biological control candidates has generated considerable discussion and controversy over the past 2 1/2 decades, and continues to stir controversy (Turnbull & Chant, 1961; Watt, 1965; van den Bosch, 1968; Huffaker et al., 1971; Zwrlfer, 1971; Zwrlfer & Harris, 1971; Ehler, 1976, 1982; Zwrlfer et al,, 1976; van Lenteren, 1980; Pimentel et al., 1984; Legner, 1986b). However, the manner in which the best biological control candidates can be chosen is not clearly delineated for most groups of organisms (DeBach, 1974; Coppel & Mertins, 1977; Pimentel et al., 1984); even though there is a common desire for prejudgment, if for no other reason than to expedite a biological control success. Parasitic and predaceous arthropods (Insecta and Acarina) and arthropod pathogens (Nematoda, viruses, bacteria, fungi, etc.) are in a distinct category that usually defies accurate prejudgment of biological control potential. Theoretical guidelines based on laboratory studies and mathematical models are not always useful to judge performance in nature. The extremely small size of parasitic and predaceous arthropods, their high dispersal capacity, unique sex determination mechanisms, differential response to varying host densities and climate, distribution patterns and size, unreliable sample techniques, dependence on alternate hosts, and possibilities of rapid genetic change at the introduction site (Messenger, 1971; Eikenbary & Rogers, 1973; McMurtry et al., 1978; Attique et al., 1980; Mohyuddin et al., 1981; Legner, 1986b) all contribute to the impossibility of making universally applicable judgments about performance under natural conditions. Further, release from attacks by specific hyperparasitoids, cleptoparasitoids, and predators make predictions of their performance highly uncertain. Even sophisticated population models such as those developed for the winter moth, Operophtera brumata (Linnaeus), could not predict the exceptional performance of the tachinid parasitoid Cyzenis albicans Fallrn against this host in Canada (Hassell, 1969a, 1969b, 1978, 1980; Embree, 1971; Waage & Hassell, 1982). Because risks to the environment posed by parasitic and predaceous arthropods are very low, the inability to predict their impact has not been a major obstacle to their deployment in successful biological control. At the same time, selection of these biological control agents for importation

has not been unsophisticated and lacking in scientific judgment as was suggested by van Lenteren (1980). There are valid scientific criteria for determining probable good candidates that are especially useful for elimination of those with little likelihood for success or that possess certain undesirable characteristics such as hyperparasitism (Luck et al., 1981) and cleptoparasitism. A s s e s s i n g Natural E n e m y Potential Coppel and Mertins (1977) proposed a list of 10 desirable attributes of beneficial organisms to aid in assessment of their capabilities prior to widespread dissemination that are closely interrelated and difficult to separate. However, they do categorize organisms and weigh their potential according to a scientific plan. The list, obviously developed from efforts on prior biological control projects, considers ecological capability, temporal synchronization, density responsiveness, reproductive potential, searching capacity, dispersal capacity, host specificity and compatibility, food requirements and habits, hyperparasitism, and culturability. Additional categories of importance to a broad understanding of the niche of a potential biological control agent are systematic relationships and anatomical attributes (fossorial structures, heavy sclerotization, type of spermatheca), physiological attributes (synovigenic or proovigenic), cleptoparasitism, and genetic data (number of founders, collection locality, strain characteristics). Consideration of these attributes in a more holistic approach to natural enemy acquisition is desirable because it incorporates interrelations among qualifications that cannot be detected from an accumulation of single, even well-quantified sets of data. Biological control researchers traditionally have acquired data under these various categories whenever possible, which has greatly aided in the interpretations of the dynamics in biological control successes. However, there has not been a systematized plan for data acquisition and storage. The collection of facts in the different groups is meant not only to form a database for more accurate predictions of success, but also to raise biological control pursuits to a more intercommunicative realm. The absence of a data collection system in the past has unquestionably resulted in the loss of valuable information about biological control organisms. Critics of a more systematized data acquisition scheme point to the weaknesses of data secured in experimental fashion, but overlook the fact that even incomplete data can elevate one's understanding to the "educated empiricism" of Coppel and Mertins (1977). A step toward improving data acquisition (the tracking of field-released beneficial species) has begun in the United States at the U.S. Department of Agriculture Agricultural Research Service (USDA/ARS) Biological Control Documentation Center, Beltsville, Maryland, as described in Chapter 6. A different database, with slightly different emphases, has been

Chapter 5 Explorationfor Natural Enemies developed for biological control programs by the International Institute of Biological Control (Greathead & Greathead, 1992). Although there is even more room for additional information about the natural enemies of a given host to help the foreign explorer, it is becoming increasingly possible to appraise performance in nature. The knowledge comes from a combination of laboratory and field studies both in the places of origin of the respective natural enemies and at their introduction sites. For example, among the parasitoids attacking endophilous synanthropic flies, we find the different natural enemy species naturally distributed within certain ecological zones. Cooler, more humid environments harbor different species and strains than those found in hot and drier areas. Marked seasonal abundances, and host and microhabitat preferences are demonstrated by the different species (Legner, 1986b; Legner et al., 1990; Legner & Gordh, 1992). Thus, it is possible to estimate which species are better suited for biological control in a given area based on knowledge of ecological requirements. Additionally, accumulated information on temporal synchrony with the target hosts allows a high degree of certainty in the prediction of which species is most capable of exerting a regulative effect on a single host species in a multihost habitat (Legner, 1986b). Data on density responsiveness, reproductive potential under different ambient temperatures and humidities, searching capacity in different environments and strata of the host habitat, dispersal rates, host specificity and parasitoid food requirements, systematics, synovigenic characteristics, mass production, and genetic variability provide a base from which to judge the likely performance of particular species in different areas. The data also provide a means to properly sample for host destruction (Legner, 1986b). All parameters probably will never be quantifiable, however, as demonstrated by the discovery of a group of polygenes in parasitic Hymenoptera that begin phenotypic expression in the mother prior to the appearance of her progeny (Legner, 1989, 1991). Such ecological information can also provide better understanding about difficulties faced in prior biological control attempts. For example, in Australia the opinion of some researchers that predatory and parasitic natural enemies of symbovine flies have been duly tested in biological control is based on previous attempts at introduction. However, basic information now available on species that were tried, such as Aphaereta pallipes (Say), Aleochara tristis Gravenhorst, and Heterotylenchus spp., suggests that these candidates were poorly suited to their targeted hosts in the introduced environment. They were incapable of exerting much pressure against them because of different climatic preferences (Legner et al., 1974; Legner, 1986b). Research performed on the pink bollworm, Pectinophora gossypiella; navel orangeworm, Amyelois transitella; and carob moth, Ectomyelois ceratoniae (Zeller) has al-

95

ready laid the foundation for accurate decisions on which species of natural enemies have potential for reducing their respective host densities (Legner & Medved, 1979; Sands & Hill, 1982; Legner & Silveira-Guido, 1983; Naumann & Sands, 1984; Legner, 1986b). Clues were found to which regions of the world might be searched for additional candidates. A common criticism of a systematized approach to data collection and evaluation is a lack of adequate and sustained funding, which suggests that a certain degree of adequacy in financial support ought to be secured before new projects are embraced. More biological control researchers are faced with the necessity for holistic studies with the outcome that basic data are obtained more frequently. An example is the biological control of chestnut gall wasp, Dryocosmos kuriphilus Yasumatsu, in Japan, which was guided largely by data acquired about the natural enemies in their place of origin, China (Murakami et al., 1977, Murakami & Ao 1980). Another example is the Comstock mealybug biological control success in California (Meyerdirk & Newell, 1979; Meyerdirk et al., 1981), which was guided by basic research on natural enemies in Japan (Murakami, 1966). Also, the success of the North American egg parasitoid, Telenomus alsophilae, against the South American geometrid Oxydia trychiata (Bustillo and Drooz, 1977) was based on results of studies on the parasitoid in North America (Fedde et al., 1979).

PLANNING, PREPARATION, AND EXECUTION OF A FOREIGN COLLECTING TRIP Planning a n d Preparation

Permits, Regulations, and Quarantine Facilities The first steps in planning and organizing an exploration trip are to obtain the permits necessary to import the collected material and to coordinate with an authorized importation quarantine facility (see Chapter 6) for handling the shipped material. Permits may be necessary from both national agencies and local (state or provincial) agencies. Separate permits may be required for importation into quarantine and for release from quarantine (as is the case in the United States). Coordination with a quarantine facility should include expected dates of shipments; arrangements for clearance of shipped material through customs and agricultural inspection; and expectations for material handling, sorting, and subsequent shipping of natural enemies to the researcher.

Funding There is a need for a long-term stable commitment so that chronic pest problems can be pursued. Ongoing search

96

E. F Legner and T. S. Bellows

missions usually require a minimum of 12 to 18 months of preparation, and the explorer must have assurance that funds will be available when the trip finally is conducted. Funds should include planning for support staff, space, and facilities in the home institution to handle shipped material while the explorer is overseas. Funds will also usually be necessary for host colony development and maintenance for a period of several months before and after the exploration, as well as for maintenance of any imported natural enemies. Planning funds for the actual exploration trip should include anticipated travel and subsistence costs as well as support for local guides, unanticipated travel, air transport for shipped material, and local purchases of supplies. In some countries local travel to and from field sites must be provided by official experiment station drivers, and funds for this service must also be incorporated into the budget planning process. Additional funding is often desirable to establish cooperative projects of extended collection and shipment with colleagues in foreign locations. Traditional sources of funding include national and state or provincial governments, commodity groups, experiment stations, and universities. Experiment station staff might use sabbatical leaves for extended studies abroad, academic responsibilities permitting. A full-time person might be hired to carry on broad biological field studies abroad, as is currently practiced by the USDA/ARS in biological weed control.

The Explorer/Collector The explorer must have a broad knowledge of the target pest and its natural enemies, including their geographic and host range, host plants, biology, and taxonomy. These duties have often been assigned to full-time foreign explorers, but more recently have been undertaken by academic or professional staff from state or federal agriculture experiment stations or other agencies. These staff are usually scientists already working on the target pest or its close relatives. The explorer must be able to travel, often under adverse circumstances. A knowledge of the languages and customs of the areas where explorations are to be conducted is highly desirable. However, the cooperation of colleagues or contacts (such as former students) in the area being contemplated for search is highly important for maximizing the often compressed time frame within which an explorer may be obligated to perform his or her assignment. Because of personal promotion constraints that require research, publication, and teaching, university academic appointees often cannot afford the time required to thoroughly search for and study targeted natural enemies in the field, either foreign or domestic. On the other hand, because of their own time commitments and responsibilities, it may not be appropriate to ask or expect foreign colleagues to

search and ship to the home quarantine facility the desired natural enemies. Collections for a particular program may also be obtained through the services of intermediary organizations (USDA/ARS will usually respond to requests for natural enemy collection and shipment from U.S. collaborators, and other international organizations, such as the International Institute for Biological Control, are also able to provide such services), but experience has shown that biological control workers who know what they need and who physically participate in the collecting process tend to make a better showing in terms of successful introductions.

Planning the Trip Before departing on the trip, a detailed itinerary should be developed for use in coordination with the quarantine facility and other staff involved in the program. Passports, visas, immunizations, etc. must be obtained, often significantly in advance; and for some countries this may require letters of cooperation or requests from national or provincial officials. Contact with foreign collaborators well in advance of the proposed trip can provide valuable information on suitable times or seasons and locations to be included in the exploration. Where guides will be valuable or necessary, foreign colleagues can often advise on the availability and costs of these services. The purpose of the itinerary in planning with other staff of the program does not preclude alterations in the itinerary once the trip is underway. However, the itinerary should include days and times to expect shipments; and, if possible, dates and times for planned contact by telephone, FAX, or telegram on a frequent basis to apprise the staff of the quarantine facility and home institution on developments and any changes in the expected dates of shipments and other itinerary changes. C o n d u c t i n g the Exploration The previously mentioned realities concerning the explorer notwithstanding, the procedure for setting up a preplanned foreign exploration trip typically involves a literature search, taxonomy studies, and studies of museum material; or possibly voucher specimens and explorers' notes from earlier trips dealing with the same pest, and correspondence with collaborators abroad to determine the best season to search. The latter may include referrals from colleagues, local agricultural extension people, botanists, botanic gardens, and nature preserves (especially in the search area); and a letter of introduction from the host country's consulate to institutions requesting their cooperation and ideally temporary use of their facilities. Permits are then obtained (refer to Chapter 6 for proce-

Chapter 5

Exploration for Natural Enemies

dural details) that involve technical and bureaucratic requirements. In the United States the agency is USDA/ APHIS (Animal and Plant Health Inspection Service). Permits are required not only for importation into the home country, but also often by the host country where regulations may govern the export of living as well as dead (museum) materials. Individual states or provinces may impose further restrictions or conditions on either import or export. Advance arrangements must be made with the receiving quarantine laboratory to assure timely availability of host material. In addition to a valid passport, the necessary visas, and the immunization inoculations, the explorer may wish to obtain and carry letters of authorization from host institutions, USDA, and proper officials in the country of search, showing names of cooperating institutions and/or individual collaborators, as well as a supply of personal business cards. In the host country shipping materials may be difficult to find, so it is prudent to carry essential items, such as shipping boxes, tape, and labels. The field journal recorded by the collector should include names of contacts, villages, farms, host plants, other pests noted, and possible sources of beneficial organisms for other pests. Ideally, photographs should supplement the written record, but even a small camera may pose an unacceptable complication to an already "overloaded" explorer.

Travel The fundamentals of travel for foreign exploration are not different in principle to those of any foreign travel. Nonetheless, some special applications require some discussion. Foreign explorers must travel "self-contained." Necessary supplies include drinking water, water purification tablets, medicine, and high-energy foods. Provision should especially be made for care of the feet (including antifungal medications) because long hours of field work in hot climates will subject them to risk of infection, and for intestinal disorders, that (although unlikely to be life-threatening) can limit time planned for travel and searching. Provisions in the expedition equipment must include all the necessary items for collections and shipment. The explorer should have a thoroughly planned itinerary and tickets before leaving the home country, because tickets can be extremely difficult to obtain in some locations. Nonetheless, the explorer can be flexible and prepared to alter the itinerary should circumstances (such as particularly productive or unproductive collecting in a particular location) warrant.

97

collecting. Local graduate students often are excellent guides. The explorer should collect as much material as possible. Searches are usually for native populations of natural enemies, and these may be at extremely low densities (substantially lower than more familiar pest populations). Accurate field notes should be kept, including notes on habitat types, plant communities, plant species, and host species located, as well as natural enemies found. Maps and photographs can be very helpful in defining search locations precisely. These records are especially valuable in planning future trips. The explorer should be aware that constant field work may be more taxing than customary employment. Suitable precautions (carrying water in the field, wearing hats in warm climates, and not exceeding one's physical limits) should be taken, because these will be important in permitting continued, productive exploration. Provisions should be made to maintain collected material in optimal condition while in the field. This usually will require a small, insulated ice chest or other similar container to limit changes in temperature, together with suitable collecting containers or media.

Processing Collected Material Adequate time should be allowed daily for sorting and processing collected material for storage and shipment. Depending on the amount of material found in the field, time for processing collections may exceed the time spent collecting. Access to a local laboratory facility can be invaluable in providing working space, lights, microscopes, and so on, but in general the explorer should take all the materials and equipment necessary to process collections in a hotel room or similar accommodation. Collected material should be shipped as frequently as necessary to ensure optimal condition of the material on arrival at the quarantine facility. Where possible, natural enemy stages least susceptible to the rigors of transport should be selected for shipment. Such stages would include pupae of holometabolous insects, larvae in diapause (and therefore not requiring food), or eggs; and cadavers, spores, fungal hyphal colonies in agar, etc. might be included for pathogens. Special provisions (such as ice packs and humidity-limiting materials) should be made in packaging the material where variations in temperature or humidity must be restricted during shipment. Additional details concerning packaging and shipping natural enemies are found in Chapter 6.

Collections

Shipping

The assistance of a local scientist can be invaluable in locating habitats or agricultural plantings suitable for

Shipment of collected material should always be by the most effective way possible, which is usually air freight,

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or, where this is impossible, air mail. Shipping via air freight is the preferred method, but the collector may have to hold material for several days pending return to a city with air freight service. Once in the city with such service, travel to an airport facility and making arrangements for shipping can require several hours, and substantial time should be planned for this in the itinerary. Arrangements at the airport can be complicated by language barriers, so the assistance of a local colleague may be helpful. If air mail is the transport method, it is essential that the shipper while at the foreign post office witness application of stamps to the package and (most important) their hand

$50 travelers' checks. An internationally acceptable credit card should also be carried. U.S. explorers who are federal employees on overseas duty, such as USDA staff, may obtain official assistance at U.S. embassies. State and university employees are typically viewed by embassies as traveling citizens (because they are not federal employees) and typically cannot receive special privileges or assistance unless a USDA appointment (as "collaborator," etc.) has been authorized before the trip. Inquiries at USDA and other international laboratories abroad can often yield useful information and assistance, however.

cancellation.

If at all possible, air freight and air mail shipments should be dispatched at a time when the material will arrive in the home country from Monday through Thursday. This will facilitate rapid handling of the package and minimize delays, especially avoiding the delay characteristic of weekend arrivals at ports of entry. Personnel at the quarantine facility should be notified by phone, telegram, or FAX concerning the shipment, including the expected carrier and routing, time of arrival, and the air waybill number; and should also be notified of changes in travel itinerary and expected shipment dates. The external packaging material should bear the necessary permits and address labels to facilitate recognition and handling by customs and inspection personnel. Chapter 6 provides details concerning labeling of contents, escapeproof wrapping, and affixation of proper shipping labels. These procedures must be meticulously performed to avoid delay at the port-of-entry customs and agriculture inspection.

Assistance

The assistance of a local colleague (perhaps a former student or associate of the collector) can be of exceptional value for maximizing the collection effort, especially if a relatively short stay in the area is mandated by prearranged travel itineraries, unexpected delays from local holidays or strikes, inclement weather, etc. Such a person can serve as guide, as driver of a rental vehicle, and as mentor concerning local customs; can expedite entry to private or public properties; and can assist in organizing shipment of collections. By knowing the local language, a host will be able to allay the suspicions or perhaps outfight hostility of the local inhabitants toward the presence of a "strange acting" foreigner. Obviously the collector must be able to pay promptly for expenses incurred. Fluctuating exchange rates can be a problem difficult to anticipate when making longrange plans. Surges in the inflation rate can also create unexpected expenditures. Because of such contingencies, the collector is well advised to carry perhaps 20% more than estimated or anticipated costs in the form of $20 or

Acknowledgments We are grateful to T. W. Fisher, R. D. Goeden, and G. Gordh for their suggestions concerning this chapter.

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Legner, E. F., & Silveira-Guido, A. (1983). Establishment of Goniozus emigratus and Goniozus legneri [Hym.: Bethylidae] on navel orangeworm, Amyelois transitella [Lep: Phycitidae] in California and biological control potential. Entomophaga, 28, 97-106. Legner, E. F., Sjogren, & R. D. (1984). Biological mosquito control furthered by advances in technology and research. Journal of American Mosquito Control Association, 44, 449-456. Legner, E. F., & Warkentin, R. W. (1983). Questions concerning the dynamics of Onthophagus gazella (Coleoptera: Scarabaeidae) with symbovine flies in the Lower Colorado Desert of California. Proceedings of the California Mosquito Vector Control Association, 51, 91101. Legner, E. F., McKeen, W. D., & Warkentin, R. W. (1990). Inoculation of three pteromalid was species (Hymenoptera: Pteromalidae) increases parasitism and mortality of Musca domestica Linnaeus pupae in poultry manure. Bulletin of the Society of Vector Ecology, 15(2), 149-155. Legner, E. F., Medved, R. A., & Hauser, W. J. (1975). Predation by the desert pupfish, Cyprinodon macularius on Culex mosquitoes and benthic chironomid midges. Entomophaga, 20, 23-30. Legner, E. F., Medved, R. A., & Pelsue, F. (1980). Changes in chironomid breeding patterns in a paved river channel following adaptation of cichlids of Tilapia mossambica-hornorum complex. Annals of the Entomological Society of America, 73, 293-299. Legner, E. F., Sjogren, R. D., & Hall, I. M. (1974). The biological control of medically important arthropods. Critical Reviews of Environmental Control, 4, 85-113. Luck, R. F. (1982). Parasitic insects introduced as biological control agents for arthropod pests. In. D. Pimentel (Ed.), Pest management in agriculture, CRC Handbook (Vol 2, pp. 125-284). Boca Raton, FL: CRC Press. Luck, R. F., Messenger, P. S., & Barbieri, J. (1981). The influence of hyperparasitism on the performance of biological control agents. In D. Rosen (Ed.), The role of hyperparasitism in biological control: A symposium (pp. 33-42). University of California Division of Agricultural Science. Macqueen, A. (1975). Dung as an insect food source: Dung beetles as competitors of other coprophagous fauna and as targets for predators. Journal of Applied Ecology, 12, 821-827. May, R. M., & M. P. Hassell. (1981). The dynamics of multiparasitoidhost interactions. American Naturalist, 117, 234- 261. May, R. M. & Hassell, M. P. (1988). Population dynamics and biological control. Philosophical Transactions of the Royal Society of London, Series B, 318, 129-169. McMurtry, J. R., Oatman, E. R., Phillips, P. A., & Wood, C. W. (1978). Establishment of Phytoseiulus persimilis (Acari: Phytoseiidae) in southern California. Entomophaga, 23, 175-179. Messenger, P. S. (1971). Climatic limitations to biological controls. In Proceedings of the Tall Timbers Conference on Ecological Animal Control Habitat Management 3 (pp. 97-114). Tallahassee, FL. Meyerdirk, D. E., & I. M. Newell. (1979). Importation, colonization and establishment of natural enemies on the Comstock mealybug in California. Journal of Economic Entomology, 72, 70-73. Meyerdirk, D. E., Newell, I. M., & Warkentin, R. W. (1981). Biological control of Comstock mealybug. Journal of Economic Entomology, 74, 79-84. Miller, J. C. (1983). Ecological relationships among parasites and the practice of biological control. Environmental Entomology, 74, 79-84. Mohyuddin, A. I., Inayatullah, C., & King, E. G. (1981). Host selection and strain occurrence in Apanteles flavipes (Cameron) (Hymenoptera: Braconidae) and its bearing on biological control of graminaceous stem-borers (Lepidoptera: Pyralidae). Bulletin of Entomological Research, 71,575-581. Murakami, Y. (1966). Studies on the natural enemies of the Comstock

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Sheldeshova, G. G. (1967). Ecological factors determining distribution of the codling moth, Laspeyresia pomonella Linnaeus (Lepidoptera: Tortricidae) in the northern and southern hemispheres. Entomological Review, 46, 349-361. Turnbull, A. L. (1967). Population dynamics of exotic insects. Bulletin of the Entomological Society of America, 13, 333-337. Turnbull, A. L., & Chant, D. A. (1961). The practice and theory of biological control of insects in Canada. Canadian Journal of Zoology, 39, 697-753. van den Bosch, R. (1968). Comments on population dynamics of exotic insects. Bulletin of the Entomological Society of America, 14, 112115. van den Bosch, R. (1971). Biological control of insects. Annual Review of Ecological Systems, 2, 45-66. Van Driesche, R. G., & Bellows, T. S. (1996). Biological control. New York: Chapman & Hall. van Lenteren, J. C. (1980). Evaluation of control capabilities of natural enemies: Does art have to become science? Netherlands Journal of Zoology, 30, 369- 381. Waage, J. K., & Hassell, M. P. (1982). Parasitoids as biological control agents-- a fundamental approach. Parasitology, 82, 241 - 268. Waiters, L. L., & Legner, E. F. (1980). Impact of the desert pupfish, Cyprinodon macularius and Gambusia affinis on fauna in pond ecosystems. Hilgardia, 48(3), 1-18. Waterhouse, D. F. (1974). The biological control of dung. Scientific American, 230, 100-109. Watt, K. E. F. (1965). Community stability and the strategy of biological control. Canadian Entomologist, 97, 887-895. Wilson, A. G. L. (1972). Distribution of pink bollworm, Pectinophora gossypiella (Saund.), in Australia and its status as a pest in the Ord irrigation area. Journal of the Australian Institute of Agricultural Science, 38, 95-99. Zw61fer, H. (1971). The structure and effect of parasite complexes attacking phytophagous host insects. In P. J. den Boer & G. R. Gradwell (Eds.), Dynamics of populations (pp. 405-418). Wageningen: Centre for Agricultural Publishing and Documentation. Zw61fer, H., & P. Harris. (1971). Host specificity determination of insects for biological control of weeds. Annual Review of Entomology, 16, 159-178. Zw61fer, H., Ghani, M. A., & Rao, V. P. (1976). Foreign exploration and importation of natural enemies. In C. B. Huffaker & P. S. Messenger (Eds.), Theory and practice of biological control (pp. 189-207). New York: Academic Press.

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[6 I Quarantine Concepts, Facilities, and Procedures T. W. FISHER

L. A. ANDI~S

Department of Entomology University of California Riverside, California

USDA, ARS Albany, California

INTRODUCTION

addition to the 23 listed by Coulson and Hagan (1986), new quarantine facilities have been constructed at Bozeman, MT (weeds); MD Department of Agriculture at Annapolis (weeds); and University of California at Riverside (UCR), CA (nematodes) (see Table 1 later for explanation of postal and other abbreviations). A new entomology insectary and quarantine facility at UCR was funded in 1998. Worldwide, new, or expanded quarantine facilities have been constructed in many countries (Great Britain, Canada, Australia, Thailand, Mexico, and Germany), and others are planned in the United States. This steady increase in quarantine need and capacity is due in part to (1) increased interest in biological and nonpollutive methods of pest control, and the desire to expand on the many successes already achieved through the importation of exotic natural enemies; (2) the number of new pests that are transported throughout the world each year and that are amenable to biological control; and (3) stricter prerelease information requirements about the behavior and safety of biological control candidates to assure that they will not adversely impact nontarget crops or indigenous flora or fauna. This latter concern often means prolonged studies that tie up quarantine areas for long periods thereby increasing the need for greater quarantine capacity to avoid limiting the amount of materials that can be handled. For example, in the United States, proving the environmental safety of plant-feeding arthropods for biological control of weeds can include studies with as many as 10 to 20 North American native plant species related to the (introduced) target weed. When such studies are not permitted or feasible in the country of origin of the biological control agent, these tests must be conducted in a domestic (U.S.) quarantine facility. Similarly, testing parasites against indigenous

The concept of quarantining materials and organisms to keep unwanted elements from entering new areas originated almost simultaneously with the distinction between "good and bad." Much of the information on excluding unwanted plants and plant pests from world commerce through the use of quarantine has been reviewed by Kahn (1989). Regulations governing the arrival of questionable materials to a country, state, province, or county arose with the establishment of quarantine facilities where transported items could be examined before passing on to their destination and assimilation into the general economy and environment. Ooi (1986) gives a summary overview of biological control quarantine from the perspective of developing countries. In this chapter we focus on movement of beneficial or biological control agents, facilities, regulations, and procedures involved. The primary function of a biological control quarantine facility is to provide a secure area where the identity of all incoming biological control candidates can be confirmed, and unwanted organisms, especially hyperparasites, parasitoids of predators, extraneous host or host-plant material, and so on, can be eliminated. In fact, the quarantine laboratory often represents the last chance to study and evaluate potential biological control agents in the sequence of collection, importation, and release so that only desired beneficial arthropods and/or pathogens will be released. The less known about an incoming organism, the more important the role of the quarantine laboratory becomes. The number of quarantine facilities in the United States certified to handle incoming shipments of biological control agents has increased from 4 to 26 over the past 50 years. In

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Copyright 9 1999 by Academic Press. All rights of reproduction in any form reserved.

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insect species that have been declared legally threatened or endangered and that may be present in areas near or contiguous to insect pest infested agricultural croplands targeted for parasite release may not only require more quarantine space but may also delay or prevent the colonization of newly imported biological control agents. The longer imported biological control agents remain in quarantine to carry out these tests, the greater the risk that subtle genetic changes may occur, altering the potential fitness of the biological control agent. Increasing concern over the quality of the environment is also causing a proliferation of the regulations governing the import and release of biological control agents; and explorer/collectors, quarantine officers, and project scientists are spending more time studying and complying with these domestic and foreign regulations. Air travel has reduced the amount of time required to move shipments of biological control agents from one continent to another, but the proliferation of international airports has spawned a logistical nightmare of unpredictable package routing, delayed agricultural and customs inspection, and unscheduled reloading and shipment to final destination. Frequently, material arrives dead or in weakened condition and on occasion may not arrive. Despite the increasing quarantine work load, current methods of shipping and handling quarantined biological control agents continue to prove highly workable and represent the coevolution of practical experience and regulatory concerns. Worldwide, there have been remarkably few escapes, considering the hundreds of species and millions of specimens that have been processed. This safety record is the result of a surprisingly uniform set of international protocols and procedures that have arisen out of the common problems and concerns shared by quarantine personnel and regulatory officials in each country. An excellent overview of the history and continuing role of quarantine within the context of classical biological control is presented by Coulson and Soper (1989), Coulson et al. (1991), and Ertle (1993). In this chapter, mainly from a U.S. perspective, we discuss the several statutory and technological elements of which the explorer/collector/shipper should be aware and which shape the operation of the quarantine laboratory, beginning with the collection, selection, and packaging of exotic biological control candidates in their native habitat or country of origin until their release from the quarantine laboratory or termination of the study. These include (1) national and state regulations (including required permits) as they pertain to the certification of quarantine facilities and the importation, handling, and release of natural enemies; (2) quarantine laboratory design and equipment; (3) personnel working in quarantine; and (4) quarantine operating procedures. In many respects this information supplements that presented by Fisher (1964), who dealt broadly

with quarantine facilities and handling techniques. Although we emphasize the handling of entomophagous and phytophagous arthropods, the area of our greatest expertise, the principles and general procedures discussed also should be applicable to the quarantine handling of any restricted organism as well as other biological control agents and plant material. Because the main emphasis in the 1964 quarantine article (Fisher, 1964) was on the processing of entomophagous beneficials (the mechanics of which have not changed appreciably) rather than on weed-feeding biological control agents, the latter will receive greater emphasis here.

ESTABLISHING QUARANTINE FACILITIES Minimally, a quarantine facility provides a tight security room for opening and examining incoming shipments of beneficials prior to release to other laboratories for further study, or to cooperators for field release. U.S. Department of Agriculture (USDA) certified quarantine facilities may range from a one- or two-room unit in an existing building (University of California, Davis, CA), to multi-room complex structures designed to meet specific quarantine needs, such as screening (1) weed feeding biological control agents (USDA/ARS, Albany, CA), (2) plant pathogens (USDA/ARS, Frederick, MD), or (3) entomophagous parasites and predators (UCR, CA and USDA/ARS, Newark, DE). A listing of primary biological control facilities in the United States is given in Table 1. A primary quarantine facility is one certified by the USDA (Animal and Plant Health Inspection Service, APHIS) to receive direct shipments from foreign sources that may contain live pest host material as well as the candidate natural enemies. Rigorous screening out of hyperparasites and nontarget arthropods and entomopathogens, along with studies to ascertain the host specificity and safety of releasing the candidate biological control agents, is the primary mission of a primary quarantine facility. If space or the supply of suitable host material is inadequate at the primary quarantine laboratory, the cleared material can be consigned to the secondary quarantine lab for additional prerelease safety and other tests. Location and Utilities Preferably, primary quarantine laboratories are located near (20~ usually prevent facultative hibernal diapause in host insects, depending on the species. Such an environment mimics the natural summer when insects with a facultative hibernal diapause usually continue to reproduce. Daily photophases used to prevent diapause typically range from 16 h for the onion maggot (Tolman et al., 1985) and spruce budworms (Robertson 1985a), to 18 h for the codling moth (Ashby et al., 1985) and the large white butterfly (Gardiner, 1985c), to continuous light for the tobacco hornworm (Baumhover, 1985) and the European corn borer (Guthrie et al., 1985). Some insects, such as the Egyptian alfalfa weevil, have an estival diapause and are active in nature in the spring. New generation adults estivate until fall. Under laboratory conditions of 21~ and a daily photophase of 8 h, at least some individuals of each generation will forego estivation and produce eggs. Chilling insects for several weeks to several months will typically break diapause, whether facultative or obligatory. Egg diapause has been broken in the grasshopper genus Melanoplus by exposure to 10~ for 3 to 12 months (Henry, 1985), in the Douglas-fir tussock moth by conditioning at 5 to 10~ for 4 to 6 months (Robertson, 1985b), and in the hemlock looper by storage at 2~ for 3 to 9 months (Grisdale, 1985a). Examples of chilling require-

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ments to end diapause in larvae include I~ for 18 to 35 weeks for spruce budworms (Grisdale, 1984); and 5 +__2~ for 2 to 6 months for the red oak borer, Enaphalodes rufulus (Haldeman) (Galford, 1985). Similar measures will terminate pupal hibernal diapauses. Tolman et al. (1985) were able to break diapause in the onion maggot by chilling at 1 ___ 0.5~ for 2 to 12 months. The same procedure worked well for the cabbage maggot, except chilling had to be for a minimum of 4 months (Whistlecraft et al., 1985b). Boiler (1985) noted that pupae of the European cherry fruit fly, Rhagoletis cerasi (Linnaeus), required refrigeration at 4~ for 3 to 5 months to break an obligatory diapause. There is, however, a time limit for safely refrigerating insects. The length of diapause conditioning of the egg stage can affect the sex ratio of emerging gypsy moth adults. After a short chilling period of 120 days, the sex ratio of the first 25% of hatching larvae was male biased; after a long chilling period of 180 days, it was female biased (ODell et al., 1985). The obligatory diapause in the univoltine gypsy moth has always been a problem with respect to the mass production of gypsy moth parasitoids and viruses. However, Bell (1996) discovered that KK42, a novel insect growth regulator with antihormonal properties, effectively averted diapause in the gypsy moth. His results showed that KK42 treatment of 14-day-old eggs prevented diapause in 85% of the test populations. Eggs 14 to 15 days old could alternatively be placed into cold storage and retain complete sensitivity to KK42 whenever removed. The egg age at KK42 treatment, or when chilling was initiated, was critical. Eggs had to be held at 25~ for 14 to 15 days postoviposition to withstand prolonged chilling at 5~ and still hatch successfully when once again placed at the higher temperature. However, eggs that were 21 to 22 or 29 to 30 days old when chilling was started were not responsive to KK42 whenever removed, but had to be chilled for 4 to 6 weeks first. These findings will enable development of methods to manipulate diapause in stockpiled gypsy moth eggs for use in biological control programs. Different host-insect stages and different species vary in developmental environmental requirements. Some examples indicate the range of variations and similarities. Phytophagous insect eggs frequently require moisture or high humidity to prevent desiccation, and providing just the fight amount of moisture to maintain the eggs is critical. Singh et al. (1985) held eggs of the light brown apple moth in airtight containers to maintain egg turgidity. However, prevention of fungus contamination required frequent checking of the container to remove condensed moisture. Clair et al. (1987) developed another way to control fungus contamination while providing moisture to eggs. They cut elm leaf beetle egg clusters, Xanthogaleruca luteola (MUller), from elm leaves and placed them on cloth and filter paper in a plastic petri dish. A wick of dental

cotton extending through a basal hole in the petri dish to a water reservoir beneath kept the cloth and filter paper combination moist. Exposure of the eggs to air circulation then prevented stagnant air conducive to fungal growth. This type of system could be useful for maintaining a diversity of eggs. Eggs treated with sodium hypochlorite will desiccate if not held on moist cloth and filter paper. However, closed containers are usually satisfactory for this purpose because the egg treatment also reduces fungal contamination. In producing insects, aperiodic (constant) conditions for temperature and RH are commonly used, with periodic conditions only utilized for lighting. For example, Navon (1985) reared Spodoptera littoralis with a photophase of 16 h at 24~ and 50 to 70% RH. However, sometimes workers use completely aperiodic environmental conditions (i.e., constant temperature, RH, and light) for insect rearing. Insects reared in this manner include the southern armyworm, (Wight, 1985), the lesser peachtree borer (Reed & Tromley, 1985b), the European corn borer (Guthrie et al., 1985), and the tobacco hornworm (Baumhover, 1985). Fluctuating environmental rearing conditions retain and promote insect vigor. For example, Greenberg and George (1985) cited Kamal (1958), who reported that fluctuating temperature and humidity conditions increased the longevity of several laboratory-reared calliphorid and sarcophagid species, as did a larger cage size. Experimental determination of the optimal rearing temperature for each insect and strain is necessary. Orthopterans frequently require high rearing temperatures, although some need cool conditions. McFarlane (1985) found that crickets do best at temperatures between 28 and 35~ When reared at 20~ the mean weight of the emergent adults was greater than at higher temperatures, but they would not reproduce. However, the range grasshopper requires much lower laboratory rearing temperatures than some other species. Willey (1985) reared the various stages at 22~ and variable RH, with a photoperiod of 12 h. With these conditions, completion of a generation occurred in an average of 6 months. Temperatures above 30~ resulted in lower hatch and weak grasshoppers. A few insects change forms (morphotypes) depending on rearing conditions. Forbes et al. (1985) reported that aphids reproduced parthenogenetically at 20 _+ I~ with a photophase of 16 h. The production of sexual forms required a maximum photophase of 8 to 12 h with a temperature of 15~ or less. Medrano and Heinrichs (1985) indicated, however, that nymphal density and food availability governed production of the two distinct morphotypes of the brown plant hopper, Nilaparvata lugens (St~l). They noted that a short-winged form developed with low nymphal density and plentiful food, whereas a long-winged form developed under opposite conditions. Humidity, moisture, and substrate are often critical for

Chapter 7

Culture and Colonization

insect pupation. Baumhover (1985) noted that pupation requirements of the tobacco hornworm are precise, and RH close to 85% is necessary for adult ecdysis. A dehumidifier may be necessary to remove air moisture, because each prepupa loses 4 ml of water by the time of ecdysis. Further, prepupae require complete darkness to make them inactive, and must be held individually in flat cells to allow proper pupation. Pupal hardening must precede harvesting, because injury of teneral pupae occurs easily. Similar considerations of substrate moisture and pupal handling are important in rearing fruit flies for the mass production of parasitoids (Wong & Ramadan, 1992). Pupation substrates for various insects include sand for the potato tuberworm (Etzel, 1985) and Hippelates eye gnats (Legner & Bay, 1964, 1965), sawdust for the Queensland fruit fly (Heather & Corcoran, 1985), a sawdust and ground corn cob mixture for the lesser peach tree borer (Reed & Tromley, 1985b), vermiculite for Spodoptera littoralis (Navon, 1985), and plastic soda straws for the greater wax moth, Galleria mellonella (Linnaeus) (Eischen & Dietz, 1990). The pupation medium can be quite critical, as it is in rearing the southern armyworm. Wight (1985) noted that vermiculite used for this insect must be no larger than 6-mm mesh, and must have the proper moisture content (400 ml of water in 1200 ml of vermiculite). If the medium is too wet, there is high pupal mortality, and if too dry, dead pupae or defective moths result. Lighting conditions seem to be of particular importance to adult insects. The photoperiod for rearing the immature insects can even affect the subsequent adults. For example, McFarlane (1985) found a dramatic photoperiod effect on the house cricket, Acheta domesticus (Linnaeus), with adults surviving up to twice as long with a 14-h nymphal rearing photophase as they do with a 12-h one. Adults of many insects mate and oviposit best when provided with natural light through laboratory windows. Such insects include the Queensland fruit fly (Heather & Corcoran, 1985); the saltmarsh caterpillar, Estigmene acrea (Drury) (Vail & Cowan, 1985); and the light brown apple moth (Singh et al., 1985). Lighting conditions required for different species vary greatly. Robertson (1985a) reported that spruce budworm adults mated most successfully in darkness within 24 h after emergence, and optimal oviposition also occurred in the dark at 23 to 26~ Robertson also noted that the best laboratory conditions for oviposition by the Douglas-fir tussock moth were complete darkness and 23 to 26~ (Robertson, 1985b). However, hemlock loopers required a lightdark cycle (Grisdale, 1985a). Sometimes adults mate and oviposit best if provided with a weak light during the scotophase. Guy et al. (1985) held cabbage looper moths under a photophase of 14 h, with a 0.25-W night light during the scotophase. Leppla and Turner (1975) earlier had shown that maximum fecund-

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ity of the cabbage looper was possible with low-intensity night illumination. Gardiner (1985b) likewise provided low-intensity light during scotophase by placing a 7.5-W bulb at a distance of 3 to 6 ft from Mamestra brassicae to stimulate mating and oviposition. He used a 60- to 100-W bulb at the same location during the 12-h photophase. Guthrie et al. (1985) employed a slight asynchrony in light and temperature phases to provide for mating and oviposition by European corn borer moths, with two more daily hours of higher temperature than of light. They used a room temperature of 27~ for 16 h, and of 18 to 20~ for 8 h. The lights were on for 14 h, starting 1 h after initiation of 27~ Temperature can obviously be critical by itself, however, without interacting with the photoperiod. Tolman et al. (1985) showed that survival and fecundity of the onion maggot were substantially greater at 20~ than at 15, 25, or 30~ Humidity must also be considered in providing optimal mating and oviposition conditions. Leppla (1985) reported that the velvet bean caterpillar mated and oviposited best with a RH higher than 80%, and with a source of liquid food. Wight (1985) held the oviposition cage for southern armyworm moths over a pan of water, and covered the cage with black cloth to encourage oviposition. The humidity in the cage had to be more than 50% to obtain good mating, oviposition, and egg hatch. Mating can sometimes be quite difficult to achieve in the laboratory, and may involve a variety of factors. Although Reed and Tromley (1985b) reared the lesser peach tree borer under aperiodic conditions, they held the adults under a 16-h photophase for mating and oviposition, and noted that proper environment was important to achieve mating, with outdoor conditions used when possible. Indoor conditions required adequate lighting and ventilation (to avoid pheromone accumulation). Moths observed in copula were removed, and the females were used for oviposition. Density may affect optimal mating and oviposition. Laboratory mating and oviposition of the large white butterfly required a relatively large cage (100 x 90 x 75 cm) that contained 200 adults (Gardiner, 1985c). Tobacco hornworm moths likewise required a large cage (137 X 121 X 125 cm), but for just 50 pairs (Baumhover, 1985). Lowlight conditions were also necessary (25-W light for 12 h and rheostat-reduced 7.5-W light for 12 h). On the other hand, a high density was not detrimental to mating and oviposition of the spruce budworm. Grisdale (1984) reported that placing up to 300 pairs of these moths into a screened cage (35 X 35 X 25 cm) did not impair oviposition. Even members of the same insect family can vary dramatically in ease of laboratory mating and oviposition. This is certainly true of the mosquito family Culicidae. Friend and Tanner (1985) reported that Culiseta inornata (Willis-

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ton) males often initiate mating before females have completely emerged, without special flight cages. Munstermann and Wasmuth (1985a) noted that Aedes aegypti (Linnaeus) also mates easily in confined spaces. However, these workers had to use beheaded, impaled males of the eastern tree hole mosquito, Aedes triseriatus (Say), in a forced copulation technique (Munstermann & Wasmuth, 1985b). They observed, however, that the Walton strain of A. triseriatus mated satisfactorily in a cubical cage of at least 60 cm 3. Bailey and Seawright (1984) reviewed a system useful to achieve rapid laboratory colonization of Anopheles albimanus Wiedemann, a vector of malaria, and discovered that field-collected females individually placed in 5-dram vials would produce more than 100 times the number of eggs of an equal number (500) of females placed together in a single cubical cage of 61 cm 3. The degree of clustering of ovipositing adults and the amount of space provided can affect fertility as well as oviposition, and is a production program factor. Although not directly related to the physical environment, the age of adult insects is a further consideration for mating and oviposition. ODell et al. (1985) noted that gypsy moth females would not mate once they began to lay eggs. Codling moth adults held for more than 5 days before mating had considerably reduced fecundity (Singh & Ashby, 1985). Similarly, Grisdale (1985b) recommended mating female moths of the forest tent caterpillar as soon after eclosion as possible for optimal results. Frequently, insects will have a preoviposition period between emergence and oviposition, during which they feed and develop eggs. For example, adult cabbage maggots have a preoviposition period of 6 to 7 days at 19 ___ I~ (Whistlecraft et al., 1985b), and adult onion maggots have a similar period but at 22 +__ I~ (Tolman et al., 1985). After insects have appropriate mating conditions, they need ovipositional stimulants. Insects that lay eggs in crevices will often oviposit on crinkled wax paper or on cloth. A good oviposition substrate for the hemlock looper is a six-layer-thick cheesecloth (Grisdale, 1985a), and Reed and Tromley (1985b) provided moist cotton balls to motivate the lesser peachtree borer to oviposit. Other insects can be far more fastidious in their ovipositional requirements, with ingenious systems necessary. Heather and Corcoran (1985) used hollowed-out half apples as an ovipositional substrate for the Queensland fruit fly to enable easy egg collection, and Boiler (1985) devised a clever dome made of ceresin wax that served as an oviposition substrate for the European cherry fruit fly. In the automated mass production of the melon fly, Bactrocera (= Dacus) cucurbitae Coquillett, Nakamori et al. (1992) used cylindrical plastic oviposition receptacles perforated with numerous holes and containing a cellulose sponge saturated with diluted tomato juice. Baumhover (1985) described artificial leaves composed of

outdoor carpeting sandwiched between layers of polypropylene, which served as substitutes for tobacco leaves, and were sprayed daily with a tobacco leaf extract to stimulate oviposition by tobacco hornworm moths. Behavior

Knowledge of insect behavior is obviously crucial to designing a successful rearing program. This is evident in devising an ovipositional substrate and stimulus. B lenk et al. (1985) discovered that six of seven reared noctuid species would oviposit on the underside of a paper towel on top of an oviposition cage, whereas the black cutworm, Agrotis ipsilon (Hufnagel), would only oviposit on paper toweling in the bottom of the unit. On the other hand, Guthfie et al. (1985) observed that European corn borer moths would oviposit only on smooth surfaces; and Hartley (1990) reported that polyester-cotton cloth used for oviposition by Heliothis spp. had to be replaced by a polyester-cotton cloth with a dimpled surface for oviposition by the beet armyworm, the velvetbean caterpillar, and the soybean looper, Pseudoplusia includens (Walker). Chemical ovipositional stimuli may also be necessary. Adult seed corn maggots oviposit in response to moist soil, decaying vegetation, germinating seeds, and metabolites produced by seed-borne microorganisms (Whistlecraft et al., 1985a). Likewise, rearing of the biological control agent Weiseana barkeri Jacoby, a chrysomelid that feeds on Acacia nilotica, requires the use of A. nilotica foliage to stimulate oviposition into strips of corrugated cardboard (Marohasy, 1994). On the other hand, insect-produced chemicals may deter oviposition. Boller (1985) found that the European cherry fruit fly and the Mediterranean fruit fly produced oviposition-deterring pheromones that lowered egg deposition in artificial devices. Consequently, the devices needed frequent washing. Insect responses to stimuli can simplify rearing. For example, the positive phototaxis of scale crawlers makes them easily collected. Papacek and Smith (1985) lighted a rearing room for oleander scale 2 h before work began so scale crawlers would accumulate on top of butternut pumpkins. Such positive phototaxis is a common attribute of many insects and is similarly useful in their collection. In some cases the combining of behavioral characteristics may be disadvantageous. Grisdale (1985a) reported that first-instar hemlock loopers are strongly photopositive and active, but also cannibalistic. Because the larvae drink readily, a light spray of distilled water and retention in the dark at 18~ reduce cannibalism. Light can also affect insect emergence. Willey (1985) noted that range grasshopper nymphs hatch from eggs daily about 5 to 8 h after the start of the light cycle, so daily collection is timed accordingly. Similarly, Boller (1985)

Chapter 7

Culture and Colonization

observed that the European cherry fruit fly and the Mediterranean fruit fly both emerge mostly during the moming and oviposit in the afternoon.

Techniques There are many and varied techniques for arthropod rearing. Some were previously mentioned, and other examples follow. Stockpiling refrigerated hosts is very helpful. Determination of the effects of refrigerated host material on parasitoid and predator production must be on a case-by-case basis. Legner (1979b) found that successful refrigeration of housefly pupae used to rear three pteromalid parasitoids could only occur at 10~ for 100) in the laboratory. After studying heterozygosity and effective size in laboratory populations of the aphidiid Aphidius ervi Haliday, Unruh et al. (1983) warned that genetic drift and loss of heterozygosity are more severe than would be expected from the number of individuals used to maintain cultures. Discussed were factors that make effective population sizes much smaller than would be apparent, including fluctuations between generations, haplodiploidy, sex linkage, highly variable progeny production by individual females, and highly skewed sex ratios.

Chapter 7

Culture and Colonization

Omwega and Overholt (1996) found that the effective population sizes for two geographic laboratory colonies of the braconid Cotesia flavipes Cameron from Pakistan were estimated at 3.4% and 9.0% of the number of breeding females used to continue the colonies. Approximately 1000 breeding females were used to perpetuate each colony during the first 12 laboratory generations, and during this time there was actually a slight increase in heterozygosity at the MDH (malate dehydrogenase) genetic locus in each colony. However, during the next 10 generations, only 500 females were used per generation, and there was a rapid decrease in genetic variation, as measured by electrophoresis. Therefore, using 1000 mated females to perpetuate the C. flavipes colonies maintained greater genetic variation than using 500 females. Culture Maintenance and Inbred Lines

Another procedure for maintaining genetic variability in cultures, as recommended by Bartlett (1985), Joslyn (1984), Roush (1990), and Roush and Hopper (1995), is to develop and maintain a number of inbred subcultures. Joslyn (1984) suggested that the subcultures be exposed to different variable rearing environments on a rotating schedule. Individuals from these subcultures are systematically outbred to achieve hybrid vigor in progeny that are to be field released. Outcrossing and reisolating the strains are advisable after 4 to 6 generations to prevent development of isolating mechanisms that could result in hybrid degeneration. Roush and Hopper (1995) calculated that 25 single family lines for arrhenotokous species, or 50 lines for diploid species, are needed to preserve the common alleles that seem most likely to be important for field performance. Joslyn (1984) and Roush and Hopper (1995) also indicated the importance of maintaining a high effective population size (e.g., 500) in each subculture to reduce the possible decrease of variability caused by random drift and inbreeding. Cook (1993a), in an analysis of prevention of diploid male production in parasitic Hymenoptera, suggested that maintenance of both a single large culture as well as multiple small subcultures might be best because of the biological attributes of a given host-parasitoid system. Legner and Warkentin (1985) have also suggested that one way to keep a broader range of genetic variability is to culture several separate lines from an explorer's initial acquisitions, especially because severe consequences of the founder effect that would reduce genetic variability occur in the first few generations of culture (Legner, 1979a; Unruh et al., 1983). Although each culture might assume great homozygosity in time, different cultures would be homozygous for different characteristics through random founder effects. Specimens from the lines could then, if desired, be intermated prior to field release to restore genotypic variation via hybridization (Hopper et al., 1993). However, there

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are insufficient data to decide whether homo- or heterozygosity is preferable in establishing beneficial species (Legner & Warkentin, 1985). Unruh et al. (1983) (also see Chapter 4) considered the procedure of maintaining many inbred lines with periodical mixing to attempt restoration of variability to be an uncertain technique, and instead preferred to maintain large cultures. Unfortunately, because exotic collections of entomophages might yield very few founder individuals, sustaining genetic variability might require the maintenance of subcultures. A method of reducing labor and material resources for maintaining genetic lines is to use cold storage. Gilkeson (1990) cold-stored cocooned last instars of the predatory cecidomyiid Aphidoletes aphidimyza (Rondani) for 8 months to preserve genetically important lines. Similarly, Tauber et al. (1993) stored diapausing adults of the common green lacewing for 31 weeks at 5~ with very good results; and recommended this approach for maintaining standardized stock for long-term ecological, physiological, or genetic research. Culture Maintenance and Periodical Infusions

One approach to reduce loss of genetic variability in laboratory cultures from drift, selection, and inbreeding is to periodically introduce native individuals. Joslyn (1984) commented that simulating "migration" by occasionally adding wild specimens to the laboratory culture would also add new alleles. This introduction must be proportionately large enough to fix the new alleles into the population. One danger of the technique is the possible introduction of an unwanted insect disease, although Stone and Sims (1992), as well as Davis and Guthrie (1992), noted that using wild males to mate with laboratory females reduces this hazard. According to Bartlett (1984), the effectiveness of periodical infusions depends on regular introductions of relatively large numbers of individuals. These individuals are preferably obtained from the geographic area of collection because of possible incompatibility in intraspecific crosses between spatially and/or temporally separated populations. Data on Muscidifurax parasitoids support this idea (Legner, 1988c). Bartlett (1984) also remarked that without regular introduction of native alleles, selection would reestablish the previous laboratory allele frequencies. Further, the combined processes of selection and inbreeding would have definite rapid effects on changing these frequencies. Chandra and Avasthy (1988) found that new stock of the tachinid Sturmiopsis inferens Townsend had to be introduced into the laboratory culture after three generations to restore the loss of parasitoid vigor due to inbreeding. King and Morrison (1984) felt that periodic replacement of a culture with field-collected material is costly; instead they recommended the routine monitoring of behavioral traits coupled with techniques to maintain essential characteris-

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tics, and even suggested selecting for desirable traits in mass-produced entomophages. However, in the mass production of Trichogramma spp., they stressed the need for annual culture replacement. They further recommended that culture replacement should only be from the target host on the affected crop, and in large enough numbers (>2000) to ensure a broad genetic base.

Culture Maintenance and Environmental Conditioning Bartlett (1985) recommended rearing founder individuals as nearly as possible in natural environmental regimes and densities in the laboratory. Joslyn (1984) indicated that, "A static environment leads to a static genotype and ultimately to less fit insects." The laboratory population exposed to variable "natural" environmental regimes must be large enough to allow random mating to preserve genotypic variability. When few entomophages can be field collected, varying the laboratory environment can at least maintain a pressure for adaptive fitness. In addition to maintaining a field-type laboratory rearing environment, Hopper et al. (1993) advocated forcing parasitoids to search for mates or hosts as they would have to do in nature.

Culture Maintenance and Monitoring In obtaining and maintaining genetic variability in the laboratory, it is first important to study the biology and behavior of a species very well so that information is available to compare attributes of the wild and domesticated populations, which will thereby enable detection of genetic differences (Bartlett, 1985). Hopper et al. (1993) repeatedly stressed that such genetic contributions to trait differences must be determined by reciprocal crosses or half-sib analyses, to eliminate poor nutrition and disease as contributing factors. Singh and Ashby (1985) observed that in establishing a new laboratory culture, the first genetic selection to occur would be of developmental traits such as a shortened life cycle. Behavioral, physiological, and biochemical selection follows. Therefore, it is necessary to establish standards and tolerances for insect quality testing when newly colonized insects are still genetically close to the wild population. Galazzi and Nicoli (1996) did that when they determined intrinsic rate of natural increase values for the predatory mite Phytoseiulus persimilis Athias-Henriot at the time of field collection and after a year of mass production. They concluded that 1 year of mass rearing did not affect the potential of population increase of P. persimilis and that the substitution of the mass-reared strain therefore did not appear to be necessary if a large stock of predators is maintained. They also felt that field collection of wild predators to replace the mass-reared strain would involve the risk of inducing genetic bottlenecks during the initial laboratory

population increase. Hsin and Getz (1988) suggested that monitoring developmental variation in insectary cultures with an appropriate life table might be very useful in maintaining genetic viability.

Culture Maintenance Following Field Establishment As soon as a released beneficial organism is field established, it is desirable to frequently collect individuals for further laboratory culturing and/or for translocation to other localities. A successfully field-established organism is often more vigorous and fit after confronting the hazards of nature during reproduction and development than is one raised in insectary conditions. Waage et al. (1985) also advocated the use of this procedure, believing that the preservation of genetic variability and insect quality required culturing entomophages only briefly before field release. Field collections of established entomophages could then serve as sources for initiating new laboratory cultures. They further recommended climatic matching of release areas to the source areas to facilitate greater ease of entomophage establishment. In concluding this section on the genetics of parasitoids and predators in culture, it is well to remember that not all laboratory culture deterioration is the result of genetic factors. Nutritional or environmental factors can also cause deterioration and might be correctable with no long-term effects, as noted by Bartlett (1985). In fact, Hopper et al. (1993), after reviewing genetic aspects of biological control, concluded that laboratory colony deterioration is more probably caused by poor nutrition and particularly by disease than by genetic changes. Culture a n d S y n t h e t i c Diet Singh (1984) reviewed work on rearing entomophagous parasitoids on synthetic diet; and noted that success to that date had been obtained with two ichneumonids, Itoplectis conquistor (Say) and Exeristes roborator (Fabricius); one trichogrammatid, T. pretiosum; and a pteromalid, Pteromalus puparum. Bratti (1990b) gave a detailed review of in vitro rearing techniques for entomophagous parasitoids, and observed that the extensive literature revealed that most work was still experimental, although Trichogramma spp. could be reared continuously on artificial diet. In a notable article, Dai et al. (1988) gave an account of rearing Trichogramma spp. on artificial eggs and then releasing them by the hundreds of thousands in cotton fields and pine forests in China, where the rate of parasitism was said to be similar to that of parasitoids reared on natural host eggs. Li (1992) also reported on the in vitro mass production and field release of Trichogramma spp., as well as that for another egg parasitoid, the eupelmid Anastatus japonicus Ashmead. The parasitoids were said to show good effectiveness in

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controlling cotton bollworms, pine caterpillars, sugarcane borers, and litchi stinkbugs in China. Other work on the in vitro culturing of parasitic hymenopterans has included that done on the following egg parasitoids: various species of Trichogramma (Parra & Consoli, 1992; Grenier et al. 1993, 1995; J. F. Liu et al., 1995; Z. C. Liu et al., 1995; Consoli & Parra, 1996, 1997; Nordlund et al., 1997; Xie et al., 1997); the eupelmids Anastatus sp. (Li et al., 1988; Liu et al., 1988a) and A. japonicus (Xing & Li, 1990); the scelionids Telenomus dendrolimusi Chu (Li, 1992), T. heliothidis Ashmead (Strand et al., 1988), and Trissolcus basalis (Wollaston) (Volkoff et al., 1992); and the encyrtids Ooencyrtus kuvanae Howard (Lee & Lee, 1994), O. nezarae Ishii (Takasu & Yagi, 1992), and O. pityocampae (Mercet) (Battisti et al., 1990; Masutti et al., 1992, 1993). In vitro culturing of larval ectoparasitoids has occurred for the pteromalids Dibrachys cavus (Walker) (Li, 1992) and Catolaccus grandis (Burks) (Guerra et al., 1993), and for the braconids Bracon greeni Ashmead (Xie et al., 1989b; Li 1992) and B. mellitor Say (Guerra et al., 1993). Guerra et al. (1993), in particular, were notably successful in culturing C. grandis and B. mellitor, both ectoparasitoids of the boll weevil, on an artificial diet devoid of insect components. Guerra and Martinez (1994) and Rojas et al. (1996) made later improvements to the artificial culture of C. grandis. Attempted in vitro culturing of hymenopterous larval endoparasitoids has also occurred, including the following: the braconids Cardiochiles nigriceps Viereck (Pennacchio et al., 1992), Habrobracon hebetor (Say) (Xie et al., 1989a; Li, 1992), and Microplitis croceipes (Cresson) (Greany et al., 1989; Ferkovich et al., 1991); and the chalcidid Brachymeria intermedia (Dindo, 1990, 1995; Dindo & Campadelli, 1993; Dindo et al., 1995). In addition to the preceding hymenopterous egg and larval parasitoids, an effort was made to culture an aphidiid, Lysiphlebus fabarum (Marshall) (Rotundo et al., 1988). Considerable effort has been devoted to the in vitro culturing of tachinids as well. Nettles (1986) was able to obtain relatively good yields of Eucelatoria bryani, a specific parasitoid of Heliothis spp., by raising it first in H. virescens for 20 to 28 h and then on an artificial diet supplemented with defatted, toasted soy flour. Bratti and D'Amelio (1994) and Bratti and Nettles (1995) further experimented with artificial diets for E. bryani. Others have worked with unnatural diets for culturing Pseudogonia rufifrons Wiedemann (Bratti, 1990a; Fanti, 1991; Bratti & Benini, 1992; Dindo & Campadelli, 1993). Fanti (1991) and Bratti and Benini (1992) indicated that host ecdysone in the diet was important to the development of P. rufifrons. Attempts at the in vitro rearing of Lydella thompsoni Hertig and Archytas marmoratus (Town.) yielded very limited results (Bratti, 1994). However, Mellini et al. (1993) reported on the successful in vitro culturing of Exorista larvarum. This success was followed by considerable work on refin-

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ing the in vitro diet with less expensive ingredients, and on developing techniques aimed at eventual mass production of the tachinid for augmentative control of lepidopterans feeding on tree foliage (Bratti & Campadelli, 1994; Mellini et al., 1994; Bratti & Coulibaly, 1995; Bratti et al., 1995; Mellini & Campadelli, 1996). Mellini et al. (1996) indicated that E. larvarum was relatively easy to rear in vitro because it is a gregarious larval idiobiontic parasitoid that can attack many Lepidoptera, because it has a simple relationship with its host, and because the larvae can produce primary integumental respiratory funnels either in the host or in the gelled diet so that they can display similar behavior in either. The major problem remaining in developing a mass production system is that E. larvarum oviposition on artificial substrates has not yet been obtained. Researchers have also developed artificial diets for larvae or nymphs of predaceous arthropods, including the neuropterans Chrysoperla carnea (Hasegawa et al., 1989; Letardi & Caffarelli, 1989, 1990), Chrysopa septempunctata Wesmael (Kaplan et al., 1989; Niijima, 1995), and C. scelestes Banks (Gautam & Paul, 1987). Work on diets for coccinellids includes that of Hussein and Hagen (1991), Henderson and Albrecht (1988), Chen et al. (1989b), and Hattingh and Samways (1993). There has been considerable effort in culturing the predaceous lygaeid Geocoris punctipes on prepared diets (Cohen, 1981, 1985, 1992; Hagler & Cohen, 1991), and Grenier et al. (1989) have attempted to rear the mirid Macrolophus caliginosus Wagner on artificial media. Saavedra et al. (1992) experimented with an animal tissue based diet for the pentatomid Podisus connexivus Bergroth, and Saavedra et al. (1995, 1996) obtained development of P. nigrispinus (Dallas) on meat-based diets. Zanuncio et al. (1996) similarly used a meat-based diet to rear the pentatomid Supputius cincticeps (Stal) for two generations, and De Clercq and Degheele (1992) reported on a meat-based diet for P. maculiventris and P. sagitta (Fabricius). Sumenkova and Yazlovetskii (1992) also worked with P. maculiventris (Say), and developed an adequate artificial diet based on pupal homogenate. The predaceous phytoseiids Amblyseius gossipi E1-Badry and A. swirskii Athias-Henriot were reared successfully on artificial diet by Abou-Awad et al. (1992), but Shih et al. (1993) found two artificial diets to be unsatisfactory for rearing A. ovalis (Evans). Waage et al. (1985) noted that the greatest success in the development of artificial diets for entomophagous parasitoids had been with polyphagous parasitic wasps. Although there has been progress on rearing predaceous entomophages on artificial diets, production for field release still involves living or dead hosts in almost all cases. For future success in rearing entomophages on artificial diet, Yazlovetsky (1992) emphasized the importance of accumulating further knowledge of their physiology, nutritional and digestive biochemistry, and ecology.

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Interactions b e t w e e n E n t o m o p h a g e s , Hosts, a n d H o s t Food Entomophage quality can be dependent on host quality, and in turn on host-food quality. Singh (1984) referred to two examples of interactions between prepared diets, herbivores, and natural enemies. Rearing the Asiatic rice borer, Chilo suppressalis (Walker), on artificial diet adversely affected its braconid parasitoid, Apanteles chilonus Munakata. Similarly, the tachinid Lixophaga diatraeae declined in quality when reared on larvae of the greater wax moth, unless vitamin E or wheat germ supplemented the larval beeswax pollen diet. Bloem and Duffy (1990) concluded that qualitative and quantitative protein differences in the diet of Heliothis zea affected growth of the endoparasitoid Hyposoter exiguae (Viereck), and Magrini and Botelho (1991) studied the influence of dietary proteins in the diet of Diatraea saccharalis on the egg parasitoid Trichogramma galloi Zucchi. Similarly, Bratti (1992) showed that development of the tachinid Archytas marmoratus was influenced by the diet of its factitious host, the galleriid Galleria mellonella Linnaeus. ODell et al. (1984) reported that only one of three artificial diets was suitable for culturing Rogas lymantriae on gypsy moth larvae. On the other two diets the host larvae died shortly after parasitoid oviposition. The same parasitoid had significantly higher female weights when reared on gypsy moth larvae grown on a high wheat germ diet than when grown on a commercial diet (Moore et al., 1985). Artificial diet for the host insect can sometimes result in greater parasitoid production than does natural food. Rogers and Sullivan (1991) studied development of the pupal parasitoid Brachymeria ovata (Say) on three noctuid hosts reared on soybean varieties or artificial diet; and showed that soybeans as the host food adversely affected emergence rates, size, and sometimes development period. Beach and Todd (1986) found that parasitized soybean looper larvae fed a susceptible soybean variety yielded two and a half times more parasitoids than when fed a resistant variety. Parasitoid production increased another twofold when an artificial diet was the host food. Bourchier (1991) introduced tannic acid into gypsy moth diet to study the effect on growth and development of the tachinid Compsilura concinnata (Meigan); and concluded that interactions between the host plant, the gypsy moth, and the parasitoid may provide a possible explanation for the irregular impact of the parasitoid in the field. Roth et al. (1997) similarly experimented with the effects of dietary phenolic glycosides and tannic acid on performance of the gypsy moth and its suitability as a host for the parasitoid Cotesia melanoscela. Gypsy moth growth was reduced to a greater extent on diets with phenolic glycosides than on

those with tannic acid, with resultant prolonged development, reduced cocoon weight, and higher incidences of mortality for C. melanoscela. Additionally, C. melanoscela performance was reduced slightly more by phenolic glycosides than by tannic acid. The results showed that plant allelochemicals can have profound effects on plant-herbivore-natural enemy interactions. The nutritive chemical composition of host plants also affects a host-entomophage system. Kaneshiro and Johnson (1996) found that the eulophid parasitoid Chrysocharis oscinidis (Ashmead) produced up to 40% more progeny when its agromyzid leaf miner host Liriomyza trifolii (Burgess) was reared on bean plants containing 4.88% leaf nitrogen (compared to other N levels in the 2.67 to 6.52% range). They noted that this highly significant fecundity difference could greatly affect pest/parasitoid populations in both agroecosystems and mass rearing programs. Thus, it is important to recognize that some parasitoids vary in their rates of parasitism or other quantitative attributes, depending on the type and quality of host food plant (Waage et al., 1985). With the chalcidid Brachymeria intermedia, Greenblatt and Barbosa (1981) discovered that gypsy moth larvae fed on red oak foliage, rather than on that of three other tree species, produced the largest and heaviest parasitoids. Likewise, Karowe and Schoonhoven (1992) found that the larval developmental rate and adult longevity of the braconid Cotesia glomerata (Linnaeus) were greatest when its host, Pieris brassicae, was reared on nasturtium instead of on Brussels sprouts, Swedish turnip, or rape. Similarly, Kumar et al., (1988) showed that the aphidiid Trioxys (Binodoxys) indicus Subba Rao & Sharma produced more progeny when its host aphid Aphis craccivora Koch was reared on the plant Cajanus cajan, than when reared on Dolichos lablab or Solanum melongena. Moreover, a higher proportion of female parasitoid progeny was achieved on C. cajan-reared aphids than on S. melongena-reared aphids (Kumar & Tripathi, 1988). Bhatt and Singh (1989) found that fecundity and sex ratio of the same parasitoid (T. indicus) were significantly more reduced when it was reared on A. gossypii Glover on Cucurbita maxima than when reared on two other cucurbit plants, Lagenaria vulgaris and Luffa cylindrica. Further, the population growth of T. indicus was fastest when the aphid host was reared on L. vulgaris (Bhatt & Singh, 1991). Other work was done by Hare and Luck (1990), who studied the influence of four species of citrus host plants on the aphelinid Aphytis melinus reared on California red scale; by Ugur et al. (1987), who showed that rearing the noctuid Agrotis segetum (Denis & Schiff) on different plants maximized different developmental parameters of its ichneumonid parasitoid, Pimpla turionellae (Linnaeus); and by EnglishLoeb et al. (1993), who investigated the consequences on the tachinid parasitoid Thelairia bryanti Curran of feeding

Chapter 7 Cultureand Colonization poison hemlock or lupine to its arctiid host Platyprepia virginalis (Bvd.). Numerous studies have involved the effects of resistant plant varieties on parasitoids. These have included those of Dover et al. (1987), Farrar et al. (1994), Fuentes-Contreras et al. (1996), Grant and Shepard (1985), Kumar (1997), Mannion et al. (1994), Obrycki and Tauber (1984), Obrycki et al. (1985), Orr and Boethel (1985), Orr et al. (1985), Powell and Lambert (1984), Ruberson et al. (1989b), Tillman and Lambert (1995), Vogt and Nechols (1993), and Yanes and Boethel (1983). Obviously, then, plants required for host production in entomophage rearing must be screened for detrimental effects on the entomophages. Some of these deleterious effects can come from plant chemicals consumed by the host, as noted previously. As a further example, Barbosa et al. (1982, 1990) and Bentz and Barbosa (1992) observed that the nicotine level in tobacco hornworms fed tobacco leaves affected the survival of its parasitoid, Cotesia congregata (Say). However, Farrar and Kennedy (1993) discovered an instance in which plant resistance had a direct effect on a parasitoid. Parasitism of Heliothis zea by the tachinid Archytas marmoratus (Townsend), which larviposits on the food plant of its host, was significantly reduced by methylketone-mediated insect resistance of tomato plant lines. Eucelatoria bryani, another tachinid, was not as affected because it larviposited directly into its host, without its larvae touching the resistant foliage. Somewhat similarly, the scelionid parasitoid Telenomus sphingis (Ashmead) was inhibited from parasitizing eggs of Manduca sexta (Linnaeus) on foliage of a resistant wild tomato having high densities of glandular trichomes containing 2-tridecanone (Farrar & Kennedy, 1991). Tomato leaf trichomes also interfered with the encyrtid Copidosoma koehleri B lanchard, a parasitoid of the potato tuberworm, Phthorimaea operculella (Baggen & Gurr, 1995). Characteristics other than resistance can likewise be important in choosing a host plant for a parasitoid production system. Flanders (1984) evaluated five varieties of bean plants for rearing the Mexican bean beetle, the required host for producing the parasitoid Pediobius foveolatus. Of the two varieties that were essentially equivalent in providing the highest net reproductive rate for the bean beetle, the preferred one had superior growth characteristics and was consequently the most economical to produce. Preference of an entomophage for a host on a particular plant is another important characteristic, as reported by Jalali et al. (1988), who demonstrated the preference of the braconid Cotesia kazak Telenga to attack Heliothis armigera (Htibner) larvae on cotton, tomato, or okra to that on dolichos, pigeon pea, cowpea, or chickpea. Also, the fecundity of the parasitoid was statistically greater on the first group of plants than on the second group.

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Host plants can affect the suitability of phytophages not only for parasitoids, but also for predators such as coccinellids (Hodek, 1973; Nishida & Fukami, 1989; Rice & Wilde, 1989; Emrich, 1991; Reyd et al., 1991), Geocoris punctipes (Rogers & Sullivan, 1986), and Scolothrips longicornis Priesner [a thrip predaceous on tetranychid mites (Sengonca & Gerlach, 1984)]. Legaspi et al. (1996) reported that if larvae of the predaceous lacewing Chrysoperla rufilabris (Burmeister) were fed on silverleaf whiteflies (Bemisia argentifolii Bellows & Perring) reared on cucumbers and cantaloupes, they developed satisfactorily, in comparison to those that fed on whiteflies reared on poinsettias and lima beans, which did not survive to the pupal stage. They concluded that whiteflies reared on poinsettias or lima beans either may have been nutritionally inadequate for C. rufilabris development, or may have accumulated plant compounds detrimental to the development of the lacewings. Host plants for phytophagous mites can also affect predatory mites, as shown by de Moraes and McMurtry (1987), who found an indication that adult female Phytoseiulus persimilis gained more weight when fed two-spotted spider mites, Tetranychus urticae Koch, reared on lima bean, Phaseolus vulgaris, than when fed on nightshade, Solanum douglasii. Grafton-Cardwell and Ouyang (1996) showed a direct effect of the nutritional status of host plants (citrus trees) on the reproductive potential of the predaceous phytoseiid Euseius tularensis (Congdon), indicating that the mite fed on leaf sap, as well as on phytophagous mites. The type of produce used in a host-parasitoid production system can likewise affect the parasitoid yield. Simmonds (1944) reported that the encyrtid Comperiella bifasciata Howard effected 2 to 3 times more parasitism when oranges instead of lemons were the diet of its host, the California red scale. The food source used to produce phytophages for weed control projects is similarly an important consideration. Frick and Wilson (1982) mass reared the weed-feeding tortricid Bactra verutana Zeller on a prepared diet and obtained adults that were 60% larger and twice as fecund as those reared on nutsedge plants. However, there were indications that the field flight capabilities were not as great with the diet-reared insects. Price et al. (1980) reviewed earlier studies of interactions between plants, insect herbivores, and natural enemies; and Berlinger (1992) presented a fine review of hostplant effects on herbivore rearing, with reference also to effects on entomophagous predators and parasitoids. Van Emden (1995) summarized well the types of influences that plants have on parasitoids and predators that feed on their herbivores. These influences include host-plant allelochemicals that can affect natural enemies adversely through the passage of plant toxins up the trophic pyramid; the size of the host prey; the production of plant volatiles that attract

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natural enemies, even in the absence of prey; and the effects of different plants on predator/parasitoid functional responses, as mediated through prey size, differences in defensive, and other behavior of the prey, and through effects on searching time of natural enemies. Food for Adult E n t o m o p h a g e s Although some adult entomophagous insects require special food, most parasitic Hymenoptera that do not host feed can naturally produce mature eggs with a source of carbohydrate such as honey (Waage et al., 1985). Even with a parasitoid (Aphytis melinus) that does host feed, Heimpel et al. (1997) showed that the availability of honey is very important and interacts strongly with host feeding in influencing longevity and fecundity, and also has a strong direct effect on egg resorption. For Trichogramma, Morrison (1985a) used plump raisins or honey to feed adults. Likewise, Coombs (1997) increased the longevity and fecundity of adults of the tachinid Trichopoda giacomellii (Blanchard), an agent for biological control of Nezara viridula, by feeding them raisins and water. Munstermann and Leiser (1985) fed adult predatory Toxorhynchites mosquitoes with diluted honey absorbed onto strips of cellucotton; or with raisins, apple slices, or 15% sucrose solution. Mendel (1988) showed that the longevities of one pteromalid and two braconid parasitoids of scolytid bark beetles were directly related to provision of water and honey, and inversely related to temperature; and that longevities of parasitoids given only water were directly related to body size. In the mass production of the mymarid Anaphes iole Girault for augmentation against Lygus hesperus Knight, Jones and Jackson (1990) concluded that not providing food or water to adult parasitoids achieved the greatest efficiency. Adults of some predators may require more complex diets. For adults of the common green lacewing, Morrison (1985b) used a diet composed of equal parts of sucrose and yeast flakes moistened with enough water to make a thick paste. Because this was a yeast commercially cultured on whey, it therefore contained about 65% animal protein, a necessity for high fecundity. Other ingredients may occasionally be important in adult entomophage food. For example, Moore (1985) reported that Nettles et al. (1982) showed a synergistic effect of potassium chloride and magnesium sulfate on oviposition by an insect parasitoid. Factitious H o s t s for E n t o m o p h a g e s Factitious (unnatural) hosts can sometimes simplify rearing. Similarly, a beneficial insect may have more than one type of natural host, and one of these may be easiest to rear in the laboratory. The quantity and quality of parasitoid or

predator progeny on different hosts seem to vary in the insectary according to evolutionary contact, as mentioned by Legner and Thompson (1977). Their study compared the suitability of the potato tuberworm and the pink bollworm, the original source host, as hosts for a braconid, Chelonus sp. nr. curvimaculatus Cameron. The parasitoid increased its destruction of, and its fecundity on, the factitious host, after being reared for many generations on the potato tuberworm and then for one generation on the pink bollworm. The Chelonus spp. to which this parasitoid belongs respond to kairomones in the body scales of several lepidopterans (Chiri & Legner, 1982, 1986), and might most aptly be characterized as comprising a generalist group. Fedde et al. (1982) reviewed guidelines for choosing factitious or unnatural hosts to be used for rearing hymenopterous parasitoids. They listed 43 examples of such hosts and emphasized that ease of rearing was the most important consideration, and that potential factitious hosts should be tested and not prejudged as to possible utility. For example, Rojas et al. (1995) found that the easily reared H. virescens could be used as a somewhat unsuitable factitious host for the braconid Bracon thurberiphagae Muesebeck, a parasitoid of the boll weevil, but only if several amino acids were added to the adult parasitoid diet. The supplemental adult feeding provided a 100% improvement in the fecundity of B. thurberiphagae, restored a 1:1 sex ratio, and permitted the use of H. virescens as a factitious host. A factitious host is especially advantageous if it is useful for rearing more than one beneficial insect. As an example, the greenbug, Schizaphis graminum (Rondani), was satisfactory not only for mass rearing Aphidius matricariae Haliday, an effective parasitoid of the green peach aphid, Myzus persicae (Sulzer) (Popov & Shijko, 1986; Shijko, 1989), but also for producing the predaceous cecidomyiid Aphidoletes aphidimyza (Belousov & Popov, 1989). Egg parasitoids in the genus Trichogramma are generally reared on factitious hosts, but other egg parasitoids have been as well. Halperin (1990) produced Ooencyrtus pityocampae in eggs of the silkworm, Bombyx mori (Linnaeus). Hosts for Trichogramma spp. include the Angoumois grain moth, Sitotroga cerealella (Olivier); the Chinese oak silkworm, Antheraea pernyi Gu6rin-M6neville; another type of silkworm, Samia cynthia ricini (Boisduval); the Mediterranean flour moth; and the rice moth, Corcyra cephalonica (King & Morrison, 1984). Additionally, the eggs of common noctuids and lepidopteran stored grain insects are often used. However, a few Trichogramma spp. may be host specific (Morrison, 1985a). There must be careful choosing of factitious hosts for Trichogramma. Pham Binh et al. (1995) addressed this topic. For example, in testing the suitability of pyralid species for T. evanescens Westwood, Brower (1983) found that

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the Mediterranean flour moth was by far a less suitable host than the tobacco moth, Ephestia elutella (Htibner); the almond moth, Cadra cautella (Walker); the raisin moth, C. figulilella (Gregson); or the Indian meal moth, Plodia interpunctella (Htibner). Only 59% of exposed flour moth eggs yielded emerged parasitoids, and 10% of these were runts. On the other hand, 88% of exposed almond moth eggs produced parasitoids, with only 0.4% being runts. Trichogramma reared for long periods on a factitious host can still maintain a natural-host preference. Yu et al. (1984) collected a strain of the egg parasitoid T. minutum Riley from the codling moth, and then reared it for about 22 generations on eggs of the Mediterranean flour moth. Even after that time, the parasitoid still preferred eggs of the codling moth to eggs of the Mediterranean flour moth. Pavlik (1993) studied a total of nine strains of four species of Trichogramma and also found that some strains did not lose their ability to accept and develop in their natural hosts in spite of having been reared on Mediterranean flour moth eggs for several years. However, rearing a Trichogramma sp. on a factitious host requires careful testing for retention of its host acceptance characteristics. In contrast to the preceding example, host acceptance of European corn borer eggs by T. maidis decreased with increasing numbers of generations of parasitoid rearing on the Mediterranean flour moth, and did not then improve after five generations of passaging on corn borer eggs (van Bergeijk et al., 1989). In another case, Sukhova (1989) noted the widespread use of passaging T. evanescens through natural hosts (Mamestra brassicae) to maintain quality. For rearing T. evanescens on factitious hosts, Mirzalieva and Mirzaliev (1988) recommended using eggs of the greater wax moth instead of those of Sitotroga because of the superior biological effectiveness of the produced parasitoids. In fact, Campadelli (1988) reported the greater wax moth to be an excellent substitute for rearing 47 species of Hymenoptera and 22 species of Tachinidae. For example, there are reports of its use in the mass production of Lixophaga diatraeae, a tachinid fly that parasitizes the sugarcane borer (Hartley et al., 1977; King et al., 1979; King & Hartley, 1985b). Likewise, Stowell and Coppel (1990) used the greater wax moth to mass-produce Brachymeria spp., chalcidid parasitoids of the gypsy moth. Palmer (1985) previously showed B. intermedia to be more easily reared in the insectary on the greater wax moth. On the other hand, Rotheray et al. (1984) determined that the gypsy moth was a better host for B. intermedia because parasitoids produced from the wax moth were smaller and less able to oviposit in gypsy moth pupae. Palmer (1985) found that even rearing Brachymeria for 119 generations on the wax moth did not shift the host preference of the parasitoid, because it still

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readily attacked gypsy moth pupae. However, B. intermedia is apparently a generalist, and such a host preference shift is not expected. King and Morrison (1984) noted that rearing a parasitoid on a factitious host can eventually increase its acceptance of that host, but a parasitoid reared for only a few generations on an unnatural host can still react strongly to its natural host. Predicting potential field effectiveness of generalist parasitoids and predators against specific target pests is a corollary benefit of testing host insects for production programs. Drummond et al. (1984) reported that the best host for rearing the spined soldier bug Podisus maculiventris, was the greater wax moth, in contrast to the Mexican bean beetle; the eastern tent caterpillar, Malacosoma americanum (Fabricius); or the Colorado potato beetle, Leptinotarsa decemlineata (Say). The Colorado potato beetle in fact was a suboptimal host in comparison to the other three prey species. Therefore, the spined soldier bug apparently has little potential as a field predator of this pest. As with predaceous insects, factitious hosts are sometimes advantageous for rearing predaceous phytoseiid mites. Gilkeson (1992) noted in a review of the mass rearing of phytoseiid mites that they can be grouped into those that must be reared on their natural hosts and those that can be reared on alternate food sources. For example, Amblyseius cucumeris (Oudemans) was cultured on the American house dust mite Dermatophagoides farinae Hughes, a factitious host (Castagnoli, 1989, Castagnoli & Sauro, 1990). Rearing phytoseiids on pollen is also frequently successful, although the species of pollen can be critical (Affifi et al., 1988; Englert & Maixner, 1988; James, 1989; Zhang & Li, 1989a, 1989b; Grout & Richards, 1992; Ouyang et al., 1992; James & Whitney, 1993; Yue et al., 1994; Fouly et al., 1995; Yue & Tsai, 1996; Bruce-Oliver et al., 1996; Reis & Alves, 1997; Abou-Setta et al., 1997). Regardless of the food used to raise phytoseiids or polyphagous predators, Dicke et al. (1989) advocated caution in using novel diets or in using only one species as food because performance characteristics can be adversely affected. Even the stage of a host species fed to a phytoseiid can produce substantial differences in life table parameters, as shown by Bruce-Oliver and Hoy (1990), who compared Metaseiulus occidentalis fed eggs or mixed actives of the host Tetranychus pacificus McGregor. Consequently, they noted that laboratory diet is a factor to consider in evaluating potential efficacy of natural enemies. D e a d H o s t s for E n t o m o p h a g e s The capability of rearing many predators and a few parasitoids on dead hosts simplifies production (Waage et al., 1985). Etzel (1985) described the heat processing of potato tuberworms to be used as food for producing certain cocci-

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nellids and neuropterans. In successfully using heat-killed pupae of the greater wax moth to rear the parasitoid Brachymeria intermedia, Dindo (1990) observed that the one limiting factor seemed to be acceptance, instead of suitability of the killed hosts. Sometimes, the extended refrigeration or freezing of insect eggs can facilitate their use for rearing egg parasitoids or predators. Such storage prevents the hatching of larvae that might interfere with entomophage production, as well as enables the stockpiling of host material. The technique is useful with eggs of the Mediterranean flour moth for rearing Trichogramma spp. (L. Etzel, unpublished). Nagarkatti et al. (1991) found prefrozen eggs of the tobacco hornworm to be superior for mass production of T. nubilale, with an average of about 10 large, robust parasitoids emerging from each egg. Similarly, Drooz and Weems (1982) used freeze-killed eggs of Eutrapela clemataria (J. E. Smith) to rear the encyrtid egg parasitoid Ooencyrtus ennomophagus Yoshimoto; prefrozen eggs of the southern green stinkbug facilitated propagation of the scelionid egg parasitoid Trissolcus basalis (Powell et al., 1981; Powell & Shepard, 1982); and prefrozen eggs of the Colorado potato beetle were suitable for rearing the eulophid Edovum puttleri Gressell (Maini & Nicoli, 1990). Refrigeration of eggs can typically occur for only relatively short storage periods before their suitability for parasitization decreases rapidly (Gautam, 1987; Hugar et al., 1990). However, frozen eggs are suitable for much longer periods. In propagating Trichogramma spp., Ma (1988) found no significant differences in parasitism rate or number of emerged adult parasitoids when the use of fresh, untreated eggs of the Chinese oak silkworm was compared with that of eggs stored for 1 to 9 months in liquid nitrogen and then defrosted in water at 30~ before parasitization. Wang et al. (1988) obtained similar results in rearing Trichogramma spp. on Antheraea pernyi eggs stored in liquid nitrogen for over 1000 days. For Trichogramma production in the former USSR, Gennadiev et al. (1987)emphasized that adherence to precise freezing, storage, and thawing regimes was essential in handling eggs of the Angoumois grain moth. As an alternative to prefreezing, Gross (1988) irradiated eggs of the corn earworm with 25 krad of 6~ to prevent hatching and enable their use for producing T. pretiosum. Thorpe and Dively (1985) likewise irradiated tobacco budworm eggs for Trichogramma production. Harwalkar et al. (1987) treated female potato tuberworms with gamma irradiation, and used the sterile eggs to rear T. brasiliensis (Ashmead) with no ill effects. They found no significant differences between the Trichogramma reared on irradiated or prefrozen eggs. However, when Zhang and Cossentine (1995) irradiated codling moth adults with 6~ to obtain nonviable eggs for rearing T. platneri Nagarkatti, they

found that given a choice, the Trichogramma parasitized significantly more viable than nonviable codling moth eggs, and took longer to develop in the nonviable eggs. Kfir and Van Hamburg (1988) used ultraviolet light to irradiate Heliothis armigera eggs for 2 h before parasitization by the egg parasitoids Telenomus ullyetti Nixon and Trichogrammatoidea lutea Girault. Others have also utilized ultraviolet irradiation to kill host eggs before Trichogramma production (Hirashima et al., 1990a, 1990c; Sengonca & Shade, 1991; Nordlund et al., 1997), and in one instance the workers first killed the eggs with ultraviolet irradiation and then froze them in liquid nitrogen for several months before their use for rearing Trichogramma (Hu & Xu, 1988). Morrison (1985b) froze eggs at -10~ for >24 h in airtight containers before using them as food for rearing the predaceous common green lacewing. Likewise, Baumhover (1985) used frozen tobacco hornworm eggs to rear the predaceous stilt bug, Jalysus wickhami (Van Duzee), and found that these eggs would still be suitable predator food after storage for 2 years at -23~ Similarly, Tommassini and Nicoli (1995) found that frozen Mediterranean flour moth eggs provided adequate nutrition for rearing the predaceous anthocorid Orius laevigatus (Fieber). Finally, Schanderl et al. (1988) utilized ultraviolet irradiation to kill host eggs fed to coccinellids, as did Chen et al. (1994) for raising the lacewing, Mallada basalis (Walker). Even prefrozen insect pupae are occasionally useful for parasitoid production. Grant and Shepard (1987) raised the chalcidid parasitoid B. ovata on prefrozen pupae of seven species of Noctuidae. The velvet bean caterpillar was the best host because of the extended period of suitability of the frozen pupae (up to 256 days versus 30 to 90 days for the other species). Milward-De-Azevedo and Cardoso (1996) used prefrozen pupae of the calliphorid Chrysomya megacephaia (Fabricius) to successfully rear Nasonia vitripennis. The freezing and thawing process did not affect the time of preimaginal development of the parasite, but there was a marked increase in the female sex ratio. Another example was the use of prefrozen housefly pupae for producing two pteromalid parasitoids, Muscidifurax zaraptor (Petersen & Matthews, 1984; Petersen et al., 1992, 1995) and Pachycrepoideus vindemiae (Pickens & Miller, 1978). Pawson et al. (1993) later compared the use of freeze-killed housefly pupae with freeze-killed stable fly (Stomoxys calcitrans Linnaues) pupae for rearing M. zaraptor; P. vindemiae; and a third pteromalid, Spalangia nigroaenea Curtis. However, Morgan (1992) was able to produce Muscidifurax, Pachycrepoideus, and Spalangia on radiation-killed fly pupae. This technique enabled the shipping of killed pupae to France for parasitization and then their return to the United States with developing parasitoids. The irradiated pupae were suitable as hosts for up to 8 weeks. There are examples of prefrozen arthropod stages other

Chapter 7 Culture and Colonization

than eggs being utilized for predator production. Sipayung et al. (1992) mass-produced predatory Pentatomidae and Reduviidae on prefrozen caterpillars, and Parajulee and Phillips (1993) reared the predaceous anthocorid Lyctocoris campestris (Fabricius) on previously frozen late instars of eight species of insects. Spider mites also have been prefrozen before use in phytoseiid mite production. In a biological control program against the cassava green mite, Mononychellus tanajoa (Bondar) sensu lato, a primary reason for prefreezing massproduced spider mites for 18 h was to eliminate contaminating predators, including phytoseiids, from food used to produce desired phytoseiids (Yaninek & Aderoba, 1986; Friese et al., 1987). Diapause Diapause in the life cycle often interferes with parasitoid and predator production. For example, Eskafi and Legner (1974) showed that certain temperature and photoperiod combinations would induce diapause in adults and progeny of the eye gnat parasitoid Hexacola sp. nr. websteri (Crawford). Exposing larval parasitoids within their larval hosts to a long photophase of 16 h combined with a high temperature of 32~ caused the parasitoid prepupae to enter a diapause state, termination of which required contact of the host puparia with moisture for a few hours. However, this type of easily terminated diapause only occurred following a parental generation reared at 27~ with 14-h light. With the parasitoid parental generation reared at 32~ with 16-h light and the progeny held at 27~ with 14-h light, then >90% of the prepupal progeny entered diapause and could not be induced to terminate it by exposure to moisture. With another set of progeny from the same parents reared at 32~ with 16-h light, only 35% entered diapause. This example illustrates the great complexities involved in determining which combinations of environmental regimes in the insectary will prevent, induce, or terminate diapause. In the case of Trichogramma spp., Zaslavski and Umarova (1990) showed that the interactive effects of environmental conditions in the maternal and filial generations governed larval diapause in the filial generation. Lowered temperature during development of the filial generation was the predominant diapause factor, but the photoperiod and temperature conditions of the maternal generation influenced the "norm" of this thermal reaction. Superimposed on these diapause reactions was an endogenous process running through the generations that changed diapause tendency and underlying reaction norms even under constant rearing conditions (Zaslavski & Umarova, 1990). Other examples of complex diapauses include the alfalfa weevil parasitoid system; Chelonus spp. parasitoids of the pink bollworm that terminate diapause at different intervals

| 55

(Legner 1979c); and navel-orangeworm parasitoids, where diapause seems triggered by hormonal changes in the host at different latitudes (Legner, 1983). Not only physical environmental conditions but also host conditions and host food can influence diapause in parasitoids. The physiological state of an alfalfa plant affects the yellow clover aphid (formerly called the spotted alfalfa aphid), Therioaphis trifolii (Monell), which then induces diapause in its aphidiid parasitoid Praon exsoletum Nees (Clausen, 1977). Similarly, the type of pollen used to rear predaceous mites can affect initiation of diapause. Amblyseius potentillae (Garman) and A. cucumeris entered diapause in a short-day photoperiodic regime when reared on ice plant pollen, but not when reared on pollen of the broad bean (Overmeer et al., 1989). After studying various combinations of parasitoid species, aphid species, plants, and environmental conditions, Polgar et al. (1995) concluded that internal factors via the host aphid, such as host aphid life cycle (holocyclic versus anholocyclic), aphid morph (oviparae, etc.), and host-plant quality, as well as environmental cues (temperature and photoperiod), can all be interconnected in the induction of dormancy or diapause in aphid parasitoids. Laing and Corrigan (1995) showed the importance of host species in initiating diapause in Trichogramma minutum. Diapause occurred at 15~ with a photophase of 12L: 12D in eggs of Lambdina fiscellaria fiscellaria, but did not occur in eggs of Anagasta kuehniella, Sitotroga cerealella, or Choristoneura fumiferana held under these same conditions. Appropriate environmental conditions or their combinations, particularly relating to light and temperature, are often useful for manipulating diapause (Singh & Ashby, 1985). For example, Tauber et al. (1997b) showed that a biotype of Chrysoperla carnea from San Pedro, Mexico, could be reared continuously without diapause with an intragenerational increase in photoperiod or could be reared with the regular intervention of a storage period. Diapause induction in individuals destined for storage was accomplished by rearing larvae under a long-day photoperiod and transferring the prepupae to a short-day photoperiod. Waage et al. (1985) noted that one factor to consider in rearing programs is that entomophagous insects and their hosts may have different optimal developmental temperatures. As a corollary, natural enemies may enter diapause under conditions whereby their hosts remain active. The western flower thrips, Frankliniella occidentalis (Pergande), is a year-round greenhouse pest in northern climates, whereas commercially available strains of two predaceous mites, Amblyseius cucumeris and A. barkeri (Hughes), are ineffective in the winter because of reproductive diapause induced by short-light conditions. Van Houten et al. (1995), however, were able to genetically select

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for effective nondiapausing strains of these predators within 10 laboratory generations. E n v i r o n m e n t a l Conditions Rearing conditions vary with the entomophages. For example, King and Hartley (1985c) cultured maggots of the parasitic tachinid Lixophaga diatraeae inside their larval host, the sugarcane borer, in complete darkness, whereas Morrison (1985a) reared Trichogramma spp. under constant light. Optimal conditions for entomophages can also vary in the same genus. Morrison (1985b) reared the common green lacewing under constant light. However, Chrysoperla rufilabris required a 14-h photophase for high fecundity (Nguyen et al., 1976). Singh and Ashby (1985) observed that light quality and photoperiod are important factors in insect mating and oviposition. In fact, sometimes darkness is necessary for a parasitoid to perform properly. OrtegonE. et al. (1988) reported that the braconid Meteorus laphygmae (Viereck) parasitized Spodoptera at night. Optimal rearing conditions even vary for different characteristics within a species. Miller (1995) studied rearing conditions for the coccinellid Eriopis connexa Mulsant, a predator of the Russian wheat aphid Diuraphis noxia (Mordvilko), and found that a different set of rearing conditions existed for optimal beetle size (11.8 mg), highest larval survival (91.7%), and most rapid larval growth (6.3 days). Miller (1995) developed an index based on larval developmental time, larval survival, and adult weight to determine that the composite optimal rearing conditions for beetle production were to use the Russian wheat aphid as prey at 34~ Morales-Ramos et al. (1996a) developed polynomial multiple regression models to estimate optimal levels of temperature, RH, and photoperiod to maximize production of the boll weevil parasitoid Catolaccus grandis. The maximum value of the intrinsic rate of increase (Rm) of C. grandis occurred at 29~ and 66% RH with a 16:8 (L:D) photoperiod. Of course, optimal physical conditions for development of an entomophage might not also be optimal for its host and the host plant. Fabre (1989) found that maintenance of the aphidiid Pauesia cedrobii Stary & Leclant on its host Cedrobium laportei Remaudiere on potted Atlas cedar plants required holding the system at 12~ which was satisfactory but not optimal for the parasitoid. Mating Waage et al. (1985) discussed mating problems in general and possible solutions conceming entomophages. Chianese (1985) noted that mating conditions were critical in the laboratory production of the gypsy moth parasitoid Co-

tesia melanoscela. Isolation of the cocooned parasitoids in gelatin capsules before adult emergence ensured that they remained virgins until needed. Then both sexes were combined in a screen cage under natural light. It was better to feed males before placement in the mating cage, while females were fed in the cage itself to reduce activity while males mated with them. Such females mated only once, and refrigeration of adults had to occur after mating (24 to 48 h). Nealis and Fraser (1988), who reared the braconid Apanteles fumiferanae Viereck on the spruce budworm, likewise reported on the importance of natural light for parasitoid mating. Rappaport and Page (1985) were successful in maintaining a year-round culture of the ichneumonid Glypta fumiferanae (Viereck), a parasitoid of the western spruce budworm, and attributed part of their success to the mating procedure, which was to introduce a freshly emerged female and three males 2 to 4 days old into a 0.25-liter carton with mesh-screen ends. Greenberg et al. (1995) also found that an acceptable sex ratio (65% females) was obtained in the propagation system of Catolaccus grandis, a parasitoid of the boll weevil, if a ratio of one female per three males was used during the first hour of mating, immediately after emergence. Galichet et al. (1985) also noted rather fastidious requirements for laboratory mating of the tachinid Lydella thompsoni. These included high humidity, high light intensity (at least 8,000 to 10,000 lux), and food of casein hydrolysate and honey. Mason et al. (1991) likewise reported that L. thompsoni required a strong light source to facilitate mating behavior and larviposition. Godfray (1985) discovered extremely precise mating requirements for Argyrophylax basifulva (Bezzi), a tachinid parasitoid of the greater coconut spike moth, Tirathaba complexa Butler. Just to obtain 50% mating, he had to place the flies in a large outdoor cage in bright moming sunshine at 28~ and 90% RH, with a strong breeze provided by an electric fan. Further complications were a 3-day premating period and an 8-day preoviposition period. Because the mating requirements of the predaceous mosquito Toxorhynchites minimus (Theobald) were unknown, Horio et al. (1989) found it necessary to use artificial mating for laboratory culturing, although it was not essential to remove the head of the male to achieve efficient mating, as is the case with some fastidious mosquitoes. In contrast, King and Hartley (1985c) found mating by the tachinid Lixophaga diatraeae to be easily obtained without any exacting requirements. Although some light was necessary, the type and intensity were not critical. Mating occurred readily by placing about 200 adult L. diatraeae in a small screened cage under conditions of 26~ and 80% RH with a 14-h photophase. The proportion of males placed together with females for mating can be quite low, which may be preferable to

Chapter 7

Culture and Colonization

avoid problems caused by over-mating. Palmer (1985) found that adding 25 males and 300 females of the parasitoid B. intermedia to a 4-liter jar ensured complete mating. Females mated only once and unmated females produced males. Mating occurred at 24 to 27~ after emergence in bright artificial light, with resulting progeny being 60 to 85% females. Some females require more than one mating. Bonde (1989) reported that the phytoseiid mite Amblyseius barkeri (Hughes) required multiple matings for optimal fertility. In one instance, mating problems with parasitoids occurred because of insufficient taxonomic knowledge. Faulds (1990) surmounted difficulties in rearing an imported Bracon sp. in quarantine after discovering that the imported material included two closely related species with different mating requirements. Sex-Ratio C h a n g e s In prolonged culture of parasitoids, sex-ratio changes can be a complication, as noted before. However, modified rearing conditions can sometimes ameliorate this problem. For example, a 16-year-old culture of the thelytokous pteromalid Muscidifurax uniraptor gradually began producing predominantly male progeny despite no apparent changes in culturing techniques or the host insect (Legner, 1985). Improved female production occurred by allowing oviposition only by young mothers, and in moderate temperature conditions on alternate days. Nonetheless, the proportion of >95% females was no longer attainable. It was interesting that insectary production of two freshly collected wild cultures of M. uniraptor resembled that of the changed longterm culture. The involvement of microorganisms in thelytoky (Horjus & Stouthamer, 1995; Zchori-Fein et al., 1995), as noted earlier, complicates interpretation of sex ratios in such species. Waage et al. (1985) reviewed the factors related to rearing conditions that can significantly affect the sex ratio of parasitic wasps. These factors include degree of mating (including the effects of over-mating), host size, crowding, and high temperatures. At least some parasitic female wasps can respond to external cues by regulating the sex of eggs oviposited. These females tend to lay male eggs in small hosts, in already parasitized hosts, and in response to physical and chemical effects of crowding. Also, male larvae tend to be competitively superior, so there is a differential survival of males in superparasitized hosts. An example of female sterility correlated with crowding of the parental females during oviposition was reported by Gerling and Fried (1997), who found the phenomenon in the aphelinid whitefly parasitoid, Eretmocerus mundus Mercet. They did not determine whether the sterility was caused by crowding alone or possibly by the activity of microorganisms acting under crowded conditions.

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Provision of abundant food and space can partially alleviate male-biased sex ratios in the laboratory (Waage et al., 1985). A consequence of food and space limitations is that female progeny production can decline with increasing parasitoid to host ratios (Legner, 1967). Moreover, Fox et al. (1990) reported one instance in which the quality of host food affected the sex ratio of a parasitoid. A greater percentage of female parasitoids was achieved from diamondback moth larvae (Plutella xylostella [Linnaeus]) reared on collard plants with high leaf nitrogen than was achieved on unfertilized plants. Similarly, Shukla and Tripathi (1993) showed the offspring sex ratio of the aphidiid Diaeretiella rapae (Mclntosh) to be significantly affected by three species of food plants upon which its host, Lipaphis erysimi Kalt, was reared. As noted previously, Bhatt and Singh (1989) likewise found a host-plant effect on the sex ratio of the aphidiid Trioxys pallidus. Parasitoids vary in the combined factors that govern their sex ratios. For example, the sex ratio of the encyrtid Epidinocarsis lopezi (DeSantis) did not change in response to parasitoid density or to situations when the parasitoid oviposited in already parasitized hosts, but could vary due to host-size distribution and differential mortality in mass rearing (Van Dijken et al., 1989). Tillman et al. (1993) discovered that host species could also be a determinant in the sex ratio of parasitoids. Microplitis croceipes had a significantly greater female to male ratio than either Cotesia kazak or M. demolitor Wilkinson had when reared on Heliothis zea. However, the sex ratios were not significantly different when the three parasitoid species were reared on H. armigera. Likewise, Rojas et al. (1995) showed that rearing the boll weevil parasitoid Bracon thurberiphagae on the relatively unsuitable factitious host H. virescens resulted in a male-biased sex ratio, which, nonetheless, could be restored to a 50:50 ratio with the addition of several amino acids to the diet of the adult parasitoid. This supplemental nutrition also improved the fecundity 100%. Besides the factors mentioned earlier, age of the parasitoid female can affect sex of the progeny. Hirashima et al. (1990b) reported that the trichogrammatids Trichogramma chilonis Ishii and T. ostriniae Pang & Chen produced the highest percentage of female progeny on the first day of adult life. Likewise, Leatemia et al. (1995) found that with T. minutum the offspring sex ratios of long-lived females were male-biased (50 to 62% males), while those of shortlived females were female-biased (74 to 82% females). Greenberg et al. (1995) showed that as female adults of the boll weevil parasitoid Catolaccus grandis aged from 5 to 10 days, the percentage of female progeny increased from 64.0 to 77.2, respectively. A further increase in female age, from 20 to 25 days, resulted in a declining percentage of female progeny from 54.0 to 48.5. Contrarily, the sex ratio of the progeny of the predaceous mite Phytoseiulus persi-

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milis also changed with age, but in this case the older females produced more females than males (Chang et al., 1990). In producing three species of fruit fly p~asitoids, Wong and Ramadan (1992) obtained the highest numbers of female progeny when they allowed mating for the first 4 days of adult life, prior to host exposure. Thereafter, production of female progeny remained significantly high during adult female ages of 5 to 30 days for Diachasmimorpha tryoni (Cameron) (= Biosteres tryoni [Cameron]), 5 to 15 days for D. longicaudata, and 6 to 20 days for Psyttalia fletcheri (Silvestri). Wong and Ramadan (1992) also showed that oviposition in younger fruit fly larvae (second instar) by D. tryoni and D. longicaudata resulted in significantly fewer female progeny, whereas a similar effect did not occur with P. fletcheri. Hailemichael et al. (1994) found that in rearing the ichneumonid Xanthopimpla stemmator (Thunberg), a solitary endoparasitoid of pupae of Old World lepidopteran stalk borers, the sex ratio (female to male) of the parasitoid progeny increased with host age. Females comprised 47% of total parasitoid progeny emerging from 1-day-old laboratory-reared pupae of the sugarcane borer, and 84% of those from 6-day-old pupae. Cold temperatures can also affect parasitoid sex ratios. Hoffman and Kennett (1985) demonstrated that prolonged exposure of Aphytis melinus to winter temperatures caused a male bias in F1 sex ratios, and they briefly reviewed published reports of similar effects of low temperatures on parasitoids. Even just cool temperatures can alter sex ratios, as indicated by Yadav and Chaudhary (1988), who showed that while the female offspring of the encyrtid egg parasitoid Cheiloneurus pyrillae Mani outnumbered males at all rearing temperatures, the proportion of females declined with decreasing constant temperatures from 30 ~ to 17.5~ Mani and Krishnamoorthy (1992) found that 30~ was also optimum for maximizing female production of the encyrtid Anagyrus dactylopii (Howard). Autoparasitism introduces another complication in sexratio determination. As shown with the aphelinid Coccophagus atratus Compere, brood sex ratios are dependent on the relative availability of hosts for the male progeny and hosts for the female progeny (Donaldson & Walter, 1991). However, a further complication reported by Hunter et al. (1993) is the formation of males in an autoparasitoid species (the aphelinid Encarsia pergandiella Howard) by loss of one set of chromosomes from fertilized eggs. Such males then develop as primary parasitoids, and not in the normal fashion as hyperparasitoids on sibling females. Once formed, the "primary" male trait is apparently heritable, although at a low and variable rate. Chromosome loss resulting in male formation has also been noted in a non-autoparasitoid species, Nasonia vitripennis. A supernumerary chromosome labeled paternal sex ratio (PSR) transmitted via the sperm causes supercondensation and destruction of paternal chromosomes in fertilized

eggs, thus effectively converting diploid (female) eggs into haploid (male) eggs (Beukeboom & Werren, 1993a, 1993b; Werren & Beukeboom, 1993). However, an additional complication with this insect is the presence, as reported by Breeuwer and Werren (1993), of maternally inherited bacteria (later identified as Wolbachia, as noted previously) that cause reproductive incompatibility, also resulting in destruction of paternal chromosomes and conversion of diploid eggs into male ones. Dobson and Tanouye (1996) showed that the transmission and ability of PSR to induce chromosome loss is not dependent on Wolbachia, with comparisons suggesting an absence of interactions between PSR and Wolbachia when they occur together. McAllister and Werren (1997) studied the origin and evolution of the PSR chromosome in Nasonia, and Reed and Werren (1995) examined the early cytological events associated with paternal genome loss induced by the PSR chromosome and by Wolbachia. Contrary to paternal genome loss, the sex ratio in N. vitripennis can be distorted toward nearly all female families by a cytoplasmic element termed maternal sex ratio (MSR), as reported by Beukeboom and Werren (1992). Obviously, sex determination in N. vitripennis, and perhaps in other Chalcidoidea, is very complex, with additional research necessary to sort out genetic, cytoplasmic, microorganism-caused, and possibly other effects. Further information on sex ratios can be found in King (1993), Luck et al. (1993), and Wrensch and Ebbert (1993). Also see Chapter 23. Rearing Density a n d E n t o m o p h a g e to H o s t Ratios Provision of adequate food and space is not only important for maintaining a suitable sex ratio but also for optimizing progeny production. In rearing the red scale parasitoid, Aphytis lingnanensis, Papacek and Smith (1985) recommended a uniform rearing density of 30 to 50 oleander scales per square centimeter on the surface of butternut pumpkins. Propp and Morgan (1983) stressed the importance of using suitable parasitoid to host ratios to prevent superparasitism in mass-producing the pteromalid Spalangia endius Walker on the housefly, and Raupp and Thorpe (1985) noted that increasing parasitoid to host ratios may result in multiple stinging and increased larval mortality. Wong and Ramadan (1992) minimized superparasitism in producing fruit fly parasitoids by exposing them for a limited period of time to excess numbers of host larvae. Chianese (1985) used the ratio of eight mated females of the parasitoid Cotesia melanoscela to 40 gypsy moth larvae for 3 h for oviposition, and achieved 70 to 80% parasitism. With a Korean strain of C. melanoscela, Kolodny-Hirsch (1988) achieved maximum parasitoid production with a ratio of five females (8 days old) to 50 first- and secondinstar larvae for 24 h at 28~ with a light intensity of 1452

Chapter 7 Culture and Colonization

lux. For Trichogramma spp., Morrison (1985a) obtained maximum fecundity with a ratio of one female parasitoid per 100 host eggs. However, in culturing T. perkinsi Girault and T. exiguum Pinto & Platner on eggs of the pyralid Corcyra cephalonica, a ratio of one parasitoid per 16 eggs resulted in parasitism of over 95% (Balasubramanian & Pawar, 1988). With T. maidis, Wajnberg et al. (1989) reported that superparasitism seems to be genetically controlled, apparently for number of eggs deposited in each host as well as for frequency distribution of the eggs among hosts. Such evidence would have a beating on mass-rearing conditions. Obviously, then, experimentation must determine the proper entomophage to host ratio for maximizing progeny yield per unit of host material. For example, Harris and Bautista (1996) tested the host suitability of Bactrocera dorsalis for development of the braconid parasitoid Biosteres arisanus and showed that increases in host egg to female parasitoid ratios of 5:1, 10:1, 20:1, 25:1, and 30:1 corresponded with increases in parasitoid progeny yield up to a plateau at the 20:1 ratio. In another system, Mishra and Singh (1990) found that increasing the number of female parasitoids of Lysiphlebus delhiensis (Subba Rao & Sharma) from 1 to 8 in a cage of 200 Rhopalosiphum maidis (Fitch) for 24 h increased the percentage of parasitization as well as the number of parasitoids emerged, but decreased the rate of multiplication, the search rate, and the proportion of female offspring. Also, the presence of males can decrease progeny production, as Kumar et al. (1988) showed with the parasitoid Trioxys indicus. Whether or not a parasitoid is gregarious can be a further complication. In mass-producing the gregarious braconid ectoparasitoid A1lorhogas pyalophagus Marsh on the pyralid host Chilo partellus (Swinhoe), Ballal and Kumar (1993) reported that the optimal ratio of one host per parasitoid provided a high percentage of parasitism with the maximal number of cocoons and healthy adults. Munstermann and Leiser (1985) cautioned that in rearing the predaceous mosquito Toxorhynchites amboinensis (Doleschall), the ratio of predaceous larvae to prey larvae is critical. Too little prey can result in cannibalism among the predaceous larvae, and too much prey can result in adult prey emergence in the Toxorhynchites pans. For the common green lacewing, Morrison (1985b) used a modified ice cream carton as an oviposition unit, in which 500 adults produced approximately 79,000 eggs in 21 days. Morrison (1985b) emphasized that each adult needed 2.5 cm 2 of "resting" space to prevent a reduction of longevity and fecundity caused by overcrowding. For larval green lacewings, Bichao and Araujo (1989) reported that the best initial density was 2000 lacewing eggs per 32 • 22 • 7 cm container, and specified host egg quantities required for larval development. In propagating the predaceous mite Phytoseiulus persimilis, the greatest efficiency resulted

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from a ratio of one predator to 20 prey, and a density of 250 to 300 females of the spider mite prey on kidney bean leaves (Osakabe et al., 1988). For rearing the phytoseiids Amblyseius victoriensis (Womersley) and Typhlodromus doreenae Schicha, James and Taylor (1993) cautioned that high densities (7.7 prey per 4 cm 2 of A. victoriensis or 9.0 prey per 4 cm 2 of T. doreenae, versus one predator per 4 cm 2) resulted in a reduced daily oviposition of about 70 and 50%, respectively. Adequate space and abundant, well-fed hosts for cultures of entomophagous parasitoids and predators will usually prevent cannibalism, mortality, lowered longevity and fecundity, and reduced fitness (Waage et al., 1985). An exception reported by Wajnberg et al. (1985) was that Drosophila melanogaster Meigen suitability for the eucoilid endoparasitoid Leptopilina baulardi (Barbotin, Carton & Kelner-Pillault) increased from 50% for Drosophila reared in optimal laboratory conditions to 90% for those reared in crowded conditions. In a somewhat similar situation, Kazimirova and Vallo (1992) found that significantly higher percentages of parasitization and parasitoid emergence occurred when smaller Mediterranean fruit fly pupae originating from a high larval density were exposed to the diapriid Coptera occidentalis Muesebeck. Temperature is also a factor interacting with hosts and space in entomophage production. Isenhour (1985) found that at high host densities, the ichneumonid Campoletis sonorensis (Cameron) parasitized significantly more thirdinstar larvae of the fall armyworm, Spodoptera frugiperda (Smith), at 25~ than at 30~

Behavior An understanding of behavior can be an important component of entomophage culture. For example, the positive phototaxis and negative geotaxis of Trichogramma spp. provide greater ease of manipulation (Morrison, 1985a). In fact, most entomophagous parasitoids exhibit positive phototaxis, which facilitates their collection. The anemophototactic response of predaceous mites likewise makes collection easy (Chalkov, 1989), although Zhurba et al. (1986) first starved P. persimilis to further stimulate migration into a collection container. Waage et al. (1985) recommended rearing entomophagous insects on their natural hosts on natural food sources to provide all necessary behavioral stimuli. While this is desirable, it may not be possible in mass production. King and Hartley (1985c) noted that volatile substances produced by feeding sugarcane borers attract Lixophaga diatraeae, which then larviposits when it contacts borer frass. However, these researchers developed a mass production scheme for this tachinid by rearing it on the greater wax moth, a factitious host whose use did not simulate field conditions but did greatly facilitate production. Semio-

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chemicals produced by plant-fed H. zea were found to be similarly important in stimulating responsiveness of the parasitoid M. demolitor Wilkinson (Herard et al., 1988a, 1988b). However, such responsiveness was generally lacking in parasitoid females reared from hosts fed artificial diet, so Herard et al. (1988b) recommended "imprinting" the emerging females by exposing them to frass from plantfed hosts. For in vitro rearing of the egg parasitoid Ooencyrtus kuvanae, Lee and Lee (1994) had to treat the artificial eggshell of polypropylene film with an ethanol extract from gypsy moth egg masses to stimulate ovipositing by the wasp. Thus, the ovipositional behavior of the parasitoid would not be expected to change in culture. In the case of the in vitro rearing of the ectoparasitoid Catolaccus grandis, however, Guerra et al. (1994) found that short-chain saturated hydrocarbons (alkanes) could elicit oviposition behavior, as could volatiles emanating from an artificial diet devoid of insect components that was specifically developed for the in vitro rearing of ectoparasitoids. They suggested that a synergistic combination of n-hexane and diet might be used to optimize the mechanized production of noncontaminated eggs. After using n-hexane for two consecutive generations to stimulate oviposition for in vitro rearing, Guerra and Martinez (1994) found no apparent adverse effects on the general behavior and reproduction of the parasitoid. Feeding behavior is also important to entomophage production potential. Although a short life cycle of 15 days positively influences production of large numbers of the red scale parasitoid, Aphytis lingnanensis (Papacek & Smith, 1985), host feeding is a negative influence, with each female destroying an average of 46 scales, while laying an average of 57 eggs (Rosen & DeBach, 1979). Pteromalid parasitoids of Diptera that reproduce by arrhenotoky require host feeding early in their adult life for maximum fecundity, whereas early host feeding reduces fecundity of thelytokous populations (Legner & Gerling, 1967). Host-feeding behavior of insect parasitoids complicates their propagation so that special attention to the parasitoid to host ratio and to parasitization exposure time is necessary. Lasota and Kok (1986a) determined that for optimal production of Pteromalus puparum, a gregarious endoparasitoid of the imported cabbageworm, Pieris rapae (Linnaeus), exposure of 10 freshly formed host pupae to each parasitoid pair for 6 days provided sufficient hosts for host feeding, and sufficient time for egg formation and oviposition before the pupae became too old. Lasota and Kok (1986b) concluded that balanced parasitoid to host ratios are important in the mass production of gregarious parasitoids to optimize host utilization while maintaining parasitoid quality. Host feeding can likewise occur in adult tachinids. Nettles (1987) found that exposing adults of Eucelatoria bryani

to their host, the corn earworm, or to host hemolymph, significantly increased their fecundity. Also, feeding by the host itself sometimes can be important. Chianese (1985) noted that poorly fed gypsy moth larvae would cannibalize other larvae and eat cocoons of their own parasitoid, Cotesia melanoscela. Special T e c h n i q u e s a n d C o n s i d e r a t i o n s Following are a few examples of the many special techniques developed for producing parasitoids and predators, and other considerations that are important. Some of these pertain to the handling of eggs. With eggs laid on a natural substrate, the deposition sites can be cut out and grouped for exposure to egg parasitoids (Morrison, 1985a). Clair et al. (1987) used a cork borer to cut out clusters of elm leaf beetle eggs from elm leaves so that they could be grouped together in a small petri dish for efficient exposure to attack by the eulophid egg parasitoid Oomyzus (= Tetrastichus) gallerucae (Fonscolombe). In research that could prove useful in the future when in vitro culturing of parasitoids may become routine, Eller et al. (1990) studied factors affecting oviposition by the braconid M. croceipes into artificial substrates. Among other things, they discovered that hemispherical substrates with a volume of 35 to 40/zl were preferred; that more eggs were laid in colored substrates, with the highest number oviposited in blue substrate; and that the number of eggs laid increased with the color concentration. Kainoh and Brown (1994) found that Chelonus sp. nr. curvimaculatus females would actively oviposit into artificial eggs constructed with various amino acids or insect culture media sandwiched between Parafilm | sheets. The amino acids arginine, histidine, and lysine stimulated intense ovipositional activity from Chelonus adults, but more parasitoid eggs were oviposited into artificial eggs containing Trichoplusia ni larval hemolymph than were those containing amino acids or artificial insect culture media. In anticipation of the artificial rearing of the predaceous anthocorid Orius insidiosus (Say), Castane and Zalom (1994) successfully developed a gelatinous ovipositional medium made from carrageenan salt of potassium chloride and covered with paraffin wax. They noted that an artificial substrate is useful in mass rearing of insects because the medium is available for use at any time of the year, and the likelihood of colony contamination by pathogens or pesticide residues is reduced. Age of adult entomophagous females is an important factor in determining the most efficient ovipositional period for a production program. Ramadan et al. (1989) reported that 94.4% of the total progeny of adult females of the braconid Diachasmimorpha tryoni were produced during the age interval of 5 to 20 days, and that progeny production and the ratio of female progeny declined significantly

Chapter 7

Culture and Colonization

thereafter. Likewise, as mentioned previously, Greenberg et al. (1995) showed that in the mass production of the boll weevil parasitoid Catolaccus grandis, the maximum percentage of female progeny (between 54.0 and 77.2%) was attained by ovipositing females that were 5 to 20 days old. Two factors to be considered in rearing egg parasitoids are the age of the host eggs and their fertilization status. Reznik and Umarova (1990) indicated that Trichogramma embryophagum (Hartig) and T. semblidis (Aurivillius) preferred to oviposit into young eggs of the Angoumois grain moth and suggested that old eggs inhibited oviposition by some Trichogramma spp. At least in some cases, successful parasitoid development may only occur in fertilized host eggs, and is possibly related to amino acid content, as indicated for the scelionid Telenomus remus Nixon, which parasitizes the noctuid Spodoptera litura (Fabricius) (Gautam, 1986). In China, mass production of Trichogramma spp. involves the grinding of freshly emerged oak silkworm female moths to extract infertile eggs (King & Morrison, 1984). Cleaning and drying the eggs follows, after which storage at low temperatures occurs for several weeks before use. Similarly, King and Hartley (1985c) extracted parasitoid maggots from adult females of the tachinid Lixophaga diatraeae with a small blender. Dispensing the maggots with a special machine followed their chemical treatment, collection, rinsing, and suspension in 0.15% agar solution (Gantt et al. 1976; King & Hartley, 1985c). Mechanical extraction of maggots from fecund females of Archytas marmoratus was performed by Gross (1994), who then applied them in aqueous suspension into corrugated cardboard disks (13-cm in diameter by 2-cm in depth) (19.5 maggots per cm 2) against approximately 600 mature larvae of Galleria mellonella. David et al. (1989) tried to increase parasitism by the tachinid Sturmiopsis inferens by removing the parasitoid chorion before inoculation, but found this to be unnecessary. They also discarded the technique of hand inoculating individual host larvae when they discovered that tachinid maggots suspended in 0.15% agar were just as effective in host finding. It is not unusual for other tachinids to also require special rearing efforts. For instance, Mellini and Campadelli (1989) experimented with rearing Pseudogonia rufifrons on artificial diet, and with using chemical and physical techniques for in vitro hatching of the tachinid eggs. They found centrifugation of uterus-extracted eggs in saline solution to be the most effective procedure for obtaining high egg hatch without affecting larval viability. Cannibalism among predaceous entomophages, and predation by hosts require special attention. To prevent larval cannibalism in green lacewings, Morrison (1985b) sealed larvae in separate chambers and fed them through an organdy cloth with prefrozen lepidopteran eggs. To reduce

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similar cannibalism among the larvae of the carabid Calosoma sycophanta Linnaeus, a predator of the gypsy moth, Weseloh (1996) reared them in groups in plastic containers having 3 cm of moist peat moss in the bottom. By feeding the larvae with gypsy moth pupae placed on top of the peat moss in the ratio of at least 0.5 pupae per day per larva, the larval mortality from cannibalism was reduced to 50%. In a case of host predation of its parasitoid, Chianese (1985) reduced gypsy moth larval predation of parasitoid cocoons of Cotesia melanoscela by regularly collecting cocoons that were sufficiently hardened to prevent handling damage. Kairomones and pheromones may concentrate in insectrearing cages where there is little air movement, and hence no odor gradient to stimulate normal insect response. Chiri and Legner (1982) showed that the parasitoid Chelonus sp. nr. curvimaculatus responded to kairomones emitted by body scales not only from its natural host, the pink bollworm, but also from unnatural hosts such as the beet armyworm. Chiri and Legner (1982) speculated that high populations of beet armyworms in cotton fields would reduce pink bollworm parasitization because of kairomonal distractions. Similarly, a uniform accumulation of kairomones or pheromones in enclosed insectary spaces could interfere with insect production and would make necessary the adequate provision of fresh air. In working with the parasitic tachinid Bonnetia comta (Fallrn), Cossentine and Lewis (1986) used host odor to induce larviposition by moistening filter paper with an aqueous suspension of fecal material of the black cutworm. Rubink and Clement (1982) found that fecal pellets from late instar larvae of the black cutworm provided the greatest intensity of larviposition by this tachinid. Likewise, Grenier et al. (1993) reported that surface treating artificial host eggs with Ostrinia nubilalis scale extract, or a mixture of compounds found in O. nubilalis egg masses, stimulated oviposition by the egg parasitoid Trichogramma brassicae. Waage et al. (1985) remarked that host defense reactions are important in rearing some parasitoids. It is inadvisable to produce parasitoids on hosts exhibiting defense reactions such as encapsulation of parasitoid eggs or larvae, or to field release them on such hosts. For example, even after rearing the braconid Leiophron uniformis (Gahan) for 11 generations on an alternate host, Lygus lineolaris (Palisot de Beauvois), DeBolt (1989) still found no increased parasitoid resistance to encapsulation by that host. However, Strand and Vinson (1982) noted that eggs lack such defense mechanisms and may be useful factitious hosts. They demonstrated that a recognition hormone from a normal host stimulated oviposition by a scelionid parasitoid, Telenomus heliothidis, in eggs of nonhosts. Such recognition hormones could thus be useful for producing specific egg parasitoids in nutritionally acceptable nonhosts.

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As with herbivorous insect production, extended storage of entomophagous insects is very useful. Morrison and King (1977) reviewed various techniques and concluded that in almost all, low temperatures were used to reduce developmental rates. The potential duration of a low-temperature storage period varies with the entomophage species. Of parasitoids stored the longest, prepupae of the pteromalid Pteromalus puparum held at 10~ for up to 15 months still eclosed and produced viable progeny, although the mean number of adults emerging per host chrysalis declined progressively after 4 months (McDonald & Kok, 1990). Storage of adult females of the bethylid Scleroderma guani Xiao & Wu, also at 10~ had no significant influence on their ability to parasitize after 6 months (Chen et al., 1989a). Similarly, Palmer (1985) reported that storing adults of the gypsy moth parasitoid Brachymeria intermedia for at least 5 months at 10~ and 50% RH was possible, although there was a mortality of 30 to 50%, depending on sex ratio (males were unable to survive prolonged storage). However, it was best not to store Brachymeria intended for field release for longer than 48 h at 16~ On the other hand, mummies of Trioxys indicus could be held for up to 1 month at 4~ prior to field release of the adults on aphid hosts (Singh & Agarwala, 1992). Storage of other parasitoids is often only suitable for days instead of months. Papacek and Smith (1985) noted that storage of the California red scale parasitoid, Aphytis lingnanensis, could not exceed 3 days at 16~ Maggots of the tachinid Archytas marmoratus contained within corrugated cardboard disks could also only be effectively stored for 3 days at 10 and 18~ before Galleria mellonella larvae were introduced for parasitism, without significantly affecting the percentage recovery of A. marmoratus adults (Gross, 1994). Pupae of Campoletis chlorideae Uchida, an ichneumonid parasitoid of the Heliothis armigera, could be stored at 8~ for just 10 to 15 days without reduced adult life span, and adult emergence fell to 42% after 35 days of storage (Patel et al., 1988). Holding freshly formed cocoons or 1-day-old mated adults of the braconid Cotesia marginiventris (Cresson) at either 5 or 10~ for longer than 20 days caused a sharply rising mortality, significantly reduced adult longevity and fecundity, and produced a preponderance of male progeny (Jalali et al., 1990). Similarly, cocoons of the braconid Allorhogas pyralophagus Marsh held at 5 or 10~ for 35 days yielded parasitoids that produced only male progeny (Ballal et al., 1989). However, Adiyaman and Aktumsek (1996) were able to satisfactorily store the ichneumonid Pimpla turionellae as either pupae or adults at 4~ for 30 days. Jalali and Singh (1992) found that cold storage differentially affected four species of Trichogramma, with the maximum storage period being 49 days at 10~ Some workers have experimented with the use of conditioning periods before cold storage. Singh and Srivastava

(1988) reported that a conditioning period of 72 h at 12 to 15~ for newly formed aphid mummies containing Trioxys indicus before a 10-day storage period at 6~ allowed maximum adult emergence (78%). However, they still obtained good emergence (72%) after a month of storage at 4~ following a 72-h prestorage period at 12 to 15~ Concerning entomophagous predators, Morrison (1985b) found that measurable viability reduction occurred with eggs of the common green lacewing held at 13 to 14~ and 70 to 80% RH for more than 10 days. However, Tauber et al. (1993) were able to store adults of the green lacewing at 5~ and short-day length for 31 weeks, with about 97% survival, greater than 90% of mating pairs producing fertile eggs, and fecundity 50 to 70% that of unstored females. Chang et al. (1995) duplicated these results of storing green lacewing adults for 31 weeks, and noted also that high survival and excellent poststorage reproduction occurred with a high carbohydrate diet before storage and a carbohydrate and protein diet during and after storage. Tauber et al. (1997a) found that adults of a Honduran population of a congeneric lacewing, Chrysoperla externa (Hagen), could be held at 10~ for up to 4 months with a high survival and a high poststorage oviposition rate. They reported that the long-term storage trait was just one of the characteristics that gave the species great potential for mass rearing and use in augmentative biological control. Other predators can also be stored for extended periods. Freshly emerged adults of the clerid Thanasimus formicarius (Linnaeus) could withstand cold storage (4~ for more than 8 months with only 4.2% mortality and no adverse fecundity effects, provided that they could feed at 3-month intervals on their bark beetle hosts (Faulds, 1988). Longterm storage of the predatory midge Aphidoletes aphidimyza was accomplished in its diapause state by Tiitanen (1988), who reported that 66% of diapausing larvae emerged after 7 months at 10~ and by Gilkeson (1990), who indicated that less than 9% mortality occurred after larval storage at 5~ for 8 months. However, the best commercial storage regime to avoid protracted adult emergence was at I~ for up to 2 months after conditioning for 10 days at 5~ (Gilkeson, 1990). Various factors should be considered and tested before cold storing entomophages. As noted before, cold storage can affect progeny sex ratios. As further examples, Clausen (1977) reported that prolonged cold storage of adult Aphidius smithi Sharma & Subba R a o m a parasitoid of the pea aphidminactivated sperm in males or mated females, and Chianese (1985) found that refrigeration of Cotesia melanoscela adults must not occur until after mating. Chilling can also affect entomophage behavior, as noted by Herard et al. (1988a), who observed that chilling pupae of Microplitis demolitor caused most emerging females to be unresponsive to semiochemicals produced by their plant-fed host insect. In concluding this discussion on storing parasitoids and

Chapter 7 Cultureand Colonization predators, we must remember that diapause can be useful in this regard. Although diapause can be an aggravating annoyance in arthropod production, it can also be a beneficial tool in manipulating entomophage rearing. The key is to acquire a complete knowledge of all factors that govern inducement, maintenance, and termination of the diapause state in the particular species being reared. Life cycles of entomophages in the laboratory usually vary between 8 and 42 days, depending on temperature and excluding the effect of diapause. However, it is common for most species to develop in 14 to 30 days. At 26.7~ and constant light, the egg parasitoid Trichogramma pretiosum averages 9.5 days, and T. minutum averages 8 days (Morrison, 1985a). Brachymeria intermedia develops in 15 to 30 days at 24~ (Palmer, 1985), and the common green lacewing requires about 30 days at 26.7~ and ca. 75% RH, with constant light (Morrison, 1985b). Obviously, a thorough study and knowledge of the biological attributes and interactions involved in a rearing system will enable optimal production of a natural enemy. For example, after a detailed rearing study of the interaction of the tachinid Archytas marmoratus with a factitious host, the greater wax moth, Coulibaly et al. (1993) discovered rather precise information that resulted in more efficient production. The adult female tachinids were found to larviposit about 75% of their planidia between the 6th and 1 lth hours from the beginning of the photophase (14 h photophase, 70% RH, 27~ on days 13 and 14 following adult eclosion. High adult yields of the parasitoid (ca. 57%) were then obtained by artificially parasitizing full-grown host larvae with two to eight planidia (Coulibaly et al., 1993). A variety of problems can arise in rearing any entomophage, with solutions requiting adjustments of rearing techniques. A good example of such problem solving was that of Palmer (1985), who developed a production system for rearing the parasitoid B. intermedia on the greater wax moth. Regular removal of moths and scales from oviposition units prevented the scales from interfering with parasitoids ovipositing in pupae. Inactive Brachymeria in the oviposition jars required stimulation by increasing light intensity and/or temperature. The situation where parasitoids were active but the parasitism rate was low involved one or more factors: the wax moth pupae were too old when presented to the parasitoids, the ratio of parasitoids to hosts was too low (25 females to 300 cocoons was necessary), or the photophase was too short (had to be more than 10 h). Furthermore, overheated oviposition jars caused a high mortality of ovipositing Brachymeria (the required temperature was 24 to 26~ Karelin et al. (1989) reported about a number of rearing system modifications that together resulted in a dramatic increase in the commercial production of the common green lacewing. Important changes involved cage shape and volume, oviposition substrate, feeding and egg collection

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methods, and partial mechanization. The modified system yielded 5.6 to 8.7 million eggs per month from just one production line that consisted of 60 cages for adults, 60 cell cages for larvae, and 120 cages for group rearing. Nordlund and Morrison (1992) reviewed other techniques used for rearing Chrysoperla spp., and mentioned a hot wire vacuum removal device with potential for resolving the problem of egg collection. Later, Nordlund and Correa (1995b) described an adult feeding and oviposition unit (AFOU) and a hot wire egg harvesting system that could provide the basis for an automated adult handling and egg harvesting system for the mass production of green lacewings. With respect to oviposition by two species of the brown lacewing genus Sympherobius, the frayed fringe of a coarsely woven cloth stimulated copious egg laying in culture (T. W. Fisher, personal correspondence). Another commercially produced entomophage is the aphelinid Encarsia formosa Gahan, a parasitoid of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood). Popovet al. (1987) described a rearing system that evolved to produce 17 million parasitoids from a 150 m 2 greenhouse area in the same time in which only 1 million had been formerly produced with previous techniques. Massive rearing programs for Trichogramma spp. exist in China, in particular. Tseng (1990) reported on a machine that dramatically improved Trichogramma production efficiency by preparing host eggs on cards, and Liu et al. (1988b) described a computer-controlled machine that successfully made artificial egg cards at the rate of 1200 per hour. It was possible to rear over 6 million Trichogramma individuals from each set of 1200 cards, and these Trichogramma reportedly parasitized sugarcane borer eggs at the rate of 75 to 86% when released inundatively in the field. In mass production technology, notable advanced systems have been or are being developed for the Africa-wide Biological Control Program of the International Institute of Tropical Agriculture (IITA) (Herren, 1987, 1990; Haug et al., 1987). Hydroponic culture techniques were devised for producing cassava, Manihot esculenta (Herren, 1987), and semiautomated systems were in use for producing organisms at three trophic levels (cassava; the cassava mealybug, Phenacoccus manihoti Matile-Ferrero; and its encyrtid parasitoid, Epidinocarsis lopezi) (Haug et al., 1987; Neuenschwander et al., 1989; Neuenschwander & Haug, 1992). For planning the mass production of natural enemies of the cassava green mite, Klay (1990) proposed and described a population model to optimize use of prey material and to minimize labor. Similarly, Carey and Krainacker (1988) discussed extending basic principles of stable population theory in mite populations to include mite mass-rearing. For parasitoid rearing, Carey et al. (1988) used the example of rearing the braconid Diachasmimorpha tryoni on the

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Mediterranean fruit fly to present demographic methods for determining the optimal balance in host-parasitoid rearing systems and for determining optimal harvest rates. Quality The quality of produced entomophages is dependent on their genotype, nutrition, and rearing environment; and is obviously critical to a biological control program. It is futile to expend resources for entomophage production if insufficient quality of the product results in ineffective field establishment or pest control. Moore et al. (1985) discussed quality of laboratory-produced insects, and noted that rearing objectives must first be established. Selection and quantification of species traits pertinent to the objectives then enables establishment of quality standards, and tolerances. Routine assessment measurements of the variables made during insect production are compared to the standards, and quality control regulatory actions for correcting differences between actual and intended quality are then made. It would be impractical to use all the possible quality assessment tests listed by Moore et al. (1985). However, even for very small production programs, it is advisable to use appropriate tests to achieve desired results. Pragmatically, Singh and Ashby (1985) felt that the standard life history measurements of fecundity, fertility, and weights of adults and pupae are adequate as quality indicators. However, entomophage release programs can also include percentage of parasitism or predation rate (Moore et al., 1985). Chambers and Ashley (1984) defined industrial quality control ideas and evaluated their applicability to insect rearing. Bigler (1989) discussed quality control requirements in three successful biological control programs and concluded that careful analysis of each particular situation was necessary for determining significant field performance parameters. A review of quality assessment and control procedures used in mass production of several insect parasitoids revealed the following. King and Morrison (1984) noted that quality assessment of Trichogramma production typically consists of keeping records on numbers reared, parasitization rate, and sex ratio. Quality assessment tests used by Morrison (1985a) for Trichogramma production were percentage of parasitized eggs, percentage of emergence from parasitized eggs, and sex ratio. For performing the tests, it was necessary to take at least three samples of about 200 eggs from each oviposition unit. Accepted quality assessment standards were 80 +_ 10% of parasitism of 48-h-old eggs, 90 _ 5% of adult emergence, and a sex ratio of 1.00 female to 1.25 males. Nordlund et al. (1997) used a number of quality control parameters, including development time,

adult longevity, sex ratio, pupation rate, percentage of pupae to emerge as adults, adult female body length, number of H. zea eggs parasitized by a female, and percentage of deformed females, to assess and to compare T. minutum reared in vitro for 10 generations to those reared in vivo on irradiated H. zea eggs. Cerutti and Bigler (1995) also used most of these criteria to assess the quality of T. brassicae but noted, in particular, the evaluation of fecundity on eggs of the natural host, an indirect measure of the acceptance and suitability of natural-host eggs. Dutton et al. (1996) likewise evaluated the fecundity of T. brassicae on its natural host (the European corn borer) but incorporated this measurement together with walking speed and life span to calculate a quality index. This index, plus a measure of the fecundity on the factitious host (Anagasta kuehniella), showed a correlation to T. brassicae field parasitism, for different T. brassicae populations. For quality control of Trichogramma spp. in China, vigor is maintained in laboratory cultures by forcing adult females to fly several feet in search of host eggs to eliminate weak individuals (King & Morrison, 1984). In the former USSR, combining quality control and quality assessment of Trichogramma was possible by use of a device through which the parasitoids had to pass a distance of 3 m to reach host eggs, with quality assessment then determined from the numbers of eggs parasitized (Torgovetskij et al., 1988). Flight quality assessment tests have been used for Encarsia formosa (Doodeman et al., 1994; Roskam et al., 1996), T. brassicae (Dutton & Bigler, 1995), and the rhizophagid Rhizophagus grandis Gyllenhal--a predator of Dendroctonus micans Kugelann (Couillien & Gregoire, 1994). ODell et al. (1985) used parasitoid size, longevity, and fecundity parameters to check quality of gypsy moth parasitoids. A variety of factors affected these parameters, including host diet, host density, microbial infection of the host, and environmental changes. Quality assessment in production of Cotesia melanoscela, a parasitoid of gypsy moth larvae, consisted of determining fecundity, defined as the number of progeny produced (ca. 100), instead of the number of eggs laid (ca. 1000) (Chianese, 1985). Palmer (1985) used the following quality assessment parameters in producing the gypsy moth parasitoid B. intermedia: (1) production totals per cage, per week, and per month; (2) percentage of successful parasitism; (3) female to male ratio; and (4) percentage of recovery from storage. The standard and minimal acceptable values for percentage of parasitism were 70 to 75 and 60%, respectively. King and Hartley (1985c) used the following standards in assessing the quality of mass-produced Lixophaga diatraeae: (1) puparial weight (male = 14 mg, female = 20 mg), (2) percentage of parasitism (90%), (3) number of maggots per female (70), and (4) maximum of adult longevity (male = 29 days, female = 24 days).

Chapter 7

Culture and Colonization

COLONIZATION OF E N T O M O P H A G O U S ARTHROPODS Liberation P r o c e d u r e s Entomophages propagated in the insectary are field released to effect establishment. Establishment may occur with ease and rapidity or with difficulty over a long time, or may not occur at all. The ease of insectary rearing does not correlate with ease of field establishment. In analyzing the successful biological control of the alfalfa blotch leaf miner, Agromyza frontella (Rondani), in the northeastern United States, Drea and Hendrickson (1986) noted that none of the most abundant and most easily reared European parasitoids became established. The most successful species were obtained by laboriously collecting 30,000 to 40,000 host puparia in Europe and subjecting them to specially developed laboratory recovery techniques to obtain healthy parasitoid individuals for field release. Working with the same leaf miner, Harcourt et al. (1988) directly field released a genetically diverse group of 586 adults of the braconid Dacnusa dryas (Nixon) in eastern Ontario. The release site served as a "field nursery" for parasitoid reproduction, with specimens collected and released at various other sites. Within 3 years, the parasitoid had reduced leaf miner populations 50-fold. They subsequently collapsed to subeconomic levels. Desirable characteristics of this successful parasitoid were high dispersal capacity, host specificity, synchronization with the host life cycle, and high adaptability to diverse environmental conditions. Another technique in field establishment is to make many releases over a short time. Krishnamoorthy and Singh (1987) obtained complete biological control of the citrus mealybug in southern India by introducing the encyrtid parasitoid Leptomastix dactylopii Howard. Repetition of field releases occurred 9 to 24 times over a short period of 2 to 4 months. Two orchards received 11,394 and 26,380 adults of the parasitoid, respectively. It is obviously best to rapidly biologically control a new pest. Discovery of the citrus blackfly in Barbados in 1964 prompted quick biological control importations in the same year before the blackfly reached problematic levels. The aphelinid parasitoids Eretomocerus serius Silvestri and Encarsia clypealis increased rapidly and controlled the blackfly within 9 months (Bennett, 1966; Bennett & van Wherlin, 1966; Clausen, 1977). Rapid biological control also occurred when the southern green stinkbug first appeared in Hawaii in late 1961. Importations of the parasitic scelionid Trissolcus basalis and the tachinid Trichopoda pennipes pilipes (Fabricius) in 1962 resulted in control of the pest by 1965 (Clausen, 1977).

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An example of swift biological control was that of the ash whitefly, Siphoninus phillyreae (Haliday), an aleyrodid that invaded and rapidly spread throughout California beginning before mid-1988 when it was first detected (Pickett et al., 1996). In 1989, outbreak populations occurred on ornamental trees in several major urban centers. Within 3 years of the whitefly's invasion of California, the aphelinid Encarsia inaron (Walker) was imported, mass reared, and released in 43 of 46 affected counties. Within 2 years of initial releases, E. inaron rapidly spread and established, and the infestation density of the ash whitefly decreased by 90 to 95%. The preserved economic value of the saved ornamental trees was estimated to be nearly $300 million in retail replacement values (Pickett et al., 1996). Field releases may consist of immature instead of mature entomophages. Katsoyannos and Argyriou (1985) released the aphelinid Encarsia perniciosi (Tower) against the San Jose scale, Quadraspidiotus perniciosus Comstock, by suspending squash fruit infested with parasitized scales in almond orchards. For field colonization of the aphidiid Pauesia sp., Kfir et al. (1985) suspended small logs heavily infested with parasitized black pine aphids 1.5 to 2.0 m high in trees. They reported rapid spread and establishment of the parasitoid, due to its high dispersal rate and searching ability. For control of the Colorado potato beetle, Hough-Goldstein et. al. (1996) obtained excellent results by releasing nymphs of the pentatomid Perillus bioculatus (F.) in small plots. Control was nearly as good when the predator was released in the egg stage if the eggs were protected in screened cups. Takahashi (1997) found that second-, third-, and fourthinstar larvae were the optimal stages of the coccinellid, Coccinella septempunctata brucki Mulsant, to release in alfalfa fields to control the blue alfalfa aphid, Acyrthosiphon kondoi Shinji. The optimal release time was early March when the maximum temperature was around 10~ With the predaceous coccinellid Chilocorus nigritus (Fabricius), Hattingh and Samways (1991) found that the adult was the most suitable stage for field release. This is because first-instar larvae cannot attack adults of the host scale, Aonidiella aurantii, and because adult beetles mass-reared on oleander scale will increase feeding rates when released on A. aurantii, whereas beetle larvae will not readily accept the dietary change (Samways & Wilson, 1988). Shepherd (1996) also addressed the issue of which stadium of biological control insects should be field released, as well as the issue of timing the releases. Particular reference was made to the leaf-mining moth, Dialectica scalariella (Zeller), a gracillariid that attacks the weed Paterson's curse (Echium plantagineum). Besides its utility in classical biological control, a "field insectary" is particularly useful for inoculative augmenta-

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tion, where early season releases of small numbers of entomophages at key locations can achieve effective biological control. This is advisable when the entomophage has a short life cycle, high fecundity, and great vagility, yet cannot persist around the year. An example was the release of Pediobius foveolatus on Mexican bean beetles in small areas of snap beans, Phaseolus vulgaris, from which they spread to adjacent soybean fields (Stevens et al., 1975; King & Morrison, 1984). Similar inoculative releases of this parasitoid protected urban gardens from damage by the Mexican bean beetle (Barrows & Hooker, 1981). Likewise, Halfhill and Featherston (1973) made inoculative releases of the parasitoid Aphidius smithi, in field cages on the pea aphid, and then allowed the millions of progeny to spread to adjacent alfalfa. Inoculative and inundative releases of biological control agents are now rather common in greenhouses. Ravensberg (1992) provided an excellent historical and technical review of the use of natural enemies in European greenhouse crops. Hansen (1988) effectively protected cucumbers grown in greenhouses from the onion thrips, Thrips tabaci Lindeman, by making three to four releases of the predatory phytoseiid mite Amblyseius barkeri (Hughes) at rates of 300 to 600 per square meter. Establishing the predator before the thrips appeared enhanced success. Periodic colonization of Encarsia formosa was successful against the greenhouse whitefly in Canada (Clausen, 1977). In certain areas of Australia the parasitoid has become permanently established and effective both in greenhouses and outdoors. In this regard, Gerling (1966) determined that temperatures above 24~ were necessary for the parasitoid to control the whitefly. King and Morrison (1984) also noted the extensive use of E. formosa in Europe to augmentatively control the greenhouse whitefly. Stinner (1977) generally reviewed the efficacy of inundative field releases; and Goodenough (1984) reviewed improved packaging and distribution equipment, materials, and procedures for releasing the egg parasitoid, Trichogramma pretiosum (also see Reeves, 1975; Jones et al., 1977; Jones et al., 1979; Bouse et al., 1980, 1981). Likewise, Smith and Wallace (1990) described ground systems for releasing T. minutum in plantation forests. Gardner and Giles (1996) obtained good results from the simulated mechanical distribution and release of commercially produced eggs of Chrysoperla rufilabris in an egg/vermiculite mixture, as well as from spraying an aqueous suspension of C. rufilabris eggs or of Anagasta kuehniella eggs parasitized with T. pretiosum (Gardner & Giles, 1997). Similarly, Sengonca and Loechte (1997) developed spray and atomizer techniques that allowed a targeted deposition of intact eggs of the common green lacewing on sugar beet plants in the field. Aircraft releases of entomophagous parasitoids have occurred with Trichogramma spp. (Ridgway et al., 1977; Bouse et al., 1981; Smith et al., 1990), with Lixophaga

diatraeae (Ridgway et al., 1977), and with Chelonus spp. in cotton fields (E. F. Legner, unpublished). A classic example of this type of release was the distribution by air of Neodusmetia sangwani (Rao) to control the Rhodes grass mealybug Antonina graminis (Maskell) in Texas in a very large and successful program (Dean et al. 1979). Aerial-release technology was crucial for liberating the cassava mealybug parasitoid, Epidinocarsis lopezi, and cassava green mite predators in Africa, because ground releases would have been a major obstacle to achieving rapid control of the pests in the huge cassava belt (Herren, 1987). Notable features of the systems developed were an automatic acceleration of the parasitoids in the release device before ejection to reduce deceleration effects outside the aircraft, and a streamered container for predaceous mites that allowed retention in the cassava plant canopy for effective mite dispersal (Herren et al., 1987).

Collection a n d Dissemination Once entomophages establish at various loci in the range of a pest, a program of field collection and distribution to effect complete dissemination is advisable. For example, van den Bosch et al. (1959) used alfalfa cuttings and mechanical sweeper collections to increase the distribution of Praon exsoletum and Trioxys utilis Muesebeck on their host, the yellow clover aphid, a serious pest that invaded California in the 1950s. Collection and distribution also followed the establishment of the braconid Microctonus aethiopoides (Nees) on the Egyptian alfalfa weevil in California. Parasitized adult weevils collected from estivation sites on trees produced parasitoids used for further field distribution (L. Etzel, unpublished). Two primary benefits of this technique were the high vigor and fitness of the recovered parasitoids, and the reduced costs resulting from using nature as an "insectary." Similarly, the Animal and Plant Health Inspection Service (APHIS) of the United States Department of Agriculture (USDA) distributed the ichneumonid Bathyplectes anurus (Thomson) for biological control of the alfalfa weevil Hypera postica (Gyllenhal) and the Egyptian alfalfa weevil H. brunneipennis (Kingsley et. al., 1993). This parasitoid has only one generation per year in nature, with two diapauses in its life cycle, and is thus very difficult to culture. Field establishment in the eastern United States required direct field releases of annually imported wild stock from Europe. After several years, B. anurus finally increased to sufficient abundance at some sites to enable the collection of large numbers that could be redistributed to other areas. A large program subsequently developed by APHIS effected a more general dispersal of this and other species (Kingsley et al., 1993). One of the largest collection and distribution programs

Chapter 7

Culture and Colonization

in the history of biological control occurred in Mexico in 1950 through 1953, following importation of several Indian and Pakistani species of parasitoids to be used against the citrus blackfly. A special gasoline tax levied to support this program funded a peak employment of 1600 workers (Clausen, 1977). As mentioned, difficulties with mass production make collection and distribution programs particularly desirable. Harris and Okamoto (1983) reported that sex-ratio problems in culture prevented rearing the braconid fruit fly parasitoid Biosteres arisanus in large numbers. A method subsequently developed for parasitoid distribution first involved exposing papaya fruits preinfested in the laboratory with oriental fruit flies to field populations of the parasitoid for 24 h. After the recovered fruit fly larvae completed development on a diet in the laboratory, parasitoids emerged from the resulting puparia. This method allowed one technician to process over 11,000 parasitoids per day. Small-scale collection and distribution can also be effective. Campbell (1975) developed a simple technique for citrus growers to distribute Aphytis melinus for control of California red scale. It involved placing a basket with scaleinfested oranges in an orchard where the parasitoid was active, replacing half the oranges two weeks later, and taking the exposed oranges to new orchards for colonization. Successful redistribution of native beneficial arthropods is also possible. The predaceous phytoseiid Euseius hibisci (Chant) was easily colonized in citrus orchards against the citrus thfips, Scirtothrips citri (Moulton), by transferring orange-branch terminals infested with the predator to six centrally located trees per 4 ha (Tanigoshi & Gfiffiths, 1982; Tanigoshi et al., 1983). The mite readily dispersed aerially among groves within one season, resulting in a dramatic reduction of insecticide treatments. Another method of field colonizing this predator was to place bundles of lima bean seedlings containing the laboratory-reared mite into crotches of citrus trees. An important consideration in relying on the field redistribution procedure is that a successful entomophage might reduce pest populations relatively rapidly, and thereby prevent easy collections. Furthermore, although field collection and distribution of established entomophages can be an expedient method of enlarging their establishment areas, caution is necessary to avoid the simultaneous dispersal of pest insects, hyperparasitoids, and other unwanted organisms. The Australian biological control program against black scale resulted in transferring many indigenous species around the country, including predaceous coccinellids and lepidopterans. Unfortunately, the distributed species also included the native hyperparasitoids Coccidoctonus whittieri (Girault) and Myiocnema comperei Ashmead (Clausen, 1977).

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Principal Factors Influencing E s t a b l i s h m e n t or Effectiveness

Species and Biotypes It is not unusual for an entomophage species to have biotypes that vary in characteristics such as climatic or host population suitability. For example, King et al. (1978) demonstrated differences between populations of the tachinid Lixophaga diatraeae. Also, Jalali and Singh (1993) discovered that populations of Trichogramma chilonis Ishii collected from two of six cotton ecosystems in different agroclimatic zones of India were superior for mean fecundity, longevity, net reproductive rate, and rate of increase per female per generation. Likewise, Haardt and Hoeller (1992) showed pronounced differences among six isofemale lines of the aphid parasitoid Aphelinus abdominalis (Dalman) with respect to life history traits. In fact, crossing experiments revealed reproductive barriers that indicated the possible existence of sibling species. Work with species biotypes has included that for T. evanescens (Ram et al., 1995), T. exiguum (Gomez et al., 1995), and Microctonus spp. (Phillips & Baird, 1996; Goldson et al., 1997; Phillips et al., 1997). Obrycki et al. (1987) reported that there are two observed biotypes of Edovum puttleri, an egg parasitoid of the Colorado potato beetle. They believed that matching biotypes to the agronomic and climatic conditions of the release areas would be important in achieving maximum control. Ruberson et al. (1989a) also compared the two biotypes and suggested using the intraspecific variability for genetic improvement. Because of species biotypes, workers may seek the same entomophage species from many different areas and then rear the different collections separately to maximize field effectiveness of the released species. However, Clarke and Walter (1995) reviewed the literature on the classical biological control tactic of multiple introductions of conspecific populations of a natural enemy, and concluded that out of 178 identified projects, only 11 achieved eventual success with a second or later introduction of a conspecific population; and the success of at least 5 of these was thought to be due to sibling species. They suggested from their analysis that importation of different species, instead of additional biotypes, would be a more productive use of resources. Sujii et al. (1996) performed a multivariate analysis on 21 potential biological control insect agents found feeding on the weed sicklepod (Senna obtusifolia) in Brazil, based on frequency of occurrence of each species, degree of insect/host association, and damage level. They determined on the basis of feeding guilds that introductions of a number of these species could be considered, and concluded that multivariate analysis can be a potentially useful tool in selecting candidates to be biological control agents. At the

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pest level, Barbosa and Segarra-Carmona (1993) reviewed criteria for the selection of pest arthropod species as candidates for biological control. Especially in inundative release programs, the suitability of the released entomophage for its intended host must first be determined. For example, in South Africa, the egg parasitoid T. pretiosum was mass-produced and liberated against Heliothis armigera, but with poor results, caused at least partly by H. armigera being a generally unsuitable host (Kfir, 1981). Harrison et al., (1985) likewise stressed the importance of precise taxonomic identification and biological testing of Trichogramma spp. before mass production for inundative releases. They found that T. pretiosum was preferable to T. exiguum to augmentatively control Heliothis spp. on Mississippi central delta cotton, because T. pretiosum could develop at the 35~ temperatures common in that area. To find suitable egg parasitoids for field release, Wuehrer and Hassan (1993) biologically tested 47 strains of Trichogramma and two strains of Trichogrammatoidea for their ability to attack the diamondback moth, Plutella xylostella. Likewise, Li et al. (1994) found that Trichogramma sp. nr. sibericum Sorokina, an indigenous species collected from eggs of the blackheaded fireworm, Rhopobota naevana (Htibner), a tortricid pest in cranberry fields, showed a high laboratory parasitism of fireworm eggs, whereas commercial T. minutum and T. evanescens displayed a low parasitism rate. Although the affinity to its natural host decreased after 17 generations reared on eggs of the noctuid Peridroma saucia (Htibner), percentages of acceptance and of parasitism by T. sp. nr. sibericum were still higher than those of the commercial Trichogramma. Another example of seeking a parasitoid species that is effective against its intended host was the selection of T. (Trichogrammanza) carverae (Oatman & Pinto), one of four candidate indigenous species of Trichogramma collected from vineyard egg masses of Epiphyas postvittana, as a potentially commercially viable biological control agent (Glenn & Hoffmann, 1997; Glenn et al., 1997). Inundative release trials using small blocks within commercial vineyards showed that >75% of the egg masses in the vineyard could be parasitized by T. carverae at release rates of 70,000 Trichogramma per hectare with as few as 30 release sites per hectare (Glenn & Hoffmann, 1997). Landry et al. (1993) developed a rapid DNA analysis system that enabled them to characterize individuals from species of the egg parasitoid genera Anaphes and Trichogramma. They stressed the importance to commercial biological control of being able to distinguish genetic variations that would be undetectable by traditional taxonomy. Similarly, Edwards and Hoy (1995a) used a randomly amplified polymorphic DNA polymerase chain reaction (RAPD-PCR) technique, together with discriminate analysis, to distinguish individuals of two biotypes of the walnut aphid parasitoid, Trioxys pallidus, in the laboratory. They

then used the technique to determine the fate of an insecticide-resistant biotype of the parasitoid after field release (Edwards & Hoy, 1995b). Likewise, Messing and Croft (1991) proposed that electrophoretic markers could be used to track the degree of field establishment and dispersal of imported foreign biotypes of phytoseiid mites. Climate and Weather

As noted earlier, researchers generally make every effort to obtain entomophages from areas with climates similar to those at the release sites. In an examination of the establishment of introduced parasitoids, Stiling (1990) concluded that the climatic origin of a parasitoid had a large influence on its establishment rate. Messenger and van den Bosch (1971) reported the classic example of the importation of two climatic biotypes of the parasitic braconid T. pallidus to control the walnut aphid, Chromaphis juglandicola (Kaltenbach), in California. A biotype of the parasitoid from France controlled the pest in the cooler coastal walnut-growing areas of California, whereas a biotype from Iran brought the aphid under control in the warmer Central Valley (Messenger & van den Bosch, 1971). Current weather is likewise important in parasitoid releases. Laboratory experiments by Gross (1988) determined that unfavorable temperatures and RHs, and levels of free water at eclosion could have pronounced adverse effects on emergence of the egg parasitoid Trichogramma pretiosum. He noted the importance of identifying these effects on Trichogramma emergence at field liberation sites. The commonly erratic results of Trichogramma releases might be due to inattention to such factors (Gross, 1988). Bourchier and Smith (1996) confirmed this by analyzing the effects of weather conditions on the field efficacy of mass-released T. minutum. Temperature, the most important single variable, caused up to 75% of the variation in field parasitism, but there was also a significant negative relationship between the mean RH and the odds of parasitism in the field. Poor weather conditions following a release made laboratory quality parameters ineffective in predicting field efficacy. Chihrane and Lauge (1994, 1996, 1997) verified the importance of temperature on the effectiveness of inundative field releases of T. brassicae against the European corn borer. They showed that heat shocks of 44~ for 6 h resulted in lower fecundity and in drastically reduced proportion of female progeny. Wang et al. (1997) found that a higher mean temperature adversely affected the level of parasitism by T. ostriniae on European corn borer during hotter times of the season and conversely that lower temperatures (< 17~ reduced the egg parasitism during cooler periods. Other investigators have also considered weather effects on entomophage releases. Releases of the coccinellid Chilocorus bipustulatus Linnaeus against the white date scale,

Chapter 7 Cultureand Colonization Parlatoria blanchardi (Targioni-Tozzetti), in date palm oases at 700- to 1600-m elevation in northern Niger were most successful during the rainy season (Stansly, 1984); and Smith (1988) considered the effect of wind and other factors on the fate of T. minutum released inundatively against the spruce budworm. Weather, because of fluctuating temperatures, governs the seasonal appearance of pests. Consequently, Yu and Luck (1988) referred to the use of temperature-dependent, stagespecific developmental rates for timing parasitoid releases.

Habitats If a pest insect attacks a variety of both economic and noneconomic plants, it is advisable to attempt to establish natural enemies of the insect on the greatest possible number of alternative plant hosts. Such establishment on noneconomic plants will increase reservoir populations of the beneficial organisms where they will be unaffected by pesticides (Argyriou, 1981). In South Africa, Hattingh and Samways (1991) established the coccinellid Chilocorus nigritus on the nontarget scale Asterolecanium sp. on giant bamboo. The coccinellid then easily moved to adjacent citrus orchards to attack the target prey, the California red scale. Noncrop vegetation can be beneficial for introduced natural enemies even if their hosts are not found there. Dyer and Landis (1996, 1997) studied the habitat relationships of the ichneumonid Eriborus terebrans (Gravenhorst), the most abundant imported parasitoid of the European corn borer in Michigan. Their studies indicated that E. terebrans needs woodlot habitats adjacent to cornfields for sources of sugar and moderate microclimate unavailable in early season corn. They suggested that perennial habitats adjacent to annual agricultural crops may be necessary to provide resources needed for the successful maintenance of natural enemies and effective biological control. Dix et al. (1995) generalized that field edges where crops and edge vegetation meet provide a necessary habitat for maintaining natural enemies; and thus should be managed as to plant species and arrangement, consideration of optimal field sizes, and number of edges. Tietze (1994) also emphasized the importance of field edge grass, weed, and shrub communities that contain a high diversity of species due to their resource spectrum, thus having great regulation potential. Wissinger (1997) suggested that many indigenous and introduced natural enemies that attack pests of annual crops might be "cyclic colonizers" that, following disturbance in the crops, disperse to permanent refugia where they delay reproduction, overwinter, and then recolonize the following year. Therefore, effective biological control strategies in annual crop systems must provide permanent habitats that can act as reservoirs for natural enemies. Such strategies will depend on an increased information base about seasonal cy-

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cles, dispersal behavior, and overwintering ecology of natural enemies (Wissinger, 1997). Pesticides in habitats always present a problem for entomophage releases. For example, Maier (1993) was only able to establish the encyrtid Holcothorax testaceipes (Ratzeburg) on the gracillariid leaf miner Phyllonorycter blancardella in unsprayed apple orchards. In another situation, Mansour et al. (1993) reported unusual effects of pesticides used in apple orchards where augmentative releases of the phytoseiid mite Typhlodromus athiasae Porath & Swirski were made. Laboratory tests revealed that the insect growth regulators triflumuron and fenoxycarb and the fungicide triadimenol caused only a slight mortality of the phytoseiid but a highly significant reduction in fecundity, whereas the same pesticides increased the fecundity of the phytophagous mite Tetranychus cinnabarinus Boisduval.

Adaptation One possibility in the successful introduction of a biological control agent into a new environment is that the agent may have genetically adapted to the new pest population, habitat, and/or climate. Hopper et al. (1993) noted that instances where an introduced species is rare for a long time and then suddenly increases dramatically in population size may indicate genetic adaptation, but may also be explained by demographic models. Nonetheless, lack of postrelease adaptation of an entomophage to a new environment or specific host races can cause either failure in field colonization or reduction in effectiveness. For example, the encyrtid Metaphycus luteolus (Timberlake) from Californian brown soft scale would not adapt to the brown soft scale found in Texas (Clausen, 1977).

Dispersal Entomophage dispersal varies greatly between species. Nevertheless, even entomophages that disperse slowly can be effective biological control agents, as shown with the Rhodes grass mealybug parasitoid, Neodusmetia. Also, the red wax scale, Ceroplastes rubens Maskell, which is serious on citrus in Japan, was controlled successfully by the encyrtid Anicetus beneficus Ishii & Yasumatsu. However, inasmuch as the natural spread of the parasitoid was at the rate of only 1 mi in 2 years, successful control of the scale required parasitoid distribution from the area of initial establishment (Clausen, 1977). Hosts can often considerably assist parasitoid dispersal. As Clausen (1977) noted, the occurrence of alate females in many species of aphids can greatly facilitate dispersal of early parasitoid stages carried in their bodies. Rapid dispersal of Praon exsoletum occurs because it frequently parasitizes the winged adult of its host, the yellow clover

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aphid, which then carries the immature parasitoid for long distances during aphid migratory flights. Trioxys utilis, on the other hand, depends mainly on its own locomotion for dispersal, because it usually kills its host before the aphid can reach the winged stage (Schlinger & Hall, 1959). Some entomophages can disperse phenomenally by their own locomotion. The encyrtid Anagyrus indicus Shafee et al. dispersed as much as 61 km in 1 year after being released in Jordan against Nipaecoccus viridis (Newstead), a citrus pest (Meyerdirk et al., 1988). Releases of 41,054 had been made over an 18-month period, some directly into the trees and some into organdy sleeves tied around infested branches. In Turkey, the aphelinid Eretmocerus debachi Rose and Rosen was imported from Califomia in 1986 for release against the whitefly Parabemisia myricae (Kuwana), an aleyrodid that was one of the most serious citrus pests. Eretmocerus debachi was also capable of spreading 60 km in a year, and reduced the pest population from 17 immature stages per leaf to less than 0.1 stages per leaf within 3 years (Sengonca et al., 1993). Another instance of remarkable dispersal was reported by Agricola et al. (1989), who introduced an encyrtid parasitoid, Gyranusoidea tebygi Noyes, into Togo against the pseudococcid Rastrococcus invadens Williams. The parasitoid significantly controlled the pest in a range of ecological conditions at up to 100 km from each release point within a year. Contrarily, although Omwega et al. (1997) concluded that Cotesia flavipes, an exotic endoparasitoid of Chilo partellus in northern Tanzania, had dispersed about 60 km/year, and Mason et al. (1994) suggested that Lydella thompsoni, a parasitoid of the European com borer, had dispersed from Delaware at about 50 km/year, there was no indication that either of these parasitoids was exerting effective biological control of its host. Too much dispersal or uneven dispersion can be troublesome with augmentation programs. Augmentative releases of the coccinellid Hippodamia convergens Gurrin in Califomia field crops are useless because the beeries immediately leave the release sites (DeBach & Hagen, 1964). In commercial greenhouses, problems of obtaining even dispersion of coccinellids and chrysopids make them unsuitable for augmentative biological control (Chambers, 1986). Augmentative releases of the tachinid Lixophaga diatraeae against the sugarcane borer resulted in rapid dispersal from the release sites, which negated the effects expected from releasing mated females at different rates in three adjacent fields (King et al., 1981). However, there was some indication that the parasitoids remained more confined to sugarcane fields surrounded by woodlands. In experiments on the problem of retaining augmentatively released parasitoids in a target area, Trichogramma pretiosum produced significantly higher parasitization rates

on com earworm eggs on field peas and cotton when it had prerelease exposure to com earworm eggs in the laboratory (Gross et al., 1981). There is also the possibility of using kairomones to improve the efficiency of augmentatively released parasitoids (Gross et al., 1975, 1984). Hare et al. (1997) showed this in field experiments in which the parasitoid Aphytis melinus, which had been insectary reared on oleander scale on squash, was released to attack Califomia red scale on citrus trees. Specimens of A. melinus that had been preconditioned by exposure to the red scale kairomone O-caffeoyltyrosine produced a greater than expected number of progeny compared to the control strain in all comparisons. They concluded that prior exposure of commercially reared A. melinus to O-caffeoyltyrosine may improve its effectiveness in augmentative release programs to control California red scale. The augmentative use of parasitoids and predators with relatively low dispersal capabilities requires their introduction into a crop at multiple points of release, as for Neoseiulus fallacis (Garman), a phytoseiid predator of the twospotted spider mite in strawberries (Coop & Croft, 1995); for T. brassicae released against the European corn borer (Greatti & Zandigiacomo, 1995); and for T. platneri released against the codling moth in apples (McDougall & Mills, 1997). An extrapolation of the work by Justo et al. (1997) indicates that 90% parasitism of eggs of the southem green stinkbug can be achieved by releasing 2000 Trissolcus basalis adults at 50-m intervals in a tomato field. To manage the dispersal of the curculionid Apion fuscirostre Fabricius for classical biological control of the weed Scotch broom (Cytisus scoparius), Isaacson et al. (1996) used Geographic Information Systems (GIS) distance measures. A useful tool for quantifying dispersal parameters of parasitoids is the fluorescent dust marking and recapture method used by Corbett and Rosenheim (1996), who found that the tiny mymarid Anagrus epos (Girault), an egg parasitoid of the westem grape leafhopper, Erythroneura elegantula Osbom, not only could disperse up to 13 m/day but also showed strong upwind displacement in one trial. Follett and Roderick (1996) recommended that gene-flow estimates be used to characterize dispersal capabilities in biological control organisms. They studied populations of the coccinellid Curinus coeruleus Mulsant, a predator of the leucaena psyllid, Heteropsylla cubana Crawford, to determine population structure and estimate levels of gene flow, and concluded that the inferior dispersal ability of C. coeruleus likely limits its rapid widespread establishment in release programs. Each parasitoid or predator used in arthropod biological control work must be studied for its dispersal characteristics. However, in a study of four species of egg parasitoids in two families that attacked four genera of hemipteran pests in three families, Hirose et al. (1996) proposed the

Chapter 7 Cultureand Colonization generalization that polyphagy and high dispersal rate are the main characteristics of effective natural enemies of naturally occurring mobile pests. Numbers and Generation Time

It is preferable to release as many entomophages at a site as possible. Beirne (1975) declared that biological control projects in Canada were much more successful with releases of > 800 individuals per liberation. Similarly, Hopper and Roush (1993), after analyzing previous introductions and using a mathematical model, suggested that a threshold of about 1000 insects per release would provide the best prospect for establishment of introduced parasitoids. Hopper et al. (1993) noted that the relationship of successful establishment of introduced biological control agents with the numbers released and the types of release habitats could be explained by a consideration of the Allee effect. Namely, the degree of dispersal of introduced species depends on the type of habitat into which they are released. With habitats that are less delimited, larger numbers of a species must generally be released to prevent population extinction by failure of the dispersing males and females to find each other (Allee effect). However, large numbers of some entomophages are difficult to obtain, which typically makes establishment much more troublesome. Laricobius erichsonii (Rosenhauer), a derodontid predator of the balsam woolly adelgid, Adelges piceae (Ratzeburg), not only has a single generation a year but also has a very slow annual dispersal rate. Considerably more effort was therefore necessary for its establishment than for that of other species (Clausen, 1977). Some entomophages released in small numbers have become rapidly established. Such rapid establishment occurred with the encyrtid parasitoids Metaphycus stanleyi (Compere), M. helvolus (Compere), and M. lounsburyi (Howard), and with the pteromalid Scutellista cyanea Motschulsky, all released against the black scale in southern California. However, large releases of the encyrtid Diversinervus elegans Silvestri were necessary to achieve recoveries, but rapid spread then followed (Clausen, 1977). Establishment of the braconid Apanteles pedias Nixon on the spotted tentiform leaf miner, Phyllonorycter blancardella (Fabricius), occurred in Ontario following release of only two females in May of 1978. For parasitization, Laing and Heraty (1981) had placed the females in a fine mesh sleeve cage over susceptible hosts on apple branches. By autumn of 1979, they found 25.7% parasitization at the original site, and recovered the parasitoid at a distance of 43 km. High rates of reproduction and dispersal were two factors that enabled establishment from such a small release. Nealis and Quednau (1996) were only able to release

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between 200 and 600 gravid female adults of the European tachinid fly, Ceranthia samarensis, an endoparasitoid of the gypsy moth, in each of 5 years in southeastern Ontario. In two of the years they did free releases of the adults, with trees in the immediate vicinity of the releases seeded with susceptible age classes of gypsy moth larvae. In the other 3 years, they released into large cages enclosing entire oak trees onto which young gypsy moth larvae had been released. Both release techniques were successful, with parasitism by field-released females observed in every year. Drea and Hendrickson (1986) attributed successful control of the alfalfa blotch leaf miner in the northeastern United States partly to a colonization procedure that emphasized timing, environmental conditions, and parasitoid numbers. Proper scheduling of diapause termination in groups of parasitized puparia enabled timing of periodic releases throughout the growing season. The release of parasitoids in an area of sequential alfalfa harvesting ensured the continual presence of susceptible hosts. As Drea and Hendrickson (1986) noted, use of the term "adequate numbers" concerning parasitoid releases is vague. With the alfalfa blotch leaf miner, releases of very small numbers of the two parasitoid species that became the most important resulted in successful control. During 1977 and 1978, liberations in the original release fields totaled only 3307 Chrysocharis punctifacies Delucchi and 5207 Dacnusa dryas. Drea and Hendrickson (1986) used a "dribble release" technique whereby they liberated only a few dozen parasitoids weekly. They felt that repeated releases were more important than the liberation of large numbers at any one time. Others have also achieved successful establishment with releases of small numbers of parasitoids. Fabre and Rabasse (1987) obtained establishment of the aphidiid Pauesia cedrobii by inserting 225 adults per sleeve cage placed on cedar branches with colonies of the cedar aphid Cedrobium laportei. In combating the arrowhead scale, Unaspis yanonensis Kuwana, Furuhashi and Nishino (1983) twice released 100 adults of the aphelinid Aphytis yanonensis DeBach & Rosen on each of three trees in citrus groves. Parasitism reached 80% and there was a marked decline of the scale within 6 months. Seasonal characteristics can affect the necessary numbers of released parasitoids required for establishment. Campbell (1976) reported that successful establishment of the California red scale parasitoid A. melinus in the Riverland district of South Australia in summer and early autumn required colonizing 100 adult wasps into every third tree in every third row of a citrus orchard, but in late autumn establishment required the release of 1000 adults per tree. Widespread establishment of the same parasitoid in the Sunraysia district of New South Wales followed either about 50 small releases, each consisting of 100 to 300

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parasitoids per tree, or placement of pumpkins covered with parasitized hosts in citrus trees. Seasonal characteristics were also important for maintaining numbers of field-released Cotesia melanoscela. Wieber et al. (1995) reported that November/December field placements of C. melanoscela cocoons were most effective, with 74 to 92% emergence of adults during peak periods of susceptible stages of the host, the gypsy moth. Spring-placed cocoons were far more susceptible to natural enemies, and did not have the proper environmental diapause cues for synchrony of adult emergence with host stage susceptibility. On the other hand, Nealis and Bourchier (1995) offered the opposite view. In southern Ontario, they compared the vulnerability to predation and to hyperparasitism of an introduced European strain of C. melanoscela and an Asian strain of the parasitoid with no diapause stage. The nondiapause characteristic of the Asian strain decreased its exposure time and therefore reduced its vulnerability to predation and to hyperparasitism. They concluded that inundative release programs involving Cotesia spp. would be more effective by using a nondiapause strain and by making releases as early as possible in the season to minimize exposure to hyperparasitoids. Fielding et al. (1991) studied the impact of release numbers of the predatory rhizophagid beetle Rhizophagus grandis Gyllenhal, the most important specific entomophage of the great European spruce bark beetle Dendroctonus micans (Kugelann). They concluded that colonization levels by the predator 4 weeks after release at > 1000 predators per hectare were equal to those resulting from low-density introductions (50 to 100 predators per hectare) 2 years after release. Evans and Fielding (1994) later indicated that populations of D. micans were at low levels, with strong evidence that R. grandis was well established, spreading, and an important factor in regulating the bark beetle populations. In comparison with the low-density R. grandis releases, Kinawy (1991) used total releases of only 683 adults of the coccinellid Chilocorus nigritus to successfully control the coconut scale insect Aspidiotus destructor Sign over the Dhofar plain in southern Oman in only 24 months after the last release. Augmentative inoculative releases of small numbers of parasitoids or predators can also be successful. Releases of the phytoseiid mite Metaseiulus occidentalis at the rate of only 64 per tree early in the season resulted in effective control of the McDaniel spider mite Tetranychus mcdanieli McGregor in California (Croft & McMurtry, 1972; McMurtry et al., 1984). However, releases of nine phytoseiid species at 1200 mites per tree over 4 weeks to control the avocado brown mite, Oligonychus punicae (Hirst), were unsuccessful (McMurtry et al., 1984). Pickett and Gilstrap (1986) controlled the Banks grass mite, O. pratensis (Banks), and the two-spotted spider mite on corn in Texas by making early season inoculative releases of the phyto-

seiid mites Phytoseiulus persimilis and Amblyseius californicus (McGregor). They noted, though, that a reduced cost of production and application of the predaceous mites would be necessary to make the procedure commercially feasible. Grafton-Cardwell et al. (1997) evaluated the effectiveness of six species of phytoseiid mites released at the rate of one per leaf on young potted citrus trees to control T. urticae and Panonychus citri in single- and mixed-species infestations. Infestations averaging 10 T. urticae per leaf were >85% controlled within a week, but infestations averaging 22 P. citri per leaf required 3 weeks for 74 to 80% control. The four more specialist phytoseiids--Phytoseiulus longipes Evans, Galendromus occidentalis (Nesbitt), G. helveolus (Chant), and Neosieulus californicus (McGregor) - - were all effective predators. Of the two generalist phytoseiids, Euseius stipulatus Congdon and Amblyseius limonicus Garman & McGregor, A. limonicus Garman & McGregor was not effective in controlling P. cirri at any time during the 6-week sampling period. Galendromus occidentalis was the most effective species in controlling both pest species in a mixed infestation. In a greenhouse environment, Rasmy and Ellaithy (1988) effectively controlled the two-spotted spider mite on cucumbers by releasing 10 predatory P. persimilis mites per plant at the first sign of spider mite damage. However, large release numbers are essential for most entomophages used in augmentative biological control programs. While field testing the effectiveness of mass-produced Trichogramma strains, Hassan et al. (1988) released 400 to 9000 parasitoids per apple tree in four to six treatments to control the codling moth and the summer fruit tortrix, Adoxophyes orana. When Johnson (1985) used T. pretiosum against Heliothis spp. on cotton, he was unable to increase field parasitism by three low-level releases, two at 12,500 per hectare, followed by one at 37,500 per hectare made at 7-day intervals. Daane et al. (1996) had mixed results when they inundatively released the common green lacewing to suppress two vineyard pests, Erythroneura variabilis Beamer and E. elegantula, and they had to release at least 20,000 larvae per hectare to achieve any significant pest reductions. Morales-Ramos et al. (1995) made inundative releases of the boll weevil parasitoid Catolaccus grandis over 2 years, and successfully reduced boll weevil survival (from egg to adult) to only 0.5 to 11.8%, in comparison to a survival of 72.8 to 78.2% in the control cotton fields. They used four methods of calculating the effectiveness of the parasitoid: percentage of parasitism, graphic Southwood and Jepson method, densities of emergence holes, and life table analysis. They later developed an age structured computer simulation model (ARCASIM) to understand the complexities of the interactions between cotton fruiting and population dynamics of the boll weevil and C. grandis (Morales-Ramos et al., 1996b). Based on the simulations,

Chapter 7

Culture and Colonization

the best strategy for augmentative releases of C. grandis against the boll weevil was to release the parasitoid at weekly intervals, instead of using a single release at an optimal time. The simulations revealed that success of the augmentative releases depended on the numbers of adult boll weevils immigrating into the release area, and also showed that cultivation practices can effectively disrupt the effect of the augmentative releases (Morales-Ramos et al., 1996b). Branquart et al. (1996) used a "Bombosh" model to determine the number of coccinellid larvae to field release for the control of potato aphids. The lower rate of increase of predators requires their introduction in large numbers early in the development of aphid populations. The parameters of this model were estimated by laboratory experiments on the observed rate of increase in aphid numbers and on the predatory efficiency of ladybird larvae. Meadow et al. (1985) noted that augmentative releases of the predaceous cecidomyiid Aphidoletes aphidimyza had only been done on a large scale in greenhouses in Finland and in the former USSR. They experimented with using it to control the green peach aphid. In small plots of tomatoes and peppers in greenhouses and the field, they achieved effective control at varying rates, for example, two to three midge pupae per plant, with two sequential releases. A later monograph on this predator by Kulp et al. (1989) presented information on rearing methods and applications. Stenseth and Aase (1983) investigated the numbers of Encarsia formosa required to control the greenhouse whitefly on cucumbers in Norwegian greenhouses. Three introductions of five parasitoids per plant at fortnightly intervals resulted in adequate control when there was an initial number of 10 to 30 adult whiteflies per 100 plants, whereas at lesser host densities only three parasitoids per plant were necessary. They noted that parasitoid introduction before the first of March in Norwegian greenhouses was not successful, probably because of the deleterious effect of lowlight intensity on parasitoid reproduction. Van de Veire and Vacante (1984) released the same parasitoid on greenhouse tomatoes by hanging 40 paper disks, each with ca. 110 parasitized whitefly pupae, at intervals over an area of 1500 m 2. This suggested rate was according to the recommendation of Woets (1978) for greenhouse whitefly control (also see Woets, 1973; and Woets & Van Lenteren, 1976). Rumei (1991) used an improved plant-pest-parasitoid (PPP) model to evaluate different methods (the Dutch method, the "pest in first" method and the "banker plant system" method) of releasing E. formosa. Subsequently, Van Roermund et al. (1997) developed a simulation model that could be used to evaluate a number of release strategies for E. formosa on the greenhouse whitefly on several crops and under various greenhouse climate conditions. The model was based on biological characteristics of both insect species, which re-

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lated to development and to the searching and parasitization behavior of E. formosa in relationship to host-plant characteristics and greenhouse climate. Hoddle et al. (1997) used the Beltsville strain of E. formosa to control the silverleaf whitefly, Bemisia argentifolii, on greenhouse-grown poinsettias. At a high release rate of three parasitoids per plant per week over 14 weeks, egg to adult survivorship for B. argentifolii was 1% and parasitism was 12%, versus the control, which had egg to adult survivorship of 71%. The net reproductive rate (Ro) for the control population of B. argentifolii was 17.1, indicating a rapidly increasing population. The net reproductive rate for the whitefly population subject to the high release rate was 0.32, indicating declining B. argentifolii population growth, which was attributed to high levels of in-house wasp reproduction. At harvest, the number of whiteflies per leaf at the high release rate was not significantly different from that found on commercially sold plants. Del Bene (1990) successfully controlled three leaf miner species infesting chrysanthemum and gerbera plants in commercial greenhouses by releasing the eulophid ectoparasitoid Diglyphus isaea (Walker) at the rate of 5 to 30 adults per 10 m 2. However, because of a zero tolerance for mines on chrysanthemum, the parasitoid could only be used for the first weeks of plant development, after which time the early formed lower leaves with mines were removed at flower harvest. Rutz and Axtell (1981) reported that weekly releases of a native strain of Muscidifurax raptor caused a significant reduction in the housefly population at a poultry farm. They released 5 parasitoids per bird per week (150,000 parasitoids per week) by placing parasitized housefly pupae at 10 to 15 spots on the manure in each poultry house. Petersen et al. (1992) developed a program to field-rear a similar parasitoid, M. zaraptor, to control houseflies in beef cattle pens. They exposed about 50,000 freeze-killed housefly pupae to a single field release of M. zaraptor. Subsequently, at 2-week intervals, an additional six lots of 50,000 freezekilled pupae were set out for the parasitoids to attack. The result was a mean parasitoid emergence of 56.4% over the study period. Kfir (1981) warned about published entomophage release figures. He stressed that citing the total number of Trichogramma released per unit of crop is meaningless without specifying the sex ratio and quality. An important principle in entomophage releases, particularly for inoculative releases of a classical biological control agent, is that quality should take precedence over quantity (Neuenschwander, 1989). An example of quality problems was given by Andress and Campbell (1994) who reported that commercially purchased fly pupal parasitoids, primarily M. raptor and Spalangia nigroaenea, were ineffective against stable flies despite weekly releases of high numbers. Parasitoid shipments contained neither the number requested nor the

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expected quality and species purity. Likewise, Lawson et al. (1997) found that variation in performance of Trichogramma spp. from different insectaries and among shipments from the same insectary was common, as did Vasquez et al. (1997), who noted inconsistent responses between shipments of commercially available trichogrammatid products, indicating potential problems with quality control. Obrycki et al. (1997) also focused on quality control in their consideration that periodic augmentative releases of natural enemies may be the biological control method of choice for annually disturbed habitats. However, they also emphasized the importance of choosing appropriate natural enemies to match the characteristics of annual cropping systems; of enhancing the effectiveness of released individuals; and of studying biological, biosystematic, ecological, and economic aspects associated with the releases. Biotic Interactions

Release methods have been developed to enhance the interaction between a pathogen, parasitoid, or predator, and the organism it attacks. In classical biological control, it is advantageous to release a beneficial organism when the susceptible stage of its host occurs in greatest numbers. For example, Nechols and Kikuchi (1985) recommended releasing the encyrtid Anagyrus indicus when the third nymphal stage of its host, Nipaecoccus vastator (Maskell), is the most numerous, to provide the longest exposure period for the most suitable host stages. For timing inundative releases (196,000 parasitoids per hectare) of T. brassicae to control the European corn borer on sweet corn, Yu and Byers (1994) found that using pheromone traps resulted in the greatest reduction in damage. Because European corn borer phenology varied among fields, general-area degree-day accumulation for postdiapause development could not adequately be used to determine the timing of releases for individual fields (Yu & Byers, 1994). In augmentative biological control efforts, release of host material along with the beneficial organism may be desirable to increase the beneficial population. In a laboratory experiment, Nickle and Hagstrum (1981) successfully increased numbers of the braconid Habrobracon hebetor in a simulated peanut warehouse by releasing the parasitoid together with preparalyzed host individuals of the almond moth. In a greenhouse system, Parr (1972) placed spider mites on cucurbits to allow the predator Phytoseiulus persimilis to increase its population in time to control the increase of the endemic spider mite population. For the control of filth flies in dairies, Petersen (1986) made earlyseason releases of nonparasitized freeze-killed housefly pupae, as well as of housefly pupae parasitized with the pteromalid M. zaraptor. The freeze-killed pupae, which remained suitable as hosts for 4 weeks in the spring, appar-

ently provided substrate for sufficient parasitoid population increase to effectively control houseflies and stable flies in the dairies. As another example of this technique, releases of a field-crop insect, the imported cabbageworm, together with two parasitoids early in the growing season, successfully reduced pest damage (Parker & Pinnell, 1972). A corollary technique in weed biological control projects is to fertilize the target weed to provide a better substrate for establishment of a biological control agent. Kuniata (1994) applied nitrogen fertilizer to the weed Mimosa invisa, a serious pest in rangeland, plantations, subsistence gardens, and nonproductive areas in Papua New Guinea, thereby significantly increasing numbers of a psyllid, Heteropsylla spinulosa Muddiman, Hodkinson & Hollis, an imported biological control agent. Perring et al. (1988) discussed a different approach to augment natural biological control of the potato aphid, Macrosiphum euphorbiae (Thomas). In one season when tomatoes were planted earlier than normal, a population of green peach aphids developed that supported parasitoids. The presence of the early season parasitoid populations provided high levels of potato aphid parasitism when that pest later migrated to the tomatoes. Cloutier and Johnson (1993) suggested that manipulation of the polyphagous phytoseiid Amblyseius cucumeris was important to promote development and survival of its protonymphs on the western flower thrips, Frankliniella occidentalis. The phytoseiid protonymphs are small relative to the thrips, and have difficulty attacking living thrips when they are the only available prey. Therefore, providing adult phytoseiids ensures the presence of dead thrips upon which the protonymphs can feed until they become independent predators. Other biotic interactions that a released beneficial organism must face are not desirable. These include competition, disease, parasitism, and predation. For example, competition with native parasitoids may complicate field colonization of exotic parasitoids, as could have been the case with parasitoid releases against the beet leafhopper, Circulifer tenellus (Baker), in the Imperial Valley of California (Clausen, 1977). Competition between introduced parasitoids may also interfere with field colonization or effectiveness. Krause et al. (1990) assayed multiparasitism effects of two gypsy moth parasitoids, Cotesia melanoscela and Glyptapanteles flavicoxis Marsh, a recent import. Because of competitive interactions, they concluded that G. flavicoxis should be field released only after the oviposition period of the first generation of C. melanoscela. Furthermore, McMurtry et al. (1984) suggested that competition with, or interference by, the native predator Euseius hibisci may have limited the abundance of nine species of phytoseiids augmentatively released at the rate of 1200 mites per tree to control the avocado brown mite, because the releases neither affected the average densities

Chapter 7

Culture and Colonization

of the brown mite nor those of the total phytoseiids. However, in an orchard with few phytoseiids, Penman and Chapman (1980) were able to control the European red mite, Panonychus ulmi (Koch), with releases of the phytoseiid Amblyseius fallacis (Garman) at 300 per tree. Heinz and Nelson (1996) investigated the interspecific relationships of two parasitoids, Encarsia formosa and E. pergandiella, and a coccinellid predator, Delphastus pusillus (LeConte), which were tested in all possible combinations for the inundative control of the silverleaf whitefly in greenhouse cage tests. While all combinations provided significant whitefly control, combinations of the predator with one or both of the parasitoids provided the greatest levels of suppression. The results suggested that the types of interspecific interactions, instead of the numbers, among natural enemies may be important to the outcome of inundative biological control programs (Heinz & Nelson, 1996). Other interactions such as predation and cannibalism can also pose problems. Dreistadt et al. (1986) reported that the efficacy of inundatively releasing eggs of the common green lacewing to suppress the tulip tree aphid, M. liriodendri (Monell), was prevented by predation, cannibalism, highly erratic viability of the commercially produced green lacewing eggs, and lacewing larval entrapment on the sticky release tapes used. Effects of host plants on natural enemies constitute another factor in the success of a project. Duso (1992) found that different grape varieties, characterized by glabrous or hairy leaf undersurfaces, caused dramatically different effects on the colonization of the phytoseiid mites Amblyseius aberrans (Oudemans) and Typhlodromus pyri Scheuten. Population densities of the two predators were markedly higher on the varieties with hairy leaf undersurfaces, and were largely independent of prey availability. The critical factors associated with the hairy leaves appeared to be a favorable microclimate, an improved protection from macropredators or from being dislodged, a large availability of shelter and oviposition sites, and an increased capacity for retaining wind pollen (an alternate food source). In a greenhouse environment, Nihoul (1993) showed that high temperature and light intensity resulted in a higher density of glandular trichomes on tomato plants, which trapped a higher percentage of the predatory mite Phytoseiulus persimilis, allowing increased damage by spider mites. Also in greenhouses, Ekbom (1977) noted that control of the greenhouse whitefly with E. formosa was more effective on tomatoes than on cucumbers. Van Lenteren et al. (1995) showed that selection of less-hairy cucumber plants improved biological control of the greenhouse whitefly by E. formosa, with the finding and killing of more hosts per unit of time by the parasitoid. They concluded that plants can be selected that promote the effectiveness of natural enemies. Heinz and Zalom (1996) studied the effect of tomato

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trichomes on a coccinellid, Delphastus pusillus, that attacks the silverleaf whitefly. They compared two tomato varieties, one of which had trichome-based resistance to the whitefly, and three times the number of trichomes as the other. They found that with this system, the plant resistance and the biological control agent did not act additively to suppress the whitefly. The predator had significantly slower walking speeds and reduced lifetime fecundities on the resistant tomato variety; however, this was compensated for by longer residency times, and so there was a neutral effect of the trichome-based resistance on silverleaf whitefly biological control. Additional information on interactions between hostplant resistance and biological control agents can be found in a review by McAuslane (1994). Another effect of host plants is that they can affect entomophages indirectly by controlling the phenology of the host. Schaefer et al. (1983) colonized Pediobiusfoveolatus against the Mexican bean beetle by placing parasitized larval mummies in nurse plots near soybean fields. They had planted the nurse plots with locally adapted bean varieties before normal soybean planting dates to provide reservoirs for early increases in bean beetle and parasitoid populations. Likewise, Correa-Ferreira and Moscardi (1996) planted a trap crop of early maturing soybeans in which they inoculatively released 15,000 per hectare of the egg parasitoid Trissolcus basalis when the first stinkbugs were detected. The inoculative releases resulted in the stinkbug population being held below the economic threshold level during the most critical stage of stinkbug attack on the main crop, which indicated that this technique could be an important component of the soybean integrated pest management (IPM) program in Brazil.

Autoparasitism Autoparasitism can complicate field-release methods. Colonization of autoparasitic aphelinids to control armored scales requires special procedures, such as successive releases of mated and unmated females (Clausen, 1977).

ADDENDUM This chapter has focused on factors involved at three trophic levels for producing arthropods for biological control, and on some aspects of field colonization. Space limitations precluded discussions of facilities or of other types of biological control agents, including microorganisms, invertebrates such as planarians or nematodes, and vertebrates such as fish. Moreover, examples of specific references for entomophage production could not be grouped and discussed by family. In general, Waage et al. (1985) noted that most parasitoids reared for biological control belong to

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the Ichneumonoidea, Chalcidoidea, and Tachinidae, whereas reared predators are primarily found in the Coleoptera, Diptera, Heteroptera, Neuroptera, and Phytoseiidae. A knowledge of biologies is necessary for production of organisms. Good starting references for entomophage biologies are books by Clausen (1940, reprinted 1972), Clausen (1977), DeBach (1964), and Waage and Greathead (1986). A book by Van Driesche and Bellows (1996) also includes information on natural enemy biology, as well as on biological control methods. A review of entomophage mass production, with emphasis on specific systems, was given by Monison and King (1977). Shaffer (1983) listed references that give mean laboratory developmental periods for 113 different insect and mite species at constant temperatures, including those for several predators and parasitoids. Thompson (1986) reviewed nutrition and in vitro culturing of insect parasitoids, and Bratti (1990b) presented a review of in vitro culturing. King and Leppla (1984), Singh and Moore (1985a, 1985b), and Anderson and Leppla (1992) edited useful books on general insect rearing, including information on entomophage production; and Leppla and Ashley (1978) edited a valuable book on insect-rearing facilities. King and Hartley (1992) described a program (for multiple-species insect rearing and the necessary facilities, and Singh and Clare (1992) introduced the concept of insect rearing management (IRM). Edwards et al. (1987) published a reference on arthropod species in culture, primarily in the United States, and Hunter (1997) compiled a list of North American suppliers of beneficial organisms. Concerning field colonization, Ehler (1990) and Roush (1990) presented theoretical considerations of introduction strategies. Hopper (1996) reviewed techniques for making biological control introductions more effective, and Van Driesche (1993) discussed methods for the field colonization of new biological control agents. For documentation of liberations, the Agricultural Research Service Biological Control Documentation Center of the USDA has established a computerized database called "releases of beneficial organisms" (ROBO), and has published annual reports that detail beneficial organism releases in the United States and its territories for the years 1981 to 1983 (Coulson et al., 1988; Coulson, 1992, 1994). ROBO currently contains all importation and release records only for the years 1981 to 1985; these will be published on a CD-ROM, and skeletal importation records will be available on the world wide web for those years (current Internet address: http://www.ars-grin.gov/nigrp/robo.html) (J. R. Coulson, personal communication). Because of the impossibility of entering all historical and current data into the original and now archaic ROBO computer system, personnel in the Biological Control Documentation Center are in the process of developing a revised ROBO with a modem computer system in the Germplasm Resources Information Network (GRIN). Associated with this system will be the

ability of all biological control workers with Internet access to directly enter importation/release data into ROBO, so that eventually the data can be current and usable for all researchers (J. R. Coulson, personal communication). References Abou-Awad, B. A., Reda, A. S., & Elsawi, S. A. (1992). Effects of artificial and natural diets on the development and reproduction of two phytoseiid mites Amblyseius gossipi and Amblyseius swirskii (Acari: Phytoseiidae). Insect Science Applications, 13, 441-445. Abou-Setta, M. M., Fouly, A. H., & Childers, C. C. (1997). Biology of Proprioseiopsis rotendus. (Acari: Phytoseiidae) reared on Tetranychus urticae (Acari: Tetranychidae) or pollen. Florida Entomologist, 80, 27-34. Adiyaman, N., & Aktumsek, A., (1996). The effects of low temperature on fecundity of pupae and adults of female Pimpla turionellae L. (Hymenoptera: Ichneumonidae). Turkish Journal of Zoology, 20, 1-5. Afifi, A. M., Potts, M. F., Patterson, C. G., & Rodriguez J. G., (1988). Pollen diet of some predator mites. Transactions of the Kentucky Academy of Science, 49, 96-100. Agricola, U., Agounke, D., Fischer, H. U., & Moore, D. (1989). The control of Rastrococcus invadens Williams (Hemiptera: Pseudococcidae) in Togo by the introduction of Gyranusoidea tebygi Noyes (Hymenoptera: Encyrtidae). Bulletin of Entomological Research 79, 671678. Allen, H. W., & Brunson, M. H., (1947). Control of Nosema disease of potato tuberworm, a host used in the mass production of Macrocentrus ancylivorus. Science, 105, 394. Amis, A. A., & Snow, J. W. (1985). Conotrachelus nenuphar. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol. 1, pp. 227235). New York: Elsevier. Anderson, T. E., & Leppla, N. C. (Eds.). (1992). Advances in insect rearing for research and pest management. Boulder, CO: Westview Press. Andress, E. R., & Campbell, J. B. (1994). Inundative releases of Pteromalid parasitoids (Hymenoptera: Pteromalidae) for the control of stable flies, Stomoxys calcitrans (L.) (Diptera: Muscidae) at confined cattle installations in west Central Nebraska. Journal of Economic Entomology, 87, 714-722. Ankersmit, G. W. (1985). Adoxophyes orana. In E. G. King & N. C. Leppla (Eds.), Handbook of insect rearing (Vol. 2, pp. 165-175). New York: Elsevier. Argyriou, L. C. (1981). Establishment of the imported parasite ProspalteIIa perniciosi (Hym.: Aphelinidae) on Quadraspidiotus perniciosus (Hom.: Diaspididae) in Greece. Entomophaga, 26, 125-130. Ashby, M. D., Singh, P., & Clare. G. K., (1985). Cydia pomonella. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol. 2, pp. 237-248). New York: Elsevier. Baggen, L. R., & Gurr, G. M. (1995). Lethal effects of foliar pubescence of solanaceous plants on the biological control agent Copidosoma koehleri Blanchard (Hymenoptera: Encyrtidae). Plant Protection Quarterly, 10, 116-118. Bailey, D. L., & Seawright, J. A. (1984). Improved techniques for mass rearing Anopheles albimanus. In E. G. King & N. C. Leppla [Eds.], Advances and challenges in insect rearing (pp. 200-205) Washington, DC: U.S. Government Printing Office. Balas, M. T., Lee, M. H., & Werren, J. H. (1996). Distribution and fitness effects of the son-killer bacterium in Nasonia. Evolutionary Ecology, 10, 593-607. Balasubramanian, S., & Pawar, A. D. (1988). Improved technique for mass rearing of Trichogramma spp. (Hymenoptera: Trichogrammatidae) in the laboratory. Plant Protection Bulletin, India, 40, 12-13.

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Ballal, C. R., & Kumar, P. (1993). Host-parasitoid interaction between Chilo partellus (Swinhoe) and Allorhogas pyralophagus Marsh. Biological Control, 7, 72-74. Ballal, C. R., Singh, S. P., Jalali, S. K., & Kumar, P. (1989). Cold tolerance of cocoons of Allorhogas pyralophagus (Hym.: Braconidae). Entomophaga, 34, 463-468. Barbosa, P., & Segarra-Carmona, A. (1993). Criteria for the selection of pest arthropod species as candidates for biological control. In R. G. Van Driesche & T. S. Bellows, Jr. (Eds.), Proceedings: Steps in classical arthropod biological control (pp. 5-23). Symposium, Baltimore, MD, September 30, 1990, Lanham, MD: Thomas Say Publications in Entomology: Entomological Society of America. Barbosa, P., Saunders, J. A., & Waldvogel, M. (1982, March). Plantmediated variation in herbivore suitability and parasitoid fitness (pp. 63-71). In Proceedings, 5th International Symposium on Insect-Plant Relationships, Wageningen, The Netherlands. Barbosa, P., Kemper, J., Gross, P., & Martinat, P. (1990). Influence of dietary nicotine and colony source of Manduca sexta (Lepidoptera: Sphingidae) on its suitability as a host of Cotesia congregata (Hymenoptera: Braconidae). Entomophaga, 35, 223-232. Barrows, E. M., & Hooker, M. E. (1981). Parasitization of the Mexican bean beetle by Pediobius foveolatus in urban vegetable gardens. Environmental Entomology, 10, 782-786. Bartlett, A. C. (1984). Genetic changes during insect domestication. In E. G. King & N. C. Leppla (Eds.), Advances and challenges in insect rearing (pp. 2-8). Washington, DC: U.S. Government Printing Office. Bartlett, A. C. (1985). Guidelines for genetic diversity in laboratory colony establishment and maintenance. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol. 1, pp. 7-17). New York: Elsevier. Bartlett, A. C., & Wolf, W. W. (1985). Pectinophora gossypiella. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol. 2, pp. 415-430). New York: Elsevier. Battisti, A. P. I., Milani, N., & Zanata, M. (1990). Preliminary accounts on the rearing of Ooencyrtus pityocampae (Mercet) (Hymenoptera, Encyrtidae). Journal of Applied Entomology 110, 121-127. Baumhover, A. H. (1985). Manduca sexta. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol. 2, pp. 387-400). New York: Elsevier. Bay, E. C., & Legner, E. F. (1963). Quality control in the production of Hippelates collusor (Tsnd.) for use in the search and rearing of their natural enemies. Proceedings of the New Jersey Mosquito Exterminating Commission 1963,403-410. Beach, R. M., & Todd, J. W. (1986). Foliage consumption and larval development of parasitized and unparasitized soybean looper, Pseudoplusia includens (Lep.: Noctuidae), reared on a resistant soybean genotype and effects on an associated parasitoid, Copidosoma truncatellum (Hym.: Encyrtidae). Entomophaga, 31,237-242. Beirne, B. P. (1975). Biological control attempts by introductions against pest insects in the field in Canada. Canadian Entomologist, 107, 225236. Bell, R. A. (1996). Manipulation of diapause in the gypsy moth, Lymantria dispar L., by application of KK-42 and precocious chilling of eggs. Journal of Insect Physiology, 42, 557-563. Belloncik, S., Lavallre, C., & Quevillon, I. (1985) Euxoa scandens and Euxoa messoria. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol 2, pp. 293-299). New York: Elsevier. Belousov, Y. V., & Popov, N. A. (1989). Rearing of Aphidoletes aphidimyza (Diptera, Cecidomyiidae) on greenbugs. Acta Entomologica Fennica, 53, 3-5. Bennett, F. D. (1966). Current status of citrus blackfly and introduced parasites in Barbados. Agricultural Society of Trinidad, Tobago Journal, 66, 35-36. Bennett, F. D., & van Wherlin, L. W. (1966). Occurrence of the citrus black fly in Barbados. Agricultural Society of Trinidad, Tobago Journal, 66, 31- 34.

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Bentz, J.-A., & Barbosa, P. (1992). Effects of dietary nicotine and partial starvation of tobacco hornworm, Manduca sexta, on the survival and development of the parasitoid Cotesia congregata. Entomologia Experimentalis et Applicata, 65, 241-245. Berlinger, M. J. (1992). Importance of host plant or diet on the rearing of insects and mites. In T. E. Anderson & N. C. Leppla (Eds.), Advances in insect rearing for research and pest management (pp. 237-251). Boulder, CO: Westview Press. Beukeboom, L. W., & Werren, J. H. (1992). Population genetics of a parasitic chromosome: Experimental analysis of PSR in subdivided populations. Evolution, 46, 1257-1268. Beukeboom, L. W. (1993a). Deletion analysis of the selfish B chromosome, paternal sex ratio (PSR), in the parasitic wasp Nasonia vitripennis. Genetics, 13, 637-648. Beukeboom, L. W. (1993b). Transmission and expression of the parasitic paternal sex ratio psr chromosome. Heredity, 70, 437-443. Bhatt, N., & Singh, R. (1989). Bionomics of an aphidiid parasitoid Trioxys indicus: 30. Effect of host plants on reproductive and developmental factors. Biology of Agricultural Horticulture, 6, 149-158. Bhatt, N., & Singh, R. (1991). Bionomics of an aphidiid parasitoid, Trioxys indicus Subba Rao & Sharma. 35. Influence of food plants on the life table statistics of the parasitoid through its host Aphis gossypii Glover. Insect Science Applications, 12, 385-390. Bichao, M. H., & Araujo, J. (1989). Mass-rearing of Chrysoperla carnea (Stephens) (Neuroptera, Chrysopidae) larvae: Optimization of rearing unit yield. Boletim da Sociedade Portuguesa de Entomologia, 0(113), 117-124. Bigler, F. (1989). Quality assessment and control in entomophagous insects used for biological control. Journal of Applied Entomology, 108, 390-400. Blenk, R. G., Gouger, R. J., Gallo, T. S., Jordan, L. K., & Howell, E. (1985). Agrotis ipsilon. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol 2, pp. 177-187). New York: Elsevier. Bloem, K. A., & Duffey, S. S. (1990). Effect of protein type and quantity on growth and development of larval Heliothis zea and Spodoptera exigua and the endoparasitoid Hyposoter exiguae. Entomologia Experimentalis et Applicata, 24, 141-148. Boiler, E. F. (1985). Rhagoletis cerasi and Ceratitis capitata. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol 2, pp. 135144). New York: Elsevier. Bonde, J. (1989). Biological studies including population growth parameters of the predatory mite Amblyseius barkeri [Acari: Phytoseiidae] at 25~ in the laboratory. Entomophaga, 34, 275-287. Bourchier, R. S. (1991). Growth and development of Compsilura concinnata (Meigan) (Diptera: Tachinidae) parasitizing gypsy moth larvae feeding on tannin diets. Canadian Entomologist, 123, 1047-1056. Bourchier, R. S., & Smith, S. M. (1996). Influence of environmental conditions and parasitoid quality on field performance of Trichogramma minutum. Entomologia Experimentalis et Applicata 80, 461468. Bouse, L. F., Carlton, J. B., & Morrison, R. K. (1981). Aerial application of insect egg parasites. Transactions of the ASAE, 14, 1093-1098. Bouse, L. F., Carlton, J. B., Jones, S. L., Morrison, R. K., & Ables, J. R. (1980). Broadcast aerial release of an egg parasite for lepidopterous insect control. Transactions of the ASAE 23, 1359-1363, 1368. Branquart, E., Hemptinne, J. L., Bruyere, M., Adam, B., & Gaspar, C. (1996). Biological control of potato aphids by ladybird beetles. Mededelingen Faculteit Landbouwkundige en Toegepaste Biologische Wetenschappen Universiteit Gent, 61,905-909. Bratti, A. (1990). In vitro rearing of Pseudogonia rufifrons Wied. (Diptera: Tachinidae) on pupal hemolymph of Galleria mellonella L. and on meridic diets. Bollettino dell'Istituto di Entomologia "Guido Grandi" della Universit~ degli Studi di Bologna, 44, 11-22 (in Italian, with Italian and English summaries). Bratti, A. (1990b). In vitro rearing techniques for entomophagous parasi-

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Culture and Colonization

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Wajnberg, E., Pr6vost, G., & Boul6treau, M. (1985). Genetic and epigenetic variation in Drosophila larvae suitability to a hymenopterous endoparasitoid. Entomophaga, 30, 187-191. Wang, B., Ferro, D. N., & Hosmer, D. W. (1997). Importance of plant size, distribution of egg masses, and weather conditions on egg parasitism of the European corn borer, Ostrinia nubilalis by Trichogramma ostriniae in sweet corn. Entomologia Experimentalis et Applicata, 83, 337-345. Wang, C. L., Wand, H. X., Lu, H., Gui, C. M., Jin, Z. T., Cheng, G. M. (1988). Studies on technique of long term keeping host eggs of Trichogramma under ultralow temperature. Colloques de I'INRA, 43, 399401. Werren, J. H. (1997). Biology of Wolbachia. Annual Review of Entomology, 42, 587-609. Werren, J. H., & Beukeboom, L. W. (1993). Population genetics of a parasitic chromosome: Theoretical analysis of PSR in subdivided populations. American Naturalist, 142, 224- 241. Werren, J. H., Zhang, W., & Guo, L. R. (1995). Evolution and phylogeny of Wolbachia: Reproductive parasites of arthropods. Proceedings of the Royal Society of London, Series B, 261, 55-63. Werren, J. H., Hurst, G. D. D., Zhang, W., Breeuwer, J. A. J., Stouthamer, R., & Majerus, M. E. N. (1994). Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). Journal of Bacteriology, 176, 388-394. Weseloh, R. M. (1996). Rearing the cannibalistic larvae of Calosoma sycophanta (Coleoptera: Carabidae) in groups. Journal of Entomological Science, 31, 33-38. Wheeler, R. E. (1984). Industrial insect production for insecticide screening. In E. G. King & N. C. Leppla (Eds.), Advances and challenges in insect rearing (pp. 240-247). Washington, DC: U.S. Government Printing Office. Whistlecraft, J. W., Tolman, J. H., & Harris, C. R. (1985a). Delia platura. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol. 2, pp. 59-65) New York: Elsevier. Whistlecraft, J. W., Tolman, J. H., & Harris, C. R. (1985b). Delia radicum. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol. 2, pp 67-73). New York: Elsevier. Wieber, A. M., Webb, R. E., Ridgway, R. L., Thorpe, K. W., Reardon, R. C., & Kolodny-Hirsch, D. M. (1995). Effect of seasonal placement of Cotesia melanoscela (Hym.: Braconidae) on its potential for effective augmentative release against Lymantria dispar (Lep.: Lymantriidae). Entomophaga, 40, 281- 292. Wight, D. P., Jr. (1985). Spodoptera eridania. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol. 2, pp.459-464). New York: Elsevier. Willey, R. B. (1985). Arphia conspera. In P. Singh & R. F. Moore (Eds.), Handbook of insect rearing (Vol. 1, pp. 435-450). New York: Elsevier. Wissinger, S. A. (1997). Cyclic colonization in predictably ephemeral habitats: A template for biological control in annual crop systems. Biological Control 10, 4-15. Woets, J. (1973). Integrated control in vegetables under glass in the Netherlands. Bulletin O.I.L.B./S.R.O.P., 1973/4, 26-31. Woets, J. (1978). Development of an introduction scheme for Encarsia formosa Gahan (Hymenoptera: Aphelinidae) in greenhouse tomatoes to control the greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae). Medelingen Faculteit Landbouwkundige, Rijksuniversiteit Gent, 43, 379-385. Woets, J., & Van Lenteren, J. C. (1976). The parasite-host relationship between Encarsia formosa (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Homoptera: Aleyrodidae). Bulletin O.I.L.B./ S.R.O.P., 1976/4, 151-164. Wong, T. T. Y., & Ramadan, M. M. (1992). Mass rearing biology of larval parasitoids (Hymenoptera, Braconidae, Opiinae) of tephritid flies (Diptera, Tephritidae) in Hawaii. In T. E. Anderson & N. C. Leppla

Chapter 7

Culture and Colonization

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]8] Life Table Construction and Analysis for Evaluating Biological Control Agents T. S. BELLOWS

IL G. VAN DRIESCHE

Department of Entomology University of California Riverside, California

Department of Entomology University of Massachusetts Amherst, Massachussetts

INTRODUCTION

numbers of individuals surviving to fixed points in the life cycle, together with their reproductive output at those points. Mortality usually is assigned to specific causes. Such information can be organized by either age or stage, but age of individual insects rarely is known with precision in field populations, whereas developmental stages can usually be determined. Hence this information, for insects and other arthropods, most often is organized by stage, producing stage-specific instead of age-specific life tables. Inspection of such tables allows determination of stage survival rates and comparisons of the degree of mortality contributed by agents acting at differing points in the life cycle or in different populations (Bellows et al., 1992a). Life tables may be constructed in two ways. In the first, data are collected that present the fate of a real group or cohort, typically a generation of individuals, whose numbers and mortalities are determined over the course of time for each of a series of stages; this method has been referred to as a horizontal life table. An alternative approach, more applicable to continuously breeding populations than those breeding in discrete generations, is to examine the age structure of a population at one point in time and to infer from it the mortalities occurring in each stage. Such an approach requires assumptions that the population has reached a stable age distribution, and mortality factors acting on the population are constant. Theoretically, age distribution may be stable if the population is either expanding or declining exponentially or is remaining at an unchanging density. In practical terms, life tables of this type reflect only the type and magnitude of mortality acting in a short time period immediately preceding the sampling date. Consequently, one such life table will present an incomplete picture of the total pattern of mortality across the whole season, which may undergo major changes if specific fac-

Many approaches exist for evaluating the impact of natural enemies in biological systems. One method, presented in this chapter, is the construction and analysis of life tables. Other approaches include manipulative experiments (Chapter 9). A thorough examination of a particular system may require more than one approach to fully address questions concerning interactions among the species. The topics covered in this chapter apply to natural enemies of all types, but much of the detail is presented with reference to insect parasitoids. The chapter is divided into five subsequent sections. We first review the types of life tables and data necessary for their construction. We next address measuring the quantitative impact of natural enemies on their target populations m these are the questions of "how much" mortality is caused by natural enemies. Next we consider how life tables may be employed to assess the ecological role of natural enemies m the questions of "what type" of impact is the natural enemy having on the dynamics of the system (e.g., stabilizing, destabilizing, neutral). We then suggest a general framework for the experimental use of life tables in the study of host-naturalenemy systems. We finish with a discussion on how the topics developed in this chapter should be applied to pathogens, predators, and beneficial herbivores.

DEFINITIONS AND DATA COLLECTION T y p e s of Life Tables Life tables, first applied to the study of animal populations by Deevey (1947), are organized presentations of Handbookof BiologicalControl

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tors act more strongly at some times than they do at others. Life tables developed in this manner are referred to as vertical life tables. Southwood (1978) provides a description of the terminology and conventional organization of both types of life tables. Both types of construction have application in the evaluation of natural enemies in insect life tables. Horizontal construction is most typical for insects breeding in discrete generations, and their construction and analysis is essentially a direct representation of the cohort for which the life table is constructed. Both horizontal and vertical construction are applicable for continuously breeding populations, but their relationships to the populations studied differ from one another. A horizontal life table may be constructed for a cohort defined somewhat arbitrarily by the researcher, and analyses then apply to that cohort. A horizontal life table cannot be constructed for the population as a whole, because the identity of the individuals studied relative to any particular generation is, by definition, not known. Multiple horizontal life tables, studied throughout a season, give a fuller picture of the dynamics of continuously breeding populations. Vertical life tables may be employed for continuously breeding populations in a similar way, recognizing that analysis of data collected in vertical life tables requires some specific assumptions when applying the results to the population as a whole. The goal of constructing life tables for evaluating the impact of natural enemies is to obtain quantitative estimates of the mortality caused by each natural enemy. These estimates are typically measured as rates, the per capita number of individuals dying from a particular cause. Caution must be employed to distinguish between sequentially acting and contemporaneously acting factors. When data are collected, the sampling program also must permit factors that act contemporaneously to be distinguished from one another. Subsequently, suitable analytical procedures may be employed to correctly calculate the mortality caused by each factor. These matters are discussed more fully later. T y p e s of Data U s e d in Life Table C o n s t r u c t i o n The initial construction of a life table requires estimates of numbers entering successive stages in a life history. These may be obtained in two fundamentally different ways. The first of these methods is to measure the density of each stage several times during the generation or study, providing stage-frequency data. These data may then be analyzed by a variety of techniques to provide estimates of numbers entering successive stages (see Southwood, 1978; and McDonald et al., 1989 for reviews). These data do not, however, provide information on the causes of death in the separate stages. Assignment of causes of death must come from additional information collected during the study, such as dissections to determine parasitism or disease incidence, or by exclusion experiments as discussed later. An important alternative method for obtaining estimates

of the numbers entering successive stages is to measure the recruitment to each stage of interest (Van Driesche & Bellows, 1988; Bellows et al., 1989a; Van Driesche et al., 1991). This approach provides direct assessment of the processes that contribute to stage densities (Fig. 1), and thus permits immediate construction of the life table without recourse to stage-frequency analysis. The recruitment approach is particularly important because very few methods of stage-frequency analysis for two-species coupled systems (e.g., host-parasitoid systems, Bellows et al., 1989a, 1989b) have been developed. The objective of life table construction usually is to assess the mortality rate assignable to a particular agent. The way in which the data are collected concerning the action of natural enemies can affect the accuracy of the estimates. Losses from parasitism must be assessed at the time of attack, in the host life stage in which the attack occurs. Attempts to score parasitism in a subsequent stage that is not the stage attacked but is the stage from which the parasitoid emerges will lead to incorrect estimates because losses may be obscured by subsequent mortality from other factors. Additionally, scoring parasitism at emergence may be further flawed if mortality levels are incorrectly associated with the host density of the more mature stage, rather than with the density of the earlier stage that was actually attacked. Mortality rates can, in some circumstances, be estimated in the absence of stage density information without the formal construction of a life table. Gould et al. (1990) and Elkinton et al. (1990) have described an approach where groups of individuals are collected at frequent intervals (but without density information); these individuals are then held at field conditions, and their death rates during specific intervals are recorded. The cause of death of each individual dying during the interval is noted, and by a mathematical process the original mortality rates assignable to each cause are calculated. The process is repeated for samples collected throughout the season, and the interval-specific mortality rates may then be used to calculate the total mortality assignable to each cause during the study. When density information also is available, this approach is applicable to most mortality factors. In cases where density information is not available, the method is applicable to many, but not all, factors (Elkinton et al., 1990, 1992). This approach requires that recruitment to the host population be zero once mortality sampling has begun; if host recruitment is an ongoing process, then the analysis cannot correctly quantify mortality rates. Finally, some mortality due to natural enemies (e.g., host feeding) is not readily quantifiable using the approaches discussed earlier. For these factors, experimental methods may be employed to estimate mortality rates. This is usually accomplished by measuring (either in the laboratory or in the field) the frequency of occurrence of these factors (such as host feeding) relative to some other, more readily quan-

Chapter 8

Life Table Construction and Analysis

(a) Single-Species System

RECRUITMENT

MOLTING

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(b) Joint Host-Parasitoid System

RECRUITMENT h _ _ ~

MOLTING

v

MORTALITY

MORTALITY

PARASITISM I~ MOLTING v

MORTALITY

FIGURE 1 Processes affecting the number of individuals in a particular stage of a population at any particular instant in time. (a) In a single species system, the principal processes are recuitment to the population, molting to the next stage, and losses from mortality. (b) In a coupled host-parasitoid system, additional processes affect the numbers present: parasitism contributes losses to the host but recruitment to the parasitoid poulation, and both molting and mortality affect the parasitoid population.

tifiable, event such as parasitism. Once this relative frequency is known, extrapolation from the frequency of the observed event (e.g., parasitism) to the frequency of the unobserved event is possible (Van Driesche et al., 1987). A p p l i c a t i o n s to Biological Control

causes might be specific natural enemies (the most explicit and generally desirable case), or general action of groups of natural enemies (e.g., "parasitism", cf. Carey, 1989, 1993). Several approaches to obtaining these estimates are available.

Systems

When life tables are constructed to assess the magnitude or role of mortality from natural enemies, three issues require careful attention: (1) accurate determination of total numbers entering successive stages and those dying from natural enemies a n d from all other sources of mortality; (2) assessment of all additional natural-enemy-caused mortality other than parasitism or predation per se, as, for example, host feeding by adult parasitoids; and (3) correct focusing of the sampling regimen in relation to the spatial and temporal scale of host distribution and natural-enemy attack. D e t e r m i n i n g Total N u m b e r s Entering S t a g e s Life table construction requires that estimates be obtained for numbers entering successive stages. More detail is required, however, to provide an evaluation for specific natural enemies. Estimates must be obtained for the numbers dying due to specific causes in each stage. These

Stage-Frequency Analysis Traditionally, methods for quantifying numbers entering a stage have made use of stage-frequency data, and a variety of techniques have been developed for treating such data to extract estimates of numbers entering stages [see Southwood (1978) and McDonald et al. (1989) for reviews]. These methods are not immediately applicable for use in quantifying processes in joint host-parasitoid or other natural-enemy systems (Bellows et al., 1989a, 1989b) but must be modified to permit analysis of multispecies systems. An exception to this case is where the natural histories of the species under study cause all members of the generation to be present in a single stage at a single moment of time (e.g., due to diapause at the end of the stage), and in these cases a single sample at that time may be an accurate estimate of total losses to parasitism provided significant losses have not occurred due to mortality from other fac-

2.02.

T.S. Bellows and R. G. Van Driesche

tors. However, the more usual case is for recruitment, molting, and mortality to overlap broadly. In such cases no single sample provides an accurate estimate of total generational losses to parasitism (Simmonds, 1948, Miller, 1954; Van Driesche, 1983; Van Driesche et al., 1991). Several approaches have attempted to rectify the biases inherent in sample percentage of parasitism; and recommendations have included scoring parasitism after parasitoid oviposition in the host population is complete (Miller, 1954), using mathematical formulae for adding up successive levels of parasitism (Smith, 1964), and estimating parasitism from pooled samples of larvae in instars too old for parasitoid attack and too young for parasitoid emergence (Hill, 1988). None of these approaches provides an accurate estimate for the numbers dying due to a specific natural enemy for populations where recruitment, molting, and mortality overlap (Van Dfiesche, 1983). However, methods developed for determining numbers entering a stage of one species (see Southwood, 1978; McDonald et al., 1989 for reviews) may be adapted to the problem of estimating total entries simultaneously for two species, the host and the parasitoid (Bellows et al., 1989a, 1989b). The graphic technique of Southwood and Jepson (1962), for example, may be used with certain modifications. Because the accuracy of this technique is strongly affected by mortality and because parasitism is a significant source of mortality, the application of the technique is limited. Bellows et al. (1989b) develop seven variants of the method applicable to different life histories and sampling requirements. The method appears to be suitable primarily for cases where independent estimates of host recruitment are available or where total mortality in the system is less than 20%, although specific cases discussed by Bellows et al. (1989b) permit its application in other situations. A modification of Richards and Waloff's (1954) second method may be used to estimate mortality for a stage where parasitism is the sole source of mortality (Van Driesche et al., 1989). Further work in extending single-species analytical techniques to the case of two interacting species will probably add to the methods available for analyzing systems in this manner. These modifications appear to be applicable to both discretely breeding and continuously breeding populations.

Recruitment One important alternative to the stage-frequency approach is to directly measure the numbers recruited into each stage (Birley, 1977; Van Driesche & Bellows, 1988; Van Driesche, 1988a, 1988b; Lopez & Van Driesche, 1989). If this approach is taken, total numbers entering the stage are found by adding together recruitment for all time periods during the study or generation. Total numbers dying in each stage from parasitism also must be estimated in some manner. For parasitism this may be achieved by direct

measurement of recruited individuals into the "parasitized host" category (Van Driesche & Bellows, 1988; Van Driesche, 1988a, 1988b, Lopez & Van Driesche, 1989). Total parasitoid recruitment divided by total host recruitment then gives the proportion of hosts in the generation killed by the parasitoid. When applied to systems with discrete generations, this approach provides estimates of mortality per generation. When applied to systems with overlapping generations, this approach provides estimates of total mortality during the course of the study. If recruitment cannot be directly measured for the stages of interest, it may be estimated from data on recruitment to a previous stage together with density estimates for the stage of interest (e.g., Bellows & Birley, 1981; Bellows et al., 1982). A review of techniques for estimating recruitment in host-parasitoid systems is presented by Van Driesche et al. (1991).

Population Growth Rates When constructing life tables for continuously breeding populations, methods additional to those discussed earlier may be applied. These have as a unifying theme the use of population growth rates as predictors of population increase between samples, with the difference between observed and expected population sizes being an estimate of the numbers dying between sampling times. These methods differ in the approach used for calculating growth rates. The approach was first developed by Hughes (1962, 1963) who proposed its use for such continuously breeding insect species as the cabbage aphid, Brevicoryne brassicae (Linnaeus). Hughes estimated the growth rate from the age-class distribution of a population in the field. An assumption of the method is that a stable age distribution, required for the estimation of the growth rate parameter Rm, has been attained when the population is studied. Carter et al. (1978) criticized the validity of this assumption and stated that instar distribution in the field should not be used to calculate R m. Hutchinson and Hogg (1984, 1985) used caged cohorts of the pea aphid, Acyrthosiphon p i s u m (Harris), to determine survival and fertility schedules and from these estimated the population growth rate R m. This modified approach employs the assumption that small deviations from the stable age distribution would have little effect on the population growth rate. The difference between observed densities and those projected from the estimated population growth rates represent the aggregate effects of all causes of reduced reproduction, including mortality and reduced fertility of diseased or parasitized individuals. Quantifying the effects of separate factors requires additional information on the individual sources of mortality (Hutchinson & Hogg, 1985). Poswal et al. (1990) similarly constructed vertical life tables for the aphid Acyrthosiphon kondoi Shinji. An alternative approach that avoids the general limita-

Chapter 8

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LifeTable Construction and Analysis

tions of the methods discussed earlier is to measure directly in the field the per capita reproduction (e.g., recruitment) of adult females chosen randomly from the population over a short interval (Lopez & Van Driesche, 1989) and derive population rates of increase from these data. Such estimates of recruitment, together with density estimates of adult females, allow projections of population growth for comparison to actual population levels on subsequent sample dates. This approach has the advantage of not making any assumptions concerning age structure and does not compound the effects of mortality and reduced fertility of parasitized and diseased individuals.

Death Rates One technique exists that permits the quantification of mortality rates (the goal of life table analysis) without first constructing a life table (Gould et al., 1990). The method consists of scoring the death rates of individuals in the population at intervals throughout the study and analyzing the observed rates to provide estimates of the independent, or marginal, mortality rates assignable to each cause (cf. Royama, 1981a). This is accomplished by collecting samples of the stages of interest at frequent intervals and rearing the collected individuals under field conditions. These individuals are reared only until the next sampling date, and during the intervening period the numbers of individuals in the sample dying from specific causes are recorded. The proportions of individuals dying are used to calculate the marginal mortality rates for each cause or each factor using the equations given by Elkinton et al. (1992) [see also Gould et al. (1990)]. The aggregate losses in the population to a specific factor are calculated from the losses in each sampling interval during the study. This method may be applied to a population provided that all hosts have entered the susceptible stage before the first sample (i.e., there is no recruitment to the population during the study). It has the particular advantage that population density data are not required to obtain estimates of mortality rates. The method is capable of providing estimated rates for factors that act contemporaneously. The method does not, however, provide the traditional stagespecific estimates of loss due to a particular factor if a factor can affect more than one developmental stage, because all stages are treated together during the study. The method does provide "interval-specific" loss rates, and calculates aggregate loss rates from these rather than from stage-specific loss rates. The method is applicable to many, but not all, types of natural-enemy and host interactions (see Elkintonet al., 1992).

preferable for most situations (Van Driesche & Bellows, 1988; Lopez & Van Driesche, 1989; Van Driesche et al., 1991). It has the advantages of directly measuring the events of interest (the occurrence of parasitism), avoids compounding sequential and contemporaneous factors, and does not require complicated analytical techniques to construct the life table. It is applicable to both discretely breeding and continuously breeding populations. When recruitment measurement is not possible, stagefrequency analysis provides a potential solution for obtaining estimates of numbers entering stages. A suitable stagefrequency analysis must be selected to extract estimates of numbers entering stages from the stage-frequency data. Although several techniques are available for use with single-species populations, few have been extended to incorporate the special considerations necessary for application to multispecies, host-natural-enemy systems (Bellows et al., 1989a, 1989b; Van Driesche et al., 1989). The two other approaches, growth rate and death rate analysis, do not estimate numbers entering stages but instead estimate numbers or proportions dying. Growth rate analysis may be applied specifically to continuously breeding populations and provides a measure of total mortality during specific time periods. Separating this aggregate measure into component rates for specific factors requires additional information. Death rate analysis provides a method for estimating mortality rates for specific time periods without the need for data on stage density and allows the contributions of contemporaneous factors to be quantified separately. Additional S o u r c e s of Mortality C a u s e d by Parasitoids The presence of a natural enemy in a system may result in host deaths not obviously attributable to the natural enemy. This applies particularly in the case of insect parasitoids (Table 1). Such losses may be difficult to quantify directly in field populations. They may resemble predation

TABLE 1 Factor

Impact in host population

Parasitism

Hosts in which parasitoid progeny develop

Host feeding

Hosts killed by adult parasitoid feeding

Ovipositor piercing and envenomization

Hosts killed by mechanical trauma or venom

Enhanced susceptibility to other factors

Unparasitized or parasitized hosts dying at increased rates following disturbance by foraging parasitoids

Lost natality

Reduced fertility of parasitized adult hosts prior to death due to parasitism

Comparison of Methods Of the methods discussed earlier, directly measuring recruitment to both the host and parasitoid populations is

Types of Host Mortality Caused by Parasitoids

204

T.S. Bellows and R. G. Van Driesche

in that mortalities of these types often result in missing individuals that leave no traces or artifact (such as empty leaf mines, which can stand in the stead of the dead organisms). Such mortality is typically assigned to "predation" or "other" categories by default. Levels of these mortalities may not be trivial. They may equal or exceed losses attributed to demonstrable parasitism (DeBach, 1943; Alexandrakis & Neuenschwander, 1980; Jervis et al., 1996) and may be critical in explaining biological control successes in which observed levels of parasitism are low (Neuenschwander et al., 1986; Briggs et al., 1995).

Host Feeding Host feeding has been recorded in over 20 families of Hymenoptera (Jervis & Kidd, 1986) and is nearly ubiquitous in some genera (e.g., Tetrastichus and Aphytis, Bartlett, 1964). Hosts killed in this manner may or may not have previously received an oviposition. The role of host feeding in field populations has received little study because the process usually does not leave identifiable remains. Field levels of host feeding of Sympiesis marylandensis Girault could be noted in life tables of Phyllonorycter crataegella (Clemens) as a distinct mortality factor because leaf mines preserved recognizable cadavers (Van Driesche & Taub, 1983). DeBach (1943) used field exclusion techniques to infer the level of mortality due to host feeding on the black scale, Saissetia oleae (Bern), by the parasitoid Metaphycus helvolus (Compere), and concluded that of the 70 to 97% mortality typically caused by this parasitoid, 45 to 77% was due to host feeding instead of parasitism. In a field study of the armored scale Aspidiotus nerii Bouch6, host feeding by Aphytis chilensis Howard was found to contribute half of all host mortality based on field counts of dead and parasitized scales (Alexandrakis & Neuenschwander, 1980). For mobile hosts where cadavers neither adhere to plant surfaces nor are retained in galls or leaf mines, individuals killed by host feeding disappear and cannot be scored directly. In such cases laboratory data may be used to estimate parasitism to host-feeding ratios and, together with levels of field parasitism, to estimate host-feeding losses (Legner, 1979; Chua & Dyck, 1982; Van Driesche et al., 1987). Use of laboratory data must take into account such complexities as selective host feeding on hosts of ages different from those usually parasitized (often younger stages, Chua & Dyck, 1982), host feeding in habitat zones not suitable for oviposition (Legner, 1977), or changing host-feeding to parasitism ratios at varying host densities (Collins et al., 1981).

Deaths from Ovipositor Piercing and Envenomization Hosts also may die from mechanical trauma of ovipositor piercing. This process is distinct from host feeding, and

younger hosts may suffer this mortality more than older hosts (Rahman, 1970; Neuenschwander & Madojemu, 1986; Hammond et al., 1987; Neuenschwander & Sullivan, 1987; Van Driesche et al., 1987). Deaths unrelated to parasitism also occur in species that paralyze their hosts when host death occurs in paralyzed hosts in which no oviposition takes place [e.g., Sympiesis marylandensis, Van Driesche & Taub, 1983; the eulophid Pnigalio flavipes (Ashmead), Barrett & Brunner, 1990].

Enhanced Susceptibility to Other Factors Parasitism may make hosts more susceptible to predation [Godwin & ODell, 1981 (p. 383); Jones, 1987] or disease (Godwin & Shields, 1984). Such events, occurring after parasitoid attack, do not change actual parasitoid-caused losses. Such factors may, however, obscure the actual rate of parasitoid attack, with deaths of parasitized hosts later eaten by predators being assigned in life tables to secondary agents of mortality instead of to parasitism. These deaths can be assigned correctly to the original cause (parasitism) by careful design of the sampling scheme, particularly by measuring recruitment, as discussed earlier. A more complicated situation arises in evaluating natural enemies of plants, because death may result from several factors acting together. In some cases, the presence of one factor can enhance the detrimental effect of another (Huffaker, 1953; Andres & Goeden, 1971; Harris, 1974). One approach to quantifying the relative contributions and interactions of these multiple factors is to use field experimental plots with different combinations of natural enemies (McEvoy et al., 1990, 1993). The presence of parasitoids in systems can also lead to healthy individuals experiencing greater mortality from other factors. For example, Ruth et al. (1975) noted that when greenbugs, Schizaphis graminum (Rondani), were exposed to the braconid Lysiphlebus testaceipes (Cresson), 41.0 to 62.0% of the aphids left their feeding sites, often falling to the soil. Such aphids were more likely to die due to high soil temperature before reestablishing themselves on plants than were undisturbed aphids. Pea aphids also leave their host plants when disturbed by parasitoids (Tamaki et al., 1970). In addition to effects on individual hosts, the presence of parasitoids may cause changes at population levels in other mortality factors. For example, introduction of exotic parasitoids suppressed winter moth, Operophtera brumata (Linnaeus), in British Columbia (Embree & Otvos, 1984), but apparently did so by making ground-inhabiting pupal predators more effective (Roland, 1988). While the preceding types of losses are properly assignable in a life table to the actual cause of death, it is important to be aware of any enhancement in levels of mortality caused by the presence of a natural enemy. This enhance-

Chapter 8 LifeTable Constructionand Analysis ment may be significant and must be considered when evaluating the overall impact of a natural enemy in a system.

205

pling of both parasitized and unparasitized individuals. Sampling schemes also must use spatial and temporal scales appropriate to the species studied.

Lost Natality

Parasitoids may limit host population growth by suppressing natality through several mechanisms, including sterilization, reduced daily fertility, or reduced longevity. Some euphorine braconids sterilize host adults shortly after parasitoid attack (Smith, 1952; Loan & Holdaway, 1961; Loan & Lloyd, 1974). For example, Microctonus aethiopoides Loan attacks and sterilizes reproductively mature female alfalfa weevils, Hypera postica (Gyllenhal) (Loan & Holdaway, 1961; Drea, 1968), causing a rapid degeneration of already developed eggs. This results in a 50% loss in total population natality (Van Driesche & Gyrisco, 1979). Parasitism of Nezara viridula (Linnaeus) by the tachinid Trichopoda pennipes (Fabricius) reduces lifetime (but not daily) fecundity by 74% (Harris & Todd, 1982) by reducing adult life span. Dipteran parasitism [mainly the sarcophagid Blaesoxipha hunteri (Hough)] of the grasshopper Melanoplus sanguinipes (Fabricius) reduced both the proportion of females producing egg pods and the number of pods per laying, producing an overall reduction in natality of 76% (Rees, 1986). The myrmecolacid strepsipteran Stichotrema dallatorreanum Hofeneder reduced numbers of mature eggs in field-collected adults of the tettigoniid Segestes decoratus Redtenbacher in Papua, New Guinea by 67% (Young, 1987). Parasitism by the pteromalid Tomicobia tibialis Ashmead reduced progeny production of the bark beetle Ips pini (Say) by 50% (Senger & Roitberg, 1992). Parasitism of the sow thistle aphid Hyperomyzus lacticae (Linnaeus) by the aphidiid Aphidius sonchi Marshall reduced total fertility by a variable amount depending on the age of the host when parasitized. Aphids parasitized in the third, fourth, or adult stages suffered 92.4, 85.5, and 77.8%, respectively, loss of lifetime reproductive capacity (Liu & Hughes, 1984). Similar relationships have been reported for the pea aphid when parasitized by Aphidius smithi Sharma & Subba Rao (Campbell & Mackauer, 1975) and for the green peach aphid, Myzus persicae (Sulzer), when parasitized by Ephedrus cerasicola Stary (H~gvar & Hofsvang, 1986). Such effects appear to arise mainly from reduced adult longevity, but may also involve a reduced daily rate of progeny production prior to adult death. Polaszek (1986) showed that parasitized aphids experienced reductions in embryo number and length within 3 days after parasitoid attack. When life tables are constructed for such continuously breeding species as aphids, lost fecundity may be listed as a type of "mortality" (Hutchinson & Hogg, 1985). Impact of S a m p l e Design The sampling regimen used to score mortality caused by a natural enemy must ensure adequate and unbiased sam-

Behavioral Biases

Parasitized hosts may behave differently than unparasitized hosts in ways that render them more or less vulnerable to detection. They also may occupy different habitats than do healthy individuals. Many of these behaviors result from differences in mobility between parasitized and healthy individuals,= and consequently these differences may be more likely to affect relative, instead of absolute, sampling regimes. Traps may have differing efficiencies for parasitized and healthy individuals. Yano et al. (1985) reported that levels of parasitism in the leafhopper Nephotettix cincticeps Uhler were distinctly higher (13 % versus 3 %) in individuals taken in sweep nets than in those collected at the same date and location in light traps because parasitism damaged thoracic muscles and weakened the insect's flight ability. Wylie (1981) reported that levels of parasitism of flea beetles [Phyllotreta striolata (Fabricius) and P. cruciferae (Goege)] by the euphorine braconid Microctonus vittatae Muesebeck were lower in beetles collected in traps baited with allyl isothiocyanate than in beetles collected with a vacuum suction device, but only when beetles were reproductively active. Parasitized beetles are sterilized and hence, according to the author, reacted like nonreproducing beetles, which are less attracted to host-plant odors. Parasitism also may influence movement of hosts between habitats. The potato aphid Macrosiphum euphorbiae (Thomas) when parasitized by diapause-bound Aphidius nigripes Ashmead leaves its habitat (Brodeur & McNeil, 1989), while those bearing parasites not bound for diapause do not. Wylie (1982) reports that flea beetles (Phyllotreta cruciferae and P. striolata) parasitized by Microctonus vittatae emerged from overwintering sites earlier than unparasitized beetles; consequently, samples of beetles in the crop exhibited a steady decline in percentage of parasitism over a 10-day emergence period, unrelated to changes in parasitism in the entire population. Ryan (1985) attributed decrease in percentage of parasitism of larvae of the larch casebearer, Coleophora laricella (Htibner), on larch foliage to the selective drop of parasitized larvae to the undergrowth, an unsampled habitat zone. Parasitism can also affect rates of host movement within the habitat, making hosts more likely to be seen and collected (if done by hand) or caught in traps. The isopod Armadillidium vulgare Latreille moved farther and rested less often when parasitized by the acanthocephalan parasite Plagiorhynchus cylindraceus (Schmidt & Kuntz), making parasitized individuals more easily detectable in its habitat (Moore, 1983).

206

T.S. Bellows and !~ G. Van Driesche

Most of the difficulties posed by these behaviors can be avoided by using absolute, instead of relative, measures of population density during sampling. Care must be taken to sample all occupied habitats and, where necessary, subsample different portions of the population to provide relative rates of parasitism in each. These partial rates may be weighted by the densities in each habitat to provide an overall estimate of numbers dying from parasitism in the population as a whole. Studies evaluating predation instead of parasitism may need to take into account similar effects.

Biases Affecting Detection of Density Dependency Problems in detecting existing density dependency can occur if either the spatial scale or the timing of the sampling regime is inappropriate. If hosts are strongly clumped and clumps are distributed on a spatial scale that is meaningful to parasitoids, their activity may be concentrated on dense clumps, either from aggregation of foragers or from greater progeny production and retention in locally host-rich areas. In such cases, the sampling program must provide samples from patches of different densities, and each sample must consist of individuals from a given density instead of a mixture of hosts from high- and low-density patches (Heads & Lawton, 1983). If samples are based on mixtures of individuals from patches of strongly differing densities, any density dependency can be obscured (Hassell, 1985a, 1987; Hassell et al., 1987). Pooling of samples from high- and low-density periods in a time series may have the same effect as pooling high- and low-density samples collected at one time from several locations, obscuring temporal density dependence. Finally, it should be emphasized that parasitoid-caused mortality acts on hosts selected for oviposition, not hosts from which adult parasitoids emerge. Nevertheless, estimates of parasitism often are based on rearing parasitoids from host instars or stages subsequent to the one attacked. Mortality levels are then associated incorrectly with the density of the host at the time the samples were collected rather than with the density of the host when it was actually attacked. Density dependency of a mortality factor will only be detectable if its level is measured accurately and associated correctly with the host density upon which it acts.

ASSESSING QUANTITATIVE IMPACT OF NATURAL ENEMIES With one or several well-constructed life tables for a host population affected by a natural enemy, questions concerning the amount of mortality (both in absolute terms and in relation to other sources) in the host population can be examined.

P a r a m e t e r s in t h e Life Table The objective of life table analysis for natural-enemy evaluation is to estimate the attack rate of specific natural enemies to permit comparisons between agents or populations. Some of the methods discussed earlier under life table construction (such as measurement of recruitment) yield these rates directly and do not require further calculations from a life table. Where these methods have been used, construction of a life table and further analysis to determine the quantitative impact of the natural enemy may not be necessary. Construction of a life table in these cases may be useful if additional analyses, such as those relating attack rates to population densities, are desired. Other methods described previously will require that density and mortality information be subjected to further calculations to arrive at attack rates for the different factors in the life table. The components of a life table typically include the numbers entering each of several life stages (lx) in an insect's life cycle, numbers dying within each stage (dx) due to specific factors, together with estimates of rates of loss in each stage (Table 2a) (Southwood, 1978). Mortality rates are typically expressed in proportions. Several different types of mortality rates have been included in life tables. These include real mortality, apparent mortality, indispensable mortality, marginal attack rates, and k-values. It is likely that more than one mortality factor will act contemporaneously at some point in the life table. It is appropriate, therefore, when seeking an index for assessing the impact of natural enemies, to select one that will have the same meaning when describing both contemporaneous factors and those that act alone within a stage. Real mortality, apparent mortality, and indispensable mortality are primarily of value when considering factors that act alone in a stage. Marginal rates are applicable both to factors acting alone and contemporaneously acting factors. Real mortality is the ratio of the number dying in a stage (dx) to the number initially entering the first stage in a life table (/o): real mortality = dx/lo. This column sums to the total mortality in the life table. This column may be useful for comparing the role of factors within generations (if calculated for sequential, noncontemporaneous factors) (Southwood, 1978)i Apparent mortality (denoted by qx) is the ratio of the number dying in a stage to the number entering the stage, or the number dying from a factor to the number subject to that factor: qx = dflx. When only one mortality factor occurs in a stage (or where more than one occurs and they act sequentially), then the apparent mortality (the proportion of animals dying from a factor) is the same as the proportion initially attacked by the factor (the marginal attack rate). Southwood (1978) suggests that this measure may be used for comparisons among independent (noncontemporaneous) factors or to compare the same factor in different life tables.

207

Chapter 8 LifeTable Construction and Analysis TABLE 2

Impact of Sequential versus Contemporaneous Factors in a Life Table Apparent mortality

Stage

Factor

Ix

Stage dx

100

50

Factor dx

Marginal death rate

Stage qx

Factor qx

Real mortality Stage dxllo

Factor dxllo

(a)

Stage 1 1.1 1.2 Stage 2

50

0.500 0.000

25 0

0.500 0.000

25

2.1 2.2 Adults Sex ratio Fertility F~ progeny Ro

0.500 50 0

0.500 0.5 0

0.500

0.5 0 0.250

0.5 0

0.25 0

25 0.5 200 2500 25 (b)

Stage 1

100

75

1.1 1.2 Stage 2

25 2.1 2.2

Adults Sex ratio Fertility F1 progeny Ro

0.750 37.5 37.5

0.500 0.500

0 0

0.000 0.000

0

0.750 0.375 0.375

0.000

0.375 0.375 0.000

0 0

0 0

25 0.5 200 2500 25

Apparent mortalities, because they are calculated on a stage- or factor-specific basis, are not additive, but the product of their associated stage survival rates (1 - stage apparent mortality) yields the total survival in the life table. Indispensable mortality has been little used. It is described as "that part of the generation mortality that would not occur, should the mortality factor in question be removed from the life system, after allowance is made for the action of subsequent mortality factors" by Southwood (1978), who also describes its calculation. This type of calculation entails an assumption that subsequent mortality factors in the life history act in a density-independent manner. Huffaker and Kennett (1966) suggested that indispensable mortality may be used to assess the value of a factor in a biological control program, but this applies primarily to comparisons within a life table, rather than among several life tables, because its value depends on the quantitative level of other mortalities in the life table, which may vary in different systems. The proportion of individuals entering a stage that are attacked by an agent is termed the marginal rate of attack or marginal attack rate (Royama, 1981b; Buonaccorsi & Elkinton, 1990; Elkinton et al., 1992). This measure of mortality has the most consistent interpretation among life tables or among factors within a life table; it is the only

measure whose calculation permits correct interpretation of the impact of contemporaneous mortality factors. The details of its calculation depend somewhat on the nature of a specific factor (Elkinton et al., 1992). For factors that act alone in a stage, the apparent mortality is the marginal attack rate. When two or more factors act contemporaneously, the apparent mortality will be different from (and smaller than) the marginal attack rate. For such contemporaneous factors, determining the number attacked by a factor must account for those that receive attacks from more than one type of agent. Two general approaches are available in these cases, either (1) assessing the attack rate as it occurs (e.g,, measuring recruitment by dissection for parasitism), which directly estimates the marginal attack rates; or (2) calculating the attack rate from the observed death rates of individuals succumbing to the various factors (Buonaccorsi & Elkinton, 1990; Elkinton et al., 1992; Gould et al., 1992c). The equations employed in calculating marginal attack rates from observed numbers dying vary for different categories of natural enemies. Equations for contemporaneous parasitism differ slightly from those used when predation and parasitism occur together (Elkinton et al., 1992). The product of (1 - marginal rates) for all factors is equal to the overall survival rate for the life table. In addition to these measures of mortality, k-values may

208

T.S. Bellows and R. G. Van Driesche

also appear in life tables, k-values are marginal survival rates on a logarithmic scale, and are the negative logarithm of ( 1 - the marginal attack rate) for a factor. Although equivalent in principle to the marginal rate, their calculation has been a source of difficulty in cases of contemporaneous factors. The explicit calculation of a k-value requires the number of attacked individuals and the number of individuals initially exposed or subject to the factor (Varley & Gradwell, 1960, 1968; Varley et al., 1973), the same information necessary for calculating marginal rates. Use of the numbers observed dying due to a factor can only lead to correct calculation of a k-value if factors act strictly sequentially in a stage or in successive stages, k-values for contemporaneous factors cannot be calculated from the number observed dying because the action of each factor is obscured by the action of others. A lack of appreciation of this crucial distinction has led to the incorrect calculation of k-values in many studies. Because k-values are logarithms of survival rates, their sum (when each has been properly calculated) is equal to the logarithm of total survival, in the same way that the product of survival rates for separate factors yields the overall survival in the life table. Evaluating the effects of the natural enemies in a system must be made with respect to some standard of host population growth potential. An appropriate standard for populations with discrete generations is the population net rate of increase Ro, which is the ratio of population sizes in two successive generations. Similarly, the intrinsic rate of inc r e a s e R m could be used for continuously breeding populations. Calculation of Ro from a life table requires data on fertility of the population, which often can be measured or estimated. The product of overall proportion survival and fertility yields an estimate of Ro. When Ro = 1 (or R m = 0), the population is neither increasing nor decreasing. Values for Ro greater than unity (or R m > 0) imply an increasing population, while values of Ro less than unity (or R m < 0) imply that the population is decreasing in density. In the context of biological control programs, a value of Ro greater than unity implies a need for greater natural-enemy action to reduce Ro and contain the population. Comparisons among factors and life tables are most easily accomplished with reference to marginal rates, the values of which are independent of the presence of additional, contemporaneous factors in the system (this is not true for either apparent or real mortality). Marginal rates assigned to a particular factor are directly comparable among different life tables, even when those life tables contain differing numbers or quantitative levels of other factors. When correctly quantified, k-values may be used equivalently. I n t e r p r e t i n g Life Tables A series of examples will serve to illustrate the relationships among life table parameters together with their interpretation.

The simplest case for a life table is when each factor acts independently and sequentially, so that no overlap occurs among stages subject to individual factors (see Table 2a). In this case, the marginal death rate and the apparent mortality for each factor are the same. In this example, where 50% of the individuals die in each of two successive stages, real mortality declines from stage 1 to stage 2, because only 25 individuals die in stage 2. When two factors act contemporaneously (see Table 2b) (in Tables 2, 3, and 4 factors occurring within a stage act contemporaneously), marginal rates and apparent rates differ. The proportion actually attacked is higher than the proportion ultimately dying from the factor. This is because some animals attacked by factor 1.1 are also attacked by factor 1.2. Because some animals may be attacked by both factors contemporaneously, but can die from only one, the total number of attacks exceeds the total number of animals dying. The total number dying in the population is the same as in Table 2a because the marginal rates of two factors are the same in both tables, but their sequential action in Table 2a leads to different numbers dying from each. This underscores an important feature of marginal rates that renders them so particularly valuable for comparison--the marginal rate is the proportion that would die due to that factor in the absence of other independent factors or when that factor is acting alone (Elkinton et al., 1992). This feature is constant for marginal rates in any combination with other factors. No other measure of mortality has this uniformity of representation or meaning across different life tables. It may be observed that factors with large "apparent" mortalities add only a small amount of additional "real" mortality to systems in which there is already substantial mortality. Table 3a is a hypothetical table with only one mortality factor, causing 0.90 loss in stage 1. This reduces numbers entering the final stage by 90%. In Table 3b, an additional source of mortality is added, attacking 0.80 of insects in stage 1 and acting contemporaneously with factor 1. The addition of this second factor, which attacked 80% of the insects in the stage (i.e., had a marginal rate of 0.80), raises the stage apparent mortality rate from 90%, (see Table 3a) to 98% (see Table 3b), thereby adding 8% "real" mortality. The effect of this second source of mortality, however, on the numbers entering the final stage is not an 8% but an 80% drop in density (from 10 adults in Table 3a to 2 in Table 3b). Again, the marginal rate reflects the contribution of the factor. In each of the preceding life tables, values were given for fertility and sex ratio. These values may be multiplied by the total number surviving to the adult stage to provide an expected number of progeny in the first stage in the next generation. The ratio of this number of F1 progeny to the original number entering the life table is an estimate of Ro. In the first three life tables, Ro is greater than unity, implying an increasing population. In Table 3b, Ro = 1, imply-

Chapter 8 TABLE 3

209

LifeTable Construction and Analysis

Impact of Single versus Two Contemporaneous Factors in a Life Table Apparent mortality

Stage

lx

Stage dx

100

90

Factor

Factor dx

Marginal death rate

Stage qx

Factor qx

Real mortality Stage dxllo

Factor dxllo

(a)

Stage 1

0.900

1.1 1.2

90 0

Adults Sex ratio Fertility F~ progeny Ro

10 0.5 100 500 5

Stage 1

100

0.900 0.000

0.900 0.9 0

0.9 0

(b) 98

0.980

1.1 1.2

54 44

Adults Sex ratio Fertility F1 progeny Ro

0.900 0.800

0.980 0.54 0.44

2 0.5 100 100 1

ing that this population is stationary. The difference between the Ro estimates for Table 3a and b is 80% and reflects the addition of the second mortality factor. Life tables for actual systems typically contain more than one or two factors, but interpretations of the various rates are made in the same way. Thus for a population of Pieris rapae Linnaeus larvae (Tables 4a and 4b), high levels of both parasitism by Cotesia glomerata (Linnaeus) and

TABLE 4a

predation occurred, as expressed by the large marginal rates for these factors. These contributions are s o m e w h a t less clear in the apparent and real mortality rates. The contemporaneous action of these mortalities causes a much greater n u m b e r of individuals to be attacked by each than to actually die from each, because a number of parasitized individuals are lost to predation prior to parasitoid emergence. The contributions of a specific mortality agent may ad-

Life Table for a Pieris rapae-Cotesia glomerata System, Parasitoids Present Apparent mortality

Stage

Egg Infertility Larvae

Factor lx

Stage dx

10.669

0.128

10.540

0.0271

Factor dx

Marginal death rate

0.128

0.012

Stage qx

Factor qx

0.012

10.51

C. glomerata Predation Pupae Predation Adults Sex ratio Fertility FI progeny Ro

0.54 0.44

0.867 0.981

0.008

0.310

0.008

After Van Driesche, R. G., & Bellows, T. S., Jr. (1988). Ecological Entomology, 13, 215-222. aValue from Norris (1935).

Factor dx/lo

0.012 0.012 0.985 0.442 0.555

0.310

0.0186 0.50 356a 3.328 0.311

Stage dx/lo

0.012 0.997

4.660 5.853

Real mortality

0.436 0.548 0.000

0.31

0.001

210

T.S. Bellows and R. G. Van Driesche TABLE 4 b

Life Table for Pieris rapae-Cotesia glomerata S y s t e m , Parasitoids R e m o v e d

Apparent mortality

Stage Egg Infertility Larvae

Factor

Stage

Factor

lx

dx

dx

Marginal death rate

10.669

0.128 0.128

0.012

10.540

0.2044

Factor

Stage

Factor

qx

qx

dx/lo

dJlo

0.012 0.012

0.981 0 10.33

C. glomerata Predation Pupae Predation Adults Sex ratio Fertility F1 progeny Ro

Stage

0.012

10.33 0.000 0.981

0.063 0.310

0.012 0.969 0 0.968

0 0.980 0.310

0.063

Real mortality

0.006 0.31

0.005

0.1411 0.50 356 a 25.11 2.354

After Van Driesche, R. G., & Bellows, T. S., Jr., (1988). Ecological Entomology, 13, 215-222. aValue from Norris (1935).

ditionally be evaluated by removing it from the life table and recalculating the survival and reproduction parameters. Comparisons between tables with and without the action of the natural enemy provide an index of its contributions to the system. This has been done by removing parasitism from Table 4a and recalculating the remaining parameters (Table 4b). Comparison of the two tables reemphasizes that "real mortality" is not very sensitive to the addition of another factor. For the cases in Tables 4a and 4b, the predation marginal rate was 98.1%, and the addition of an 86.7% parasitism marginal rate for parasitism added only 1.6% to the stage real mortality (Table 4a versus 4b). The presence of this factor, however, resulted in an 87% (equal to the marginal rate for this factor) reduction in numbers entering the last stage, reducing it from 0.141 to 0.0186. Thus parasitism was crucial in reducing the net rate of reproduction of the population from 2.4 to 0.31. The use of this technique assumes that the marginal rates of the other factors do not change with the removal of the factor of interest. Evaluating the specific contribution of any particular factor in a life table requires the careful selection of an appropriate index. Because apparent mortality in a stage can rise only to 1.0, the value of additions of further mortality agents for a stage is not well reflected by rises in apparent mortality. In general, the higher the level of mortality within a stage from a pre-existing factor, the smaller will be the rise in apparent mortality to that stage from the addition of another factor. Thus, increases in apparent or real mortality in a stage due to the addition of a new mortality agent do not adequately reflect the contribution of the new mortality agent. In contrast, the marginaldeath rate of any factor in a system is a direct reflection of its impact on reducing the numbers entering the final stage in the

table, and therefore its contribution in reducing host densities. Of the available measures for expressing mortality in life tables, marginal rates most accurately express the individual contributions of particular factors, particularly when two or more factors act contemporaneously, k-Values, when properly calculated to reflect the marginal rate, are similarly useful, because they are functionally interchangeable with marginal rates (on logarithmic scales) as expressions of mortality. The overall contribution of specific mortality agents in life tables can be examined by addition or subtraction of such factors, manipulating numbers in the life table to reflect their absence or presence. Such manipulations allow hypotheses to be formulated concerning the impact of specific agents. Such hypotheses can be formulated in terms of changes in the net reproduction rate (Ro) of the population. Ro is a particularly suitable index because it expresses the ability of the population to reproduce itself given the state of all sources of mortality in the system. It cannot be overemphasized that the percentage of mortality due to parasitism (or other agents) observed in populations is relatively meaningless in the absence of quantitative values for all mortalities acting in the parasitized stage. These additional mortalities are nearly always essential for estimating the marginal death rate due to any one specific factor (Royama, 1981b; Elkinton et al., 1992). (One exception is when parasitism is being measured as a comparative parameter between treatments in experiments in which only a relative contrast is being measured, and other factors are known to be similar or constant between treatments.) The relative importance of a mortality factor is most effectively expressed with respect to the reproductive dynamics of the insect it attacks, that is, the fertility of the host and a full quantitative description of all mortalities.

Chapter 8

LifeTable Construction and Analysis

Even if any given natural enemy does not cause the population of the host immediately to decline, it may be valuable if it increases the overall mortality, because Ro may become less than unity after the addition of some additional factor or natural enemy (e.g., Aphytis paramaculicornis DeBach and Coccophagoides utilis Doutt on olive scale, Huffaker & Kennett, 1966).

DETERMINING ECOLOGICAL ROLES OF NATURAL ENEMIES Role Q u e s t i o n s a n d D e n s i t y R e l a t e d n e s s A basic precept of biological control is that effective natural enemies will contribute to a reduced and stable pest density. Both of these features are relative termsmthe new pest density would be lower than the previous density, and would exhibit fewer fluctuations than the population without the natural enemies. In this context, natural enemies may play one or more of a variety of roles in the ecology of a natural-enemy and pest system. Most of the features desired in natural enemies fall into one of two categories: (1) the natural enemy will reduce the pest density and (2) the natural enemy will aid in stabilizing the pest density. This section deals with how the analysis of life table data can contribute to testing hypotheses concerning these and related roles for natural enemies. Testing such hypotheses from life table data usually requires examining several life tables for trends or contrasts in the impact that natural enemies have on pest populations. Consequently, where in the previous sections we were concerned with the proper construction of, and quantifying factors in, life tables, here we will deal with the analysis of such features where several life tables are available for the same system. These might arise from sequential sampling of the same population over several generations, from contemporaneous sampling of several populations in different areas, or from both. The types of questions that can be addressed depend somewhat on the types of data that are available. Natural enemies may play either or both of the previously mentioned roles in an ecological system, which leads to several possibilities in the structure of natural-enemy and pest interactions. The classical interaction envisaged by many authors is the situation where both roles are embodied in the same natural-enemy species, so that the natural enemy contributes quantitatively to the suppression of survival or reproduction (so that Ro < 1 or R m < 0 at high densities) and also contributes to stabilizing the system at the new, reduced density. Such an outcome would indeed be optimal and desirable, because no further additions to the system are needed for success in the context of either reducing population density or maintaining stability. Two additional situations also are possible. The natural enemy

2 | I

may contribute to reductions in survival or fertility (thus contributing mortality in the life table so that Ro will be reduced) without contributing to stability per se. In such a situation, the system may be stabilized by some other factor in the life table (e.g., Harcourt et al., 1984), or may be relatively unregulated. Finally, the natural enemy may contribute to stability or regulation without increasing the total level of mortality in the life table, perhaps by replacing an existing factor with a new one that causes an equivalent level of mortality but acts with an increased level of density dependence. Identifying the role of particular natural enemies in a particular system may not provide a comprehensive answer to the question of what features are significant in shaping the dynamics of pest and natural enemy populations. Addressing that question may require an evaluation of the role of several or all of the factors operating in the system. Many of the available theories concerning host and parasitoid dynamics (Beddington et al., 1978; May, 1978; Hassell, 1985b; Murdoch et al., 1992, 1995, 1996; Bonsall & Hassel, 1995; Mills & Getz, 1996; Murdoch & Briggs, 1996) employ some density-related property as a stabilizing mechanism. These appear in various forms and can all be considered under the general heading of density dependence. These theories generally provide testable hypotheses concerning the role of natural enemies, although conducting the tests in a statistical sense can be difficult, as discussed later. Four cases concerning density dependence in a life table may be distinguished: (1) there may be no density dependence in the system, (2) density dependence may be attributable to a natural enemy under investigation, (3) density dependence may be due to some other factor in the life table, or (4) density-related factors may exist but may be masked by stochastic factors. In addition, more than one factor may be density dependent, which requires careful consideration in constructing tests of hypotheses. Hypotheses about density dependence are usually tested against the null hypothesis that no density dependence is present in the system. Other theories have proposed dynamics of pest and natural-enemy systems that are not characterized by densitydependent stabilizing mechanisms (see Chapter 2). The hypotheses provided by such theories are not as readily testable by analyzing life table data, because they are characterized by dynamics that do not have deterministic relationships between measured variables (such as density and mortality). These theories may provide more readily testable hypotheses following further development. Ecological Roles a n d H y p o t h e s e s Before considering in detail some specific role questions and techniques for testing their related hypotheses, it is helpful to review some terms and their meanings. We will imply here by the term regulation the tendency of a popu-

212

T.S. Bellows and K G. Van Driesche

lation to move toward some mean value. This does not imply a reduction in density, which we will term suppression. Regulation is often considered to be due to the action of some density-related factor. In general, density relatedness may be viewed as falling into one of three categories: density dependence (where proportional mortality increases as density increases), inverse density dependence (where proportional mortality decreases with increasing density), and density independence (where proportional mortality neither increases nor decreases with mortality). Density dependence may further be defined as direct density dependence, where the factor is related to the density of the generation in which it acts, or delayed density dependence, where the factor is related to the density of the generation prior to the one in which it acts. Density relatedness may be expressed among portions of a population in different locations (over space) or between successive generations of the same population (over time), or both. Finally, a key factor is the mortality factor most closely related to, or responsible for, change in total generational mortality among several generations in a population; in general, it is simply the most variable mortality factor in the system. The term key factor does not imply either that the factor is regulatory or that it is the factor most responsible for determining the mean density of the population. Natural enemies may be important either as sources of mortality or as regulating factors without being the key factor in a system. The role questions best addressed by the examination of several life tables is whether or not the natural enemies function as regulating factors. Such regulation usually is reflected in hypotheses as density-dependent mortality, and consequently life tables are often examined to determine whether the mortality imposed by a natural enemy acts in a demonstrably regulating or a density-dependent manner. Several mechanisms have been proposed that fall into this category (see Chapter 2). In most cases the proportion of pests dying due to the natural enemy increases with pest density. Inverse density dependence also can act, in some cases, as a stabilizing factor (Hassell, 1984), as can simple spatial heterogeneity (May, 1978; May & Hassell, 1988; Pacala & Hassell, 1991). It is crucial, when considering relationships between density and mortality, both to quantify correctly the proportional losses assigned to a factor and to associate this mortality with the density and stage on which the factor acts. For example, parasitoids attacking only young larvae are acting on a population whose density may be very different from the late larval population from which the parasitoids emerge (Van Driesche & Bellows, 1988). Similarly, when not all individuals in the population are susceptible to natural-enemy attack, the proportional mortality must be related to the density of susceptible individuals. A less rigorous approach will confound the underlying relationships by associating mortality rates with unrelated densities from inappropriate stages in the life table.

The possible alternative hypotheses related to natural enemies acting as a regulating factor are twofold: (1) they may act in a destabilizing manner (i.e., they are acting either in a destabilizing inverse density-dependent manner or in a delayed density-dependent manner), or (2) they may not contribute to regulation but serve solely as an additional density-independent mortality in the life table. In this second case, the density-independent mortality may have a small variance, or have a larger variance and be catastrophic in nature.

Analytical T e c h n i q u e s The analysis of population and life table data for the purpose of detecting stability and regulation has followed two rather distinct approaches. The first of these addresses general questions of population stability with reference solely to density counts in successive generations. The second is concerned with density relatedness of specific factors in life tables. Although the overall objective of the two approaches is similar, they employ somewhat different analytical techniques and we will treat them here separately.

Tests for Population Stability Tests for population stability focus on the general question of dynamical behavior of a population over several generations, without reference to causal mechanisms. The general framework for this question arises from Morris's (1959) proposal for the detection of stability in a population. In this context, stability is the tendency of a population to grow or decline in a manner that moves it toward an equilibrium when it is displaced from it. Such a population would tend to decrease when denser than the equilibrium value, and to increase when below the equilibrium value. Such populations are in contrast to those that either grow or decline exponentially and those that exhibit a random, but undirected, trajectory through time. In this light, if a population is characterized by the logarithm of its density in generation t, X,, then the dynamics of an unstable population may be expressed by X,+l = r + X, + e,

(1)

where r is the growth rate between generations and et is a stochastic error term representing random deviations in r. Stable populations may be represented, in contrast, by Xt+I = r + bXt + et

where b takes values between - 1 and 1 and represents density-dependent restrictions on population growth. Several analytical tests for detection of stability by examining series of population censuses have been developed. Much of this work has followed Morris's (1959) original

Chapter 8

Life Table Construction and Analysis

proposal, offering criticisms and improvements. The original proposal involved regressing X,+ 1 against Xt and testing the slope of the regression for significant difference from 1, the null hypothesis value for no regulation. The general concept has been accepted by most workers, but its application to hypothesis testing has proved problematic. The first-order autocorrelation in the time series of Eq. (1), together with the presence of sampling errors in the abscissal values Xt, creates such significant biases in the regression slope that the test is generally considered inadequate (Varley & Gradwell, 1968; Bulmer, 1975; Pollard et al., 1987) because it rejects the null hypothesis in a large proportion of cases when the null hypothesis is true (i.e., it has a large likelihood of a type I error). A number of parametric (regression) as well as simulation tests have been proposed to overcome this difficulty. The first parametric test presented was that of Varley and Gradwell (1968), who proposed a modification of the criteria for rejecting the null hypothesis by suggesting that double regressions be performed, and that the slope estimates b (for the regression of Xt+ 1 on Xt) and slope estimate b~y (for the regression of X, on Xt+ 1) be performed. The null hypothesis would be rejected only when both regression slopes differed significantly from unity and both b and 1/bxy are less than unity. Simulation studies have indicated that, while it has a low likelihood of a type I error, this test also has relatively poor power (that is, it fails to reject the null hypothesis in a large proportion of cases when the population is stable); as a statistical test it is overly conservative. Other parametric tests have been proposed. Bulmer (1975) introduced a test statistic based on the reciprocal of Von Neuman's ratio for time series analysis, and a modification of this statistic for cases when there are errors in sample estimates of population counts (the usual case). Slade (1977) suggested using two other statistics developed previously for estimating slopes of relationships where error occurs on both axes, the major axis test (Deming, 1943) and the standard major axis test (Ricker, 1973, 1975). Dennis and Taper (1994) proposed a similar regression model and outlined bootstrap and jackknife techniques to allow for hypothesis testing. A number of simulation studies have been conducted to assess the error rate (for type I errors) and the power of these various tests (Slade, 1977; Vickery & Nudds, 1984; Gaston & Lawton 1987; Holyoak, 1993; Holyoak & Lawton, 1993; Fox & Ridsdill-Smith, 1995). The general conclusions of these workers is that these tests are not all robust, and that many have acceptable error rates and power only in exceptional circumstances. In addition, the power of these types of tests is clearly related to the length of the census available for analysis, and censuses in excess of 15 to 20 generations appear to be necessary to ensure an acceptable degree of power (Hassell et al., 1989; Bonsall & Hassell, 1995; Fox & Ridsdill-Smith, 1995). Fox and Ridsdill-Smith (1995) proposed that, as an initial or

213

general standard for testing for stability or regulation in a population census over several generations, Bulmer's (1975) (first) test be employed, because it seems to have the greatest degree of applicability and the fewest drawbacks in use. The variation on Bulmer's (1975) statistic proposed by Reddingius and den Boer (1989) may also be of value, although this test has not received the extensive attention of earlier proposals and has not yet been subject to testing by Monte-Carlo simulation, as have the earlier tests. Alternatives to parametric, or regression, tests have been developed by several workers using Monte-Carlo techniques. These generally take the form of proposing population models for the two hypotheses under consideration (the null hypothesis of no stability and the alternative hypothesis of stability). The models, which incorporate various components of stochastic variation, are then used to simulate a long series of synthetic populations with parameter values taken from the natural population under study. The dynamics of these synthetic populations are then summarized in one or more statistics, and the same statistic is calculated for the natural population. The distribution of the statistic from synthetic populations is compared with observed value of the statistic from the natural population; and if the observed value lies near the extreme end of the synthetic distribution (usually beyond the 5% most extreme cases), the null hypothesis is rejected. This procedure has provided some very helpful insight into the behavior of the parametric tests discussed earlier, and has provided "simulation" tests that appear able to distinguish stable from unstable populations. Slade (1977) proposed one such test based on simulated distributions of the t-value associated with the usual regression slope b. Pollard et al. (1987) found this test insufficient, and developed a test based on likelihood ratios that appears both to have an acceptable type I error rate and a sufficient power to identify stable populations, although the matter of errors in density estimation was not addressed by this technique. Reddingius and den Boer (1989) developed a similar test that does provide for errors in density estimation, and provided a fuller examination of its power than have other researchers, although they did not provide any information on the error rate of their proposed index under the null hypothesis. Either one of the last two proposals would be suitable Monte-Carlo techniques for examining censuses for evidence of stability, but both require much more extensive use of computing than do the parametric tests of the previous paragraph.

Tests for Density Relatedness in a Specific Factor Populations are affected by both biotic factors, which may show some form of density relatedness, and abiotic factors, which with few exceptions are density independent in their action. When the variation from year to year in the amount of mortality inflicted by density-independent factors

214

T.S. Bellows and R. G. Van Driesche

is greater than the mortality caused by density-dependent factors, the population's dynamical behavior is dominated by these density-independent processes and, consequently, may not show stability in the sense discussed earlier. This does not preclude the presence of potentially regulatory mechanisms, but may make difficult their detection by examination of population census data (Hassell, 1985b). Consequently, tests have been developed to examine specific factors for attributes that could contribute to stability, even if they are acting in concert with other factors that obscure their effects. The original approach was predicated on the view that temporal density dependence (sensu Nicholson, 1954) was the primary, or perhaps only, mechanism that could contribute to regulation of a system. Following this line of reasoning, Varley and Gradwell (1968) suggested plotting survival against density on log scales (the familiar plot of k-value versus log density). Regression analysis was used to determine if the slope of the relationship was significantly greater than 0, implying density dependence (because mortality rate was increasing with density). They recognized, however, that the estimate of density was employed on both axes (on the ordinal scale as a component of the k-value), and that the errors of estimation occur on both axes. These conditions preclude the application of usual tests for significance of the regression slope, complicating the issue of rejecting the null hypothesis of no density dependence. This issue received considerable attention subsequently, but no completely satisfactory solution has been proposed. Thus the technique of k-value analysis continues to be employed to provide initial assessments of density relatedness mdensity dependence, delayed density dependence, or inverse density dependence--in long-term studies of populations. Royama (1981a) suggested that an alternative approach might be to attempt to determine a priori what factors in a life table were density independent, identify them and quantify their impact on mortality, and subsequently examine the remaining factors for density relatedness. This proposal appears promising, but Royama did not address issues relating to statistical testing of hypotheses in this framework. Examining factors for temporal density dependence in the host population is but one step in the search for regulating features in a life table. Other forms of density relatedness were soon appreciated as potential contributors to population stability, particularly density dependence occurring within a generation but over some spatial scale. These include interference among parasitoids (Hassell & Varley, 1969; Hassell, 1970), aggregation (Hassell & May, 1973, 1974; Beddington et al., 1978), inverse density dependence (Hassell, 1984; Hassell et al., 1985), host refuges (Reeve & Murdoch, 1986), specific types of natural enemy search behavior such as sigmoid functional response (Hassell et al., 1977; Hassell & Comins, 1978), invulnerable life stages

or invulnerable fractions of populations (Murdoch et al., 1987), and even simple spatial patchiness or heterogeneity (May, 1978). Not all these features have been found in natural field systems, although many are well known from laboratory systems. Some are known from some field systems and not from others [e.g., lack of aggregation of Aphytis melinus DeBach against Aonidiella aurantii (Maskell) (Reeve & Murdoch, 1985), but presence of aggregation of parasites attacking bivalves (Blower & Roughgarden, 1989)]. Occasionally a particular behavior usually considered to contribute to regulation via density dependence is found to be present, but stabilizing density dependence cannot be demonstrated (Smith & Maelzer, 1986). In some cases, the ability to detect certain mechanisms is dependent on the scale of measurement, for example, in cases of aggregation (Hassell et al., 1987) or the assessment of patch sizes as perceived by the natural enemy (Heads & Lawton, 1983). Our understanding of what types of behaviors and features of natural enemies and their host populations can enhance stability has advanced rapidly, faster than have statistical developments for handling these special testing needs. The intricate correlations and interdependencies among such life table variables as mortality and the density on which it acts are not completely understood for most of these types of factors. This makes the development of statistical tests that have acceptable error rates and have sufficient power a difficult task. In many of the articles cited in the preceding paragraph, researchers have employed various statistical techniques in an effort to demonstrate the presence (or absence) of a particular behavior. Most of these appear rational, but normal statistical assumptions are often violated. In addition, linear models relating behaviors to density have been employed when a priori considerations indicate that such models cannot apply and curvilinear models would be more appropriate. This is not to suggest that such studies have failed in their objectives, but only to point out that the suitability of most statistical techniques for use in detecting regulating behaviors has not been evaluated. Hence no standard statistical analytical technique has emerged for the evaluation of these behaviors. In light of the plurality of features of biological systems that can affect their dynamics, and the potentially masking effects of random (density-independent) factors (Hassell, 1985b, 1987), no simple analysis will likely serve to provide definitive answers to questions of density relatedness or the presence of other stabilizing mechanisms in life tables. Carefully planned studies contrasting the behavior of systems both with and without natural enemies may permit simpler comparisons of system dynamical behaviors and testing of hypotheses. These ideas are outlined later. Complementary to the use of statistical analytical techniques, computer models will continue to be a useful tool in the exploration of the role of any given factor in a life

Chapter 8

215

Life Table Construction and Analysis

table. Such models can be used to generate hypotheses about the behavior of systems in the presence and absence of particular factors, such as natural enemies. Quantitative, explicit life tables may well be the key element in obtaining the necessary information with which to construct models from which hypotheses can be generated. These hypotheses subsequently can be tested only with reference to data from natural populations. This emphasizes the significance of accurate, well-constructed life tables for both the generation and the testing of hypotheses about system behavior and dynamics.

EXPERIMENTAL DESIGNS FOR LIFE TABLE STUDIES Construction and analysis of life tables for separate host populations having and lacking a natural enemy is a powerful approach to natural-enemy assessment. Researchers can maximize the power of life table data to reveal both the total mortality contributed by an agent and the ecological role of the agent through careful use of such planned contrasts. The required contrast of populations having and lacking a natural enemy can be achieved by organizing comparisons in one of three general ways: 1. Time may be used to organize the with and without contrast for cases of introduction of new agents where studies of the host population's dynamics can be initiated prior to the introduction (the "without" treatment) and then continued after the agent' s establishment (the "with" treatment) (Quezada, 1974; Dowell et al., 1979; Bellows et al., 1992a). 2. Geography may be used, where plots in one location with the agent present are contrasted to plots in similar but separate locations lacking the agent (e.g. Gould et al., 1992a,b). This is feasible chiefly with new agents that have not yet occupied their full potential range. This approach is less applicable to native or previously introduced agents, because sites having and lacking the agent are likely to differ in some factor of ecological importance to the agent. Contrasting life tables between the native home and the area of introduction (after establishment of a species) can be particularly helpful [e.g., winter moth in England (Varley & Gradwell, 1968; Hassell 1980) versus Nova Scotia (Embree, 1966)]. 3. Exclusion may be used in which some type of barrier is erected to deny the agent access to a portion of the pest population. Methods to create such barriers have been reviewed by Luck et al. (1988) and also in Chapter 9. Generally, natural enemies may be excluded from plots by the use of cages, mechanical barriers at plot edges, selective insecticides, or in some cases by hand picking, by the presence of dust, or by ants.

Each method (time, geography, exclusion) of creating the desired with and without natural-enemy condition has certain limitations that may potentially confound the interpretation of results. Contrasts structured on time (before and after studies) are frequently criticized, for example, on the basis that no two years are ever identical in terms of weather, etc., and hence results may differ because of features other than the presence or absence of the natural enemy. Contrasts based on geography may be criticized because sites that appear similar to the researcher may in fact differ in nonapparent yet important ways. This may be compensated for by utilizing a set of three or more sites for both the with and without treatments. This, however, may be beyond the resources of many research projects, especially those attempting to construct life tables at each study site. Exclusion-based contrasts are criticized because the means used as barriers often change the physical or chemical environment of the pest population in one treatment group (the without) but do not do so in the other treatment. Cages, for example, may increase insect development due to within-cage greenhouse effects and also may prevent emigration of the pest under study. Selective pesticides may alter reproductive rates of pests in treated plots, either directly or through changes in plant chemistry. For reviews of such biases in exclusion studies see Luck et al. (1988) and Van Driesche and Bellows (1996). In general terms, biases such as these are best controlled by the simultaneous use of two methods of establishing the desired with and without contrast. In such cases, each method (time, geography, exclusion) provides the researcher the opportunity to assess the degree of bias of the other method. For example, if, in terms of Fig. 2, the consequences of before and after contrasts are determined at

TIME

BEFORE INTRODUCTION

NATURAL ENEMY

>.. "r" ft..

AFTER INTRODUCTION

N1

N2

N3

N4

RELEASE AREAS


0.03% but 16 other compounds were highly toxic at concentrations levels -24 h postexposure to toxin). Ability to disperse and search.

a

e

reduced to such low levels that natural enemy populations are decimated by lack of prey or hosts or they are forced to emigrate (Boyce, 1936; Bartlett, 1964). This may be particularly serious when natural enemies are highly host specific (Heathcote, 1963). These actions result in natural enemy to pest ratios that favor the numerical increase of the pest. This problem has been suggested as a reason why natural enemies do not develop pesticide resistance as rapidly as their hosts (Georghiou, 1972; May & Dobson, 1986; Tabashnik, 1986; Chapter 24). Ingestion of Pesticide-Contaminated Hosts or Prey

Mortality of coccinellid predators such as Menochilus sexmaculatus (Fabricius), Coccinella undecimpunctata Linnaeus, and Scymnus syriacus Le Conte has been reported following consumption of aphids poisoned with malathion (Satpathy et al., 1968) and demeton (Ahmed, 1955). Herbert and Harper (1986) reported mortality of Geocoris punctipes (Say) nymphs that fed on Helicoverpa zea (Boddie) larvae injected with beta-exotoxin of Bacillus thuringiensis Berliner. When adult females of Bracon hebetor were exposed to larvae of the almond moth, Ephestia cautella (Walker), that had been treated topically with various insecticide dosages, parasitoid mortality increased with dosage (Press et al., 1981). Mortality or sedation occurred in all individuals of the jumping spider Phidippus audax (Hentz) that ate live third-instar H. zea larvae previously fed a wheat germ diet containing 40 ppm abamectin (Roach & Morse, 1988). Emerging adult endoparasitoids can suffer mortality from insecticide residues contacted as they bore through contaminated host integument, egg chorion, or scale covers (Plewka et al., 1975; Flanders et al., 1984; Delorme et al., 1985; Cohen et al., 1988).

CONSEQUENCES OF DISRUPTING BIOLOGICAL CONTROL Unilateral chemical control of arthropod pests can result in population explosions of both target and nontarget orga-

nisms due to various reasons including hormoligosis (Ferro, 1987; Risch, 1987), pesticide resistance (Georgihou, 1986; Metcalf, 1986), and the destruction of natural enemies (Ripper, 1956; Bartlett, 1964; Reynolds, 1971; Metcalf, 1986). The disruptive effects of pesticides on natural-enemy populations have been recognized for more than 100 years; Comstock (1880) noted that pyrethrum sprays against scale insects did more harm than good by destroying beneficial insects. Pest outbreaks resulting from the destruction of natural enemies are classified as pest resurgences and secondary pest outbreaks (pest upsets) (Barlett, 1964; van den Bosch et al., 1982). Numerous arthropod species including scale insects, aphids, whiteflies, leafminers, lepidopterans, tetranychid mites, and eriophyid mites often undergo resurgences and secondary pest outbreaks (Ripper, 1956; Reynolds, 1971). Resurgences and secondary pest outbreaks have been reported on such crops as cotton, rice, deciduous fruits, and citrus (Metcalf, 1986).

Resurgences Resurgences are characterized by a rapid numerical increase of a targeted pest population after use of a broadspectrum pesticide. Although biological control of the target pest may be only partly effective, the absence of biological control following pesticide treatment results in increased problems (van den Bosch et al., 1982). However, pesticide-induced reductions of natural-enemy populations may not always be the cause. Hardin et al. (1995) emphasize that efforts should be made to demonstrate a cause and effect relationship between any particular mechanism and resurgence. Conservation of natural enemies may conflict with the control of populations of major pests. This situation is frequently encountered when early-season pesticide applications disrupt biological control and commit the grower to chemical control for the remainder of the season (Havron et al., 1987). Examples from 14 crop systems including more than 23 pests (and associated natural enemies) that have exhibited or have high potential for pest resurgences are listed in Tables 2 and 3. Pesticide resistance

Chapter 13 TABLE 2

303

Enhanced Biological Control through Pesticide Selectivity

Examples of Ecological Selectivity by Modification of a Pesticide to Reduce Potential Pest Resurgences

Crop

Pest

Natural enemy

Pesticide used

Reference

Reduction of Pesticide Dosage

Alfalfa

Therioaphis maculata

Praon palitans Trioxys utilis Various predators

Demeton

Stern et al., 1959

Asquith et al., 1980

Apples

Panonychus ulmi

Stethorus punctum

Cyhexatin

Cereals

Aphids

Predators

Pirimicarb

Poehling & Dehne, 1984

Forest

Bupalus piniaria

Cratichneumon nigritarius

Tetrachlorvinphos Diflubenzuron

Wainhouse, 1987

Peas

Acyrthosiphon pisum

Coccinella septempunctata Syrphus vitripennis Chrysopa carnea

Pirimicarb

Hellpap & Schmutterer, 1982

Sorghum

Schizaphis graminum

Coccinelids

Various materials

Teetes et al., 1973

Soybeans

Plathypena scabra

Geocorids, spiders

Carbaryl, methomyl

Tumipseed, 1972

Soybeans

Helicoverpa zea

Geocoris punctipes Nabis spp.

Carbaryl

Tumipseed, 1972

Tobacco

Manduca sexta

Polistes spp.

TDE, endrin

Lawson et al., 1961

Alfalfa

T. maculata

P. palitans T. utilis

Mevinphos

Stem & van den Bosch, 1959

Alfalfa

Hypera postica

Bathyplectes curculionis

Methyl parathion

Wilson & Armbrust, 1970

Use of Nonpersistent Pesticides

in the primary pest and resurgence of that pest can be tightly coupled and may work synergistically (Hardin et al., 1995). However, Hardin et al. argue that insecticide resistance is not a mechanism underlying resurgence, but it may magnify the level of resurgence. Resurgences have been reported in natural ecosystems as well as agroecosystems (Turnock et al., 1976). Decimation of natural enemies of the European spruce sawfly, Diprion hercyniae (Hartig), caused by applications of DDT over a 3-year period in New Brunswick, Canada, resulted in a resurgence of the sawfly when pesticide applications were terminated (Neilson et al., 1971). In southwest Texas, insecticidal control efforts were associated with increased populations of the southern pine beetle, Dendroctonusfrontalis Zimmerman, due in part to elimination of predators (Vitre, 1971).

S e c o n d a r y Pest O u t b r e a k s Secondary pest outbreaks, or pest upsets, are characterized by the rapid numerical increase to pest status of a nontargeted, phytophagous arthropod population after use of a broad-spectrum pesticide applied for control of another pest in the ecosystem (van den Bosch et al., 1982). The nontarget pest is usually assumed to be under substantial or complete biological control until the pesticide reduces natural-enemy effectiveness. Examples from 10 crop systems including more than 14 pests (and associated natural ene-

mies) that have exhibited or have potential for pest upsets are listed in Table 4. Pesticides inducing pest outbreaks are generally those that are exceptionally toxic to the biological control agents involved but not to the pests (Bartlett, 1964). The most serious pest upsets are caused when pesticides decimate natural enemies without significant destruction of the host and persisting residues or repeated applications restrict subsequent natural enemy activity. In fresh-market tomatoes biological control of the agromyzid leafminer Liriomyza sativae B lanchard was disrupted by methomyl applications for the tomato fruit worm, H. zea, and the tomato pinworm, Keiferia lycopersciella (Walsingham), which attack the fruit (Johnson et al., 1980a, 1980b). Weekly pesticide applications for continuous protection of the fruit resulted in secondary outbreaks of the leaf miner due to destruction of its effective natural enemies. Indirect evidence of secondary pest outbreaks has been recorded in natural ecosystems. A pest upset of pine needle scale, Phenaecaspis pinifoliae (Fitch), on lodgepole and Jeffrey pines followed a malathion fogging program directed at mosquitoes in California (Luck & Dahlsten, 1975). Following 24 applications of malathion bait sprays to eradicate the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), in northern California, a 90-fold increase was observed in an endemic gall midge Rhopalomyia california Felt infesting coyote brush, Baccharis pilularis DC (ssp. consanguinea) (Ehler et al., 1984).

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M.W. Johnson and B. E. Tabashnik TABLE 3

Ecological Selectivity by Modification of Pesticide Application M e t h o d s to Reduce Potential Pest Resurgences

Pest

Crop

Pesticide used or application method or target site

Natural enemy

Reference

Temporal Discrimination

Alfalfa

Hypera postica

Bathyplectes curculionis

Carbofuran

Davis & Hoyt, 1979

Alfalfa

H. postica

B. curculionis

Methyl parathion

Wilson & Armbrust, 1970

Apples

Phyllonorycter blancardella

Apanteles ornigis

Oxamyl

Weires et al., 1982

Apples

Panonychus ulmi

Amblyseius fallacis

Various materials

Croft & Brown, 1975

Apples

Lymantria dispar

Apanteles melanoscelus

Dimilin

Granett et al., 1976

Grapes

Erythroneura elegantula

Anagrus epos

Various materials

AliNiazee & Oatman, 1979

Hops

Phorodon humuli

Anthocoris nemoralis

Dimefox, mephosfolan

Solomon, 1987

Pears

Psylla pyricola

A. nemoralis

Pyrethroids

Solomon, 1987

Tomatoes

Trialeurodes vaporariorum

Encarsia formosa

Oxamyl

Way, 1986

Wheat

Eurygaster integriceps

Trissolcus grandis

Various materials

Novozhilov, 1976

Vegetables

Pieris brassicae

Apanteles glomeratus

Various materials

Novozhilov, 1976

Vegetables

Plutella cruciferarum

Chorogenes spp.

Various materials

Novozhilov, 1976

Wheat

Sitobion avenae

Various predators

Benomyl

Powell et al., 1985

Apples

Tetranychus mcdanieli

Typhlodromus occidentalis

Tree periphery

Hoyt, 1969

Apples

Panonychus ulmi

Amblyseius fallacis

Tree periphery

Metcalf, 1972

Beans

Liriomyza trifolii

Oenonogastra microrhopalae

Granulars in soil

Oetting, 1985

Forest

Bupalus piniaria

Cratichneumon nigritarius

Outbreak epicenters

Wainhouse, 1987

Hops

Phorodon humuli

Anthocoris nemoralis

Soil drench

Solomon, 1987

Tobacco

Manduca sexta

Polistes spp.

Upper plant

Lawson et al., 1961

Tomatoes

Trialeurodes vaporariorum

E. formosa

Soil drench

Way, 1986

Citrus

Lepidosaphes beckii

Aphytis lepidosaphes

Strip treatment

Debach & Landi, 1961

Habitat Discrimination

Habitat Partitionment

Secondary pest outbreaks involve nontarget pests usually under substantial or complete biological control until pesticide applications reduce natural-enemy effectiveness. Here again, possible correlations between the effectiveness of a natural enemy based on its searching behavior and the potential to accumulate residues while searching must be considered. Even low levels of pesticide in the agroecosystem may be great enough to impair the searching abilities of the most effective natural enemies, which would lead to an increase in the nontarget pest. Bartlett (1964) suggested that pest outbreaks following treatments are often important indicators of the presence of efficient natural enemies. However, he pointed out that following an upset by naturalenemy elimination, normally less efficient or sometimes even rare species often gain temporary superiority by earlier ingress and may maintain a numerical advantage for long periods. The earliest influx of natural enemies may consist of the most mobile and seasonably abundant forms, or sometimes those species (frequently coccinellid predators) that are ordinarily attracted to high host densities. He sug-

gested caution in predicting natural-enemy efficiency strictly on temporary abundance, particularly following recovery from a pesticide upset.

TECHNIQUES TO REDUCE THE NEGATIVE IMPACT OF CHEMICALS ON NATURAL ENEMIES Crop Monitoring and Economic Thresholds Probably the best method for reducing the overall negative impact of chemicals on natural enemies is to avoid pesticide applications altogether. When pesticides are used in the management of pests they should be applied only when necessary and economically justifiable (Higley & Pedigo, 1996a). Decisions concerning the need for or suitability of a pesticide application require knowledge of the pest's impact on the crop and some method of monitoring the pest to determine when it may cause problems (Stem et

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Chapter 13 Enhanced Biological Control through Pesticide Selectivity TABLE 4

Crop

Ecological Selectivity by Modification of Pesticide Application Methods or Pesticide to Reduce Potential Secondary Pest Upsets

Primary pest

Secondary pest

Natural enemy

Pesticide used or application method or target site

References

Temporal Discrimination

Alfalfa

Hypera postica

Various species

Various species

Carbofuran

Davis & Hoyt, 1979

Apples

Dysaphis plantaginea

Panonychus ulmi

Stethorus punctum

Hull & Starner, 1983b

Apples

Various pests

P. ulmi

Amblyseius fallacis

Chloropyrifos Methidathion Diazinon Demeton

Apples Walnuts

Platynota idaeusalis

P. ulmi

Stethorus punctum

Cydia pomonella

Chromaphis juglandicola

Trioxys pallidus

Apples Cotton

Various pests

P. ulmi

A. fallacis

Tree canopy

Croft, 1975

Pectinophora gossypiella

Helicoverpa zea

Orius spp.

Lower plant canopy

Davis & Hoyt, 1979

Cotton Cotton

Anthonomus grandis

H. zea

Lygus spp.

H. zea Spodoptera exigua Trichoplusia ni

Various species Various species Various species Various species

Pheromone/trap crop Safflower trap crop

Lloyd et al., 1972 Mueller & Stern, 1974

Cucumbers

Thrips tabaci

Trialeurodes vaporariorum Tetranychus urticae

Encarsia formosa Phytoseiulus persimilis

Below plants

Pickford, 1983

Peanuts Peanuts Vegetables

Elasmopalpus lignosellus E. lignosellus

Various species Various species

Various species Various species

Trialeurodes vaporariorum Myzus persicae

Verticillium lecanii

Granulars in soil Directed spray Soil application

Adkisson, 1972 Adkisson, 1972 Way, 1986

Liriomyza spp.

Chrysonotomyia punctriventris Ganaspidium utilis

Trap crop

Johnson, 1987

Fenvalerate Various materials

Croft, 1975 Hull et al., 1985b Riedl et al., 1979

Habitat Discrimination

Fungusspecies

Watermelon Dacus cucurbitae

Habitat Partitionment

Apples

Platynota idaeusalis

P. ulmi

Stethorus punctum

Alternate-row middle

Hull et al., 1983

Citrus

Lepidosaphes beckii

Aonidiella aurantii

Aphytis spp

Strip treatment

DeBach et al., 1955

Apples Apples Pears

C. pomonella

Tetranychus mcdanieli

Typhlodromus occidentalis

P. ulmi

S. punctum

C. pomonella

Various mite species

T. occiclentalis

Azinphos-methyl Various materials Azinphos-methyl

Hoyt, 1969

P. idaeusalis

Apples

P. idaeusalis

Reduction of Pesticide Dosage

Hull & Beers, 1985 Westigard, 1971

Selective Insecticides with Reduced Rates of Broad-Spectrum Compounds

P. ulmi

al., 1959). On watermelon in Hawaii, L i r i o m y z a spp. are present in plantings during more than 95% of the growth cycle but densities surpass treatment levels less than 7% of the time (Johnson et al., 1989). In comparison, melon aphid, A p h i s g o s s y p i i Glover, is present less than 80% of the time, but densities may surpass treatment levels on more than 35 % of sample dates. An understanding of the effectiveness of natural enemies is essential to avoid applying pesticides when biological control is adequate (Wilson, 1985). Unfortunately, few monitoring systems have been developed that consider the

S. punctum

Azinphos-methyl Methyl parathion (E)

Hull & Starner, 1983a

influence of natural enemies (Flaherty et al., 1981; Li, 1982; Tanigoshi et al., 1983; Wilson et al., 1984). One of the first systems developed was used to predict the necessity of acaricide treatments for European red mite suppression on apple. Treatment decisions are based on the relative densities of the spider mite and its predator A. f a l l a c i s (Croft, 1977). Using predator to prey ratios, the probability of biological control within a week's time is estimated; acaricide applications are recommended only when biological control is estimated to be inadequate. The impact of pesticide treatments on natural enemies of secondary pests

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M.W. Johnson and B. E. Tabashnik

should also be considered when decisions are made to treat for primary pests. Pest management manuals produced for alfalfa hay (Flint, 1985c), almonds (Flint, 1985b), cotton (Flint, 1984), tomatoes (Flint, 1985a), and walnuts (Flint, 1987) advise growers of various natural enemies that should be conserved to avoid secondary upsets. Several parameters must be considered to permit a pesticide to be used in the most efficient and least disruptive manner. One must first define the biological target (Hull & Beers, 1985). Prerequisites for defining the target are (1) identification of all pests and associated natural enemies that may be affected by pesticide applications in a given habitat, (2) knowledge of the behavior and microhabitats of targeted pests and associated natural enemies, (3) knowledge of the dosage responses of pests and associated natural enemies to available pesticides, and (4) knowledge of all feasible application methods for each compound. This information will provide the basic foundation for maximizing benefits derived from pesticide selectivity. After the biological target is defined, one must then determine options available for the most efficient use of a pesticide with minimal nontarget effects. Vorley & Dittrich (1994) state that the "IPM fit" of a pesticide can be defined by the level of control provided for at least one target pest, the selectivity to key natural enemies, and the risk of resurgence of secondary pests.

Pesticide Selectivity Bartlett (1964) defined pesticide selectivity as the capacity of a pesticide treatment to spare natural enemies while destroying the target pest. Selectivity differs from specificity, which is the capacity of a compound to cause extraordinarily high mortality in a particular species. Specificity may be considered as an extreme type of selectivity. Selectivity is a relative measure expressed as the natural enemy to pest ratio produced by one pesticide treatment compared with the ratio produced by a reference pesticide treatment (Bartlett, 1964). Many authors divide pesticide selectivity into physiological selectivity and ecological selectivity based on the mechanism by which a pesticide treatment causes differential mortality to pests and their natural enemies (Metcalf, 1972, 1982; Watson, 1975; Newsom et al., 1976; Hull & Beers, 1985). Ecological selectivity results from differential exposure of pests and natural enemies to a pesticide. Physiological selectivity results from physiological differences in susceptibilities of pests and associated natural enemies to a pesticide as discussed later. Such physiological differences in the natural enemy may be inherent or may be a product of laboratory or field selection. Strategies used to develop selective techniques of pesticide use are dependent on the system under consideration.

Physiological Pesticide Selectivity Development of physiologically selective compounds is reviewed by Mullin and Croft (1985) and Croft (1990d). Effective use of physiologically selective compounds to enhance biological control is dependent on several factors including the type of pests (primary, secondary) targeted for control and relative levels of pesticide resistance in nontargeted pest and natural-enemy species. When pest resurgence is the primary consideration, the major objective of physiological selectivity is to manipulate the natural enemy to pest ratio to favor the natural enemies by differential mortality of the pest. However, high pest mortality is counterproductive if surviving natural enemies starve or emigrate from the treated crop in search of prey or hosts (Smith, 1970; Tabashnik, 1986). Such loss of natural enemies may also produce a result similar to pest resurgence. Therefore, sucessful prevention of pest resurgences using physiological selectivity requires that a significant portion of the pest population survives the treatment. The pest density that can be tolerated is a function of many factors including the economic threshold, densities of pest and natural enemies following the pesticide treatment, numerical responses of the pest and natural enemies, host crop, and relevant environmental parameters (temperature, humidity, etc.). Few current pest management recommendations include intentional retention of pest populations following treatment. When secondary pest outbreaks are the foremost concern and the primary pest lacks effective natural enemies, survival of the primary pest after treatment is less important than a potential resurgence problem. In situations where the secondary pest exhibits pesticide resistance to a wide range of compounds, it will generally be preferable to use compounds with high specificity to control the primary pest. This tactic avoids destruction of the secondary pest's natural enemies and reduces further development of resistance in the secondary pest. Unfortunately, current industrial development and production of selective compounds is limited due to small market demand, developmental costs, and potential investment losses if targeted species develop pesticide resistance (Newsom et al., 1976; van Emden & Peakall, 1996). If a mechanism had been established in the 1970s to foster development of selective pesticides by assisting manufacturers to meet regulatory requirements, perhaps selective compounds would be more widely used in agriculture now (National Research Council, 1996). Efforts have been made by the Working Group on Pesticides and Beneficial Organisms, International Organization for Biological Control, West Palearctic Regional Section (IOBC/WPRS), to identify registered pesticides (acaricides, fungicides, insecticides, herbicides) and plant growth regulators that have selective properties when used at recommended field rates (Franz et al., 1980; Hassan et

Chapter 13

Enhanced Biological Control through Pesticide Selectivity

al. 1983, 1987, 1991). Hassan (1985, 1989) reviewed standard assay techniques for analyzing the side effects of pesticides on biological control agents including parasitoids, predators, and a fungal pathogen. These assay techniques are used by the IOBC/WPRS Working Group to identify physiologically selective pesticides. Because no single assay provides sufficient information, a series of sequential tests are used to analyze fully the potential detrimental effects of pesticides. These tests include an initial laboratory test, semifield tests, and a field test (Hassan, 1985). Initial laboratory assays use fresh, dry pesticide residues deposited on glass, leaf, or soil surfaces. Compounds found harmless to specific biological control agents in the laboratory test are not subjected to further testing. Semifield tests include an initial toxicity test and a residue persistence test. Initial toxicity tests consist of applying pesticides to natural materials in the field (protected from direct exposure to sunlight and precipitation) or under simulated field conditions in an environmental chamber. In initial toxicity tests, natural enemies are exposed to treated plants or soil, after which mortality and beneficial capacity are assessed. Pesticide impact on a natural enemy's beneficial capacity is defined as the reduction in parasitism (for parasitoids)or oviposition (for predators) of exposed insects compared with untreated controls. In field tests, effects of field-applied pesticides on beneficials are determined by exposing natural enemies to weathered residues on treated substrates. Field tests are designed according to the crop inhabited by the natural enemy and the timing and number of pesticide treatments used in standard agricultural practices. Compared with most conventional assays used for pest and beneficial species (Theiling & Croft, 1988), the IOBC/ WPRS Working Group tests differ significantly with respect to pesticide exposure rates, exposure periods, and assessment of pesticide impact on the beneficial capacity of the natural enemy. Exposure rates are based on recommended commercial application rates. Exposure periods normally range from one to several weeks (Hassan, 1985) as compared with the short exposure periods (24 to 48 h) used in most conventional assays to determine lethal concentrations or dosages (Theiling & Croft, 1988). Estimates of acute mortality do not provide a complete assessment of the negative impact of pesticides on biological control agents due to the effects of sublethal dosages on longevity, fecundity, and behavior (Wright & Verkerk, 1995). Pesticides are categorized depending on reductions in beneficial capacity of the natural enemy: < 50% = harmless; 50 to 79% = slightly harmful; 80 to 90% = moderately harmful; and > 99% = harmful (Hassan, 1985). The IOBC/WPRS Working Group has evaluated more than 60 compounds involving 19 natural enemy species (Franz et al., 1980; Hassan et al., 1983, 1987). Twenty-five compounds have been identified as relatively selective to at least one or more natural enemies based on their toxicity

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and persistence (Hassan et al., 1987). The IOBC/WPRS methods may provide the best way to identify currently available physiologically selective compounds for use in pest management programs. Pesticide selectivity has been achieved predominantly by using insecticides to which biological control agents are naturally tolerant (Mullin & Croft, 1985). This approach is restricted by the limited commercial availability of selective compounds (Newsom et al., 1976; Mullin & Croft, 1985). Some negative impacts of insecticides on beneficials may be reduced by laboratory selection for insecticide resistance to those compounds not naturally selective for natural enemies (Croft & Morse, 1979; Hoy, 1985; Johnson & Tabashnik, 1994; Chapter 12).

Laboratory Selection for Resistance Laboratory selection for increased pesticide resistance in natural enemies has long been advocated (DeBach, 1958) but only relatively recently has been successful with arthropod predators (Hoy, 1987). Phytoseiid mites among this group include Phytoseiulus persimilis Athias-Henriot, Amblyseius fallacis, A. nicholsi Ehara & Lee, and Typhlodromus (Metaseiulus) occidentalis (Nesbitt) (Hoy, 1987; Huang et al., 1987). Probably the most successful results of laboratory selection have occurred in T. occidentalis resistance to carbaryl, methomyl, dimethoate, permethrin, and fenvalerate (Hoy, 1985). Selected strains of T. occidentalis are now commercially produced for mass releases in almond and apple orchards (Headley & Hoy, 1987). An insect predator, the common green lacewing, Chrysoperla carnea, also has been selected for carbaryl resistance (Grafton-Cardwell & Hoy, 1986). Studies conducted using parasitoids in selection programs have had limited success compared with that for predators (Hoy, 1987; Johnson & Tabashnik, 1994). Several attempts have been made to artificially generate resistant parasitoids (Pielou & Glasser, 1952; Robertson, 1957; Adams & Cross, 1967; Abdelrahman, 1973; Havron, 1983; Hsieh, 1984; Delorme et al., 1985). Although moderate responses to selection have been obtained, in most cases the selection response has not been adequate to incorporate the selected strain into an IPM program. Selection conducted on colonies established from field populations of Aphytis melinus, a parasitoid of the California red scale exhibiting low levels of resistance to various insecticides, produced a parasitoid strain approximately 20 times more resistant to carbaryl than did a standard susceptible colony (Rosenheim & Hoy, 1988a, 1988b). Azinphos-methyl resistance was increased 7.5-fold in the parasitoid Trioxys pallidus Haliday, which attacks the walnut aphid, Chromaphis juglandicola Kaltenbach, in California (Hoy & Cave, 1988). Efforts are currently underway to implement laboratory-selected strains of A. melinus (Rosenheim & Hoy,

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M.W. Johnson and B. E. Tabashnik

1988b; Spollen & Hoy, 1992) and T. pallidus (Hoy & Cave, 1988; Hoy et al., 1990, 1991) in commercial IPM programs, but results are still preliminary. More detailed discussion of genetic improvement of natural enemies is provided (Chapter 12).

Ecological Selectivity Due to the limited number of physiologically selective compounds available, greater potential for achieving pesticide selectivity appears to be through the development and use of ecologically selective strategies (Davis & Hoyt, 1979). Ecological selectivity can be accomplished by modification of either the pesticide or the delivery methods (Hull & Beers, 1985). Ecological selectivity is achieved by reducing the detrimental nontarget effects of broad-spectrum (not physiologically selective) pesticides and thereby conserving naturalenemy populations. Many changes required to make compounds more ecologically selective must be accomplished during the development or manufacturing phases of the materials. Properties that may be altered include degree of systemic action, formulation, encapsulation, and overall persistence (Newsom et al., 1976; Graham-Bryce, 1987). Growers' abilities to employ ecologically selective tactics through alteration of the physical and chemical properties of the toxicant and its carriers are limited by the number of selective products marketed by the chemical industry. However, growers can modify the dosage or application rates. Nonpersistent compounds also can be used to limit the impact of pesticide residues on natural-enemy populations. Reduction of Application Rates

Perhaps the most readily accomplished modification of a material is the reduction of the application rate. Because broad-spectrum compounds are biologically active against a wide range of organisms, label rates may be higher than required for effective control of some pests. Turnipseed et al. (1974) reported that reduced rates of carbaryl and methyl parathion effectively controlled bean leaf beetle [Cerotoma trifurcata (Forster)], velvet bean caterpillar (Anticarsia gemmatalis Htibner), green cloverworm [Plathypena scabra (Fabricius)] and corn earworm [Helicoverpa zea (Boddie)] infesting soybeans. Although reduced rates may provide only partial control of a primary pest, benefits may be derived from conservation of the natural enemies. Pest resurgences can be reduced if treatments for the primary pest are properly timed, target sites are restricted, and optimal application tactics are employed (Way, 1986). If the primary pest has no effective natural enemies and its economic threshold is extremely low, then it may not be feasible to reduce pesticide dosage to conserve the natural enemies of secondary pests. In this situation, primary pest control may be possible if applications are timed to coin-

cide with the presence of highly susceptible life stages of pests with discrete generations (see Table 4). Hull and Beers (1985) reported that insecticide applications for the tufted apple bud moth, Platynota idaeusalis (Walker), on apple could be reduced approximately 75% below label dosage rates if properly timed. This reduction in pesticide rate allowed Stethorus punctum (Le Conte) to control the European red mite. Selectivity can also be achieved by combining reduced dosages of broad-spectrum materials with physiologically selective compounds or synergists. Hull and Starner (1983a) demonstrated effective control of P. idaeusalis on apple when using either encapsulated methyl parathion or azinphos-methyl in combination with low rates of permethfin or fenvalerate (see Table 4). These combinations suppressed the leafroller without destroying populations of S. punctum necessary for European red mite conrol. Laboratory studies showed that when the larvicide Bacillus thuringiensis was combined with reduced dosages of binapacryl, tricyclohexyltin hydroxide, or fentin hydroxide, selective mortality of the diamondback moth, Plutella xylostella (Linnaeus), was achieved with no toxicity to its parasitoid Thyraeella collaris Gravely (Hamilton & Attia, 1977). Pyrethroids tend to be more toxic for Helicoverpa zea than for the common green lacewing, Chrysoperla (Chrysopa) carnea (Rajakulendran & Plapp, 1982a). When cypermethrin, tralomethin, fluvalinate, and flucythrinate were each combined with chlordimeform at a ratio of 1 part pesticide to 10 parts chlordimeform, the selectivity was significantly increased for H. zea as compared with the pyrethroids alone (Rajakulendran & Plapp, 1982b). More research is needed on the potential value of reducing application rates of broad-spectrum compounds alone and in combination with physiologically selective compounds or synergists to reduce their impact on natural enemies (Hull & Beers, 1985). Nonpersistent Pesticides

Persistence of a given pesticide is partially a function of the rate applied (Busvine, 1971). Persistent pesticide residues can reduce pest and natural-enemy populations to low levels. Residues of carbaryl and carbophenothion applied to soybeans caused high mortality of Mexican bean beetle, Epilachna varivestis Mulsant, 21 days following treatment (Flanders et al., 1984). High pest mortality can indirectly reduce natural-enemy efficacy if surviving natural enemies starve or emigrate from the treated crop habitat in search of hosts. Compounds that have long-term residual activity are usually detrimental to natural enemies that disperse into an area shortly after treatment or survive an initial pesticide treatment in a protected stage or refuge (Bartlett, 1964; Flanders et al., 1984). When applied at field rates, temephos and triazophos residues require approximately 21 days to lose their activity against Aphytis africanus Quednau that attacks the California red scale, Aonidiella aurantii (Mas-

Chapter 13 EnhancedBiologicalControl through Pesticide Selectivity kell) (Schoones & Giliomee, 1984). Acephate residues on citrus caused mortalities in excess of 50% for more than 14 days in the predatory mite Eusieus stipulatus Athias-Henriot, the California red scale parasitoid Aphytis melinus, and the mealybug destroyer Crytolaemus montrouzieri (Bellows et al., 1985). Parasitism of European corn borer [Ostrinia nubilalis (Htibner)] eggs by Trichogramma nubilale Ertle & Davis was reduced more than 20 days following carbaryl treatment on green pepper (Tipping & Burbutis, 1983). Compounds that maintain residual activity for long periods, relative to the life cycles of affected natural enemies, are not appropriate for integrated programs. Many investigations on the impacts of pesticides on natural enemies have focused on the immediate or contact toxicity of the pesticide (Theiling & Croft, 1988). Unfortunately, little quantitative information exists describing the relationship between residue dissipation and postapplication survival of natural enemies (Bellows et al., 1985). As stated previously, current work by the IOBC/WPRS Working Group on Pesticides and Beneficial Organisms involves screening of the long-term effects of pesticide residues on natural enemies (Hassan, 1985). Residues are considered harmful to parasitoids when parasitism rates are reduced more than 30%. In approximately 64% of the natural-enemy-pesticide combinations examined by the Working Group, pesticides applied at standard rates were highly toxic more than 16 days after application (Hassan et al., 1987). In tests with the whitefly parasitoid Encarsia formosa, amitraz (insecticide), tetradifon (acaricide), and chinomethionate (fungicide) had harmful effects on initial contact but minimal residual effects 5 days after application (Hassan et al., 1987). Pirimicarb in granular form was highly toxic on contact with Trichogramma spp., but harmless 5 days after application (Hassan et al., 1987). Singh (1989) lists several "relatively safe" pesticides used in integrated control programs.

Modification of Application Methods Great progress in reducing the negative impacts of pesticides on natural enemies has been achieved through the modification of delivery or application methods. Strategies employed include temporal discrimination, habitat discrimination, and habitat partitionment. In temporal and habitat discrimination, pesticides are applied when the natural enemies are absent or in low numbers due to either seasonal or cyclic occurrence (temporal asynchrony: Croft, 1990e) or to habitat preferences (spatial asynchrony: Croft, 1990e), respectively. Habitat partitionment involves the restriction of pesticide applications to limited sections of a planting or orchard to establish refuges in which natural enemies are protected.

Temporal Discrimination Pest resurgences and upsets can be avoided by applying pesticides when biological

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control agents do not occupy the habitats or crop systems commonly shared with the targeted pest (see Tables 3 and 4). This is practiced in temperate climates where many pests establish populations in crop hosts in the spring prior to associated natural enemies (Davis & Hoyt, 1979; Powell et al., 1985; Solomon, 1987). Bartlett (1964) suggested that pesticide treatments should be eliminated when natural enemies are present and that pest destruction should be maximized when natural enemies are absent or less efficient. However, drastic reductions in prey or host populations prior to immigration of natural enemies may hamper later biological control of targeted pests. Hoyt (1969) reported that prebloom applications of oxythioquinox to control Tetranychus mcdanieli McGregor on apple caused such low prey levels that its predator Typhlodromus occidentalis suffered mortality due to starvation and did not increase to an effective density until late in the season. This led to economically significant populations of Tetranychus mcdanieli. Natural enemies that share the targeted pest's habitat at the time of application might avoid mortality if they are inactive or are in a relatively resistant stage (Davis & Hoyt, 1979). Conservation of the braconid Apanteles ornigis Weed can be achieved by applying oxamyl treatments for spotted tentiform leafminer on apple prior to parasitoid emergence in the spring (Weires et al., 1982). Granett et al. (1976) reported that early-season treatments of diflubenzuron for gypsy moth control on apple inhibited the emergence of the endoparasitoid A. melanoscelus (Ratzeburg) from moth hosts due to the presence of susceptible stages at application time. However, later season treatments selectively killed gypsy moth larvae, but allowed survival of mature parasitoids ready to emerge.

Habitat Discrimination When natural enemies are present in a crop, it is often possible to conserve their populations by directing pesticide applications to those habitats that the pests occupy preferentially compared with the biological agents (see Tables 3 and 4). Pest resurgences involving tetranychid mites on deciduous fruit crops have been avoided by applying pesticides only to the peripheral areas of the tree canopy and thereby preserving the phytoseiid predators commonly found deep inside the canopy (Hoyt, 1969; Metcalf, 1972). Pesticide treatments frequently can be limited to those vertical or horizontal strata of a plant in which the highest ratio of targeted pests to natural enemies exists. Endrin and TDE applications directed at tobacco hornworm [Manduca sexta (Johannson)] larvae feeding on the upper portions of tobacco plants conserved Polistes spp. wasps that prey on M. sexta larvae on the lower tobacco leaves (Lawson et al., 1961). Treatments for the pink bollworm, Pectinophora gossypiella (Saunders), directed at the lower leaf canopy of cotton allow survival of anthocorid predators (Orius spp.) that attack Heliothis eggs and larvae (Davis & Hoyt, 1979). When high

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infestations of Thrips palmi Kamy on watermelon are limited to the vine tips, oxamyl applications may be directed there, thus conserving parasitoids of Liriomyza leafminers that are found predominatly in the basal foliage canopy (Johnson, 1986; Lynch & Johnson, 1987). Polyphagous pest species often have highly mobile adult stages that move among adjacent plant hosts, both domestic and wild (Nishida & Bess, 1957). This behavior can be exploited to reduce natural-enemy mortality by directing pesticide applications at trap crops. Parasitoids that attack Liriomyza leafminers infesting watermelon foliage can be suppressed by insecticides applied directly to the crop for control of melon fly, Dacus cucurbitae Coquillet. However, com (Zea mays Bonaf.) borders planted adjacent to watermelon attract melon flies seeking a resting spot. Once in the com trap crop, melon fly control is achieved when flies ingest malathion-treated bait. This reduces amounts of pesticides applied directly to watermelon and thereby conserves the leafminer parasitoids (Johnson, 1987). Habitat discrimination can be achieved using baits and treated seeds because target pests usually seek the treated substrate and mortality occurs following contact or ingestion (Newsom et al., 1976). Due to the low chemical dosages required, natural enemies are spared. Newsom et al. (1976) reviewed the advantages of seed treatments versus broadcast applications of pesticides. These included cost reduction as a function of insecticide rates used, no additional costs for application methods or equipment, reduced environmental pollution, minimal contact with nontarget species, and reduced selection pressures for the development of pesticide resistance. Pest species controlled using seed treatments include seed maggots, rootworms (Newsom et al., 1976), wireworms (Metcalf, 1982), aphids (Reynolds et al., 1957), and thrips (Reynolds, 1958). Baits have been used extensively to control pest species of ants such as the imported fire ants, Solenopsis spp. (Anonymous, 1972). Baits are removed from the soil surface rapidly by ants and there is thus limited exposure to nontarget species (Newsom et al., 1976). Unfortunately, some nontarget effects have been recorded with the use of mirex for ant control (Harris & Bums, 1972). Other insects controlled by the use of baits include tephritid fruit flies (Steiner et al., 1965, 1970), leaf-cutting bees (GrahamBryce, 1987), grasshoppers, cutworms, armyworms, and crickets (Metcalf et al., 1962). Unique approaches to habitat discrimination may be developed based on the physical properties of a compound or its formulation. Systemic materials offer great potential for the control of foliage pests without exposing natural enemies to chemical residues on the plant surface. Suppression of greenhouse whitefly on small tomato plants can be achieved with oxamyl applied as a soil drench without directly affecting subsequent releases of the whitefly paras-

itoid Encarsia formosa (Way, 1986) (see Table 3). Soil drenches of dimefox or mephosfolan can be used on hops for early-season control of the damson hop aphid, Phorodon humuli (Schrank), without disrupting later biological control provided by the anthocorid Anthocoris nemoralis (Linnaeus) (Solomon, 1987). Aldicarb, oxamyl, and disulfoton granules applied to potting media for control of Liriomyza trifolii (Burgess) on beans did not reduce parasitism by the braconid Oenongastra microrhopalae (Ashmead) (Oetting, 1985). Adkisson (1972) reported that use of granular insecticides in peanuts for control of the lesser cornstalk borer, Elasmopalpus lignosellus (Zeller), was effective and reduced potential problems with the approximately 40 secondary pests on peanuts. Habitat discrimination has great potential for conserving natural enemies, but this tactic requires a good understanding of the habitat preferences of pests and natural enemies. In addition, variation in habitat preferences correlated with plant phenology and seasonal changes must be determined. This is clearly demonstrated by the seasonal movement patterns of the predatory mite Amblyseius fallacis in apple orchards in Michigan. Spring populations (April to early June) of the predator are found in the ground cover beneath apple trees where they prey on the two-spotted mite, Tetranychus urticae Koch. Around mid-June, A. fallacis enters the tree canopy to attack the European red mite, Panonychus ulmi (Koch), and other tetranychid species (Croft, 1975). Early-season populations of the predator may be conserved if insecticide sprays for San Jose scale, oyster shell scale, apple aphid, rosy apple aphid, and woolly apple aphid are limited to the apple tree canopy prior to the movement of A. fallacis into the apple foliage canopy. Understanding the habitat preferences of A. fallacis has been a key component in apple pest management. Habitat Partitionment Temporal and habitat discrimination cannot be used when targeted pests and natural enemies are present in identical or highly overlapping habitats or when it is impossible to limit pesticide application to specific habitats. However, it may be possible to establish refuges in a crop in which natural enemies may be protected from pesticide applications. This can be done either by using spot treatments (Bartlett, 1964) or by partitioning a crop into sections and applying treatments to a limited number of the total sections at any one time (Hull & Beers, 1985). Both methods can help to prevent pest resurgences and secondary pest upsets. Many pests (aphids, tetranychid mites) have clumped distributions within their host crops (Southwood, 1978). This can lead to high pest densities confined to small areas of a total planting or orchard. Natural enemies in a planting or an orchard may be conserved by using spot treatments in which pesticide applications are limited to areas where

Chapter 13 EnhancedBiologicalControl through Pesticide Selectivity the pest has surpassed the economic threshold and the pest to natural enemy ratio is unfavorable. Conservation of natural enemies by partitioning a crop into uniformly distributed sections and treating only a portion of the sections at any one time has been used successfully in citrus and deciduous fruit orchards (Hull & Beers, 1985). This method, referred to as strip treatment, was used in citrus to reduce pest resurgences of the purple scale, Lepidosaphes beckii (Newman) (DeBach & Landi, 1961) (see Table 3) and secondary pest upsets of the California red scale, Aonidiella aurantii (DeBach et al., 1955) (see Table 4). Orchard rows were divided into groups of three pairs; each first pair in each group was treated with oil sprays for purple scale control. After 6 months the second pairs were treated, and 6 months later the third pairs were treated. This treatment pattern reduced total natural-enemy mortality and allowed safe dispersal of parasitoids of L. beckii and A. aurantii from untreated to treated sections after oil residues dissipated. On apples in Pennsylvania, more than 95% of all pesticides are applied using the alternate-row middle method (Lewis & Hickey, 1964; Hull et al., 1983). Pesticides are applied to every other orchard row pair on a 7- to 9-day cycle. This method is effective in reducing secondary upsets of the European red mite (Hull et al., 1983) (see Table 4). Although most common in orchard crops, this technique has good potential in crops with relatively long growth cycles such as alfalfa and cotton.

CONCLUSIONS Significant reductions in the the negative impact of chemicals on natural enemies would be achieved if pesticides were applied only when necessary. This requires development of economic thresholds and sampling programs along with evaluations of biological control effectiveness. Economic thresholds should be a cornerstone of every IPM program (Higley & Pedigo, 1996a). However, relatively few thresholds exist compared with the number of crop pests for which chemicals are applied (Poston et al., 1983; Peterson, 1996). More studies are needed on yield responses of plants to arthropod injury so that economic thresholds (warning thresholds, action thresholds, density treatment levels) can be developed to reduce unnecessary pesticide use. Implementation of economic thresholds will require monitoring programs that estimate population densities of both the pest and its natural enemies (Higley & Pedigo, 1996b). When pesticides are applied, their direct and indirect effects can disrupt biological control. Acute mortality is a well-documented direct effect of pesticides on natural enemies. Estimates of acute mortality alone, however, do not

31 1

provide a complete assessment of the direct impact of pesticides on natural enemies because longer term, sublethal effects can also be important. Sublethal effects of pesticides can have a negative impact on natural enemy searching behavior. This is significant because efficient searching behavior is essential to the effectiveness of biological control agents. In addition, natural enemy populations can suffer indirect effects of pesticides through ingestion of contaminated hosts or prey and reduction of host and prey populations needed for parasitism and food, respectively. Of these factors, short-term mortality and reduction in host or prey populations probably have the greatest impact. Due to cumulative uptake of toxins, biological control agents that are highly mobile and efficient searchers may be at a disadvantage compared with their less mobile competitors when pesticide residues are present. Studies are needed to determine if acquisition of pesticide residues in treated habitats by natural enemies is correlated with their mobility and searching efficiency. Data now exist that show pesticide-induced repellency can reduce searching efficiency (Campbell et al., 1991; Longley & Jepson, 1996). A fuller understanding of these phenomena are essential for integration of biological and chemical controls. The IOBC/WPRS Working Group on Pesticides and Beneficial Organisms, together with other workers, has made significant progress in identifying available compounds that can be used in integrated programs. Registration of pesticides should include tests on their impact on natural enemies commonly found in the crop systems where materials will be applied. Resulting information should be provided on pesticide labels. Without this information, one cannot make intelligent pesticide selections. In addition to the type of information that the IOBC/WPRS Working Group has provided, data are needed on the impact of pesticides on natural enemy populations from different areas. Studies have shown that natural enemy responses to pesticides vary with locality. This information would allow a grower to select the least disruptive pesticide for use in integrated programs and would also provide information on the ability of natural enemies to develop pesticide resistance. Greater efforts are needed to develop additional ecologically selective techniques in the areas of temporal and habitat discrimination and habitat partitionment. This will require more basic studies of the ecology of pests and the associated natural enemies to fully utilize ecological selectivity. Significant progress has been made in the integration of chemical and biological controls over the last 30 years. However, progress to date is insufficient considering the wide range and number of crop systems that still rely heavily on chemicals for pest suppression. The need to further develop strategies to reduce the pesticide impact on natural

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enemies will increase as problems with pesticide resistance increase and as more attention is directed toward the reduction of chemical use in agriculture.

Acknowledgments The thoughtful comments of J. Rosenheim and L. LeBeck were appreciated. This work was supported by USDA grants HAW00945 and HAW00949. This is Journal Series No. 3342 of the Hawaii Institute of Tropical Agriculture and Human Resources.

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[14[ Environmental Management to Enhance Biological Control in Agroecosystems D. K. LETOURNEAU

M. A. ALTIERI

Department of Environmental Studies University of California Santa Cruz, California

Division of Insect Biology University of California Berkeley, California

INTRODUCTION

Funderburk, 1985; van Emden, 1988; Andow, 1991; Altieri et al., 1993; Tonhasca & Byrne, 1994; Altieri, 1994; Wratten & Van Emden, 1995). In the last 20 years, the majority of efforts have been directed at analyzing the effects of reduced tillage and vegetational diversification of agroecosystems. The effects of pest resistant varieties on the suitability of hosts or prey for natural enemies have also been studied. Research is targeting transgenic plants (Johnson & Gould, 1992; Johnson, 1997; Riggin-Bucci & Gould, 1997) to evaluate their compatibility with biological control agents. Research on other types of cultural manipulation such as strip harvesting, trap cropping, and use of nests or artificial shelter has been minimal, with the exception of advances in the use of food sprays (Hagen, 1986) and kairomones (Lewis et al., 1976; Nordlund et al., 1981a, 1981b, 1988; Lewis & Martin, 1990; Metcalf, 1994) to enhance the activity of specific natural enemies. A virtual explosion of literature reporting the effects of multiple cropping systems on insect dynamics has emerged (Root, 1973; Litsinger & Moody, 1976; Perrin, 1977; Altieri et al., 1978; Perrin & Phillips, 1978; Bach, 1980a, 1980b; Risch, 1980, 1981; Andow, 1983b; Letourneau & Altieri, 1983; Altieri & Liebman, 1986; Andow, 1991; Parajulee et al., 1997; Skovgard & Pats, 1996). This accumulated information provides a basis for designing crop systems with vegetational attributes that enhance reproduction, survival, and efficacy of natural enemies. Unfortunately, because agricultural land use is dictated mainly by economic forces, pest control plans are seldom made on the basis of habitat management. Economies of scale that dominate the agricultural sector in developed countries allow farmers to reduce unit production costs by increasing farm size and by becoming more specialized. For this rea-

efficacy of parasitoids and predators as agents of biological control depends on conditions set by production technologies such as varietal development, cropping systems, tillage practices, and chemical inputs. Yet trends in agriculture over the last several decades, which include decreasing environmental heterogeneity, increasing fertilizer and pesticide input, increasing mechanization, and decreasing genetic diversity (USDA, 1973; Bottrell, 1980; Whitham, 1983; Altieri & Anderson, 1986; Levins, 1986; Giampietro, 1997), create agricultural environments that pose serious impediments to pest population regulation by natural enemies. In particular, drastic reductions in plant biodiversity and the resulting epidemic effects can adversely affect ecosystem function with further consequences on agricultural productivity and sustainability (Fig. 1). The development and current acceptance of integrated pest management (IPM) programs, the cumulative restrictions and bans on various pesticides, and the growing concerns about pesticide contamination and increased production costs are among the reasons for increasing research efforts toward long-term alternatives and supplements to chemical insecticides. Since van den Bosch and Telford (1964) wrote their pioneering chapter describing habitat modifications to encourage satisfactory biological control of insect pests in agroecosystems, numerous articles have appeared documenting the importance of manipulating the environmental properties of crop fields to make them more favorable to natural enemies and less amenable for insect pests (van Emden & Williams, 1974; Price & Waldbauer, 1975; Perrin, 1980; Cromartie, 1981; Thresh, 1981; Altieri & Letourneau, 1982, 1984; Risch et al., 1983; Herzog &

HandbookofBiologicalControl

319

Copyright 9 1999 by Academic Press. All rights of reproduction in any form reserved.

320

D.K. Letourneau and M. A. Altieri

AlterationofEcosystemFunctionI (e'g"lack~ iaturalc~176 I ArthrR;ddBii~ pR:dUBCtioinn

[

l

I

I~ HabitatDestrucAi:nl:bdity[

I Agricultural IntensificationI andSpecialization FIGURE 1 Lines of influence between intensification, arthropod biodiversity, and properties of agricultural ecosystems.

son, environmental manipulation strategies with demonstrated effectiveness in experimental systems, such as cotton/alfalfa strip cropping for management of Lygus spp. in cotton (Stern et al., 1964), or the use of Rubus sp. plantings and now Prunus sp. around vineyards for conservation of grape leafhopper parasitoids (Doutt & Nakata, 1973) have not been adopted on a regional scale. We recognize that the prevailing political and economic context of modern farming does not support the maintenance of landscape diversity. This has been one of the main obstacles to the implementation of many of the alternative strategies reviewed in this chapter. However, increasing interests in sustainability (Francis et al., 1990; National Research Council, 1991) and biodiversity (LaSalle & Gauld, 1993; Marc & Canard 1997; Stinner et al., 1997), coupled with global marketing strategies, have resulted in distinct changes in policy recommendations that have begun to encourage agricultural diversification on different scales in the 1990s (e.g., Barghouti et al., 1992; Holt et al., 1995). Rabbet al. (1976) characterize the effective environment of an organism as (1) weather, (2) food, (3) habitat (shelter, nests), and (4) other organisms. Thus, environmental management for biological control concerns the functional environment: the physical and biotic elements that directly or indirectly impact survival, migration, reproduction, feeding, and behaviors associated with these processes. Although pest populations can be controlled directly through cultural control methods that modify the habitat, we do not offer a thorough review of this topic. Instead, our objectives are to discuss conservation (maintenance of natural-enemy abundance and diversity) and enhancement (via increased immigration, tenure, longevity, fertility, and efficiency) strategies that can be used to manipulate natural enemies in

agroecosystems. In general, habitat management regimes to increase natural-enemy effectiveness are directed at: (1) enhancing habitat suitability for immigration and host finding, (2) provision of alternative prey/hosts at times when the pest is scarce, (3) provision of supplementary food (food sprays, pollen and nectar for predators and parasitoids), (4) provision of refugia (for mating or overwintering), and (5) maintenance of noneconomic levels of the pest or alternative hosts over extended periods to ensure continued survival of natural enemies. Examples of cropping techniques that enhance a particular parasitoid population through effects on some of the preceding processes are shown in Table 1, and have been reviewed by Powell (1986). Useful approaches borrowed from conservation biology are reviewed in Letourneau (1998). The manipulation of entomophagous insects must be approached from several levels, from agroecosystem processes to ecophysiological features of individual organisms. The range of manipulatable elements and their degree of flexibility depend on characteristics of the agroecosystem; these linkages will be described in a section on agricultural habitats. A review of research on modes of environmental management will summarize current knowledge on tactics of input, removal, or adjustments of biotic and physical/ chemical elements of the agroecosystem by manual or mechanical means. This will be followed by a discussion of the biological mechanisms involved in natural-enemy responses to cultural practices and a section on relevant ecological theory to stimulate further research on this topic. Thus, we consider the role, methods, and future directions of environmental management as a prophylactic control strategy (sensu Vandermeer & Andow, 1986) in a variety of agroecosystems.

CLASSIFICATION OF AGROECOSYSTEMS Each region has a unique set of agroecosystems that result from climate, topography, soil, economic relations, social structure, and history. Various farming system features can be modified and some can be expected to affect the dynamics of insect populations (Table 2). The agroecosystems of a region often include both commercial and local-use agricultures that rely on technology to different extents depending on the availability of land, capital, and labor. Some technologies in modem systems aim at efficient land use (reliance on agrochemical inputs), while others reduce labor (mechanical inputs). In contrast, resourcepoor farmers usually adopt low technology, labor-intensive practices that optimize production efficiency and recycle scarce resources (Mattson et al., 1984; Altieri, 1989). Common, area-wide environmental management techniques are difficult to design and implement given the differences in climate, agricultural products, and economic

Chapter 14 TABLE 1

Environmental management practice

Use of kairomones

Provision of alternative hosts

Provision of food other than host

Environmental Management to Enhance Biological Control in Agroecosystems

Examples of Environmental Manipulation Resulting in Increased Parasitism of Specific Insect Pests in a Range of Cropping Systems

Parasitoid(s) affected

Pest regulated

Cropping system or environmental diversity element

Trichogramma spp. Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) Cardiochiles nigriceps Vier. (Hymenoptera: Braconidae)

Heliothis zea (Boddie) H. zea

Soybeans, tomatoes, corn Soybeans, tomatoes, corn

H. virescens (F.)

Soybeans, tomatoes, corn

Macrocentrus spp. (Hymenoptera: Braconidae) Lydella grisescens R.-D. (Diptera: Tachinidae) Horogenes spp. Anagrus epos (Girault) (Hymenoptera: Mymaridae) Eurytoma tylodermatis Ashm. (Hymenoptera: Eurytomidae) Emersonella niveipes Girault (Hymenoptera: Eulophidae) Lysiphlebus testaceipes Cress. (Hymenoptera: Aphidiidae)

Cydia molesta (Busck) (Lepidoptera: Olethreutidae) Ostrinia nubilalis (Htibner) (Lepidoptera: Pyralidae) Plutella xylostella Erythroneura elegantula Osborn (Homoptera: Cicadellidae) Anthonomus grandis Boheman (Coleoptera: Curculionidae)

Weeds in peaches

Chelymorpha cassidea (F.) (Coleoptera: Chrysomelidae) Schizaphis graminum (Rodani) (Homoptera: Aphididae)

Morning glories in sweet potatoes

Tiphia popilliavora Rohwer (Hymenoptera: Tiphiidae)

Phyllophaga spp. (Coleoptera: Scarabeidae) Lachnosterna spp. (Coleoptera: Scarabeidae) Aphids

Nectar from weeds; honeydew from scale insects in various crops

Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) Cotesia medicaginis (Hymenoptera: Braconidae) Aphytis proclia (Walker) (Hymenoptera: Aphelinidae)

Colias philodice Godart (Lepidoptera: Pieridae) Quadraspidiotus perniciosus (Comstock) (Homoptera: Diaspididae)

Various species

Malacosoma americanum (F.) (Lepidoptera: Lasiocampidae) Laspeyresia (Cydia) pomonella (Busck) (Lepidoptera: Olethuridae) Rhabdoscelus obscurus (Boisduval) (Coleoptera: Curculionidae)

Lixophaga sphenophori (Villeneuve) (Diptera: Tachinidae) Adoption of special cropping practices

321

Macrocentrus ancylivorus (Hymenoptera: Braconidae) Bathyplectes curculionis (Thomson) (Hymenoptera: Ichneumonidae) Aphidiids Lysiphlebus testaceipes Anagrus sp. Trichogramma spp. (Hymenoptera: Trichogrammatidae)

After Cromartie, 1981; Altieri & Letourneau, 1982; and Powell, 1986.

Ragweeds in maize

Crataegus in cabbage Blackberries in vineyards Ragweeds in cotton

Sunflowers near sorghum

Nectar from the honeyplants Phacelia and Eryngium in apples Nectar from weeds; honeydew from aphids in alfalfa Nectar from the honeyplant Phacelia tanacetifolia Benth. (Hydrophyllaceae) in orchards Nectar from weeds in apples

Nectar from Euphorbia spp. weeds in sugarcane

Ancylis comptana (Froelich) (Lepidoptera: Olethreutidae) Cydia molesta Hypera postica (Gyllenhal) (Coleoptera: Curculionidae)

Intercropping strawberries and peaches

Aphids S. graminum

Strip harvesting of alfalfa Resistant cultivars of barley and soybeans Mixed cropping maize and beans

Empoasca kraemeri Ross & Moore (Coleoptera: Cicadellidae) Heliothis zea

Time of first cutting of alfalfa

Mixed cropping maize and soybeans

322 TABLE 2 Type of determinants

D.K. Letourneau and M. A. Altieri Agroecosystem Determinants for the Type of Agriculture in a Given Region Factors

Radiation Temperature Rainfall Irrigation Soil conditions Slope Land availability Biological Insect pests and natural enemies Weed communities Plant and animal diseases Soil biotab Background natural vegetation Photosynthetic efficiency Cropping patterns Crop rotation Socioeconomic Populationdensity Social organization Economic (prices, markets, capital and credit availability) Technical assistance Cultivation implements Degree of commercialization Labor availability Cultural Traditional knowledge Ideology Gender issues Historical events

Manipulation amenability a

Physical

X X

X X X X X X X X X X

aFactor amenable to manipulation through habitat management and expected to directly or indirectly affect the impact of arthropod natural enemies as biological control agents. bAs influenced by fertilizing regimes, composting,etc.

the main challenges facing agroecologists today is identifying the types of biodiversity assemblages (either at the field or at the regional level) that will yield desirable agricultural results (i.e., pest regulation). This challenge can only be met by further analyzing the relationship between vegetation diversification and population dynamics of herbivore and natural-enemy species, in light of what the unique environment and entomofauna of each are and the diversity and complexity of local agricultural systems. According to Vandermeer and Perfecto (1995), two distinct components of biodiversity can be recognized in agroecosystems. The first component, planned biodiversity, is the biodiversity that is associated with the crops and livestock purposely included in the agroecosystem by the farmer, and that will vary depending on management inputs and crop spatial-temporal arrangements. The second component, associated biodiversity, includes all soil floras and faunas, herbivores, carnivores, decomposers, etc. that colonize the agroecosystem from surrounding environments and that will thrive in the agroecosystem depending on its management and structure. The relationship of both biodiversity components is illustrated in Fig. 2. Planned biodiversity has a direct function, as illustrated by the bold arrow connecting the planned biodiversity box with the ecosystem function box. Associated biodiversity also has a function, but it is mediated through planned biodiversity. Thus, planned biodiversity also has an indirect function, illustrated by the dotted arrow in the figure, which is realized through its influence on the associated biodiversity. For example, the trees in an agroforestry system create shade, which makes

Agroecosystem Management

and political structure of each agricultural system. Many farming systems are in transition, with changes forced by shifting resource needs, unequal resource availability, environmental degradation, economic growth or stagnation, political change, etc. Strategies amenable to labor-intensive operations will be radically different from those designed for mechanized, large-scale operations. Specialization and concentration of crops are the most important factors limiting the application of many environmental management options for a particular region. All agroecosystems are dynamic and subjected to different levels of management so that the crop arrangements in time and space are continually changing in the face of biological, cultural, socioeconomic, and environmental factors. Such landscape variations determine the degree of spatial and temporal heterogeneity characteristic of agricultural regions, which in turn conditions the type of biodiversity present, in ways that may or may not benefit the pest protection of particular agroecosystems. Thus, one of

f

Promotes

Planned Biodiversity

Ecosystem Function e.g., pest regulation, nutrient cycling

I Creates conditions that promote

~\\,,.

/I

Associated Biodiversity

._..._~

Promotes

Biodiversity of Surrounding Environment

FIGURE 2 The relationship between planned biodiversity (that which the farmer determines, based on management of the agroecosystem) and associated biodiversity (that which colonizes the agroecosystem after it has been set up by the farmer) and how the two promote ecosystem function. (Modifiedfrom Vandermeer and Perfecto, 1995.)

Chapter 14

it possible to grow only sun-intolerant crops. Thus, the direct function of this second species (the trees) is to create shade. Yet along with the trees might come small wasps that seek out the nectar in the tree's flowers. These wasps may in turn be the natural parasitoids of pests that normally attack the crops. The wasps are part of the associated biodiversity. The trees create shade (direct function) and attract wasps (indirect function) (Vandermeer & Perfecto, 1995). The key is to identify the type of biodiversity that is desirable to maintain and/or to enhance the implementation of ecological services, and then to determine the best practices that will encourage the desired biodiversity components. As shown in Fig. 4, there are many agricultural practices and designs that have the potential to enhance functional biodiversity, and others that negatively affect it. The idea is to apply the best management practices to enhance and/or to regenerate the kind of biodiversity that can subsidize the sustainability of agroecosystems by providing ecological services such as biological pest control but also nutrient cycling, water and soil conservation, and SO on.

Although each farm is unique, farms can be classified by type of agriculture or agroecosystem. Functional grouping is essential for devising area-wide habitat management strategies. Five criteria can be used to classify agroecosystems in a region: (1) the types of crop and livestock; (2) the methods used to grow the crops and produce the stock; (3) the relative intensity of use of labor, capital, and organization, as well as the resulting output of product; (4) the

Natural Ecosystem

~

323

Environmental Management to Enhance Biological Control in Agroecosystems

disposal of the products for consumption (whether used for subsistence or supplement on the farm or sold for cash or other goods); and (5) the structures used to facilitate farming operations (Norman, 1979). Based on these criteria, it is possible to recognize seven main types of agricultural systems in the world (Grigg, 1974): 1. 2. 3. 4. 5. 6. 7.

Shifting cultivation systems Semi-permanent rain-fed cropping systems Permanent rain-fed cropping systems Arable irrigation systems Perennial crop systems Grazing systems Systems regulated by farming practices (alternating arable cropping and sown pasture)

Systems 4 and 5 have evolved into habitats that are much simpler in form and poorer in species than the others, which can be considered more diversified, permanent, and less disturbed, therefore inherently containing elements of natural pest control (Fig. 3). Clearly then, modern systems require more radical modifications of their structure to approach a more diversified, less disturbed state. Figure 4 provides a series of diversification options for such systems. (Alfalfa is treated here as a quasi-perennial crop.) If it is argued that such modifications are not possible in largescale agriculture due to technical or economic factors, then this point provides a strong conservative argument in favor of small, multiple-use farms.

I

.,.._

Degree of Environmental Simplification and Need for Increased Artificial Control

Traditional polycultures

Mixed Modern ond/qr fruit orchards organic small org~c c o n jl~ ventionol form with or without ground vegetation management

Artificial Intensively Managed Ecosystem

Modern annual monocultures V alfalfa small grains row crops vegetables

FIGURE 3 Management intensity continuum between ecosystems and agricultural ecosystems in relation to the need for artificial pest control measures.

324

D.K. Letourneau and M. A. Aitieri

Modern Agricultural Systems

J

Annual Crop Based

Perennial Crop Based

I Small Grains II Vegetables Row Crop Monocultures

I Alfalfa

I I Vineyards I

Diversification Strategies crop sequences and rotations multiple cropping (inter, strip, etc.) no-tillage living mulches managed fallows mulch farming windbreaks

Agroforestry (combined crop-tree - - ~ production)

Ag ro- Pa st o ra I " " ' - - ~ Systems

FIGURE 4

Crop/Livestock Mixed Farming

~

cover cropping perennial polycultures and mixed orchards intercrop w/annual crops mulching shelterbelts surrounding vegetation manipulation

Agro- Silva-Pastoral Systems

Plant diversification strategies in annual and perennial crop systems.

MODES OF ENVIRONMENTAL MANAGEMENT Vegetational designs across appropriate levels of scale comprise an obvious form of environmental management. At the regional level, landscape vegetation mosaics influence the distribution of food and shelter resources, and, therefore, the colonization patterns of insects (Andow, 1983b; Ryszkowski et al., 1993). On a smaller scale, herbivores and their natural enemies respond to localized patterns of plant spacing, plant structure, and plant species (or varietal) diversity. Environmental components and their management in agroecosystems have three main dimensions: temporal, spatial, and biological (Fig. 5). Other means of biotic management through inundative releases and classical biological control are discussed elsewhere (Chapter 11). Mechanical modes of environmental management, such as cultivating, mowing, and harvesting, affect the structure and permanence of the habitat and thus the life processes of insects in agroecosystems. Chemical inputs, such as the periodic application of water, fertilizers, behavior-modifying agents, and pesticides, affect rates of growth and survival of pests and natural-enemy populations. The impact of pesticides will be treated here only in terms of drift effects (see Chapters 13 and 24). Biotic, physical,

chemical, and mechanical manipulations are imposed on agroecosystems often as a means to achieve objectives unrelated to insect pest management. Nevertheless, the range of environmental manipulations designed for higher yields is sufficiently broad to permit incorporation of tactics that simultaneously improve pest control (see Table 2). Vegetation M a n a g e m e n t Frequently disturbed monocultures favor the rapid colonization and growth of herbivore populations; initial conditions of enemy-free space and high abundance of pests further reduce the ability of natural enemies to regulate them (Price, 1981). In most farming situations these negative factors can be minimized or eliminated by providing continuity of vegetation (and the associated food and shelter) in time and space, thus aiding natural enemies (Table 3). Many studies document direct behavioral and physiological effects of plants on natural enemies (van Emden, 1965; Leius, 1967; Campbell & Duffey, 1979; Nettles, 1979; A1tieri et al., 1981; Boethel & Eikenbary, 1986; De la Cruz & Litsinger, 1986; Elzen et al., 1986; Letourneau, 1987, 1990; Dicke & Sabelis, 1988; Panizzi, 1988; Barker &

Chapter 14

Environmental Management to Enhance Biological Control in Agroecosystems

325

Components of Environmental Diversity

Temporal Dimensions

monoculture rotation sequential cropping continuous cropping fallow

annual/perennial crop within field/ out of field vegetation phenology planting dote (early/late) asynchronous planting harvesting dote time of weeding long/short maturing crop favorable/unfavorable season timing of climatic events

Spatial Dimensions

species-pure crop multiple cropping agroforestry large/small field aggregated/scattered fields complex/simple surrounding habitat(weeds, hedgerows, woodland, grasslands, etc.) high/low planting density weedy/weed-free uniform/mixed varieties local/regional crop mosaics trap crops

Biological Dimensions

tolerant/susceptible variety resistant/pure line/multigeneric uniform staggered plant age monophogous/polyphogous pest + n.e. large/small pest complex + n.e. multi/univoltine pests + n.e. apparent/non-apparent crop high/low chemical defenses in crop linear/complex trophic chains exotic/native pest + n.e.

FIGURE 5 Temporal, spatial, and biotic components of environmental diversification of agricultural ecosystems (n.e. = natural enemies of arthropod pests).

Addison, 1997). Some entomophagous insects are more abundant in the presence of particular plants even in the absence of hosts or prey, or they are attracted to or arrested by chemicals released by the herbivore's host plant or other associated plants (Monteith, 1960; Shahjahan, 1974; Nettles, 1979; Martin et al., 1990; Geitzenauer & Bernays, 1996; Stapel et al., 1997). Parasitism of a pest can be higher on some crops than on others (Read et al., 1970; Martin et al., 1976; Nordlund et al., 1985; Johnson & Hara, 1987; Gerard, 1989; Lewis & Gross, 1989; Idris & Grafius, 1996; Bautista & Harris, 1996), and different parasitoids can be associated with particular crops or crop habitats even if the same host is attacked (Lewis & Gross, 1989; Felland, 1990; van den Berg et al., 1990). Noncrop plants within and around fields can be used to benefit biological control agents (Altieri & Whitcomb, 1979a, 1979b; Barney et al., 1984; Norris, 1986; Bugg & Wilson, 1989; Kiss et al., 1997). Rapidly colonizing, fastgrowing plants offer many important requisites for natural enemies--such as alternative prey or hosts, pollen or nect a r - a s well as microhabitats that are not available in largescale, weed-free monocultures (van Emden, 1965; Doutt & Nakata, 1973; Cerutti et al., 1989; Idris & Grafius, 1995),

but these interactions can be difficult to define precisely and to implement in control programs (Flaherty et al., 1985). Outbreaks of certain types of crop pests are more likely to occur in weed-free fields than in weed-diversified crop systems (Dempster, 1969; Flaherty, 1969; Root, 1973; Smith, 1976a; Altieri et al., 1977; Ofuya, 1989). Crop fields with dense weed cover and high diversity usually have more predaceous arthropods than do weed-free fields (Pimentel, 1961; Dempster, 1969; Flaherty, 1969; Pollard, 1971; Root, 1973; Smith, 1976b; Speight & Lawton, 1976; Bottenberg et al., 1990; Wyss, 1995; Schellhorn & Sork, 1997). Carabidae (Dempster, 1969; Speight & Lawton, 1976; Thiele, 1977), Syrphidae (Pollard, 1971; Smith, 1976b; Cowgill, 1989), and Coccinellidae (Bombosch, 1966; Pertin, 1975) are abundant in weed-diversified systems. Relevant examples of cropping systems in which the presence of specific weeds has enhanced biological control of particular pests are given in Table 3. The potential for managing weeds as useful components of agroecosystems is great, but not all weeds promote biological control (Powell et al., 1986) even if entomophagous insects are more abundant in the system (Gaylor & Foster, 1987; Bugg et al., 1991).

326

D.K. Letourneau and M. A. Altieri TABLE 3

Crop

Selected Examples of C r o p - N o n c r o p or C r o p - C r o p Combinations That Enhanced the Biological Control of Specific Crop Pests

Weed species or intercrop

Apples

Phacelia sp. and Eryngium sp.

Apples

Natural weed complex

Apples

Natural weed complex

Beans Brassica

Natural weed complex Beans

Brussels sprouts

Natural weed complex

Brussels sprouts

Spergula arvensis L. (Caryophyllaceae)

Brussels sprouts

Brassica kaber (DC.) (Brassicaceae)

Cabbage

Crataegus sp.

Cabbage

White and red clover

Cacao

Coconut

Cole crops

Quick-flowering mustards

Collards

Corn

Factor(s) involved

San Jose scale [Quadraspidiotus perniciosus (Comstock)] and aphids Dysaphis plantaginea Pass. and Aphis pomi (DeGeer) Tent caterpillar (Malacosoma americanum) and codling moth [Laspeyresia pomonella (L.)] (Lepidoptera: Olethreutidae) Epilachna varivestis L. Brevicoryne brassicae and Delia brassicae Imported cabbage butterfly [Pieris rapae (L.)] (Lepidoptera: Pieridae) and aphids [Brevicoryne brassicae (L.)] (Homoptera: Aphididae) Mamestra brassicae L. (Lepidoptera: Noctuidae), Evergestis forficalis L. (Lepidoptera: Pyralidae), B. brassicae B. brassicae

Increased abundance and activity of parasitic wasps (Aphelinus mali and Aphytis proclia) Increased abundance of aphidophagous predators Increased activity and abundance of parasitic wasps

Telenga, 1958

Increased predation on eggs Higher predation and disruption of oviposition behavior Alteration of crop background and increase of predator colonization

Andow, 1990 Tukahirwa & Coaker, 1982 Smith, 1976b; Dempster, 1969

Increase of predators and interference with colonization

Theunissen & den Ouden, 1980

Attraction of syphids [Allograpta obliqua (day)] (Diptera: Syrphidae) to B. Kaber flowers Provision of alternate hosts for parasitic wasps (Horogenes sp.) Interference with colonization and increase of ground beetles

Altieri, 1984

Provision of nest sites for ants [Oecophylla smaragdina (F.) and Dolichoderus thoracicus (Smith) (Hymenoptera: Formicidae)] Increased activity of parasitic wasps [Cotesia glomerata (L.) Hymenoptera: Braconidae] Increased abundance of predators Increased abundance of predators ( Chrysoperla carnea, Coccinellidae, Syrphidae)

Way & Khoo, 1991

Increase in beneficial insects and interference with colonization

Altieri et al., 1978

Diamondback moth [Plutella maculipennis (Curtis)] (Lepidoptera: Yponomeutidae) Erioischia brassicae, cabbage aphids, and imported cabbage butterfly (Pieris rapae) Helopeltis theobromae Miller

Cabbageworms (Peiris spp.)

B. brassicae

Cole crops

Amaranthus retroflexus L. (Amaranthaceae), Chenopodium album, Xanthium strumarium L. (Asteraceae) Beans

References

Pest(s) regulated

Green peach aphid (Myzus persicae)

Leafhoppers (Empoasca kraemeri), leaf beetle (Diabrotica balteata LeConte) (Coleoptera: Chrysomelidae) and fall armyworm [Spodoptera frugiperda (Smith)] (Lepidoptera: Noctuidae)

Wyss, 1995 Leius, 1967

van Emden, 1965

Dempster & Coaker, 1974

NAS, 1969

Tukahirwa & Coaker, 1982 Horn, 1981

(continues)

Chapter 14

327

Environmental Management to Enhance Biological Control in Agroecosystems

TABLE 3 (continued)

Crop Corn

Weed species or intercrop Giant ragweed

Pest(s) regulated European corn borer (Ostrinia

nubialis)

Factor(s) involved Provision of alternate hosts for the tachnid parasite, Lydella

References Syme, 1975

grisescens Corn

Sweet potatoes

Leaf beetles (Diabrotica spp.) and leafhoppers (Agallia lin-

Cotton

Alfalfa

Plant bugs (Lygus hesperus and

Increase in parasitic wasps

Risch, 1979

Prevention of emigration and synchrony in the relationship between pests and natural enemies Increased abundance of predators

Marcovitch, 1935

Population increase of parasitic wasps (Eurytoma sp.) Increased populations of predators Increased abundance of predators Population increase of parasites

Marcovitch, 1935

gula) L. elisus)

Cotton

Alfalfa, maize and soybeans

Cotton

Forage cowpeas

Corn earworm (H. zea) and cabbage looper [Trichoplusia ni (Htibner)] (Lepidoptera: Noctuidae) Boll weevil (Anthomonus gran-

Ragweed and Rumex

dis) Heliothis spp.

Cotton

crispus Cotton

Sorghum or maize

Corn earworm (H. zea)

Peaches

Strawberries

Strawberry leaf roller (Ancylis comptana) and Oriental fruit moth (Grapholita molesta)

Sesame

Cotton

Corn borer (Ostrinia furnacalis Guen6e) (Lepidoptera: Pyralidae) Heliothis spp.

Squash

Maize

Diaphania hyalinata (L.) (Lep-

Peanuts

Maize

idoptera: Pyralidae) Soybeans

Cassia obtusifolia L. (Fabaceae)

Nezara viridula (L.) (Heteroptera: Pentatomidae), Anticarsia gemmatalis (Lepidoptera:

(Macrocentrus ancylivora, Microbracon gelechise, and Lixophaga variabilis) Abundance of spiders [Lycosa

DeLoach, 1970

Smith & Reynolds, 1972 DeLoach, 1970

Raros, 1973

sp. (Araneae: Lycosidae)] Increase of beneficial insects and trap cropping Habitat more suitable for parasitoids/alternate hosts for Trichogramma spp. Increased abundance of predators

Laster & Furr, 1972

Increased abundance of parasites (Hymenoptera, carabids and spiders)

Bosch, 1987

Topham & Beardsley, 1975

Letourneau, 1987

Altieri et aI., 1981

Noctuidae) Sugar beet

Matricaria chamomilla L., Lamium purpureum L. and

Aphis fabae L., Atomaria linearis Stephen, Diplopoda spp.

others Sugarcane

Euphorbia spp. weeds

Sugarcane weevil [Rhabdoscelus obscurus (Boisduval)]

Provision of nectar and pollen for the parasite Lixophaga

Sweet potatoes

Morning glory (lpom-

Argus tortoise beetle (Chely-

Provision of alternate hosts for the parasite Emersonella sp.

Carroll, 1978

Colonization source for Aphidius rhopalosiphi DeStefani Perez females

Vorley & Wratten, 1987

sphenophori oea asarifolia

Winter wheat

Roem et Schult) (Convolvulaceae) Grassland

morpha cassidea)

Cereal aphids

328

D.K. Letourneau and M. A. Altieri

Leius (1967) found that the presence of wildflowers in apple orchards resulted in an 18-fold increase in parasitism of tent caterpillar pupae over nonweedy orchards; parasitism of tent caterpillar eggs increased fourfold, and parasitism of codling moth larvae increased fivefold. A cover crop of bell beans [Vicia faba Linnaeus (Fabaceae)] in rain-fed apple orchards in northern California decreased infestation by the codling moth. This lower moth infestation was correlated significantly with increased numbers of predators (Aranae, Coccinellidae, Syrphidae, and Chrysopidae) on the trees (Altieri & Schmidt, 1985). Similar results were obtained by Dickler (1978) in Germany. In New Jersey peach orchards, control of the oriental fruit moth increased in the presence of ragweed (Ambrosia sp.), smartweed (Polygonum sp.), lambsquarter (Chenopodium album Linnaeus) (Chenopodiaceae), and goldenrod (Solidago sp.). These weeds provided alternate hosts for the braconid parasite Macrocentrus ancylivorus Rohwer (Bobb, 1939). O'Connor (1950) recommended the use of a cover crop in coconut groves in the Solomon Islands to improve the biological control of coreid pests by the ant Oecophylla smaragdina subnitida Emery. In Ghana, coconut served this purpose by providing enough shade for cocoa to support high populations of the ant O. longinoda Latreille, which kept the cocoa crop free from cocoa caspids (Leston, 1973). Annual crops diversified with cover crops also suffer less damage. For example, Brust et al. (1986) reported dramatically higher predation rates of Lepidoptera larvae ~ black cutworms (Agrotis ipsilon [Hufnagel]), armyworms (Pseudaletia unipunctata Haworth), stalk borers (Papaipema nebris [Guen6e]), and European corn borers [Ostrinia nubilalis (Htibner)]~tethered to corn sown into a grass-legume mixture than to corn in monoculture. Carabid beetles were more abundant in that living mulch system and were among the larval predators in both systems. Temporal refugia for predators can result in increased densities early in the season whether they be provided by the crop itself (e.g., De la Cruz & Litsinger, 1986; Coli & Ciurlino, 1990), by other crops (e.g., Murphy et al., 1996), or by permanent noncrop vegetation (Chiverton, 1989; Oraze et al., 1989; Thomas, 1989; Zhuang, 1989; Wratten & Thomas, 1990). The roles of vegetational mosaics and corridors in the conservation of natural enemies are undoubtedly important, but are difficult phenomena to investigate experimentally. A number of studies have shown that natural enemies move from noncrop habitats to crop fields, but relative vagility of natural enemies and scale of plot designs constrain our abilities to assess landscape-level movement patterns (van Emden, 1988; Hansson, 1991). For example, Rodenhouse et al. (1992) found that predaceous arthropods in soybean were more abundant if the plots contained noncrop corridors. In contrast, Pavuk and Barrett (1993) found no difference in larval parasitism of the green clover worm, Plathy-

pena scabra (Fabricius) (Lepidoptera: Noctuidae), among these treatments. Landis and Haas (1992) found, in a larger scale comparison, higher parasitism levels of European corn borer, Ostrinia nubilalis (Htibner), near wooded sites. Our abilities to assess natural-enemy movement patterns, and to design landscapes to encourage their early arrival and sustained presence in crop fields depend on large-scale empirical studies now feasible using Geographic Information Systems (GIS) technologies (Liebhold et al., 1993). In summary, design of vegetation management strategies must include knowledge and consideration of (1) crop management in time and space, (2) composition and abundance of noncrop vegetation within and around fields, (3) soil type, (4) surrounding environment, and (5) type and intensity of management. The response of insect populations to environmental manipulation depends on their degree of association with one or more of the vegetational components of the system. Extension of the cropping period, planning temporal or spatial cropping sequences, inclusion of "insectary" plants, or maintenance of movement corridors may allow naturally occurring biological control agents to sustain higher population levels on alternative hosts or prey and to persist in the agricultural environment throughout the year. Because farming systems in a region are managed over a range of energy inputs, levels of crop diversity, and successional stages, variations in insect dynamics are likely to occur that are difficult to predict. However, based on current ecological and agronomic theory, low pest potentials may be expected in agroecosystems that exhibit the following characteristics: 1. They have high crop diversity through mixtures in time and space (Cromartie, 1981; Altieri & Letourneau, 1982; Risch et al., 1983; but see Andow & Risch, 1985; Nafus & Schreiner, 1986; Altieri, 1994; Coil & Bottrell, 1995). 2. There is discontinuity of monoculture in time through rotations, use of short maturing varieties, use of crop-free preferred host-free periods, etc. (Stem, 1981; Lashomb & Ng, 1984; Desender & Alderweireldt, 1990). 3. There are small, scattered fields creating a structural mosaic of adjoining crops, and uncultivated land potentially providing shelter and alternative food for natural enemies (van Emden, 1965; Altieri & Letourneau, 1982). Pests also may proliferate in these environments depending on plant species composition (Altieri & Letourneau, 1984; Collins & Johnson, 1985; Levine, 1985; Slosser et al., 1985; Lasack & Pedigo, 1986; Mena-Covarrubias et al., 1996; Panizzi, 1997). However, the presence of low levels of pest populations or alternative hosts may be necessary to maintain natural enemies in the area. 4. They have a dominant perennial crop component. Orchards are considered more stable, as permanent ecosys-

Chapter 14 EnvironmentalManagement to Enhance Biological Control in Agroecosystems tems, than are annual crop systems. Because orchards suffer less disturbance and are characterized by greater structural diversity, possibilities for the establishment of biological control agents are generally higher, especially if floral undergrowth diversity is encouraged (Huffaker & Messenger, 1976; Altieri & Schmidt, 1985). 5. They have high crop densities in the presence of tolerable levels of weed background (Shahjahan & Streams, 1973; Altieri et al., 1977; Sprenkel et al., 1979; Andow, 1983a; Mayse, 1983; Buschman et al., 1984; Ali & Reagan, 1985). 6. There is high genetic diversity resulting from the use of variety mixtures or several lines of the same crop (Perrin, 1977; Whitham, 1983; Gould, 1986; Altieri & Schmidt, 1987). All the preceding generalizations can serve in the planning of a vegetation management strategy in agroecosystems; however, they must take into account local variations in climate, geography, crops, local vegetation, pest complexes, etc., which might change the potential for pest development under some vegetation management conditions. The selection of component plant species also can be critical (e.g., Bugg et al., 1987; Naranjo, 1987; van den Berg et al., 1990). Systematic studies on the "quality" of plant diversification with respect to the abundance and efficiency of natural enemies are needed. While 59% of the 116 species of entomophages in documented studies reviewed by Andow (1986) exhibited increased abundances when plant species were added to the system, 10% decreased in abundance and 20% were either not affected by vegetational diversity or were variable, sometimes increasing and other times decreasing. Gold et al. (1991), Perfecto and Sediles (1992), and Toko et al. (1996) found no significant difference in the abundance of specific entomophagous arthropods in response to crop diversification. Similarly, parasitization rates of bean flies were constant despite the addition of maize or other bean varieties in Malawi (Letourneau, 1994). Nafus and Schreiner (1986) found lower parasitism rates in corn intercropped with squash. The addition of squash decreases the abundance of the coccinellid Coleomegilla maculata (De Geer) on squash because of a nonuniform distribution of prey (Andow & Risch, 1985). The anthocorid Orius tristicolor (White), however, another generalist predator, is more abundant on squash when corn is incorporated. In this case, plant architecture and nonuniform distribution of prey are beneficial (Letourneau 1990). Perfecto et al. (1986) found that plant density and diversity interact negatively to determine ground beetle emigration rates. Mechanistic studies to determine the underlying elements of plant mixtures that enhance or disrupt colonization and population growth of natural enemies will allow more precise planning of cropping schemes and will increase the chances of a beneficial effect beyond current levels.

329

M e c h a n i c a l Crop M a n a g e m e n t Mechanical manipulations of the environment vary along two important parameters, severity of disturbance and frequency of disturbance. Across a range of agroecosystem types, low-input, perennial systems, for example, present a contrast to mechanized, annual crop production systems (Fig. 6). Yet slight modifications in cultural practices for sowing, maintaining, and harvesting annual crops can effect substantial changes in natural-enemy populations, which bring them nearer to those observed in less disturbed perennial counterparts (Barfield & Gerber, 1979; Arkin & Taylor, 1981; Blumberg & Crossley, 1983; Herzog & Funderburk, 1985).

Cultivation and Tillage Current trends in tillage practices reflect attempts to limit mechanical disturbance of the soil. The objectives in emphasizing surface tillage and no tillage as alternatives to plow tillage are to control soil erosion, enhance crop performance, and use energy more efficiently (Sprague, 1986). Tillage practices have profound effects on the relative densities of pests and natural enemies in a crop field. Minimum tillage systems can conserve and enhance natural enemies of important crop pests (House & All, 1981; Luff, 1982; Blumberg & Crossley, 1983). However, All and Musick (1986) suggest that each crop-pest-enemy interaction must be considered independently. Table 4 demonstrates this point by depicting significant but often divergent responses within the Carabidae, a prominent predaceous group in tillage response studies. Deep plowing, surface disking, and other manipulations of the soil can affect ground-dwelling arthropods, whether they inhabit the soil consistently or intermittently (e.g., Funderburk et al., 1988; House, 1989a, 1989b; Stinner &

high

frequent severe disturbance

infrequent,severe disburbance

low

frequent, mild disturbance

infrequent,mild disturbance

annuals

perennials

Mechanization Index *

Length of Crop Tenure FIGURE 6 Severalfactors determine the level and frequency of disturbance. The intensityof mechanization and crop tenure are amongthe most important. Within the constraints of crop production, the use of modified cultivation and strategies will favor various natural enemies. *Determined as a function of plowing depth and compaction.

330 TABLE 4

D.K. Letourneau and M. A. Altieri R e s p o n s e by Carabid Beetles to Tillage Practices and Cover C r o p p i n g in Annual and Perennial A g r o e c o s y s t e m s

Tillage practice

Crop

Carabid taxa

No tillage

Corn

Mowed cover crop

Corn

No tillage

Alfalfa

Amara spp., Pterostichus spp., and Amphasia spp. Pterostichus spp. and Scarites spp. Carabids

Conservation tillage No tillage

Soybeans

Carabids

Soybeans

Carabids (9 genera)

No tillage

Wheat, soybeans, corn Apples

Various practices

Spring wheat

Harpalus spp. and Amara spp. Anisodactylus senctaecrucis F., Stenopophus comma F., Harpalus aeneus F., Amara spp., and Bradycellus supestris Say carabid larvae 40 species

No tillage

Apples

Cover crop

Apples

No tillage

Carabids (especially Harpalus sp.) Pterostichus spp., Amara spp.

Response

References

Higher population density

Brust et al., 1985

Higher abundance than in herbicidekilled cover crop in early season No significant difference in abundance or diversity Higher species richness and abundance Higher species richness, abundance, and biomass Higher abundance

Laub and Luna, 1992

Higher abundance in natural vegetation plots; diversity not significantly different

Holliday & Hagley, 1984

Cropping system and tillage regimes change community composition Higher abundance in weedy plots than in clean individual plots Lower abundance with cover crop of mixed grass and bell bean than with clean cultivation

Weiss et al., 1990

Barney & Pass, 1986 House & All, 1981 House & Stinner, 1983 House, 1989

Altieri et al., 1985 Altieri & Schmidt, 1985, 1986

Agonum spp. Platynus spp. Microlestes spp.

House, 1990). The extent of direct mortality depends on their distribution with respect to soil depth and their phenologies. Less directly but potentially as important are effects caused by the removal of resources and natural enemies associated with living undergrowth and plant residues. Few studies have addressed the mechanisms of population and community response to soil manipulations. Therefore, effects due to mechanical disturbance and secondary effects due to weed removal are often confounded. It is difficult to assess experimentally the impact of natural enemies on crop pests in these systems; and the causal links between tillage practices, numbers of natural enemies, and level of biological control have been demonstrated in only a few cases, as discussed later [see Risch et al. (1983) and Letourneau (1987) for similar discussions on the paucity of mechanism studies in intercropping experiments]. Brust et al. (1985) showed that significantly higher densities of carabids, including Amara spp., Pterostichus spp., and Amphasia spp., in no-tillage systems were the major factor in reducing black cutworm damage significantly below the level achieved in conventional corn systems. Their conclusions were based on comparing treatments with and

without soil insecticides. Carcamo (1995) showed that carabid population responses to tillage practices can depend on the species, but found that species diversity and evenness were higher in reduced tillage barley than in conventionally tilled fields. Variable responses were also found for different species of carabids under different tillage intensities by Clark et al. (1997). Other studies show that herbivore damage is reduced in no-tillage fields despite similar predator abundance in tilled and no-till fields. For example, reduced rootworm (Diabrotica spp.) damage to corn in notillage fields compared with plowed fields reflected lower herbivore densities (Stinner et al., 1986). Although spider density was highest in no-tillage systems, predators in general did not exhibit higher densities. In such cases efficiency instead of abundance of predators and parasitoids may be enhanced; the vegetative component may provide alternative resources to entomophages. For example, Foster and Ruesink (1984) showed that the flowering weeds associated with reduced tillage in corn are important nectar sources that increase survival and fecundity of the braconid Meteorus rubens (Nees), an important parasitoid of the black cutworm.

Chapter 14 EnvironmentalManagement to Enhance Biological Control in Agroecosystems Ants are generalist predators sensitive to tillage practices in agroecosystems (Risch & Carroll, 1982). Altieri and Schmidt (1984) report greater species richness, abundance, and predation pressure in uncultivated orchard systems than in those cultivated twice in 6 weeks. Lack of nest disturbance and habitat suitability due to vegetational cover may have been important causes of greater ant abundance. Similar results were predicted for a highly effective predator of bollworm [Heliothis zea (Boddie)] Iridomyrmex pruinosis (Rogers), in Arkansas cotton fields (Kirkton, 1970) based on field observations. Carroll and Risch (1983) and Letourneau (1983) sampled ant activity in lowland tropical Mexico where farming practices are in transition between slashand-burn and mechanized cropping practices. The number of ant species at tuna baits in maize fields was similar whether they had been plowed or sown into slash (20 to 23 spp.). However, in central Texas, spring plowing decreased and species richness (as detected with surface and underground baits) from 12 species to 2 species. Among the species that were no longer present at baits (after plowing) were species that prey on Solenopsis invicta Buren queens (C. R. Carroll, personal communication 1985). Pests also can be suppressed directly by plowing the soil (Watson & Larsen, 1968) and burying stubble (Holmes, 1982). For example, Talkington and Berry (1986) significantly reduced the adult emergence of Fumibotys fumalis (Guenre), a pyralid moth pest, in peppermint fields by burying the prepupae into the soil; tillage depth was directly correlated with level of reduction. In locations where natural enemies are not effective, deep burial of infested stubble with the conventional moldboard plow may be necessary to effect control of a pest (Umeozor et al., 1985). The study by Telenga and Zhigaev (1959) on Bothynoderes punctiventris Germer, the beet weevil, however, shows how differential effects on pests and their natural enemies can be achieved through carefully planned tillage practices. Although deep plowing action destroyed over 90% of the weevil eggs, surface tillage with a disk increased the survival of a parasitoid on those eggs, which ultimately caused a greater level of pest suppression than did deep plowing. Disk-harrowed or plowed plots produced substantially fewer parasitoids of Meligethus sp. pollen beetles than did fallow fields or plots of rape that had had direct drilling of winter wheat (Nilsson, 1985). The effects of these practices on parasitism rates were not studied, but a regional use of direct drilling was recommended. A more subtle effect of plowing involves its impact on weed composition in the field. Studies in northern Florida (Altieri & Whitcomb, 1979a, 1979b) have shown that weed-species composition changes markedly with date of plowing. December plowing stimulated populations of goldenrod (Solidago altissima Linnaeus) (Campanulaceae) and also 58 predator species that feed on the aphids (Uroleucon spp.) and other herbivores associated with this weed.

331

By plowing the land in October, camphor weed populations were enhanced along with the 30 predator species associated with camphor weed herbivores.

Mowing, Harvesting, and Weeding Pruning and mowing crops often results in (1) the arthropod movement from cut plant material, and (2) a period of new growth. These factors can have important consequences on the quality and synchrony of natural-enemy activity. Weeding can also stimulate crop colonization by associated arthropods. The extent to which movement will occur depends on distance and arthropod mobility, but some weeding practices leave associated arthropods intact and promote such movement. When patches of stinging nettle (Urtica dioica Linnaeus) (Urticaceae) are cut in May or June, predators (mainly Coccinellidae) are forced to move into crop fields (Perrin, 1975). Similarly, cutting the grass-weed cover has been reported to drive Coccinellidae onto trees in orchards of southeastern Czechoslovakia (Hodek, 1973). Gange and Llewellyn (1989) manipulated the movement of both males and females of the predatory black-kneed capsid[Blepharidopteris angulatus (Fallrn)] from alder windbreaks to orchards by timing tree pruning with peak aphid densities on Alnus. Some of the best examples of natural-enemy movement prompted by vegetation cutting were shown in alfalfa stripcutting systems. Van den Bosch and Stern (1969) compared densities of several predators, including Geocoris pallens Sthl, Nabis americoferus Caryon, Orius tristicolor White, Chrysoperla carnea (Stephens), and Hippodamia spp. in strip cut and solid cut fields. Movement out of the field was uncommon even for these mobile predators in strip cut fields; most of them moved onto adjacent plants, so that on a field-wide basis these predators were conserved. Strip cutting also reduced mortality of Aphidius smithi Sharma & Rao by providing shelter from adverse physical conditions and host scarcity. Host availability for the parasitoid Cotesia medicaginis (Muesebeck) in alfalfa is altered through a different mechanism; oviposition rates of the alfalfa butterfly Colias philodice eurytheme Godart peak on new growth following harvest. This causes periodicity in the availability of early instar larvae. Strip cropping can spread the vulnerable stages more evenly over time, and thus can favor the maintenance of A. medicaginis populations over the season. The use of fire to prepare land for cropping by "slash and burn" or by reducing crop residue affects resident natural enemies and incoming colonists. Burning of old, fallow vegetation in a tropical slash-and-burn system decreased ant abundance and foraging activity for more than 4 months (Saks & Carroll, 1980). Although fire has been used as a tool for direct control of pests (Komareck, 1970), generalizations on its effect on natural enemies are not possible. An isolated study showed that controlled burning increased spi-

332

D.K. Letourneau and M. A. Altieri

der and ant densities and biomass due to increased food supply for herbivores in the form of succulent plant growth after the burn (Hurst, 1970). Little is known about specific taxa, and much less is known about effects of fire on predator to prey ratios, arthropod community structure, and habitat suitability. Chemical Inputs to t h e S y s t e m Fertilizer, irrigation, and pesticide treatments are important components of production strategies in modern agricultural and silvicultural systems. Although the influence of water and fertilizer applications on herbivores is complex (Scriber, 1984; Louda, 1986), fertilizer and herbivory levels may be causally related through changes in plant quality or phenology that affect the dynamics of predator-prey and host-parasitoid interactions. Pesticides, however, have direct detrimental effects on natural enemies and therefore their use in environmental management must be limited to situations where they are timed carefully or selectively applied. Novel advances in the use of behavior-modifying chemicals (Lewis & Nordlund, 1985; Lewis & Martin, 1990) provide powerful new tools for the manipulation of biological control agents. Pollutants can also disturb biological control of crop pests and are discussed later. Fertilizer

Soil amendments can have a profound effect on the physiological condition of a crop plant. Consequences of these changes for pest management depend on soil variability; the growth, developmental, and biochemical responses of the plant; the direct effects of these changes on herbivores; and the secondary impact on natural enemies. A considerable amount of work has been done on herbivore response to fertilizers that increase nitrogen (N) levels in plants. Mattson (1980) suggests that foliage N level is a major regulator of herbivory rate. Although increased plant quality (higher N) commonly leads to improved performance by individual insects (e.g., growth rates, survival, and fecundity), general statements on the direct responses of herbivores to N fertilizer are not possible due to the array of responses by different species (Scriber, 1984; Letourneau, 1997). Other experiments on links between soil amendments and pest management concern effects on the pest via their response to resistant and susceptible varieties under conditions of different sources or levels of calcium, magnesium, nitrogen, phosphorus (P), potassium (K), or sulfur (Kindler & Staples, 1970; Manuwoto & Scriber, 1985; Culliney & Pimentel, 1986; Shaw et al., 1986; Davidson & Potter, 1995). The environment of a natural enemy is affected by soil amendments through changes in plant quality, as well as by concomitant changes in the herbivores.

Direct effects of fertilizer on biological control are not well documented. Many herbivores exhibit marked increases in population growth on nitrogen-enriched hosts. Concern emerges for the ability of natural enemies to track their prey/hosts under these conditions, but biological control of mites was maintained among apple treated with three levels of nitrogen fertilizer (Huffaker et al., 1970). Although the fecundity of the herbivore Panonychus ulmi (Koch) increased with N level up to a fourfold increase when Amblyseius potentillae (Garman) predators were not present, the predators were able to compensate for most of the increase in prey reproduction. In contrast, fertilized (NPK) cotton plots exhibited higher levels of Heliothis zea than did control plots despite significantly higher population densities of Hippodamia convergens Gu6rin-M6neville, Coleomegilla maculata langi Timberlake, and Orius insidiosus (Say) in fertilized cotton (Adkisson, 1958). Chiang (1970) demonstrated that fertilized midwestern corn fields (at 50 tons of manure per acre) had significantly fewer (half) corn rootworms than did unfertilized control plots. Although ground beetles and spiders were not affected, the populations of predaceous and herbivorous mites were three times higher in manure treatment plots. Through three seasons of field and laboratory experiments, Chiang concluded that predation by mites accounted for a 20% control of corn rootworm under natural field conditions and a 63% control when manure was applied. Other effects of fertilizers on natural enemies may be predicted based on the combined information of related studies. For example, the parasitoid Diaretiella rapae (McIntosh) attacks the green peach aphid Myzus persicae (Sulzer) more readily when the aphid is associated with Brassica spp. (Read et al., 1970). The mustard oils in crucifers serve as attractants for the wasp. It has also been shown-demonstrated that some glucosinolates are inversely related to N fertilizer level (Wolfson, 1980). Therefore, soil fertility may have dramatic effects on pest control by constraining the production of semiochemicals that play an important role in mediating interactions between plants, herbivores, and natural enemies. Synchrony of predators and their prey can be modified by frequency and levels of fertilizer applications. For example, low nutritive quality of host plants may cause immature herbivores to develop more slowly, thus increasing their availability to natural enemies (Feeny, 1976; Moran & Hamilton, 1980; Price et al., 1980). For example, a predaceous pentatomid bug regulated more efficiently Mexican bean beetles on nutritionally poor plants than it did on highly nutritional ones (Price, 1986). Benrey and Denno (1997) showed that Pieris rapae larvae that developed slowly had higher parasitism rates by Cotesia glomerata than did larvae that grew more rapidly on the same hostplant species. If fertilizer increases the nutritive value of crops, then pests may grow more rapidly or feed more

Chapter 14 EnvironmentalManagement to Enhance Biological Control in Agroecosystems efficiently, thus passing through windows of vulnerability more often (see Bernays, 1997). Host-plant phenology can also be driven by fertilizer inputs. Hogg (1986) suggests that the timing of square availability was one factor influencing predation and parasitism rates of H. zea in cotton. Although his data are taken from early- and late-season peaks in square production, and not from changes caused by soil fertility, they are indicative of indirect effects of plant quality that could be influenced by fertilization. Fertilizer-caused changes in nutritive quality of host plants may indirectly affect the survival and reproduction of natural enemies by determining prey quality. Although direct examples of fertilizer effects have not been determined experimentally, nitrogen content is an important aspect of prey quality. For example, nitrogen content may be responsible for higher egg production by H. convergens when fed apterous instead of alate green peach aphids (Wipperfiirth et al., 1987). Analogous effects may occur with prey of different quality due to host-plant condition. Zhody (1976) found that size, fecundity, and longevity of the aphelinid wasp Aphelinus asychis (Walker) was dependent on the food composition of its host Myzus persicae. However, low-quality food can also impair the ability of a host to encapsulate the parasitoid (E1-Shazley, 1972a, 1972b). Nutrients in the host plant also can modify toxic effects to parasitoids (Duffey & Bloem, 1986) and can influence their sex ratio (Greenblatt & Barbosa, 1981). Host size is often an important determinant of egg fertilization by ovipositing females (Charnov, 1982). The sex ratio of Diadegma insulare (Cresson) reared from larvae of Plutella xylostella Linnaeus from field plots over a wide range of N fertilizer inputs showed a strong tendency for female bias in heavily fertilized plots (Fox et al., 1990), and Jansson et al. (1991) found increased parasitism rates in high N fields. Rates of host feeding by Encarsia formosa Gahan on whiteflies were higher on fertilized host plants (Bentz et al., 1996). Although studies on direct effects of nitrogen on crop architecture and subsequent effects on searching efficiency are not available, some studies suggest that these interactions can occur. Soil nutrient levels can influence plant size, leaf area, canopy closure, and crop architecture. These conditions define searching arenas for natural enemies (Kemp & Moody, 1984). Predator-prey or parasitoid-host contact rates are a function of habitat preference, searching area, prey density, and dispersion patterns. For example, Fye and Larsen (1969) found that the searching efficiency of Trichogramma spp. was dependent on structural complexity. Hutchison and Pitre (1983), however, did not find such an effect for Geocoris punctipes (Say) on H. zea. Shady conditions resulting from overgrowing vegetation reduced parasitism levels of Pieris spp. by Cotesia glomerata (Linnaeus) (Sato & Ohsaki, 1987). In addition to direct effects of fertilizer on host-plant

333

growth form, levels of key chemical constituents in the soil can indirectly affect natural-enemy activity by influencing weed composition in a field. Fields in Alabama, with low soil potassium, were dominated by buckhorn plantain (Plantago lanceolata Linnaeus) (Plantaginaceae) and curly dock (Rumex crispus Linnaeus) (Polygonaceae), whereas fields with low soil phosphorus were dominated by showy crotalaria (Crotalaria spectabilis Roth.) (Fabaceae), morning glory (Ipomoea purpurea Roth.) (Convolvulaceae), sicklepod (Cassia obtusifolia Linnaeus) (Fabaceae), Geranium carolinianum Linnaeus (Geraniaceae), and coffee senna (Cassia occidentalis Linnaeus) (Fabaceae) (Hoveland et al., 1976). Soil pH can influence the growth of certain weeds. For example, weeds of the genus Pteridium occur on acid soils while Cressa sp. inhabits only alkaline soils. Other species (many Compositae and Polygonaceae) grow in saline soils (Anonymous, 1969). Water

Flooding fields, draining land, and irrigating crops with furrow, drip, or sprinkler methods can affect plant quality and relative humidity (RH) at field level and are all manipulations that can affect biological control on a local scale. The barren desert valleys of southeastern California are suitable habitat for the predaceous earwig Labidura riparia (Pallas) due to favorable conditions produced with the development of irrigation agriculture (van den Bosch & Telford, 1964). Expansion of arable land through irrigation in the developing regions of Africa, Asia, and South and Central America may have global effects on the distribution of natural enemies. As in the case of fertilizer research, much experimental work on the effects of plant stress from water conditions has targeted herbivores (e.g., Miles et al., 1982; Bernays & Lewis, 1986; Louda, 1986). Water availability can affect palatability, feeding duration, developmental time, migration, survival, and fecundity of plant feeders. Thus, many important effects of water conditions on natural enemies are indirect and are mediated through changes in host/prey abundance and dispersion or through qualitative changes similar to those discussed in the previous section (fertilizer). For example, rape plants under drought conditions had increased proline levels and an associated shift in the balance of free amino acids (Miles et al., 1982). Cabbage aphids reached adulthood much faster on these stressed plants. Availability of suitable hosts for parasitoids may be decreased both temporally (duration of vulnerable stages) and absolutely (if parasitoids require slower development than the host) if plants are not well watered. Direct effects of water include mortality during irrigation and impacts of relative humidity. Ferro and Southwick (1984) and Ferro et al. (1979) review the importance of RH on small arthropods. Crop architecture and watering re-

334

D.K. Letourneau and M. A. Altieri

gimes cause large deviations from ambient temperature and humidity levels (Ferro & Southwick, 1984) within foliage boundary layer microhabitats. Irrigation of soybean caused a substantial (4 to 9~ decrease in canopy temperature and a 16% increase in RH 15 cm above the ground (Downey & Caviness, 1973). Prolonged periods of such irrigation effects can have important consequences for natural enemies because developmental time, and thus population growth and synchrony, are driven by temperature and RH. The tachinid Eucelatoria armigera (Coquillett) completes development at different rates depending on temperature and host species (Jackson et al., 1969). Holmes et al. (1963) showed that parasitism levels of the wheat stem sawfly by Bracon cephi (Gahan) were enhanced by soil moisture and temperature levels that slow plant ripening. Early initiation of pivotal irrigation in Mississippi soybean fields caused rapid canopy closure that allowed establishment of Nabis spp. to be synchronized with the presence of lepidopteran larvae whereas Nabis spp. levels increased too late in the season in dryland soybeans (Felland & Pitre, 1991). Leigh et al. (1974) also reported highest population levels of Geocoris pallens Sthl, G. punctipes (Say), and Orius tristicolor in dense canopies encouraged by both irrigation and close spacing of a cotton crop. Force and Messenger (1964) showed that a few degrees dramatically affect changes of the innate capacity for increase (r) in parasitoids under laboratory conditions. Cotesia medicaginis reaches its maximum longevity at 55% RH; longevity decreased sharply at levels above and below that value (Allen & Smith, 1958). This was not deemed an important factor, however, in determining parasitism levels of Colias spp. larvae in alfalfa. However, it is known that scale parasitoids in arid citrus groves require irrigated conditions for effective biological control (DeBach, 1958b). The vertical profile and general microclimate depend not only on water inputs but also on mulch practices, row direction, windbreaks, and crop spacing (Hatfield, 1982), all of which are manipulable. Apparently the severity of effects caused by drought conditions depends on many factors, including the availability of free water and nectar in the habitat. Bartlett (1964) found that caged Microterys flavus (Howard) adults were able to function well at extremely low RH if provided with a honey-water mixture. It may be possible to favor mobile natural enemies at the expense of their hosts with the provision of water sources during drought conditions. Use of Semiochemicals

The discovery that the behavior of certain parasitic insects is influenced by chemicals produced by their hosts triggered considerable interest in the use of semiochemicals for manipulating predators and parasitoids in the field, especially for aggregating and/or retaining released parasi-

toids in target locations (Gross, 1981). The various opportunities for, and limitations of, manipulating natural enemies using semiochemicals have been reviewed by Vinson (1977); Nordlund et al. (1981a, 1981b, 1988); Powell (1986); Hagen (1986); and Lewis and Martin (1990). According to Lewis et al. (1976), host or prey selection is perhaps the most important step in the searching behavior of entomophagous insects that can be manipulated to improve biological control. The use of semiochemicals should be directed at (1) increasing effective establishment of imported species, (2) improving performance and uniform distribution of released species throughout the target area, and (3) optimizing abundance and performance of naturally occurring entomophages (Greenblatt & Lewis, 1983). Based on the environmental factors that influence search behavior, it is possible to devise three main habitat management techniques using semiochemicals: 1. Directing strategies at improving habitat characteristics: use of semiochemicals to make crops more attractive, or to define a more complex mosaic of local search areas (Altieri et al., 1981, but see Gardner & van Lenteren, 1986) 2. Enhancing host plant characteristics: breeding programs directed at improving chemical attractiveness of crops or crops with extrafloral nectaries 3. mimicking high-pest densities through application of diatomaceous earth or artificial eggs impregnated with kairomones (Gross, 1981) Lewis and Martin (1990) encourage research on multitactic semiochemical packages that combine mating, oviposition, and feeding deterrents with formulations to increase parasitism of crop pests. Advances in the chemical mediation of these interactions (e.g., Williams et al., 1988), the effects of parasitoid adaptation and learning (Lewis et al., 1990; Kester & Barbosa, 1991; Turlings et al., 1993), and an evaluation of the potential for resistance to develop (e.g., Turlings & Tumlinson, 1991) will allow wise application of these habitat management techniques. Pesticide Drift

Aerial application of insecticides inevitably results in low-level inputs to nontarget areas. Indeed, half the material applied to a field under ideal conditions can drift a considerable distance downwind (Ware et al., 1970). Is inadvertent disruption of natural enemies a common consequence of dilute pesticide inputs downwind of a target field? Although a great deal is known about the effects of direct spraying of various insecticides on natural enemies, now including community level effects (e.g., Croft & Slone 1997), very little experimental work has been conducted to determine effects of low-level inputs (see Chapters 13 and 24). Biological control will be disrupted given sufficient

Chapter 14 EnvironmentalManagement to Enhance BiologicalControl in Agroecosystems frequency, intensity, and toxicity of sprays (Ridgway et al., 1976; Riehl et al., 1980) even if dosages are sublethal (e.g., De Cock et al., 1996). However, Risch et al. (1986) found that the ratio of natural enemies to herbivores was increased by low, driftlevel concentrations of carbaryl. Furthermore, they found that arthropod abundance dropped significantly more in an old field than it did in a corn monoculture. Their results suggest that: (1) low concentrations of insecticides have different effects on herbivores and natural enemies depending on whether the nontarget habitat is a crop field or a field of natural vegetation that serves as a source of colonizers, and (2) these impacts cannot be predicted from a knowledge of effects at high concentrations. Chemical drift can be minimized by spraying when winds are less than 2 m/sec, using adjuvants, formulating inert emulsions, and using larger droplet sizes (Gebhardt, 1981). Windbreaks surrounding field and regional-wide spray synchrony are forms of cooperative efforts for drift reduction of the effects of low-level pesticide applications. Although not a problem of drift, purposeful sprays of herbicides to crop fields can have nontarget effects similar to low-level insecticide application. Baker et al. (1985) have shown that Orius spp. and Nabis spp. densities were decreased by monosodium methanearsenate, but the abundance of spiders, Geocoris spp., Hymenoptera, and coccinellids was not. Herbicide application can also modify weed species composition in agricultural fields and thereby affect natural enemies (see section on the effects of vegetational diversity). Dust and Pollution Effects

Dust and pollutants of many types can influence the efficacy of predators and parasitoids as biological control agents. Environmental management then includes consideration of placement of the sources and control of pollutant influx with respect to agricultural fields. It has long been known that some pest outbreaks are caused or exacerbated by dust-fall on crop foliage. Bartlett (1951) found that many "inert" dusts (as described on the pesticide manufacturer's label) rapidly killed Aphytis chrysomphali (Mercet) and Metaphycus luteolus (Timberlake). Experimental tests by DeBach (1958a) demonstrated an increase in California red scale populations on citrus trees in response to the application of road dust to plants [and see references in van den Bosch & Telford (1964)]. Mechanisms may be mechanical interference or desiccation (Edmunds, 1973). It is also possible that leaf temperature, which can be raised 2 to 4~ by dust cover (Eller, 1977), is a relevant factor. Planned placement of roads and timing of cultivation can reduce the level of dust-fall on crops. Strawberry growers in California profit from daily or twice-daily watering of roadways through the reduction in losses from mites. Ap-

335

parently, the dust inhibits biological control of phytophagous mites by predaceous species. The influx of gaseous air pollutants is more difficult to detect and to control. Sulphur dioxide is a common effluent that has documented, negative effects on a variety of organisms (Petters & Mettus, 1982), including honeybees (Ginevan et al., 1980). However, acute exposure of Bracon hebetor (Say) females to SO2 in air causes no reduction of their fertility and fecundity. Petters and Mettus (1982) suggest that damage to parasitic wasps may accrue in the earlier stages, or behavioral avoidance of contaminated areas may explain reports of lower parasitoid and higher herbivore levels near sources of SO2 pollution than on crops distant from the course. Melanic morphs of the generalist coccinellid predator Adalia bipunctata (Linnaeus) occur disproportionately often in the vicinity of coal-processing plants in the United Kingdom. Although earlier investigators suggested a mechanism involving selective toxicity of air pollutants, Muggleton et al. (1975) attribute the differences to sunshine levels (negatively correlated with smoke). Whether the coloration of such predators affects their efficiency as biological control agents is not known. Other sources of contamination include auto traffic, drainage from selenium-rich soils (Gerling, 1984), and ozone (Trumble et al., 1987). The literature on these contaminants addresses direct effects on herbivores, but little is known about effects on natural enemies. We could speculate about indirect effects based on current knowledge. For example, the impact of ozone depletion on ultraviolet (UV) radiation, which interacts with plant secondary compounds to slow larval development (Trumble et al., 1991), may result in increased exposure time of hosts to parasitoids. Lead as a contaminant from auto exhaust, now regulated in some areas, has been reported to concentrate in higher trophic levels (Price et al., 1974). Any such concentration of toxic compounds potentially sets up conditions that favor pests. Some pollutants are inadvertently added to the crop field with soil amendments, such as sludge, manure, and chemical fertilizer (Wong, 1985). Suggestions to use sewage sludge as a nutrient source for crops constitute a clever solution to both waste management and soil fertilization. However, Culliney et al. (1986) found a general response of low arthropod diversity when sludge containing heavy metals and toxic chemicals was applied to cole crops. This type of response is common in communities under pollution stress.

MECHANISMS OF ENEMY ENHANCEMENTS An examination of host-selection processes of entomophagous insects, including host or prey habitat location, host or prey location, and host or prey acceptance (Vinson, 1981), can provide insights into the biological mechanisms

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D.K. Letourneau and M. A. Altieri

by which environmental management enhances biological control. The purposeful design of crop habitats for effective biological control requires a detailed understanding of such mechanisms through basic research. Two initial guidelines among the complex set of interactions between the environment and natural enemies are useful for consideration: (1) the effective environment must be redefined for each phase of host or prey search, and (2) enemies differ in their response to environmental management schemes. During migration and habitat location, the effective environment may be the local area, a regional landscape, or a series of distant habitat patches with long-distance travel between them. The interplay of colonizer source location, wind patterns, vegetation texture, and host or prey density becomes important on a large scale. Maximum levels of natural control require at the onset both sufficient numbers of natural enemies and temporal synchrony of these invasions. Regional environmental management for enhancing the success of habitat location by natural enemies then would focus on the arrangement of colonizer sources in relation to target sites of potential pest problems as well as on the timing of enemy colonization. Rabb (1978) addressed these needs when he criticized the propensity of single commodity, closed system approaches to pest management in research and decision making as deficient for problems that demand attention to "large unit ecosystem heterogeneity." Dispersal ranges of natural enemies vary. Migration often occurs in high currents along paths of turbulent convection. Even weak flying insects can disperse over long distances and across wide areas by exploiting the ephemeral but very structured nature of air movement (Wellington, 1983). For example, robust hosts and minute parasitoids can exhibit coupled displacement in long-distance migration, as shown by the Australian plague locust, Chortoicetes terminifera Walker and its egg parasitoid, Scelio fulgidus, Crawford, which disperse independently on wind currents to the same location (Farrow, 1981). Cumulative numbers over a growing season, however, may be irrelevant if immigration rates of natural enemies are very slow in relation to rising levels of the pest (Doutt & Nakata, 1973; Letourneau & Altieri, 1983; Williams, 1984). Information on source constitution, phenology, and flight patterns then are necessary to design and manage regional-scale agroecosystems for optimal biological control. Flight capacity studies and mathematical models to describe movement patterns based on continuous diffusion or discrete random walk equations have focused on predicting dispersal and migration of herbivores (Okubo 1980; Stinner et al., 1983, 1986). Detailed biological information (Duelli, 1980) coupled with predictive models of natural-enemy movement may aid in predicting synchrony. In some cases, synchronies are difficult to achieve because local species are adapted to exploit natural conditions of prey or host phenologies. For exam-

pie, coccinellid beetles in California estivate during times of prey availability; irrigated crops provide a continuous food supply that was not available before agricultural expansion occurred (Hagen, 1962). During host or prey location, factors such as the physical texture of plant surfaces, chemical and structural attributes of plants, microclimatic conditions, and patch heterogeneity come into play. Flaherty (1969) showed enhancement in the control of herbivorous mites on grape vines with Johnson grass ground cover. The grass acted as a source of predaceous mites. In the prey location study of Flaherty (1969) and in the habitat location phase study of Doutt and Nakata (1973), the cumulative total number of natural enemies was not as important as the temporal synchrony with growing herbivore populations. Coil and Bottrell (1996) found that plant structural characteristics were important determinants of parasitism levels in monocultures versus mixed crop stands of the Mexican bean beetle. During host or prey acceptance and predation or parasitism, environmental factors operate indirectly through their effects on host or prey behavior and on host or prey quality, and alter levels of vulnerability of natural enemies to mortality factors. Examples of the mechanisms of host or prey selection on all levels of enemy behavior are provided in Table 5. Cutting across these levels of behavioral organization are activities other than those directly associated with predation or parasitism such as migration to overwintering sites, mating, and acquisition and use of resources other than the primary prey or hosts. Therefore, the interdependence and variability of resource needs and factors such as proximity and availability of resources in time become vital aspects of the environment. These are factors of "habitat suitability" for natural enemies; a reduction of the relative energy expenditure needed, in a particular environment, to fulfill the resource needs of a particular parasitoid or predator will increase its efficiency as a biological control agent. Conservation of natural enemies through habitat management techniques adapted to the prevailing agronomic schemes then can be of great benefit to farmers. Small changes in agricultural practices may increase natural-enemy populations or enhance efficacy. However, predators and parasitoids are extremely diverse and each family represents a particular range of responses to environmental modification as well as a range of effectiveness as biological control agents (e.g., McMurtry & Croft, 1997). Several examples of habitat management techniques that have been reported to increase the effectiveness and abundance of specific predator groups are given in Table 6. Although each of the management practices discussed in this chapter can, as single factors, affect the abundance, richness, and efficacy of natural enemies, they also interact in ways that can be complementary, disruptive, or simply unpredictable. Brust (1991) found that tillage practices, organic matter, and irrigation regimes interacted to determine

Chapter 14 TABLE 5

337

Environmental Management to Enhance Biological Control in Agroecosystems

M e c h a n i s m s of Predator or Prey Efficacy in S u p p r e s s i n g Pests, Including Long- and Short-Range Host or Prey Selection

Enemy

Herbivore

Plant

Mechanism

Reference

Flint et al., 1979; van Emden & Hagen, 1976; Hagen 1986 (and references within) Thrope & Caudle, 1938

Host/Prey Habitat Location Chrysoperla carnea

Aphids

Cotton

Detection of caryophyllene from foliage; detection of indole acetaldehyde from honeydew and phenology-specific plant volatile by gravid females

Exeristes ruficollis Grav. (Hymenoptera: Ichneumonidae) Diaretiella rapae

Pine shoot moth

Cotton

Attraction to pinene and oil of pine as gravid female

Cabbage aphid

Crucifers

Attraction to allyl isothiocyanate; increased parasitism

Trichogramma spp.

Heliothis zea

Soybeans

Campoletis sonorensis (Cam.) (Hymenoptera: Ichneumonidae) Collops vittatus Say (Coleoptera: Melyridae) Microplitis demolitor (Hymenoptera: Braconidae)

H. virescens

Cotton, sorghum

Response of gravid females to volatiles of Amaranthus retroflexus Plant volatiles attract parasitoid to host habitat

Aphids

Cotton

Pseudoplusia includens

Soybeans

T. minutum Riley and T. pretiosum Riley (Trichogrammatidae) Leptopilina clavipes (Hartig) (Hymenoptera: Eucoilidae)

H. virescens

Soybeans and natural vegetation

Drosophila sp.

Fungus

Trichopoda pennipes (F.) (Diptera: Tachinidae) Trichogramma spp. and Chelonus sp. (Hymenoptera: Trichogrammatidae & Braconidae) T. brassicae

Green stink bugs

Coccinellid adults Aphidoletes aphidimya (Rondani) (Diptera: Cecidomyiidae) Amblyseius fallacis (Garman) (Acari: Phytoseiidae) and Phytoseiulus macropilis (Banks) (Acari: Phytoseiidae) Amblyseius limonicus Garman & McGregor, A. californicus (McGregor), A. anonymus Chant & Baker, Cydrodromella pilosa (Chant) (Acari: Phytoseiidae) Coleomegilla maculata and Geocoris punctipes

Male response to caryophyllene in foliage 7- and 8-Carbon hydrocarbons, aldehydes and ketones attract parasitoid to plant Discrimination preference for hosts at different heights

Read et al., 1970; Titayaavan & Altieri, 1990 Altieri et al., 1981 Elzen et al., 1983

Flint et al., 1981 Ramachandran & Norris, 1991 Flanders, 1937; Thorpe, 1985

Attracted to odor of mushrooms at stage of decay most likely to contain young maggots Attracted to sex pheromones of hosts

Vet, 1983

Pink bollworm

Intense searching response to hexane soluble chemical in moth scales

Ostrinia nubilalis Hbn. and Mamestra brassicae L. (Lepidoptera: Pyralidae & Noctuidae) Aphids

Egg extracts cause upwind locomotion

Jones et al., 1973; Chiri & Legner, 1983; and see Wang & Zong (1991) Renou et al., 1992

Aphid

Tetranychus urticae Koch (Acari: Tetranychidae)

Harris & Todd, 1980

Arrest response to simple sugars in honeydew Oviposition stimulus from honeydew

Wilbert, 1977

Attraction/arrestment by prey kairomones

Hislop & Prokopy, 1981

Hagen, 1986

Monochychellus tanajoa (Bondar) (Acari: Tetranychidae)

Cassava

Attraction to mite-infested leaves

Janssen et al., 1990

H. zea and Spodoptera frugiperda

Corn

Aggregation responses to aqueous larval homogenates

Gross et al., 1985

(continues)

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D.K. Letourneau and M. A. Altieri

TABLE 5 (continued) Enemy

Platycheirus spp. and Syrphus spp. (Diptera: Syrphidae) Anthocorids

Brevicoryne brassicae

Brassica spp.

B. brassicae

Encarsia formosa Gahan (Hymenoptera: Aphelinidae)

Trialurodes vaporariorum (Westwood) (Homoptera: Aleurodidae) H. zea

Brussels sprouts (Brassica oleracea gemmifera (Brassicaceae) Hirsute cucumber varieties

Trichogramma pretiosum and Chrysopa rufilabris Burm. (Neuroptera: Chrysopidae) Predaceous mites

Hirsute cotton varieties

Herbivorous mites

Ficus carica L. (Moraceae)

Bessa harveyi (Townsend) (Diptera: Tachinidae) Adalia bipunctata

Larch sawfly

Larch

Aphids

Radishes and Chinese cabbage

Coccinellids

Aphids

Hirsute potato varieties

Coleomegilla maculata

Ostrinia nubilalis

Corn

Phytoseiulus persimilis

Tetranychus urticae

Orius tristicolor

Predaceous mites

Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) Eotetranychus willamettei (Ewing) (Acaft: Tetranychidae) Lygus lineolaris (Palisot de Beauvois) (Heteroptera: Miridae) Tetranychid mites

Lima bean Phaseolus lunatus Squash

Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae)

Spodoptera exigua (Htibner) (Lepidoptera: Noctuidae)

Metaseiulus occidentalis (Nesbitt) (Acari: Phytoseiidae) Peristenus pseudopallipes (Loan) (Hymenoptera: Braconidae)

Mechanism

Plant

Herbivore

Grapes

Apples and peaches

Corn seedlings

Reference

Chandler, 1968

Visual detection of aphid (or colored paint) aggregations stimulated oviposition Deterred by waxy leaves

Way & Murdie, 1965

Trichome mat hinders movement and searching efficiency

Hulspas-Jordaan & van Lenteren, 1978

Increased trichome density reduced ability for small predators to locate and destroy host-prey Glandular hairs correlated with increased or decreased rate of prey consumption depending on predator species Nonhost odors reduce host finding

Treacy et al., 1985

Nonglandular hairs caused larvae to change direction more frequently and thereby encounter prey more frequently Reduction in adult searching time; larval mobility impaired; but these effects were attenuated in the field Presence of nonhost plants increased searching area and decreased predation efficiency Damaged host plant produces volatiles attractive to predators Presence of other plant species enhanced early colonization of predators and improved synchrony

Shah, 1981

Close proximity of colonizer source allows improved synchrony

Flaherty, 1969

Odor of flowering Erigeron spp. attracted parasitoids

Shahjahan, 1974

Possible role of pubescence in determining predator-prey contact rates on different plants Volatiles from damaged leaves attract female wasps

Putnam & Herne, 1966

Rasmy, 1977; Rasmy & Elbanhawy, 1974

Montieth, 1960

Obrycki & Tauber, 1984 Risch et al., 1982

Dicke et al., 1990 Letourneau & Altieri, 1983; Letourneau, 1990

Turlings et al., 1991

Host/Prey Acceptance and Suitability

Hyposoter exiguae (Viereck) (Ichneumonidae)

H. zea

Tomatoes

Increased tomatine in host-plant reduced adult parasitoid longevity, size, and survival

Campbell & Duffey, 1979

(continues)

Chapter 14

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Environmental Management to Enhance Biological Control in Agroecosystems

TABLE 5 (continued) Herbivore

Enemy

Mechanism

Reference

Predators attacking prey on resistant varieties had increased mortality rates Match of effective parasitoid species with preferred hosts to increase parasitism levels in different crop habitats

Rogers & Sullivan, 1986 Johnson & Hara, 1987

Plant

Geocoris punctipes

Anticarsia gemmatalis

Soybeans

Eulophid parasitoids

Liriomyza spp. (Dip-

Various crops

tera: Agromyzidae)

Functional and Numerical Response

M. occidentalis

Tetranychus urticae

Amblyseius hibisci (Chant)

Oligonychus punicae

(Phytoseiidae)

Strawberries

(Hirst) (Acari: Tetranychidae)

levels of predaceous arthropod activity in peanut agroecosystems; predators were not important regulators of Diabrotica undecimpunctata howardi Barber (southem corn rootworm) in conventionally tilled, dry farmed systems, but decreased tillage or increased irrigation or both enhanced most predators. Henze and Sengonca (1992) showed how crop rotation schemes can influence weed composition and crop to weed ratios, which affect aphid densities, and aphid to coccinellid ratios. Increased coccinellid densities may respond to stand density, with different species preferring dense plantings [e.g., Propylea quatrodecimpuncta (Linnaeus)] and more sparse plant stands (e.g., Coccinella spp.) (Honek, 1983). Comparative studies of different suites of management practices such as in organic versus conventional production systems (Andow & Hidaka, 1989; Kromp, 1989; Pfiffner, 1990; Drinkwater et al., 1995) provide integrative, system level effects on natural enemies in crop habitats.

THEORETICAL ASPECTS OF ENVIRONMENTAL MANAGEMENT Enemy-Free Space Perhaps the most general level of theory to guide habitat management for biological control is that of ecological and/ or evolutionary escape from predators and parasitoids. Price (1981) acknowledges, in his theory of enemy-free space, that pest irruption is a likely consequence of agricultural practices that foster the spatial and temporal isolation of herbivores from their natural enemies (Price, 1981; Altieri & Letourneau, 1982, 1984; Risch, 1987). Bernays and Graham (1988) postulate that the evolution of diet specializa-

Prey fecundity increased with N level in plants, but functional and numerical response of predator compensated at least 80% Numerical increases in predator population due to pollen availability

Hamai & Huffaker, 1978

McMurtry & Scriven, 1966, 1968

tion in insect herbivores could be due to the escape of specialists from their natural enemies. Denno et al. (1990) offer supporting evidence for willow beetles. Pest introduction to a novel environment is a classic example of relatively enemy-free conditions when specialized consumers on herbivores are left behind. Temporary release of pests also occurs under conditions of insecticide-caused pest resurgence and secondary pest outbreaks. Evolutionary changes in native crop pests (host shifts) constitute yet another process that may result in a reduction of predation or parasitism pressure. It has been our objective in this chapter to review ways to reduce enemy-free space through environmental manipulations. It is our contention that theory and basic research contribute vital knowledge for designing and integrating methods to enhance, instead of to mitigate, the ecological factors that cause herbivores "to be caught between the devil" (natural enemies) "and the deep blue sea" (host-plant defense/nutrient deficiency) (Lawton & McNeill, 1979).

Island B i o g e o g r a p h i c Theory The insular nature of cultivated areas has motivated several analogies concemcrops as islands available for colonization by arthropods (Price & Waldbauer, 1975; Strong, 1979; Simberloff, 1986). The development of arthropod communities in crops has been analyzed using MacArthur and Wilson's (1967) theory of island biogeography, which allows the prediction of colonization rates and mortality/ emigration rates, on a comparative basis, with respect to crop area, distance from the sources of colonizers, and crop longevity (assuming that the system has aspects of equilibrium). The species composition, structure, and abundance

340

D.K. Letourneau and M. A. Altieri TABLE 6

Predator family

E x a m p l e s of E n v i r o n m e n t a l M a n i p u l a t i o n Affecting Efficiency a n d A b u n d a n c e of Particular P r e d a t o r Families

Environmental management practice(s)

References

Neuroptera Chrysopidae

Hemerobiidae

Mowing of luceme to force movement to adjacent crops Protein-based food sprays in cotton and alfalfa Interplanting or adjacent plantings of sorghum with cotton and cabbage Placing hollow fibers containing caryophyllene in alfalfa Spraying artificial honeydew Protein and sugar sprays in artichoke

van den Bosch & Telford, 1964 Hagen, 1986 Perrin, 1977 Hagen, 1986 Hagen, 1986 Neuenschwander & Hagen, 1980

Hemiptera Anthocoridae

Lygaeidae

Pentatomidae Nabidae

Planting of legumes (crimson clover, vetch), barley, sorghum, and corn as early sources of Orius insidiosus Presence of weeds facilitates dispersal of anthocorids to aphid-infested Brussels sprouts Intercropping maize for control of thrips on squash Maintaining Lagopsis supina as a dominant weed in apple orchards supports early sources of O. sauteri Com, alfalfa, or thistles growing adjacent to apple orchards Presence of flowering willows adjacent to apple trees Addition of chopped sunflower seeds on sugar beet for enhancement of Geocoris spp. Drilled planted soybeans Uses of cotton varieties with extrafloral nectarines Selection of hirsute varieties preferred by G. punctipes for oviposition Provision of supplemental plant feeding (potato foliage for Podisus maculiventris) (Say) Hamiptera: Pentatomidae No-till practices and repeat cropping of soybeans

Whitcomb, personal communication Smith, 1976b Letourneau & Altieri, 1983; Letourneau, 1990 Yu-hua et al., 1997 McCaffrey & Horsburgh, 1986 Solomon, 1981 Tamaki & Weeks, 1972 Ferguson et al., 1984 de Lima & Leigh, 1984 Naranjo, 1987 Ruberson et al., 1986 Hammond & Stinner, 1987

Coleoptera Carabidae

Coccinellidae

Double cropping barley/wheat and soybeans No-tillage agricultural practice Corn intercropped into a grass-legume mixture Presence of weeds in cereal fields Presence of chrysomelid on several weeds as alternate hosts of Lebia beetles Cover cropping in apple orchards Intercropping with white and red clover Presence of grassy border strips, hedges, wooded areas for survival of spring-breeding beetles Spraying of sucrose solution, artificial honeydew and protein-based food sprays Strip cropping and cutting alfalfa in cotton fields Proximity of forest edges or hedgerows to crop fields Cutting stinging nettle (Urtica dioica) or grass weed cover to force beetle movement to crops Increasing corn planting density Double cropped barley-soybeans

Ferguson & McPherson, 1985 House & Stinner, 1983 Brust et al., 1985 Speight & Lawton, 1976 Hemenway & Whitcomb, 1967 Altieri & Schmidt, 1986 Dempster & Coaker, 1974 Wallin, 1985 Hagen, 1986 Schlinger & Dietrick, 1960 van Emden, 1965 Perrin, 1975; Hodek, 1973 Risch et al., 1982 Ferguson et al., 1984

Diptera Syrphidae

Occurrence of flowering plants (pollen sources) in the vicinity of crops or provision of flowers (wild mustard) within crops Spraying of Wheast | plus sugar or honey

van Emden, 1965, Altieri & Schmidt, 1986 Hagen, 1986

Hymenoptera Formicidae

Vespidae

Use of sugar sources such as extrafloral nectaries and crushed sugarcane, to attract ants Moving colonies to sites of high pest concentration Providing adequate harborage for ground nests of beneficial ants Growing annual crops adjacent to permanent ant habitat Use of shade trees supportive of Oecophylla spp. Use of cover crops in orchards and groves Provision of artificial structures for nesting of Polistes annularis (L.) (Hymenoptera: Vespidae) in cotton and tobacco and of P. fuscatus (F.) in cabbage

Carroll & Risch, 1983 Carroll & Risch, 1983 Buren & Whitcomb, 1977 Leston, 1973 Leston, 1973 van den Bosch & Telford, 1964 Lawson et al., 1961; Gould & Jeanne, 1984 (continues)

Chapter 14

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Environmental Management to Enhance Biological Control in Agroecosystems

TABLE 6 (continued)

Predator family Aranae (spiders)

Acarina (mites)

References

Environmental management practice(s) Maintenance of weed cover in sugarcane Crop fields surrounded by perennial, less disturbed habitats Cropping systems with lower soil disturbance (no tillage, mulching, orchards, etc.) Addition of pollen to enhance Amblyseius hibisci (Chant) in avocados Dusting of cattail pollen (Typha sp.) to enhance tydeid mites in grapes as alternate prey for Metaseiulus occidentalis Weed ground cover supportive of two-spotted mites as alternate prey for M. occidentalis

of arthropods colonizing a crop field, however, are the result of highly dynamic processes; and the assumption of equilibrium is often inappropriate. Nevertheless, some predictions from the theory seem to hold. For example, species richness is positively correlated to size on oceanic islands. Similarly, in mainland communities, the number of herbivores associated with a plant is a positive function of the local area planned for, or covered by, that species (Strong, 1979). Larger host islands probably collect more individuals by random probability of encounter. Further, patch detection by dispersers (apparent) may increase with size. Whatever the cause, the effect of an increase in the number of herbivores with an increase in size is important for consideration in pest management strategies. However, any increase in species diversity must be defined by the proportion in each trophic level, at least, and if possible, by the component species' biologies before it can be analyzed in terms of pest management potentials. MacArthur and Wilson's (1967) model treats all members of a species source pool as equivalent colonizers. Clearly, the application of this theory to dynamic and temporary crop islands requires the consideration not only of the number of species and pattern of occurrence, but also of the order and strength of colonizer establishment by trophic level [Altieri & Letourneau, 1984; Robinson & Dickerson, 1987; Thomas & Janzen, 1989; and see Kadmon & Pulliam (1993)]. Extinction rates depend on resource availability in the system. Because the plants are supplied to the system, or "reset" at certain intervals (Levins & Wilson, 1980), the resource base may be more predictable for herbivores, at least early in the season. The immigration rates of natural enemies to large expanses of monoculture may be similarly increased, though spread from the edges may be slow, and thus favor the development of herbivore populations. The equilibrium theory of biogeography does not allow for comparisons of single, large crop fields versus a network of

Ali & Reagan, 1985 Reichert & Lockley, 1984 Riechert & Lockley, 1984 McMurtry & Scriven, 1966 Flaherty et al., 1971 Flaherty et al., 1971

several small fields of the same total area; yet the contrasting designs are likely to differ in terms of suitability for biological control (Price, 1976). Although the body of theory based on island community development suggests questions and organizes thought on crop design, the impediments to its application lie in four areas: (1) the frequent disturbance of most crop fields reduces the rigor and applicability of equilibrium models; (2) the few current empirical data available on diversity, size, and distance relationships do not constitute a sufficient basis for environmental design recommendations (Simberloff, 1986); (3) the theory does not distinguish pests and beneficials [see Stenseth (1981)]; and (4) the economic impact of "changing island size" will be viewed as exceedingly risky until demands for more certainty in the theory are met (Simberloff, 1986). Liss et al. (1986), however, presented a modification of the MacArthur and Wilson model that incorporates colonizer source composition and changes in "island" habitats over time. They call for further research toward understanding the organization of species pools as sources of arthropod communities in agroecosystems. Kruess and Tscharntke's (1994) study of clover weevils, distance of "islands" from source pools, and parasitism rates demonstrates the kind of studies needed to evaluate the applicability of aspects of island biogeography to agricultural settings. Consumer Dynamics Once the natural enemies are within the habitat of their prey or hosts, studies of consumer dynamics become important in predicting the outcome of their interactions. Traditionally, trophic interaction studies in manipulated as well as in natural systems have concentrated on two trophic levels (i.e., plant-herbivore, predator-prey, host-parasite). Many data (Clark & Dallwitz, 1975; Mattson & Addy, 1975; Podoler & Rogers, 1975; Morrow, 1977; Gilbert,

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1978; McClure, 1980; Kareiva, 1982; Murdoch et al., 1995) and much theory (Murdoch & Oaten, 1975; Hassell, 1978; May & Anderson, 1978; Clark & Holling, 1979; Murdoch, 1979) on consumer dynamics in two-level systems demonstrate the regulation of populations at the lower trophic level (plant, prey, or host) by natural enemies. Conversely, natural enemies have been ineffective in other cases, at least in the prevailing prey densities (Southwood & Comins, 1976; Strong et al., 1984; Walker et al., 1984). The effectiveness of natural enemies as regulators of herbivore populations depends not only on behavioral and developmental responses of individual enemies and on responses of the entire population to changes in prey or host densities (Murdoch, 1971; Murdoch & Oaten, 1975; Fox & Murdoch, 1978), but also on variation in plant parameters (density, secondary compounds, and associated plant species). The ability of natural enemies to regulate the herbivores depends on the herbivore population's intrinsic growth rate (era) (e.g., Getz, 1996) and size distribution (e.g., Murdoch et al., 1997), which in turn reflects the quality of the plant diet. Even small changes in R m caused by slight differences in plant quality (variety, secondary chemistry, and nutrients) may determine whether parasites or predators can control the herbivore populations (Lawton & McNeill, 1979; Price et al., 1980). The effectiveness of regulation also reflects subtle differences in the timing and distribution of population events in both predator and prey populations (Hassell, 1978; May & Anderson, 1978). Theory and data on interactions involving three trophic levels in a complex habitat are ultimately more suitable as a basis for applying consumer-resource theory to environmental management strategies (Duffey & Bloem, 1986; Price, 1986; Letourneau, 1988; Sabelis et al., 1991). Thus, the goal of such prophylactic measures of pest control is to avoid the provision of enemy-free space in agricultural environments, and instead to present pests simultaneously with deleterious effects (mortality) caused by their natural enemies and with selectively defensive or suboptimal properties of their food plants. Therefore, studying systems as communities of at least three trophic levels will contribute an understanding of complex interactions that is different from that likely to be gained purely as a by-product of results from two-level studies (Orr & Boethel, 1986). Effects of V e g e t a t i o n a l Diversity Root (1973) proposed two hypotheses to explain the tendency for low herbivore abundance in diverse vegetation. The "resource concentration" hypothesis predicts that many herbivores, especially those with a narrow host range, are more likely to find, survive, and reproduce on hosts that are in pure or nearly pure stands. "The enemies" hypothesis incorporates the third trophic level. Root (1973) predicted that complex vegetation would provide more resources for

natural enemies (alternate hosts, refugia, and nectar and pollen); as a result, herbivore irruption would be rapidly checked by a higher diversity and an abundance of enemies. Sheehan (1986) extends the resource concentration concept to predict that specialist enemies will respond to mixed vegetation differently, and probably less favorably, than will generalist predators and parasitoids, because of the importance of alternate prey for generalists. The designation of host-prey specialization categories, however, tends to rely on only one aspect of the resource spectrum of parasitoids and predators (Letourneau, 1987). A range of species (or even individual) characteristics, such as relative vagility, resource needs, and habitat location cues may determine the response of parasitoids and predators to vegetational diversity. Theoretical concepts of connectivity (sensu Pimm, 1982) and guilds (Hawkins & MacMahon, 1989) may be important in guiding the design of habitats that optimize natural-enemy conservation. For example, the inclusion of insectary plants in a monoculture adds a functional guild of nectar and pollen producers, which then increases the actual number of trophic linkages in the system. Russell (1989) and Corbett and Plant (1993) suggest that some of our experimental results underestimate the impact of mixed vegetation on enemy enhancement, simply because of mismatched experiment scales with respect to relevant enemy movement patterns [but see Ramert & Ekbom (1996)]. The maintenance of heterogeneity within an agroecosystem may also affect the success of establishment of imported biological control agents. The debate over the degree to which ultimate levels of regulation are attained by singleversus multi-species releases in classical biological control projects continues (Turnbull, 1967; van den Bosch, 1968; Ehler & Hall, 1982; Van Driesche & Bellows, 1996), but analyses of environmental factors as raw materials or as constraints are rarely considered (Beime, 1985). Certainly factors such as species richness, climatic gradients, and disturbance levels are important in assessing the susceptibility of largescale communities to biological invasion (Fox & Fox, 1986). O p t i m a l Foraging Implicit in environmental management for biological control are considerations of optimal foraging theory. During the host-prey selection process, natural enemies exhibit a chain of responses to stimuli. Several are exemplified in Table 5 as mechanisms with potential for manipulation. The objectives of biological control are to exploit natural processes that allow maximum prey encounter and foraging rates by natural enemies while, in most cases, achieving their persistence in the agroecosystem. Thus, this body of theory is useful for predicting enhancement mechanisms and for evaluating the consequences of under- and overexploitation. The aggregation of foraging parasitoids in patches of

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higher host density has been a critical feature thought to be responsible for successful biological control (Beddington et al., 1978; May & Hassell, 1981; Murdoch & Briggs, 1996). Models of optimal patch use predict predation-parasitism levels between patches, based on host-prey densities (Cook & Hubbard, 1977; Waage, 1979; Iwasa et al., 1984), but the power of these models varies and results depend on the particular spatial scale examined (Hopper et al., 1991; Ives et al., 1993). Murdoch et al. (1985) examined the importance of this searching behavior using the successful olive scale Aphytis paramaculicornis DeBach & Rosen and Coccophagoides utilis. Doutt system, and found little evidence that these parasitoids aggregate in areas of high pest density. Waage (1983) found that Diadegma spp. attacking Plutella xylostella (Linnaeus) aggregated in patches with greater host density; yet the proportion of hosts parasitized at high host densities was not greater. Roland (1986) found similar results with Cyzenis albicans: egg distribution does not affect the level of parasitism. Krivan (1996) showed how prey switching within the context of optimal foraging can lead to the persistence of predators and prey. However, field results can be complicated by community level effects (e.g., Moran & Hurd, 1997). Predictive models then can be used to clarify the mechanisms involved in enemy behavior and their importance. It may be possible to take advantage of the "simple rules" that foragers use for decisions on how long to remain in a patch, which hosts or prey to seek and to accept, when and where they will oviposit, and (especially for hymenopterous parasitoids) what the sex ratio will be. If these "decisions" are made in response to environmental cues, then they are potentially manipulable in the field (Kareiva & Odell, 1987). Dicke et al. (1985) found that searching eucoilid parasitoids remained longer in a patch with moderately higher kairomone concentrations regardless of the actual density of Drosophila melanogaster Meigen, its host. The opposite effect could occur if prey or prey cues are difficult to find in a particular cropping system [see Spencer et al., (1996)]. Theoretically, if resource patch boundaries are vague (Schmidt & Brown, 1996), actual biological control could be reduced even if prey are aggregated. Charnov and Skinner (1985) call for careful reflection of both the proximate causes of such responses and the evolutionary causes as complementary approaches that enhance theory and application. It is also relevant to consider the ultimate population effects on natural enemies given habitat manipulations that exploit behavioral cues and maximize prey reduction. Fewer studies direct such attention to predator fitness. One example shows that although juvenile mantids exhibit a strong type II functional response, such behavior quickly increases beyond the maximum gain in characteristics related to fitness (Hurd & Rathet, 1986). We are not aware of studies addressing ultimate effects of enemy recruitment through enhanced habitat location cues at times of low prey

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abundance [but Murdoch et al. (1985) do examine local extinction of prey; and theoretical considerations of local extinctions, spatial patchiness, and regional stability of host-parasitoid interactions (Hassell et al., 1991) may help predict these effects]. Thus, the definition of "optimum" may initially depend on maximum influx and efficiency of natural enemies on a local scale, but the ultimate benefits to farmers may depend on large-scale and long-term effects on populations of predators and parasitoids. Thus, enemy response to environmental manipulation will benefit through life table studies over many generations (Hassell, 1986), optimal foraging models that include long-term population changes, and metapopulation models that consider spatial dynamics relative to interpatch heterogeneity (Taylor, 1991; Murdoch et al., 1992; Letourneau, 1998).

CONCLUSIONS Several manipulable components of agroecosystems provide the raw material for planned habitat management. Research on vegetation management, consumer dynamics, use of semiochemicals, and multitrophic level models of agricultural systems represent some of many advances providing direction. Renewed interest in sustainable agriculture as a response to growing concerns about ground water contamination, soil erosion, occupational health and consumer health, and safety set the stage for long-term planning for pest management. Implementation of habitat management for biological control is a viable option not only as an important component of IPM programs but also as an assurance of constancy of production under low-input and resource-conserving agricultural management. Data and practical experience reported in this chapter provide ample evidence that it is possible to stabilize insect communities in agroecosystems by designing and constructing vegetational architectures that support populations of natural enemies or that have direct deterrent effects on pest herbivores. What is difficult is that each agricultural situation must be assessed separately, because herbivoreenemy interactions will vary significantly depending on insect species, location and size of the field, plant composition, surrounding vegetation, and cultural management. One can only hope to elucidate the ecological principles governing arthropod dynamics in complex systems, but the biodiversity designs necessary to achieve herbivore regulation will depend on the agroecological conditions and socioeconomic restrictions of each area.

Acknowledgment Discussions with P. Barbosa, L. R. Fox, and K. Kester improved the quality of this chapter. We appreciate the comments of T. W. Fisher, G. Gordh, and T. S. Bellows, who carefully reviewed earlier versions of the manuscript. Many thanks to M. Hemler, R. Krach, E. Letourneau, and L.

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Schmidt for excellent technical assistance. D. K. Letourneau was supported by USDA Competitive Grant No. 85-CRCR-11590 (to D. K. L. and L. R. Fox) and by UC/Santa Cruz Social Sciences Divisional Research Grants.

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Chapter 14

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1151 Biology of Parasitic Hymenoptera G. GORDH

E. F. LEGNER

L. E. CALTAGIRONE

USDA, Agricultural Research Service Kika de la Garza Subtropical Agricultural Research Center 2301 S. International Blvd. Weslaco, Texas 78596

Department of Entomology University of California Riverside, California

Division of Biological Control University of California Berkeley, California

For insects developing in this manner the larva is always the parasitic form. These insects have been called protelean parasites (Caullery, 1950; Sellier, 1959; Askew, 1971) to distinguish them from other groups of organisms that develop parasitically. The term "parasitoid" was proposed earlier (Reuter, 1913), and in the past 15 years this term has gained widespread acceptance among ecologically and ethologically oriented workers. Several criteria are used to distinguish parasitoids from other parasitic animals. These include (1) the parasitic behavior is expressed only during the larval stage; (2) the adult stage is free living [exceptions to (1) and (2): adult female of some Strepsiptera]; (3) the parasitoid larva typically kills and consumes one host; (4) the body size of the parasitoid approximates that of the host; (5) the parasitoid life cycle is relatively simple; (6) the parasitoid shares relatively close taxonomic affinity with hosts (insects on insects); (7) parasitoids display a reproductive capacity between true parasites and free living forms (Doutt, 1959). Exceptions to each criterion are found among parasitic Hymenoptera. While these criteria provide a useful framework for instruction, they may inaccurately portray the fundamental nature of insect parasitism. Our perception of insect parasitism must be altered as the biology and the development of parasitic insects become better documented. Indeed, parasitic insects display a prodigious array of progenitive strategies (Clausen, 1940; Askew, 1971; Price, 1977). They develop internally (endoparasitoids), externally (ectoparasitoids), or initially in one area and finally in the other (Shaw, 1983). Solitary parasitism is a condition in which a parasi-

INTRODUCTION Ecological and evolutionary aspects of parasitoid biology have become focal points of entomological research during the past 20 years to an extent unparalleled in the development of entomology. Here we review the principal features of parasitic Hymenoptera anatomy, development, biology, and reproduction as these features relate to biological control. Available space does not permit treatment of all parasitic insects. Parasitoids are the group of natural enemies of greatest importance in biological control of pests. Of 1193 species of parasitoids and predators included in the world review of biological control programs by Clansen (1978), 907 (76.03%) were parasitoids; of these, 765 (84.34%) were Hymenoptera, 125 (13.79%) were Diptera, and 17 (1.43%) belonged to other groups. Our discussion will emphasize the parasitic Hymenoptera because of their numerical dominance and their importance in biological control. Definitions Parasites are organisms that live in or on, and at the expense of, other organisms (hosts), each individual parasite completing all or a major part of its life cycle in or on one individual of the host. This is a form of a somewhat prolonged symbiosis involving at least two unrelated species. One symbiont (the parasite) lives at the expense of the other symbiont (the host). The parasite provides no benefit to the host, which is weakened or otherwise damaged, and is eventually destroyed, or rendered unable to reproduce.

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toid larva completes development in a one-to-one relationship with its host; supernumerary eggs or larvae are eliminated. In contrast, gregarious parasitism involves the development of more than one individual in one host. Some species of parasitoids are obligatorily solitary or gregarious, while others are facultatively so. Beyond this basic architecture for parasitism we see numerous variations on themes that are influenced by habitat, adult female anatomy, oviposition behavior, host taxa, host biology, and numerous other factors (Price, 1980). This necessitates special terms for these kinds of interactions. For instance, the term idiobiont was proposed for parasitoids that kill immediately or shortly after initial parasitization, permanently impairing or preventing further development of the hosts (Askew & Shaw, 1986). Typically idiobionts are ectoparasitic, attack concealed hosts, and express a broad host spectrum (generalists). In contrast, the term "koinobiont" was proposed for parasitoids that do not kill rapidly, permanently impairing or preventing further host development. Typically koinobionts are endoparasitic, attack exposed hosts, and reveal a limited host range (specialists). Some koinobionts may induce their hosts to consume more of their food (Hunter & Stoner, 1975) while others cause the reverse response (Doutt, 1963). Exceptions to this classification are easy to find. When females of more than one species oviposit in a host individual, the condition is termed multiple parasitism. Facultative multiple parasitism is the association of more than one species of parasite on a host simultaneously. Obligatory multiple parasitism is a very rarely encountered phenomenon, and one whose functional significance is not clearly established (Salt, 1968). The condition in which a parasitoid prefers to distribute her progeny in hosts already parasitized by a different species is called cleptoparasitism. Examples are discussed by Arthur et al. (1964), Piel and Covillard (1933), Spradberry (1969), and Syme (1969). Cleptoparasitism is considered as an evolved advantageous multiparasitic strategy by Gauld and Bolton (1988). Superparasitism is common in parasitic Hymenoptera, and has been defined in several ways: (1) one female allocating more eggs to a host than can successfully develop to maturity; (2) several conspecific females allocating more eggs to a host than can successfully develop to maturity; and (3) several females, not necessarily conspecific, allocating more eggs to a host than can successfully develop to maturity. The latter definition includes the original concept of superparasitism as defined by Howard and Fiske (1911). Each definition views the phenomenon in a different way, with disparate effects on the fitness of ovipositing females. As generally accepted, superparasitism is the condition in which an individual host receives more parasitoids of the same species than can develop to maturity, regardless of whether the parasitoids (eggs or larvae) were distributed by a single female or by several females. Various aspects of

superparasitism involving single females and several females of the same species have been studied by van Dijken and Waage (1987). Superparasitism and the great majority of cases of multiple parasitism are temporary conditions; eventually the supernumerary individuals are eliminated. The incidence of each condition is dependent on the number of parasitoid progenies to be distributed and the number of susceptible hosts available. Hyperparasitism is a multilevel trophic system in which one species develops as a parasitoid of another parasitoid. The species attacking the free-living organisms (herbivore or predator) is called a primary parasitoid; the primary parasitoid is attacked by a secondary or hyperparasitoid. Hyperparasitism is rare in the Coleoptera and Diptera, but reaches elaborate development in the Parasitica (Gordh, 1981; Sullivan, 1987). Hyperparasitic development takes many forms including facultative hyperparasitism, obligatory hyperparasitism, adelphoparasitism, and tertiary hyperparasitism. Facultative hyperparasites can complete feeding and development as a primary parasite or use a primary parasite as a host. Obligatory hyperparasites must complete feeding and development using a primary parasite as host.

I m p o r t a n t A n a t o m i c a l Features of Parasitic Hymenoptera Parasitic insects are common in the Holometabola; they are found in the Hymenoptera, Diptera, Strepsiptera, Coleoptera, and Lepidoptera. Hymenoptera are the most important group of insects from the viewpoint of applied biological control. The Hymenoptera include about 125,000 nominal species, but many parasitic species await description and the order will be shown substantially larger. Traditional classifications include the suborders Symphyta (= Chalastogastra: sawflies, wood wasps) and Apocrita (= Clistogastra: bees, wasps, ants). Few species of Symphyta are parasitic, and Symphyta assume a minor position in parasitism because nearly all species are phytophagous. The Apocrita are sometimes subdivided into two infraorders: the Parasitica and the Aculeata. Alternative classifications reflect several infraorders (Rasnitsyn, 1988). Certain anatomical features have undoubtedly contributed to the evolutionary success of the apocritan Hymenoptera. Important features include an appendicular ovipositor, a constricted waist (petiole), and accessory gland secretions. The great majority of these parasitoids exhibit the ability to provide for their progeny. Together, these features have made parasitism a highly successful lifestyle and consequently have focused attention on apocritan Hymenoptera as an important group in applied biological control. The pertinence of each factor is explained next.

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Appendicular Ovipositor The Symphyta and the Parasitica are among the few Holometabola with a lepismatid-like ovipositor (E. Smith, 1970). The significance of this tubular, elongated, egg-laying structure as an adaptation for parasitism cannot be overemphasized. This type of ovipositor permits precise placement of the egg in habitats that other insects cannot reach without elaborate anatomical modifications involving other regions of the body (Rasnitsyn, 1968).

Accessory Gland Secretions These secretions are associated with the reproductive system of most Insecta. They serve to lubricate the egg, provide a substrate for fungal growth, induce gall formation, and constitute venoms for the subduction of prey and host. Use of glandular secretions against potential hosts is a cardinal landmark in the evolution of parasitism by Hymenoptera.

Constricted Waist (Petiolate Abdomen) The Aculeata and the Parasitica display a constriction between the thorax and the abdomen. The constriction forms a small, ringlike second abdominal segment, termed the petiole. This constriction promotes abdominal flexibility, which enables the adult to sting hosts and prey into paralysis and also permits egg deposition in confined spaces.

Progeny Provisioning Ancestral Hymenoptera presumably displayed a phytophagous larval stage (Iwata, 1976). This is seen today in Symphyta females that place their eggs in plant tissue. The behavioral transition from placing an egg in plant tissue to the present condition in which an apocritan female places an egg in or on a host must have occurred early in the evolution of parasitic habits.

PARASITIC HYMENOPTERA IMPORTANT IN BIOLOGICAL CONTROL The large number of taxa involved, and the comparatively small number of those that have been used in biological control suggest the enormous possibilities that this group offers for pest control. Here we highlight briefly significant features of biology for the most noteworthy families.

The Parasitica The Parasitica form the largest division of the Hymenoptera, and the group that is most important to biological control. Biologically, the Parasitica primarily are composed of species that are parasitic, but some groups include gall formers and other phytophages.

Ichneumonoidea This superfamily is among the oldest groups of Parasitica and has a fossil record extending into the Cretaceous (Rasnitsyn, 1980). Ichneumonidae are the largest family in this superfamily, and the host spectrum is broad with focus on Holometabola. All ichneumonids are parasitic but they do not attack Mecoptera, Siphonaptera, or Strepsiptera. Larvae, pupae, and immatures in cocoons are preferred. Adults are often associated with moist habitats and extensive ground cover. Braconidae are related to Ichneumonidae. All species are primary parasites, but host associations have not been established for most species (Matthews, 1974). Current information suggests that braconids display an exceptionally broad host range, mostly Holometabola, but do not attack Trichoptera, Mecoptera, or Siphonaptera. One subfamily, the Aphidiinae, generally regarded as important in biological control, includes about 300 species, all of which are primary internal parasites of aphids. They are sometimes regarded as a distinct family near the Euphorinae (van Achterberg, 1984).

Ceraphronoidea This superfamily includes two extant families, Ceraphronidae and Megaspilidae, which early classifications placed in the Proctotrupoidea (Masner& Dessart, 1967; Dessart, 1986). Ceraphronidae are very poorly studied, but species apparently develop as endoparasites of larval Diptera, such as Cecidomyiidae. Pupation occurs inside the mature larval integument. Some species attack Thysanoptera, Lepidoptera, and Neuroptera (Chrysopidae, Coniopterygidae). Megaspilidae develop as ectoparasites of diverse taxa. They are hyperparasites of aphidiids on Aphididae, or primary parasites of Coccidae, Mecoptera, Neuroptera, and Diptera. Some myrmecophiles probably attack Diptera.

Evanioidea This group is of questionable development and composition (Townes, 1950; Crosskey, 1951) and members have been placed among the Ichneumonoidea and Proctotrupoidea in some classifications. Three included families are Evaniidae, Aulacidae, and Gasteruptiidae. Evaniidae are widespread, are predominantly tropical, and under domestic

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conditions are typically encountered around drains and on windows. All species apparently are endoparasites of cockroach oothecae (Townes, 1949; Brown, 1973). Aulacidae are cosmopolitan, solitary egg-larval endoparasites of wood-boring Coleoptera and Hymenoptera (Hedicke, 1939; Oehlke, 1983; Benoit, 1984). Gasteruptiidae are widespread. Adults visit flowers and rotting logs in search of hosts that include bees and wasps. They show transitional behavior between cleptoparasitism and ectoparasitism.

Trigonaloidea This superfamily represents a lineage whose members have been placed in many superfamilies (Townes, 1956). The Trigonaloidea includes one extant family, the cosmopolitan Trigonalidae, and one fossil family, the Ichneumonomimidae. Biological studies are limited (Raff, 1934; Cooper, 1954). Species are hyperparasites of larval Hymenoptera and Tachinidae; some develop as primary endoparasites on Symphyta in Australia. Adult females oviposit on vegetation. Frequently several thousand eggs are discharged during one ovipositional episode; the eggs are consumed by larval Symphyta or Lepidoptera and hatch, and the parasitoid larva penetrates the host's hemocoel.

Chalcidoidea This superfamily is among the numerically largest, biologically most diverse and geologically oldest of the Parasitica (Yoshimoto, 1975; Gordh, 1979; Gibson, 1986). Chalcidoids feed as primary and secondary parasitoids, inquilines, gall inducers, and seed eaters. Development may be internal, external, solitary, or gregarious. Chalcidoids attack all stages of their hosts, including the adult (LaSalle, 1990), and may serve as hosts to chalcidoids, and the host spectrum extends from spiders and ticks to aculeate Hymenoptera. They are among the most important groups for applied biological control (DeBach & Schlinger, 1964). Here we briefly treat families most conspicuous in biological control attempts. Aphelinidae are primary or hyperparasitoids that develop externally or internally. The biology of many species is unusual and males of some species are hyperparasitic (heteronomous) (Broodryck & Doutt, 1966; Kennett et al., 1966; Walter, 1983; Viggiani, 1984). The higher classification of aphelinids is relatively well studied (Yashnosh, 1976, 1983; Hayat, 1983). Most species attack sternorrhynchous Homoptera and several species are important in biological control of scale insects (Rosen & DeBach, 1979) and whiteflies (Greathead, 1986). Chalcididae are primary and hyperparasitoids of Lepidoptera and to lesser extent Diptera, Coleoptera, and other Hymenoptera (Burks, 1940; Boucek, 1952, 1974). As hyperparasitoids they attack Tachinidae developing as primary

parasitoids of Hymenoptera and Lepidoptera. Development typically is solitary as endoparasitoids of the last instar larva and pupa. Some species have been used in biological control. Encyrtidae are all endoparasitoids, and predominantly primary parasitoids; some species are hyperparasitic (Gordh, 1979, 1981). The host spectrum of Encyrtidae is broad, but most species are associated with Homoptera (Tachikawa, 1981). Encyrtids are important in biological control of mealybugs and scale insects. Polyembryony is known in many species (see later). Eulophidae (including Elasminae) are predominantly primary parasitoids; some species are hyperparasitoids and a few are phytophagous (Boucek & Askew, 1968). Development is solitary or gregarious, internal or external. The host spectrum of eulophids is extensive, and includes all immature stages, often attacking concealed Lepidoptera and Diptera. They are important in some biological control programs involving sawflies on pine, and leaf miners. Eurytomidae are typically solitary, rarely gregarious, ectoparasitoids; some species are endoparasitic of cecidogenic insects. The first instar is hymenopteriform, often with five pairs of spiracles. The host spectrum and feeding strategies of eurytomids are diverse: many species are carnivorous, developing as parasitoids of gall makers or other phytophages in seeds and stems, or as parasitoids of eggs (tree crickets); others are phytophagous, developing in seeds, or in galls induced by other insects. Mymaridae developed early in the history of the Apocrita (Yoshimoto, 1975). All species develop as internal parasitoids of insect eggs (Burks, 1979a; Huber, 1986). Typically larvae are solitary and prefer Auchenorrhyncha whose eggs are concealed within plant tissues, under bark, and in soil. Pupation occurs inside the host egg. Some species have been successful in biological control programs (Clausen, 1978). Pteromalidae are a large, biologically diverse, taxonomically difficult group of chalcidoids (Graham, 1969). Egg shape, size, and number are highly variable. Up to 700 eggs per female have been reported. The first instar larva is hymenopteriform, having 13 segments with head and mandibles sometimes large. Ectoparasitic larvae exhibit an open respiratory system, while that of endoparasitic forms is closed. They are solitary or gregarious, but typically they are ectoparasitoids. Their feeding spectrum is very diverse: their hosts are typically Holometabola larvae and pupae in stems, leaf mines, galls, and similar habitats; some species are larval-pupal parasitoids; some are predaceous on cecidomyiid larvae or coccoid and delphacid eggs; some are gall inducers and gall feeders. Torymidae develop either as gall inducers, phytophages of seed endosperm, primary ectoparasitoids of gall inducers, ectoparasitoids of aculeate Hymenoptera, or hyperparasitoids (Grissell, 1979; Narendran, 1984). The torymid egg

Chapter 15 Biology of Parasitic Hymenoptera

is of variable shape, typically sausagelike. The larva is hymenopteriform; those of parasitic species often have spines, while those of phytophagous species are spineless. Trichogrammatidae are primary, solitary, or gregarious internal parasitoids of insect eggs. Some taxa are among the smallest insects (Megaphragma ca. 0.20 mm long) (Doutt & Viggiani, 1968; Burks, 1979b). The larvae undergo hypermetamorphic development: the first instar larva is sacciform or mymariform; the last instar is segmented, robust, and spineless. The family displays a broad host spectrum that includes principal orders of Holometabola, Hemiptera, and Thysanoptera. Trichogrammatidae are used extensively in biological control programs. More information on applied ecology has been published on Trichogramma than on any other comparable group of Parasitica.

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escent. When the host is ready to pupate, the larval parasitoid develops rapidly. Proctotrupoids pupate externally in rows on the host's venter, with the apex of the gaster remaining attached to the host. A cocoon is not formed (Townes & Townes, 1981). Scelionidae are solitary, internal egg parasitoids of Hemiptera, Lepidoptera, Mantodea, and Aranaea. The family is the largest and taxonomically among the best studied proctotrupoids (Masner, 1976, 1980; Galloway & Austin, 1984). Many species appear host-family specific and seem to prefer eggs in aggregations. Egg marking with semiochemicals has been noted in several species. Phoresy is widespread and probably common (Orr et al., 1986). The first instar larva is teleaform. Several species show strongly female-biased sex ratios. Males of most species are protandrous and combative, and sibling mating appears common.

Proctotrupoidea The Proctotrupoidea have a fossil record in the Jurassic, which suggests that they are older than the Chalcidoidea. They are more abundant than chalcidoids in the oldest amber deposits (Cretaceous). Taxonomically, the extant fauna of Proctotrupoidea is substantially smaller than the Chalcidoidea. Family-level classification has been reviewed and tentative phylogenies have been proposed (Kozlov, 1970). All species are primary parasitoids and resemble Chalcidoidea; both groups have small body size and reduced wing venation. Proctotrupoids have not been used extensively in biological control, but some groups are important in controlling pests. Some species exert a negative influence when attacking predators (e.g., Heloridae, Townes, 1977). Diapriidae are internal parasitoids of Diptera pupae within puparia and frequently are encountered in damp habitats (Nauman, 1987). Some species are myrmecophilous, probably attacking inquilines. Gregarious development has been reported, but the biology of most species has not been studied in detail. Females oviposit into either host pupa or host larva. Platygasteridae are usually univoltine, gregarious, internal parasitoids. Hosts include gall-forming Cecidomyiidae, mealybugs, and whiteflies. Females oviposit in eggs or early instar host larvae. Oviposition is site specific (e.g., the eggs may be laid either in the nerve cord, in the gut, or in the brain). Development is completed within the mature larva. Some species exhibit hymenopteriform larvae; many species are hypermetamorphic. Polyembryony occurs in the family (Marchal, 1906; Ivanova-Kasas, 1972). Some reports suggest species of platygasterids are useful in biological control (Clausen, 1978; Jeon et al., 1985; Lee et al., 1985). Proctotrupidae (Serphidae) develop as solitary or gregarious internal parasitoids of Coleoptera or Diptera. Adults are taken in damp, concealed habitats under bark, leaf litter, and fungal gardens. The polypodeiform first instar is qui-

Cynipoidea The group is large and poorly studied compared with other Parasitica (Konigsman, 1978). Current estimates indicate about 30% of the species are phytophagous (Nordlander, 1984). Cynipoids branched early from generalized parasitic Hymenoptera and Nordlander believes Cynipoidea are primitively parasitic. Fossil Cynipoidea have been taken in Taimyrian and Canadian amber, which makes them as old as chalcidoids (Rasnitsyn & Kovaley, 1988). Eucoilidae are endoparasitic in schizophorous Diptera larvae. The family was subordinated within the Cynipidae in early classifications. Females oviposit in young host larvae and development proceeds through three to five instars. Pupation occurs within a host puparium. Hypermetamorphosis is probably universal with the first instar eucoiliform, with thoracic lobes and caudal projection for emergence from the egg. The respiratory system gradually develops, with the first instar lacking spiracles, while the fifth instar exhibits eight pairs. Figitidae (including Anacharitinae) are solitary, primary internal parasitoids of Neuroptera and Diptera. Little is known of their biology (Miller & Lambdin, 1985). The egg is laid in the neuropteran hemocoel and hatches, and the larva feeds internally until the host spins its cocoon. Next the figitid migrates outside and feeds externally. Figitids overwinter as diapausing larvae within the host's body. Among dipteran hosts, Syrphidae and saprophagous cyclorrhaphans seem preferred. Ibaliidae are solitary egg-larval parasitoids. The most detailed account of development and biology is provided by Chrystal (1930). Females locate eggs or hosts boring in wood and oviposit into the egg or early larva of Siricidae. First instar larva is polypodeiform; later larval stages are hymenopteriform. Early larval development is internal while later development is external. The fourth instar larva has large mandibles but does not feed. Pupation occurs in

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the host's tunnel. One species is used in Tasmania and in New Zealand to control siricids in pines (Kerrich, 1973). Aculeata Despite their large numbers, widespread geographic distribution, and diverse biologies, the parasitic aculeate Hymenoptera are not a highly important group in applied biological control. Parasitism in this group is found in the more primitive taxa. Their hosts are insects of limited economic significance. Higher forms behave as predators. Complex parasitic relationships are found among social bees and ants, but these are beyond this discussion.

the site of encounter, but a few species transport the host to a protected place, or construct a cell for it before ovipositing. The egg is hymenopteriform and is "glued" to the host. Development of the larvae is gregarious. Bethylids are not host specific, but species in certain genera are associated predominantly with certain host families. Females adjust the number of eggs laid on a host based on the host size; if mated, they also control the sex ratio (female bias).

PRINCIPAL ASPECTS OF PARASITOID BIOLOGY Developmental Stages

The Egg Chrysidoidea Chrysidoids are generalized Aculeata and sometimes they are regarded as the most primitive superfamily, apparently near the Pompilioidea. Fossil dryinids are found in Taimyrian and Canadian amber. All chrysidoids are parasitic, and nearly all are primary parasitoids. Their host associations are cohesive at the family level, each of many genera attacking a family or a group of related families. Dryinidae are another group with a fossil record dating from the Cretaceous (Ponomarenko, 1981). Species attack auchenorrhynchous Homoptera (Cicadelloidea, Fulgoroidea). A number of female dryinids exhibit chelate forelegs with which they capture their host. Before oviposition they temporarily paralyze the nymphal host (Olmi, 1984a, 1984b). Female dryinids sometimes host feed. The first instar larva is sacciform, but later stages are hymenopteriform. A thalacium is formed from cast larval exuviae (as in the Rhopalosomatidae). Dryinidae apparently lack Malpighian tubules. Polyembryony and thelytoky have been reported in a few species (Ivanova-Kasas, 1972; Ponomarenko, 1975). Chrysididae are parasitoids of Hymenoptera and phasmid eggs. Host associations reflect the higher classification of the Chrysididae: primitive subfamilies attack sawflies and phasmid eggs, while derived ones attack aculeate Hymenoptera (Bohart & Kimsey, 1982). Cleptoparasitism is expressed in forms that feed on the host and food in its cell. First instar chrysidid larvae are planidiform and typically attack the prepupal stage of the host. Complex female behavior of derived lineages is noted in host attack: she gnaws into the host cocoon to oviposit or gnaws into mud cells and then into the host cocoon inside. Females sometimes seal holes with saliva. Thanatotic behavior is reported in many species. Bethylidae are primary external parasitoids of Coleoptera and Lepidoptera larvae (Evans, 1964, 1978). Females search for hosts, often in concealed habitats, and sting them into paralysis. Host paralysis is temporary or permanent, depending on the species. Typically oviposition occurs at

Parasitic insect eggs are variable in size and shape. This variability is a consequence of the enormous number of taxa involved and the developmental requirements of the insect embryos contained in these eggs. The variability in size and shape partially reflects a compromise between needs of the developing embryo and problems associated with oviposition. The nomenclature and early literature associated with parasitoid eggs were characterized by Clausen (1940), were reviewed by Hagen (1964), and are summarized here. Research on egg anatomy during the past 20 years has shown that shape alone is not diagnostic and that unrelated taxa share identical shapes (Hinton, 1969). With the application of electron microscopy we now see that chorion morphology, eggshell complexity, micropylar position, number, and configuration are important features that must be described, studied, and understood. The number of taxa for which information must be collected is very large. The eggs of Hymenoptera are briefly reviewed here. The hymenopteriform egg is the hypothetical ancestral form or the generalized type found in Hymenoptera. Typically the egg is sausagelike with rounded poles and a body several times longer than wide. The acuminate egg is typically long and narrow, and generally is adapted for extrusion from the long ovipositor of parasitic Hymenoptera that attack insects that induce galls or live in galleries and tunnels. This egg is found in some Ichneumonoidea and Chalcidoidea. The stalked egg is elongate with a constricted stalklike projection from one or both poles. Stalk length is variable, sometimes corkscrew shaped, and often several times longer than the remainder of the egg. Stalked eggs are found in most superfamilies of parasitic Hymenoptera: Chalcidoidea (most families), Chrysidoidea, Cynipoidea, Evaniioidea, Ichneumonoidea, and Proctotrupoidea (most families). The pedicellate egg is an apparent variation of the stalked egg in which one end is modified to anchor the egg to its host. Most pedicellate eggs are deposited externally on the host, but some are internal and attached to the host via the ventral surface of the egg. The pedicel may originate from the stalk, from the body of the egg, or from

Chapter 15 Biology of Parasitic Hymenoptera

a modified micropylar structure. This form is distributed among Parasitica, including Chalcidoidea and Ichneumonoidea. The encyrtiform egg is unusual in that it changes shape after oviposition. Within the ovary it is shaped as two spheres connected by a stalk. After oviposition one sphere collapses, all of the cytoplasm being accumulated in the main body of the egg, which then appears stalked. Encyrtiform eggs are always deposited inside the body of the host, with the collapsed sphere projecting from the stalk outside the host's body. An aeroscopic plate, used for embryonic and larval respiration, usually is found on the stalk and sometimes projects onto the body of the egg. This type of egg is characteristic of Encyrtidae (Maple, 1947) and Tanaostigmatidae (LaSalle & LeBeck, 1983).

The Embryo Embryology concerns the development of the individual organism, typically within the egg (Counce, 1961). A mature egg is distinguished by the animal pole, close to which the nucleus is found, and by the vegetal pole that is opposite the animal pole. The yolk is accumulated in the vegetal pole (Balinsky, 1970). The animal pole is more active in physiological exchange during oogenesis. The internal portion is fluidlike and differs from the surface. Mature eggs undergo "aging" among some species, resorption in others, and a combination of both in others. Aged eggs of Hymenoptera may be deposited or resorbed. Embryos develop into male or female progenies, depending on the kind of parthenogenesis. In some cases eggs may hatch within the mother, which kills her. The state of meiosis at oviposition varies (Baerends & van Roon, 1950; Bronskill, 1959). Cleavage is the subdivision of the one-celled egg into smaller units, called blastomeres, by mitotic divisions. Each division results in a reduction in size of the ensuing blastomeres. The total mass of living substance available at the start is not increased appreciably when cleavage is complete. The ova of most arthropods are centrolecithal (i.e., the yolk is massed centrally and surrounded by a peripheral shell of cytoplasm). Cleavage occurs only in the peripheral region and is termed superficial. Some endoparasitic Hymenoptera have little yolk (isolecithal) and show total cleavage (Bronskill, 1959, 1960). Yolk components are called deutoplasm and include protein yolk bodies, lipid yolk bodies, and glycogen particles. Some chalcidoids apparently lack yolk. Cleavage usually begins soon after the egg is laid, but exceptions occur and some eggs hatch inside the mother. The duration of cleavage varies, but generally it is finished after 6 to 8 h at 23~ Gastrulation is the process through which three germ layers are formed: the ectoderm, mesoderm, and entoderm. Germ layers produce body organs and appendages. Gastrulation occurs in diverse ways among Hymenoptera, and

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may differ among species of one family. The duration apparently ranges from 1 to 12 h. Segmentation occurs early in development of some Hymenoptera, and later in others. Two embryonic membranes, the serosa and the amnion, usually envelop the insect embryo, but in Hymenoptera, one or both may be rudimentary or absent. Embryonic envelopes function in protection and nutrition, and usually occur well developed in species with little yolk. Eggs with little yolk are usually minute when deposited in the host. Then, probably by osmosis or active absorption of host fluid, they gradually become larger (Imms, 1931; Simmonds, 1947c). Expanding eggs of this type have been called hydropic (Flanders, 1942). In those species in which the trophamnion is broken and cells of the membrane move in the host's hemolymph, these cells increase in size proportional to the growth of the larval parasitoid (Hagen, 1964). They become greatly enlarged while retaining their trophic function because the larva feeds on these cells (Jackson, 1928; O. Smith, 1952). Host nutrition influences the development of these cells and, through them, the development of the parasitoid larva. Some membranes persist, coveting the larva. For example, the chorion may remain intact until after first larval ecdysis (Flanders, 1964) or the chorion may be shed early and the developing embryo is enveloped by a trophic membrane that remains without disintegrating until after the parasitoid larva sets itself free in the host (Caltagirone, 1964). The embryology of an endoparasitic hymenopteran, Coccygomimus turionellae, is discussed in detail by Bronskill (1959). Egg orientation is similar in all Hymenoptera studied and follows Hallez's (1886) law of orientation within the polytrophic ovariole. The anterior pole is directed toward the head of the parent female. However, during oviposition, the posterior pole emerges first. The dorsal, ventral, and lateral sides vary within the same individual. The embryo remains in the original cephalocaudal axis during the entire development, but just before eclosion it rotates 180 degrees on the longitudinal axis. Eclosion from the egg usually occurs when histogenesis is complete. Exceptions occur and first instar larvae of some internal parasitoids are precociously emerged embryos (Imms, 1931). Eclosion is not always immediate, and some eggs may overwinter in the completely incubated condition. Eclosion by parasitoids may require very high relative humidity (Gerling & Legner, 1968). Specific host organs may serve as oviposition sites, and chorions may be coated to avoid encapsulation in the host (King et al., 1968). Polyembryony is a form of asexual reproduction in which many embryos develop from repeated division within one egg (Marchal, 1898, 1904). It has been reported in several groups of insects (Silvestri, 1906, 1923, 1937; Kornhauser, 1919; Leiby & Hill, 1923, 1924; Leiby, 1929; Parker, 1931; Daniel, 1932; Paillot, 1937; Doutt, 1947,

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1952; Ivanova-Kasas, 1972). Among parasitic Hymenoptera, polyembryony is known in Braconidae, Encyrtidae, Platygasteridae, and Dryinidae; and is best documented in the Encyrtidae (Doutt, 1947; Cruz, 1981, 1986a, 1986b). Generation time in polyembryony varies from several weeks to a year. Embryo development begins just as in monoembryony. Polar nuclei, however, do not enter directly into the blastula stage, but produce an embryonic membrane (trophamnion) that surrounds the developing embryo-like area. The trophamnion extracts nutrients from the host hemolymph (Koscielska, 1962, 1963). The embryo then divides into small groups of cells (morulae) enclosed by the trophamnion. The trophamnion then changes into a chainlike structure with the morulae arranged in a row or branching cluster. This finally breaks up and separate embryos are formed. The number of embryos from a haploid egg is less than that from a diploid egg. The Larva

Larval Hymenoptera typically consist of a head, three thoracic segments, and 9 to 10 abdominal segments. Apocrita lack thoracic or abdominal appendages, except in Proctotrupoidea and Cynipoidea (see later). Frequently larvae show five instars, but variation is common. Determining the primitive condition is difficult because only a few taxa have been studied. The number of mandible exuviae is used as evidence for determining instar numbers, but dimorphism may occur within one larval instar, and sexual dimorphism in the larvae can be striking. The anatomy of final instar parasitic Hymenoptera larvae has been described (Short, 1978; Finlayson & Hagen, 1979; Gillespie & Finlayson, 1983). Conventional larval development is seen in many Hymenoptera. The eruciform larva is shaped like a caterpillar with a well-developed head capsule, thoracic legs, and abodominal prolegs. The Symphyta express this larval type that may represent the ancestral condition for Hymenoptera. The hymenopteriform larva represents the generalized larval form seen in the Apocrita. The body is spindle shaped, without thoracic legs, featureless with pale to translucent integument, and head capsule weakly developed or absent. The mandibulate larva has a large, sclerotized head, large falcate mandibles, and body-tapered posteriad. The caudate larva has a body with long, segmented, flexible caudal appendages. The function of caudal appendages is not established; sometimes they are reduced in later instars and lost in the last instar. The caudate form is displayed by some endoparasitic ichneumonid larvae. The vesiculate larva has the proctodaeum everted, and displays short caudal appendages with vesicles at the bases. This larva is seen in some Ichneumonidae and Braconidae. The mymafiform larva displays a conical anterior process and the abdomen of some species is segmented. This larval form is found in

Mymaridae and Trichogrammatidae. The sacciform larva is ovoid, featureless, and without segmentation. It is found in Dryinidae and Trichogrammatidae. The polypodeiform larva is segmented with paired, short, flexible projections from thoracic and abdominal segments. It is found in Cynipoidea and Proctotrupoidea. Many Parasitica are hypermetamorphic and larvae change in shape during successive instars as a normal consequence of development. Several first instar morphs are diagnostic of some Hymenoptera families. Thus, the teleaform larva is seen in Scelionidae: the first instar is not segmented, weakly cephalized with prominent protuberances or curved hooks cephalad, and the body has a caudal process with girdles or tings of setae around the abdomen. The cyclopoid larva is seen in Platygasteridae: the first instar shows a large swollen cephalothorax, very large, falcate mandibles and bifurcate caudal processes. The planidiform larva is seen in the Perilampidae and in a few Ichneumonidae: the migratory first instar is legless and somewhat flattened, and often displays strongly sclerotized, imbricated integumental sclerites and spinelike locomotory processes. The form is often confused with the triungulin (Heraty & Darling, 1984). The eucoiliform larva is seen in Eucoilidae, Charipidae, and Figitidae: the first instar displays three pairs of long thoracic appendages but lacks the cephalic process and girdle of setae of the teleaform larva. Subsequent instars are polypodeiform. Defense from and evasion of predators are important to parasitoid larvae. First instars use various methods of locomotion from moving sluglike to jumping. Fast locomotion is typical of species that lay their eggs a distance from the host (Clausen, 1976). Exposed larvae are protected by spines and sclerites. Internal parasitoid larvae often show large or well-developed mandibles (Salt, 1961), presumably used in defense. Also, cytolitic enzymes, secreted by one parasitoid to kill another, have been suggested as a method of eliminating competitors (Spencer, 1926; Thompson & Parker, 1930; O. Smith, 1952; Salt, 1961; Gerling & Legner, 1968). Identification of the toxic compound or compounds has been difficult. Methods of eliminating competitors can be sophisticated. For instance, physiological suppression of supernumerary parasites is common among Parasitica (Fisher, 1971). Typically, young larvae are eliminated without physical contact between competitors. Nevertheless, mechanisms of suppression are poorly understood. Encapsulation of moribund parasite eggs and larvae by host phagocytes may result in death of supernumerary individuals via anoxia. Altematively, older parasitic larvae may consume nutrients essential for development of young larvae and death of the younger individuals results from inanition. First-instar larvae show diversity in respiration (Clausen, 1950). Endophagous larvae respire through the integument or obtain air from outside the host through tubelike struc-

Chapter 15

Biology of Parasitic Hymenoptera

tures (a membranous cocoon attached to the host tracheae). The final instar may possess a different spiracle arrangement and number while early instars may lack spiracles (Hagen, 1964). The prepupal stage begins when the last larval instar stops feeding, voids meconia, and shows little movement. Although this is often referred to as a resting stage, the animal is active physiologically. The onset of prepupal formation may vary among individuals developed from eggs deposited during a short period (ca. 24 h) or it can occur synchronously (Gerling & Legner, 1968; Legner, 1969a). Connection between midgut and hindgut begins when the last larval instar is fully fed, and is completed during the prepupal stage. The prepupal stage lasts less than 24 h; meconia are eliminated as pellets or encased in a peritrophic sac (Gerling & Legner, 1968).

The Pupa The pupal stage of parasitic Hymenoptera has been superficially studied, and most work is limited to line drawings or photographs of the habitus. Most hymenopteran parasitoids do not spin cocoons. However, fully fed endophagous larvae can construct membranous cocoons while immersed in the host fluids. Similar cocoonlike structures are found between gregarious (polyembryonic) pupae. The duration of the pupal stage can be variable or remarkably equal among the progeny of one female per day (Legner, 1969a). Typically, the progenies of one ovipositional episode all exit the host immediately after eclosion from the pupa, or they may remain inside for variable lengths of time depending on when the adult bites through the encasing host (Legner, 1969a). Oogenesis-Ovisorption-Spermatogenesis Oogenesis in arrhenotokous Hymenoptera resembles diploid-diploid organisms, but spermatogenesis is highly modified (Crozier, 1975, 1977). Male Hymenoptera are hemizygous, and spermatogenesis is modified to ensure that a balanced set of chromosomes is transmitted via the sperm. The first division is abortive, with no karyokinesis (Crozier, 1975). In most Hymenoptera, the sperm of a haploid male are genetically identical. Parasitica ovarioles have been characterized as proovigenic or synovigenic. Both conditions are generally viewed as species characteristics. However, the distinction is probably artificial, and when all parasitic Hymenoptera have been studied, we will see a continuum between conditions termed "proovigenic" and "synovigenic." Most eggs are laid by neonate females and the oviposition period of an adult female is usually short. Synovigenic species generally synchronize oogenesis with oviposition and the oviposition

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period of an adult female is relatively long. Conventional wisdom holds that synovigenic species are more effective in biological control because they are longer lived and can reproduce at lower densities of the host population. This has yet to be demonstrated. Synovigenic species are further divided into subgroups where ovulation is internally or externally induced. Ovisorption is "the capacity of the follicle cells to dissolve and absorb the oocyte" (DeWilde, 1964). Several factors influence this phenomenon in which vitellogenesis is interrupted and the oocyte dies in the follicle. Follicle cells cease to participate in egg formation; they may divide and absorb the dead oocyte. Their nuclei become pycnocytic, and the cells break down and are absorbed through the ovarian sheaths (King, 1963; Richards & King, 1967). From a biological control viewpoint, ovisorption is important in parasitoids where effectiveness as natural enemies depends in part on their conservation of reproductive material, correlated with a high searching capacity (Doutt, 1964). Ovisorption has been reported in several orders of insects (Pfeiffer, 1945; Highnam et al., 1963). When certain Parasitica that ovulate yolk-replete eggs are deprived of hosts, the process of oogenesis and ovisorption occurs synchronously. This enables a female to deposit newly formed, viable eggs after a period of inhibited oviposition (Flanders, 1935b, 1942; Medler, 1962; Hopkins & King, 1964, 1966; King & Richards, 1968a; King & Ratcliffe, 1969). Under other conditions, inviable and viable eggs may be indiscriminately deposited in a host (Geding & Legner, 1968). Partially absorbed, viable eggs may produce diploid males (Flanders, 1943b), embryonic starvation (Flanders, 1957, 1959b), or change the normal sex ratio (King, 1962). Ovisorption occurs when conditions are unfavorable for mature eggs (Flanders, 1942; Edwards, 1954b; LaBergrie, 1959; Phipps, 1966) or when parasitism has taken place (Palm, 1948). Host feeding, oviposition, and ovisorption are closely related processes that affect fecundity, longevity, and host-killing capacity of the parasitoid (DeBach, 1943b; Legner & Gerling, 1967; Legner & Thompson, 1977). Storage of mature eggs in muscular oviducts of hydropic species is correlated with the ability to discharge a large number of eggs quickly during one insertion of the ovipositor, or a large number of eggs singly if hosts are available. Rapid egg deposition probably is responsible for the high number of braconid species yielding a preponderance of male progeny (Clausen, 1940). Anhydropic species with short oviducts ovulate when environmental conditions are favorable for immediate egg deposition. The rate of oviposition may be governed by the number of ovarioles (Clausen, 1940). In gregarious species the number of eggs deposited per host may be influenced by the number of mature eggs in the ovarioles, which at

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least in one case is regulated by a polygenic system (Legner, 1987b, 1988a, 1989b). Because ovisorption may preclude ovulation in some anhydropic species, the responsiveness to oviposition stimuli may be a function of the frequency of oviposition (Flanders, 1942; Legner & Gerling, 1967; Gerling & Legner, 1968). Females of anhydropic species may lose the ability to respond to oviposition stimuli if deprived of hosts for long periods (Jackson, 1937). Fecundity is sometimes lowered after ovisorption has occurred (King, 1962).

Oviposition Strategy a n d Progeny N u m b e r Anatomy of the female reproductive system has been studied in some Parasitica (Iwata, 1959a, 1959b; 1960a, 1960b, 1962; Copeland & King, 1971, 1972a, 1972b, 1972c; Copeland, 1976). Parasitoids have developed ovipositional strategies that are essential for optimizing lifetime performance (Cook & Hubbard, 1977; Hubbard & Cook, 1978; Waage, 1979; Iwasa et al., 1984). Some Parasitica can restrain oviposition, but egg retention lasts only a few days because intrinsic pressure of egg accumulation forces oviposition (Lloyd, 1938; Simmonds, 1956). Adult Parasitica possess a high inherent fecundity, are long lived, and actively search for hosts. Within a generation they can increase progeny production in response to rising host densities (Flanders, 1935a; DeBach & Smith, 1941; Burnett, 1951). This increase can be induced through mechanical and sensory processes (Madden & Pimentel, 1965; Legner et al., 1966; Legner, 1967a, 1967b). Contributions have been made concerning the behavioral mannerisms whereby this acceleration becomes possible (Wylie, 1965a, 1966a, 1966b). The relationship between parasitoid density and effective rate of reproduction has been studied (DeBach & Smith, 1947; Burnett, 1953, 1956, 1958a, 1958b, 1967; Bouletreau & David, 1967; Legner, 1967b). Factors involved in determining the effective rate include temperature, humidity, host size, adult parasitoid food, and larval competition. Temperature and humidity influence parasitoid efficiency and oviposition. Low temperature can reduce the oviposition capacity and act with host density to reduce the number of hosts contacted by the parasitoid (Burnett, 1951). In some species, the greatest influence of temperature results from its differential effect on fecundity and rate of development of the host and parasitoid (Burnett, 1949). In other species, an increase in temperature combines with an increase in host density to induce a greater percentage of parasitoid emergence during one parasitoid generation (Burnett, 1951). This illustrates the importance of optimum temperature for maximum host destruction. Parallel results were obtained in a field experiment (Burnett, 1951). Greenhouse studies show that with an increase in temperature,

efficiency of the parasitoid increases and percentage of parasitism rises (Burnett, 1953). Humidity influences the oviposition rate of parasitoids (Martin, 1946; Martin & Finney, 1946). Higher humidities generally promote longer adult longevities (Legner & Gerling, 1967; Olton & Legner, 1974). Parasitoid females estimate host size, and those of gregarious species adjust the number of eggs laid in response to that estimate, larger hosts receiving more eggs (Edwards, 1954a). The ability to estimate host size and to adjust clutch size in response to that estimate appears widespread in bethylids (Legner et al., 1966; Gordh et al., 1983; Gordh & Medved, 1986). An optimal size for ectophagous parasitoids is manifest in species attacking synanthropic flies (Legner, 1969a). Adult parasitoids often distribute their progeny in such a way as to avoid competition. In superparasitized hosts supernumerary eggs and larvae die (Salt, 1961). Gregarious parasitoids discriminate among hosts, although the ability may be imperfect or temporary. Under some conditions, females refrain from laying supernumerary eggs; under other conditions (e.g., scarce healthy hosts) restraint fails and females oviposit into parasitized hosts. Thus, for lack or failure of discrimination, or by breakdown of restraint, superparasitism and thereby competition occur. Four modes of competition are usually recognized: (1) physical attack, (2) physiological suppression, (3) injury, and (4) selective starvation. Supernumerary larvae of gregarious parasitoids are not always eliminated as early as solitary parasitoids. Often, final instar, gregarious larvae are found dead. Death of weaker competitors from food shortage has usually been implied. Adults dwarfed from severe competition also support this idea (Wylie, 1965b). Suffocation has been shown in some examples. Larval competition can be reduced by the female producing unfertilized eggs when superparasitism is possible (Holmes, 1972). Male larvae can compete effectively under crowded conditions (Wylie, 1966b). Sex Regulation Sex-ratio theory has been dominated by research on vertebrate animals since Darwin developed the principles of natural selection. Conventional wisdom held that sex ratios typically fluctuated around 1:1 (Fisher, 1930). Later work with Parasitica shows that sex ratios of parasitic insects often deviate from 1:1 (Hamilton, 1967). Apparent from this research is that adult female wasps control the sex of their offspring and that numerous factors shape proximate and ultimate sex ratios in parasitic organisms. Insect sperm stored in the spermatheca retain their vitality for many years (Lillie, 1919), and are quiescent, except when females are in contact with oviposition sites (Flanders, 1939). The sperm at the opening of the spermatheca

Chapter 15

Biology of Parasitic Hymenoptera

must be exposed to an activating agent before they can migrate through the spermathecal duct to the oviduct where the egg is fertilized. The agent apparently originates in the spermathecal gland, which presumably secretes a fluid that is slightly alkaline (Flanders, 1946a, 1946b; Lensky & Schindler, 1967). The capacity of the spermathecal gland, adjusted to the rate of egg deposition, is probably an important factor in determining the sex ratio (Flanders, 1947, 1950). Three anatomical types of spermathecae have been described in Hymenoptera (Flanders, 1939, 1956). Type I is found in the honeybee, and in Typhia. The spermathecal duct can be bent into a valve at its juncture with the capsule and several sperm can be discharged simultaneously. Glandular fluids activate and transport sperm and regulate the number of sperm released on each egg as it passes along the oviduct. The spermathecal gland empties into the sperm capsule instead of the spermathecal duct as in other species. Type II is found in ichneumonids and braconids. The spermathecal gland empties into the lumen of the spermathecal duct. The short exit passage from the capsule to the spermathecal duct is narrow, limiting the rate of sperm passage. The gland is voluminous in ichneumonids; braconids have a smaller gland that is accompanied by a contractile reservoir. Type III occurs in chalcidoids. The spermathecal gland is very small and secretions only activate sperm. The spermatozoa in these species are extraordinarily long. Hymenoptera regulate the sex ratio of their offspring (Crew, 1965; Hamilton, 1967; Charnov, 1979; Charnov et al., 1981; Green et al., 1982). Factors involving the adult female can influence fertilization of an egg by arrhenotokous Hymenoptera, and thus change the sex ratio. Some factors are female age (Wilkes, 1963; Legner & Gerling, 1967; Legner, 1985b), mating response changing with age (Crandell, 1939), sperm depletion (Gordh & DeBach, 1976; Nadel & Luck, 1985), rate of oviposition (Legner, 1967a, 1967b), delaying or interrupting oviposition (Wilkes, 1963; Legner & Gefling, 1967; Legner, 1985b), host density (Flanders, 1939), changing parasite density (Wylie 1965a, 1965c, 1966b), host size (Holdaway & Smith, 1932; U1lyett, 1936; Taylor, 1937; Legner, 1969a), multiple copulation by females (Flanders, 1946b), female discrimination (Flanders, 1939; Legner & Gefling, 1967; Werren, 1984), and ratio of different hosts (Flanders, 1959a). The haplodiploidic sex-determining mechanism in Hymenoptera results in the whole genetic complement carried by the male subjected to natural selection; thereby deleterious mutations are eliminated (Gauld, 1984). Thus, sibmating, which is common in those species exhibiting female-biased sex ratios, is not deleterious. Temperature extremes also influence sex ratio in Parasitica (Wilson & Woolcock, 1960; Flanders, 1965; Bowen & Stem, 1966; Quezada et al. 1973; Gordh & Lacey, 1976). High temperatures can influence the sex ratio through ster-

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ilizing effects during postembryonic development (Wilkes, 1959). Sex-ratio upsets can be induced by low temperature (Schread & Garman, 1933, 1934; Lund, 1938; DeBach & Argyriou, 1966; DeBach & Rao, 1968). Fertility of parasitoids subjected to low temperatures during development may be adversely affected (van Steenburgh, 1934; Anderson, 1935). Larvae stored at 15~ may not change the sex ratio of their offspring, but pupae stored at this temperature can produce a greater proportion of male progeny (Hanna, 1935). Chalcidoid larvae stored near 0~ can sustain a greater male mortality, causing a predominantly female sex ratio (DeBach, 1943a; DeBach & Argyriou, 1966; DeBach & Rao, 1968). Moursi (1946) reviewed cases where low temperature especially seemed to produce sex-ratio changes in parasitoids. He considered as causes: (1) inadequate stimulation of the spermathecal gland, (2) depletion of spermathecal secretions, and (3) failure of spermathecal nerves and muscles to function or synchronize the discharge of sperm with the expulsion of eggs through the oviduct. Prolonged exposure of males to low, nonlethal temperatures may induce gonad malnutrition in mature larvae and pupae (Flanders, 1938). Some third-instar chalcidoid larvae stored at low temperatures transform into adults with changed fecundities that produce a preponderance of female progeny (Legner, 1967a). Prolonged storage of mature chalcidoid larvae at low temperature does not influence the sex ratio of surviving adults (Legner, 1976). Males are produced by deuterotokous Hymenoptera in populations that would otherwise be 100% females and thelytokous (E. L. Smith, 1941; Flanders, 1945; Bowen & Stem, 1966; Legner, 1985b). These males can be produced after periods of hot weather (E. L. Smith, 1941; Gordh & Lacey, 1976) or during oviposition at high temperature (Legner, 1985a). Extranuclear substances, such as microorganisms and/or chemicals, are suspected to be involved in the expression of thelytoky. The manner in which thelytoky becomes incorporated in a hybrid arrhenotokous population of Muscidifurax raptor Girault & Sanders (Legner, 1987a, 1987c; 1988b), and the switch from thelytokous to arrhenotokous reproduction in Trichogramma spp. after treatment with antibiotics (Stouthamer & Luck, 1988; Stouthamer, 1989) implicate microorganisms. Thus, thelytoky may actually originate as an infection and may be accompanied by reduced parasitoid vigor (Legner & Gerling, 1967; Legner, 1988c). Sex ratio can be shaped by differential mortality of immature parasitoids (Jenni, 1951; Wilkes, 1963). In multiparasitism, the first individual present usually survives. Often, mortality among gregarious larvae involves females more than males (Vandel, 1932; Grosch, 1948). Superparasitism and subsequent larval competition can reduce female progeny (Kanungo, 1955). Conceivably, this mechanism may contribute to the stability of the system by

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avoiding over-exploitation of the host through reducing the number of females in the next generation. However, the proportion of females can be higher as a result of an increase in superparasitism in mass culture units (Martin & Finney, 1946). The stage or the species of hot can influence parasitoid sex ratio. Thus, a thelytokous braconid produces only female progenies when oviposition occurs in beetle larvae, but males are produced when eggs are laid in adult beetles (Kunckel & Langlois, 1891). One sawfly feeding on alder is usually unisexual, but closely related species feeding on birch are bisexual (Bischoff, 1927). One aphelinid is unisexual when reproducing on San Jose scale growing on peach trees, and bisexual when reproducing on San Jose scale growing on melon (Flanders, 1944a). A gall-forming eurytomid is unisexual on one variety of Acacia and is bisexual on another (Flanders, 1945). Microorganisms (viruses, bacteria, spiroplasmas) can alter sex ratios by selective elimination of immature males or females (Werren et al., 1981, 1986; Skinner, 1982, 1985; Vinson & Stoltz, 1986). Stoltz and Vinson (1977) and Stoltz et al. (1976) found viruses in the calyx epithelial cells of endoparasitoids; Fleming and Summers (1986) found them in the lumen of the oviduct. These viruses were passed from parent to offspring, males transmitting viral DNA to females during copulation (Stoltz et al., 1986). Host F e e d i n g Host feeding is a phenomenon in which female parasitoids wound hosts with the ovipositor or mandibles and consume hemolymph at the wound. This behavior affects the biology of the parasitoid and the dynamics of populations in many ways. Marchal (1905) concluded that the ovipositor was used more often for host feeding than for oviposition. Host feeding prolongs the life of the female and supplies protein needed for oogenesis (King & Hopkins, 1963). Neonate adult synovigenic Hymenoptera may not have mature eggs and host feeding may provide nutrients necessary for egg development. Some females with mature eggs in the ovaries will not oviposit until after host feeding (Moursi, 1946). Other females will oviposit immediately after emergence, but if hosts are withheld during middle age, host feeding is required for additional oviposition. Adults of some species do not contain mature eggs at the pupal stage, but oviposition occurs before host feeding (Flanders, 1936). Host feeding among parasitoids has not been sufficiently studied, but it has been reported in numerous species in 18 families (Jervis & Kidd, 1986); it may be important in applied biological control (Van Driesche et al., 1987). It is unknown in proovigenic species, in some species whose males and females develop in unrelated hosts, and in species where yolk-deficient eggs are stored in the oviducts. In

some cases, the published record may be erroneous. Host feeding has been reported in many species of bethylids, but this is questioned (Gordh, unpublished). The close association of host feeding and oviposition in many Parasitica probably indicates that the habit of ovipositing in other insects evolved with host feeding by adults. Adult predacious habits preceded parasitic oviposition. Bartlett (1964) reasoned that the widespread occurrence of predation by adults of 20 families of parasitic Hymenoptera provides little evidence of the evolutionary pathways through which predation by adult parasitoids might have developed. In the Ichneumonoidea, predation by adults is commonly encountered in the form of host feeding. The habit appears more widespread among the Ichneumonidae than among other Parasitica, and the adults of some species completely consume their hosts. Host-feeding patterns in Chalcidoidea are not consistent. In some genera of Pteromalidae, Eulophidae, and Aphelinidae it is the rule. Host feeding is prominent in encyrtid genera such as Metaphycus and Microterys, but it is conspicuously absent in some species of these genera. Host feeding appears sporadic within the Eupelmidae and Eurytomidae, and appears infrequently in the Trichogrammatidae. Predation by adult Cynipoidea is poorly represented, and seems best expressed by Figitidae. Predation by adult Proctotrupoidea has been noted in Scelionidae. Although a few cases are known where specific stages of hosts are preferred, there usually is less specificity shown in host feeding than in ovipositional attack (Bartlett, 1964). Host feeding has direct effects on the host population, and some parasitoids kill a significant number of hosts by feeding directly on them. Host feeding by parasitoids is often associated with mutilation of the host. This is detrimental to parasitoid reproduction because associated species are affected (Flanders, 1951). Early workers felt that host feeding may work against the regulation of host densities by destroying hosts inhabited by immature parasitoids (Hartley, 1922; Flanders, 1953b). However, host destruction through host feeding is important in natural mortality of synanthropic Diptera (Legner, 1979b). Within the Parasitica, host feeding is not necessary to obtain amino acids because they are found in honeydew and plant nectaries (Zoebelein, 1956a, 1956b). Nevertheless, diet in general is influential on fecundity (Bracken, 1969). The effects of host feeding on host regulation also have been considered (Flanders, 1953b). Parasitism is more effective than predation at low population densities. Protein requirements of the parasitoid are minimal. Eggs produced by a parasitoid, but not deposited, are absorbed and the egg material is used to prolong life (Flanders, 1950, 1953b). Higher host populations are needed to maintain host-feeding species. However, host-feeding habits of adult parasitoids appear valuable in reducing high host populations and may be an advantage in periodic inundative releases.

Chapter 15

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Host feeding affects oogenesis and ovisorption. When deprived of hosts, many Parasitica resorb the mature eggs (Flanders, 1935b; Grosch, 1948; Grosch et al., 1955). Experimental studies with starvation and diets of honey and host blood have demonstrated subtle differences in longevity, oogenesis, and egg resorption (Edwards, 1954b; Gerling & Legner, 1968). D i a p a u s e in Parasitoids Diapause is a state of arrested growth or reproduction of many hibernating or estivating arthropods. Diapause differs from quiescence. For instance, eggs of some parasitoids deposited in hosts hatch, but the parasitoid larva do not develop further until the host is about to form the puparium. Sometimes this behavior is regarded as a form of quiescence instead of diapause. Borderline cases occur, but physiological mechanisms can be recognized in diapausing insects that are absent from quiescent insects (Tauber & Tauber, 1976). The arrest is facultative (environmental stimuli direct the organism to continue or to terminate development) or the arrest is obligatory. In facultative and obligatory diapause, control of development is exercised by the endocrine system (Beck, 1968). The causes of diapause in the Parasitica are not simple. Individuals may enter diapause at a time when the environment is favorable to continuous development and increase of the species. Older females can decrease the percentage of their progeny entering diapause. Females in which development had passed through diapause produce a much lower incidence of diapause in their progeny. Prolonging an adult female's life by change in diet causes an increase in progeny diapause. Diapause incidence can increase if unnatural hosts are used as larval food. The physiological state of the parent female before and during oviposition can influence the proportion of her progenies that enter diapause (Flanders, 1944b, 1972; Simmonds, 1946, 1947b, 1948; Schneidermann & Horwitz, 1958; Saunders, 1962, 1965, 1966a, 1966b). The effects of temperature on diapause are variable (Saunders, 1967) and temperature may affect the induction of diapause through photoperiodic influences (Sullivan & Wallace, 1967). High temperatures tend to avert diapause in long-day species; low temperatures may avert diapause in some cases. Temperatures are important in determining whether photoperiod can act. Temperature and photoperiod may act differently on different developmental stages to cause diapause (Eskafi & Legner, 1974). Parasitoid development can depend on the physiological state of the host, or parasitoids can have their own photoperiodic responses. Pupal diapause can be determined by the photoperiod applied during the larval stage (DeWilde, 1962; Danilevskii, 1965). Photoperiod can induce diapause in the parasitoid while the host remains active (Geyspitz &

Kyao, 1953; Maslennikova, 1958). Some photoperiodic responses of the host and parasitoid are difficult to separate. Some endoparasitoids diapause only when in hosts that are themselves in diapause (Doutt, 1959). Photoperiod is an important factor in intraspecific geographic differentiation and in shaping evolution. Photoperiodic response in local populations of an insect species may differ according to the latitude at which the species occurs without being accompanied by distinguishing morphological features. These populations may differ in the intensity of response, in the effect of temperature on the response, and in the critical photoperiod. At higher latitudes populations tend to become univoltine and to exhibit obligatory diapause. Moreover, photoperiod-induced diapause tends to be more intense in populations of high latitudes. Two seasonal forms exist, the long day and the short day. Seasons exert their influence according to the particular form. Doutt (1959) felt that the intervention of diapause in some stage of the life of a parasitoid may be essential for synchronization of development between host and parasitoid. Flanders (1944b) considered diapause in parasitoids as adaptive in that it delays development until the host attains the stage presumably most suitable for the nutritional requirements of the parasitoid. Simmonds (1946, 1947b, 1948), however, attributed diapause to a physiological maladjustment during development. He did not feel diapause was adaptive to enable a species to survive a period unfavorable to further growth. Andrewartha (1952) and Hodek (1965) found that diapause in the adult stage may take the form of a failure to mature eggs or sperm and may be manifested by an extended preovipositional period. The preoviposition period of the adult could be prolonged by subjecting feeding larvae to lower temperatures. Walker and Pimentel (1966) have found a correlation between longevity and diapause. Genetics Electrophoretic techniques have revolutionized genetic studies of parasitic Hymenoptera. Electrophoresis has established low levels of variability in cultured stock compared with recently collected wild cultures (Legner, 1979a; Unruh et al., 1983). The stock used to start colonies of some parasitoids possessed only a fraction of the gene pool of the parental wild populations (Unruh et al., 1983). However, Hymenoptera generally show lower genetic variability than do other insect orders (Crozier, 1971, 1975; Metcalf et al., 1975). Small laboratory colonies lose large amounts of behavioral variability after a few generations in culture (Legner, 1979a; Unruh et al., 1983). Today we recognize that the aspects of parasitoid genetics are more complex than suspected. Studies on the pteromalid genus Muscidifurax show extranuclear phases in the inheritance of polygenes for quantitative reproductive traits

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(Legner, 1989a). Males of this wasp can change the female's oviposition phenotype upon mating, by transferring an unknown substance capable of regulating such change. This change is passed to the offspring. It appears as if a proportion of the genes in the female are phenotypically plastic and can change expression under the influence of substances in the male seminal fluid. The intensity of this response is different depending on the genetic composition of both the male and the female. Full expression occurs in the F1 female (Legner, 1988a, 1989a). Behavioral changes after mating are permanent as revealed by increases or decreases in the response maintained for 16 days following a particular mating (Legner, 1987b, 1989b). There is no change back to the original behavior following a second mating with a male of the opposite genotype (Legner, 1989a). Speculations on the nature of the substance in the male seminal fluid have included microorganisms, accessory gland fluids, and such behavior-modifying chemicals as prostaglandins (Legner, 1987b, 1988a). Because inheritance of such genes seems to occur in a stepwise manner, the entire process has been termed "accretive inheritance" (Legner, 1988b, 1989a). The inheritance scheme in the pteromalid Muscidifurax is fundamentally important to a wider understanding of genetics of Hymenoptera. The kinds of genes capable of phenotypic alteration in mated females before being inherited by their progenies have been termed "wary genes" because they, or precursors of them, are tested in the environment in an attenuated manner before inheritance by the offspring (chromosomal inheritance) (Legner, 1985b, 1989a). We do not know whether such genes possess chemical precursors capable of changing the female's phenotype or are inherited extranuclearly after mating. The ability of the male substance to switch a polygene locus "on" or "off" in the mother suggests that a locus may exist in two states: active and inactive. In Muscidifurax at least eight loci are thought to be active in determining multiple oviposition behavior (Legner, 1991). In the process of hybridization, wary genes may serve to quicken the pace of evolution by allowing natural selection for both nonlethal undesirable and desirable characteristics to act in the parental generation. Wary genes that are detrimental to the hybrid population thus might be more prone to elimination and beneficial ones may be expressed in the mother before the appearance of her active progeny (Legner, 1987b, 1988a). If wary genes occur more generally in Hymenoptera, their presence might partially account for the rapid evolution thought to have occurred in certain groups (Hartl, 1972; Gordh, 1975, 1979). Selective

Breeding

Increasing the average number of progenies through selective breeding is seen as a possible benefit to biological

control. Studies of Parasitica have been conducted with this objective in mind (Wilkes, 1942, 1947; Allen, 1954). Several generations are required for the desired effects, which may include increased fecundity as well as reduced larval mortality. Hybridization techniques may be useful for increasing the fecundity and the host destructive capacity of parasitic insects (Legner, 1972, 1988b). However, the choice of parental race is very important for success (Legner, 1988b), and should probably be restricted to cohorts from similar climatic zones, because negative heterosis could result (Legner, 1972). Insemination by old males of some chalcidoids is not always successful and females inseminated by them produce fewer female progenies (Wilkes, 1963; Gordh & DeBach, 1976). In some Parasitica the female may be less fecund after copulation, possibly because she exercises greater discrimination in host selection. Some Parasitica oviposit as readily before copulation as they do afterward. Sex ratios in these species are determined partly by the amount of oviposition prior to mating. In aphelinids where oviposition instincts are permanently changed by copulation, male production is obligatory before copulation and is facultative afterward. Insemination has a profound and irreversible effect on behavior of some Parasitica, and hefttable traits for fecundity and other reproductive behavior are expressed in the mother immediately after mating at an intensity dictated by the male's genome through an extranuclear phase of inheritance (Legner, 1987b, 1988a).

ECOLOGY OF PARASITIC HYMENOPTERA The interaction of parasitoid and host is behaviorally complex and ecologically multifaceted. Laing (1937) proposed three steps in the attack activity of a parasitoid: (1) attraction to the host habitat, (2) attraction to host individuals in the habitat, and (3) acceptance or rejection of the host. Flanders (1937a) concurrently proposed a fourth step in the process. His steps were (1) host habitat finding, (2) host finding, (3) host acceptance, and (4) host suitability. A fifth component, host regulation, is important from a biological control standpoint (Vinson, 1975b). Restatements of the procedures in host selection include those by Salt (1935, 1958), Thorpe and Caudle (1938), Doutt (1964), Hodek (1966), Weseloh (1981), and Vinson (1976, 1984). Habitat Location Davis (1896) first observed, without indicating the cause, that some plants such as Nicotiana, Pelargonium, Datura, and Eucalyptus were repellent to the aphelinid Encarsia formosa Gahan, a whitefly parasitoid. Later, Picard and Rabaud (1914) observed that many parasitic Hymenoptera attack species in several orders, provided the hosts feed

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on one species of food plant. Thus, natural enemies are often attracted to a habitat instead of directly to a host in the habitat. Recognizing this concept is important to biological control (Kulman & Hodson, 1961; Hagen et al., 1970). Numerous environmental factors affect parasitoids to bring about this attraction. These include leaf structure (Milliron, 1940; Thompson, 1951; Putnam & Herne, 1966; Downing & Moilliet, 1967), bud size (Graham & Baumhoffer, 1927; Arthur, 1962), plant variety (Franklin & Holdaway, 1966), host-plant odor (Altieri et al., 1982; Vet & Bakker, 1985; Vet & van Alphen, 1985), plant infestation (Flanders, 1940), soil type (Fleschner & Scriven, 1957), leaf exudations (Rabb & Bradley, 1968), honeydew (Milliron, 1940), fungal odor (Madden, 1968; Greany et al., 1977) odor of host food (Laing, 1937; Thorpe & Jones, 1937; Thorpe & Caudle, 1938; Edwards, 1954a), excreta of the host insect (Flanders, 1935a), host pupation depths (Ullyett, 1949), visual stimuli of the plant (Chandler, 1966, 1967), height of host location (McLeod, 1951; Thorpe, 1985), repellent effects of the plant (Davis, 1896; Speyer, 1929), host insect dioecy and habitat (Stary, 1964), and presence of alternative hosts (Eikenbary & Rogers, 1973). Food of a host may positively or negatively affect its parasitoids (Simmonds, 1944; Smith, 1957; Lawson, 1959; Hodek, 1966).

Host Location After the host habitat is located, hosts are located by random and directed search (Ullyett, 1943, 1947; Doutt, 1959). Olfaction is widely used by parasitoids in locating hosts (Bouchard & Cloutier, 1985; Dicke et al., 1985; van Alphen & Vet, 1986) and this behavior may be acquired (Vet, 1983, 1985). Parasitoids seem more attracted to higher densities of host and to certain patterns of host distribution (Legner, 1967b, 1969b). Host trail odors may facilitate searching (Price, 1970). Other olfactory stimuli exist (Vet & Bakker, 1985; Vet & van Alphen, 1985), and some physical host characteristics affect host selection (Weseloh, 1969, 1971a, 1971b, 1972; Weseloh & Bartlett; 1971; Wilson et al., 1974). Adding kairomones to a habitat can enable some parasitoids to locate their hosts more efficiently [Jones et al., 1971; Gross et al., 1975; Altieri et al., 1982; cf. Gardner & van Lenteren (1986)]. For example, T r i c h o g r a m m a spp. respond to chemical extracts of host moth scales and some braconids respond to extracts of host larval frass (Jones et al., 1973; Beevers et al., 1981; Noldus & van Lenteren, 1983, 1985). Synthesis of kairomones may enhance biological control on a larger scale (Vinson, 1968, 1975a, 1975b, 1976; Lewis et al., 1971, 1972; Weseloh, 1974). In some cases, however, kairomones may function to confuse parasitoids into lesser efficiency (DeBach, 1944; Chiri & Legner, 1982, 1983).

Host A c c e p t a n c e After the parasitoid has located the host, decisions must be made by the female parasitoid as to whether the host is acceptable for oviposition. Numerous cues suggest the host may be suitable for attack, including host odor, host size, host location, shape and motion, and host physiology (Bryden & Bishop, 1945; Arthur et al., 1969; Legner & Olton, 1969; Legner & Thompson, 1977). Salt (1935) termed host acceptance a "psychological selection." Huffaker [in Doutt (1959)] suggested it be called "ethological selection." A few species of parasitoids are host specific, but most attack several hosts in nature. However, no parasitoid is indiscriminate. Under natural conditions, a parasitoid will attack only a few of the species on which development is possible. Superparasitism is widespread in the Parasitica. Host discrimination (the ability to identify parasitized hosts) is intimately associated with superparasitism. The relationship between discrimination and superparasitism has been considered (van Lenteren et al., 1978; Bakker et. al., 1985) and many parasitoids discriminate parasitized hosts and avoid superparasitism. Flanders (1951) indicated that a "spoor effect" may be present. Chemoreceptors on the ovipositor that mediate female oviposition behavior are probably widespread in the Parasitica (Narayanan & Chaudhuri, 1955; Wylie, 1958; Greany & Oatman, 1972; Hawke et al., 1973; Domenichini, 1978; Van Veen & Van Wijk, 1985). An aversion to superparasitism is expressed by many parasitoids ready to oviposit. Biologists interpret this aversion as a mechanism to conserve eggs and increase efficiency in searching for hosts. From the viewpoint of applied biological control, superparasitism is important and mathematical models have been developed to address parasite distribution and the avoidance of superparasitism (Bakker et al., 1972; Rogers, 1975; Griffiths, 1977; Narendran, 1985). The ability to recognize parasitized hosts and selectively oviposit upon them must be important for hyperparasites. This is an aspect of host selection that has not been studied. Indeed, discrimination by hyperparasites must be complex because hyperparasitism has been derived independently several times in many distantly related lineages (Gordh, 1981). Beddington and Hammond (1977) developed a mathematical model for this system to analyze the implications of hyperparasitism for biological control. Tertiary hyperparasitism is a condition in which hyperparasites attack one another. Tertiary hyperparasitism has been divided into interspecific tertiary hyperparasitism (allohyperparasitism) (Sullivan, 1972; Matejko & Sullivan, 1984) and intraspecific tertiary hyperparasitism (autohyperparasitism) (Bennett & Sullivan, 1978; Levine & Sullivan, 1983). Biologically, tertiary hyperparasitism is a scheme of development that has rarely been documented in the field. It seems to arise from intensive competition, particularly in systems in which primary and secondary parasitoids are

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adelphoparasitic (Zinna, 1962). Its significance may be restricted to the laboratory, or to unusual circumstances best exemplified in aphid or scale parasites.

Parasitoid A t t a c k a n d Host Defenses Hosts do not necessarily represent passive resources placed at the disposal of the parasitoids (Doutt, 1963). At the individual level, physical interaction of parasitoid and host can be dynamic. A host may ward off a parasitoid externally before oviposition has occurred (Hinton, 1955; Cole, 1957, 1959), or may overcome the parasitoid internally after oviposition (Salt, 1935, 1955a, 1955b, 1957, 1960, 1963a, 1963b, 1965, 1966, 1967, 1968; Walker, 1959; Hadorn & Walker, 1960; Salt & van de Bosch, 1967; Streams, 1968). Internal defense reactions involve cellular (encapsulation and melanization) and humoral phenomena (D. Griffiths, 1960, 1961; K. Griffiths, 1969). Encapsulation is the formation of a cyst by host cells around foreign objects. Encapsulation occurs in epidermal, tracheal, gut, muscle, and nervous tissue. Hemolymphic capsules are formed by the hemocytes congregating and differentiating into two layers. Cells of the inner layer form connective tissue fibers. Opinions differ concerning whether these inner cells form a true syncytium and whether connective fibers are formed directly from the cell cytoplasm or are secreted by them (Schneider, 1950, 1952; Muldrew, 1953; Griffiths, 1960; Petersen, 1962; van den Bosch, 1964; Nappi & Streams, 1970). Melanization reactions involve the deposition of pigment around a parasitoid. It is thought that melanization is associated with encapsulation and is essentially a cellular phenomenon. The melanin formed is derived from tyrosine by way of phenolase reactions. Apparently, the substrate and enzyme are physically separated within certain blood cells normally, but injury causes the reaction to proceed. Humoral reactions are poorly understood and two viewpoints have been expressed concerning the role of encapsulation in defense. One view holds that hemocytes play a primary role in causing the death of living eggs and larvae of parasitoids. The other view argues that humoral phenomena cause immunity, and hemocytes merely act as scavengers. The first viewpoint is favored because living parasitoids have been found encapsulated. Host defense responses vary with the species of the host and parasitoid involved. In general, different hosts utilize different defense mechanisms against the same parasitoid, and different parasitoids cause similar defense reactions in the same host. Temperature, superparasitism, and multiple parasitism also affect immune responses. Parasitoids also may simply starve to death in a host that is unsuitable for its development (Flanders, 1937b)

Host Suitability Oviposition by a parasitoid is not necessarily an index of host suitability. The attractiveness of the host to the adult parasitoid is often independent of its suitability for larval parasitoid development. Muldrew (1953) suggested that a once-susceptible host population (that probably contained a few resistant individuals) may become totally resistant to parasitoid attack. Alternatively, some host-plant species may provide a superior nutritional source for host insects that results in higher survivorship by parasitoids (Mueller, 1983). In contrast, the host plant may confer on the host insect an immunity to parasitization (E. L. Smith, 1949; Flanders, 1953a; J. Smith, 1957). In a slightly different context, there is widespread observation and very recent unpublished experimental evidence that citrus trees that have received treatments of DDT or other insecticides change their nutritional value to favor pest insect species. Scale insects, for example, are stimulated to reproduce and grow at a faster rate. The effect of chemical pesticides and fertilizers on plants and their phytophages (insects, mites) was called "trophobiosis" by Chaboussou (1966, 1971). Parasitoids are also eliminated by the treatments so that host increase is unchecked for some time following a treatment. The so-called "DDT check method" (DeBach, 1955) to exclude the activity of natural enemies, therefore, may give distorted information on the actual value of the parasitoids and predators eliminated, because the host plants are artificially stimulated. Partial resistance of the plant to a pest may render the parasites of the pest more effective as controlling agents (van Emden & Wearing, 1965; van Emden, 1986).

SUMMARY At least 65,000 species of Hymenoptera are parasitoids, but only 765 species have been used in biological control programs worldwide. In this chapter we have reviewed the various major taxonomic groups and the unique adaptations (morphological, physiological, behavioral, and ecological) that make it possible for them to exploit a diversity of hosts in diverse environments. Among the other taxa that include parasitoidsmDiptera, Coleoptera, Strepsiptera, and Lepidoptera - - the Hymenoptera stand alone in the numerous species that are parasitoids. Their plasticity as a group is exemplified by their different mode of embryonic development, by interactions (trophic and otherwise) with their hosts, by the sex-determining mechanism, and by the intricate diversity of host selection processes. These and related topics are summarily reviewed based on a large list of publications that is by no means exhaustive.

Chapter 15

Biology of Parasitic Hymenoptera

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Chapter 15

Biology of Parasitic Hymenoptera

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[16[ Terrestrial Arthropod Predators of Insect and Mite Pests K. S. HAGEN,* N. J. MILLS,* G. GORDH,* and J. A. MCMURTRYw *Division of Biological Control, University of California, 1050 San Pablo Avenue, Albany, CA 94706 ~Insect Biology, Wellman Hall, University of California, Berkeley, CA 94720-3112 r of Entomology, University of Queensland, St. Lucia, Queensland 4072, Australia w of Entomology, University of California, Riverside, CA 92521

search for prey at each successive stage of its development and the success of this search determines the individual's growth and survival. Thus, both age structure and energetics are essential elements of predation. This was initially considered by Hassell et al. (1976) and Beddington et al. (1976) but more elegantly incorporated into a conceptual framework by Gutierrez et al. (1981, 1990), where predator satiation (Mills,1982a) and predator-prey life ratio (Sabelis, 1992) are the important factors influencing the impact of predation. At the population level, predators are typically less specialized and are seldom confined to attacking a single prey species. Thus, predator population development will often be determined by the abundance and characteristics of several prey species--the conquences of these factors have yet to be fully explored. The less specialized nature of predators and their requirement for a greater prey abundance to ensure oviposition and survival have generally led to their being considered less suitable than parasitoids in classical biological control (Huffaker et al., 1971; Huffaker et al., 1976). Conversely, predators can attack a wider range of prey stages than parasitoids and can continue to attack prey throughout their development. This means that predators have a distinct advantage over parasitoids in that they do not need to be synchronized with a single susceptible stage in the life cycle of their prey. The historical record, in fact, indicates that predators are no more difficult to establish (Hall & Ehler, 1979), and do not perform any less effectively than parasitoids in achieving complete success in the control of target pests (Hall et al., 1980). Hokkanen (1985) also noted that predators have been more effective against certain groups of pests (such as the Coleoptera) and in annual

INTRODUCTION Terrestial arthropod predators are important natural enemies. However, they often are overlooked and their impact underestimated in both natural and managed ecosystems due to a number of factors. For example, in contrast to all other natural-enemy groups, the duration of the interaction between a predator and each prey item is so brief that direct estimation of a predator's impact in the field is frequently impossible [see Wratten (1987), Luck et al. (1988) and Stuart and Greenstone (1990) for a discussion of methods for the indirect assessment of predation]. This brief duration of interaction, the tremendous overall diversity of the group, their frequent nocturnal activity, their more restrictive rearing requirements, and many other characteristics, all pose greater obstacles for the detailed investigation in comparison with other natural-enemy groups. The majority of predators are carnivorous throughout their life cycle, though in some groups, predation is confined to either juvenile (e.g., Syrphidae, Chrysoperla) or adult stages (e.g., Asilidae, Empidae). An interesting variation on this theme is found among some Miridae. The vulnerable first nymphal instar is often phytophagous but rapidly shifts to a predatory diet as it increases in size and searching capacity. There is also considerable variation in the number of prey consumed by predators, forming a continuum that extends from the near parasitoid characteristics of the vedalia beetle through to the voracious appetite of Chrysoperla carnea (Stephens). Conceptually, the action of predators is fundamentally different and more complex than that of parasitoids (Sabelis, 1992). At the individual level, a typical predator must

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cropping systems compared with more stable habitats. They have also been particularly effective against those pests that have no parasitoids, such as the Adelgidae and Tetranychidae. The use of predators in classical biological control may continue to fall behind that of parasitoids due to increasing environmental concerns over importations of less specialized natural enemies. However, their importance in augmentation and conservation is likely to increase in the future as pest management becomes less reliant on the use of synthetic insecticides. Predaceous arthropods are represented in nearly all taxa that make up the subphyla Chelicerata, Uniramia, and Crustacea, which compose the phylum Arthropoda (Hagen, 1987; New, 1991; Sabelis, 1992). We are concerned here only with the predaceous taxa that belong to the Chelicerata and Uniramia.

SUBPHYLUM CHELICERATA The Chelicerata is composed of three classes of over 63,000 known species. The most important class with regard to applied biological control is the Arachnida, divided into 13 orders. We will consider only the two most important, the Araneae (spiders) and Acariformes (mites).

Nevertheless, some studies suggest that spiders can be a significant mortality factor acting on some pest species, and have certain inherent traits as potentially effective predators. Some spiders have been shown to exhibit a sigmoidal or density-dependent functional response, characterized by a high plateau (Riechert & Lockley, 1984; Provencher & Coderre, 1987; Riechert, 1992). This high plateau (where no further increase in attacks occurs in response to increasing prey density) can be attributed to the characteristic of spiders killing many times more prey than they actually consume. Theoretically, a stable predator-prey interaction can be maintained by a sigmoidal functional response alone, without a numerical response of the natural enemy (Hassell, 1978). This, along with a self-limitation factor in the dynamics of polyphagous predators like spiders, may contribute to regulation of pest populations at low levels (Riechert & Lockley, 1984; Riechert, 1992). Some selectivity also occurs because of such factors as location in the microhabitat, size limitations of the prey, characteristics of the web, foraging behavior, and palatability of the prey. The impact of generalist arthropod predators was demonstrated by preserving or removing spiders in an experimental vegetable garden; by mulching and/or providing flowering plants, the spider assemblages were increased and insect damage was reduced (Riechert & Bishop, 1990). In this study where spiders were removed from manipulated plots, insect damage increased, proving that spider predation was the critical cause.

Class A r a c h n i d a

Subclass Araneae Of the 87 families that belong to Araneae, 10 contain species that have been involved in biological control studies, but thus far there is no evidence that spiders as individual species can achieve regulation of a pest insect or mite population. Spiders are considered to have a stabilizing influence on species. Although spiders are ubiquitous, are entirely carnivorous, and prey predominantly on insects, their effect on pest populations is poorly known. This probably can be attributed to several factors, including the secretive habits of many species, the difficulty of evaluating the impact of generalist predators on a given pest species, and the general lack of knowledge of and/or interest in spiders. Moreover, spiders possess few of the biological traits usually considered important for natural-enemy effectiveness (Riechert & Lockley, 1984). They have long life cycles relative to those of insect or mite pests (usually 1 year or one season), thus they cannot exert a within-season numerical response to increasing pest densities. Spiders do not have distinct preferences for a given prey species, and switching to a more abundant food source seems to be a rare occurrence (Riechert & Lockley, 1984). Also, most spiders exhibit territorial behavior; therefore, a marked density-dependent response through immigration is unlikely.

Families of Spiders Having Potential Importance in Biological Control Although there have been numerous surveys of the spider faunas in different agricultural habitats and laboratory studies to determine feeding by spiders on various pest species, there have been relatively few attempts to evaluate the impact of spiders on pest populations [see reviews by Riechert and Lockley (1984), Nyffeler and Benz (1987), and Young & Edwards (1990)]. A complete listing of references is not attempted here.

Therididae and Linyphiidae The Therididae and Linyphiidae are two families of web builders (scattered, irregular strands and sheet webs, respectively) prevalent in many agroecosystems, such as field crops. Although various species have been observed to feed on insect pest species, there are few data available concerning their impact on pest populations. A Theridion species represented 63% of the spider population on avocado foliage in Israel (Mansour et al., 1985). Branches from which spiders were removed showed damage from feeding of geometrid larvae, while no damage occurred on branches on which spiders were undisturbed. Prey consumption by a linyphiid, Lepthyphantes tenuis (Blackwall), followed a type II functional response, increasing as the density of wheat aphids rose and then leveling

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out, but the numbers of aphids killed and not eaten had a simple linear correlation with prey density (Mansour & Heimbach, 1993).

Micryphantidae The Micryphantidae are mainly small spiders (rarely more than 2 mm) that could easily be overlooked as potential natural enemies. Life table studies indicated that micryphantids were an important mortality factor in the life cycle of Spodoptera litura (Fabricius) by preying on the newly hatched larvae and disturbing the larval colonization of taro leaves (Yamanaka et al., 1973; Nakasuji et al., 1973). Micryphantids were also observed on avocado leaves, feeding on spider mite Oligonychus punicae (Hirst) (McMurtry & Johnson, 1966). Erigone atra (Blackwall) demonstrated similar responses to grain aphid densities as the linyphiid L. tenuis (Mansour & Heimbach, 1993). Araneidae and Tetragnathidae Orb weavers in the families Araneidae and Tetragnathidae are also frequently mentioned as comprising a large proportion of the spider faunas in some ecosystems. Their abundance and estimated predation pressure on insect populations in grassland ecosystems was pointed out by Nyffeler and Benz (1987). Orb weavers are the dominant group in some crops, such as cotton and soybeans, in the United States (Whitcomb & Bell, 1964; LeSar & Unzicker, 1978; Nyffeler et al., 1989; Young & Edwards, 1990). In general, these spiders are limited to drifting, flying, or hopping prey ensnared in the webs. There is no conclusive evidence that they are significant.biological control agents on crops, but experimental studies are lacking. Clubionidae There is some evidence that the Clubionidae are significant predators of lepidopteran pests under some conditions. This family consists of hunting spiders that are primarily nocturnal and commonly construct silken tubes for retreats. Bishop and Blood (1981) showed direct numerical relationships between clubiionid, Chiracanthium diversum Koch and oxyopid Oxyopes mundulus Koch with larval populations of Heliothis on cotton in Australia. The former species was considered more important because of its numerical dominance, its densities sometimes being nearly as high as Heliothis spp. Although these spiders were considered incapable of controlling the pests by themselves, their role as part of the predator complex was considered important, as was their apparent ability to regulate small numbers of the larvae present between peaks in Heliothis activity. Chiracanthium mildei Koch was the dominant species of spider on apple trees in Israel in an experiment in which spiders were removed from three to six apple trees and egg masses of S. littoralis (Boisduval) were added (Mansour et al., 1980a). Spodoptera littoralis larvae and leaf damage were observed 5 days later on the trees from

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which spiders were removed, while on the control trees no live larvae or damaged leaves were observed. In addition to causing direct mortality, these spiders also were observed to interfere with the colonization and aggregation behavior of the larvae (Mansour et al., 1981). Chiracanthium mildei also showed a functional response to increasing densities of 4-day-old Spodoptera larvae (Mansour et al., 1980b). The response by individual spiders starved 4 days leveled off at about 180 larvae consumed in an 18-h. period at prey densities of 250 and 300 larvae per cage. It has been pointed out that spiders may consume considerably more prey in the laboratory than would be available in the field (Nyffeler & Benz, 1987).

Lycosidae The Lycosidae, or wolf spiders, are primarily ground-inhabiting hunters that will also forage on lowgrowing vegetation. Coates (1974) considered Pardosa crassipalpus (Purcell) to be one of the most important natural enemies of mite Tetranychus cinnabarinus (Boisduval) on strawberries in South Africa. Because of its nocturnal habits, it previously had gone unnoticed. An intensive quantitative evaluation of spider predation was conducted in rice fields in Japan by Kiritani et al. (1972). A team of observers recorded all predation events by spiders twice weekly at different times of the day and formulae were derived to estimate the total predation per day of the prevalent spiders on the green rice leafhopper, Nephotedtex cincticeps Uhler, and the brown rice plant hopper, Nilaparvata lugens (St~l), as well as on other spiders and miscellaneous prey. It was estimated that the two hopper species comprised at least 80% of the diet of Lycosa pseudoannulata Boes et Str. The percentage of each of the two species of prey in the spider's diet varied according to their relative abundance in a given season. An orb weaver in the Tetragnathidae and a micryphantid also utilized the same prey (up to 50% of their diet). Further quantitative studies on L. pseudoannulata indicated that this predator is important in reducing the density of the green rice leafhopper. Lycosa has two and a partial third generations and its population growth fits a logistic curve (Kiritani & Kakiya, 1975). Lycosa spp. were considered second in importance to ants in predation on the cattle tick Boophilus microplus (Can.) in Queensland, Australia (Wilkinson, 1970). An estimated 50% of the engorged females were killed by these two groups of predators. More nocturnally active lycosid species survive pesticide treatments compared with dielactive species that are exposed in cotton fields during applications (Hayes & Lockley, 1990). Oxyopidae The Oxyopidae is another family of hunting spiders common on low-growing plants. Oxyopus species occur worldwide in agroecosystems (Young & Lockley, 1985; Young & Edwards, 1990). Oxyopus salticus Hentz can either search actively or assume an ambush be-

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havior (Young & Lockley, 1986). These workers found that predation success on Lygus lineolaris (Palisot de Beauvois) was inversely related to prey size. They suggested that early-season Lygus nymphs of any size may suffer high levels of predation by the large immature and adult spiders present during that time, while mainly small nymphs would be preyed on by the predominantly small immature spiders present later in the season. Studies by Nyffeler et al. (1987b) demonstrated that O. salticus is a generalist predator. Its diet in a Texas cotton field included Solenopsis invicta Buren (red imported fire ant) (22%), leafhoppers (17.2%), dipterans (15.6%), aphids (14%), and spiders (14%). Predaceous arthropods, including fire ants, made up 42% of the spider's diet. The major cotton pests (boll weevils, cotton fleahopper, and Heliothis spp.) were not numerous. Oxyopus salticus killed an estimated 4.5% of the arthropods present per week. Although the green lynx spider, Peucetia viridens (Hentz), fed on some of the major cotton pests, over 50% of its diet consisted of beneficial arthropods (Nyffeler et al., 1987a). In an experimental plot in which 45,000 O. sertatus Koch were released, the population density of cecidomyiid Contarina inouyei Mani was reduced to ca. 25% of the level of the control plot in a cryptomeria forest in Japan (Kayashima, 1961).

Salticidae Species in the Salticidae (jumping spiders) are common in agroecosystems and prey on various pests (Riechert & Lockley, 1984; Young & Edwards, 1990). These spiders generally are diurnal and hunt their prey visually. In greenhouse experiments, Muniappan and Chada (1970) and Homer (1972) showed that Phidippus audex (Hentz) and Metaphidippus galathea (Walck), respectively, suppressed populations of the greenbug on seeding plants. However, because only one prey and one predator species were present in the experimental systems, it is invalid to conclude these predators are important under field conditions. Functional responses of Marpissa tigrina Tikader suggested that this species is a highly efficient predator of a psyllid on citrus in India (Sanda, 1991), but 18 species of spiders, mainly salticids, preying on citrus psyllids in South Africa did not appear to directly influence the populations of the psylla to any great extent (Van den Berg et al., 1992). Thomisidae The Thomisidae (crab spiders) frequently are mentioned as potentially important predators of crop pests (Riechert & Lockley, 1984; Young & Edwards, 1990), but no quantitative studies on predator-prey interactions have been conducted. Putman and Herne (1966), using chromatographic methods, found that spiders, the most abundant of which was Pliodromus praelustrus Keyserling, showed a functional response to increasing densities of spider mites [Panonychus ulmi (Koch) and Bryobia

rubrioculus (Scheuten) (= arboreus)] in a peach orchard. Feeding occurred even at very low densities. They concluded that spiders are part of the complex of minor predators, which aids the major predators in maintaining the density of P. ulmi at low levels. Conclusions There is no evidence that spiders, as individual species, can achieve regulation of a pest insect or mite population. It is more likely that the assemblage of spider species contribute a stabilizing influence on pest species (Riechert & Lockley, 1984; Riechert & Bishop, 1990). Therefore, laboratory or greenhouse experiments investigating the effect of single species of spiders on single species of pests are of questionable relevance to the field situation. A potential adverse effect of spiders on biological control is that of destruction of more effective specific parasitoids and predators or of competition with these natural enemies for prey (Whitcomb & Bell, 1964; Nyffeler et al., 1987a, 1987b). On the other hand, spiders could have a buffering effect on large population fluctuations by stabilizing numbers of the specific enemy, thereby preventing local annihilation of both the pest and the enemy. Although there is a paucity of information on the importance of spiders in biological control, the evidence is sufficiently encouraging to warrant further study and to attempt to preserve them in the ecosystem.

Subclass Acari Order Parasitiformes In the subclass Acari, there are 331 known families of which at least 20 include predaceous species, but only 4 families in the suborder Mesostigmata and 7 in the suborder Prostigmata are discussed here.

Suborder Mesostigmata (= Gamasida) Phytoseiidae The Phytoseiidae, containing over 1000 described species, are essentially ubiquitous inhabitants on higher plants, including both annual and perennial agroecosystems. The importance of phytoseiids in the biological control of phytophagous mites has been shown in various situations (e.g., McMurtry, 1982; McMurtry & Croft, 1997). Life Histories Phytoseiids go through developmental stages typical of most gamasid mites, (i.e., egg, hexapod larva, octapod protonymph and deutonymph, and adult). Generation times generally require 6 to 10 days at warm temperatures (usually less than that of their prey, such as tetranychid mites and thrips) (McMurtry et al., 1970; Sabelis, 1985). Development can be continuous in warm climates, while in temperate climates species overwinter as

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inseminated adult females. A reproductive diapause, regulated by photoperiod and influenced also by temperature, has been found in some species. Except for a few known thelytokous species, phytoseiid females must mate to reproduce. Mating usually occurs as soon as the female molts to the adult stage. The male is attracted at close range by a female sex pheromone (Rock et al., 1976; Hoy & Smilanick, 1979). Many species require multiple matings to produce their full complement of eggs. However, a single mating is sufficient for some species, especially among those that have a high reproductive potential and strongly female-biased sex ratio (Bounfour & McMurtry, 1987). In the species investigated, all the eggs are fertilized; however, during embryo development, some eggs lose the paternal set of chromosomes, with the haploid eggs presumably developing into males and the diploid eggs presumably developing into females. This phenomenon has been termed parahaploidy (Hoy, 1979) or pseudoarrhenotoky (Schulten, 1985). Fecundity of Phytoseiulus and some Neoseiulus species average over 60 eggs per female, with a rate of up to 4 eggs per day at the peak in the oviposition period (McMurtry & Rodriguez, 1987). In general, those species having a high fecundity rate have a rapid developmental period as well, resulting in a high intrinsic rate of increase (rm) (Sabelis, 1985). Such species (e.g., P. persimilis AthiasHenriot) are usually specialized predators closely associated with Tetranychus species developing in patchily distributed colonies with dense webbing. These predators have been most widely used in applied biological control of spider mites. However, many species have lower rates of reproduction (1 to 2 eggs per day) and development, with consequently lower intrinsic rates of increase (Tanigoshi, 1982). Such species tend to be more general feeders that utilize foods such as pollen, small insects, and eriophyid mites as well as tetranychid mites. Thus, these phytoseiids seem to be "k-selected" species.

Predator Attributes Although phytoseiids are best known as predators of spider mites (which certainly reflects their prime importance in applied biological control), relatively few species are dependent on this kind of prey for food; and the majority of species are probably general feeders that subsist on a variety of foods, including pollen (McMurtry & Rodriguez, 1987; McMurtry & Croft, 1997). Therefore, species present in a given ecosystem should be investigated for their potential as predators of other pests in addition to spider mites. For example, certain phytoseiids have been found to be important natural enemies of thrips, including Euseius tularensis Congdon on Scirtothrips citri (Moulton) (Tanigoshi et al., 1985) and E. addoensis on S. aurantii Faure (Grout & Richards 1992), respectively, and N. barkeri (Hughes) on Thrips tabaci Lindeman (Ramakers, 1980). Phytoseiids have also been recorded attacking other

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groups of phytophagous mites. There is one documented case of control of a tarsonemid mite (cyclamen mite on strawberries in California) (Huffaker & Kennett, 1956). Several species of phytoseiids were able to develop and reproduce on the tarsonemid Polyphagotarsonemus latus (Banks) (McMurtry et al., 1984). Control of eriophid mites has not been demonstrated, but these mites can be an important alternate food for phytoseiids, which may result in stabilizing spider mite populations at lower levels than would occur without this source of food (Hoyt, 1969). Specialized feeding on tetranychid mites has evolved, apparently independently, in several unrelated groups of phytoseiids, including Phytoseiulus, Neoseiulus, Galendromus (= occidentalis group of Typhlodromus) (McMurtry, 1982; McMurtry & Croft, 1997). Species in these three groups are usually associated with Tetranychus species that form colonies with dense webbing. The long mediodorsal setae possessed by these phytoseiids may facilitate their movement through the webbing, which may entangle species in other genera (Sabelis & Bakker, 1992). It has been demonstrated that some of these species show attraction or arrestment responses to kairomones present on mites, webbing, or feces of certain species of spider mites (Sabelis & Dicke, 1985). The predators Phytoseiulus persimilis, Galendromus occidentalis (Nesbitt), and Amblyseius potentillae (Garman) showed a strong positive response to kairomones from a preferred prey species, but showed little or no response to a species in a different genus of spider mite with which it is not associated under field conditions. However, P. persimilis responded to kairomones of both a favorable prey species, T. urticae Koch, and an unfavorable one, T. evansi Baker & Pritchard (de Moraes & McMurtry, 1985). The capacity for attacking and feeding on tetranychid prey varies with the phytoseiid species and is determined, at least in part, by the size and reproductive capacity of the predator. Phytoseiulus persimilis, a relatively large and highly fecund species, consumes 10 to 12 spider mite eggs during nymphal development and 14 to 22 eggs per day per ovipositing female (Takafuji & Chant, 1976; Sabelis, 1981). Ovipositing females of P. longipes Evans, given single stages of T. pacificus McGregor, fed on 31 eggs, 30 larvae, 23 protonymphs, 15 deutonymphs, or 4 adult female prey per day (Badii, 1981). These rates are lower in smaller species, such as G. occidentalis (Laing, 1968; Sabelis, 1981). The prey consumption capacity for phytoseiids is thus much lower than for the common insect predators of spider mites, such as Stethorus or Scolothrips species. An advantage to this characteristic is that phytoseiids can develop and reproduce at low prey densities compared with the larger predators. This, along with a short generation time, can result in a numerical response to prey increase with a shorter lag time even when the pest mite numbers are still relatively low.

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Some Genera and Species Groups and Their Possible Importance Phytoseiulus is a small genus in which all known species are specialized predators of spider mites (mainly Tetranychus species) that develop in dense colonies with much webbing. Phytoseiulus persimilis has a lower oviposition rate on other genera of spider mites, such as Panonychus or Oligonychus (Ashihara et al., 1978), while Phytoseiulus longipes showed no reproduction on Panonychus citri (McGregor) and only a low rate on Oligonychus punicae (Badii & McMurtry, 1984). Phytoseiulus persimilis has been studied and used in biological control programs more than any other phytoseiid. Its use has been mainly for mite control in greenhouses and to some extent on strawberries outdoors (McMurtry, 1982; McMurtry & Croft, 1997). Galendromus is a genus whose species show a close association with tetranychid mites. Galendromus occidentalis is the major predator of various Tetranychus species on deciduous tree crops and grapes in western North America, and G. helveolus Chant (= floridanus) appears to be an important predator of Eotetranychus sexmaculatus (Riley) in Florida (McMurtry, 1982). The species studied do not show a close association with spider mites having less patchy distributions and producing relatively little webbing. For example, G. occidentalis does not appear effective in controlling Panonychus ulmi (Hoyt, 1969) and other species in this category. Moreover, it does not respond to chemical cues from that mite as it does to cues from Tetranychus species (Hoy & Smilanick, 1981; Sabelis & van de Baan, 1983). Unlike the Phytoseiulus species, those in the G. occidentalis group that have been studied can subsist and even increase on other types of prey, such as eriophyid and tydeid mites. Typhlodromus includes the widely distributed T. pyri Scheuten, common on deciduous fruit crops, and also some species on subtropical crops (such as T. athiasae Porath & Swirski, T. phialatus Athias-Henriot, and T. exhilaratus Ragusa). These species are more general in their food habits, because they have been reported to reproduce on pollen, on eriophyid and tenuipalpid mites, and on tetranychids (Chant, 1959; Swirski et al., 1967b). Field studies in several countries indicate that T. pyri can be important in maintaining Panonychus ulmi and sometimes Tetranychus uricae at low densities, although it may not be capable of keeping pace with high densities of this mite (McMurtry, 1982; Nyrop, 1988; Croft et al., 1992). Neoseiulus (sensu Muma et al., 1970) is a genus that contains various potentially valuable predators of tetranychid mites, including N. fallacis (Garman), N. californicus (McGregor), N. chilenensis (Dosse), N. bibens (Blommers), and N. longispinosus (Evans) (McMurtry, 1982; McMurtry & Croft, 1997). These mites usually are found in close association with Tetranychus species and all have a high reproductive capacity when feeding on Tetranychus (Ma &

Laing, 1973; Blommers, 1976; Ball, 1980). Neoseiulusfallacis has an impact on P. ulmi as well as Tetranychus species on deciduous fruit trees (Croft & McGroarty, 1973). Other species of Neoseiulus are more generalized in their food habits, feeding on other small arthropods as well as pollen. Neoseiulus barkeri and N. cucumeris are used for thrips control on greenhouse-grown vegetables. Because they subsist on a variety of foods, they are sometimes released even before the pest thrips are detected (van Rijn & Sabelis, 1990). Amblyseius sensu stricto is a large genus that is well represented in more humid regions and seems to consist largely of species that utilize a variety of food types. Amblyseius potentillae, which has the potential of controlling P. ulmi on deciduous fruit trees in Italy [where it is referred to as A. andersoni (Chant) and in the Netherlands as A. eharai Amitai & Swirski], and A. herbicolus (Chant) (= deleoni Muma & Denmark) are considered potentially effective predators of P. citri in Japan and Australia (Tanaka & Kashio, 1977; Beattie, 1978). Swirski et al. (1967a) showed that A. swirskii Athias could utilize many types of mites and insects found on citrus trees in Israel. Euseius is a common genus in tropical and subtropical regions of the world. All species that have been studied reproduce readily on pollen and in some cases pollen seems to be a more favorable food than animal prey (McMurtry & Rodriguez, 1987). Euseius species frequently are the most abundant phytoseiids on citrus and other subtropical tree crops. Although seasonal population peaks sometimes are correlated with the abundance of pollen from the host tree or other nearby sources, studies have indicated that various species have some impact on Panonychus species (either citrus red mite or European red mite) in such countries as the Netherlands, South Africa, Australia, Chile, and the United States (McMurtry, 1982; McMurtry & Croft, 1997). Their potential as predators of thrips and other small insects also deserves further investigation. The importance of such "generalist" phytoseiids seems to be in stabilizing pest populations at low densities rather than in suppression of populations that have increased to higher numbers (McMurtry, 1992). Ascidae This is a large and diverse family, common in such habitats as soil, humus, litter, foliage, bark, flowers, and nests of vertebrates. The food habits of most species are unknown; most are thought to be predaceous on such groups as nematodes and small arthropods but some may be pollen or fungus feeders (Lindquist & Evans, 1965). Species in the genus Blattisocius have some potential for biological control of certain pest insects in stored products. Blattisocius tarsalis (Berlese) is a cosmopolitan species that preys on eggs of many insect species, especially Lepidoptera in stored grains and in laboratory cultures (Darst & King, 1969; Haines, 1981). This species has a short, non-

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Terrestrial Arthropod Predators of Insect and Mite Pests

feeding larval stage ( + 24 h) and predaceous protonymphal and deutonymphal stages that consume a mean of 3.7 eggs of Ephestia cautella (Walker). The generation time (egg-egg) is as short as 7 days at 27~ Adult female mites consumed ca. 2.6 Ephestia eggs per day and laid 1.6 eggs per day with a mean total of 26 eggs per female. The intrinsic rate of increase was high in relation to that of the moth. The developmental and oviposition rates were much lower on Tribolium eggs (Haines, 1981). Adult female mites are phoretic on moths. The preferred location for attachment on Plodia interpunctella (Htibner) is at the base of the wings or on the dorsum of the abdomen, where up to 14 mites per moth have been observed (Darst & King, 1969). Experimental studies by Flanders and Badgley (1960, 1963) and White and Huffaker (1969) showed that B. tarsalis was the major factor contributing to regulation of Anagasta kuehniella (Zeller) in laboratory ecosystems. Graham (1970) and Haines (1981) concluded that this mite can exert effective control of E. cautella in the absence of insecticides, and that they can utilize eggs of Tribolium as an altemate food source. Laelapidae This is a diverse family of mites ranging from generalist predator species to facultative parasites to obligate parasites on warm-blooded animals. They are found commonly in such habitats as manure, litter and soil, stored grain, and nests of various vertebrates and insects (Krantz, 1978). Evidence that laelapid mites may have a suppressive effect on pest insect populations was given by Chaing (1970). Corn plots in Minnesota that received manure applications showed higher populations of predaceous mites and lower populations of the corn rootworm, Diabrotica longicornis (Say), than did nonmanured plots. Laboratory observations confirmed that a Androlaelaps sp. and a Stratiolaelaps sp. fed on eggs and larvae of com rootworm. Chaing concluded that the predaceous mites accounted for a 19.7% control of rootworms under natural conditions and a 63.0% control, in the manured plots. Some Hypoaspis species are associated with phytophagous dynastine scarab beetles and are known to feed on beetle eggs. Some Hypoaspis mites, considered important mortality factors of Oryctes beetles, were introduced to Tokelau Island for attempted biological control of O. rhinoceros Linnaeus, a serious pest of coconuts (Swan, 1974). Macroehelidae Mites of this family are common inhabitants of humus, litter, or other habitats at or near the ground level. A few occur in such places as nests of birds, mammals, bees, ants, or even on the fur of animals (Krantz, 1978). Macrocheles is the largest genus (over 700 species) and the one containing species of potential value in biological control of noxious flies. Most Macrocheles species have phoretic adult females, commonly on muscoid flies or scarabeiid dung beetles (Krantz, 1978). These species prey

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on the eggs and small larvae of muscoid flies, and may have preferences for certain species. For example, M. muscaedomesticae (Scopoli) prefers housefly eggs to those of Stomoxys calcitrans (Linnaeus) or Fannia canicularis (Linnaeus) (Kinn, 1966; Singh et al., 1966); it also feeds on nematodes (Rodriguez et al., 1962). Both mated or unmated females are phoretic, and arrhenotoky apparently is the general mode of reproduction. Therefore, all mature females carried to a new dung habitat by a scarabeiid beetle or fly can begin laying eggs immediately after arrival (Axtell 1969). Most Macrocheles studied have a high reproductive potential, with the ability to complete a generation in as short a time as 4 days, or about 3 generations to 1 of the fly. Some species produce over 150 progeny in 10 to 12 days. Six of seven species treated had a higher intrinsic rate of increase (Rm) than that of Musca domestica (Linnaeus) at several temperatures (over 0.9 R m in some instances) (Cicolani, 1979). Evidence by Jalil and Rodriguez (1970) suggests that Macrocheles muscaedomesticae responds to chemical cues from the fly eggs as prey and from the adult flies as carriers. Various studies have shown that M. muscaedomesticae can reduce fly populations by 60 to 90%. Krantz (1983) reviewed this work and listed some limiting factors in the successful use of these mites in biological control of flies in poultry or dairy farms, and suggested some points on which further study is needed. It was pointed out that certain Macrocheles species not occurring in domestic habitats might be more effective than M. muscaedomesticae. Macrocheles species also have been investigated for control of flies that breed in dung pads in pastures and rangelands. Because of the ephemeral nature and wide scattering of dung pads in these situations, it is not surprising that the macrochelid mites in such habitats have evolved close phoretic relationships with insects, primarily scarabeiid dung beetles. More than 180 known species of Macrocheles are associated with dung beetles, which are themselves major competitors with flies for dung as a food resource (Krantz, 1983). Extensive studies have been conducted in Australia on the biological control potential of Macrocheles species on bush fly Musca vetustissima Walker. Experiments with the indigenous Macrocheles glaber showed that bush fly breeding could be controlled by as few as 50 mites in a 1000-ml dung pad. The mites are phoretic on several species of native dung beetles, but they must arrive at the dung pad soon after the flies have laid their eggs. If the eggs escape predation, the larvae are able to escape by burrowing into the wet dung. Thus, the daily flight activity of the beetles plays an important role (Wallace et al., 1979). Macrocheles peregrinus Krantz was introduced from Africa and released in northern Australia, where indigenous species of the M. glaber group do not occur. The high reproductive potential of this species (life cycle of 3 days

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at 27~ was considered a factor in its rapid establishment, and the fact that it is phoretic on many dung beetle species, including some introduced from Africa to effect fly control, was thought to be important in its rapid and extensive dispersal (Wallace & Holm, 1983). By early 1985 (less than 5 years after its introduction), it had spread to within 50 km of the northern range of the M. glaber-perglaber complex (Halliday & Holm, 1985). Krantz' (1983)review of the biological control potential of macrochelids against flies in pastoral settings points out some of the aspects on which more information is needed, including systematics, feeding habits, prey preferences, relationships with the beetle carders (specificity, time of flight, etc.), and interactions with other mites.

Uropodidae These mites are common inhabitants in such ecosystems as litter, detritus, rotting wood, stored products, and manure. They are phoretic in the deutonymphal stage, commonly on insects, to which they attach by means of an anal pedicel. The feeding habits of most species are unknown, but the family apparently includes feeders on such things as fungi, organic detritus, nematodes, and insect eggs and larvae (Krantz, 1978). Fuscuropoda vegetans (DeGeer) has been studied as a potential biological control agent of muscoid flies in poultry facilities. This species has a relatively long life cycle (24 days plus 7 to 11 days preoviposition) compared with macrochelid mites but its oviposition rate was lower on housefly eggs than on nematodes (4 versus 7 eggs per day) (Jalil & Rodriguez, 1970). Control of housefly populations was demonstrated experimentally (O'Donnell & Axtell, 1965; Rodriguez et al., 1970). The latter authors suggested that F. vegetans complemented Macrocheles in biological control of fly populations, because the uropodids prefer larvae and the macrochelids prefer eggs.

Order Acariformes

Suborder Prostigmata (= Actinedida) Tydeidae These mites are common foliage-inhabiting species on a wide variety of crops. They develop through the egg and three nymphal stages to the adult in as short a time as 9 days at 30~ Homepronematus anconai (Baker) has a fecundity of over 40 eggs per female and a fairly high intrinsic rate of increase (0.278 at 30~ (Knop & Hoy, 1983). There are conflicting opinions on whether foliageinhabiting tydeids are predaceous, phytophagous, pollenophagous, or saprophagous. Various species probably can be placed in any of these categories. The literature on feeding habits of Tydeidae has been reviewed by Hessein and Perring (1986). These authors also conducted a study demonstrating the impact of tydeid predation on a pest population. On both individual tomato leaflets and tomato seedlings, H. anconai prevented the tomato russet mite, Aculops lycopercicae (Massee), from reaching damaging numbers. The ty-

deid also fed and reproduced on pollen alone (Knop & Hoy, 1983; Hessein & Perring, 1986).

Bdellidae Bdellids are medium- to large-sized mites (up to 4 mm) commonly occurring on low-growing vegetation, in soil or humus, and, in some cases, on trees or under bark. Prey include such small arthropods as Collembola, aphids, larvae of Diptera, and mites in the Tetranychidae and Penthaleidae (Alberti, 1973; Krantz, 1978). The prey is captured with the aid of silken threads, which also serve to anchor it to the substrate while the predator sucks out the body fluids (Alberti, 1973). Some species of bdellids are active only during the cool season and estivate in the egg stage during the summer, their phenology being synchronized with such pests as Collembola and mites of the family Penthaleidae and the genus Bryobia (Tetranychidae) (Snetsinger, 1956; Wallace, 1967; Soliman & Mohamed, 1972). Neomolgus aegyptiacus Soliman consumed ca. 70 Collembola during the larval and three nymphal stages over a 22-day developmental period at 17 to 19~ (Soliman & Mohamad, 1972). This species was always observed in association with Collembola. Bdellids were demonstrated to be important biological control agents of the collembolan Sminthurus viridis Linnaeus (lucerne flea), a pest of alfalfa in Australia. Studies by Wallace (1967) indicated that no outbreaks of S. viridis occurred when numbers of Bdellodes lapidaria Kramer exceeded 20 per square meters. A classical biological control program involved the introduction of N. capillatus (Kramer) from the Mediterranean area and its establishment in more arid parts of Australia where B. lapidaria did not occur (Wallace, 1974; Ireson & Webb, 1995). Anystidae The "whirligig" mites have been observed feeding on such prey as aphids, thrips, leafhoppers, scale crawlers, and spider mites. They have been evaluated as biological control agents of collembolans and penthaleid mites (Michael, 1995). Cheyletidae Cheyletids are predators that assume an "ambush" mode characterized by lack of motion, extended legs, and palpi abducted at a wide angle. The prey is grasped with the palpi and paralyzed within a few seconds (Wharton & Arlian, 1972). Various species occur in orchards, where they prey on such arthropods as scale crawlers and different mite species, including tetranychids and phytoseiids. They are considered to be of little importance in spider mite control because of low reproductive potential and prey consumption capacity (Laing & Knop, 1983). They also have been observed to feed on mites in the Tenuipalpidae (Haramoto, 1969) and Eriophyidae (Sternlicht, 1970), but no information is available on whether they have a significant impact on populations of these families of mites.

Chapter 16

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Some cheyletids prey on scale insects, usually by hiding under an empty scale or in other protected places on leaves or twigs, where they attack wandering crawlers (Gerson et al., 1990). Chetotogenes ornatus (Canestrini & Fanzago) was reported to be the dominant acarine predator of chaff scale, Parlatoria pergandii Comstock, on the bark of citrus trees in Israel (Avidov et al., 1968). It showed a densitydependent response to scale populations and peaked in late summer at the "critical, ebb period of the chaff scale's populations." It was considered "an enemy of some importance" on the chaff scale, but laboratory studies showed a relatively slow development rate, low fecundity, and only two generations per year. On the other hand, there is evidence that cheyletids have potential for controlling acarid grain mites in stored grains. Cheyletus eruditus (Schrank) is often found in stored grains in sufficient numbers to suggest that it is an important predator (Norris, 1958; Solomon, 1969; Jeffrey, 1976; Bruce, 1983). The potential for manipulating C. eruditus for biological control of acarid mites was demonstrated by Pulp~in and Verner (1965) in Czechoslovakia. They found that if the predator is present before the beginning of July and the infestation rate has not exceeded 1000 mites per 500 g of grain, spontaneous control can occur if there is one predator to 75 to 100 pest mites. They also showed possibilities of transferring predators from granaries where they are abundant to those where they are scarce, and they described a method whereby up to 25,000 mites could be collected in 1 h. Zdarkova (1986) reports additional work on production and utilization of C. eruditus for control of stored product mites in Czechoslovakia. Although C. eruditus does not have a rapid rate of development or a high prey consumption capacity (Beer & Dailey, 1956; Solomon, 1969), fecundity is fairly high (up to 130 eggs per female) and all progeny are usually female (Summers & Witt, 1972; Hughes, 1976). It also has the ability to survive and find prey at very low prey densities. However, as the predator density increases and the prey density decreases, cannibalism becomes a major factor (Solomon, 1969; Burnett, 1977).

Stigmaeidae Species in the genera Zetzellia and Agistemus have been studied as potential predators of phytophagous mites and insects on crop plants. These mites are similar in size to, or slightly smaller than, tetranychid mites and develop through egg, larval, protonymph, and deutonymph stages to the adult. Zetzellia mali (Ewing) is common in deciduous orchards in North America. It occurs most frequently along the midrib on the undersides of the leaves and feeds on all stages of spider mites, eriophyid rust mites, and eggs of small insects, as well as on pollen. Zetzellia mali's rate of development and reproductive potential are lower than those of most phytoseiid mites, and thus the species is classed as a "k-selected" instead of an

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"r-selected" predator. Therefore, its value in biological control is questionable (Laing & Knop, 1983; Santos & Laing, 1985). Agistemus species have similar biologies and general feeding habits as Zetzellia species, and they sometimes reach high population densities on foliage. Collyer (1964) observed A. longisetus Gonzalez in numbers as high as 100 per leaf in some orchards and considered it a potentially valuable predator of tetranychid mites in the genera Panonychus, as well as of eriophyid and tenuipalpid mites. Collyer reported higher rates of fecundity and development than have been observed for most stigmaeids. Laing and Knop (1983) and Santos and Laing (1985) reviewed the food sources, host plant, and geographic ranges, as well as potential value of Stigmaeidae in biological control. On the basis of laboratory and field studies, Oomen (1982) considered Agistemus species to" be the most effective predators of the tenuipalpid mite, Brevipalpus phoenicus (Geijskes), on tea in Indonesia. Tenuipalpids have a lower reproductive potential than tetranychids, so the stigmaeids could be more effective predators of this family.

Erythraeidae and Trombidiidae The subcohort Parasitengona includes several families of moderate to very large, reddish mites (from 500 to over 10,000 species) that are general predators of small arthropods. Although the efficacy of these mites may be limited by slow developmental rates (1 to 3 generations per year), they could act as stabilizing factors in the ecosystem. The Erythraeidae and Trombidiidae are characterized by active larvae (many are parasitic on insects), quiescent protonymphs, predaceous deutonymphs, quiescent tritonymphs, and predaceous adults. These are largely ground-inhabiting species, although some (such as the erythraeid genus Balaustium) are arboreal, feeding on various soft-bodied insects and mites in orchards. Virtually no quantitative studies have been done on the effects of the predation by these families of mites on pest insect and mite populations. Various associations and potentials for biological control are reviewed by Lindquist (1983), Laing and Knop (1983), Eikwort (1983), and Welbourn (1983).

SUBPHYLUM UNIRAMIA The subphylum Uniramia, which is made up of animals that belong to the classes Myriapoda and Hexapoda, contains the majority of invertebrate predators that have been used in biological control programs. Apparently, there have been no species in the Myriapoda that have been used directly to control pests; thus, the Hexapoda has been the source of most species used in biological control, and these predators have come from the subclass Pterygota (winged insects). The five other orders in Hexapoda, which formerly

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fell under the taxon "Aptera" (wingless insects), thus far have been of little importance to applied biological control. Class H e x a p o d a

Subclass Pterygota Of the 29 orders that make up the subclass Pterygota, 9 orders contain families of terrestrial predators: only the families that comprise species that have been involved in biological control programs are discussed here. In general, as the insect taxa advanced phylogentically, the more specialized their prey spectra became. All foraging strategies of predators, including random searching, hunting, ambush, or trapping, are exploited in the higher pterygote orders. Order Orthoptera

Most families in Orthoptera are composed of phytophagous species, but there are a few among the over 22,000 species that are predaceous. The food habits of Orthoptera can be determined by examining mandibles and feculae, even of dead specimens (Gangwere, 1969). Gryllotalpidae Dissections of the alimentary tract of two freshly killed mole cricket species in the genus Scapteriscus showed that S. acletus Rehn & Hebard was primarily carnivorous while S. vicinus Scudder was herbivorous (Matheny, 1981).

Gryllidae Among its nine subfamilies only the Oecanthinae (tree crickets), Nemobiinae (ground crickets), and Trigonidiinae are considered predaceous enough to offset their feeding on flowers and leaves. Even the common pestiferous field cricket, Gryllus assimilis (Fabricius), can be predaceous; it was recorded by Smith (1959) to have destroyed up to 50% of the egg pods of a grasshopper species in Canada. Ground cricket Pictonemubius ambitiosus (Scudder) was recorded to have eaten radioactive labeled velvet bean caterpillar eggs placed in a Florida soybean field (Buschman et al., 1977). Metioche vittaticollis (St~l), a trigonidiinine found commonly in Asian rice fields, preyed on eggs of five rice pest insect species under cage conditions, but did not feed on rice seedlings; however, it could be reared on shredded carrots (Rubia & Shepard, 1987). Tettigoniidae Species in the Listrosclinae are predaceous (Key, 1970a), and some Conocephalinae appear in biological control literature. The tropical Asian Conocephalus longipennis (Dehaan) consumes eggs of two moth species in Malaysian rice fields and is considered beneficial even though it also feeds on flowers and young grains; it can reach an estimated density of about 20,000 per hectare and it may make an important contribution to pest control

in rice fields during the first half of the growing season (Manley, 1985). In Philippine rice fields, this species destroyed from 17 to 65% of the rice yellow stem borer egg masses (Pantua & Litsinger, 1984). Unspecified tettigoniids were considered to have consumed the largest proportion of medium to large velvet bean caterpillar larvae in Florida soybean field study plots (Godfrey et al., 1989). Two species of predaceous katydids prey on brood in unguarded Polistes wasp nests in Central America (O'Donnell, 1993). Order Mantodea

This is the only hemimetabolous order other than Odonata composed entirely of predaceous species. Both nymphs and adults are generalist predators. The 1800 or so known species are distributed mostly in the tropics and make up 8 families or 1 family, Mantidae, with 34 subfamilies (Brues et al., 1954; Key, 1970b). Most of the praying mantids are cryptically colored to match the background where they sit and wait for prey. Some species appear as lichens on bark; others are vividly colored as the flowers they sit in to ambush visiting floral insects and some species resemble in color and form flowers that appear to attract insects (Wickler, 1968). There have been extensive studies made on mantid prey recognition (Rilling et al., 1959), prey capture (Mittelstaedt, 1957; Roeder, 1963), and response to prey density (Holling, 1966; Mook & Davies, 1966; Hurd et al., 1978; Eisenberg et al., 1981; Matsura & Nakamura, 1981; Hurd & Rathet, 1986; Paradise & Stamp, 1991). The biologies of only a few species have been described. Tenodera sinensis (Saussure) and Mantis religiosa (Linnaeus) are now the most widely distributed temperate species. The temperate species are univoltine and overwinter in the egg stage. The eggs are placed in cases, oothecae, which can contain several hundred eggs each (Eisenberg & Hurd, 1990), but as the adults of T. sinensis age, the size of the egg cases and numbers of nymphs hatching decrease; 200 nymphs hatch from the first case, but only 25 hatch from the sixth (Butler, 1966). Tenodera sinensis deposits its oothecae on dead, uptight plant stems, while the oothecae of M. religiosa, whose adults forage closer to the ground, were found in dense grasses (Eisenberg & Hurd, 1990). Litaneutria minor (Scudder) is a ground dweller but deposits its egg cases on low shrubs (Cannings, 1987). Eggs hatch during the spring in temperate climates, and the nymphs molt 3 to 12 times before attaining the adult stage. The role of mantids as biological control agents is still uncertain even though many U.S. gardeners and organic growers purchase egg cases from eastern suppliers who collect T. sinensis and M. religosa oothecae from fields during winter. In China, oothecae are either collected or reared for release in various agricultural crops. Hurd and Eisenberg (1984) conducted replicated releases of T. sinensis oothecae in a seminatural field community of

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

low vegetation to determine the impact of releases on herbivore biomass (dry weight) and abundance. The results from this experiment and a previous one led Hurd (1985) to conclude there may be some agricultural situations in which some mantids will prove to be effective biocontrol agents, but his information and results from releases in more or less natural communities do not support this notion. A review on the use of mantids in China as biological control agents in certain agricultural crops by Olkowski and Thiers (1990) is somewhat more positive. However, the few articles available in Chinese describing pest suppression in the field by mantids (mainly using Hierudula patellifera Serville and T. sinensis) do not provide enough detail to draw definitive conclusions on the use of mantids in agricultural crops, but under certain conditions there appeared to be suppression of pests such as aphids. Ge (1986) reported many instances of storing and releasing field-collected oothecae, mainly in cotton. He also obtained oothecae for release from mantids reared on artificial diets. The artificial diet used by Ge contained mostly pig liver, aphid powder, sugar, and water mixed with a little yeast and agar. Three mantid species have now been accidentally introduced into North America: T. sinensis from Asia, M. religiosa from Europe, and Iris oratoria (Linnaeus), which was introduced from the Mediterranean area into southern California in the early 1950s (Gurney, 1955); I. oratoria has become quite common in San Joaquin Valley cotton fields.

Order Dermaptera The 1860 or so species of earwigs in the world are divided into seven families that are mainly found in the tropics and subtropics (Steinmann, 1989). In California, only 1 of the 21 species present is considered native to the state (Langston & Powell, 1975). It appears that many species are predaceous, and some of the cosmopolitan omnivorous species that can be pestivorous have been used as biological control agents. Remarkably little is known about the biology of most species in the Dermaptera. Of the few species that have been studied, eggs are deposited in groups either in the soil, under stones, beneath bark of trees, or in sheaths of leaves. The eggs are groomed and protected by the mother. Besides several genera of ectoparasitic earwigs of mammals that practice viviparous reproduction, in Hawaii predaceous species Sphingolabis hawaiiensis (Bormans) removes the thin embryonic membrane at the time the egg emerges (Marucci, 1955). The mother feeds the fully formed first- and second-instar nymphs bits of prey. Apparently, feeding young nymphs by the mother is common among the earwigs that have been studied. There are four to seven instars and with the molting of each instar there is an increase in antennal segments (Brindle, 1987). Earwigs are mainly nocturnal and remain close to the

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soil, though some species are diurnal and move from plant to plant, rarely going to the ground. At least some of the obligatory predatory species use their caudal forceps to capture and hold prey while they feed. Terry (1905) was one of the first to recognize the importance of earwigs as predators of insect pests. He observed three species feeding on leafhoppers and psyllids in Hawaiian sugarcane fields. The few predaceous species that have been recorded occur in four families. Carcinophoridae Three species in this family have been observed to be predaceous during at least part of their life cycle. Euborellia annulipes (Lucas), a cosmopolitan wingless species, is omnivorous but prefers insect food, often feeding almost exclusively on cane leafhoppers. It is noctumal, remaining hidden in leaf sheaths or under fallen trees or stones (Terry, 1905). According to Bharadwaj (1966), it feeds on Cosmopolites sordidus (Germar) in Jamaica and on larvae of Sesamia inferens Walker infesting sugarcane, but also attacks stored vegetables and roots of greenhouse vegetables; it is a possible carrier of endoparasites of fowls, and invades households in the U.S. Gulf states. The west African earwig, Euborellia cincticollis (Gerstaecker), which has been reported from California, has a biology similar to that of E. annulipes. It feeds on aphids and other arthropods as well as plants in the laboratory; in California it feeds on cantaloupes (Knabke & Grigarick, 1971). Anisolabis eteronoma Borelli fed on tephritid larvae in rotting fruit on the soil--the nymphs fed on fruit fly larvae developed faster than those fed on fruit alone (Marucci, 1955). Chelisochidae The black earwig, Chelisoches morio (Fabricius), is an Oriental, Australian, and Afrotropical diurnal species, which was considered to be an important predatory earwig in the agricultural areas of the Hawaiian Islands (Terry, 1905). Eggs are deposited in a heap in the sheaths of large-leaved succulent plants. It is a general predator and has been recorded attacking Brontispa spp. (Coleoptera: Chrysomelidae) mining coconut fronds in Micronesia and New Caledonia (Waterhouse & Norris, 1987). Forficulidae Anechura harmandi (Burr) was the most important and numerous predator of eggs and young larvae of the herbivorous lady beetle Henosepilachna niponica (Lewis) in central Japan (Ohgushi, 1986). Doru taeniatum (Dohrn), a Neotropical species that now occurs in California, Texas, and Florida, was observed eating eggs of the velvet bean caterpillar, Anticarsia gemmatalis Htibner, in Florida soybean fields and became radioactive after having preyed on labeled A. gemmatalis eggs placed in the field (Buschman et al., 1977). This nocturnal earwig is common in Central America, occurring primarily

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on large grasses and feeding on eggs and small larvae of Spodoptera frugiperda (Smith) on corn; it also can reproduce on grass pollens. It spends most of its time on plants and deposits its eggs in leaf sheaths, and is inactive during the Honduran dry season, hiding in leaf sheaths; thus, Jones et al. (1987) suggest that it may not be an important predator of S. frugiperda during this period. Jones et al. (1988) described the biology and produced a life table of D. taeniatum based on laboratory studies. Forficula auricularia Linnaeus, the European earwig, is an omnivore; aphids appear to be a preferred prey (Skuhravy, 1960; Asgari, 1966). It can be reared rather easily (Lamb & Wellington, 1974). Buxton and Madge (1976) and Madge and Buxton (1976) found F. auricularia to be a successful predator of the damson-hop aphid, Phorodon humuli (Shrank), in the laboratory; in the field, Campbell (1978) found the European earwig and two Anthocoris spp. were the most abundant predators when the damson-hop aphid populations declined (damage to the plants by earwigs was rarely seen). From the numbers of earwigs trapped over a 2-month period, it was estimated that the earwigs ate over 50,000 aphids per day. The European earwig eats aphids in various field crops and is an efficient predator of cereal aphids in low aphid population densities (Sunderland & Vickerman, 1980; Sunderland, 1988). Because pear psylla increased when F. auricularia nymphs were adversely affected by codling moth sprays, this indicated that the earwig preyed on the psyllids (Sauphanor et al., 1993). In Washington State, F. auricularia was reared on dog food in the laboratory and then released on prebearing apple trees provided with artificial retreats at a rate of five or six adults per tree (Carroll & Hoyt, 1984). This resulted in a decline in 3 weeks from over 500 Aphis pomi DeGeer per tree to less than 50, compared with over 3000 per tree in trees free of earwigs (Carroll & Hoyt, 1984). However, using similar methods on bearing apple trees infested with A. pomi failed to slow aphid population growth (Carroll et al., 1985). Serological assays of predators feeding on A. pomi in Ontario apple orchards indicated among the several polyphagous arthropods that of a total of 79 F. auricularia collected, 44 were seropositive, which indicated that the earwig is a potentially important predator of A. pomi (Hagley & Allen, 1990). Labiduridae Labidura riparia (Pallas), the striped earwig, is a worldwide species in the tropicalsubtemperate regions. It is a nocturnal generalist predator that is considered an important potential biological control agent because it rarely feeds on plants and has become common in California and in the southern states (Schlinger et al., 1959; Price & Shepard, 1977; Kharboutli & Mack, 1993). It is the most studied predaceous earwig. This species uses its caudal forceps to catch and hold prey while feeding. Eggs are deposited in the ground, are

brooded over, and then are moved by the mother. There are six instars and the species can be reared on a commercial cat food (Shepard et al., 1973). In cultivated areas it is mostly found associated with field crops. In cotton, L. riparia was reported to feed on eggs and larvae of S. litura in Egypt (Bishara, 1934), but actually the prey was S. littoralis according to Ammar and Farrag (1974), who studied the biology and behavior of L. riparia in Egypt. In soybeans, Buschman et al. (1977) believed that L. riparia was responsible for most of the predation of the velvet bean caterpillar eggs and larvae among the 20 different predators that they observed during 1973 in Florida; in 1982, Labidura riparia ate the greatest proportion of these small larvae on the ground, while in 1981 the ant Pheidole morrisi Forel was the major consumer of all the velvet bean caterpillar larvae in Florida soybean plots (Godfrey et al., 1989) and similarly, in 78 Florida citrus groves, Tryon (1986) found that on and in the soil beneath citrus trees ants were the dominant predator in 74 groves and L. riparia was dominant in 4 where the ants were not present; in Brazilian sugarcane fields, the earwig is an important predator of Diatraea saccharalis (Fabricius) eggs and first-instar larvae (Bueno & Berti-Filho, 1987). In Florida, studies at night in corn indicated that there was an unusually low adult male to female ratio of L. riparia on the plants: Waddill (1978) suggested that the odd sex ratio may be explained by the fact that females required more food than males. In the laboratory studies, Waddill (1978) provided Diabrotica balteata LeConte as prey. In Florida cabbage fields, where pupae of Trichoplusia ni (Htibner) were placed on the undersurface of cabbage leaves, L. riparia and sparrows consumed from 4 to 90% of the pupae over a 3-day period (Strandberg, 1981a). Because the earwigs were noctumal and the birds were diumal in their feeding activity, Waddill calculated that the earwigs consumed an overall average of 42% of the placed pupae. Earwigs were active the entire year but fewer were caught during winter months (Strandberg, 198 lb). Labiidae Sphingolabis hawaiiensis occurs from the Philippines to New Guinea, in the New Hebrides, and in the Hawaiian Islands. In Hawaii, this earwig was found by Marucci (1955) to prey on Oriental fruit fly larvae in rotten fruit and in the soil but did not eat fruit fly puparia. The earwig attacks frontally by using its mandibles and caudal forceps. The adults provided their first two instars with fragments of fruit fly larvae that the adults had killed and only partially consumed. The adults kill more prey than they eat.

Order Thysanoptera The families Aeolothripidae and Thripidae in the suborder Terebrantia, and Phlaeothripidae in the suborder Tubulifera, contain species that are predaceous, mainly on small insects (such as thrips, aphid nymphs, scales, or insect eggs)

Chapter 16 TerrestrialArthropod Predators of Insect and Mite Pests and on the eggs and immature stages of mites. A few, such as Franklinothrips species, may be obligate predators, but most appear to be partially or even primarily phytophagous. There are no obvious modifications in the mouthparts or other parts of the body for the predatory mode of life (Lewis, 1973). Palmer et al. (1989) present an excellent introduction to economically important Thysanoptera, outlining the diversity and biology of thrips and giving a key for identification.

Aeolothripidae Thrips in this family are generally fast moving, with slender legs. A small hook on the second tarsus may aid these predators in grasping prey (Lewis, 1973). Predaceous Aeolothrips species have mainly been reported as thrips predators (Lewis, 1973; Ananthakrishnan, 1984). Aeolothrips intermedius Bagnall developed more rapidly on thrips larvae (average: 12 days larva-adult at 24~ than on tetranychid mites (average: 19 days); development was not completed on aleyrodids or psyllids and no feeding occurred on aphids. Adults needed to feed on flowers to attain sexual maturity. (Bournier et al., 1979). This Palearctic species has three or four generations per year in southern France (Bournier et al., 1978). Observations on Franklinothrips species indicate that they are obligate predators, primarily on other thrips, Lewis, 1973; Ananthakrishnan, 1984). Franklinothrips tenuicornis Uzel and F. vespiformis Crawford prey on thrips on various tropical crops in the Western Hemisphere. These species were not considered sufficiently abundant to affect thrips control on cacao in Trinidad or on avocado in California (Callan, 1943; McMurtry, 1961). Aleurodothrips fasciapennes (Franklin) completed development on whiteflies and spider mites, but the highest percentage reached maturity on armored scales. In Florida, significant correlations occurred between numbers of thrips and the purple scale, Lepidosaphes beckii (Neuman) (Selhime et al., 1963). A short life cycle permits the completion of 1.5 to 2 generations for every generation of the purple scale. Both laboratory and field studies suggested that this species is a factor in the biological control of purple scale. The impact of this thrips on purple scale is reviewed by Palmer and Mound (1990). Thripidae Scolothrips species are predators of tetranychid mites and possibly are the most specialized of the predaceous thrips. Scolothrips sexmaculatus (Pergande) is a North American species that is associated mainly with Tetranychus species characterized by dense colonies with extensive webbing. Both larvae and adults of this species showed a tendency to be arrested by spider mite webbing, after which penetration into the silken network of the prey colony occurred. When mite eggs were replaced on clean leaves without webbing, the thrips rarely preyed on them, but continued searching (Gilstrap & Oatman, 1976). These

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workers observed that any stage of T. pacificus could be utilized as prey, although small thrips larvae had some difficulty in capturing large mites. The front tarsi were used to hold and manipulate the prey during feeding. Apparently, mites were not perceived until contact was made. Scolothrips sexmaculatus has a relatively rapid rate of development (under 10 days at 35~ The intrinsic rate of increase is comparable to, or even exceeds, that of some phytoseiid mites associated with Tetranychus mites. For example, values for S. sexmaculatus of 0.26 at 30~ (Coville & Allen, 1977) and 0.304 at 35~ (Gilstrap & Oatman, 1976) compare favorably with those of Galandromus occidentalis (Tanigoshi et al., 1975), an effective predator of spider mites on many crops. Scolothrips species are more voracious than phytoseiid mites, but consume fewer prey than some other specialized insect predators of mites e.g., Stethorus spp. in the Coccinellidae). Larvae of both S. sexmaculatus and S. longicornis Priesner consume 40 to 60 mite eggs during development under various temperature conditions, while ovipositing adults consume 80 to 100 eggs per day at 35~ At the same temperature, the thrips females laid an average of 14 to 16 eggs per day. Scolothrips sexmaculatus had a fecundity of well over 200 eggs per female over a wide range of temperatures (Gilstrap & Oatman, 1976; Gerlach & Sengonca, 1986). Other Scolothrips species known to be associated with tetranychid mites are listed in Lewis (1973), Ananthakrishnan (1984), and Chazeau (1985). Some thrips considered pests and assumed to be strictly phytophagous have been found to be predaceous. Insecticide applications formerly were made to control F. occidentalis (Pergande) on cotton in Califomia. However, various field observations of this thrips feeding on Tetranychus species prompted further investigations. Marcano-Brito (1980) showed that F. occidentalis could complete development on mite eggs alone compared with eggs plus a cotton leaf, with the egg consumption during larval development averaging 182 and 72, respectively. Trichilo and Leigh (1986) demonstrated a functional response to increasing egg densities by both larval and adult thrips, but predation was reduced by spider mite webbing. Pollen and nectar were also utilized as foods. Gonzalez and Wilson (1982) and Pickett et al. (1988) considered F. occidentalis an important member of the beneficial arthropod complex on cotton, for its effect not only as a predator of spider mites but also as a food source for other predators, such as Orius tristicolor White. Other phytophagous species, such as F. tritici (Fitch) and Thrips tabaci, also have been observed to feed on tetranychid mites (Lewis, 1973; Boykin et al., 1984).

Phlaeothripidae Predaceous species in this family utilize various kinds of prey and nonprey foods. They have been investigated mainly concerning their roles as predators of spider mites. Haplothrips faurei Hood, a common spe-

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cies in North American orchards, develops and reproduces on spider mites and on moth eggs and to a lesser extent on pollen and on eriophyid mites. Feeding on the mite Panonychus ulmi was confined mainly to the egg stage, averaging 143 eggs consumed during a developmental period of 8 to 10 days at 24~ (Putman, 1965). Ovipositing females consumed 43.6 eggs per day and laid 3.3 eggs per day. This species was considered most important in reducing the winter egg population of P. ulmi by preying on late summer and autumn populations on peach trees. Chromatograms of thrips collected during this time indicated that nearly 100% had fed on spider mites. In a December sample of twigs, an estimated 76% of the winter eggs of P. ulmi were destroyed by the thrips (Putman, 1965; Putman & Herne, 1966). Haplothrips victoriensis Bagnall is considered a major factor in maintaining Tetranychus urticae at low levels on seed alfalfa in South Australia. If the ratio of thrips to motile mites went below 1:10, such as after an insecticidal treatment, mite populations could increase rapidly (Bailey & Caon, 1986). Larvae completed development on either spider mite eggs or alfalfa flowers (presumably the pollen), with faster development on the latter. Adults survived only a short time without flowers, although they ate mite eggs. Some Haplothrips spp. prey on diaspine scales (Palmer & Mound, 1990). These Haplothrips species seem to be opportunist feeders whose numbers probably are not closely correlated with any single prey species. Some species in this genus are considered crop pests (Ananthakrishnan, 1984). Leptothrips mali (Fitch) is common in North American deciduous fruit orchards. This species attacks eggs and motile forms of spider mites, grasping the prey with its front legs (Parrella et al., 1982). Development on eggs of Panonychus ulmi was completed in 19 days at 29.4~ but required 23 days on pollen. Fecundity of 13 eggs per female in laboratory-reared thrips was lower than for field-collected ones, suggesting that additional nutrition, possibly from apple rust mite, was utilized in the field. Parrella et al. (1982) concluded that this species was not able to maintain mite populations at low levels, but it was a factor, along with the coccinellid Stethorus punctum LeConte, in reducing populations from higher levels. Order Heteroptera

Although the majority of the terrestrial species of the Heteroptera are plant feeders, there are thousands that are predatory. In North America alone, there are 3834 species in 677 genera listed, along with many references to biologies of predaceous species, in a catalog of Heteroptera edited by Henry and Froeschner (1988). A readily usable key to genera was written by Slater and Baranowski (1978), and Yonke (1991) prepared a key to immature true bugs, along with biological notes. A general coverage of biology of all families is found in Miller (1971).

The original feeding habit and habitat of Heteroptera are thought to be phytophagous and terrestrial by Sweet (1979), but Cobben (1978) believes that carnivory was the original feeding strategy and their primitive lifestyle was semiaquatic. Cohen (1990), studying the feeding adaptations of five predaceous species in four different families of Heteroptera, found that the toothed mandibular stylets penetrate, rasp, and cut prey tissues; and the maxillary stylets form salivary and food canals that deliver saliva and remove liquified prey contents from within. From this work, Cohen concluded that the morphological, physiological (protolytic enzymes), and behavioral adaptations permit a concerted predigestion of prey from within and allow the predators to feed efficiently on prey that are equal to, or greater than, them in size. However, even the predaceous species feed on plant tissues or plant secretions (i.e., Chu, 1969; Stoner, 1972; Tamaki & Weeks, 1972a; Naranjo & Stimac, 1987). Anthocoridae, Miridae, and Nabidae oviposit into plant tissue and will oviposit into Parafilm| blocks of water-soaked cellulose sponge; the Parafilm | has to be stretched for anthocorids but not for nabids (Shimizu & Hagen, 1967). Heteropteran predators are active in many agricultural crops: in alfalfa fields (Smith & Hagen, 1956; Rakickas & Watson, 1974; Benedict & Cothran, 1975; Neuenschwander et al., 1975; Guppy, 1986; Braman & Yeargan, 1990; O'Neil, 1992); in apple orchards (Collyer, 1953a, 1953b; Lord, 1971; Fauvel, 1974; Rhcz, 1988; Arnoldi et al., 1991, 1992); in citrus trees (Van den Berg & Bedford, 1988); in cocoa fields (Entwistle, 1972); in cotton fields (Whitcomb &Bell, 1964; van den Bosch & Hagen, 1966; Ridgway et al., 1967; Falcon et al., 1968; van den Bosch et al., 1969; Irwin et al., 1974; Ehler & van den Bosch, 1974; Wilson & Gutierrez, 1980; Gonzalez et al., 1982; Schuster & Calderon, 1986; Gravena & Pazetto, 1987; Gravena & Da Cunha, 1991; Kapadia & Purl, 1991; Snodgrass, 1991); in coffee fields (LePelley, 1968); in corn fields (Davis et al., 1933; Knutson & Gilstrap, 1989); in pears (Herard 1986); in potato fields (Biever & Chauvin, 1992a; Hough-Goldstein & Whalen, 1993); in rice fields (Kenmore, 1980; Yasumatsu et al., 1981; Napompeth, 1982; Chang & Oka, 1984; Manti, 1991); in soybean fields (Dumas et al., 1964; Irwin & Shepard, 1980; McCarty et al., 1980; Richman et al., 1980; Isenhour & Yeargan, 1981, 1982; Buschman et al., 1984; O'Neil & Stimac, 1988; Godfrey et al., 1989); in sugarcane fields (William, 1931; Guagliumi, 1973); in sugar beet fields (Tamaki & Weeks, 1973; & Long, 1978); and in strawberries and vegetables mostly in greenhouses (Gilkeson et al., 1990; Steiner & Tellier, 1990; Villevielle & Millot, 1991; Gillespie & Quiring, 1992; Higgins, 1992; Van de Veire & Degheele, 1993). The general importance of Heteroptera in applied biological control was reviewed by Clausen (1940), Sweetman (1958), and Carayon (1961a). Biological control literature

Chapter 16 TerrestrialArthropod Predators of Insect and Mite Pests mostly deals with Anthocoridae, Berytidae, Lygaeidae, Miridae, Nabidae, Pentatomidae, Phymatidae, and Reduviidae. Anthocoridae About 400 species of minute pirate bugs or flower bugs are distributed in nearly all parts of the world; in North America north of Mexico, there are about 90 species recognized (Kelton, 1978; Henry, 1988). Hodgson and Aveling (1988) presented an excellent review on the biology and ecology of anthocorids; most are generalist predators, but there is some plant feeding by most species while some feed on pollen and a few feed on blood. The predaceous species, after contacting the prey, feed by extending their rostra directly forward and everting the stylets beyond the tips of the labral sheaths; in contrast, the mirids retract their labial segments to expose the stylets when feeding (Anderson, 1962b). Eggs are usually deposited horizontally into plant tissue with only the circular whitish caps (opercula) visible at an oblique angle on the plant surface. The structure of the opercular surface varies between species (Sands, 1957). When eggs are deposited into a leaf blade or a petiole, an elongate bulge often is visible on the plant surface; eggs can also be deposited in bark crevices. If the plant tissue becomes dry before the eggs hatch, the embryos are usually killed. There are five instars and the nymphs usually feed on the same prey as adults, with younger nymphs feeding on smaller prey stages. Common prey are mites, thrips, aphids, psyllids, and lepidopteran eggs and small larvae. In temperate regions, there are usually one to three generations and most species overwinter as adults. Short photoperiods induce reproductive diapause in some species (Parker, 1975; Kingsley & Harrington, 1982; Ruberson et al., 1991). Anthocorinae The greatest importance of anthocorids is as endemic natural enemies attacking agricultural pests. In Chu's (1969) review, 40 references to anthocorids feeding on about 20 species of Lepidoptera are listed, mostly Orius species. Other anthocorid genera that include species important to natural and applied biological control are Anthocoris, Lyctocoris, Montandoniola, and Xylocoris (Hodgson & Aveling, 1988). The biologies of about a dozen Anthocoris spp. have been investigated. Their range of prey is generally wide, but the range of plants inhabited depends on the species. Anderson (1962a) studied the bionomics of six Anthocoris spp. in England and found two of these species on 12 different tree species; one was on 11, two were on 7, and one was found on only 1 tree species. Thus, the latter Anthocoris species is restricted to feeding on prey that occurs on one plant species. The polyphagous A. nemorum (Linnaeus) is the most ubiquitous European species. Collyer (1967), using 30 literature references, records A. nemorum associated with 35

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different arthropod prey in 20 families of insects and 5 mite families on 17 different plants; Hill (1957) recorded and observed this predator associated with over 33 plant species. Prey of A. nemorum, other than pear psylla, noted in the literature since 1965, were listed by Herard (1986), and included 34 insect species in four orders and 5 mite species on at least 16 different plants. There were five references to A. nemorum feeding on pear psylla in Europe. As Anderson (1962c) and Herard and Chen (1985) point out, although a diversity of prey is accepted, there are great differences in the nutritive values for the predator. In an olfactometer, A. nemorum was attracted to certain plant leaf volatiles (tomato, willow) and reacted to, and distinguished between, odors coming from certain tetranychids but not to aphid species (Dwumfour, 1992). The efficiency of A. nemorum to capture prey aphids increased as the predator to prey ratio increased (Evans, 1976a). This anthocorid was unable to survive on sycamore trees unless there were 5 small sycamore aphids per 10 cm 2 of leaf, while A. confusus Reuter required 14 aphids per same leaf area (Dixon & Russel, 1972). Russel (1970) suggests that under natural conditions, the number of anthocorids that reach maturity is dependent on the number of young aphids available during the early stages of the anthocorid's development. If leaf surfaces are hairy, more thorough searching occurs but less surface area is covered compared with leaves with waxy surfaces (Lauenstein, 1980). Anthocoris nemorum and A. nemoralis (Fabricius) were the most abundant aphidophagous insects consuming hop aphids on hops (Campbell, 1977). Because A. nemoralis develops faster than A. nemorum, they ate fewer hop aphids. It appears that A. nemorum may have more of an impact on aphids and mites than on the myriad other prey it attacks. It has been collected in France and sent to the western United States for release against Psylla pyricola Forester, but it did not become established (Herard, 1986). Anthocoris nemoralis, a common Palearctic species, was accidentally introduced into eastern Canada, and later successfully was introduced into British Columbia from Europe in 1963 to control pear psylla (McMullen & Jong, 1967). It has made its way to California where it occurs commonly feeding on several exotic psyllids that attack omamental plants (Hagen & Dreistadt, 1990). Although A. nemoralis is a generalist predator, its prey and plant habitat range is narrower than A. nemorum. Herard (1986) listed 11 insect and 5 mite species as prey of A. nemoralis in addition to pear psylla. There are five European references to its feeding on pear psylla, and it is considered to be one of the most important predators of Psylla pyri (Linnaeus) and P. pyricola. In England, A. nemoralis appeared to have a strong density-dependent relationship with P. pyricola populations (Hodgson & Mustafa, 1984). In eastem Canada, it is considered the predominant predator of pear psylla (Hagley & Simpson, 1983). The searching patterns of A.

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nemoralis correlated well with the distribution of pear psylla on pear leaves (Brunner & Burts, 1975). Dempster (1968) notes that while predation by A. nemoralis and A. sarothamni Douglas & Scott (psyllid predator on scotch broom) on Arytainia psyllids was density dependent, they were incapable of controlling the numbers of their prey because of the variability in contemporaneous mortality caused by other predators. Anthocoris antevolens White, a Nearctic predaceous species commonly found on deciduous trees and shrubs, is transcontinental in Canada and the northern United States. It preys on psyllids and aphids and is considered an important predator of pear psylla (Anderson, 1962b; Watson & Wilde, 1963; Madsen & Wong, 1964; Nickel et al., 1965; Kelton, 1978). Anthocoris melanocerus Reuter, a northwest Nearctic species, has a similar biology to A. antevolens, but it also occurs on herbaceous plants; many of the same authors mentioned under A. antevolens also studied A. melanocerus. Based on laboratory cage studies, Tamaki and Weeks (1968) found that A. melanocerus suppressed Myzus persicae (Sulzer) on sugar beets below control populations; however, on broccoli the predator was only temporarily suppressive. In cages, egg cannibalism of the predator was as high as 95%. Anthocoris confusus, another common European species, has a similar biology to A. nemoralis (Hill, 1965) but is somewhat less ubiquitous; it is more of a tree-dwelling species. In England, A. confusus appears to feed mainly on callaphidid aphids on four major host trees (Anderson, 1962a) including the sycamore aphid Drephanosiphum platanoides (Schrank) (Russell, 1970; Dixon & Russel, 1972). The prey suitable for nymphal development may not be suitable for egg production because A. confusus will not reproduce on Aphis fabae Scopoli because this aphid induces a reproductive diapause (Anderson, 1962a). Evans (1976a) obtained a high numerical response in A. confusus when prey density of Aulacorthum circumflexus (Buckton) increased from one up to eight adult aphids per day; above this density, there was no increase in reproductive rate. Also, there can be mutual interference between the adult anthocorids that leads to a density-dependent decrease in egg production due mainly to an increased tendency for adults to migrate out of areas of high predator density (Evans, 1976d). As the age of the plants increased, the numbers of eggs deposited decreased considerably; plant topography can strongly influence the search pattern (Evans, 1976b, 1976c). The biology of Montandoniola moraguesi (Puton), also in the Anthocorinae, is similar to that of Anthocoris spp., but differs in that it apparently only feeds on Phlaeothripidae, including the Cuban laurel thrips. Gynaikothrips ricorum (Marchal) (Tawfik & Nagui, 1965; Funasaki, 1966). During 1964, the Cuban laurel thrips was found infesting Chinese banyan trees, Ficus retusa Linnaeus, at the Hono-

lulu International Airport. It quickly spread to the other Hawaiian Islands within a year, resulting in defoliated trees. Montandoniola moraguesi was obtained from the Philippines and introduced to Oahu and Kauai Islands in 1964 (Davis & Krauss, 1965), and in one year the predator spread considerably and reduced the thrips populations on five islands (Funasaki, 1966). It also has been observed to prey on Liothrips urichi Karny, which was introduced into the Hawaiian Islands to control the weed Clidemia hirta (Linnaeus) D. Don (Funasaki et al., 1988). Orius is another economically important genus in the subfamily Anthocorinae with 21 species recognized in the Western Hemisphere (Herring, 1966). Its species are smaller than Anthocoris but have similar biologies. Carayon and Steffan (1959) reviewed the feeding habits of 13 species of Orius and concluded that most species are polyphagous and all probably suck plant juices. The most common prey for the majority were thrips, followed by Homoptera, lepidopteran eggs and small larvae, and mites. Orius pallidicornis (Reuter) apparently feeds exclusively on cucurbit pollen (Carayon & Steffan, 1959). Feeding on plant liquids helps sustain Orius when prey are scarce (Kiman & Yeargan, 1985), but can be a detriment if a crop is treated with systemic pesticides because the toxins kill the predators when they ingest the contaminated plant sap (Ridgway et al., 1967). There is much written about the four or five species of Orius that are involved in natural and biological control of many pests in a diversity of crops. Ryerson and Stone (1979) list 164 selected references to the bionomics for O. insidiosus (Say) and O. tristicolor alone. Orius insidiosus was mainly a midwestern-eastern North American species, but is now transcontinental and has spread into Central and South America. In agriculture, it is essentially associated with corn, soybeans, and to a lesser extent apple trees. Barber (1936) found it on a wide variety of plants but particularly on corn; it could develop as nymphs when exposed only to corn silks but no reproduction occurred. Dicke and Jarvis (1962) found corn pollen to be important in building up populations of the predators. Eggs are deposited into moist corn silks and nymphs feed on the silks and insects, particularly Heliothis zea (Boddie), when they are older. The life cycle is about 24 days during the summer (Barber, 1936). Nymphal development was completed on Acer pollen plus green beans, but not on green beans alone; development was faster on diets containing arthropod prey than on diets lacking prey. Also, Kiman and Yeargan (1985) found an adult diet of H. virescens (Fabricius) eggs resulted in higher fecundity for O. insidiosus than for spider mites or a thrips species. The association of O. insidiosus with corn is apparently long-standing because it is attracted to volatiles (hexane extracts) of corn silks (Reid & Lampman, 1989). The synamone brings O. insidiosus to corn silks where eggs of H.

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

zea, as well as those of a more recent prey, the European corn borer. Ostrinia nubilalis (H~ibner), are commonly de-

posited (Reid, 1991). Corn earworms and fall armyworms feeding on resistant corn foliage or meridic diets containing resistant corn silks were subject to increased mortality by Orius insidiosus (Isenhour et al., 1989). When densities of O. insidiosus and spiders averaged two to five per plant, survival of small southwestern corn borers on whorl and tassel stage corn was reduced (Knutson & Gilstrap, 1989). The insidious flower bug was by far the most abundant predator encountered in Arkansas grain sorghum fields; it was sampled as a predator of H. zea to determine if predator to prey ratios could be established (Steward et al., 1991). On soybeans, O. insidiosus commonly feeds on soybean thrips larvae occurring mainly on trifoliate leaves, which accounted for a concentration of the Orius eggs in the upper parts of the plant and caused a decline in the thrips populations (Isenhour & Yeargan, 1981). Crop phenology is also an important factor. In strip-planted soybean and corn in Kentucky, populations of O. insidiosus peaked on corn during the period of silking and pollen shed, while predator density was greater on early planted soybeans compared to June planted soybeans (Isenhour & Yeargan, 1981). Corn and alfalfa adjacent to apple orchards in Virginia apparently served as alternate sites for O. insidiosus populations throughout the growing season (McCaffrey & Horsburgh, 1986b). These authors determined that thistles also harbor a large number of predators, and calculated temperature threshholds for development (McCaffrey & Horsburgh, 1986b) and functional response of O. insidiosus to the European red mite at different temperatures (McCaffrey & Horsburgh, 1986a). Orius insidiosus was successfully introduced into the Hawaiian Islands against H. zea in a 1951 classical biological control program (Funasaki et al., 1988). Orius minutus (Linnaeus) is a common European species that was probably introduced into British Columbia with the importations of shrubs and herbaceous plants (Kelton, 1978, Lattin et al., 1989). It has a similar biology to Anthocoris and other Orius spp. in that it is a general predator and feeds to some extent on plants. Herard (1986) lists 18 recent references of O. minutus feeding on mites, thrips, Diptera, Lepidoptera, Coleoptera, coccids, aleyrodids, and aphids; it is one of six Orius species that has been recorded feeding on pear psylla. Spider mites, particularly the European red mite, are common prey of O. minutus (Collyer, 1953a, 1953b; Berker, 1958). Niemczyk (1978b) found that one O. minutus per 5 to 10 apple leaves can keep the European red mite at a low level if the mites do not exceed two to five mites per leaf prior to the appearance of the predator. Orius minutus and O. vicinus Ribaut could reduce the European red mite and other mites in vineyards in the absence of Phytoseiidae (Duso & Girolami, 1983). Niemczyk (1978a) reared many generations in the labora-

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tory using eggs of the Angoumois grain moth, Sitotroga cerealella (Olivier), which was a better food than Mediterranean flour moth eggs, the European red mite, the twospotted spider mite, or the green apple aphid. Orius majusculus (Reuter) can be mass cultured on A. kuehniella and geranium leaves (Alauzet et al., 1992); and and O. laevigatus (Fieber) are released against psyllids, aphids, and mites but are mostly used against thrips (Rudolf et al., 1993). Orius sauteri (Poppius), an Asian species, is mass-reared in China for field release, but we are not certain which pests are the targets. It has been reared from eggs to adults on aphids, mites, thrips, rice moth, pollen, and artificial eggs (Zhou & Wang, 1989). Soybean sprouts served as the best ovipositional medium; a mean of 52 eggs was obtained per predator on one bean plant seedling (Zhou et al., 1991a). Orius insidiosus has been released in greenhouses to control thrips (Van de Veire & Degheele, 1993). Orius tristicolor resembles O. insidiosus in its size and biology, but it is more widespread in North America (Anderson, 1962b; Kelton, 1978). It is commonly found in alfalfa, cotton, and other low crops as well as in flowering heads of many herbaceous plants. Early studies on the biology of O. tristicolor involved using spider mites as prey (Butler, 1966; Askari & Stem, 1972a, 1972b), but its preferred prey is probably thrips for it is most commonly associated with thrips in the field. A diet of pollen plus thrips was found most suitable for development of O. tristicolor nymphs, but adult longevity and total egg deposition increased when adults were fed green bean plus pollen plus thrips (Salas-Aguilar & Ehler, 1977). Stoltz and Stem's (1978) results from laboratory feeding studies of O. tristicolor exposed to western flower thrips supported the correlation of field data associating the two species. Letourneau and Altieri (1983) described the interactions of O. tristicolor and the western flower thrips in squash monocultures and polycultures of squash, corn, and cowpea; and suggest that the determining factor for differential colonization by Orius in monocultures and polycultures of squash was the attraction of Orius to the crop habitat during its prey location process. Once in the habitat the alarm pheromone of the western flower thrips nymphs becomes a prey-finding kairomone for O. tristicolor (Teerling et al., 1993). The importance of O. tristicolor as a mortality factor of aphids is not clear. In Goodarzy and Davis' (1958) study, it is considered to be one of the most important predators of Therioaphis maculata Busk., the spotted alfalfa aphid, in Utah. However, Neuenschwander et al. (1975) show only a minor affect on pea aphid and spotted alfalfa aphid populations in California alfalfa fields. In Idaho potatoes, O. tristicolor abundance was strongly correlated with the presence of thrips, but did not appear to be the cause of green peach aphid decline (Hollingsworth & Bishop, 1982). The searching behavior of O. tristicolor is similar to

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many other predators: once it is in the habitat of the prey, predators search more rapidly with a slow turning rate when starved, but after contacting prey, the searching speed decreases and the turning rate increases (Shields & Watson, 1980). Light intensity can also influence turning ratios of starved females of O. tristicolor: under direct current (DC)powered incandescent light there was no effect on activity levels or turning ratios, but under alternating current (AC) powered incandescent light, the distances traveled were greater regardless of light level (Shields, 1980). Under 12h photoperiods, O. tristicolor ate twice as many mite eggs as when held in the absence of light (Askari & Stem, 1972b). In applied biological control, the capacity for thrips control by Orius on squash was demonstrated by Letourneau and Altieri (1983) using predator inclusion-exclusion cage experiments. It is released with phytoseiids to control western flower thirps attacking vegetables in greenhouses (Gillespie & Quiring, 1992; Cloutier & Johnson, 1993). Orius tristicolor was released twice in Hawaiian classical biological control programs: in 1962 against the microlepidopteran Ithome cancolorella Chambers that attacked kiwi, and in 1964 against the Cuban laurel thrips (Davis & Krauss, 1963, 1965), but apparently O. tristicolor never became established (Clausen, 1978). Orius tantillus (Motschulsky) is considered to have great potential as a predator of Thrips palmi Karny in the Philippines (Mituda & Calilung, 1989).

Lyctocorinae The subfamily Lyctocorinae contains species that are commonly found under bark, in stored grain, and in leaf or straw litter. The few species involved in natural and biological control literature are mainly in two genera. Lyctocoris beneficus (Hiura) occurs in Japan and Korea, and its biology has been excellently studied and described by Chu (1969). Because this anthocorid attacks overwintering larvae and newly emerging adults of the striped rice stalk borer, Chilo suppressalis (Walker), in straw piles and in barns, it was considered a natural enemy that could be reared and possibly used in augmentative releases against the stalk borer. Chu (1969) found that L. beneficus fed on 45 of the 73 different species in nine insect orders that he exposed to the anthocorid. This generalist predator, however, prefers a habitat of somewhat dry rice paddy straw. The best insectary diet to mass rear the predator was Tribolium larvae, but Chu (1969) also made some progress in developing an artificial diet for the bug; furthermore, he calculated growth and reproductive energetic values of L. beneficus. This predator did not have any influence on borer populations in paddy stubble because it could not attack free-crawling borers. Thus, it is limited to preying on borers infesting straw piles. Lyctocoris campestris (Fabricius) is a worldwide gener-

alist predator of stored product insects that produces best growth and reproductive responses when exposed to grain moths instead of to common stored product-infesting beetles (Parajulee & Phillips, 1993). Lyctocoris elongatus (Reuter) and Scoloposcelis flavicornis Reuter (= S. mississippensis Drake & Harris) are predators of bark beetles attacking standing and felled pines. Schmitt and Goyer (1983) determined the developmental times and described the immature stages of both anthocorids. Xylocoris flavipes (Reuter), a cosmopolitan species called the warehouse pirate bug, is commonly found associated with stored product insect pests. This association prompted Jay et al. (1968) to explore the possibility of its being a biological control agent of stored product pests, and their first tests showed that the anthocorid successfully inhibited population buildup of four species of beetles that attack stored grain. Populations of Tribolium were significantly reduced in stored peanuts by releasing various densities of X. flavipes (Press et al., 1975) and it also controlled moths infesting stored peanuts (Brower & Mullen, 1990). Also, the saw-toothed grain beetle populations infesting shelled corn were reduced 95% by releases of the predator (Arbogast, 1976). Increases of residual populations of almond moth, saw-toothed grain beetle, and T. castaeum (Herbst) in small quantities of rolled oats were curtailed by releasing X. flavipes (LeCato et al., 1977). In laboratory studies, LeCato and Arbogast (1979) effectively reduced populations of Angoumois grain moth in small quantities of grain because the predator killed the prey before it entered the grain to cause damage. Xylocoris flavipes is more effective in coarsely particulated media than in fine media (Press et al., 1978). Wen and Deng (1989) found that a Xylocoris sp. in China gave effective control of T. confusum Jacquelin duVal in stored wheat grain but not in wheat flour. Releasing parasitoids of almond moth eggs and larvae was compatible with the predation of X. flavipes (Brower & Press, 1988; Press, 1989). The release of 50 pairs of X. flavipes into empty corn bins with infested residues of grain with stored product insect pests resulted in good reduction of smaller pest species but not larger moth larvae; thus Brower and Press (1992) believe by releasing specific parasitoids for control of the moths and primary grain pests, the whole pest complex might be greatly reduced before the newly harvested grain is brought to the bins for storage. Xylocoris galactinus (Fieber), a cosmopolitan generalist predator, is found associated with stored grains, but prefers moist habitats; thus, it is also commonly found in manure heaps, in hot beds, and under bark. Chu (1969) made an extensive study of its biology. He exposed X. galactinus to over 60 different species and the predator fed on 43 species of insects in 22 families scattered in nine orders; he also had some success rearing it on artificial diets and was able to mass-rear it on T. castaneum larvae infesting cracked

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

corn. Xylocoris galactinus has five generations in Japan compared with three for L. beneficus. Berytidae The stilt bugs are essentially phytophagous (Froeschner & Henry, 1988), but Elsey and Stinner (1971) and Elsey (1972a, 1973) found Jalysus spinosus (Say) to be predaceous on eggs of H. virescens and Manduca sexta (Linnaeus) on tobacco plants, and at times it was the most numerous predator of Heliothis eggs in North Carolina tobacco fields (Elsey, 1972a). This predator can only prey on eggs, dead insects, or slow-moving insects such as aphids, and cannot penetrate the serosa of 1- or 2-day-old M. sexta eggs (Elsey, 1972b). Lygaeidae This is the second largest family in the Heteroptera, with about 3000 species in North America. Ashlock and Slater (1988) list 322 species in 85 genera and include references to their biologies. Apparently only the subfamily Geocorinae contains predaceous species, and only 4 or 5 species of the 25 species in Geocoris that occur in North America north of Mexico have been involved in the biological control studies. In Readio and Sweet's (1982) key and discussions of the species of Geocorinae that occur in the United States east of the 100 meridian, four of the five important species are covered. Geocoris spp. are generalist predators that require some feeding on plants for optimal development and reproduction (York, 1944; Sweet, 1960; Ridgway & Jones, 1968; Stoner, 1970; Tamaki & Weeks, 1972b; Naranjo & Stimac, 1985, 1987; B u g g e t al. 1987, 1991). Readio and Sweet (1982) show a prey list of Geocoris species in the United States, and Tamaki and Weeks (1972b) list prey of Geocoris species from the world literature. The prey are mostly Heteroptera, Homoptera, Coleoptera, Lepidoptera, and Acarina. Unlike the Anthocoridae, Nabidae, and Miridae; Geocoris spp. deposit their oval eggs singly, either horizontally on plant surfaces or in soil duff. Eggs are often parasitized by scelionids. The nymphs usually attack the same type prey as the adults. They locate prey visually, but use their antennae to find plant food or possibly the correct habitat (Readio & Sweet, 1982). Geocoris atricolor Montandon is a western North American species found in alfalfa and cotton fields. It was reared in the laboratory on potato tuber moth larvae and string beans by Dunbar and Bacon (1972a, 1972b), who determined its developmental time for eggs and nymphs and fecundity under six different temperatures. Geocoris atricolor was more similar in its responses to various temperatures to G. pallens Stgd than to G. punctipes (Say), which developed and oviposited best at the lower temperatures tested. Geocoris bullatus (Say) occurs across the northern United States in sandy soil areas and readily feeds on seeds even in the presence of prey (Sweet, 1960). It did not lay

40 |

eggs on a diet of seeds and beans or of pea aphids and beans unless sugar beet leaves were provided (Tamaki & Weeks, 1972b). In the northwest United States, it is usually abundant in forage and vegetable crops along with G. pallens and became most abundant (25 per square foot) in orchard floor vegetation, particularly under peach trees infested with Myzus persicae. Geocoris bullatus reduced the number of green peach aphids on fallen leaves returning to each tree by more than half, thus, an average of more than 10,000 more oviparae returned to the trees where predators were excluded from the orchard floor (Tamaki, 1972). Under laboratory conditions, Tamaki and Weeks (1972a) found coccinellids were the most effective in reducing high densities of aphids, but the omnivorous nabids and geocorids were more effective at low aphid densities because they could sustain themselves on fewer prey. They also found that in a mixture of caterpillar and aphid prey, G. bullatus attacked only a few caterpillars; thus, the caterpillars interfered only slightly with predation on the aphids. In a greenhouse study, G. bullatus was released in cages with M. persicae infesting sugar beets and suppressed the aphids so there was only a 9-fold increase in 28 days compared with a 2000-fold increase in cages without Geocoris (Tamaki & Weeks, 1972b). By providing chopped sunflower seeds as a supplemental food in sugar beet plots, the number of Geocoris eggs laid on sugar beet plants was doubled compared with controls (Tamaki & Weeks, 1972b). Geocoris bullatus also preys on Lygus spp., and Chow et al. (1983) determined the functional response of the predator to three different densities of Lygus nymphs at three different temperatures. Geocoris pallens occurs throughout the western United States east to central Texas, mostly in open, disturbed habitats and agricultural fields (Readio & Sweet, 1982). It has a similar biology to G. bullatus but is more southern in its distribution. Butler (1966) and Dunbar and Bacon (1972a) determined its egg and nymphal development at several different temperatures. Tamaki and Weeks (1972b) obtained similar responses when they tested progeny of overwintered G. pallens. However, when they tested progeny from first generation adults, there was a consistent 4~ difference over the entire regression line in the rate of egg development; the developmental threshold of the eggs from the overwintered adults was about 10~ and those from the first generation was about 15~ In field studies in cotton, G. pallens was an effective predator of H. zea larvae (van den Bosch et al., 1969), Lygus bugs (Leigh & Gonzalez, 1976), cabbage looper (Ehler et al., 1973), pink bollworm (Irwin et al., 1974), and mites (Gonzalez et al., 1982); it also suppressed M. persicae on sugar beets (Tamaki & Weeks, 1973). Because certain pesticides, including herbicides and defoliants, besides insecticides can reduce Geocoris populations, the choice of more sparing pesticides is valid. Yokoy-

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ama et al. (1984) determined the acute toxicity of 22 pesticides, noting those materials that are particularly suitable for use in cotton. Geocoris punctipes occurs across the southern two-thirds of the United States and extends southward into Colombia. It is commonly found associated with agricultural crops such as alfalfa, cotton, lettuce, peanuts, soybeans, and sugar beets (Readio & Sweet, 1982). It appears to be the most studied geocorine species among the natural enemies of agricultural pests. It has a similar biology to G. pallens, but because it is one of the largest Geocoris species, it consumes more prey. Butler (1966) determined the number of bollworm eggs consumed by adults and nymphs of G. punctipes, the number of different size lygus bug nymphs consumed per individual adult, and number of first-instar lygus bugs consumed by individual G. punctipes nymphs of different ages in 24 h (1967). The number of soybean looper eggs consumed daily at four different temperatures was determined by Crocker et al. (1975). At 25~ in the laboratory, the developmental time of G. punctipes eggs was about 10 days for a total nymphal development of about 27 days, and the preoviposition period was about 5 days with a mean fecundity of 178 eggs; the diet was coddled fifth-instar larvae of the beet armyworm and a section of green string bean (Champlain & Sholdt, 1967a). Champlain and Sholdt (1967b) also determined the temperature range for the development of the immature stages. After testing eight different diets, Dunbar and Bacon (1972b) concluded that insect eggs were preferred by G. punctipes, even though complete nymphal development occurred on pea aphids with green beans and two-spotted spider mites and green beans. No adults were produced on pea aphids alone, and no eggs were deposited with a diet of the spider mites and green beans. With green beans (provided as a water source) and fresh Heliothis eggs, G. punctipes produced significantly more eggs with higher fertility than when fed fresh Sitotroga cerealella eggs; frozen eggs could be useful for temporary rearing even though fecundity was significantly lower than on fresh eggs (Lopez et al., 1987). Cohen (1984) measured the food consumption and utilization from first-instar nymphs to adults of G. punctipes fed eggs of H. virescens and found that food absorption efficiency was 95.2% and growth efficiency was 52.9%; and he also determined the ingestion efficiency and protein consumption by G. punctipes fed pea aphids (Cohen, 1989). In addition, Cohen improved a method of encapsulating a semidefined artificial diet in wax that was fed successfully to G. punctipes, G. pallens, and several other predaceous insects (Cohen, 1983). Cohen further simplified an artificial diet for G. punctipes by making a paste of fresh beef liver, fat ground beef, sugar solution, wheat germ, fresh spinach, coupled with a salt solution that was squeezed onto sheets of stretched Parafilm| and rolled into

a sausagelike cylinder; on this diet. G. punctipes was reared for at least three generations (Cohen, 1985). It has been cultured on the artificial diet for over 50 generations, and Hagler and Cohen (1990) incorporated vertebrate-derived antigens into the diet and determined that simulated prey ingestion could be detected up to 48 h. Crop plants and weeds can have direct and indirect influences on the predation performance of Geocoris, as well as on any of the predaceous hemipterans that at times are herbivorous. Application of systemic insecticides to cotton showed not only the importance of natural populations of Geocoris, Nabis, and Orius predators in "regulating" Heliothis spp. populations but also the fact that the heteropteran predators fed on cotton because they were reduced in numbers by systemic soil treatments that had minimal impact on Chrysopa larvae and hymenopteran parasitoids (Ridgway et al., 1967). York (1944) had already demostrated that Geocoris fed on plants as a water source but required leafhopper eggs or nymphs for complete development. Stoner (1970) tested many plants and found G. punctipes could live over 20 days on certain seeds, about 9 days on cotton leaves, 12 days on dandelion pollen, and 3.5 days on water alone, but required arthropod prey for normal development and fecundity. Big-eyed bugs were also found to use cotton extrafloral nectar as an alternate food (Yokoyama, 1978). Geocoris punctipes did feed more on nectared cotton without H. virescens eggs; however, when Heliothis eggs were present, there was no difference in feeding on nectared versus nectarless plants (Thead et al., 1985). Sprenkel et al. (1979) found the planting dates, row widths, and to a degree the seeding rate of soybeans influenced populations of three lepidopteran pests and the abundance of G. punctipes, Nabis spp., and spiders; by planting early, predation and parasitization of the lepidopteran pests were increased. There also can be interactions between predaceous species such as spider Oxyopes salticus and Geocoris spp. that prefer Heliothis spp. eggs but will feed on the spider's eggs. The big-eyed bug adults ate all eggs or emerging spiderlings from a single unguarded egg sac, and the adult O. salticus females fed on more active prey such as larger Geocoris nymphs and adults (Guillebeau & All, 1989). These and other results suggest that inundation of fields with Geocoris spp. is unlikely to reduce O. salticus populations, but predation by increased O. salticus populations could decrease geocorid populations. Also, the intraspecific competition between G. punctipes for H. zea first-instar larvae significantly reduced the number of larvae consumed per individual and suggested to Guillebeau and All (1990) that exceeding an optimal density of Geocoris in the field could reduce the biological control of H. zea. Releases of G. punctipes in field cages in cotton showed that about 252,000 adults per acre were ineffective, but a

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

release of 630,000 per acre reduced the egg and larval populations of H. virescens by 88% (Lingren et al., 1968). The number of H. virescens eggs consumed per G. punctipes by intermediate predator densities (10,756 to 16,134 per ha) increased significantly as prey density increased (16,134 to 48,402 per ha), but the percentage of eggs consumed remained constant (1.0 to 2.0% per predator per 48 h), suggesting a type I functional response (Hutchison & Pitre, 1983). In field cages, G. punctipes and Nabis spp. could significantly reduce the Mexican bean beetle populations by preying on eggs and first-instar larvae of the beetles on soybeans (Waddill & Shepard, 1974a). When G. punctipes were released in cages over alfalfa infested with Bemisia tabaci (Gennadius), 40% of the whiteflies were destroyed (Becker et al., 1992). Geocoris ochropterus (Fieber), an important general predator of crop pests in India, was reared on frozen ant pupae for potential release against tea insect pests (Mukhopadhyay & Sannigrahi, 1993). Miridae This is the largest family of the Heteroptera; Henry and Wheeler (1988) believe the number of species will reach 20,000 in the world faunas. Most known species are phytophagous, but scattered in the Miridae are at least 25 genera containing species that are mostly generalized predators. There are 98 mirid species that are common to North America and the Old World including some predaceous species (Wheeler & Henry, 1992). Some of the most distinctive mirid pest species are at times predaceous, and Schuh (1974) and Wheeler (1976) believe ancestral mirids were generalized predators. Mirids usually deposit their eggs in plant stems and in living or dead twigs, but some coccophagous species deposit their eggs beneath old female scale coverings (Wheeler & Henry, 1978b). There are five nymphal instars and the young usually feed on the same plant or prey as the adult. In temperate climates there is usually one generation, but mirids can have overlapping broods. Overwintering usually occurs in the egg stage and, at times, in the adult stage (Wheeler & Henry, 1992). Some predaceous species have played important roles in classical and natural biological control. Natural control of the European red mite by mirids was observed by Gilliatt (1935) in Nova Scotia apple orchards; when nicotine sprays were used in the orchard, the nymphal stages of mirids were quickly killed and populations of the mite made rapid increases. He also tested other pesticides that were less harmful to the predators. Certain pesticides on pear trees reduce predaceous mirids, which allows pear psylla populations to increase (Westigard, 1973). Descriptions of the various stages and biologies of many mirid species found in European orchards are nicely covered by Fauvel (1974). Only a few genera that contain predaceous species will be discussed here. The predaceous genera fall under many

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different higher taxa, but it appears that the Isometopinae, Deraeocorinae (at least the tribe Deraeocorini), and many genera in the subfamily Orthotylinae contain most of the predaceous species. Blepharidopterus angulatus (Fallrn), the black-kneed capsid, is a Palearctic species that was probably inadvertently introduced into North America after 1935. It occurs in Europe, the former USSR, North Africa, and Canada (ranging from British Columbia to Nova Scotia) (Henry & Wheeler, 1988). Collyer (1952) found this mirid to be most numerous in commercial fruit orchards in England infested with the European red mite, Panonychus ulmi, where it is an important predator of the mite (Muir, 1966). It also attacks other mites, aphids, and thrips. An adult female B. angulatus can consume 4000 adult female mites; nymphs and adults were observed to suck leaves and fruitlets but no damage to plant tissue occurred (Collyer, 1952). Blepharidopterus angulatus also feeds on aphids and leafhoppers. Glen (1973, 1975) made extensive studies of the searching, food requirements, and energetics of the mirid exposed mainly to lime aphids and constructed a model to predict prey densities required for optimal development. Under field conditions, first-instar B. angulatus should require a prey density about nine times greater than that required in later instars. Campylomma verbasci (Meyer-Dtir) is a European species that was inadvertently introduced into North America where it now occurs across the continent in the northern United States and southern Canada. It is a parthenogenetic species and an important predator of pear psylla in British Columbia (McMullen & Jong, 1970) and France (Fauvel & Atger, 1981); it preys on eggs of the European red mite on apple in Nova Scotia (Gilliatt, 1935; Lord, 1971), England (Collyer, 1953a), and Poland, but alone it could stop the increase of neither mites nor aphids in Poland (Niemczyk, 1978c). In Ontario apple orchards, serological assays revealed that the mirid preyed on Aphis pomi (Hagley & Allen, 1990). In the laboratory it ate two A. pomi a day compared with two larger mirids, Lepidopsallus minisculus Knight (which ate over six aphids) and Hyaliodes vitripennis Say (which consumed over three aphids), and all three mirids ate tetranychid mites (Arnoldi et al., 1992). Both C. verbasci and Atractotomus mali (Meyer-Dtir) can be a pest of apples depending on the host cultivar and prey availability (Wheeler & Henry, 1992). Campyloneura virgula (Herrick-Shaeffer) is another parthenogenetic Palearctic polyphagous species, which was recently discovered in British Columbia and now extends down the West Coast into northern California. It is predaceous on small arthropods found on a variety of trees and shrubs (Lattin & Stonedahl, 1984). It overwinters in the egg stage in the British Isles, but as an adult on the continent of Europe (Southwood & Leston, 1959). Along with anthocor-

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ids, it displayed an ability to regulate pear psylla populations in untreated pear orchards in France (Bouyjou et al., 1984). Ceratocapsus modestus (Uhler) may be important in the control of leaf gall-forming phylloxera (Wheeler & Henry, 1978a). Carvalho et al. (1983) summarized the predaceous habits of this genus and described many new South American species. The genus Cyrtorhinus is composed of valuable species that show a marked preference for particular plants and their associated delphacid plant hoppers, but a species may turn to related plants and plant hoppers in the vicinity of its regular associated habitat and prey eggs. The genus at one time contained a group of species that have distinct large sinuous arolia between the claws and another group with only two very fine parallel small setae between the claws (Usinger, 1939). When Carvalho and Southwood (1955) revised the genus, they gave the genetic name Tytthus to the latter group; it also contains some very important natural enemies and will be discussed later. Cyrtorhinus fulvus Knight, a Pacific Island species, prefers taro as a plant host, where it oviposits in leaf petioles and the nymphs and adults feed on the eggs of the taro leafhopper, Tarophagus proserpina (Kirkoldy) (Matsumoto & Nishida, 1966). It was purposely introduced from the Philippines to Hawaii in 1938, where it quickly became established and controlled the leafhopper (Fullaway, 1940); later the predator was sent to seven Pacific islands and became established and provided good control in Fiji, Guam, Ponape, and Samoa (Waterhouse & Norris, 1987). By removing the predators by hand every other day in Hawaiian plots, Matsumoto and Nishida (1966) obtained a significant increase in taro leafhopper populations compared with plots where C. fulvus was not removed. Cyrtorhinus lividipennis Reuter is an Asian species that also occurs on Guam and the Philippine Islands (Chiu, 1979; Yasumatsu et al., 1981). Initial introductions into the Hawaiian Islands to control the corn delphacid Peregrinus maidis (Ashmead) failed, but later it not only became established but also provided effective control of P. maidis and has shown an adaptation to dry corn agroecosystems (Liquido & Nishida, 1985b, 1985c). In Philippine rice plots, predators such as large spiders, coccinellid beetles, dragonflies, damsel flies, lizards, and toads were removed by hand, while plant hoppers, small spiders, and C. lividipennis were removed with mouth aspirators by Hsieh and Dyck (1975). These authors concluded that spiders and C. lividipennis played an important role in regulating the rice green leafhopper, Nephotettix virescens (Distant). The brown plant hopper, Nilaparvata lugens, is also a prey of C. lividipennis (Chua & Mikil, 1989; Manti, 1991). The mirid eats all stages of the brown plant hopper and its functional response to both eggs and first-instar nymphs was determined by

Sivapragasam and Asma (1985). It also attacks the brown plant hopper on rice in Guam (Usinger, 1939), and prevented increases of this plant hopper in drilled, but not transplanted, rice fields in Fiji (Hinckley, 1963). In the Philippines, Kenmore (1980) considered predation by generalist natural enemies a more significant source of brown plant hopper mortality than that of parasitism. He found spiders, veliid Microvelia, and mesoveliid Mesovelia, which feed on prey falling on the water surface, to be apparently important in suppressing brow plant hopper populations. In the event that inoculative releases of C. lividipennis became necessary to control delphacids, Liquido and Nishida (1985a) developed methods of mass-culturing the mirid on a factitious prey, eggs of the Mediterranean fruit fly. The body dimensions of the predators fed on the fruit fly eggs were equal to those that received its normal prey, the corn leafhopper; the duration of eggs and of nymphal instars was not significantly different and fecundity was the same, but longevity of the mirid fed its natural prey was much longer. The genus Deraeocoris is composed of some 70 species in North America and was last revised by Knight (1921). At that time he called attention to some species that were quite specific to woolly aphids, Eriosoma spp., which in their nymphal stages resembled the aphids because of a coveting of white, powdery, flocculent material. Furthermore, Knight believed there were also phytophagous species in the genus because they were associated with certain plant species. Today, however, it appears that most species are general predators (Henry & Wheeler, 1988). Deraeocoris lutescens (Shilling) is a general predator in European orchards; it is partially phytophagous and overwinters in the adult stage (Collyer, 1953b). Collyer (1953b) and Fauvel (1974) briefly describe its stages and biology. Herard (1986) cites references on its occurrence in Europe and its association with pear psylla. Deraeocoris nebulosus (Uhler) is a generalist predator that occurs throughout most of the United States and Canada on more than 50 species of ornamental trees and shrubs (Wheeler et al., 1975). These authors studied its biology by exposing the mirid mainly to the oak lace bug as prey, because the predator could be important in suppressing populations of lace bugs and other pests on ornamentals. Deraeocoris ruber (Linnaeus) is distributed widely in Europe, but is more common in southern Europe and has spread to the eastern United States and South America (Henry & Wheeler, 1988). It is found on many trees, bushes, and herbs, where it feeds on various insects and mites, but prefers feeding on prey larger than the red spider mite (Collyer, 1953b). It is a common predator of aphids on hazel in Italy, overwinters in the egg stage (Viggiani, 1971), and is an occasional predator of Psylla pyri (Herard, 1986).

Chapter 16

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Diaphnocoris provancheri (Buryae) (= pellucida Uhler) occurs across North America on many trees and shrubs and is predaceous on aphids (Kelton, 1980). It is also an effective predator of P. ulmi on apple trees in Nova Scotia where it occurs with three other mirid species (Lord, 1971). In the same orchards, MacLellan (1962) found what was probably D. provancheri preferably attacking fresh codling moth eggs, unlike the three other mirid species present, but all the mirids attacked young codling moth larvae. Heterotoma meriopterum (Scopoli) is another Palearctic species inadvertently introduced into North America where it occurs from British Columbia to Nova Scotia and New York (Henry & Wheeler, 1988). Fauvel (1974) illustrates some of its stages. Herard (1986) found it to be one of the most common mirids in French pear orchards, also occurring on hawthorn and nettle where it feeds on psyllids and aphids. On pear trees, eggs are deposited in young twigs and overwinter there, but normal and unavoidable pruning of pear trees in winter intensely depressed predator populations in the orchard; thus hawthorn trees can be useful for mirid survival and retention near the orchards; also, the pear prunings can be saved for mirid emergence (Herard, 1986). Collyer (1953b) found it mainly predaceous on P. ulmi and less so on aphids in apple trees in England. In the subfamily Isometopinae, Corticoris signatus (Heidemann) and Myiomma cixiformis (Uhler) prey on obscure scale Melanaspis obscura (Comstock) infesting oaks in Pennsylvania (Wheeler & Henry, 1978b). The predaceous habit of this subfamily on diaspine scales was first reported by Hesse (1947), who noted the nymphs and adults of Letaba bedfordi Hesse preying on and reducing heavy infestations of citrus red scale in South Africa. Wheeler and Henry (1978a) review the feeding habits reported in the literature for the subfamily and describe the biology and illustrate nymphs of several species. Lygus spp., the notorious pests on many agricultural crops, are at times predaceous. Wheeler (1976) lists 20 arthropod species in five insect orders as prey. However, lygus also can serve as prey to at least four predatory heteropteran families. Whalon and Parker (1978) employed an immunological microdouble-diffusion technique to determine the presence of apple-infesting L. lineolaris Palisot de Beauvois in predator gut contents, using antibodies developed in rabbits. Macrolophus caliginosus Wagner is considered a good candidate for release in greenhouses because it is a polyphagous predator that has been used against whiteflies (Malausa et al., 1987). It would be more effective against Myzus persicae than Tetranychus urticae based on preference and functional responses of M. caliginosus to both prey (Foglar et al., 1990). The genus Phytocoris is one of the largest in the Miridae, but the habits of most species are poorly known. The

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nymphs and adults of some Phytocoris spp. are concealed as they crouch in the crevices of the bark, apparently awaiting prey (Knight, 1921). Some Phytocoris spp. in western North America are of Palearctic origin (Stonedahl,1983). Spanagonicus albofasciatus (Reuter), a widely distributed New World species, has mixed reviews as a predator. Wene and Sheets (1962) considered it a pest in Arizona cotton fields, but Butler (1965) tested it in the laboratory and found it to eat spider mite eggs; hyaline plant bug eggs; cotton aphids; bollworm eggs and young larvae; lygus bug eggs; and eggs, larvae, pupae, and adults of the banded whitefly. Thus, Butler considered S. albofasciatus (Reuter) a potentially important predator in Arizona cotton fields. Its stages and development were studied by Musa and Butler (1967). In Arizona, it is found commonly on 12 different plants in 10 different plant families (Stoner, 1965). In Florida soybean fields, it was observed to feed on Heliothis zea and Pseudoplusia includens (Walker) eggs by Neal et al. (1972) and on velvet bean caterpillar eggs in the same area by Buschman et al. (1977). Stethoconus japonicus Schumacher, an adventive predator of the azalea lacebug, is the first host-specific lacebug predator established in the Western Hemisphere (Henry et al., 1986). It showed the highest biological control potential for species of Stephanitis lacebugs, but also preys on hawthorn lacebugs. The biology of this oligophagous mirid is described by Neal et al. (1991) and Neal and Haldemann (1992). The biology of Stethoconus praefectus (Distant), which attacks Stephanitis typicus Distant, a pest of coconut palms, was studied by Mathen and Kurian (1972). Tytthus mundulus (Breddin) occurs naturally in Australia, Java, the Philippines, and Fiji Islands (Usinger, 1939). A search for more natural enemies of the sugarcane leafhopper, Perkinsiella saccharicida Kirkaldy, for release in the Hawaiian Islands was made in the Queensland area of Australia by F.A.G. Muir in 1920, where he discovered T. mundulus feeding on the embedded leafhopper eggs. He returned to the Hawaiian Islands with a few of the mirids that were carefully studied before release in July 1920. Another lot of T. mundulus was collected in Fiji by Pemberton and these were also released in Hawaii during 1920. By 1923, the sugarcane leafhopper was no longer a problem (Pemberton, 1948). There can be 10 generations of the predator per year (Swezey, 1936). It often consumes the leafhopper eggs and then its own eggs in the same sites, but asynchrony of com leafhopper in time and place explains why T. mundulus is not an effective predator of Peregrinus maidis infesting com (Verma, 1955). It was also successfully introduced into Jamaica and Mauritius (Williams, 1957). In South Africa, T. mundulus imported from Mauritius did not become established against the green leaf sucker, Numicia viridis Muir, but the inadvertently introduced T. parviceps (Reuter) apparently did become estab-

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lished (Carnegie & Harris, 1969). Both of these Tytthus spp. are cultured and released in South Africa (Greathead, 1971). Releases of T. mundulus were made in Florida in 1984 but establishment is not yet confirmed (Henry & Wheeler, 1988). Attempts were made to introduce T. mundulus against the sugarcane leafhopper in Ecuador several times but the material died in shipment in 1977. Bianchi (1980) hand carried the predator and made releases in Ecuador, but its establishment there is questionable. In transit, T. mundulus nymphs can be fed housefly eggs inserted into leaf tissue (Stevens, 1975). Nabidae The damsel bug family contains 31 genera and about 380 species m all known species are predaceous (Lattin, 1989). The subgeneric taxa of Nabis (Reduviolus and Tropiconabis) are not used here. The bionomics of Nabidae have been reviewed by Lattin (1989). Eggs and oviposition into plant tissue are similar to that of the Anthocoridae. There are usually five instars but only four in Himacerus apterus Fabricius. This species also differs from most nabids (which apparently overwinter as adults) in that it overwinters in Europe in the egg stage (Koschel, 1971). Most adults of Nabis alternatus Parshley, N. americoferus Carayon, and N. capsiformis (Germar) enter an adult reproductive diapause state during late fall; and at least N. alternatus can have up to five generations in Arizona (Stoner et al., 1975). In alfalfa fields in Kentucky, N. americoferus has three generations, while in soybeans there is only one (Braman & Yeargan 1990), and in Ontario alfalfa fields there are two (Guppy, 1986). Nabids are considered polyphagous or generalist predators, but some may feed on plants. This was first suspected when the heteropteran predators were differentially killed compared with mandibulate predators in cotton treated with systemic insecticides (Ridgway et al., 1967). Laboratory tests demonstrated that N. americoferus and G. pallens feed on the cotton terminals (Ridgway & Jones, 1968). Furthermore, Stoner (1972) found that first instars of N. alternatus, N. americoferus, and N. capsiformis can be sustained on pollens, certain seeds, and legumes, but no nymphal development occurs (compared with geocorines where some development does occur). Nabids fed on cotton leaves alone survived about as long as those exposed only to water. Stoner concluded from comparing the responses of Geocoris and Nabis with plant feeding that Nabis spp. are more predaceous than Geocoris spp. One should be aware that plant feeding, though minor, can involve plant pathogen transmission, because N. alternatus possibly transmits a yeast plant pathogen (Burgess et al., 1983). Nabid prey range is wide among the species studied. Several genera within the subfamily Prostemmatinae are predators of soil-dwelling lygaeid species of the Blissinae, Geocorinae, and Rhyparochromidae (Lattin, 1989). There are at least six Nabis spp. that have received attention as

important natural enemies of agricultural crop pests, and a Himacerus species is considered to be a common predator of forest pests. It appears that no nabids have been intentionally introduced as a natural enemy; however, Anaptus major (Costa), a European species, was introduced into North America, probably in ship ballasts (Lattin, 1989). Himacerus apterus is a common Palearctic species that is predominantly brachyapterous in the adult stage (P6ricart, 1987). In early nymphal instars, it lives on low plants feeding on mites and small insects, and later moves to trees where it feeds on various defoliators (Koschel, 1971). Koschel (1971) made an extensive study of H. apterus that was prompted by observations on its predation of various defoliating moth and tenthredinid larvae infesting pines; it was considered as a candidate predator that could be masscultured and released in forests. However, Koschel concluded it would be too difficult to mass-culture because H. apterus only deposits about 20 eggs per female and is very cannibalistic. Nabis alternatus is a transcontinental North American species (Henry & Lattin, 1988). Taylor (1949) found N. alternatus to be the most numerous insect predator in Utah alfalfa fields, and laboratory studies showed that up to 200 eggs per female were deposited into alfalfa stems. Nymphs consumed an average of 80 pea aphids or 29 lygus bugs to mature; they also fed on thrips and on first- and secondinstar grasshopper nymphs, but died when exposed to alfalfa weevil larvae (Taylor, 1949). An accurate count of the number of Lygus nymphs consumed and required by N. alternatus was made by Perkins and Watson (1972). They found that early-stage nabids successfully preyed on the first 3 lygus instars and only the larger nabid instars were easily able to attack all lygus instars; first-instar N. alternatus require about 7 first-instar lygus nymphs and a fifthinstar nabid required about 91 first-instar nymphs for its development to adult, or a total of about 158 first-instar lygus nymphs for all 5 nabid instars compared with about 57 third-instar nymphs (Perkins & Watson, 1972). Nabis alternatus also is an effective predator of aphids. The "predator power" of N. alternatus was determined by exposing the nabids to green peach aphids on sugar beet plants in field cages under three different temperatures (Tamaki et al., 1981). When nabids insert the eggs into alfalfa stems, only about 5% will hatch if the stems are allowed to dry, while over 55% will hatch if the alfalfa continues to grow (Richards & Harper, 1978). Predation of noctuid eggs and young larvae by N. alternatus was demonstrated by Barry et al. (1974). They used the nabid alone and in comparison with Geocoris punctipes and Chrysoperla carnea in field cages over soybeans infested with H. zea and Trichoplusia ni; the nabid was the only predator that consistently resulted in significantly greater regulation of the pest populations--defoliation, pod damage, and H. zea numbers were all significantly reduced. Nabis alternatus

Chapter 16 Terrestrial Arthropod Predators of Insect and Mite Pests

also is able to grasp flea beetle adults with its front legs and to feed on them (Burgess, 1982). Bjegovic (1968) observed N. feroides Remane catching flea beetles and paralyzing them by injecting saliva; this nabid is also considered to be an important predator of cereal leaf beetle eggs. Nabis americoferus is the most common nabid in North America and was called N. ferus (Linnaeus) in Nearctic literature until Carayon (1961b) distinguished differences between the two species. Developmental rates, consumption rates, and reproductive capacity vary with temperature as well as with diet, and temperature thresholds and degree days required for certain developmental stages can vary with the geographic origin of insect populations. This was pointed out by Braman and Yeargan (1988) where the thermal unit requirements calculated for nymphal development of a population of N. americoferus from Ontario (Guppy, 1986) were nearly 20% greater than for a Kentucky population, though thermal unit requirements for egg stages were similar (Braman et al., 1984). Nymphs fed larvae of the alfalfa blotch leaf miner developed faster than those fed pea aphids (Guppy 1986), and when Bramon and Yeargan (1988) used green bean pods instead of soybean seedlings as an ovipositional substrate, egg production was often lowered in the three nabid species studied. Pea aphids were preferred three times over potato leafhopper nymphs (Flinn et al., 1985). Egg-to-weight relationships suggested that N. americoferus was more efficient at producing eggs than was N. roseipennis Reuter (O'Neil, 1992). Evaluation of predation by N. americoferus in field cages has been conducted against several lepidopteran pests and aphids. In cotton, released nabids appeared to perform more effectively against H. zea than do geocorids or chrysopids (van den Bosch et al., 1969). Releases of a coccinellid, a geocorid, and N. americoferus singly and in combination were made against the green peach aphid, the zebra caterpillar, and the bertha armyworm on caged sugar beets (Tamaki & Weeks, 1972a). The release of Coccinella transversoguttata Feldermann alone and in combination with the other predators was effective in reducing the aphid population. The nabid and G. punctipes were also effective against the aphids but only for about 1 week. The nabids alone and in some combinations were superior to all other treatments in reducing the populations of the noctuid species when these larvae were small. Among other predators in cotton, N. americoferus showed potential as a predator of the pink bollworm (Irwin et al., 1974) and the cabbage looper (Ehler et al., 1973). Nabis capsiformis is a pantropical species and the most widespread nabid known; human activities may have had little or no role in its dispersal because its ability to disperse through flight is well established (Lattin, 1989). In Mississippi, N. capsiformis deposited about 105 eggs per female at 26 to 28~ (Hormchan et al., 1976), and about 200 eggs per female at 28~ (Hormchan et al., 1976); in Queensland,

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Australia, females deposited about 200 eggs (Samson & Blood, 1979). A life table was produced at both locations. In Australia, Samson and Blood (1980) compared the voracity and searching ability of N. capsiformis with Chrysopa signata Schneider and Micromus tasmaniae (Walker) as predators of Heliothis pests associated with cotton; the adult female N. capsiformis and third-stage C. signata were the most voracious predatory stages while the Micromus consumed few H. punctigera Wallengren eggs or young larvae. The searching efficiency of second-instar C. signata was more efficient than third-instar N. capsiformis, while third-instar M. tasmaniae attacked very few eggs (Samson & Blood, 1980). In soybean fields in the southeast United States, N. capsiformis is one of five species of Nabis present in fields by early July and remains abundant during the growing season (Funderburk & Mack, 1989); in Florida soybean fields, N. capsiformis was the major consumer of small velvet bean caterpillar larvae, Anticarsia gemmatalis Htibner (Godfrey et al., 1989). Buschman et al. (1977) also found in Florida soybean fields that chrysopids, spiders, and three Nabis spp. were the most frequently recorded consumers of radioactive eggs of the velvet bean caterpillar. Nabis ferus is a common Palearctic species (Carayon, 1961b). It occurs commonly in grasses, bushes, and low crops. Herard (1986) lists prey of N. ferus noted in recent literature; the list included aphids on many plants, lygus in strawberries, noctuid eggs and larvae in cotton, Colorado potato beetle larvae, dipteran larvae, and thrips; the majority of these references are in Russian. Nabis roseipennis is widespread east of the Mississippi River but also extends westward through Colorado into British Columbia (Slater & Baronowski, 1978). It was one of the first nabids whose biology was studied. Mundinger (1922) described the immature stages and gave details on oviposition into grass stalks: the nabid first probed near the top of the stalk with her proboscis and then deposited an egg into the stalk. Isenhour and Yeargan (1982) found N. roseipennis most often oviposited in median leaflet petioles of soybeans and noted stratification of oviposition sites along the vertical aspect of the soybean plant by Orius and Nabis. In Kentucky soybean fields, N. roseipennis produced the greatest number of nymphs compared with N. americoferus and N. rufusculus Reuter; all three species were also present in alfalfa fields (Braman & Yeargan, 1990). Like other previous Nabis spp. mentioned, N. roseipennis is a generalist. It is a common predator of lepidopteran eggs and larvae such as the green clover worm in the laboratory and soybeans (Sloderbeck & Yeargan, 1983; Yeargan & Braman, 1989), soybean looper in soybeans (Richman et al., 1980), H. zea on cotton (Donahoe & Pitre, 1977), and H. virescens on cotton (Nadgauda & Pitre, 1987). In the laboratory, the nymphs and adults survived and matured satisfactorily on small Heliothis larvae, but development was slow compared with feeding on larger

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larvae, which accelerated development and maintained a high growth potential (Nadgauda & Pitre, 1987). Predation rates on Lygus nymphs were determined in the laboratory at different temperatures by Nadgauda and Pitre (1986). Predatory rates of N. roseipennis were also determined by laboratory feedings of potato leafhopper nymphs and adults, while peak populations of four Nabis spp. monitored in alfalfa fields coincided with the peak density of the leafhopper (Rensner et al., 1983). Although the nabid attacked third-instar larvae of the boll weevil, it would not attack third-instar Mexican bean beetle larvae (but did eat its eggs) (Wiedenmann & O'Neill, 1990b). Nabis rufusculus is very similar to N. roseipennis in morphology, biology, and distribution (Mundinger, 1922). It occurs in Kentucky alfalfa and soybean fields. In soybeans it has one generation per year: sweep sampling recovered fewer nymphal nabids in comparison with suction or shake sampling, and thus was less satisfactory in assessing population trends (Braman & Yeargan, 1990). Pentatomidae This is one of the largest families of Heteroptera with over 2500 described species (Miller, 1971). The family contains many phytophagous pests, but there are also a few important predaceous species that have been involved in biological control projects. The predaceous species all belong to the subfamily Asopinae, which has over 300 species in 27 genera in the New World (Thomas, 1992); very few, if any, are prey specific, and the first-instar nymphs often feed on plant liquids (Esselbaugh, 1949; Froeschner, 1988). Ishihara (1941) reviewed the feeding habits of predaceous Heteroptera, particularly the Pentatomidae; and in his table of 27 asopine species in 20 genera, 18 are listed as preying on Lepidoptera (mainly larvae), 15 on coleopteran larvae, 7 on hymenopteran larvae, 6 on Hemiptera, 3 on Diptera, and 1 on a neuropteran larva. Most of the species listed by Ishihara fed on species in more than one insect order. Over 90 insect species have been reported as prey of Podisus maculiventris (Say) (McPherson, 1980). Predaceous pentatomids deposit clusters of barrel-shaped eggs with elongate chorionic processes that ring the opercular cap on plant surfaces (Esselbaugh, 1949). When the nymphs hatch, they often remain clinging to their eggshells until the first molt. There are five nymphal instars and each instar can be of different color. Saini (1985, 1988) has published color photographs of all stages of 19 (including 5 predaceous) pentatomid species occurring in Argentina-some of which range into North America. When a prey is detected, the nymphs and adults extend their broad rostra directly forward in an attempt to pierce it and inject paralyzing enzymes, but the success of the attack and subduing the victim varies between the prey species (Marston et al., 1978) and the age of the predator (Morris, 1963). Overwintering occurs in either the egg or adult stage depending on

the species. Predators that were fed less frequently laid fewer eggs, less often and later in life (Wiedenmann & O'Neil, 1990a). The following asopine species are some that have been studied as biological control agents, have been considered as potential natural enemies, or have been imported to control specific introduced pests. Andrallus spinidens (Fabricius) is a circumtropical nonspecific predator of lepidopteran larvae. In rice fields in West Malaysia, where its abundance coincided with outbreaks of Melantis leda (Linnaeus), Manley (1982) concluded that the predator was of limited importance at low prey densities but of much greater value at outbreak densities because of the short life cycle and continuous feeding habit of the predator. In India, A. spinidens was observed feeding on the noctuid Rivala sp. infesting soybeans by Singh and Singh (1989), who also studied its biology. Apateticus crocatus (Uhler) is a North American species and is considered an important predator of Malacosoma spp. and Ellopia somniaria Hulst caterpillars in Victoria, British Columbia The fifth instar refused animal food, preferring plant juices (Downes, 1921). Apateticus cynicus (Say), a North American species that is univoltine, overwinters in the egg stage and produces few eggs; thus, it is not considered an outstanding predator (Jones & Coppel, 1963). Eocanthecona furcellata (WolD, an Asian and Pacific Island species, was released in Florida against the Colorado potato beetle and the eastern tent caterpillar in 1981, but by 1988 recovery had not yet been reported (Froeschner, 1988). Li et al. (1988) developed an artificial diet for this generalist predator. The functional response of the predator with Lotoia lepida (Cramer) as prey was measured in India (Senrayan, 1988). There is greater larval survival when exposed to leaves and prey than on prey ~/lone (Senrayan, 1991). Eocanthecona furcellata can be reared on frozen moth larvae (Yasuda & Wakamura, 1992). Euthyrhynchus floridanus (Linnaeus) ranges from the southeastern United States to Brazil. A biology of this nonspecific predator was determined by feeding it Agrotis ipsilon (Hufnagel); its developmental period was longer than any other asopine (Oetting & Yonke, 1975). It is found in soybean fields and overwinters in the adult stage. It was reared on larvae of Galleria mellonella (Linnaeus) but also fed on H. virescens larvae and on all stages of Epilachna varivestis Mulsant (Ables, 1975). Like Alcaeorrhynchus grandis (Dallas), the egg stage is prolonged in E. floridanus, being 19 days in the former and 16 days for the latter compared with about 5 days for P. maculiventris, when reared under similar conditions (Richman & Whitcomb, 1978). Oechalia schellembergii (Guerin-Menville), an asopine species occurring in Australian alfalfa and cotton fields, is a natural enemy of H. punctigera. First-instar nymphs molted to the second instar if alfalfa stems were present but

Chapter 16 Terrestrial Arthropod Predators of Insect and Mite Pests

not if their own eggs or eggs of H. punctigera only were available, and the second instar did not develop to the third instar on alfalfa stems alone (Awan, 1987). Awan et al. (1989) found that female O. schellembergii took relatively less time to locate wandering fourth-instar larvae of H. punctigera than stationary larvae and that movement of prey increases attack frequency. They also reported the predators responded positively to prey larval frass; predators with blocked vision and olfaction searched sporadically with extended rostra and used their front tarsi to locate prey. It is interesting that Trissolcus basalis (Wollaston), the parasitoid successfully introduced against Nezara viridula (Linnaeus), also parasitized the eggs of O. schellembergii as well as another asopine predator (Cermatalus nasalis Westwood) in alfalfa fields in South Australia (Awan, 1989). Perillus bioculatus (Fabricius), a widely distributed Nearctic species, has received much attention as a natural enemy of the Colorado potato beetle, Leptinotarsa decimlineata (Say), particularly in Europe where the beetle has invaded. Tamaki and Butt (1978) constructed life tables and determined the feeding potential of the different life stages of the predator and the amount of potato leaf foliage consumed by the larvae and adults of the beetle; thus, given the number of life stages of the predators and defoliators, the amount of predation and defoliation can be predicted. The predator overwinters as an adult and feeds on eggs and larvae of the potato beetle, and deposits about 100 eggs per month. The first instar feeds on the plant while later nymphal stages are essentially predaceous and complete development in about a month after consuming over 400 beetle eggs (Knight, 1923; Landis, 1937). Frozen potato beetle larvae can be used to rear the predator nymphs but not egg-laying females; however, permanent rearings can be made using frozen pupae (Franz, 1967). The predator was introduced into France (Trouvelot, 1932), Germany (Franz & Szmidt, 1960), Hungary (Jermy, 1962), Russia (Beglyarov & Smetnik, 1977), Czechoslovakia (Tadic, 1964), and Italy (Tremblay & Zouliamis, 1968), but appar: ently never became permanently established in Europe (Szmidt & Wegorek, 1967; Beglyarov & Smetnik, 1977; Jermy, 1980) because it could not overwinter successfully: thus, periodic colonization of the predator is called for (Szmidt & Wegorek, 1967). In small-plot field studies in Delaware, releases of P. bioculatus in conjunction with bacterial insecticides provided significant control of the beetles for at least 2 weeks, suppressing larval populations by 76% compared with plots treated only with bacterial insecticide (Hough-Goldstein & Keil, 1991). Release of nymphs at either 1.6 per row-meter or 9.8 per row-meter significantly reduced the number of L. decimlineata larvae in small plots, and the number of beetle egg masses was significantly reduced by the higher release rate or by the lower release rate in combination with a bacterial spray

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(Hough-Goldstein & Whalen, 1993). Biever and Chauvin (1992a) obtained 30 and 62% reduction of the Colorado potato beetle populations by releasing one to three P. bioculatus per plant, respectively, and the same authors (1992b) obtained best results by releasing the predator 4 days after potato plant emergence. Picromerus bidens (Linnaeus) is a common Palearctic asopine species that was inadvertently introduced into North America about 50 years ago and is now found in Quebec and the northeastern United States (Javahery, 1986; Froeschner, 1988). Lariviere and Larochelle (1989) made a world review of the distribution and bionomics of the predator. It is univoltine and overwinters primarily in the egg stage. Picromerus bidens occurs on a wide diversity of plants; in Europe it has been recorded on over 30 plant species and over 50 in North America. Its prey range is also broad because it has been reported attacking over 35 different insect species in six orders. If there is any preference for certain prey, it may be defoliating Symphyta of the Hymenoptera. According to Lariviere and Larochelle (1989), many authors have indicated the importance of this predator in reducing various insect pest populations, particularly tenthredinids and diprionids. Mayne and Breny (1948) found P. bidens not to be a good control agent of the Colorado potato beetle in Europe because the predator did not disperse easily in the fields and was too much of a generalist predator, while Javahery (1986) noted that its low rate of reproduction was another weakness. There are some early references to P. bidens being an effective predator of bedbugs (Clausen, 1940). Podisus spp. have attracted much attention of biological control researchers. The genus is widespread in the New World, and most species are generalist predators. Coppel and Jones (1962) compared the biologies of four Podisus spp. associated with the introduced sawfly Diprion similis (Hartig) in Wisconsin and found their biologies quite similar. One of the species was P. maculiventris. Podisus maculiventris occurs transcontinentally in North America and has been exported to Europe and Korea (Froeschner, 1988). It also was sent to China in 1983 from the United States, but as of 1987 no recoveries had been made (Wang & Gong, 1987). It overwinters as an adult in deciduous woods and their borders (Jones & Sullivan, 1981). Among the 90 prey species listed by McPherson (1980) that were taken from the literature, the main prey consisted of about 50 species of Lepidoptera, 17 of Coleoptera, and 6 of Symphyta (Hymenoptera). Both prey defense by large webworms and age of the adult P. maculiventris had important effects on the functional response curves (Morris, 1963). Mukerji and LeRoux (1969a, 1969b, 1969c) exposed different size wax moth larvae to different stages of P. maculiventus and measured resulting functional responses. They found that prey size was an important component of the predation process for all stages of the

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predator. These authors also studied the energetics of P. maculiventris using wax moth larvae as prey. Warren and Wallis (1971) fed frozen fall armyworm and tent caterpillar larvae and live wax moth larvae to P. maculiventris and determined duration from egg to adult at four different temperatures m at the lowest (50~ no development occurred. From one field-collected female, 1174 eggs were laid in 126 days. Comparable sized larvae of five different lepidopteran species that attack soybeans were exposed on soybean plants to fifth-instar P. maculiventus nymphs, but no significant effect on the ability of the predator to contact any prey of the larvae was found; however, once contact was made, the behavior of the prey larvae significantly affected the ability of the predator to subdue them (Marston et al., 1978). Marston et al. (1978) concluded that in pest management programs involving releases of P. maculiventris, the mortality of prey larvae will vary between species (e.g., H. zea), with mortality of about 60% being considered intermediate of the five pest larval species tested. Lopez et al. (1976) found third-instar nymphs and adults of P. maculiventris were the most efficient predators of third-instar larvae of H. zea and H. virescens compared with a coccinellid, a chrysopid, and a geocorid species. Releases of P. maculiventris adults at a rate of 100,000 per acre in field cages over cotton resulted in a substantial reduction of H. virescens larvae (Lopez et al., 1976). Releases of adult predators in greenhouse cotton naturally infested with Peridroma saucia (Huebner) larvae resulted in 75% of the cutworm larvae being consumed within 48 h (Ables & McCommas, 1982). Podisus maculiventris that was contaminated with Trichoplusia ni single-embedded nuclear polyhedrosis virus was released in field cages containing cabbage looper larvae and initiated virus infections and epizootics in 3 to 4 weeks (Biever et al., 1982). There are some insecticides that are compatible with P. maculiventris. The predator is generally more susceptible to organophosphorus and carbamate insecticides than to the velvet bean caterpillar, fall armyworm, or corn earworm, but is more tolerant of certain pyrethroids (Yu, 1988). Coleopteran prey, such as Tenebrio molitor Linnaeus, were exposed as small and large larvae at different intervals to P. maculiventris in the laboratory to determine the influence of low prey inputs on survival and reproduction; the predators provided with prey survived regardless of feeding interval, but those predators fed less frequently and laid fewer eggs less often and later in life (Wiedenmann & O'Neil, 1990a). The predator survives long periods without prey and adjusts its weight loss by reducing reproductive effort when prey becomes scarce (O'Neil & Wiedemann, 1990; Legaspi & O'Neil, 1993). Larger P. maculiventris females laid eggs at younger ages and more frequently than smaller females (Evans, 1982a), but smaller species of asopines, like Perillus circumcinctus St~l that is a specialist

predator on certain chrysomelid larvae, exploit the prey populations more effectively than the generalist Podisus maculiventris. Evans (1982b) concludes the key difference in the habits of the two predators is in timing of reproduction. Well-timed oviposition by specialist females ensures that offspring mature when prey are easily harvested. In contrast, the poor timing (late oviposition) by the larger generalist female results in most offpsring facing a prey shortage of chrysomelid larvae in the system investigated. A major attempt to introduce P. maculiventris into France to control the introduced Colorado potato beetle was made in the 1930s, but the predator did not become established. Couturier (1938) believed that in France the relative dryness of the summer months was the chief obstacle to the establishment of the bug. However, Drummond et al. (1984) evaluated Colorado potato beetle larvae as prey compared with larvae of Galleria mellonella, Epilachna varivestis, and Malacosoma americanium (Fabricius), finding that this potato beetle was a suboptimal prey because the survival of P. maculiventris decreased and its developmental time increased. In the former USSR, releases of second and third instar P. maculiventris in fields at predator to prey ratios of 1:10 to 1:30 (amounting to 210,000 predators perhectare) in early potatoes resulted in good control of the Colorado potato beetle, and three releases of 100,000 predators perhectare on eggplants during the summer amounted to 90 to 100% control and a yield of 37,400 kg compared with 4,500 kg in untreated control fields (Khloptseva, 1991). To increase the retention of released P. maculiventris adults against E. varivestis in snap bean plots, the adult female predators were dewinged; significantly fewer E. varivestis larvae were found on the plants treated with released predators over a 21-day period and a higher yield of snap beans was obtained. Lambdin and Baker (1986) obtained the reduction by releasing 5 or 10 adults per 3.1-m plots. A release of five P. maculiventris per cage significantly reduced the 50 E. varivestis fourth instars placed on soybeans in small field cages, but Waddill and Shepard (1975) found that P. maculiventris did not reach adulthood when fed only eggs or first instars of E. varivestis, but the predator matured when fed later instars or pupae of the beetle. These authors also obtained the usual functional response curves. In caged field soybeans infested with E. varivestis, O'Neil (1988) estimated the area searched by P. maculiventris by calculating the number of prey attacked and the number of prey available for attack and leaf area. As leaf area increased, the predator searched a larger area. When O'Neil (1989) compared the functional response of P. maculiventris in both the laboratory and field, the low number of attacks in the field suggested that the influence of handling time was trivial and that predation was associated primarily with the predator's ability to find prey in the soybean canopy. Applying the results of the laboratory study to a field

Chapter 16 Terrestrial Arthropod Predators of Insect and Mite Pests

setting is difficult because of the differences in the relative magnitudes of prey density and corresponding attack rates between laboratory and field results (O'Neil, 1989), but a more detailed search model was developed based on varying E. varivestis larvae as prey exposed on different size field-caged plants to adult P. maculiventris (Wiedenmann & O'Neil, 1992). Male P. maculiventris produce a long-range aggregation pheromone that was identified and synthesized by Aldrich et al. (1984). A similar type of pheromone was found in P. fretus Olsen by Aldrich et al. (1986). In both cases, the aggregation pheromones became kairomones because four species of natural enemies were attracted to the artificial pheromones (Aldrich, 1988). Life history studies have been made of nearly all the North American Podisus spp., and their biologies are similar to P. maculiventris. However, the distribution and prey range does vary somewhat between species. Podisus modestus (Dallas) is a northern arboreal forest species that preys on sawfly defoliators of conifers (Coppel & Jones, 1962; Tostowaryk, 1971). Podisus placidus Uhler is a midwest to eastern species that preys mainly on lepidopteran larvae and sawfly larvae (Coppel & Jones, 1962; Oetting & Yonke, 1971), and was considered for introduction into Yugoslavia to control the fall webworm (Tadic, 1964). Podisus sagitta Fabricius occurs from the southern United States to Brazil and it naturally feeds on Epilachna larvae in Mexico. DeClereq and Degheele (1990) reared it on wax moth and beet armyworm larvae, and like most asopines, it took about 1 month to develop from egg to adult and to deposit about 600 eggs; lower threshold temperatures for egg and nymphal development were estimated as 13.3 and 12.2~ for P. sagitta, and for P. maculiventris, 10.7 and 11.7~ respectively (DeClereq & Degheele, 1992a). These same authors (1992b) reared both predators on a bovine meat diet. Podisus serieventris Uhler ranges from the midwestern to eastern United States and from British Columbia to Nova Scotia in Canada (Froeschner, 1988). Its population increased and decreased in conjunction with an outbreak of black-headed budworm on conifers in Nova Scotia (Prebble, 1933). Coppel and Jones (1962) collected it from pines infested with sawflies. In Brazil, entomologists are evaluating the role of asopine species as predators of defoliators in various crops and forests. Among the natural enemies of geometrid larvae infesting eucalyptus trees, Alcaeorrynchus grandis, P. connexivus Bergroth, P. nigrolimbatus Spinola, and Thynacanta marginata (Dallas) are involved (Berti Filho & Fraga, 1987; Zanuncio et al., 1989). In Brazil, T. marginata is common in soybean fields, P. maculiventris is found in cotton fields, and A. grandis is found in cassava fields (Grazia & Hildebrand, 1987). In Argentina soybean fields, four predaceous pentatomids (P. nigrolimbatus, P. nigrispinus Dallas, Oplomus cruentus (Burmeister), and Stiretrus

4 | |

decastigma Herrich-Schaeffer) are found and their eggs can be distinguished from eight phytophagous pentatomids found in soybean fields (Saini, 1984); and the biology and morphology of the latter two species are described by Saini (1989). Podisus nigrolimbatus is also a predator of Pyrrhalta (= Xanthogaleruca) luteola (Muller), which defoliates elms in Argentina (Artola et al., 1983). Goncalves (1990) determined predatory capacities of Podisus connexivus and P. nigrolimbatus in the laboratory and reviewed the literature dealing mainly with Neotropical asopine species. Stiretrus anchorago (Fabricius) ranges from Kansas in the west to the east coast of the United States and south to Panama; its color becomes darker to the south and is called variety fimbriatus (Froeschner, 1988). Its immature stages were described by Oetting and Yonke (1971). This species may be more narrow in its prey associations compared with most known asopine species. At least compared with P. maculiventris, S. anchorago is more selective of the prey it eats (Waddill & Shepard, 1975). It has been reported to be the most numerous pentatomid attacking E. varivestis in Mexico; in the laboratory it feeds voraciously on E. varivestis but is reluctant to feed on Galleria mellonella. It feeds on alfalfa weevil larvae, Hypera postica (Gyllenhal), but even though it completes its development to adult, the predator does not oviposit (Richman, 1977). Waddill and Shepard (1974b) determined the duration of the S. anchorago stages at three different constant temperatures and like P. maculiventris, it completes its life cycle in about 1 month (Richman & Whitcomb, 1978). Also like P. maculiventris, the males produce an aggregation pheromone that attracts both sexes and nymphs, and the pheromone has been identified and synthesized (Kochansky et al., 1989). Phymatidae The biology of this family is similar to the Asopinae in that both deposit eggs in groups on plant surfaces and have five nymphal instars. The biology of only one species has been studied in detail. Balduf wrote 10 articles on the biology and quantitative food habits of Phymata americana Melin, a common North American species. Based on his recording of over 830 different insect prey species of this predator, which sits and waits in fresh flowers that possess nectar and pollen, Balduf (1948) made a summary of his studies and concluded that the phymatid attacked beneficials as well as pests. Reduviidae This is one of the larger families of Heteroptera. Most known species are predaceous, mostly on insects, but some suck blood from birds and mammals. The biology and ecology of many subfamilies are poorly known (Miller, 1971). Readio (1927) is still one of the best general references to the biology of the Nearctic species. Most species appear to be generalist predators in their habitats, which can be restrictive and thus narrows the prey range.

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They kill their prey by injecting saliva when piercing the body of the prey with their stylets, and practice preoral digestion of the prey's internal structures, whose liquefaction permits ingestion (Cohen, 1993). Motion and form of the prey are the main stimuli for attack by some reduviids (Parker, 1971), and motion plus a kairomone is necessary to induce attack of others [e.g., Phonoctonus fasciatus (Palisot de Beauvois) and P. subimpictus St~l preying on the cotton stainer Dysdercus superstitiosus (Fabricius) in Nigeria (Parker, 1972)]. The species of Emsinae have raptorial front legs and are essentially ambush-type predators, but some are highly specialized predators of spiders and use the spider webs to find their prey (Snoddy et al., 1976). Apparently, some species in the Apiomerini smear plant resins on their front tibiae to help capture prey (Miller, 1971). Some reduviids prey on termites: Salyavata variegata Amyot & Serville nymphs coat themselves with termite nest crumbs and debris for protection, and also use spent carcasses of freshly killed Nasutitermes species as bait to attract more termites (McMahan, 1983). Reduviid eggs are deposited singly or in groups and may be partially covered with a glutinous substance by the female. Inoue (1986) found that the ovipositional sites for Agriosphodrus dohrni Signoret are selected based on the architectural structure of plants (in cherry trees) and height above ground. These sites provide protection from storms in Japan and hibernation sites for nymphs. The females actively select a density-dependent ovipositional site. There are five nymphal instars. Nearctic species may have several generations a year but usually there is only one, and overwintering can occur in any stage depending on the species (Readio, 1927). Readio (1927) summarized the beneficial effects of Reduviidae, believing that the family is of considerable importance even though he knew of only a few cases where a harmful insect was controlled solely by reduviids. Because reduviids are mainly generalist predators, have low fecundity, and are usually monovoltine, their importance as natural enemies of insect pests is limited. There are 31 subfamilies of Reduviidae recognized in the world faunas (Davis, 1969; Miller, 1971), and in North America there are 10 subfamilies (Froeschner, 1988). At least three contain species that have been involved in applied biological control research. These are the Harpactorinae, Peiratinae, and Reduviinae.

Harpactorinae This is the largest subfamily and contains most species that have been studied as natural enemies. Most of these species are in the genera Apiomerus, Arilus, Montina, Sinea, Sycanus, and Zelus. Apiomerus crassipes (Fabricius) adults, like many phymatids, visit flowers in search of prey; therefore, usually more beneficial insects are prey than are pests (Swadener & Yonke, 1973; Bouseman, 1976). Nymphs have rarely been observed in the field but were reared in the laboratory.

The tibiae of the forelegs have long setae coated with a sticky substance produced by secreting glands of the tibiaemthe substance did not come from plant resins because plants were not involved in the rearing (Swadener & Yonke, 1973). An adult of A. crassipes was observed feeding on the Florida harvester ant in the field and fed on ants and on Diabrotica adults in the laboratory (Morrill, 1975). Apiomeris spissipes (Say) adults prefer Coleoptera and Diptera but little is known about what nymphs feed on in the field. Readio (1927) found nymphs under rocks. Cade et al. (1978) observed A. spissipes capturing harvester ants along their foraging trails and at the periphery of their nests; about 29% of the Pogonomyrmex nests examined in Texas had reduviids present. Arilus cristatus (Linnaeus), the wheel bug, is one of the largest and most easily recognized assassin bugs and has a painful bite if handled carelessly. This generalist predator ranges from Illinois in the West to the East coast. It is commonly found in fruit and nut trees and also in flowers (Readio, 1927; Underhill, 1954) and soybean fields (McPherson et al., 1982). Montina confusa (St~l) is commonly found feeding on lepidopteran defoliators in Brazilian eucalyptus forests. Its biology and morphology were examined in the laboratory by rearing it on Galleria mellonella (Bueno & Berti Filho, 1984a, 1984b). The genus Sinea is mainly Nearctic but there are a few Neotropical species. Of the 11 North American species (Readio, 1927; Froeschner, 1988), the biologies of only 3 have been studied in detail. Sinea confusa Caudel occurs in the southwest and ranges to Central America. It is the most common reduviid found in Arizona crops (Werner & Butler, 1957). Duration of development of eggs and nymphs was determined at five different constant temperatures by Butler (1966), and Fye (1979) measured the prey preferred and quantities eaten of Lygus hesperus Knight, Aphis gos-

sypii, Heliothis zea, Trichoplusia ni, Pectinophora gossypiella, and Bucculatrix thurberiella Busck; and looked at the searching ability in petri dishes and on artificial cotton plants. Fye (1979) concluded that S. confusa is an indiscriminate feeder and because of the small numbers of adults usually present in cotton fields, their overall impact, even though they feed on a large number of cotton pests, is limited. Generally the feeding by the predators in their various instars was proportionate to the size of the prey and predator. Sinea diadema (Fabricus) is one of the most common North American reduviids, and is distributed throughout most of the United States (Slater & Baranowski, 1978). Balduf and Slater (1943) added to the biology of that contributed by Readio (1927). In Illinois it overwinters in the egg stage and completes two generations a year. In addition to the 14 prey species recorded in the literature, Balduf and Slater (1943) observed 19 additional prey species attacked. Balduf made extensive studies on weights of prey (adult

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

Drosophila flies) ingested compared with weights gained by S. diadema nymphs, and found that assimilation is inversely proportional to the amount of food ingested, while elimination (fecal wastes) is directly proportional to the quantity of prey ingested (Balduf, 1950). Sinea spinipes (Herrich-Schaeffer) occurs from Colorado and Texas in the West to the East Coast; its biology was extensively investigated by Readio (1927). It overwinters as an adult and has one generation a year. Its nymph preys on nymphs of phytophagous pentatomids, fall webworm larvae, and other caterpillars in fruit, nut, and forest trees. Sycanus, an Asiatic genus, contains several species that have been utilized in applied biological control. According to Rao et al. (1971), S. leucomesus Walker was introduced into tea plantations in the Cameron Highlands of Malaysia from the lowlands in 1940 to prey on two mirid pests, Helopeltis bradyi Waterhouse and H. cinchonae Mann. The predator became established along with two other introduced reduviids, Isyndus heros (Fabricius) and Cosmolestes picticeps St~l. Simultaneously, two other reduviids, Euagorus plagiatus Burmeister and Rhinocoris marginalis Thunberg, were introduced but did not become established; and three endemic reduviids in the highlands, Endochus cameronicus Miller, Isyndus, sp., and Euagorus sp., were reared and released. The degree of control of the tea mirid pests by the reduviids is uncertain (Rao et al., 1971). Sycanus indagator (Walker) was imported from India and its feeding behavior was studied in the laboratory (Bass & Shepard, 1974). It was released in field cages in Florida soybean fields as a predator of Pseudoplusia includens and in field cages over cabbage plants infested with T. ni. Greene and Shepard (1974) concluded from laboratory and field studies that survival and larval consumption were too low to suggest success of the predator in Florida cabbage or soybean fields. It apparently did not become established (M. Shepard, personal communications, 1992). The genus Zelus is distributed throughout the tropical and temperate areas of the Western Hemisphere; and there are nine species found in the United States, Canada, and northern Mexico (Hart, 1986). The three species that have received the most attention are Z. luridus St~l, Z. renardii Kolenati, and Z. tetracanthus St~l. Zelus luridus is the valid name for the species referred to as Z. exsanguis Uhler in the biological literature; the latter species occurs only south of the United States, except perhaps southern Texas (Hart, 1986). Zelus luridus occurs in Arizona and Colorado in the West and extends to the East Coast. In Kansas, it overwinters as a nymph curled up in a leaf on the ground in some protected place and has one generation per year (Readio, 1927). West and DeLong (1955) found large nymphs overwintering in Ontario, Canada, and observed that the bug did not feed on plants but was a generalist predator of aphids and large tent caterpillars. These authors believed cannibalism was probably a

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necessity for the first-instar nymphs. After feeding on caterpillars infected with microsporidia, Zelus excreted viable spores that infected caterpillars feeding on contaminated foliage (Kaya, 1979). Zelus renardii is found in the southwestern United States and extends south to Guatemala, but also has been inadvertently introduced to the Hawaiian and Philippine Islands, Johnston Island, and Samoa (Hart, 1986). It is a generalist predator with the nymphs commonly feeding on aphids, leafhoppers, and thrips, while the adults will eat any arthropod that they can catch and hold. Furthermore, Z. renardii or Nabis spp. were observed to severely reduce survivorship of lacewing larvae (Rosenheim et al., 1993). Butler (1966) determined duration of stages influenced by five different temperatures, and Mbata et al. (1987) studied its reproductive behavior. Fye (1979) researched the same biotic factors of Z. renardii that he investigated for Sinea confusa and found he could not rear first-instar Z. renardii on bollworm eggs, but Lingren et al. (1968) observed adults to consume about 42 bollworm eggs or 75 first instars per day. In Hawaii, because Z. renardii had been involved in reducing sugarcane leafhopper populations at times, it is called the leafhopper assassin bug (Zimmerman, 1948). Zelus tetracanthus (= socius Uhler) ranges from southern Canada to Brazil and Paraguay (Hart, 1986). As common as this assassin bug is, apparently not much is known about its biology; however, Butler (1966) did determine duration of eggs and nymphal stages at five different temperatures.

Peiratinae This subfamily is composed of three genera in North America (Melanolestes, Rasahus, and Sirthenia) and embraces only a few species. These species are nocturnal and mainly ground dwellers but are attracted to lights and can inflict a painful bite. Their biologies are poorly known (Readio 1927). Apparently, the best known biology is of M. picipes (Herrich-Schaeffer), which was described by Readio (1927). He exposed many different insects that are found under rocks to adult M. picipes but the assassin bug only ate scarab larvae; Readio believed the nymphs also may be restricted to such prey. Eggs of the predator are deposited under rocks. Reduviinae This subfamily contains many nocturnal species, and their biologies are poorly known. One species, however, has been introduced into many tropical places. Platymerus laevicollis Distant (= P. rhadamanthus Gerst), an east African species, is a generalist predator, but because its habitat is more or less restricted to crowns of palms and its adults attack adult Oryctes spp., it was considered a potential natural enemy of O. rhinoceros (Linnaeus) (Vanderplank, 1958). It was first sent to India from Zanzibar, and later to Mauritius, Pakistan, Malaya, and 10 Pacific islands (Greathead, 1971; Rao et al., 1971) but apparently became established only in the Laccadive Islands (Water-

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house & Norris, 1987). It has a painful bite if handled carelessly (Miller, 1971).

Superorder Neuropteroidea The 4500 or so species of lacewings in the world are divided into three orders. Because Megaloptera are aquatic in their larval stages, the alder and dobson flies will not be discussed here. All larvae of Neuropteroidea are apparently predaceous. A key to the larvae of all families of Neuropteroidea is nicely presented by Gepp (1984a), and Gepp (1990) illustrates the eggs of lacewing families. The food habits of adult Neuropteroidea are mostly predatory but some feed only on honeydew nectar or pollen. The monograph by Killington (1936, 1937) on British Neuroptera, the extensive revision by Asp6ck et al. (1980) of the Neuroptera of Europe, and the reviews found in the neuropterology series edited by Gepp et al. (1984, 1986) and by Mansell and Asp6ck (1990) provide the bases for knowing this important group of insects. Also, the review of the biology of Neuroptera by Balduf (1939) is an extensive and valuable reference. The two orders discussed here are the Raphidioptera and Neuroptera (= Planipennia).

Order Raphidioptera Asptck (1986a) reviews the present knowledge of snake flies of the world, noting that the distribution of the two families Raphidiidae and Inocelliidae is essentially Holarctic. The adults and larvae are mandibulate general predators living mostly in arboreal habitats. The elongate eggs are usually deposited in groups in bark crevices, and the flatish larvae search for arthropods found under loose bark or on trunks and branches of trees, though some larvae live in the soil. The adults hunt for the smaller insects associated with trees and bushes. The generation time is usually 2 or 3 years. Tauber (1991b) reviews the biology and presents a key to the larvae of both families. Asptck (1986a) mentions the unclarified economic significance of Raphidioptera and points out that these insects may act as effective predators of phytophagous arthropods living in and on forest and fruit trees and believes these predators could be introduced into areas where snake flies do not occur naturally, particularly in the Southern Hemisphere. About 90 years ago, a Raphidia sp. from California was sent to New Zealand to control the codling moth, but it did not become established (Clausen, 1978).

lnocelliidae Little biological information is known about this family that contains five genera and 17 species, though Asptck (1986a) states that the species in this family are arboreal and have longer larval periods requiring 3 years to complete their development. Asptck et al. (1974) and Tauber (1991a) discuss details on larval biology and morphology.

Raphidiidae The 26 genera of this family embrace 151 species that live in forests and orchards (with some larvae found in the soil) (Asptck et al., 1974, 1975; Asptck 1986a). Woglum and McGregor (1958) describe the biology and morphology of Agulla bractea Carpenter and the biology of A. astuta (Banks) in 1959. The larvae of both species were observed in the field preying on black scale eggs and crawlers on citrus trees in southern California. The adult snake flies were also collected in the citrus trees. The biologies of both Agulla spp. were found to be similar. The adults were fed black scale crawlers and aphids and deposited batches of eggs in about a week; first-instar larvae did not feed, and there were 10 or 11 instars. Development could be completed in 1 year if larvae were exposed to the cool temperatures during winter. If kept under warm conditions, the larvae did not pupate. Some larvae completed development in 3 years if finally exposed to a cold period. All stages and the larval morphology are described for both species (Woglum & McGregor, 1958, 1959). Order Neuroptera The 4000 or so species of lacewings in the order Neuroptera compose 17 families that until recently were placed in the suborder Planipennia (Asptck et al., 1980; Gepp, 1984a; New, 1989; Tauber, 1991a). Their eggs are broadly oval with a conspicuous micropylar knob and often are placed at the end of silken threads. The eggs are deposited singly or in groups, usually near prey. Most families have campodieform larvae with three instars. All larvae are predaceous and have sucking and piercing mouthparts; they pupate in silken cocoons. Most adults are predaceous, while quite a few feed on honeydew, nectar, and/or pollen; and a few do not feed at all (Withycombe, 1923; Balduf, 1939; Clausen, 1940; Sweetman, 1958; New, 1975). The Neuroptera that are predaceous on aphids are reviewed by New (1988b; those that are predaceous on coccids, by Drea (1990a). The Neuroptera used to control arthropods in apple orchards are reviewed by Principi and Canard (1974), and Szabo and Szentkiralyi (1981); and in pear orchards, by Herard (1986). The main families that contain species involved in applied biological control are Chrysopidae, Coniopterygidae, and Hemerobiidae. Berothidae is included here because some of its species are predaceous on termites, and are potentially useful as biological control agents.

Berothidae The Berothidae family has 78 species of beaded lacewings in eight genera that are mainly tropical with only one genus occurring in Europe and one genus, in North America. Asptck (1986b) presented the state of knowledge of the family, including the biology of the only species known in any detail, Lomamyia latipennis Carpenter. It was reared on Zootermopsis angusticollis Hagen and

Chapter 16

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the three larval instars described by Tauber and Tauber (1968). Johnson and Hagen (1981) readily reared it on Reticulitermes hesperus Banks and described the use of an aggressive allomone by the first- and third-instar larvae to paralyze the termites before they consumed their prey; the second instar is quiescent in the termite galleries. Eggs are glued to each other as a cluster at the end of a single silken stalk and are deposited on termite-infested logs. The adult is able to produce and deposit eggs on a diet of honey alone (K. S. Hagen, unpublished data). Brushwein (1987) presented data on the life history, adult longevity and fertility, habitat, and seasonal occurrence of L. hamata (Walker) associated with the eastern subterranean termite R. flavipes (Kollar). This eastern U.S. predator has a biology similar to L. latipennis. Brushwein (1987) reared L. hamata larvae on live and freezer-stored termites. Tauber (1991 a) reviewed the form and habits of the immature berothids. Chrysopidae There are about 1200 species of green lacewings recognized in the world today distributed among nearly 75 genera and 11 subgenera belonging to three extant subfamilies: Nothochrysinae, Apochrysinae, and Chrysopinae (Brooks & Barnard, 1990). The largest subfamily is the Chrysopinae, which contains most of the species involved in applied biological control. The biology of the Chrysopidae is summarized in Canard et al. (1984). Canard and Principi (1984) summarize the development of 19 Chrysopidae species based on 25 references. The length of the preimaginal developmental period is about 10 days in the larval stage, and another 10 days in the cocoon. The biology of most chrysopid species is completely unknown but of those studied, eggs are deposited atop a silken filament (except for Anomalochrysa spp., which deposit eggs on the sides on leaf surfaces), either as a single unit or as multiples in clusters (Duelli, 1984b; Gepp, 1984b). All larvae are predaceous and have three instars. They are either elongate and naked or more oval and carry debris on their dorsal hairs (Gepp, 1984b). Many chrysopid larvae are generalist predators, feeding on whatever prey found in the habitat where the eggs are deposited. Like most predators, the search is intensified by short turnings when prey is contacted (B~insch, 1966). A newly hatched first-instar Chrysoperla carnea larva can travel 214 m in 15 h before it dies of starvation (Fleschner, 1950). Some chrysopid larvae are highly specific to their selection of prey e.g., Chrysopa slossonae Banks larvae have only been found associated with the woolly alder aphid, Prociphilus tesselatus (Fitch) (Tauber & Tauber, 1987a; Milbrath et al., 1993), and Italochrysa italica (Rossi) larvae feed only on early stages of the ant Cremastogaster scutellaris (Oliver) (Principi, 1946). The quantity and quality of larval prey have an influence on developmental time and adult fecundity m indeed, certain aphids eaten by larvae can cause sterility in the males that emerge (Ca-

415

nard, 1970a). Larvae of the common chrysopid species are usually more easily identified to species than are adults. Larvae of common North American species have been described by Smith (1922) and Tauber (1974, 1991a), and Japanese species, by Tsukaguchi (1978); references to descriptions of all known larvae are cited by Gepp (1984a, pp. 215-217). There can be one to several generations per year (Tauber & Tauber, 1982, 1986, 1987b). Overwintering occurs in all stages except the egg, and the stage in which the chrysopid overwinters is characteristic for genera and subgenera (Canard & Principi, 1984; Tauber, 1991a; Principi, 1992; Canard & Grimal, 1993). Adult chrysopids, depending on the genus or subgenus, either are predaceous or feed on honeydew, nectar, or pollen (Hagen, 1950; Hagen et al., 1970b; Sheldon & MacLeod, 1971; Principi & Canard, 1984). It now appears that many genera of Chrysopidae are not predaceous in their adult stage (Johnson, 1982; Principi & Canard, 1984; Brooks & Barnard, 1990), and many of the nonpredaceous species harbor a mutualistic yeast (Torulopsis sp.), which is spread by trophallaxis between adults (Hagen et al., 1970b; Johnson, 1982). The role of the yeast apparently is to synthesize missing essential amino acids that are lacking in honeydew (Hagen & Tassan, 1972; Hagen, 1986). The species in the genus Chrysopa sensu stricto are all predaceous in the adult stage. The tracheal trunks associated with the foregut crop are thinner than those of Chrysoperla spp., which do not have predaceous adults (Hagen et al., 1970b; Principi & Canard, 1984). There are also differences in the form of mandibles between predaceous and nonpredaceous species (Ickert 1968). Mating attraction can involve vibrations, mainly via abdominal jerking in both sexes; specific duet courtship songs in some chrysopid species are transmitted from abdominal movements through the legs to a leaf or a thin substrate (Henry, 1983). There are glands in Chrysopa sensu stricto that are suspected to emit sex pheromones (Henry, 1984). Some Chrysoperla spp. will mate when fed sugar and water, but others require protein in the diet of at least the females to mate; similarly, some Chrysopa spp. will mate only on sugar and water, while others require aphids (Tauber & Tauber, 1974). In any case, protein plus carbohydrate is required to obtain egg production and oviposition. Enzymatic protein hydrolysates (particularly of yeasts) plus sugar or honey are highly effective as artificial honeydew (Hagen, 1950; Hagen & Tassan, 1966). However, Chrysoperla carnea adults obtain enough transferred metabolites from larval feeding to produce from 20 to 30 eggs in their lifetime when fed on honey or sugar and water alone (Hagen & Tassan, 1966). Rousset (1984) reviewed 16 references concerning the reproductive responses of 12 different chrysopid species exposed to different adult diets. Rousset found the preoviposition period varied from 3.9 to

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13.2 days, fecundity reached as high as 960 eggs, and fertility reached as high as 99%. The four genera of Chrysopidae that contain species involved in biological and integrated control projects are Brinckochrysa, Chrysopa, Chrysoperla, and Mallada (Doutt & Hagen, 1949; Hassan, 1974; Ridgway & Kinzer, 1974; Shuvakhina, 1975; New, 1975, 1984a, 1991; Beglyarov & Smetnik, 1977; Ridgway & Vinson, 1977; Ables et al., 1979; Hagen & Bishop, 1979; Principi, 1984; Ridgway & Murphy, 1984; Tulisalo, 1984a, 1984b; Barclay 1990; Khloptseva, 1991; Tauber & Tauber, 1993). Very little has been done in classical biological control; most research has been conducted in the augmentation and conservation of chrysopids. The 16 species in the genus Brinkochrysa are mostly concentrated in the Afrotropics. Their larvae are not trash carriers (Brooks & Barnard, 1990). Apparently B. scelestes (Banks) has been the only species in the genus used in a biological control project. This chrysopid was mass-cultured using 1000 eggs of the rice moth, Corcyra cephalonica (Stainton), per larva (Patel et al., 1988). The adults are not predaceous; most eggs were obtained from females exposed to a honey and castor pollen diet (Krishnamoorthy, 1984). Releases at the rate of six second-instar larvae per tobacco plant infested with Myzus persicae reduced the aphid populations nearly 80% in the field (Rao & Chandra, 1984). The chrysopid larvae were not hindered by the glandular trichomes (or their secretions) on the tobacco plants. The chrysopid also oviposits readily on cotton and green gram in India, where larvae are considered important predators of Helicoverpa armigera, Spodoptera litura, and aphids (Patel & Vyas, 1985). It is also an effective predator of woolly apple aphid on apple in India (Thakur et al., 1988). The genus Chrysopa sensu stricto comprises some 54 Holarctic species with 27 species occurring in the western Palearctic region, 15 in the eastern Palearctic, and 4 in the Nearctic region (Brooks & Barnard, 1990). New (1980), considering the genus in a broad sense, provides a key for 25 Chrysopa species in Australia. However, none of these are actually in Chrysopa sensu stricto; most are in Mallada and Chrysoperla (Brooks & Barnard, 1990). Larvae of Chrysopa spp. sensu stricto are not trash carriers and overwinter (in diapause) in cocoons. The adults are predaceous. About six species are commonly referred to in biological control literature. Chrysopa formosa Brauer is a widespread Palearctic species found from Europe to Asia on shrubs, in orchards, and in deciduous forests (S6m6ria, 1984). The eggs are deposited singly or widely spaced in groups of 2 to 10 on undersides of leaves of herbs and deciduous trees; Tsukaguchi (1978) found eggs on 17 different shrubs and trees infested with 17 different aphid species in Japan. This species was reared in large numbers in the laboratory by feeding larvae

S. cerealella eggs that could be stored at - 8 to -18~

for up to a month without harm. Adults were fed aphids and yeast hydrolysate with honey, under a long photoperiod (Kowalska, 1976). Also, adults and larvae can be reared on lyophilized drone honeybee pupae powder (Niijima & Matsuka, 1990). Because of the high egg production and low larval cannibalism, Babrikova (1978) considered it a good candidate as a biological control agent. In 1980, he reduced Myzus persicae populations on tobacco by releasing about eight larvae per plant in Bulgaria. Lyon (1986) released C. formosa, C. perla (Linnaeus), and C. carnea in greenhouses to control aphids on tomatoes, sweet peppers, and eggplants at the rate of 10 second-instar larvae per plant each week. Lyon also released Aphelinus asychis Walker along with the chrysopids. This complex of natural enemies controlled the aphids better on green peppers than on tomatoes because young chrysopid larvae were trapped and killed by the sticky hairs on tomato leaves. Chrysopa kulingensis Navas, a predator of aphids and soft scales in Chinese pine forests, was mass reared as larvae on honeybee larvae and Corcyra cephalonica eggs. A release of this chrysopid accounted for a significant decrease in Matsucoccus populations and a 20% increase in the predator population 35 days after release compared with the control (Wang & Hu, 1987). Chrysopa nigricornis Burmeister is a common large Nearctic tree and shrub species (Smith, 1922; Toschi, 1965). It occurs in peach orchards where the larvae prey on aphids and possibly oriental fruit moth eggs (Putman, 1932). At times C. nigricornis adults are highly attracted to terpinyl acetate in oriental fruit moth bait pans hung in peach trees (Caltagirone, 1969). The egg clusters of this chrysopid are commonly seen in walnut orchards and on cottonwood trees infested with gall aphids, as well as on cotton plants infested with aphids (van den Bosch & Hagen, 1966). Chrysopa oculata Say is a common multivoltine Nearctic species that ranges from southem Canada to northem Mexico. Adults emerge in the spring and reproduction and development occurs throughout the summer and autumn until the first frost (Tauber et al., 1987). The induction and duration of diapause is positively related to the latitudinal origin of the population, which is correlated to photoperiodicity of the region (Nechols et al., 1987). Chrysopa oculata deposits eggs singly on peach leaves, where a larva can destroy over 600 Grapholita molesta (Busck) eggs or about eight larvae during its development (Briand, 1931). In Texas cotton fields both larvae and adults feed on Aphis gossypii Glover; the mature larvae apparently enter the soil to pupate (Burke & Martin, 1956). In alfalfa hay fields, C. oculata feeds mainly on pea aphids and somewhat on alfalfa weevil larvae and ignores leafhoppers and plant bug nymphs (Lavallee & Shaw, 1969). In Pennsylvania grape vineyards C. oculata is the most common lacewing, and its

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

larvae were observed to prey on grape phylloxera on wild grape vines (Jubb & Masteller, 1977). The most suitable prey for C. oculata in corn fields was Rhopalosiphum maidis (Fitch); if switched from aphids to stalk borer [Papaipema nebris (Guenre)] eggs while in third instar, more than 80% of the lacewing larvae died. Aphids were also superior to a diet of Ostrinia nubilalis or Agrotis ipsilon eggs (although C. carnea larvae did well), but larvae of both lacewing species died when given first-instar corn borer larvae. It appears that C. occulata larvae are not the generalist predators that C. carnea larvae are (Obrycki et al., 1989). Chrysopa pallens (Rambur) (= semptempunctata Wesmael) (Brooks & Barnard, 1990) is a mainly arboreal species widely distributed through the Palearctic region (Principi, 1940; Hrlzel, 1984). In Japan, Tsukaguchi (1978) found egg clusters on 19 different plants (mostly trees) infested with 16 different aphid species. He reared and described all larval instars and obtained about 3200 eggs from a female held for about 90 days. Larvae and adults of C. pallens were reared for six generations on pulverized lyophilyzed drone honeybee brood and produced as many as 2228 eggs per female held for 166 days (Okada et al., 1974). In China, Cai et al. (1985) reared C. pallens larvae and adults on artificial diets not containing insect parts for seven generations. Niijima (1989) formulated a chemically defined diet for the adult and larvae, and determined the amino acid requirements for larval development (1993a) and vitamin requirements for larval development (1993b). Its functional responses to cotton bollworms and cotton aphids were found to follow Holling's type II (Huang et al., 1990). Chrysopa pallens is an important predator of aphids on apples in Japan. The larvae can survive being exposed to chitin synthesis-inhibiting insecticides, but died at the prepupal stage in their cocoons (Kawashima, 1988). In (former) USSR greenhouses, a release of second-instar larvae at a predator to prey ratio of 1:5 or 1:10 controlled aphids on cucumbers. Releases of adult females at 1:50 resulted in an 82 to 86% reduction in aphid numbers in 3 days. The larvae resulting from the released adults completely destroyed the remaining aphids by the ninth day after the initial release (Ushchekov, 1976). Chrysopa perla is a Palearctic species that occurs commonly across the northern European countries (Greve, 1984). In the Mediterranean region it is limited to cooler and wetter areas (Srmrria, 1984). Apparently C. perla is not found in China (Yang, 1988), and only rarely is collected in Japan (Tsukaguchi, 1978). This species is associated with many different trees and shrubs (Zeleny, 1984). However, a diet of certain aphid species can limit the reproductive success of the adult while allowing larval development [e.g., Brevicoryne brassicae (Linnaeus) somewhat prolongs developmental time on C. perla larva, and when fed to adults results in lower progeny production levels,

41 7

while a diet of Megoura viciae Buckton reared on Vicia sativa (Linnaeus) virtually precluded progeny production (Canard, 1970a 1970b)]. Detailed studies on the influence of food on C. perla reproduction are described by Philippe (1972). The Australian Apertochrysa edwardsi Banks (as Chrysopa edwardsi) was satisfactorily reared as larvae and adults on B. brassicae and on acacia psyllid Acizza acaciaebaileyanae (Froggatt) (New, 1981). Both prey species are thick and waxy in the nymphal stages, which led New to conclude that A. edwardsi larvae and adults are adapted to feed on "waxy" prey. Therefore, this may be an effective species for importation against this type of prey. Chrysopa perla and six other chrysopid species were reared on one feeding of 50 to 100 mg of frozen Sitotroga cerealella eggs per larva by Kawalska (1976). By releasing 4800 C. perla eggs in about 40 m 2 of asparagus infested with Myzus persicae at a rate of 1 egg per 25 aphids, Kawalska (1976) was able to keep the asparagus free of aphids for 3 months. Weekly releases of C. perla and C. formosa were made alone and in association with Aphelinus asychis Walker against M. persicae and Macrosiphum euphorbiae (Thomas) infesting eggplants in a greenhouse, which resulted in control similar to that obtained in another greenhouse where pirimicarb was used (Lyon, 1979). In the former USSR, egg and larval releases of C. perla successfully controlled Aphis gossypii on cucumbers in greenhouses and were also effective in the field against Myzus persicae on kale and Aulacorthum circumflexus (Buckton) on ornamental plants (Ushchekov, 1989). The genus Chrysoperla contains about 50 species worldwide (Brooks & Barnard, 1990). This genus was once considered a subgenus of Chrysopa, but distinctly differs from it morphologically and even more so biologically. The adults of Chrysoperla spp. are not predaceous, but feed on honeydew and pollen that are required for egg production (Hagen, 1950; Hagen et al., 1970b; Rousset, 1984); thus far all of the Chrysoperla spp. adults studied have contained symbiotic yeasts in their esophageal diverticulae (Hagen et al., 1970b; Johnson, 1982; Principi & Canard, 1984). All species overwinter as adults (Principi, 1992). Eggs are deposited singly or loosely in groups. Larvae are generalist predators but not trash carriers (Balduf, 1939; Principi & Canard, 1984; Adams & Penny, 1985). The utilization of Chrysoperla (principally three species) in biological control has been through augmentation and conservationmthe several attempts to purposely introduce them to exotic locations have failed. Because at least some Chrysoperla spp. are honeydew feeders, they have been manipulated by applying artificial honeydew in crops to attract adults and induce oviposition where insect damage is anticipated. Chrysoperla carnea is apparently a Holarctic species. In the world literature, it has gone under at least 20 different

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names (Brooks & Barnard, 1990). In the Nearctic region it has been called: C. californica (Coquillett), C. downesi (Smith), C. mohave (Banks), C. plorabunda (Fitch) as well as a few other names that have not appeared in biological control literature. There are geographic variations in the courtship song of Nearctic C. carnea that have led some workers to suspect that this group may include several cryptic species. In their world list, Brooks and Barnard (1990) recognize C. plorabunda (Fitch) as a separate species from C. carnea, based apparently on Henry's (1983) observation that a Swiss C. carnea population did not recognize the courtship song of an American C. carnea population and failed to mate, which led him to resurrect C. plorabunda from synonomy. Henry and Wells (1990) found additional populations whose songs varied from that of the C. plorabunda population in New York (the type locality for C. plorabunda). However, the Taubers (1972, 1986, 1987b) have demonstrated that geographic variations in diapause response in C. carnea are also under polygenic control, and they (1986) resynonymized C. plorabunda under C. carnea, recommending that no name changes be implemented until a thorough taxonomic study--which considers intra- and interpopulation variation in morphological, behavioral, and ecological trials of the entire C. carnea species complexmis completed. Additional synonyms of C. carnea include C. vulgaris (Schneider) from Europe and C. sinica (Tjeder), C. nipponicus (Okamoto), and C. kurisakiana (Okamoto) from Asia (Brooks & Barnard, 1990). Chrysoperla carnea larvae are generalist predators of soft-bodied insects and spider mites. Over 70 different prey species in five insect orders have been recorded in 90 references cited by Balduf (1939) and Herard (1986). The prey are mostly Homoptera, with aphids on low-growing crops and vegetation predominating; however, psyllids, mealybugs, leafhoppers, and whiteflies are also readily consumed. Butler and Henneberry (1988) found that C. carnea larvae ate immature stages of Bemisia tabaci (Gennadius) on cotton in the laboratory. Interestingly, they also found that the presence of lacewing larvae inhibited both visitation and oviposition by Bemisia adults, even after the larvae had left the leaves, and suggested the repelling volatile semiochemical or semiochemicals be identified for possible uses as a control measure. Among the recorded lepidopteran prey, noctuids (Heliothis spp.) on cotton were the most often mentioned. Chrysoperla carnea larvae exposed to Heliothis eggs on artificial cotton plants searched mostly the top half of the "plants" where older lacewing larvae consumed 3 to 6 eggs per day; the time spent handling each Heliothis egg did not affect the rate of successful search (Butler & May, 1971). Chrysoperla carnea larvae are stimulated into a prey-seeking behavior by kairomones found in moth scales of H. zea that are associated with moth oviposition sites (Lewis et al., 1977) and acceptance of the H. zea eggs is

stimulated by an additional kairomone, probably in the accessory gland secretion, which is associated with egg deposition (Nordlund et al., 1977). Chemically defined diets have been formulated for C. carnea larvae (Hasegawa et al., 1989; Yazlovetsky, 1992). Adults of C. carnea feed on honeydew (Hagen, 1950; Hagen & Tassan, 1972) and pollen (Sundby, 1967; Sheldon & MacLeod, 1971), but the biotype C. mohave Banks (a synonym of C. carnea) is an estivating strain that eats aphids, honeydew, and probably pollen (C. Tauber & M. Tauber, 1973; M. Tauber & C. Tauber 1975). Chrysoperla carnea adults search for food and oviposition sites nocturnally, and respond anemochemotactically to volatile chemicals emanating not only from the food source (honeydew) (Hagen et al., 1970a, 1976b; Duelli, 1980, 1984a), but also from the habitat (the plant involved) (Flint et al. 1979; Hagen, 1986). The kairomone that attracts C. carnea to honeydew comes from tryptophan (Hagen et al., 1976b), and laboratory olfactometer studies with tethered C. carnea females, at least 2 days old, demonstrated that they respond positively in flight toward breakdown chemical volatiles of tryptophan, particularly indole acetaldehyde (van Emden & Hagen, 1976). After antennal contact with honeydew or hydrolized tryptophan in water, C. carnea females showed a reduced mean walking speed, and an increased mean turning frequency and tuming angle (McEwen et al., 1993b). The synomone that attracts C. carnea to a cotton habitat is the terpene caryophyllene, a common volatile coming from cotton leaves (Flint et al., 1979). Adults fly downwind at night but tum upwind when they detect honeydew; however, it appears that C. carnea adults respond to the kairomone only when a synomone (plant volatile) is received simultaneously (Hagen, 1986). This type of behavior must be considered when attempting to use artificial honeydew to attract C. carnea (and perhaps other Chrysoperla spp.) because a synomone may not be present because of species and age variation of crop plants. Of all the Neuroptera, C. carnea has been the most commonly used species in applied biological control, mainly through augmentation and conservation tactics. It rarely has been involved in classical biological control programs, but at least two attempts were made to introduce C. carnea into New Zealand. One introduction involved importation of eggs from Califomia. This failed even though adults were successively reared in the laboratory and fed a standard complete diet of dry yeasts and sugar (Hagen & Tassan, 1970). The failure to become established was probably due to the absence of yeast symbiotesmthese are apparently not present in the egg stage and would not have been previously present in New Zealand due to the absence of any honeydew or pollen feeding chrysopids (Hagen & Tassan, 1972). A similar result was noted when the cocoons of several chrysopid species were imported from India. Progeny were successfully reared in the insectary, but es-

Chapter 16 TerrestrialArthropod Predators of Insect and Mite Pests tablishment was never achieved (Rao et al., 1971). However, C. comanche, C. carnea, and Mallada basalis (Walker), which all "require" yeast symbiotes, became established in the Hawaiian Islands (Adams, 1963), suggesting that they invaded the islands as adults carrying their symbiotic yeasts. Augmentation of C. carnea in field and greenhouse situations to control insects and mite pests has been conducted both by releasing eggs and larvae (Hassan, 1974; Beglyarov & Smitnik, 1977; Ridgway et al., 1977; Stinner, 1977; Ables & Ridgway, 1981; Ridgway & Murphy, 1984; Barclay, 1990; Khloptseva, 1991; Nordlund & Morrison, 1992) and by attracting and feeding wild adult lacewings to promote egg production and oviposition (Hagen et al., 1970a; Hagen & Hale, 1974; Hagen & Bishop, 1979; Ridgway & Murphy, 1984; Barclay, 1990). Larvae of C. carnea can be reared on a variety of insects, but lepidopterans are the most widely used hosts. These include eggs and coddled larvae of potato tuberworms, Phthorimaea operculella (Zeller) (Finney, 1948, 1950); eggs of Angoumois grain moth, Sitotroga cerealella (Shuvakhina, 1969; Ridgway et al., 1970; Beglyarov & Ushchekov, 1974; Hassan, 1975; Makarenko, 1975; Morrison et al., 1975; Nordland & Morrison, 1992); frozen eggs (Kawalska, 1976), all moth stages (Tulisalo, 1984a), and larvae of Indian meal moth, Plodia interpunctella, and Mamestra brassicae. (Linnaeus) (Hassan, 1975); eggs of Mediterranean flour moth, Anagasta kuehniella (Pasqualini, 1975, Zheng et al., 1993a); and eggs of the wax moth, Galleria mellonella (Sgobba & Zibordi, 1984). McEwen et al. (1993a) obtained greater survival and faster larval development by mixing A. kuehniella eggs in a sugar solution containing yeast hydrolysate (artificial honeydew). The quantity and quality of these hosts can influence the fecundity and longevity of the resulting adult lacewings (Makarenko, 1975; Pasqualini, 1975; Zheng et al., 1993b). Other prey used to culture C. carnea larvae have included green peach aphids cultured on green pepper and spring rape (Tulisalo & Korpela, 1973), and eggs of the eucalyptus borer, Phoracantha semipunctata Fabricius (Neumark, 1952). Lacewing larvae have also been reared on artificial diets (Niijima & Matsuka, 1990). These will undoubtedly be the preferred diets in the future, especially if diet encapsulation methods are further developed (see Chapter 7). Chrysoperla spp. are much easier to mass-culture than Chrysopa spp. because they readily produce high numbers of eggs on artificial diets. The best diets are those that contain an enzymatic protein hydrolysate of yeast, sugar, or honey, either mixed or provided separately (Finney, 1950; Hagen, 1950; Hagen & Tassan, 1966). Another effective adult lacewing diet is yeast Saccharomyces fragilis cultured on whey and mixed with sugar or honey (Hagen & Tassan, 1970; Zhou et al., 1981; Nordland & Morrison, 1992). On

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these diets a female C. carnea can produce 500 to 1000 eggs in about 30 days. Because there is deterioration of C. carnea when masscultured over time, Jones et al. (1978) recommend not going beyond six generations before renewing the insectary stock, or even by the fourth generation as suggested by Niijima & Matsuka (1990). Diapausing adults can be stored at 5~ for over 30 weeks and still be reproductively effective for mass production (Tauber et al., 1993), and eggs can be stored at 8~ for up to 20 days without loss of viability (Osman & Selman, 1993). The first field releases of Chrysoperla carnea were made against mealybug Pseudococcus obscurus Essig infesting pears that were being sprayed with DDT to control the codling moth in the Santa Clara Valley, California. In the unsprayed control blocks, it became clear that the mealybug was being controlled by C. carnea (Doutt, 1948). There were no parasitoids reared from the mealybugs, and the only predators present were lacewing larvae. This situation led to mass-culturing C. carnea and to subsequently releasing egg; although the adult lacewings were killed by the DDT sprays, eggs and larvae were not harmed. Three releases of 250 eggs each per tree reduced the mealybug infestation rate of the fruit down to 12%, while 58 to 68% of the pears were infested in the DDT-treated blocks, where no lacewing releases were made (Doutt & Hagen, 1949, 1950). The pear growers were going to build an insectary to mass-culture C. carnea and integrate lacewing egg releases with the DDT spray treatments; however, when parathion replaced DDT, the new insecticide also controlled the mealybug and so the insectary project was dropped. It was not until the 1960s before C. carnea was again utilized in the field. The target pests were bollworms (Heliothis spp.), because lacewing larvae appeared to have an impact on these populations, particularly in cotton fields. Releases of C. carnea were first conducted in field cages, which demonstrated that C. carnea larvae could reduce bollworm densities. Ridgway and Jones (1968, 1969) obtained 76 to 99% reduction of H. virescens by releasing first-instar larvae against bollworms when there were few alternate prey available. Ridway and Jones (1968) also found H. zea was reduced on cotton from 74 to 90% with predator to prey ratios from 2.5:1 to 30:1. These release rates ranged from 62,000 per hectare to 741,000 per hectare. Lingren et al. (1968) got a 96% reduction of H. virescens in cages at a release rate of about 1 million C. carnea larvae per hectare. Van den Bosch et al. (1969) reduced caged H. zea larvae on cotton from 46 to 84% using predator to prey ratios of 1:4 to 1:3, respectively. A release rate of about 200,000 per hectare of 1- to 4-day-old C. carnea larvae resulted in 30% less damage to bolls by H. virescens in field cages (Lopez et al., 1976). Stark and Whitford (1987) conducted a series of third-instar C. carnea releases on caged cotton plants with 20, 40, 60, or 80 H.

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virescens eggs per cage. At the lowest bollworm density

(predator to prey of 2.8:1) 55% of the eggs were attacked, while 42% were attacked at the highest density (predator to prey ratio of 0.8:1), producing a type II functional response. From these studies, they calculated that C. carnea larvae had an average search rate of 1.08 x 10m 2 ha/predator-day (or 0.11 row-meter/predator-day). The calculation of such search rates can be useful in determining the optimal numbers for field releases. Only a few releases of C. carnea have been made in open cotton fields against bollworms. A 96% reduction of bollworm occurred at a release rate of 721,200 first and second-instar larvae per hectare, but no reduction of bollworms occurred when only adult lacewings were released (Ridgway & Jones, 1969). Gurbanov (1982) recorded a 100% reduction of H. armigera eggs in cotton at a 1:1 release ratio but only a 50% reduction of bollworm larvae; he also obtained over 95% reduction of aphids, thrips, and spider mites from these releases. In soybeans, releases of 20, 60, or 120 C. carnea eggs in cages where 1000 H. zea eggs and 500 Trichoplusia ni eggs were placed did not reduce defoliation; Barry et al. (1974) suggested that predation of lacewing eggs by Orius insidiosus that penetrated the cages over soy plants explained the ineffectiveness of C. carnea in their tests. Another lepidopteran, pink bollworm, was reduced from 33 to 80% by releasing third-instar C. carnea larvae from 1 to 12 per cotton plants (Irwin et al., 1974). Field releases against aphids began on vegetables. Shands et al. (1972b) released at the rate of about 50,000 to 100,000 C. carnea per hectare and obtained 42 to 89% reduction of Myzus persicae, but only a 22 to 34% reduction of Macrosiphum euphorbiae on potatoes. Adashkevich and Kuzina (1974), using ratios of 1:5 and 1:10 secondinstar C. carnea larvae, got no reduction, but at a 1:2 ratio using third instars obtained 50% reduction of aphids on potatoes. Releases at a ratio of one second instar to five M. persicae on vegetables (eggplants, peppers, tomatoes) accounted for reductions of aphids from 43 to 97% (Begleyarov & Smetnik, 1977). Aulacorthum solani (Kaltenbach) was reduced 90% on tomatoes using a 1:5 predator to prey ratio (Ter-Simonjan et al., 1982); they also obtained a 94% reduction of Aphis gossypii on cucumbers. A net release of 625 C. carnea eggs per tulip tree infested with Illinoia liriodendri (Monell) did not control the aphid; predation on released eggs by the Argentine ant precluded potential control (Dreistadt et al., 1986). Aphis pomi was reduced significantly on dwarf apple trees at a release rate of 335,000 C. carnea eggs per hectare, a ratio of about 1:18 (Hagley, 1989). Inoculative releases of first-instar C. carnea (= C. sinica) in Chinese wheat fields 1 month before spring harvest yielded the highest number of adults, which then spread to other crops later in the season (Zhou et al., 1991b). The density of the variegated grape leafhopper, Erythro-

neura variabilis Beamer, was reduced by up to 35% after releases of 3000 to 8000 hatching C. carnea eggs against each of the two broods of leafhoppers. These results suggest that lacewing releases can reduce initial leafhopper density up to 25 per leaf below the economic injury level of 15 per leaf (Daane et al., 1993). Releases of C. carnea against the Colorado potato beetle have given variable results. No control was achieved by releasing eggs at a 1:1 ratio, but an 86 to 95% reduction of the pest populations on potatoes was found when secondand third-instar C. carnea larvae were released at 1:1 to 1:5, at 1:10, and at 1:20 ratios by Adashkevich and Kuzina (1974) and Shuvakhina (1975). On eggplants, the Colorado potato beetle was reduced from 74 to 100% with the highest predation occurring when releasing C. carnea larvae at 1:1 to 1:5 ratios (Beglyarov & Smetnik, 1977). A release of one C. carnea larva against 80 Tetranychus urticae in cotton reduced the spider mites by 99.6% (Ishankulieva, 1979). There has also been some success controlling spider mites by releasing chrysopids. On apple trees, the European red mite was reduced when one C. carnea larva was released for every 10 to 25 leaves (Miszezak & Niemczyk, 1978). On citrus trees, a release of one first-instar C. carnea (as C. sinica) to 100 to 200 Panonychus citri reduced the mites by 90% in 5 days (Peng, 1985). Peng (1988) also made field releases of C. shansiensis (Kuwayama) against red spider mites on citrus. Releases of C. carnea eggs or larvae had controlled a variety of insect and spider mite pests of crops and ornamentals grown in greenhouses (Tulisalo, 1984b). Scopes (1969) was able to control Myzus persicae on chrysanthemums by releasing 1-day-old lacewing larvae at a predator to aphid ratio or 1:50, while third-instar larvae were effective at a ratio of 1:200. However, the potential to control Aphis gossypii on cucumbers was limited due to the hairiness of the leaf, which inhibits the locomotion of chrysopid larvae (Scopes, 1969). Aphids infesting celery, eggplants, lettuce, oats, parsley, peppers, strawberries, and tomatoes have been controlled by releasing eggs or larvae of C. carnea (Bondarenko & Moiseev, 1972; Beglyarov & Ushchekov, 1974; Tulisalo & Tuovinen, 1975; Kawalska, 1976; Rautapaa, 1977; Tulisalo et al., 1977; Hassan, 1978; Celli et al., 1986). Tetranychus urticae infesting peaches grown on a trellis system in a protected environment were controlled by placing 1000 or 1500 C. carnea eggs per tree on foliage when the spider mites became active on foliage (Hagley & Miles, 1987). Rautapaa (1977) had to release about 15 to 20 times more eggs as larvae to achieve the same decrease of Rhopalosiphum padi on oats under greenhouse conditions. Chrysopid eggs have usually been released in the field manually, either still attached to the ovipositional substrate used in the insectary (such as paper cards, cloth, or rice

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

hulls), or destalked. The latter can be scattered freely or sprinkled on a 10% sucrose or 1% methyl cellulose solution and then sprayed on foliage (Doutt & Hagen, 1950; Ridgway & Jones, 1969; Shands et al., 1972a; Barry et al., 1974; Jones & Ridgway, 1976; Peng, 1986). Larvae from destalked eggs developed faster than those from stalked eggs (Sengonca & Schimmel, 1993). There has also been considerable interest in mechanical application techniques for chrysopid eggs (McEwen, 1996; Daane & Yokota, 1997; Gardner & Giles, 1996, 1997; Sengonca & Loechte, 1997). The use of food sprays in the field can augment natural chrysopid populations by arrestment or attraction (Hagen et al., 1970a; New, 1975; Hagen & Bishop, 1979; Ridgway & Murphy, 1984; Hagen, 1986; Barclay, 1990; Evans & Swallow, 1993; Ehler et al., 1997). It is possible to retain and arrest foraging lacewing adults by simply spraying a sugar solution (10% sucrose in water) or molasses on the crop (Ewert & Chiang, 1966; Carlson & Chiang, 1973). Chrysopids are not actually attracted to the sugar sprays, but will stay in the field when they contact the sugar; thus they can be concentrated in sugar-sprayed areas (Hagen et al., 1970a). Chrysoperla spp. can be attracted to artificial honeydew and stimulated to oviposit even in the absence of aphids or other honeydew-excreting insects. By simulating a high aphid population level by spraying artificial honeydew that contain sugar and protein, it is possible to induce chrysopids to oviposit before aphids increase, thus controlling other potential pests that are not honeydew producers such as noctuids, thrips, and spider mites. Pea and spotted alfalfa aphid populations on alfalfa attained only half the population densities reached in plots not receiving protein food sprays (Hagen et al., 1970a). Similarly, M y z u s persicae populations on pepper plants were slowed and reached only half of the populations on unsprayed peppers (Hagen & Hale, 1974). M y z u s persicae, Lygus hesperus, and A u t o g r a p h a californica (Speyer) numbers were reduced in potato fields by spraying Wheast | (yeast grown on whey) in a sugar solution that increased C. carnea abundance and oviposition (Ben Saad & Bishop, 1976). Heliothis zea eggs, larvae, and damaged bolls were reduced in plots sprayed with Wheast | and sugar (Hagen et al., 1970a; Kinzer & Jones, 1973; Denver, 1974). However, Butler and Ritchie (1971) did not obtain an increase in C. carnea oviposition in cotton when sprayed with Wheast | plus honey and glycerin. A yeast plus sugar spray applied to grape vineyards did promote an increase in one case but not in a second trial (White & Jubb, 1980). Duelli (1987) got attraction but did not obtain an increase of C. carnea oviposition in Switzerland when he applied Wheast | plus sugar on alfalfa, apple, or corn, while Dean and Satasook (1983) in England obtained attraction of C. carnea to tryptophan-impregnated sticky traps but not to caryophyllene. Application of artificial honeydew will not be of any value

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if there is already honeydew present (Hagen et al., 1970a; Tassan et al., 1979). When applying food sprays, both a protein source (yeasts) and sugar must be applied. Shands et al. (1972b) and Hagley and Simpson (1981) applied protein without sugar on potatoes and apples and failed to obtain an increase of C. carnea. The artificial honeydew should be applied in swaths across the prevailing evening winds and on crops that are releasing natural volatiles (synomones); otherwise, C. carnea adults may not be attracted to tryptophan volatiles (Hagen, 1986). Shelters were provided for hibernating C. carnea adults by placing boxes in field crops or even in fallow fields as fall approached; mortality during hibernation did not exceed 2% (Sengonca & Henze, 1992). Another advantage of C. carnea is that it has a rather broad tolerance to many insecticides, particularly in its larval stage (Bartlett, 1964b; Grafton-Cardwell & Hoy, 1985). As noted earlier, lacewing eggs and larvae survived DDT treatments and controlled mealybugs in pear orchards (Doutt & Hagen, 1950). Fortunately, C. carnea larvae are also tolerant of pyrethroid insecticides because they produce pyrethroid esterase or esterases that allow them to detoxify these insecticides (Ishaaya & Casida, 1981). The tolerance to certain insecticides varies geographically among C. carnea populations. Chrysoperla carnea from areas in California with a history of heavy pesticides usage are more tolerant to certain insecticides compared with populations occurring in areas where less pesticides were used (Grafton-Cardwell & Hoy, 1985). In conclusion, since C. carnea is such a common and readily available generalist predator, it can be utilized in biological and integrated control programs against a variety of insect and spider mite pests in several ways, including mass culture and periodic colonization (although this is rather expensive today); application of behavioral chemicals and artificial food to retain, attract, and induce oviposition; and use of selective insecticides to spare naturally occurring lacewing populations. Chrysoperla externa (Hagen [= lanata (Banks)] ranges over all Latin America and north into Florida and South Carolina and was inadvertently introduced into the Hawaiian Islands (Adams, 1963; Adams & Penny, 1985). Because it is commonly found in agricultural habitats and preys on a wide range of insect pest species, its biology has been investigated and found to be similar to C. carnea (Ru et al., 1975; Crouzel & Botto, 1977; Aun, 1986; Nfnez, 1988; Barclay, 1990). However, little research was conducted on ways to augment C. externa populations until Barclay (1990) tried both releasing C. externa eggs and using supplementary food sprays to manipulate lacewing adults in Nicaraguan soybean and cornfields. Barclay reared the larvae on frozen Sitotroga cerealella eggs in individual cells, and used Wheast | plus honey as a

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paste to feed the adults. Groups of 100 lacewing eggs were cut from paper taken from the oviposition units (eggs could be held at 10~ for up to 10 days). Two releases were made in soybeans and one, in tasselling corn that amounted to release rates from 360,000 to 760,000 C. externa eggs per hectare. No significant increases in C. externa larval populations were observed in either crop; there was no significant effect on the three targeted noctuid species in soybeans (heavy rains may have reduced the number of lacewing larvae directly or indirectly through increasing fungal attack on lacewing eggs, while many eggs were also parasitized by Trichogramma spp.). There were significantly fewer H. zea larvae found in the corn release plots compared with the control 1 week after release. Even though heavy rains occurred midway through the test that reduced the number of lacewing larvae, Barclay (1990) considered there had been enough time for the eggs to hatch and the larvae to have had an impact on H. zea before the storm. Chysoperla externa adults were also manipulated in the field using Wheast| food sprays (Barclay, 1990). Chrysopid adults increased from 2.3- to 6-fold in foodsprayed corn field plots compared with check plots 24 h following each treatment application; significantly more chrysopid eggs were found in the Wheast | + sugar plots compared with plots where sugar alone was sprayed and there were more than three times as many freshly deposited green lacewing eggs found in the Wheast| treatments compared with controls. Significantly fewer C. externa eggs were found on cotton plants intercropped with corn and weeds than were found in cotton monocultures (Schultz, 1988); Schultz suggests the reduction in egg numbers is due to a corresponding decrease in number of prey (aphids) and increased presence of other predators such as earwigs. Chrysoperla rufilabris (Burmeister) is widespread in the United States but is virtually absent in the dry southwestern states and most abundant in the more humid southeastern United States (Tauber & Tauber, 1983). Under relatively humid conditions (75% RH), C. carnea and C. rufilabris are similar in almost all aspects of the life history traits that the Taubers (1983) measured. However, under low (35% RH) and moderate humidity (55% RH), C. rufilabris had a prolonged preoviposition period, a reduced fecundity, an increased preimaginal mortality, and a slower developmental rate. The larvae have a broad prey range. In southeastern United States cotton fields, C. rufilabris larvae are considered important predators of spider mites (McGregor & McDonough, 1917) and bollworms (Ewing & Ivy, 1943; Lingren et al., 1968). Fewer bollworm eggs were destroyed on pilose cotton than on smooth leaf and hirsute cotton; from functional response studies of the lacewing larvae, Treacy et al. (1987) demonstrated that cotton-leaf trichomes are mechanical barriers that reduce the mobility and predatory ability of C. rufilabris. In Florida (Buschman et al.,

1977) and South Carolina (Shepard et al., 1974; McCarty et al., 1980) relatively few chrysopid larvae were found in soybean fields, but they did consume noctuid eggs labeled with 32p. Aphids, such as the cotton aphid (Ewing & Ivy, 1943; Burke & Martin, 1956), the pecan aphid (Elkarmi et al., 1987), and citrus aphid (Hydorn & Whitcomb, 1972), are common prey. Large numbers of oriental fruit moth eggs were observed to be destroyed by C. rufilabris larvae in Vineland, Canada peach trees (Putman, 1932). Putman (1956) also observed that C. rufilabris became less abundant than C. carnea when DDT was used in Ontario peach orchards m tests showed larvae of C. rufilabris larvae were more sensitive to the insecticide. Lawrence (1974) found C. rufilabris larvae had various degrees of sensitivity to four common insecticides used to control insect pests in Florida citrus. Because C. rufilabris showed promise for manipulation on cultivated crops, methods of culturing and influence of diets in both larvae and adult lacewings were studied (Hydorn & Whitcomb, 1972, 1979; Ru et al., 1976; Elkarmi et al., 1987; Nordlund & Morrison, 1992). It was determined that C. rufilabris larvae readily prey on eggs and young larvae of the Colorado potato beetle in the laboratory, while in field cages, 84% population reduction was obtained with a release rate of 80,940 C. rufilabris larvae per hectare (Nordlund et al., 1991). However, these authors concluded that such a rate is not practical unless the cost to massculture lacewings is reduced. Larvae of C. rufilabris feed voraciously on Bemisia tabaci eggs and nymphs on the lower (under) surface of Hibiscus leaves; treatments in a greenhouse with five larvae per Hibiscus plant produced both marketable and unmarketable plants, and all plants in the 25 or 50 lacewing larvae per plant treatments remained healthy and marketable (Breene et al., 1992). The genus Mallada (= Anisochrysa) is the largest of the Chrysopidae with at least 122 described species that are worldwide but absent from much of the Neotropics (Brooks & Barnard, 1990). They are trash carriers and at least some diapause as a third larval instar (Principi, 1956; 1992; Principi et al., 1990). Of this genus, only M. boninensis Okomoto and M. basalis have been studied in any detail as natural enemies in agricultural crops. In an unsprayed Rhodesian cotton field, 81% of the fertile chrysopid eggs sampled by Brettell (1979) were M. boninensis, one of three chrysopid species present. The adults are not predaceous but a larva can destroy a total of 297 H. armigera eggs. This species is widely distributed in the Old World and is most common in Asia; Brettell (1979) suspects that it was carried to southern Africa on citrus imported from China some 200 years ago. He also found that of the four widely used pesticides in cotton, DDT was the most toxic to the larvae. This is interesting because C. carnea larvae are not susceptible to DDT (Bartlett, 1964b). Among the 10 chrysopid species collected in Guanazhou, China, M. boninensis

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

was one of three dominant species found (Wei et al., 1987). In Taiwan, Lee and Shih (1982) reared larvae of M. boninensis on nymphs of the psyllid Paurocephala psylloptera Crawford; the developmental time was somewhat longer than when the larvae were reared on Corcyra cephalonica eggs. They developed a life table for the chrysopid; and by using field cages, they found an optimal ratio of four firstinstar M. boninensis larvae per an initial prey biomass index of 158 suppressed psyllid populations within 4 to 5 days. In Japan during the summer, predation by M. boninensis is considered a major mortality factor of Ceroplastes japonicus Green on Euonymus (Miyanoshita & Kawai, 1992); and in India, it readily attacks the grape mealybug Maconellicoccus hirsutus (Green) (Mani & Krishnamoorthy, 1989; Mani, 1990). Mallada basalis larvae were reared on C. cephalonica eggs; 13 adults were obtained from each milliliter of host eggs (Chen et al., 1993). Eggs of M. basalis placed in citrus trees resulted in a reduction of Panonychus citri (Wu, 1992). Among the 11 species of Mallada in Australia, M. signata (Schneider) is a predator of Heliothis spp. in Queensland cotton. Its voracity and searching ability were studied in the laboratory by Samson & Blood (1980), who found the numbers of H. punctigera eggs and early instars attacked per day in petri dishes increased exponentially with each successive larval instar of the chrysopid. Mallada signata larval searching success and consumption of Heliothis were greater than those reported for some other chrysopids [e.g., C. carnea (Samson & Blood, 1980)]. Because Mallada spp. are similar to Chrysoperla spp. (not predaceous in the adult stage and attracted to protein hydrolysates [Neuenschwander et al., 1981)] and are often common in wild refuges as well as in crops (Pantaleoni & Sproccati, 1987), they may prove to be effective predators in crops if artificial honeydew is applied in anticipation of arthropod pest problems. Coniopterygidae According to Meinander (1990), there are 423 recognized species of dusty wings in the world today; Meinander (1972) revised the family and included references to the few biologies that are known in the family; and in 1986 he mapped the distribution of the 132 species belonging to the 10 genera present in the Americas (Meinander, 1986). Johnson (1980) reviewed the biology and produced a key to the North American genera of the Coniopterygidae, and revised the genus Aleuropteryx. The dusty wings are the smallest of all the Neuroptera, but some of the species present in agricultural and landscape habitats are important predators of spider mites, aphids, coccids, and whiteflies, and these species account for the known biologies (Quayle, 1912; Arrow, 1917; Withycombe, 1923, 1924; Collyer, 1951; Fleschner, 1952; Fleschner & Ricker, 1953; Badgley et al., 1955; Muma, 1967;

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Ward, 1970; Henry, 1976; Agekyan, 1978; Johnson, 1980; Wheeler, 1981; Rousset, 1984; Drea, 1990a; Tauber, 1991a). The adults and larvae are predaceous, often feeding on the same prey, but adults also feed on honeydew. The adults consume the whole prey with mandibulate mouthparts while the fusiform larvae suck their prey dry using piercing mouthparts; both adults and larvae detect their prey tactilely. Many dusty wings are associated with one tree or shrub species, indicating they may be restricted to specific prey. The eggs are usually laid singly on leaf surfaces or in bark crevices. The larvae usually undergo three instars (Meinander, 1972), but four instars have been observed in Conwentzia californica Meinander by Quayle (1912), in Heteroconis picticornis (Banks) by Badgley et al. (1955), and in Semidalis vicina (Hagen) by Muma (1967). The flatish cocoons have two or three layers of silk with the innermost being the thickest and are often fastened to the undersides of leaves. Some species overwinter within the cocoon as prepupae, while others overwinter as free larvae. The Coniopterygidae are divided into two subfamilies: Aleuropteryginae and Coniopteryginae. There are few species in each subfamily that have been considered important to applied biological control. Aleuropteryginine larvae have antennae and labial palpi of about equal length with long jaws that project from beneath the labrum. Aleuropteryx juniperi Ohm is a Palearctic species that was inadvertently introduced into Pennsylvania, probably on juniper nursery stock from Europe, in the early 1900s (Henry, 1976). By 1980, it had spread to Maryland, New Jersey, New York, and West Virginia (Wheeler, 1981). It occurs mainly on Juniperus spp., and in England feeds on juniper scale, Carulapsis juniperi (Bouch6) (Ward, 1970). This was also observed by Henry (1976) in Pennsylvania, and he also found it to feed on C. minima (Targioni-Tozzetti) on juniper. Henry (1976) reared A. juniperi in the laboratory on C. minima. Aleuropteryx juniperi usually lays its eggs singly on the underside of juniper needles. The larvae feed at the base of the adult scale but penetrate scale crawlers and nymphs. The adults feed on all stages of minute cypress scale and its honeydew (Henry, 1976). Stimmel (1979) mentions that A. juniperi reduced C. minima population more than any other natural enemy in experimental juniper plantings. Heteroconis picticornis (= Spiloconis picticornis Banks) was introduced from Hong Kong in 1953. Several thousand were released against spider mites and scale insects infesting citrus and avocado groves in southern California by Badgley et al. (1955), but it did not become established. These researchers described the predator's biology. The flat or scalelike eggs take the shape of the contour of the surface upon which they are laid. The larvae pass through four instars in 16 to 32 days, and feed only on diaspine or lecanine scale insects, preferring crawlers and first- and

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second-instar scale. The fourth instar selects a crevice or crack in which to spin its three-layered silken cocoon. The adults feed on both spider mites (including citrus red mite and citrus rust mite) and scale insects. They lived longest (63 days) on scale crawlers, honey, and water (Badgley et al., 1955). Hemerobiidae Among the nearly 550 described species in 40 genera of brown lacewings in the world (which now includes the former family Sympherobiidae), about 50% are in two genera: Hemerobius and Micromus (New, 1988b; Monserrat, 1990). Oswald (1993) recognizes only 25 genera in the world and provides a key to the genera. The hemerobiids are predaceous in both adult and larval stages, feeding mainly on aphids, with evidently fewer alternate food sources than chrysopids (Killington, 1936; Balduf, 1939; New, 1975). Because the adults do not need to rely on honeydew for egg production, they can produce and deposit their eggs at lower aphid densities than do chrysopids (Neuenschwander et al., 1975). Even though brown lacewing larvae and adults are rather polyphagous, different species appear to be tied to certain habitats, [e.g., conifers, broad-leaved trees, or low vegetation (New, 1975; 1988a; Monserrat & Matin, 1996)]. The most interesting biological aspect of many hemerobiids is the remarkable low temperature thresholds of all stages ~ even lower than most of their prey species. Thus, the potential for using these predators in temperate climates during cool periods is great (Neuenschwander, 1975, 1976; New, 1975, 1984b, 1988a; Canard, 1997). Eggs are deposited singly on their sides; the conspicuous projecting polar micropylar knob distinguishes a hemerobiid egg from a syrphid egg. Larvae undergo three instars, do not carry trash, and can be recognized from chrysopid larvae by their smaller heads that jerk from side to side when moving. Pupation occurs in a loosely woven silken cocoon near the feeding areas. Hemerobiids have been used in biological control in classical, in augmentative, and in conservation programs. The species involved have been mainly in the genera Hemerobius or Micromus, but the biologies of some lesser known genera have been described [e.g., Boriomyia, which is aphidophagous (Laffranque & Canard, 1975); Drepanacra, which feeds mainly on psyllids (New, 1984b, 1988a); and Sympherobius, which is predaceous on mealybugs, has been mass-cultured and released against mealybugs attacking citrus (Bodenheimer, 1951) and in Europe it feeds on aphids and European red mite in apple orchards (Principi & Canard, 1974)]. Hemerobius is a widely distributed genus of about 220 species occurring in Africa, Asia, Australia, Europe, and North and South America (Laidlaw, 1936; Carpenter, 1940; Nakahara, 1965; Kevan & Klimaszewski, 1987; New 1988a; Monserrat, 1990). Several species are Holarctic. Hemerobius humilinus Linnaeus is a Holarctic species,

but it is rarely found west of the Rocky Mountains in the United States, whereas in Canada it ranges westward to British Columbia. In the eastern United States it is found in Pennsylvania vineyards (Jubb & Mastellar, 1977) and in apple orchards preying on aphids (Holdsworth, 1970a); in the laboratory its larvae consumed both codling moth eggs and first-instar larvae (Holdsworth, 1970b). In Europe, H. humilinus is 1 of 11 species of hemerobiids occurring in apple orchards (Szabo & Szentkiralyi, 1981), where it consumes aphids and European red mites (Principi & Canard, 1974); in China, it occurs in cotton fields (Chao & Chang, 1978). Hemerobius pacificus Banks is a common species west of the Rocky Mountains in the Nearctic region (Carpenter, 1940; Nakahara, 1965). In California, it mainly occurs along the coast where it is active as a general predator in low crops during the winter and early spring (Neuenschwander et al., 1975). Its temperature threshold for development is 0.4, 4.1, and 0.6~ for egg, larva, and pupa, respectively (Neuenschwander, 1975); and has a threshold of 4.4~ for reproduction (Neuenschwander, 1976). Neuenschwander and Hagen (1980) released 20 H. pacificus eggs per plant weekly in artichoke plots from October through the end of April. They demonstrated that Hemerobius populations had a great impact on overwintering green peach aphid populations, and even though first-instar larvae of the relatively rare artichoke plume moth, Platyptilia carduidactyla (Riley), served as a secondary food source, the impact of the lacewing was measurable at least at higher the moth densities. In plots treated with protein plus sugar sprays, the densities of H. pacificus indicated arrestment of adults, and eggs were about twice to four times higher in treated plots, resulting in lower green peach aphid and artichoke plume moth populations. Hemerobius stigma Stephens was found to be an effective predator of the balsam woolly aphid, Adelges piceae (Ratzeburg), in England (Laidlaw, 1936). About 5000 eggs of H. stigma and a few eggs of H. nitidulus Fabricius collected in England were sent to eastern Canada where A. piceae had invaded during the early 1900s (McGugan & Coppel, 1962; Mitchell & Wright, 1967). It was concluded that H. stigma and H. nitidulus did not become established, based on the assumption that the brown lacewings could not survive the winters (McGugan & Coppel, 1962). However, a common native species, H. stigmaterus, Fitch, was synonymized with H. stigma by Tjeder (1960); and Garland (1978a) points out the implications of the taxonomic problem, indicating that H. stigma was already in the New World. However, Nakahara (1965) considered both names to be valid and recommended withholding judgment utilizing studies of the Old World populations as compared with the variation in the New World populations. Garland (1978b) exposed eggs of H. stigma originating in Quebec, Canada, to overnight temperatures as low as -3.8~ and

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found they survived, indicating that eggs of this species survive occasional frosts. Micromus has a nearly cosmopolitan distribution and includes from 95 to 150 specific names (Klimaszewski & Kevan, 1988; New, 1988a; Monserrat, 1990; Oswald, 1993). Micromus spp. have been used in classical biological control programs as aphidophagous predators in a variety of crops and also have been manipulated in the field and in greenhouses (New, 1975, 1988b; Khloptseva, 1991). Micromus timidus Hagen (= vinaceus Gerstaecker) was imported from cane fields in north Queensland, Australia, in 1919 and became established in the Hawaiian Islands (Williams, 1931; New, 1988a). Micromus angulatus Stephens, a Holarctic aphidophagous species, can deposit as many as 2000 eggs and in France overwinters as an adult with its hibernal diapause being induced by short photoperiods (Miermont & Canard, 1975). In the former USSR, M. angulatus lives in colonies of aphids on soybeans, clover, maize, and cabbage plants near forest fringes and has two to three generations per year; it is mass-cultured in greenhouses using bean and pea aphids grown on horse beans as prey for adults and larvae. It successfully controls aphids on cucumbers in greenhouses at predator (eggs) to prey ratios of 1:1 or 1:3 and when released every 7 to 9 days (Khloptseva, 1991). Apparently there is no cannibalism on pupae when larvae of M. angulatus are reared on aphids (Stelzl & Hassan, 1992). Micromus posticus (Walker) occurs from Texas to Florida and north into Canada (Carpenter, 1940). It preys mainly on aphids infesting citrus groves, pecan orchards, vineyards, alfalfa, cotton fields, and potato fields [see references in Miller & Cave (1987)]. Descriptions of immature stages and life table data are presented by Miller and Cave (1987); they found that in unsprayed Alabama cotton fields only a percentage of M. posticus larvae were parasitized by an ichneumonid and the figitid Anacharis melanoneura Ashmead. In Florida citrus groves as well as in the laboratory, Selhime and Kanavel (1968) found M. posticus larvae were not parasitized by Anacharis sp; however, M. subanticus (Walker) larvae in citrus were heavily parasitized, which suggested that the rarity of M. subanticus in citrus groves was the result of parasitism. Micromus tasmaniae is a common Australian and New Zealand species that preys on aphids in alfalfa (Milne & Bishop, 1987); cotton aphids (Samson & Blood, 1979, 1980); rose aphids (Maelzer, 1977); potato aphids (Hussein, 1986); and aphids, Collembola, and mites on strawberries [determined by Butcher et al. (1988) using immunological testing for proteins]. New (1984b) found M. tasmaniae commonly associated with psyllids on acacias. Samson and Blood (1979) found M. tasmaniae had a lower voracity for Heliothis eggs and larvae than did chrysopid larvae or nabids. Temperature thresholds for development were determined by Samson and Blood (1979) and by New (1984b).

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Eggs of M. tasmaniae suspended in a 0.03% xanthan gum solution (Hussein, 1984) sprayed on potato foliage yielded enough larvae to reduce Myzus persicae populations by 70% compared with the aphid abundance on untreated potato plants, while the yield of potatoes from untreated plants was reduced by 40% (Hussein, 1986). The first lacewing eggs were sprayed on potato plots at the time alate M. persicae were migrating into the potato fields and then applied twice weekly over a period of 4 weeks. The genus Nusalala consists of 20 species found in North and South America (Oswald, 1993). In Brazil, N. uruguaya (Navas) larvae completed development on two aphid species but all died at the end of the first instar when fed Toxoptera citricidus (Kirkaldy) (Souza et al., 1990). The larvae are fast moving, only feed on live aphids, and exhibit cannibalism at low food availability (Souza & Ciociola, 1995). Order Coleoptera

Coleoptera comprise the greatest number of described species (ca. 300,000) of any order, and occur in all habitats except the depths of salty seas. Crowson (1981) reviewed the morphology and biology of Coleoptera including a chapter on predaceous beetles. Balduf (1935) extensively covered the literature on the biologies of entomophagous Coleoptera up to 1933. Keys to larvae of families and many subfamilies of the order have been written by Klausnitzer (1978) and Lawrence (1991a), but little is known about the ecological importance of the many species that live in soil and in water. Even the prey spectra of many predaceous families are poorly known. However, some of the most spectacular successes in classical biological control have involved the introduction and establishment of predaceous Coleoptera, and the roles that various endemic entomophagous Coleoptera play in the natural biological control of their prey are slowly being revealed. In a survey of the food habits of beetles, Townsend Glover (1868) listed only 11 families that contained predaceous species. Today about a third of the families (54) are known to contain predaceous species (Hagen et al., 1976a), including 47 terrestrial families (Hagen, 1987). Both larvae and adults are predatory in most families. Of the four suborders, Archostemata, Myxophaga, Adephaga, and Polyphaga, only the latter two contain species that have been involved in biological control studies.

Suborder Adephaga Of the 10 families that compose the Adephaga, four are terrestrial (Geadephaga): Rhysodidae, Paussidae, Cicindelidae, and Carabidae. The rhysodids apparently are not predaceous. The paussids, which are associated with ants, will not be discussed. The Carabidae is by far the most important family in Adephaga involved in biological control investigations.

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The six aquatic families of Adephaga (Hydradephaga), Haliplidae, Amphizoidae, Hygrobiidae, Noteridae, Dytiscidae, and Gyrinidae are all essentially predatory except the Haliplidae, but little is known about their impact on their prey populations. Cicindelidae Both cicindelid adults and larvae are predaceous. The adults are active hunters, while the larvae sit and wait for their prey. The family is considered a subfamily of Carabidae by some coleopterists, but the larvae of tiger beetles differ greatly from carabids in their morphology and habits. The following comments have largely been taken from Balduf (1935), Thiele (1977), and Pearson (1988). Adults of the fast-moving, typical, diurnal tiger beetles, Cicindela spp., are usually maculate and metallic with bulgy eyes, and are commonly seen in sandy localities either near water or inland. The tropical genera, Collyris and Tricondyla, are arboreal and have tarsal pads on all legs in both sexes. The diurnal species use their eyes to locate prey. The flightless, nocturnal, black, carabid-like Amblycheila and Omus species have relatively fiat, small eyes and probably rely on contact to attack their prey. The adults of the nocturnal South America Megacephalafulgida fulgida Klug evidently locate mole crickets by phonotaxis, orienting toward cricket songs (Fowler, 1987). The size of prey captured is related to the size of the tiger beetle. The adults seize their prey by their large sickle-shaped mandibles, which are armed on the inner side with several large teeth and a molarlike tooth near the base. They ingest the fluids of their prey and use preoral digestion (Evans, 1965). Pearson and Mury (1979) found a close correlation between mandible length and median prey size captured in 13 Cicindela spp. found at edges of ponds and in 6 grassland species in southeastern Arizona. Similar correlations have been found elsewhere in the world. The adults are general predators and attack insects, arachnids, and crustacea within certain size ranges. However, some larger species respond to aggregations of smaller prey. The diurnally active adults hide in soil during the night and may hibernate in rather long burrows in the soil. The terrestrial species dig a shallow hole in the soil and deposit eggs singly, while the arboreal species deposit eggs singly in tunnels made in twigs or bark. The larvae sit and wait for prey in burrows made in the soil or in wood. Their circular, camouflaged heads and pronota form closings to the entrances of their burrows. The larvae have two or three pairs of hooks on the tergum of the fifth abdominal segment that is used to anchor them vertically. When a prey comes within range, the larva strikes quickly, throwing its front and middle legs out clear of the burrow; its abdomen remains inside. The prey is seized by large, sickle-shaped, dentate mandibles and is consumed after the larva retreats into the burrow. Like the

adults, the larvae of tiger beetles appear to be general predators of certain size prey. There are three larval instars. Generally a 2-year period is required to complete development, but development can range from 1 to 4 years depending on the species. Pupation occurs within their larval burrows, which are plugged by the mature larva. Larvae of many species hibernate within their burrows. The impact of cicindelids on regulation of agricultural insect pests is poorly known, but several articles that are now in press cite Fowler's (1987) note concerning the predatory behavior of Megacephala fulgida, which clearly implicates this nocturnal species as a primary biological control agent in the regulation of early instar populations of Scaptericus mole crickets in Brazil. Pearson (1988) mentions a personal communication from J. H. Frank, who observed M. virginica (Linnaeus) as a major predator of introduced mole crickets in southeastern United States. Carabidae Of this huge family of approximately 40,000 described species of ground beetles, the biologies of less than 100 species have been investigated, mostly western European species (Ball, 1978). As common as carabids are, their effects on pest populations are poorly known, and only a few species have been utilized in classical biological control programs. Since Balduf's (1935) synopsis of carabid biologies, there had been no exhaustive reviews until Thiele's (1977) compilation of his personal investigations together with the existing knowledge of carabid biology and ecology, which resulted in a book on the physiological and behavioral adaptations of carabids in relation to their environments. Thiele's book; the proceedings of symposia dealing with carabids edited by Erwin et al. (1979), Brandmayr et al. (1983), and Den Boer et al. (1986), papers given at the sixth European Carabidologist's meeting published in the Acta Phytopathologica Entomologica Hungaricae, 22 (14), 1987; and Luff's (1987) review on polyphagous ground beetles in agriculture provided the main bases for the following comments. Carabid food habits range from being ectoparasitoids on specific insect hosts, to obligatorily carnivores, herbivores, and omnivores. Forbes (1883) analyzed the gut contents of 175 adult specimens representing 20 carabid genera and found that 57% of the food was of animal origin (of that percentage, 36% insects; and 27% mollusks, earthworms, myriapods, and arachnids); the vegetable matter eaten, which accounted for 43%, was fungi and pollen. Similar studies, reviewed by Thiele (1977), show that intestinal contents of a species varies through the year, and one cannot generalize about the food habits of sympatric congeneric species (e.g., one Harpalus sp. diet is 50% animal matter while another Harpalus sp. in the same area is nearly

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totally phytophagous). Apparently, it is quite common for carabids to feed partly on vegetable matter (Johnson & Cameron, 1969). Although Pterostichus, Calathus, and Agonum spp. at times eat plant materials, they feed mainly on insects such as ants, aphids, and lepidopteran larvae (Thiele, 1977). In his fine review, Allen (1979) not only lists the food habits of 156 North American carabid species taken from literature, but also lists 107 North American species that have been studied ecologically or biologically. The latest review on carabid food habits by Larochelle (1990) is exhaustive. Based on 1290 references, he concludes 775 species are exclusively carnivorous, 618 species are partially or exclusively entomophagous, 85 species are exclusively phytophagous, and 206 species are omnivorous. Larochelle states in general, "Carabids are opportunistic feeders, depending on available food. It is, therefore, presumed that following more comprehensive studies, carabids will appear more omnivorous." The oligophagous predators are found more among the primitive carabids such as Cychrini (Cychrus, Scaphinotus, Brennus), which feed mainly on slugs and snails (Larochelle, 1972; Greene, 1975; Digweed, 1993) and the Carabini (Carabus and Calosoma). Many species of Carabus feed on mollusks and earthworms. Some species have long mandibles in both their adult and larval forms and appear cychrine-like, feeding mainly on mollusks (Sturani, 1962; Malausa et al., 1983). Abax parallelepipedus (Piller & Mitterpacher) and Pterostichus madidus (Fabricius) also prey on slugs (Asteraki, 1993; Symondson & Liddell, 1993). Calosoma species are commonly called caterpillar hunters, and they do largely feed on lepidopteran larvae (Burgess, 1911; Burgess & Collins, 1917; Price & Shepard, 1978; Wallin, 1991). Young (1984) observed that C. sayi DeJean adults in the laboratory did not consume the very small or the very large lepidopteran larvae but they would consume living and dead non-lepidopteran insects. Pasimachus elongatus LeConte of the Scaritini fed on six species of Coleoptera as adults and on ants and termites found under cow chips as larvae; in the laboratory 23 adult orthopterans and 18 beetle species were eaten (Cress & Lawson, 1971). Notiophilus biguttatus Fabricius (Notiophilini) adults and larvae feed extensively on Collembola. Adults use their large eyes to hunt their prey during the day (Bauer, 1975). Metabolic rate and reproduction of this species are strongly correlated with the rate of Collembola taken in as prey (Ernsting & Issaks, 1987). As the carabid tribes become more derived, it appears that the feeding trends and structures become more omnivorous. The form of the feeding apparatus of adult carabids, particularly the mandibles, offers a clue as to the feeding habits. Zhavoronkova (1969) found distinct correlations between the nature of feeding by carabids and the structure of their mandibles and proventriculi, and she distinguished

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three main feeding categories: obligate zoophages, predominant zoophages, and predominant phytophages. Evans and Forsythe (1985), after comparing many external and internal structures associated with a diversity of carabid feeding habits, concluded that although parts of the feeding mechanism directly reflect the nature of the food of different group beetles, the mechanism as a whole reflects the method of feeding instead of the specific nature of the food taken. The mechanism also appears to be focused toward three main feeding methods: fluid feeding (in which preoral digestion is important), fragmentary feeding, and mixed feeding. Tips of mandibles can wear down with age (Houston, 1981; Wallin, 1988); thus the mandibles of fluid feeders can become so worn as to appear like mandibles of a mixed feeder of phytophage. Evans and Forsythe (1985) and Forsythe (1987) suggest that the head shape in carabids may reflect locomotory adaptations more frequently than feeding adaptation, and the form of the carabid body and the shape and articulation of legs reflect their habits more often than their habitats. According to Crowson's (1982) book review of Life Forms of Carabidae, edited by Sharova and Ghilarov (1981) (in Russian), Sharova composed a dichotomous key to the various life forms of adult and larval Carabidae based on food types, locomotory categories, and habitats coupled with morphological characters such as adult and larval mandibles and types of legs, larval urogomphi, general body form, and so on. The habitats of carabids are diverse and are located and returned to by kinetic responses to gradients of abiotic factors (Thiele, 1977). However, Evans (1983, 1988) reports that certain carabids locate their habitats by responding to kairomones or synomones emanating from their habitats. Evans found that Bembidion obtusidens Fall adults were attracted to volatile metabolites of blue-green algae growing in the habitats of the beetles and their prey. Wheater (1989) found some carabids detected prey visually, while others, particularly of the tribe Pterostichini, relied on olfactory cues. There are few data on the length of carabid preoviposition periods. Not ovipositing during the year they emerge as adults may be common with the larger carabids, like Calosoma and Carabus that have either estival or hibernal dormancy periods. In some cases, oviposition does not occur until the third year after emergence (Dusaussoy, 1963). Reproduction in some species is regulated by the action of day-length photoperiods on juvenile hormone levels (Ferenz, 1986). Some species lay a single batch of eggs per season (Luff, 1973), while others lay eggs continuously at a relatively constant rate (van Dijk, 1979; Baars & van Dijk, 1984). However, the quantity of food ingested and temperature is directly tied to egg production (van Dijk, 1983). Based on years of pitfall records, Den Boer (1986) has determined the net production (R) of 64 carabid species.

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A simulation energetics model involving ingestion rate of prey resulting in egg production rate was built by Mols (1987), which involves the use of a feedback mechanism associating gut capacity with ovarial sizemthe more eggs that are in the ovaries, the less the gut capacity, which inhibits feeding via reaction of the stretch receptors in the abdomen. Carabids have been divided into spring breeding and fall breeding species depending on which season they lay their eggs. The spring breeders hibernate or enter diapause as adults, reproduce from spring to early summer, and then usually die. The fall breeders reproduce in autumn, usually hibernate as larvae, and estivate as adults. Thiele (1977) lists 36 spring breeding species and 21 fall breeding species. Of these, about 60% are nocturnally active and 22% predominantly active during the day, while 18% were variable. Eggs are usually deposited singly in the soil. However, Thiele (1977) lists 14 species in the Pterostichini that have been observed to dig a "nest" in soil or rotting wood and to deposit a group of eggs that the female remains with until the larvae hatch. Carabid larvae predominantly have three instars but some species have only two, and a few species have been reported to have four and five instars. Most larvae have similar type mandibles, with a single cutting edge with a retinaculum but without a suctorial tube or channel, and usually have prominent urogomphi (Thompson, 1979). The larvae of many species are predaceous. Others are phytophagous or omnivorous and some are ectoparasitoids, but the feeding habits of larvae are only known for relatively few species; of the 156 published feeding records of North American carabids listed by Allen (1979), 67 refer to larval feeding. Carabid larvae often kill more prey than they can consume. Once fully grown, the larvae form cells in the soil or rotting wood and pupate. The pupal period is about 1 week during the summer. Large, showy carabids were among the first beetles observed to be predaceous on caterpillars and manipulated to biologically control insect pests in Europe. In the early 1900s, Calosoma sycophanta (Linnaeus) was successfully introduced into the United States from Europe to control gypsy moth (Burgess, 1911; Howard & Fiske, 1911). This success stimulated the first detailed studies on carabid biology. Burgess and Collins (1917) described the biologies of over 30 Calosoma spp. Not until the 1960s did research on carabid biology resurge widely (Kulman, 1974; Thiele, 1977), and not until the 1980s were carabids considered again for use as biological control agents (Luff, 1987) Thiele (1977) concluded from his experiences and a review of carabid research that even though there is little hope of combating pests biologically with ground beetles, their role in natural control of many invertebrates in certain

ecosystems should be considered when developing integrated control programs and carabids could be imported in certain classical biological control programs. One of the few classical biological control attempts involving carabids was the introduction of C. sycophanta from Europe (mostly Switzerland) between 1905 and 1910. Of the 4000 Calosoma imported, 67% were released against the gypsy moth in the New England states, which resulted in C. sycophanta becoming established (Burgess, 1911). As Clausen (1956) stated, evaluating a predator of this type is difficult, but the abundance and general distribution of C. sycophanta in the areas heavily infested by the gypsy moth warrant the belief that it is one of the most important of the imported natural enemies of this pest as well as other introduced forest lepidopteran pests. From his behavioral and ecological field studies in New England on the abundance and movement of C. sycophanta in relation to gypsy moth populations, Weseloh (1985a, 1985b, 1987, 1990, 1993, 1997) correlated that a relatively low number of adult beetles can have a substantial impact on the moth populations. On the average, 40% of pupae present in his study area were destroyed by Calosoma larvae. According to Burgess (1911), a larva can kill over 50 fully grown gypsy moth larvae during a 2-week period, and the adults (which live for 2 to 4 years) in one season consume on the average about 150 large larvae. The slow numerical response of C. sycophanta is perhaps the result of its prolonged preoviposition period. Dusaussoy (1963) found that the adult C. sycophanta has a hibernal diapause and eggs are rarely produced the first year. Because none of our native Calosoma species are as arboreal in larval stages as C. sycophanta (Gidaspow, 1959), there is little competition from other predators for gypsy moth larvae and pupae. Luff (1987) reviewed the literature dealing with carabids associated with agricultural insect pests that had concentrated on aphids in north European cereal fields. Since then, carabid research on other pests in a variety of crops has expanded. In alfalfa, carabids had some impact on aphids and weevils (Lester & Morrill, 1989), and the search pattern of Calosoma affine Chaudoir was altered by high populations of Colias and Spodoptera caterpillar populations (Wallin, 1991). In apple orchards, carabids and other ground-dwelling arthropod predators were found to prey on apple maggot larvae and pupae (Allen & Hagley, 1990). Eight carabid species taken from pitfall traps in an apple orchard gave positive serological reactions to antiserum against codling moth larvae (Hagley & Allen, 1988); and Anisodactylus californicus Dejean, Harpalus pensylvanicus DeGeer, and three Pterostichus species were determined to be capable of killing and consuming mature codling moth larvae (Riddick & Mills, 1994). Pterostichus species were found to dominate the carabid community in an unsprayed apple orchard in California (Riddick & Mills, 1996) and

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predation of tethered codling moth larvae was estimated to be 60% per night during the first generation of the codling moth in spring (Riddick & Mills, 1994). Bean fields managed by a low-input cropping system had a different complex of carabid faunas compared with fields managed by conventional methods, and the complex differed from yearto-year in both systems (Fan et al., 1993). Chen and Willson (1996) documented the carabid community in soybean fields and Tonhasca (1993) reported variable response of carabid numbers in tilled versus nontilled soybeans grown both as a monoculture or an intercrop with corn. The cabbage root fly is susceptible to carabid predation (Varis, 1989; Finch & Elliot, 1992; Finch, 1996). In cereal fields (mostly barley and wheat) infested with aphids, carabids varied in number and species depending on cultural and pesticide applications (Chiverton, 1987, 1988; Helenius, 1990; Basedow et al. 1991; Chiverton & Sothern, 1991; Anderson, 1992; Ekbom et al., 1992; Lys et al., 1992; Wallin et al., 1992; Helenius et al., 1995), but there is some evidence suggesting that aphids may not be an important food for many of the generalist carabids in cereal fields (Bilde & Toft, 1997). In corn fields, large carabids did not return to paraquat- and glyphosate-treated field areas until about 28 days after application; thus, lower rates of predation of early-season lepidopteran pests by these carabid species may occur in no-tillage corn fields that utilize herbicides (Brust, 1990). Low tillage and the presence of broadleaf weeds also increase the activity density of carabid beetles in corn fields, although the weeds adversely affected corn yield (Pavuk et al., 1997). From four genera 14 carabid species were identified by immunoelectro-osmophoresis to have fed on wheat midge larvae (Floate et al., 1990). In potato fields, 19 carabid species were collected in pitfall traps, but were generally lower in sprayed than in unsprayed plots for a few days after application. There was a differential feeding by carabids of aphids on plants and those that fall to the ground (Dixon & McKinlay, 1992). Kromp (1990) found up to 48 carabid species in potato fields, and the total carabids and number of species were always higher in biological (organic) farmed fields than in conventionally farmed plots; he named four species that can be considered bioindicators for biologically farmed agroecosystems. Hance (1987) placed three species of carabids in sugar beet field cages with different levels of Aphis fabae. He found that all three species produced important reductions in aphid populations and that carabid density was a major factor in predator efficacy. In Michigan onion fields, a Bembidion species preys on eggs and first instars of the onion maggot. In field cage studies, this species reduced maggot numbers by up to 57%; thus, it may be an important biocontrol agent (Grafius & Warner, 1989). The largest of four carabid species tested, Pterostichus melanarius (Illinger), consumed the greatest number

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of carrot weevil eggs laid on carrot leaves (Zhao et al., 1990).

Suborder Polyphaga Among the 44 terrestrial families of suborder Polyphaga that contain predatory species, 14 have been involved in biological control studies of arthropod pests. That is not to imply that the other families do not contain important natural enemies, because all the predaceous species of Polyphaga have some influence in their ecosystems.

Cleridae Cleridae is a large, mainly tropical family of brightly colored beetles. The best known genera are Enoclerus and Thanasimus, which are predators of scolytid bark beetles. The majority of species appear to be subcortical predators of boring beetles on woody plants, but Phyllobaenus is generally associated with Lepidoptera (Wingfield & Warren, 1968; Farrar, 1985) and Trichodes and Lecontella are associated with Hymenoptera (Krombein, 1967; Bitner, 1972). Other genera, such as Necrobia and Corynetes, are associated with carcasses and skins and can be pests of stored meats. Detailed biological information on clerids is largely confined to the better known species that are scolytid predators, although an example of a Phyllobaenus sp. parasitizing an ant-plant mutualism in the tropics (Letourneau, 1990) provides an interesting, if aberrant, example of clerid biology. Thanasimus species occur throughout the Holarctic region and are important predators of Dendroctonus, Ips, and Scolytus bark beetles (Mills, 1983). Enoclerus species are also important predators of Dendroctonus bark beetles in western North America (Dahlsten, 1982). Adult clerids feed on adult scolytids as they aggregate to attack the host trees. Eggs are laid under the bark scales and the larvae enter the scolytid galleries to feed on the developing brood. Larger larvae are able to bore through the bark, but may also walk across the bark surface to move between galleries. Pupation occurs in cells in the bark toward the base of the trees. Clerids can overwinter as adults, as larvae, and as prepupae in pupal cells. The consumption of scolytid adults by adult clerids varies from 0.5 to 2.5 individuals per day (Berryman, 1966b; Turnbow et al., 1978; Schlup, 1987). Mean adult longevity for E. lecontei (Wolcott) is 70 days (Berryman, 1966b), for Thanasimus dubius (Fabricius) is 117 days (Mizell & Nebeker, 1982a), and for T. formicarius (Linnaeus) is 127 days (Schlup 1987). Mean fecundity of E. lecontei is 515 with individuals able to produce up to 1000 eggs (Berryman, 1966a) and that of T. formicarius is 1439 (Schlup, 1987). There appear to be three larval instars, although this may be variable because from two to five instars have been reported in the literature. The duration of development from egg to adult is 61 days for E. lecontei (Berryman, 1966b)

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and 70 days for T. formicarius (Schlup, 1987). The predation potential of the larval stages has been estimated as 44 I. typographus Linnaeus larvae for T. formicarius (Mills, 1985) and 12 D. brevicomis LeConte larvae for E. lecontei (Berryman 1966b). The adults and larvae are cannibalistic but can readily be reared in the laboratory (Lawson & Morgan, 1992). Adults require scolytid food for oviposition (freeze-stored scolytids are often acceptable) and larvae can be fed on almost any animal-based food such as stored product insect larvae (Mills, unpublished). Clerid beetles use olfactory cues in host location (Davis et al., 1983; Payne et al., 1984). For example, both sexes of T. dubius are attracted by components of scolytid aggregation pheromones: frontalin used by Dendroctonus frontalis Zimmermann; ipsdienol used by Ips species; and alpha-pinene, a host tree volatile (Mizell & Nebeker, 1982b; Lindgren, 1993). There is geographic variability in the enantiomeric composition of ipsdienol in L pini (Say) populations in North America and this is matched by variation in the response of local populations of T. dubius to enantiomeric mixtures of ipsdienol, which results in some prey populations escaping predation (Raffa & Klepzig, 1989; Herms et al., 1991). Given a choice of several prey, T. dubius preferred L arulus (Eichhoff) over D. frontalis (Mizell & Nebeker, 1982a). Clerid beetles are often dominant members of the natural-enemy complexes of scolytids and must contribute significantly to the natural control of these pests. For example, Reeve (1997) provides evidence that populations of D. frontalis decline when the abundance of T. dubius is high. Similarly, T. formicarius has been estimated to cause from 5 to 53% mortality of I. typographus brood (Mills, 1985) and from 48 to 52% mortality of Tomicus piniperda (Linnaeus) brood (Gidaszewski, 1974). Similarly, Weslian and Regnander (1992) report a 45% reduction in L typographus brood emergence from bolts caged with Thanasimus formicarius. The Palearctic T. formicarius and the Nearctic T. dubius are the only clerid species to have been used in classical biological control against bark beetles [although another clerid, Callimerus arcufer Chapin, was introduced into Fiji by Tothill et al. (1930) against the coconut moth without becoming established]. Unsuccessful releases of T. formicarius were made against D. frontalis in North America in 1894 and in 1980 (Miller et al., 1987), but apparently T. dubius has become established in Australia against L grandicollis (Eichhoff) (Berisford & Dahlsten, 1989; Lawson & Morgan, 1992). Both Berryman (1967) and Moeck and Safranyik (1984) discuss means of preserving and augmenting native clerid predators of scolytids. Coccinellidae The 3500 or so lady beetles in the world are divided into seven subfamilies" Chilocorinae, Coccidulinae, Coccinellinae, Epilachninae, Hyperaspinae, Litho-

philinae, and Scymninae. Most species are predaceous, except those in the Epilachninae (which are all phytophagous) and in the tribe Psylloborini of the Coccinellinae, which contains mostly mycophagous species; the feeding habits of the Lithophilinae are apparently unknown. The predaceous species often consume pollen or extrafloral nectar and honeydew when their prey are scarce (Carter & Dixon, 1984; Hagen, 1986). The bionomics of many coccinellids are similar at the tribal level and have been reviewed by Balduf (1935), Clausen (1940), Hagen (1962, 1974), and Hodek (1967, 1973, 1986). The taxonomic revisions of the Coccinellidae of Japan (Sasaji, 1971) and North America (Gordon, 1985) and revisions of Coccinellinae of the Palearctic and Oriental regions (Iablokoff-Khnzorian, 1982) and Australia (Pope, 1988) discuss the known prey range of various taxa. The prey spectra are fairly similar, at least at the genetic level if not at the tribal level (Schilder & Schilder, 1928). In almost all predaceous species, the adult female must feed on its prey to produce eggs. The form and placement of eggs are also similar at the genetic level. There are almost always four larval instars that generally have many similar morphological characteristics at the tribal level. The adults and larvae of the predaceous species have mandibles with one or two teeth at the apex while the mandibles of Epilachninae and Psylloborini have three or more teeth apically (Savoiskaya & Klausnitzer, 1973; LeSage, 1991; Samways et al., 1997). Many larvae in the Scymnini, Ortaliini, Hyperaspini, Coccidulini, Novini, Cryptognathini, Azyini, and Telsimiini have conspicuous waxy coatings and filaments (Pope, 1979). However, within genera such as Scymnus or Hyperaspis, there are some species that do not produce waxy filaments. Larvae feed on the same prey as adults, but early larval instars may not be able to penetrate the integument of the larger prey. Pupation occurs near the larval feeding site. Basically there are three types of pupae: those that pupate within their last larval exuviae (skin) that envelops the pupae except for a dorsal split (Chilocorinae, Novini); those where the last larval exuviae covers only the ventral surface of the body including the head (Hyperaspini); and those where the last larval exuviae is pushed back and covers the anal end of the pupae, which stands more erect on the substrate (most other species) (Phuoc & Stehr, 1974). Many coccinellids in the temperate zones are univoltine, usually being active in the summer and dormant during the winter. However, in the Mediterranean-type climatic zones, the reproductive activity is limited to the spring, thus their dormancy spanning the estival, autumnal, and hibernal periods with no oviposition for at least 9 months; during dry summers many species are bivoltine, being active and producing young in the spring and fall and being dormant during the summer and winter. In the subtropics and tropics, coccinellids may have continuous generations. Dor-

Chapter 16

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mancy occurs in the adult stage, usually as a reproductive diapause that can be induced by nutrition, photoperiod, temperature, or combinations of these (Hodek, 1973). Hippodamia convergens Guerin-Meneville is facultative in responding to adverse conditions and has exhibited all the preceding voltinisms in California (Hagen, 1962, 1974). Warm temperatures (> 18~ can offset the influence of short photoperiods during the fall and winter on H. convergens adults, which permits reproduction if enough aphids are available (K.S. Hagen, unpublished data). Coccinella septempunctata Linnaeus is more sensitive to photoperiods and is univoltine in northern latitudes, intermediate in middle latitudes, and multivoltine in southern latitudes. Thus, it is more obligatory in responding to physical conditions instead of biotic factors in its diapause induction (Hodek, 1973). In some coccinellids diapause is not expressed, [e.g., Rodolia cardinalis Mulsant, which just slows its development when temperatures are low (Quezada & DeBach, 1973)]. The searching sequence adult coccinellids use in locating their prey and ovipositional site is similar to that of other natural enemies and is composed of searching for suitable habitats (plants), searching on plants for prey, and capturing and accepting prey (Hodek, 1993). However, some captured prey may not be suitable for sustenance and reproduction and may even be detrimental (Hattingh & Samways, 1992). Apparently, vision plays a dominant role in adult coccinellids locating habitats because there are only a few cases where synomones (plant volatiles that influence host selection of entomophagous insects) have been shown to be involved [e.g., Kesten (1969) found Anatis ocellata (Linnaeus) adults more attracted to pine needle volatiles]. There also seems to be a response to the height of plants; thus general plant habitats such as trees (conifers or deciduous), shrubs, or herbs (Hodek, 1973, 1993; Mills, 1981) can be recognized as sources of essential or alternate prey. The searching behavior of the adult coccinellids can be influenced by the variations in architecture and morphology of different plant species, and even between plant varieties. The search rate and success of finding psyllid nymphs by adult Curinus coeruleus (Mulsant) are influenced by the width of subleaflets of the leucaena trees (Da Silva et al., 1992). Adults of Coccinella septempunctata Linnaeus and H. (Adonia) variegata (Goeze) searching a normal pea variety, fell off the plant nearly twice as frequently as they did on a leafless variety (Kareiva & Sahakian, 1990). A comparative study of the foraging of coccinellids on crucifers indicated a much greater influence of plant architecture on the rate of predation of cabbage aphids than of coccinellid species (Grevstad & Klepetka, 1992). The differences in the abundance and type of pubescence present can have an effect on coccinellids as well as on other natural enemies in their success of controlling arthropod pests; smaller cocci-

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nellid species and younger instars are particularly sensitive (Obrycki, 1986). On glabrous leaves with a slippery wax layer, larvae could move only along the edge or on narrow protruding veins (Shah, 1982). Adult prey searching on plants appears to be random until contact with a prey is made, although phototactic and geotactic responses may be involved. However, there is now some evidence that chemotactic and vision responses are also important. Colburn and Asquith (1970) found that Stethorus punctum (LeConte) adults were preferentially attracted to samples with European red mites in an olfactometer, indicating a distinct (volatile) kairomone is involved in detecting the prey. Obata (1986) used permeable gauze bags and nonpermeable transparent plastic bags to determine that aphidophagous Harmonia axyridis (Pallas) adults were attracted visually and olfactorily to both aphids and leaves before actual contact occurs. Visual and olfactory cues were found to be important for host location by adult Chilocorus nigritus (Fabricius), although not for larvae (Hattingh & Samways, 1995). Diomus hennesseyi Ftirsch (a small scymnine) and Exochomus flaviventris Mader (a medium-sized chilocorine) are predators of the cassava mealybug in Africa; females of these two species spent more time searching on cassava leaves previously infested with cassava or citrus mealybugs than on clean cassava leaves, indicating that the wax and/or honeydew (both products of the mealybug) contained a contact kairomone; wax from the cassava mealybug arrested both coccinellid species, and honeydew excreted by cassava mealybug arrested Exochomus and inexperienced Diomus (van den Meiracker et al., 1990), and Heidari and Copland (1993) concluded that mealybug honeydew was both a food and an arrestant for Cryptolaemus montrouzieri (Mulsant). Vision was shown to be involved in C. septempunctata adults; they detected prey (pea aphids) and a silver foil dummy about 1 cm away prior to physical contact (Stubbs, 1980). Nakamuta (1984), using a video recorder, determined that adults of C. septempunctata bruckii Mulsant visually oriented toward prey at a distance of 7 mm, and 8 mm away from a dummy aphid under light conditions; under dark conditions, they did not orient toward prey even at 2 mm, but quickly responded to prey on contact. Maxillae are involved in contact and capture of prey; amputation of the maxillary palpi decreased the number of prey captured or consumed (Nakamuta & Saito, 1985). Once a prey has been contacted or eaten, an adult coccinellid, like many other hunting predators, changes its searching behavior from a direct or smoothly curved search path to a convoluted complex path (marked by slower speeds and increased number of turns); thus, the beetle tends to stay in the vicinity of the site where the first prey was consumed. This foraging behavior was observed for Hippodamia convergens adults by Rowlands et al. (1978).

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For C. septempunctata brucki adults, the switch from an extensive search to a concentrated one is stimulated by the contact with a prey instead of the consumption of it (Nakamuta, 1986). The search for prey by adults of some Hippodamia, Coccinella, and Coleomegilla spp. can be arrested and concentrated in the field by the presence of artificial diets (containing sugars) that are sprayed on crops (Ewert & Chiang, 1966; Hagen et al., 1970a). Leaf extract and wood extract from Berberis vulgaris (Linnaeus) enhanced oviposition of C. septempunctata when sprayed on cherry trees (Shah, 1983). In the field, the number of aphidophagous coccinellids present is correlated with aphid population densities (e.g., Niemczyk & Dixon, 1988; Ferran et al., 1991; Ives et al., 1993). However, the numerical response of aphidophagous coccinellids is probably limited by satiation (Mills, 1982b), egg cannibalism (Mills, 1982b), reduced oviposition in the presence of conspecific larvae (Hemptinne et al., 1992), and optimal foraging across ephemeral patches of prey (Kindlmann & Dixon, 1993). It has long been known that coccinellid larvae conduct the same searching behavior as that described earlier for the adults, but often the forelegs as well as the head are involved in detecting prey (Fleschner, 1950; Banks, 1954, 1957; Dixon, 1959; Kaddou, 1960; B~insch, 1964, 1966; Storch, 1976; Hunter, 1978; Stubbs, 1980; Carter & Dixon, 1982, 1984; Obata, 1986). Direct contact with a prey is not always necessary before attack because fourth-instar larvae of C. septempunctata can detect an aphid 0.7 mm away (Stubbs, 1980). In the presence of honeydew, larvae spend longer periods searching in the restricted search area than if honeydew were not present (Carter & Dixon, 1984; Heidari & Copland, 1993). A C. septempunctata larva can detect a chemical marker that it secreted on plants previously searched unsuccessfully, thus reducing the retracing of its own path (Marks, 1977). The ability to capture aphids varies with the relative sizes of predator and prey and the various escape strategies of the latter, including maintaining a low profile (flat sessile aphids), walking away or dropping from the plant on sighting a coccinellid (larger predators are more conspicuous), kicking or pulling away if an appendage is grasped, and "waxing" the predator with paralyzing substances secreted from the siphunculi (Dixon, 1958, 1970; Brown, 1972a; Wratten, 1976; Hajek & Dahlsten, 1987). Some prey species are not only nutritionally unsuitable but also distasteful or even toxic to coccinellids, while some prey that are suitable for some species are not for others (Blackman, 1965; Iperti, 1965; Hodek, 1966b, 1973; Hukusima & Kamei, 1970; Hukusima & Komada, 1972; Rogers et al., 1972; H~im~il~iinen et al., 1975; Mills, 1981; Morales & Burandt, 1985; Obrycki & Orr, 1990; Hattingh & Samways, 1992; Hodek, 1993). An aphid species can be toxic in the spring but not in the fall (Takeda et al., 1964).

Different morphs of the green peach aphid fed on by H. convergens influenced levels of egg production (Wipperftirth et al., 1987). When the greenbug from two different resistant cultivars of resistant sorghums were fed to H. convergens larvae, the larval-pupal survival was reduced and the developmental time was extended compared with larvae fed greenbugs reared on a susceptible sorghum hybrid (Rice & Wilde, 1989). Only three generations at most of Harmonia conformis (Boisduval) could be reared on aphids, but when fed acacia psyllids, continuous generations were produced (Leeper & Beardsley, 1976). This may explain why several earlier introductions against several different aphid pests in the Hawaiian Islands failed. Larvae of the aphidophagous H. axyridis continuously reared on grain moth eggs or pea aphids led to conditioning in search behavior: only larvae that ate the same prey as they were reared on adopted intensive searching movements after feeding, and Ettifouri and Ferran (1993) concluded that using larvae reared on substitute prey in biological control systems may decrease the efficiency of released predators. Some plants synthesize toxins (e.g., glycoside) that are sequestered by certain aphids and can deter coccinellids from eating them (Hodek, 1966b; Nishida & Fukami, 1989). Colorful aphids are often not consumed by lady beetles (Johnson, 1907). When Hippodamia (Adonia) variegata larvae feed on A. nerii Fonscolombe infesting Cionura erecta (Linnaeus) (Asclepiadaceae), the resulting coccinellid adults are either brachypterous or apterous; if these deformed adults are fed aphids from a different species of host plant, the progenies are normal (Pasteels, 1978). Sequestering toxins from plants is not limited to aphidsm coccids such as the cottony-cushion scale are toxic to vedalia beetles when the scales are infesting certain Spartium or Genista species (Balachowsky & Molinari, 1930; Poutiers, 1930). Plant toxins may have been involved in Thompson' s (1951) failure to establish 13 coccinellid species to control two diaspine scales attacking Bermuda cedar. All species developed in cloth bags coveting scales on tree branches; however, when the coccinellids were liberated, only one species became established, indicating that the coccinellids were more fastidious than formerly believed. Biological Control with Coccinellidae Historically, a few species of coccinellids played key roles in the development of the three tactics now employed as part of the biological control strategy. The successful introduction of the vedalia beetle, Rodolia cardinalis, into California from Australia in 1888 controlled the cottony-cushion scale in 1 year, and provided the "breakthrough" for the development of the classical biological control tactic (Essig, 1931; Doutt, 1958, 1964; Caltagirone & Doutt, 1989). Since then, there have been many different exotic coccinellid species introduced against various homopterous pests around the world,

Chapter 16 TerrestrialArthropod Predators of Insect and Mite Pests but relatively few have become established. More coccidophagous species have been established than aphidophagous ones. The failure of another lady beetle (the mealybug destroyer, Cryptolaemus montrouzieri), which was unable to survive inland California winters after its introduction from Australia, sparked the research to develop the first augmentation tactics by mass-producing the predator for release in citrus groves infested with mealybugs each spring (Smith & Armitage, 1920). During the 1920s and 1930s there were 16 insectaries that mass-cultured the mealybug destroyer for periodic colonization, being the first modem system that formed the basis of the augmentation tactic of biological control. There are still a few insectaries producing Cryptolaemus, and it remains one of the few coccinellid species that is mass-cultured commercially (Fisher, 1963). Several native Hippodamia spp. responded to the spotted alfalfa aphid, (Therioaphis maculata Buckton) invasion in California, a phenomenon that led to development of the California integrated control concept during the late 1950s (Stem et al., 1959). Before any parasitoids were widely established and spotted alfalfa aphid-resistant plantings became widespread, native predators essentially controlled this aphid during the spring and fall, although they were usually not sufficiently abundant during the summer to provide control. Therefore, by applying only a single application of a selective aphicide (instead of the accepted 3 to 10 treatments of broad-spectrum insecticides), Hippodamia and other generalist predators (mainly Heteroptera) survived, resulting in predator to prey ratios that gave control during the summer (Stem et al., 1959; Smith & Hagen, 1966; Neuenschwander et al., 1975). This integration of chemical and biological control agents is a conservation tactic commonly used today in biological control. The role of coccinellids in biological control of general insect and arthropod pests has been reviewed by Essig (1931), Iperti (1961), Hodek (1966a, 1967, 1970, 1973, 1986), and Hagen (1962, 1974); in control of aphids, by Iperti (1965), Hagen and van den Bosch (1968), van Emden (1972), Frazer and Gilbert (1976), and Frazer (1988a, 1988b); and in control of diaspine scales, by Drea and Gordon (1990). Among the Coccinellidae there is a striking contrast between coccidophagous species that have frequently been successfully used in biological control and aphidophagous species that have in general been unsuccessful in biological control. From field observations on Adalia bipunctata (Linnaeus), Mills (1982b) suggested two factors that might account for this pattern. First, coccidophagous species tend to be small and feed continuously, while the aphidophagous species include some of the largest coccinellids that are characterized by long periods of inactivity due to satiation. Second, the aphidophagous species lay their eggs in batches on the surface of the host plant where they are subject to density-dependent cannibalism, whereas the coccidopha-

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gous species lay their eggs singly or in small groups often concealed beneath the prey where they escape the constraints of cannibalism. Hemptinne et al. (1992) considered that for progeny to be able to complete their development, aphidophagous coccinellids must synchronize oviposition with the early development of ephemeral aphid populations. They provided evidence that A. bipunctata avoids oviposition at later stages of aphid population development through an inhibition response to the presence of conspecific larvae, and argue that this response, in addition to satiation and cannibalism, may limit the effectiveness of aphidophagous coccinellids in biological control. However, Merlin et al. (1996) demonstrated a similar oviposition deterrent response for the coccidophagous species C. montrouzieri. Dixon et al. (1997) considered the success of coccidophagous coccinellids in biological control to be determined by their smaller generation time ratio, the generation time of the cocinnellids relative to that of their prey. They provided supporting evidence from a comparative analysis of generation times of coccinellids, aphids, and coccids, indicating that although aphidophagous species have shorter generation times than coccidophagous species, the telescoping of aphid generations leads to a mean generation time ratio of 2.4 for aphidophagous species in contrast to 0.6 for coccidophagous species. The coccinellid species that have been utilized in biological control are from the subfamilies Chilocorinae, Coccidulinae, Coccinellinae, Hyperaspinae, and Scymninae. Chilocorinae is a subfamily divided into three tribes, the Chilocorini, Platynaspini, and Telsimiini. The Chilocorini has over 200 species in 18 genera with representatives in all parts of the world (Chapin, 1965b). Most species are coccid or mealybug feeders and often deposit single eggs under scale coverings. Five genera contain species that have been utilized in biological control: Chilocorus, Cladis, Curinus, Exochomus, and Halmus (which included some species formerly placed in Orcus). Chilocorus is a large genus of about 70 species that mainly occur in Palearctic and Ethiopian regions and prey on 11 different genera of diaspine scales. Several species have been successfully introduced to control scales. Chilocorus bipustulatus (Linnaeus) from Israel was established in California against Parlatoria oleae (Colvee) (Huffaker & Doutt, 1965), and a strain from Iran gave substantial to complete biological control of P. blanchardi Targioni in Mauritania and Morocco (Iperti & Laudeho, 1969; Iperti et al., 1970). It also became established in Niger (Stansly, 1984). After C. cacti (Linnaeus) from Cuba became established in Puerto Rico and caused the reported extinction of Pseudaulacaspis pentagona (Targioni-Tozzetti), the predator disappeared for years (Wolcott, 1960), but it still contributes to control of the scale (Cock, 1985). Chilocorus circumdatus (Schonherr) was introduced from South China

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in 1895 by Koebele into the Hawaiian Islands where it became established and feeds on coccids and diaspine scales (Leeper, 1976). Chilocorus kuwanae Silvestri has been introduced into the United States and China several times since 1895 (as C. similis Rossi or C. kuwanae), but has become established only in the Santa Barbara area (Smith, 1965). Chilocorus kuwanae from Korea was introduced into the Washington, DC area in 1984 against the euonymus scale, Unaspis euonymi (Comstock). After 3 years, the predator had greatly increased in number and drastically had reduced the scale populations on test plants (Drea & Carlson, 1987; Hendrickson et al., 1991). Chilocorus nigritis (Fabricius) is an economically important biological control agent of red scale on citrus in southern Africa (Samways, 1984, 1989; Samways & Wilson, 1988). Chilocorus nigritis is apparently endemic to Reunion, A1dabra, or Madagascar, was inadvertently introduced into Kenya (Greathead & Pope, 1977) and southern Africa, and now has been successfully colonized in eastern Africa by utilizing nontarget scale insects grown on bamboo near citrus orchards. Chilocorus bipustulatus and C. infernalis Mulsant have been introduced into South Africa (Hattingh & Samways, 1991, 1992) and New Zealand (Hill et al., 1993). Chilocorus nigritis has been released and established on islands in the Indian Ocean (Greathead, 1971; Rao et al., 1971) and in the Hawaiian Islands (Leeper, 1976), and is established in Brazil (Samways, 1984) and in Oman (Kinaway, 1991). The genus Cladis has only a single species, C. nitidula (Fabricius), which occurs on various West Indian islands and has been reported from Buenos Aires (Chapin, 1965b). This species was introduced into Puerto Rico against the coconut scale, but it was more effective as a predator of Asterlecanium bambusae (Boisduval) (Cock, 1985). Curinus is also a monotypic genus whose sole representative, C. coeruleus Mulsant, is endemic to the Neotropics, but has been widely distributed in the Pacific area against the leucaena psyllid (Waterhouse & Norris, 1987). Exochomus metallicus (Korschefsky) and E. quadripustulatus (Linnaeus) have been introduced against coccids and successfully established in California. The former species is from Eritrea, Ethiopia, and is found only in the Santa Barbara area (Gordon, 1985); the latter species is found along the California coast on a variety of scale insects (Essig, 1931; Gordon, 1985). In Africa, E. flaviventris Mader has become one of the most common endemic coccinellids to prey on the exotic cassava mealybug (KanikaKiamfu et al., 1993). Halmus chalybeus (Boisduval) was sent to many locations in California from Australia in 1892 and into the Hawaiian Islands in 1874 by Koebele as Orcus chalybeus (Essig, 1931); it became established in the Santa Barbara area of California (Gordon, 1985) and in several Hawaiian Islands. Eguis platycephalus Mulsant principally a predator of

bamboo scales, was established in Puerto Rico from Cuba (Cock, 1985). The tribe Telsimiini contains a few species in Telsimia, which are from Asia and Oceania. Telsimia nitidae Chapin was introduced from Guam to the Hawaiian Islands in 1936; in the Hawaiian Islands it preys on coconut scale and Pinnaspis buxi (Bouche) (Leeper, 1976).

Coccidulinae is a subfamily that contains some of the most important species used in classical biological control. Among its genera are Rhizobius and Rodolia of worldwide fame, and also Azya and Pseudoazya, which include a few species that have been successfully imported and established. Azyini is primarily a Neotropical tribe composed of two genera, Azya with 14 species and Pseudoazya with 6 species (Gordon, 1980). The members of Azyini are all "scale" predators (armored, soft, and mealybugs). They deposit single eggs horizontally on or near their prey. Azya oribgera Mulsant was introduced into the Hawaiian Islands from Mexico by Koebele in 1908 and has been reported to feed on Coccus viridis (Green) and Ferrisiana virgata (Cockerell) (Leeper, 1976). Azya oribgera also is established on Guam (Chapin, 1965a) and was accidentally introduced into Florida (Woodruff & Sailer, 1977). It became established in Bermuda in 1957 and achieved good control of Pulvinaria psidii Maskell and apparently maintains itself in spite of the heavy predation on the coccinellids by tree lizards (Cock, 1985). Azya luteipes Mulsant is difficult to distinguish from A. orbigera and other species with two dorsal spots except by examination of male genitalia. It occurs naturally along the coastal region of South America from Bahia, Brazil, to Argentina [the references to it occurring in Florida and the Hawaiian Islands are actually A. orbigera (Gordon 1980)], and it was collected in Brazil and introduced into Puerto Rico in 1939 to prey on bamboo scale (Bartlett, 1940). Possibly unrecorded or accidental introductions were made into Surinam, Guiana, and Dominica (Gordon, 1980). Pseudoazya trinitatis (Marshall) is native to northern South America and probably Trinidad, but was introduced and established in Puerto Rico, the Virgin Islands, and possibly Saipan; the introductions into Florida, Fiji, Vat6 Island, and New Hebrides failed (Gordon, 1980). Although it was introduced mainly as a predator of the coconut scale in Puerto Rico, it has become most effective against Pseudaulacaspis pentagona (TargioniTozzetti), A. bombusae, and other scales (Cock, 1985). It has also been recorded as a predator of coconut scale in Grenada, Barbados, and Jamaica; and was established on the latter two islands from shipments from Trinidad (Cock, 1985). The tribe Coccidulini comprises about 170 species in some 28 genera; about 100 species are Australasian (Pope, 1979). Rhizobius spp., which prey mostly on coccids, is the only genus in the tribe that has been utilized thus far in classical biological control. Rhizobius forestieri (Mulsant)

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

almost always was misidentified as R. ventralis (Erichson) after its introduction into California from Australia in 1889 by Koebele (Pope, 1981). Rhizobius forestieri readily preyed on black scale in California (Bartlett, 1978), and has been recorded to attack the same scale, four mealybug species, an aphid species, and Spodoptera eggs in Hawaii after its introduction from Australia (via California) by Koebele in 1894 (Leeper, 1976). It became established in Italy and Sicily against Chrysomphalus dityospermi (Morgan) in 1908 by Silvestri, and in South Africa and New Zealand effectively attacks scales on Araucaria and Norfolk Island pine (Bartlett, 1978; Pope, 1981, Cameron et al., 1989). Rhizobius forestieri has been successfully established in Greece as a predator of black scale on olive (Katsoyannos, 1984), and in 1987 it became established on an island off southern France and effectively reduced black scale on clementine trees (Iperti et al., 1989). Richards (1981) lists 14 coccid species as prey of the adult, 9 of which are prey of adult beetles and larvae in Australia. Rhizobius ventralis is more specific; it voraciously feeds on Eriococcus coriaceus Maskell and rejects a variety of coccid pest species. This narrow prey specificity, coupled with an inability to either produce more generations than their prey or adjust to new habitats, were some of the reasons for the failure or partial failure of R. ventralis and R. forestieri as biological control agents in other parts of the world (Richards, 1981). The original description of R. lophanthae (Blaisdell) (formerly Lindorus lophanthae) was based on specimens collected in California (where it had been introduced and established in 1892 as a predator of black scale), but it is mainly a predator of diaspine scales in its native Australia and where it has been established elsewhere (Essig, 1931; Greathead, 1973). It was introduced into the Hawaiian Islands from California in 1894 where it has been recorded to prey on five diaspine species and black scale (Leeper, 1976). It has become established in Argentina and Italy on white peach scale (Waterhouse & Norris, 1987). It became established in Bermuda in 1949, but in spite of its heavy predation on Bermuda cedar scales, the cedar trees continued to decline; it also attacked palmetto scale (Bennett & Hughes, 1959). Among the many coccinellids imported into South Africa in 1900, only R. lophanthae became established and became an important addition to the predator complex on red scale (Greathead, 1971). During the 1920s it also was introduced into Mauritius where it attacked coconut scale, but because it was not very effective, other natural enemies were sought and imported after 1937 (Greathead, 1971). Actually, R. lophanthae has become established in every exotic location where it has been released except perhaps Chile (Greathead, 1973). In Peru it was introduced as a predator of citrus round scale, Selanaspidus articulatus (Morgan), but it also readily fed on citrus white scale, Pinnaspis aspidistrae (Sing) (a female R. lophanthae eats an average of 450 scales) (Marin, 1983). Rhizobius pulchellus Montrouzier from New Caledonia was accidentally

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introduced to Vanuatu (New Hebrides) in 1964, where serious outbreaks of coconut scale in coconut plantations were occurring on Vat6 Island; the predator quickly reduced the scale population, while Cryptognatha nodiceps Marshall, which successfully controlled coconut scale in the Fiji Islands, failed (Cochereau, 1969). Waterhouse and Norris (1987) consider R. satelles Blackburn the species involved in the preceding project, and note that R. satelles has been incorrectly referred to, or misidentified as, Lindorus lophanthae, R. lophanthae, R. pulchellus, and R. nigrovatus. It is common in Australia, New Zealand, New Caledonia, and South Africa; and has become widely dispersed in Vanuatu. Rhizobius satelles was introduced to Fiji, Tahiti, and Wallis Island, where it became successfully established against A. destructor (Waterhouse & Norris, 1987). The tribe Noviini has four genera and includes 73 species that are mainly found in the African-Asian-Australian regions (Gordon, 1972; Pope, 1979). Their main prey are Margarodidae, principally Icerya spp. Rodolia has been the genus chiefly involved in biological control projects. The vedalia beetle, R. cardinalis Mulsant, is famous for saving the citrus industry in California during the late 1880s (Essig, 1931; Doutt, 1958; DeBach, 1964; Caltagirone & Doutt, 1989). Ever since its introduction into California from Australia, it has given complete control, with only an occasional upset of the vedalia due to extreme winters or detrimental pesticide use (Bartlett, 1978). The vedalia was imported by 57 different countries between 1889 and 1958, ranging from temperate or desert to tropical climates, and in 55 of these countries it has been reported not only to become established but also to produce good control of the cottony-cushion scale (Bartlett, 1978). In Bermuda, the vedalia introduction did not give complete control of L purchasi because it was relatively inactive in the cooler months; and a significant increase in the scale population occurred during this period, but the introduction of Cryptochaetum iceryae (Diptera: Cryptochaetidae), an endemic Australian parasitoid, into Bermuda successfully controlled the scale during the cooler periods (Bennett & Hughes, 1959). Similarly, along the cooler northern California coast, C. iceryae is more effective than the vedalia in controlling the scale (Quezada & DeBach, 1973), and the same situation occurs along the cooler coast in South Australia (Prasad, 1989). The vedalia preys on L purchasi on nearly all the plants the scale infests, but the scale is relatively immune to attack when it infests certain species in the genera Ulex, Spartium, and Genista (Poutiers, 1930; Bodenheimer, 1951; Priore, 1963); and is not readily attacked on Coerulus laurifolius (Quezada & DeBach, 1973). Icerya purchasi has been recorded attacking 40 species in 16 different plant families in just the Hawaiian Islands (Hale, 1970). The biological attributes that make R. cardinalis such an effective predator of L purchasi in warm climates are a short generation time (three to one of the scale), a narrow prey

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specificity, a good voracity, and a high searching capacity (Bodenheimer, 1951; Quezada & DeBach, 1973). Icerya aegyptiaca (Douglas), an Asian species, was successfully controlled in Egypt by importing only six individual beetles that became established. Icerya aegyptiaca and L seychellarum (Westwood) have also been controlled in the mountainous islands of Micronesia mainly by the introduction of R. pumila Weise, but the predator has been less successful on atolls, for after dramatically reducing populations of fluted scales it then became extinct (Schreiner, 1989). Icerya monterratensis Riley & Howard in Puerto Rico and in Ecuador and L palmeri Riley & Howard in Chile were also successfully controlled by introducing R. cardinalis (Bartlett, 1978). Rodolia iceryae Jensen from South Africa did not become established when released in Israel (Mendel & Blumberg, 1991), but is considered to have potential for inoculative releases against L pattersoni Newstead on coffee in Kenya (Kairo & Murphy, 1995).

Coccinellinae is a subfamily that at present is made up of six tribes: Bulaeini, Coccinellini, Discotomini, Psylloborini, Singhikalini, and Tytthaspini. Only the tribe Coccinellini in the Coccinellinae contains species that are of importance to applied biological control, because Bulaeini (Bulaea) is essentially phytophagous (with multidentate mandibles apically like Psylloborini), Psylloborini and Tytthaspini are mycophagous, and Discotomini and Singhikalini apparently have not been involved in any applied biological control programs. Coccinellini today consists of 86 genera with over 600 species that are essentially predaceous; most are aphidophagous in the Northern Hemisphere, but it appears that in the Australian, Ethiopian, and Neotropical regions the genera have species more closely associated with other Homoptera, particularly psyllids and coccids. Most species deposit their eggs vertically in groups near their prey. On hatching, larvae remain clustered together on their eggshells for up to 1 day and often attack the unhatched eggs. This sibling cannibalism is often beneficial for the one egg eaten (which may not have hatched), nearly doubles the life of a newly hatched larva, and prolongs the search for aphids (Banks, 1956; Dixon, 1959; Brown 1972b; Dimetry, 1974; Kawai, 1978; Ng, 1986). Two or more coccinellid species have frequently been recorded from the same habitat, attacking the same aphid colonies, which suggested to Evans (1991) that there is little or no difference between intra-and interspecific interactions among coccinellids when two similarly sized individuals co-occur on a host plant. However, both Mills (1982b) and Osawa (1989, 1993) documented substantial cannibalism in the field, and Agarwala and Dixon (1992) demonstrated asymmetrical interspecific predation in the laboratory between Adalia and Coccinella species. The species diversity of immature aphidophagous coccinellids did not differ

among South Dakota row crops but did vary among years within a 13-year period (Kieckhefer et al., 1992). At least 15 genera have been utilized in biological control projects. In recent years there has been greater success in introducing and establishing aphidophagous coccinellids in the New World. Adalia bipunctata, a Palearctic species, has become widely distributed both intentionally and adventively in the temporate regions of the world and now occurs on all continents (Iablokoff-Khnzorian, 1982; Gordon, 1985; Pope, 1988). It was introduced and established in Chile in 1940 and now is found in Argentina (Zuniga, 1985). It is an arboreal predator of many different aphids [67 different species listed by Gordon (1985)] but also preys on psyllids and coccids (Herard, 1986). In France, releases of five adults per apple tree at 15-day intervals controlled Dysaphis plantaginea (Passerini) (Remaudiere et al., 1973); and in Poland, A. bipunctata adults were able to suppress apple aphids at a ratio of up to 1:250 aphid nymphs, and the Adalia larvae at a ratio of 1 predator to 60 nymphs (Niemczyk et al., 1974). On sycamore trees, there has to be more than two young sycamore aphids per 100 cm 2 of leaves for A. bipunctata to survive (Dixon, 1970). Ovipositing A. bipunctata laid eggs only when there were sufficient lime aphids on lime trees for survival of the first-instar larvae (11 small aphids per 100 cm 2 of leaf) but did not lay proportionately more eggs at higher densities (Wratten, 1973; Mills, 1982b). Ants can reduce the effectiveness of A. bipunctata controlling aphids on peach trees (Kreiter & Iperti, 1986). In France (Iperti & Kreiter, 1986) and Finland (H~im~il~iinen, 1976), A. bipunctata has one generation a year in the field, but in the New York area it has two or three (Obrycki et al., 1983). Continuous generations could be cultured in the laboratory at photoperiods of at least 14h light: 1Oh dark at 23~ for the New York populations and at LD 18:6 at 25~ for the Finland population. Aiolocaria hexaspilota (Hope), an Asian species, was observed to feed on chrysomelid eggs and larvae infesting willow in Japan (Timberlake, 1943). It was introduced to the western (former) USSR to control the Colorado potato beetle and other chrysomelids [e.g., Melasoma populi (Linnaeus), but apparently without any great success (IablokoffKhnzorian, 1982)]. Aphidecta obliterata (Linnaeus) is a European species predaceous on adelgids (Iablokoff-Khnzorian, 1982). After the balsam woolly aphid, Adelges piceae, was accidentally introduced into North America about 1900, it became a serious pest of true firs in Canada and the United States (Amman, 1966; Clark et al., 1971). Among the many different predaceous insects introduced against A. piceae, Aphidecta obliterata finally became established in Newfoundland associated with Adelges cooleyi (Gillette). Studies indicated that predation is evident only when there are more than 25 A. cooleyi per 4-in. twig; thus, even though it

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

is established in Newfoundland, it is ineffective because it does not prey at low levels of A. piceae populations (Clark et al., 1971). Aphidecta obliterata was introduced into North Carolina from Germany in 1960 and became established against Adelges piceae, but no attempts were made to determine its effectiveness in the field (Amman, 1966; Gordon, 1985). Bothrocalvia pupillata (Swartz) occurs in India, Indonesia, and China (Iablokoff-Khnzorian, 1982). It was introduced into the Hawaiian Islands from Hong Kong in 1895 by Koebele (as Coelophora pupillata) where it now preys on Toxoptera citricidus (Kirkaldy), Thoracaphis fici (Takahashe), and Selenothrips rubricinctus (Giard) (Leeper, 1976). It also preys on certain psyllids and aleyrodids in the Hawaiian Islands (Funasaki, 1988). Cleobora mellyi (Mulsant), an Australian species that is considered by some taxonomists to be in the tribe Psylloborini, is polyphagous, feeding on aphids, coccids, psyllids, and chrysomelids. It is considered an important predator of Chrysophtharta bimaculata (Olivier), a chrysomelid defoliator of eucalypts in Tasmania (Mensah & Madden, 1994), and has been established against a eucalypt-defoliating chrysomelid, Paropsis charybdis St~l, in New Zealand (Cameron et al., 1989). However, Cleobora mellyi probably is more naturally a predator of psyllids on acacias (Pope, 1988). Coccinella septempunctata Linnaeus (C-7) is the most common Palearctic coccinellid species. It was intentionally introduced into North America several times from 1956 to 1971, but these releases were unsuccessful (Angalet et al., 1979), including releases of eggs and larvae (from a stock originally collected near Paris, France) in Maine potato fields over a 5-year period where the adults overwintered in screen cages in grasslands (Shands et al., 1972d). However, a population was discovered in New Jersey in 1973 that may have resulted from an accidental introduction (Angalet & Jacques, 1975). Since 1973, C-7 has been released in every state and in southern Canada and has become widely established east of the Rocky Mountains but only marginally in the West (Gordon, 1985; Schaefer et al., 1987; Gordon & Vandenberg, 1991). C-7 is a polyphagous predator but is essentially aphidophagous. Iablokoff-Khnzorian (1982) reviewed its biology and lists as food sources over 60 aphid species (including several aphids that are toxic), thrips, aleyrodids, psyllids, leafhoppers, coccids, moths, beetles (particularly some chrysomelids), pollen, and nectar. Herard (1986) noted from literature (over 50 references since 1978) that C-7 was recorded preying on 25 different aphid species infesting some 27 different crops as well as various other insect groups, including psyllids. Cultivated and uncultivated habitats in midwestern United States play an important role in supporting populations of C. septempunctata (Maredia et al., 1992). The subspecies C. septempunctata brucki Mulsant occurs in Asia and was introduced

437

into the Hawaiian Islands from Okinawa in 1958 (Leeper, 1976). In Japan, it has an that estival diapause that is controlled by long days (LD 18:6 photoperiod) but its hibernal dormancy is not induced by short days (LD 12:12); these responses are opposite those of European C-7 populations (Hodek et al., 1984). Releases of C-7 have been made to control aphids in greenhouses and potato fields. H~im~il~iinen (1977) released larvae of both C-7 and Adalia bipunctara at intervals of a few weeks on chrysanthemums and sweet peppers infested with Myzus persicae, which prevented aphid population growth and decreased aphid numbers. One C-7 first-instar larva per 50 aphids was effective on chrysanthemums while one A. bipunctata larva per 5 to 10 aphids on sweet peppers resulted in control, but larvae of neither coccinellid species were effective in controlling Macrosiphum rosae on roses. Shands and Simpson (1972) applied a spray mixture of C-7 eggs in water and 0.25% agar on potato plants to control aphids; none of several treatments provided satisfactory control of aphids, but larvae resulting from early-season applications of eggs gave the best control of the aphids. In earlier experiments, Shands et al. (1972b, 1972c) obtained 30 to 50% control of potato aphids by introducing eggs and young larvae of C7. C-7 larvae have an impact on aphids infesting cereal crops in Finland (Rautapaa, 1972), and Ferran et al. (1986b) derived a formula that calculated the biomass of aphids consumed by each C-7 larva (regardless of instar) per square meter of wheat in France. Olszak and Niemczyk (1986) placed two C-7 adults (with hind wings removed) in caged small apple trees with either 10 or 20 Aphis pomi per tree; he noted 100% aphid mortality within 6 days for 10 aphids and 8 days for 20 aphids. Coccinella undecimpunctata Linnaeus, a Eurasian species, was introduced into New Zealand in 1874 (Miller et al., 1936; Cameron et al., 1989). Since 1959, it has been found in Western Australia, and since 1970, in Tasmania (Pope, 1988). In North America, it was first discovered in 1912 in Massachusetts; now it is found in the northeastern United States, southern Canada, British Columbia, and the Seattle area of Washington State without any intentional action by man (Wheeler & Hoebeke, 1981; Gordon, 1985). It is recorded to prey on at least 12 aphid species, most of which are pests of agricultural crops (Iablokoff-Khnzorian, 1982). Coelophora inaequalis (Fabricius) occurs in Australia, China, Indonesia, Malaysia, the Mariana Islands, Fiji, New Zealand, and the Philippines (Timberlake, 1943; Pope, 1988). It was introduced into the Hawaiian Islands from Australia, Ceylon, and China in 1894 by Koebele to control Melanaphis sacchari (Zehntner) (Leeper, 1976). It has been recorded to prey on nine aphid species and a psyllid in Hawaii (Funasaki et al., 1988). Coelophora inaequalis was also successfully introduced into New Zealand (date unknown) (Pope, 1988) and into Puerto Rico from Hawaii to

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prey on Sipha flava (Forbes) (Clausen, 1978), and may be established in Florida (Gordon, 1985). Coleomegilla maculata (DeGeer) occurs from Canada to Argentina and has been divided into at least eight subspecies by Timberlake (1943). Three subspecies occur in North America (Gordon, 1985). Even though C. maculata lengi Timberlake is aphidophagous, it can complete its larval development when fed only corn pollen (Smith, 1960). It readily feeds on European corn borer eggs (Andow & Risch, 1985; Phoofolo & Obrycki, 1997) and does not prefer aphids over Colorado potato beetle larvae; in field cage studies, C. maculata adults significantly reduces populations of Colorado potato beetle eggs and small larvae (Groden et al., 1990). Adult C. maculata aggregate in maize and cotton plots when sprayed with a yeast-sugar mixture (Nichols & Neel, 1977). Of four coccinellid species tested for aphid control under greenhouse conditions, Gurney and Hussey (1970) found C. maculata and Cycloneda sanquinea (Linnaeus) to be the most voracious in feeding on aphids, but Coleomegilla maculata larvae, because of glandular hairs on cucumber foliage, could not remain long enough to be effective. One second- or third-instar Cycloneda sanguinea larva released against 20 Aphis gossypii on greenhouse cucumbers almost eliminated the aphids after 16 and 18 days, respectively (Hussey & Bravenboer, 1971). Harmonia axyridis (Pallas), an Asian arboreal aphidfeeding species, was released in California, the Hawaiian Islands, eastern and southern United States, and Nova Scotia (Timbedake, 1943; Iablokoff-Khnzorian, 1982; Gordon, 1985; McClure, 1987; Tedders & Schaefer, 1994); France (Ongagna et al., 1993); and Greece (Katsoyannos et al., 1997). It has been recovered in Louisiana and Mississippi (Chapin & Brou, 1991), in the southeastern states (Gordon & Vandenberg, 1991; Tedders & Schaefer, 1994), and in the western states (Dreistadt et al., 1995; Lamana & Miller, 1996). Chapin and Brou (1991) listed over 14 aphid species recorded as prey, and McClure (1987) reared H. axyridis on a margarodid scale. A life table was developed by Osawa (1992). Hukusima (1971) released 30 adult H. axyridis three times in one season in apple tree plots treated with various selective pesticides; the addition of the predators held aphids at lower levels over a longer period compared with the control plots. The cotton aphid was controlled in Chinese cotton fields by a predator to prey ratio of 1:100 to 120; interplanting maize with cotton increased coccinellid populations compared with cotton alone (Dong, 1988). In France, Ferran et al. (1996) used releases of 50 larger larvae per four rose bushes to reduce rose aphids to comparable levels achieved with insecticides. Similarly, Trouve et al. (1997) found that an early release of 50 second- and third-instar larvae per plant reduced aphid abundance on hops by 72%, keeping them below the insecticide treatment threshold. Harmonia conformis (Boisduval) is widely distributed in

Australia, Tasmania, and New Zealand (Pope, 1988; Cameron et al., 1989). It has been released in California and Hawaii (often under the name Leis conformis) several times as an enemy of aphids. Koebele introduced it into Hawaii 1894 and 1904, but it only became established in 1973 when it was released against the acacia psyllid, Acizzia uncatoides (Ferris & Klyver), and dramatically reduced the pest population on the big island of Hawaii (Leeper, 1976; Leeper & Beardsley, 1976). Thousands of H. conformis were also released in coastal California against the acacia psyllid, but the species never became established (Gordon, 1985). In Australia, the predator feeds mostly on acacia psyllids and only switches to aphids when psyllids are scarce (Hales, 1979). Harmonia dimidiata (Fabricius), an Asian species (Iablokoff-Khnzorian, 1982), was collected in south China and released in California in 1925 as L. conformis against citrus aphids, but it never became established. However, a shipment of beetles from California to Florida in 1925 resulted in establishment there (Clausen, 1978; Gordon, 1985). Harmonia quadripunctata (Pontopiddian) is an Old World species associated mostly with conifers (IablokoffKhnzorian, 1982). It never was intentially introduced to North America, but Vandenberg (1990) discovered scattered specimens in various museums dating back as early as 1924. The present distribution in North America appears to be in an area near the Hudson River in the vicinity of the New Jersey-New York border. A key to the three North American Harmonia spp. is shown in Gordon and Vandenberg (1991). Hippodamia (Hippodamia) convergens Guerin is the most abundant and widespread Hippodamia species in North America (Gordon, 1985). Hippodamia spp. appear to be polyphagous, based on the variety of arthropods recorded as prey in the 195 references cited by Vanndell and Storch (1972). However, aphids are the main prey of H. convergens, and, in fact, are an obligatory requirement for optimal fecundity. Hippodamia convergens prefers low vegetation and is primarily univoltine in western North America where it migrates to mountains to spend 9 months (June to February) in aggregations. However, if aphid populations are high enough in late spring (more than two pea aphids per stem in alfalfa), the newly emerged H. convergens adults will not readily migrate to the mountains, but will remain and produce subsequent generations in the valleys (Smith & Hagen, 1966; Hagen, 1974; Neuenschwander et al., 1975). Also, artificial diets containing hydrolyzed yeast and sugar applied on crops (alfalfa) in the valley when aphid populations are low can arrest, retain, and induce oviposition (Hagen et al., 1970a). They remain reproductively dormant while in aggregations but mate just before leaving aggregation sites in February. They fly skyward to a flight ceiling of 13~ and are blown westward to the valleys by northeasterly winds (Hagen, 1962). The migra-

Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

tory flight from the overwintering sites in the mountains is necessary before H. convergens begins to search for aphids. The propensity to fly is associated with hormonal control and is correlated with ovarian development (Rankin & Rankin, 1980a, 1980b; Davis & Kirkland, 1982). Thus, relatively few H. convergens collected from overwintered aggregations and released will remain and immediately search for aphids; the beetles will react as they would when leaving their overwintering sites (Davidson, 1924; DeBach & Hagen, 1964; Kieckhefer & Olson, 1974). The few (ca. 10%) overwintered beetles that do not fly far when released are probably weakened by the parasitism of Dinocampus coccinellae (Shrank) (Ruzicka & Hagen, 1985). However, insectary-reared adults, or adults from aggregation sites that have been allowed to fly for 7 to 10 days before release, disperse more slowly and can provide short-term reductions of 25 to 84% in aphid populations (Dreistadt & Flint, 1996). If the elytra of H. convergens are glued together so they cannot fly, they can reduce green peach aphid numbers in sugar beet plots four times more than in control plots; they will also deposit more eggs than in plots where beetles able to fly were released (Tamaki & Weeks, 1973). By removing the hind wings of H. convergens, the adults ate 22 times more Heliothis zea eggs than beetles free to fly (Ignoffo et al., 1977). Regulation of greenbugs in Texas high plains grain sorghum is largely due to the suppressive action of Hippodamia convergens and H. sinuata (Mulsant); the impact of the Hippodamia spp. on greenbugs was determined by exclusion and introduction of beetles (Kring et al., 1985). Hippodamia convergens has also been utilized in classical biological control. It was sent to at least 11 countries for release, but only became established in Peru in 1937 (Clausen, 1978), and later in Chile and Argentina (Zuniga, 1985) and Venezuela (Szumkowski, 1961). After five attempts to establish it in the Hawaiian Islands, it finally was found in 1964, but only at the higher altitudes of Maui and Hawaii (Leeper, 1976). Hippodamia (Adonia) variegata (Goeze) is a Palearctic aphidophagous species absent in Japan, but extends south to India and in Africa to Kenya (Iablokoff-Khnzorian, 1982); it also has been reported in South Africa (Greathead, 1971). This species has been introduced into North America many times between 1957 and 1981 without successful establishment (Gordon, 1985; Gordon & Vandenberg, 1991); however, in 1984, Gordon (1987) reported H. variegata to be established in Quebec, apparently as an adventive species, and since then, it has been recorded from the eastern United States and the maritime provinces of Canada (Wheeler, 1993; Wheeler & Stoops, 1996). This Canadian stock of H. variegata, as well as populations from France, India, Morocco, and the former USSR, has been cultured and released widely against the Russian wheat aphid in the United States but apparently has not become established in the new release areas (Gordon, 1985; Schaefer & Dysart,

439

1988; Gordon & Vandenberg, 1991). However, H. variegata from South Africa not only became established in Chile in 1975, but also now occurs in Argentina and Brazil; in these countries, it has played an important role along with imported parasitoids in a very successful biological control program against several introduced cereal aphids (Zuniga, 1990). Hippodamia (Semiadalia) undecimnotata (Schneider) is another Palearctic species that is aphidophagous, but it also readily preys on alfalfa weevil larvae in the (former) USSR (Iablokoff-Khnzorian, 1982). It has been cultured and released in the western United States against the Russian wheat aphid, but thus far no establishment has been recorded (Gordon & Vandenberg, 1991). Lemnia biplagiata (Swartz), an Oriental species, was introduced into Taiwan from Indochina in 1925 (Clausen, 1978), and Iablokoff-Khnzorian (1982)mentions that it was introduced from Vietnam in 1927, but was already in Taiwan. Semyanov and Bereznaja (1988) concluded that this coccinellid is suitable for use as a biological agent for controlling aphid populations in greenhouses. Lemnia saucia Mulsant (= calypso in China, L. mouhoti in Laos, and L. swinhoei in Taiwan), which occurs in India, Japan, and the Philippines, was also collected in Indochina, released into Taiwan against aphids on sugarcane, and became established there (Rao et al., 1971; Clausen, 1978). Menochilus sexmaculatus (Fabricius), an Oriental species common in forests and gardens, is largely aphidophagous but also preys on psyllids, mealybugs, coccids, and spider mites (Iablokoff-Khnzorian, 1982; Cartwright et al., 1977). It was imported from Pakistan and released for 2 years against the greenbug in Oklahoma; it reproduced and remained in the field, but apparently could not overwinter there (Cartwright et al., 1977). Oenopia conglobata (Linnaeus) is a Palearctic aphidophagous species but also feeds on coccids and immature chrysomelids, as well as on pollen and nectar (IablokoffKhnzorian, 1982; Herard, 1986). It was released several times in North America from 1957 through 1982 (Gordon, 1985) but had not become established by 1990; however, a Russian strain is still being released in the western United States against the Russian wheat aphid (Gordon & Vandenberg, 1991). Olla v-nigrum (Mulsant) (= abdominalis) is a New World species extending from Canada to Argentina. It is primarily arboreal and in North America preys particularly on aphids infesting Juglans trees (Timberlake, 1943; Sluss, 1967; Gordon, 1985; Vandenberg, 1992); in the tropics, psyllids are its main prey (Vandenberg, 1992). Extensive biological studies of O. v-nigrum were made in France before releasing it in Europe, and it was compared with some other coccinellids such as Adalia bipunctata, Harmonia axyridis, H. conformis, and Hippodamia convergens. It was concluded that O. v-nigrum would be a valuable

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addition to the Mediterranean region as an aphid predator (Kreiter & Iperti, 1984; Iperti & Kreiter, 1986), while Ferran et al. (1986a) concluded that Harmonia axyridis and O. v-nigram could be used together. In the Hawaiian Islands, O. v-nigrum was introduced from Mexico in 1908 (Leeper, 1976); in these islands it is recorded to prey on aphids, psyllids, and aleyrodids (Funasaki et al., 1988) and is an important predator of the leucaena psyllid, Heteropsylla cubana (Crawford) (Waterhouse & Norris, 1987). Olla v-nigrum was introduced into Guam sometime before 1952 (Chapin, 1965a) and was introduced from Tahiti to New Caledonia in 1987 against H. cubana, which had invaded that area around 1985. By 1989, O. v-nigrum was present in most parts of New Caledonia and was an important predator of the psyllid (Chazeau et al., 1991). These authors developed a life table for the coccinellid and found the psyllid to be a highly suitable prey, though toxic to other polyphagous predators. Propylea quatuordecimpunctata (Linnaeus), a common aphidophagous Palearctic species, has been recorded to prey on at least 20 species of aphids, mainly on low vegetation in the Old World (Iablokoff-Khnzorian, 1982; Herard, 1986). Before releasing it in Oklahoma, seven aphid species associated with small grains were tested as prey in the laboratory. The beetles survived on all seven species, but the reproductive level varied (Rogers et al., 1972). Attempts to establish it in the United States from 1971 to 1982 were unsuccessful (Gordon, 1985). However, in 1968, it was discovered in Quebec (Chantal, 1972), predating any intentional releases in North America. Later it was found from the vicinity of Montreal, south along the St. Lawrence River to northern New York, Maine, Vermont, and Massachusetts; all these were considered as unintentional establishments (Schaefer & Dysart, 1988; Wheeler, 1990, 1993; Gordon & Vandenberg, 1991). Populations of P. quatuordecimpunctata from Canada, France, and Turkey did not differ significantly in either life table parameters or in critical thresholds for diapause induction (Obrycki et al., 1993).

Hyperaspinae is a subfamily composed of approximately 500 species divided into 14 genera (Pope, 1979). Duverger (1983) elevated the tribe Hyperaspini to subfamily status, removing it from the subfamily Scymninae, with most species belonging to Cyra, Hyperaspis, or Brachycantha. According to R. D. Gordon (personal communication) of the U.S. National Museum most South American species formerly described under the taxa Hyperaspis or Cleothera in reality belong to Mulsant's genus Cyra. The majority of the hyperaspine species attack the more or less sedentary homopterans such as coccids and mealybugs. Gordon (1985) lists 75 different species of prey that E1-Ali (1972) recorded associated with 60 hyperaspine species (mostly Cyra and Hyperaspis). Brachycantha spp. apparently prey on coccids, mealybugs, and aphids that infest plant roots and are attended by ants (E1-Ali, 1972).

The eggs of Hyperaspis are usually flattened and deposited singly near their prey in irregularities of the bark or in growth rings of twigs but not under scale coverings of coccids (E1-Ali, 1972). However, Cy. notata (Mulsant) (as Cleothera notata) and two other Cyra spp. deposit ovoidshaped eggs inside the ovisacs of mealybugs; their larvae feed on the eggs and pupate at the base of infested cassava plants (Sullivan et al., 1991), but there are other species that pupate on leaves. There are usually four larval instars, but McKenzie (1932) reported that the fall generation of H. lateralis Mulsant passes through only three instars (the spring generation passes through four). The few hyperaspine species that have been utilized in applied biological control belong to either Cyra or Hyperaspis. Cyra notata and C. raynevali Mulsant (as Hyperaspis or Cleothera) are Neotropical species successfully introduced from South America and established in Africa against the cassava mealybug Phenacoccus manihoti Matile-Ferro (Kiyinidau & Fabres, 1987; Lrhr & Varela, 1990; Herren & Neuenschwander, 1991; Reyd et al., 1991; Kanika-Kianfu et al., 1992). The biology of Cyra notata (= H. notata Mulsant) has been elucidated by Sullivan et al. (1991) in Columbia and by Dreyer et al. (1997a, 1997b) in Nigeria. The biology of C. raynevali (= H. jucunda Mulsant) was described by She et al. (1984) in southern Nigeria and by Kiyindou and Fabres (1987) and Reyd et al. (1991) (the latter utilizing Planococcus citri Risso as a factitious prey) in the Congo. Cyra pantherina (Fiirsch) [= Cyra jocosa (Mulsant)] occurs from Mexico to Brazil. It was introduced into the Hawaiian Islands from Mexico in 1907 by Koebele as a predator of Orthezia insignis Browne, and later was sent from Hawaii to Kenya, where it was reared in large numbers to control O. insignis attacking jacaranda trees; the establishment of the predator in Tanzania and Uganda saved the jacarandas and Orthezia is no longer a problem (Greathead, 1971). It has also been successful in the control of the same scale on the island of St. Helena (Booth et al., 1995). Cyra trilineata (Mulsant) keeps the pink sugarcane mealybug, Saccharicoccus sacchari (Cockerell), in check in Venezuela (Box, 1950) and Barbados (Coles, 1964), and also occurs in French Guiana. Cyra trilineata (as Hyperaspis) was released and established on several Caribbean Islands, where it contributes to the control of S. sacchari (Cock, 1985). The coccinellid also was sent to Puerto Rico in 1934 and 1935, but apparently did not become established; however, Wolcott (1937) believed that it became established because the sugarcane mealybug population was reduced and no outbreaks had occurred by 1937. Hyperaspis binotata (Say) is a common eastern North American species (Gordon, 1985). Arboreal soft scales are its main prey; it is an effective natural enemy of cottony maple scale [Pulvinaria innumerobilis (Rathvon)], terrapin scale [Mesolecanium nigrofasciatum (Pergande)] (Simanton, 1916), and pine tortoise scale [Toumeyella parvicornis (Cockerell)] on jack and Scotch pine (Mclntyre, 1960). A

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number of Hyperaspis spp. have been successfully introduced into new areas. Hyperaspis campestris Herbst in the former USSR is a successful biological control agent of many scale insects on grapes, citrus, and other subtropical plants. In (former) USSR tea plantations, Pulvinaria flocifera (Westwood) can be a serious pest, but releases of about 400 adult H. campestris per acre reduced the pest population below the economic level in 2 years (Bogdanova, 1956). Hyperaspis conviva Casey, an eastern North American species (Gordon, 1985), can control pine tortoise scale on jack pine in Manitoba, but the scale populations persist and increase if the scale is attended by Formica obscuripes Forel (Bradley, 1973). Hyperaspis maindroni Sicard from New Guinea became established in India to prey on the hibiscus mealybug (Rao et al., 1971). It was either H. limbalis Casey, which occurs at San Diego, California, or H. inflexa, which occurs from California to New Jersey, that was introduced into the Hawaiian Islands from California by Koebele in 1906 (Leeper, 1976). These two Hyperaspis spp. can only be identified by examining the male genitalia (Gordon, 1985); thus it is not certain which species was introduced and became established to prey on mealybugs. It is recorded to attack Trionymus insularis Ehrhorn (Leeper, 1976; Funasaki et al., 1988). Besides several Cyra spp. from South America introduced against the cassava mealybug in Africa, there are 32 endemic species of Coccinellidae recorded among the 120 arthropods associated with P. manihoti, including five Hyperaspis spp. (Neuenschwander et al., 1987). Hyperaspis senegalensis hottentotta Mulsant has been the most closely studied endemic Hyperaspis species preying on the cassava mealybug (Fabres & Kiyindou, 1985; Kiyindou et al., 1990). It was introduced into California and persisted only 1 or 2 years as a predator of ice plant scales. Hyperaspis signata (Olivier), a southeastern species (Gordon, 1985), has a similar biology to H. binotata and is an important natural enemy of the pine tortoise scale. It was introduced into Michigan from Minnesota in early 1930 and by October only 8 trees in a plantation of 690 had scale present, compared with 78 trees in May (Orr & Hall, 1931). Hyperaspis silvestrii Weise, a Mexican species, was introduced and established in the Hawaiian Islands in 1922 as a predator of avocado mealybug and the coconut mealybug (Leeper, 1976) and in the Philippines on the pineapple mealybug (Bartlett, 1978).

Scymninae is a subfamily composed of seven tribes, with the Cryptognathini, Scymnini, and Stethorini being the main ones that include species that have been utilized in applied biological control. These small pubescent coccinellids are rather prey specific (at least in their larval stages) to the genetic level. The tribe Cryptognathini is composed of approximately 50 species in eight genera, but only a few species in the genera Cryptognatha and Pentilia, which are Neotropical

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(Pope, 1979), will be discussed here. Their oval eggs are deposited beneath the coveting of the scale insect after the scale body has been eaten by the coccinellid adult. The larvae bear long, white, waxy tufts that project from their sides. When pupating, the larval skin is pushed downward and forms a base upon which the naked pupa rests (Taylor, 1935; Pope, 1979). Cryptognatha nodiceps Marshall is endemic to Trinidad and Guyana and preys on diaspine scales. It was imported into the Fiji Islands from Trinidad in 1928 to control the coconut scale, Aspidiotus destructor (Signoret). It was a remarkably spectacular success. In only 9 months after the first releases, the scale was under control in all the more important islands of Fiji; and in a further 9 months, the scale not only was controlled on every island of Fiji but also was difficult to detect (Taylor, 1935). A similar outstanding example of classical biological control was achieved in Principe by introducing C. nodiceps against the coconut scale (Simmonds, 1960). According to Greathead (1971) and Simmonds (1960), it was estimated that the production of copra in Principe Island had declined from 1400 tons per year before the scale invasion to 500 tons at the height of the infestation, amounting to an annual loss of $165,000. The problem was eliminated at a cost of $10,000 for the importation and release of C. nodiceps. During the 1930s, C. nodiceps was successfully introduced into Florida, Puerto Rico, the Dominican Republic, St. Kitts, and Nevis (Cock, 1985; Gordon, 1985; Waterhouse & Norris, 1987). However, C. nodiceps failed to control the coconut scale when it was introduced into Vanuatu (New Hebrides), but the scale was controlled by Rhizobius satelles (Chazeau, 1979; Waterhouse & Norris, 1987). The 11 Pentilia spp. range from Mexico to Argentina. Pentilia castanea Mulsant was imported from Trinidad and was established in the Dominican Republic and Puerto Rico to prey on the coconut scale (Bartlett, 1940; Cock, 1985; Waterhouse & Norris, 1987). Scymnini is the largest tribe in the Coccinellidae with over 600 described species, of which over 570 belong to Diomus, Nephus, or Scymnus (Whitehead, 1967; Pope, 1979; Gordon, 1985). Among the 22 other genera, only Clitostethus, Cryptolaemus, Pseudoscymnus, and Scymnodes include species to be mentioned here. Clitostethus spp. were considered to occur only in the Old World, but Ftirsch (1987) synonymized the New World genus Nephaspis Casey under Clitostethus Weise. Clitostethus larvae and adults are essentially predators of all stages of whiteflies. The beetles deposit their oval pale eggs horizontally among the aleyrodid nymphs on the underside of leaves. The larvae apparently do not produce a waxy coveting, threads, or plates but are often coated by wax secreted by the whitefly nymphs; the pupae are naked and found on the leaves where the larvae had fed (Agekyan, 1978; Yoshida & Mau, 1985; Bellows et al., 1992a, 1992b). Clitostethus arcuatus (Rossi), a Palearctic species, preys on

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several different aleyrodid species including the greenhouse whitefly. It moves easily on a glabrous plant surface, but larvae become trapped by foliar pubescence (Ricci & Cappelletti, 1988). In 1990 it was released in California from Israel to prey on the ash whitefly, Siphoninus phillyreae (Haliday), and has become established in coastal southern California (Bellows et al., 1992a, 1992b). Clitostethus arcuatus from Madeira became established in Cuba, preying on whitefly attacking citrus and fiddlewood (Cock, 1985). Clitostethus bicolor (Gordon) (as Nephaspis) was sent to Hawaii in 1979 from Trinidad and became established against the spiraling whitefly, Aleurodicus dispersus Russell (Funasaki et al., 1988; Waterhouse & Norris, 1989). Later shipments of C. bicolor were made from Hawaii and released against A. dispersus in Fiji and American Samoa, where it also became established (Waterhouse & Norris, 1989). Clitostethus oculatus (Blatchley) (as Nephaspis amnicola Wingo), which occurs from the southeastern United States (Gordon, 1985), the Caribbean, and Central America, was imported from Trinidad and Honduras and became established in Hawaii as an effective predator when populations of four different whitefly species are high (Kumashiro et al., 1983; Yoshida & Mau, 1985; Waterhouse & Norris, 1989); it was also established on Guam and American Samoa (Waterhouse & Norris, 1989). The genus Cryptolaemus comprises seven species that are indigenous to the Australasian zoogeographic region (Booth & Pope, 1986). The mealybug destroyer, C. montrouzieri montrouzieri Mulsant, is the subspecies being utilized today, mainly as an augmentative agent to control mealybugs in warm climates and greenhouses. They deposit their small, oval, lemon-yellow colored eggs usually into the cottony egg sac of mealybugs, or at least in the vicinity of mealybugs. The larvae are covered with white cottony wax filaments and when mature they frequently move downward and pupate within their dorsally split larval skins on or about the base of the plant (Essig, 1931; Smith & Armitage, 1931; Bodenheimer, 1951; Fisher, 1963). Larval and pupal development and reproduction were faster and greater when C. montrouzieri was exposed to Planococcus citri on Coleus leaves than to P. cirri on oleander; Aphis nerii on oleander was a much poorer prey than the mealybugs (Averbeck & Haddock, 1984). The mealybug destroyer was introduced into California in 1891 and 1892 from Sydney, Australia by Koebele, but it could only overwinter in California along the southern California coast (Clausen, 1915; Smith & Armitage, 1920; Essig, 1931). Because it initially showed great promise as a predator of mealybugs infesting citrus, Smith and Armitage (1920, 1931) developed inexpensive techniques to massculture both mealybugs and predators, and many commercial insectaries arose in southern California to produce the mealybug destroyer for the citrus growers (Fisher, 1963). However, the successful introductions of various mealybug

parasitoids led to control of mealybugs without annual releases of Cryptolaemus; thus, a number of insectaries discontinued producing the predator. Even today, some C. montrouzieri are mass-cultured for use in greenhouses (Witcomb, 1940; Doutt, 1951, 1952; Hussey & Scopes, 1985). Cryptolaemus m. montrouzieri has been imported into over 40 countries (Bartlett, 1978; Booth & Pope, 1986) including Hawaii, where it preys on at least 17 species of mealybugs (Leeper, 1976). In India, it is released against the grapevine mealybug (Babu & Azam, 1988; Srinivasan et al., 1989; Mani, 1990), but obtained poor establishment against the coffee mealybug (Reddy et al., 1991). In a few countries, it failed to become established permanently, mainly because the winters were too cold. Bartlett (1974) intentionally sought out biotypes of the beetles from the coldest areas of Australia and collected two populations that were propagated and colonized in California to broaden the genetic base for cold hardiness of the species. As a result, we now have C. m. montrouzieri persisting in the San Francisco Bay area of California where the original biotype could not persist (K. S. Hagen, unpublished). Thus, reintroducing C. m. montrouzieri, utilizing this new biotype, into the areas where the original biotype had failed to become established should be considered. Diomus is primarily a Neotropical genus, but there are a few species scattered in all zoogeographic regions (Gordon, 1985; Xiong-Fei & Gordon, 1986). The biology is known for only a few species. Diomus debilis (LeConte) lays elliptical flattened eggs on leaves and preys on mealybugs that infest salt marsh grasses (Whitehead, 1967). Diomus larvae have no apparent waxy secretions and they pupate on the plants where the larvae had fed. Mealybugs are prey for several Diomus spp. (Whitehead, 1967; Leeper, 1976; Meyerdirk, 1983; Hennessey & Muaka, 1987; Lrhr et al., 1990; Herren & Neuenschwander, 1991), as well as aphids (Leeper, 1976; Bishop & Blood, 1978), psyllids (Leeper, 1976; Pinnock et al., 1978; Leeper & Beardsley, 1976), and spider mites in Brazilian apple orchards (Lorenzato et al., 1986). Diomus notescens (Blackburn) was introduced into Hawaii from Australia by Koebele in 1894, where it preys on Nipaecoccus vastator (Maskell), P. citri, and Toxoptera citricidus (Leeper, 1976; Funasaki et al. 1988). In Australia D. notescens is considered an effective predator of Aphis gossypii on cotton (Bishop & Blood, 1978). Diomus pumilio Weise was collected in southeastern Australia in 1971 feeding on acacia psylla, Acizza uncatoides, which was rare. The predator was sent to California where it was cultured and released against A. uncatoides infesting acacias adorning the freeway landscape along the coast. Diomus pumilio was found to be widespread from San Francisco south to San Diego by the middle 1970s and has eliminated the need for insecticide treatments since then, saving the State Department of California Transportation $55,000 per year in the Bay area alone (Pinnock et al.,

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1978). Although another survey has confirmed the reduced abundance of the psyllid, Anthocoris nemoralis is now the dominant predator instead of D. pumilio (Dreistadt & Hagen, 1994). It was also sent to Hawaii as an enemy of the acacia psylla that was attacking koa trees, but it failed to become established; however, another coccinellid, Harmonia conformis, dramatically controlled the psyllid (Leeper, 1976; Leeper & Beardsley, 1976). Several Diomus spp. were collected in South America and sent to tropical Africa to prey on the cassava mealybug, Phenacoccus manihoti (Lrhr et al., 1990). At least one Diomus sp. became established widely in Africa (Herren & Neuenschwander, 1991). Diomus hennesseyi Ftirsch, an endemic African species, also attacks the cassava mealybug among some 30 other coccinellid species (Ftirsch, 1987; Neuenschwander et al., 1987; Kanika-Kiamfu et al., 1992). Nephus is composed of seven subgenera, but the few species that concern us fall under Nephus (Nephus), Nephus (Sidis), and Nephus (Scymnobius). The Nephus spp. that have been studied are all predators of mealybugs and their larvae have conspicuous waxy filaments (Whitehead, 1967). Nephus (Scymnobius) bilucernarius (Mulsant) was established in Hawaii from Mexico against the pineapple mealybug, Dysmicoccus brevipes (Cockerell) in 1930; it also preys on Nipaecoccus vastator (Leeper, 1976; Funasaki et al., 1988). Nephus (N.) roepkei (Fluiter) was imported to Hawaii from Asia several times and became established in the early 1990s, where it preys on three mealybug species and eggs of Spodoptera mauritis (Boisduval) (Funasaki et al., 1988). Nephus (Sidis) binaevatus Mulsant is endemic to South Africa and was introduced into southern California in 1922 as an enemy of the grape mealybug [Pseudococeus maritimus (Ehrhorn)] on grapes, and the citrophilius mealybug [P. calceolariae (Maskell)] on citrus, where it became established as an effective predator on citrus (Smith, 1923; Essig, 1931). Parasitoids introduced later controlled the mealybugs, reducing the importance of N. bineavatus (Bartlett, 1978); presently, it is found commonly attacking mealybugs on ornamentals in coastal California. Nephus (Sidis) reunioni Ftirsch was imported to the former USSR from Isle of R6union to combat citrus mealybugs, mainly in the Transcaucasia and Crimea; culturing methods and optimal temperatures were determined to provide material for release (Izhevsky & Orlinsky, 1988). Pseudoscymnus anomalus Chapin (endemic to Micronesia) was imported from Guam to Hawaii in 1970 as an enemy of the coconut scale (Leeper, 1976) and was also successfully established in American Samoa and Vanuatu (Waterhouse & Norris, 1987). These authors consider that the species is specific to the coconut scale. Pseudoscymnus tsugae Sasaji & McClure has been described from Japan and is considered a potential biological control agent for hemlock woolly adelgid in the eastern United States (Sasaji & McClure, 1997). Some Scymnodes species are aphid feeders, others are

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predaceous on coccids, and at least one species eats ants; all are endemic to Australia and Melanesia (Pope & Lawrence, 1990). Scymnodes (Apolinus) lividigaster Mulsant has spread naturally to New Zealand and several South Pacific Island groups, and was intentionally introduced into the Hawaiian Islands by Koebele in 1894 as an aphid predator (Leeper, 1976; Pope & Lawrence, 1990), where it proved to be of considerable value against the sugarcane aphid (Pemberton, 1948). The genus Scymnus is composed of five subgenera but only two of these concern us today--Scymnus (Scymnus) and S. (Pullus). The known larvae of both subgenera have waxy coverings with varying lengths of filaments, except the first instars that show no wax (Whitehead, 1967; Pope, 1979). The main prey of the larvae are aphids and adelgids (Gordon, 1976). There have been 17 species in the taxon Scymnus brought to the continental United States, but thus far only 2 have become established, 1 intentionally and the other accidentally. A few exotic species have become established in the Hawaiian Islands but there are no data on the introductions (Leeper, 1976). Scymnus (S.)frontalis (Fabricius), an Old World species, was collected in Turkey and is currently being cultured and released in North America against the Russian wheat aphid, Diuraphis noxia (Mordvillco). It can be recognized from other North American Scymnus (Scymnus) species by taxonomic characters described by Gordon and Vandenberg (1991). Its temperature thresholds for development and reproduction are about 5 to 10~ higher than that of D. noxia (Naranjo et al., 1990). Scymnus (Pullus) impexus Mulsant was introduced into Canada and the United States from Germany several times from 1951 to 1960 for control of the balsam woolly adelgid, but it has become established only in Oregon (Gordon, 1985). It also was exported from Germany into southeast England against adelgids and became established there (Greathead, 1976). A classical biological study of S. (P.) impexus was made by Delucchi (1954). Scymnus (P.) suturalis Thunberg is a European species that was inadvertently introduced to the eastern United States (Pennsylvania and New York), possibly via ornamental conifer nursery stock from Europe (Gordon, 1982). Its closest relative is S. (P.) coniferarum Crotch, which is an aphid predator on conifers in the western United States, and Gordon (1982) describes the characteristics differentiating the two species. Scymnus (P.) uncinatus Sicard from Mexico was introduced and established in Hawaii in 1922 for control of pineapple mealybugs (Leeper, 1976). Stethorini is a tribe of one genus containing 65 species that are found in most parts of the world (Gordon & Chapin, 1983). There are three subgenera (Pang & Mao, 1979), but because only a few species have been placed in their respective subgenera, these divisions will not always be noted here. Stethorus spp. are obligate predators of spider mites, and from most records of Kapur (1948) and all

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records listed by Gordon and Chapin (1983), it appeared to Gordon that the spider mite prey may be restricted to the family Tetranychidae. Adult Stethorus have been observed to feed at extrafloral nectaries and on aphids and their honeydew, but none produced eggs (Putman, 1955). Stethorus spp. deposit broadly ovoid eggs horizontally on the underside of leaves, usually among mite colonies (Putman, 1955; Colburn & Asquith, 1971; Raros & Haramoto, 1974). Oviposition is reduced on plants with pubescent leaves, because hooked trichomes may kill or impede the movement of larvae (Gunthart, 1945; Putman, 1955; Raros & Haramoto, 1974). The larvae are free of waxy coverings and feed on mite eggs and nymphs by extraoral digestion (Fleschner, 1950; Collyer, 1953a; Robinson, 1953; Putman, 1955; Raros & Haramoto, 1974); a larva eats about 200 tetranychids (ca. 45% eggs, 33% nymphs, 20% adults) (Raros & Haramoto, 1974). Pupation occurs at the feeding site; the pupa is "naked," pushing its last larval skin posteriorly to its base. An adult usually consumes the entire prey, and in 5 days eats about 400 tetranychids (ca. 40% eggs, 35% larvae and nymphs, and 22% adults) (Raros & Haramoto, 1974). Female beetles preferred mite eggs; and when satiated, they spent approximately 45% of their time searching, 14% feeding, and 40% resting (Houck, 1991). In another species, the females showed no significant preference for any life stage of a tetranychid (Tanigoshi & McMurtry, 1977). Oviposition begins when the European red mite, Panonychus ulmi (Koch), population ranged from 1 to 2 mites per apple leaf (Hull et al., 1977a, 1977b). Daily rates of prey consumption of ovipositing females may exceed 40 adult spider mites (McMurtry et al., 1970). Tanaka (1966) found that 50 to 100 eggs or 15 to 17 adults of P. citri were needed per day for a female to oviposit. A mean of about 4 eggs can be deposited per day over 55 days with a total of 300 to 400 eggs in a lifetime (Tanigoshi & McMurtry, 1977). Stethorus spp. are important natural enemies of spider mites, particularly the Tetranychidae in the field (Kapur, 1948; McMurtry et al., 1970). The impact of Stethorus spp. on tetranychids has been indicated by the rapid increase of mites after certain pesticide treatments on agricultural crops (Gilliatt, 1935; Readshaw, 1975; Field, 1979; Tanigoshi et al., 1983; Welch et al., 1983; Hull & Beers, 1985) and by hand removal of predators from mite-infested trees (Fleschner, 1950, 1958). The potential for these coccinellids to control spider mites in orchards or greenhouses was demonstrated by a rapid decrease of tetranychid populations after releasing Stethorus adults (Hussey & Huffaker, 1976). The use of Stethorus in the applied biological control of spider mites has been mainly through conservation (by utilizing selective pesticides) and augmentation. The results from classical biological attempts have been poor indeed (Huffaker et al., 1976). Of the 12 Stethorus spp. released in California from 1900 to 1978, Gordon (1985) found no

record of establishment. However, one species has been discovered in California, indicating successful establishment (K. S. Hagen, unpublished observations). Stethorus (Stethorus) punctillum Weise is a Palearctic species that was accidentally introduced into North America and discovered in Massachusetts and Ontario in 1950. This species is now known to occur in eastern North America from Massachusetts to Wisconsin and in the West in Oregon, Washington, and Idaho (Gordon, 1985). Stethorus (Stethorus) punctillum is reported to have reduced mite populations in Russian cotton fields and European vineyards (Kapur, 1948). It is one of the most effective predators attacking P. ulmi infesting Ontario peach orchards (Putman & Herne, 1966). In Europe, it shows a degree of specificity to fruit tree mites, notably P. ulmi and Tetranychus urticae. Wheeler et al. (1973) made collections of mites from more than 200 ornamental plant species grown in Pennsylvania, and S. punctillum was found associated almost exclusively with conifers infested with the spruce spider mite, Oligonychus ununguis (Jacobi). Stethorus (Stethorus) punctum punctum (LeConte) is a native species to North America and closely resembles S. punctillum. It ranges from southeastern Canada to North Carolina and west to Montana (Gordon, 1985). It is commonly a predator of P. ulmi in apple orchards. Its searching habits and functional responses have been studied by Colburn and Asquith (1971) and Hull et al. (1976, 1977a, 1977b). Welch et al. (1983) reviewed and compared three pest-predator models; two involved phytoseiid predators and the third, S. punctum, which included T. ulmi in Pennsylvania apple orchards [originally constructed by Mowery et al. (1975)]. Based on weekly sampling of trees, the number of S. punctum needed to control the mites was determined and the predicted number of mites per leaf was close to the actual field counts (Welch et al., 1983). Adults overwinter in the ground cover and soil around the base of the trunk of apple trees (Felland & Hull 1996). Stethorus (S.) punctum picipes Casey is a western North American species from Idaho to British Columbia south to southern California (Gordon, 1985). It feeds on tetranychids infesting cotton and citrus (Kapur, 1948), and is an effective predator of the avocado brown mite. Oligonychus punicae (Hirst), and citrus red mite, Panonychus citri (McGregor) (Fleschner, 1950, 1958; McMurtry et al., 1969; Tanigoshi & McMurtry, 1977). Multiple releases of S. picipes against the avocado brown mite at a rate of 400 to 500 adult beetles per tree resulted in an earlier increase of S. picipes in release areas, a lower peak population of the mite, and a lower percentage of damaged leaves in the release plots compared with check plots receiving no Stethorus. On caged avocado seedlings infested with avocado brown mite, introducing first-instar larvae of S. picipes 2 weeks after the initial prey infestation (prey to predator ratio averaged about 69:1) resulted in the development, maturation, and

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production of immature Stethorus offspring and initial suppression of O. punicae populations. Subsequently, overexploitation of prey occurred, with resultant starvation of the predators, and the prey population increased (Tanigoshi & McMurtry, 1977). Tanigoshi and McMurtry (1977) considered S. p. picipes to be a high-density predator but evidence (Congdon et al., 1993) suggests that it is capable of detecting and responding to very low-density populations of Tetranychus urticae in raspberries. Stethorus (Parastethorus) histrio Chazeau is a widespread and common species in Australia and is also found on Rrunion Island (Indian Ocean) and New Caledonia (Pacific Ocean) (Houston, 1980); in the Western Hemisphere it occurs in Chile and the Yucatan of Mexico (Gordon & Chapin, 1983). In Australia, Britton and Lee (1972) used the name S. nigripes Kapur, and it was introduced into California in 1974 and 1978 under this epithet (Gordon, 1985) but was never recovered until 1991 when K. S. Hagen (unpublished observations) found it established in Albany, California, preying on Tetranychus urticae on almond and citrus and on P. ulmi on citrus and Rhamnus californica Eschscholtz. At the same time that S. (P.) histrio was being released in California, S. nigripes Kapur (under the name S. loxtoni Britton & Lee) was also being released, but in far greater numbers and over a greater area. Richardson (1977) made a detailed study of all aspects of S. nigripes (calling it S. loxtoni) and argued that of all the Australian Stethorus species, this would be the species with the greatest potential of becoming established in California against T. urticae. Readshaw (1975) also shared this view, but thus far of all the Stethorus species introduced, only S. histrio has become established in California.

Sticholotidinae is a subfamily of eight tribes, five of which contain species used in applied biological control. Four tribes are natural enemies of armored scales (Diaspididae): Cephaloscymnini, Microweiseini, Sticholotidini, and Sukunahikonini (Drea & Gordon, 1990). The species in the tribe Serangiini are mainly predators of whiteflies (Gordon, 1977; Clausen, 1978; Waterhouse & Norris, 1989; Onillon, 1990). The bluntly oval eggs of the armored scale predators (Coccidophilus, Dilponis, Microweisea, Sticholotis, and some Pharoscymnus spp.) are deposited either as a single unit or as groups beneath the dorsal scale coverings of killed scales (Flanders, 1936; Muma, 1956; Brettell, 1964; Ghani & Ahmad, 1966; Ahmad & Ghani, 1971). The eggs of D. inconspicuus Pope have single slender stalks that usually project from under the scale coveting (Brettell, 1964). The whitefly predators (Catana, Delphastus, and Serangium spp.) deposit their elongate oval, translucent eggs on the underside of leaves among the whitefly immatures (Clausen & Berry, 1932; Muma, 1956; Timofeyeva & Hoang, 1978). Larvae of Sticholotidinae do not pro-

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duce waxy coverings (LeSage, 1991). Pupation occurs near larval feeding sites; pupae are exarate with all appendages free and the last larval skin pushed down posteriorly (Phuoc & Stehr, 1974). The tropical and subtropical species are multivoltine, but Coccidophilus marginata (LeConte) is univoltine in Canada, and oddly it overwinters in the third larval instar (Martel & Sharma, 1970). The tribe Microweiseini is represented by three genera that contain a few species of interest to us today. Coccidophilus citricola Brethes is a predator of red and purple scales in subtropical and temperate South America. It was introduced into California from Brazil in 1934 and 1935 as a predator of diaspine scales infesting citrus trees; it became established but disappeared a few years later (Flanders, 1936; Clausen, 1978). A mass-culturing method was developed for C. citricola in Chile and the beetle was introduced into northern Chile to prey on diaspine scales attacking olive and citrus, but it is not known if it still persists there (Aguilera et al., 1984). Coccidophilus marginata occurs in the northeastern United States and southeastern Canada where it is an important enemy of the pine needle scale (Martel & Sharma, 1970). Coccidophilus atronitens Carey is a counterpart of C. marginata, preying on the same pest but in western North America (Dahlsten et al., 1969). Microweisea coccidivora (Ashmead) is a southeastern United States species that is associated with diaspine scales on citrus in Florida (Muma, 1956). Microweisea misella (LeConte), a widespread species occurring from southern Canada to Florida and Mexico, was introduced into Bermuda to prey on Bermuda cedar scales in 1951; it became abundant but did not solve the problem because the trees continued to die (Bennett & Hughes, 1959). The tribe Serangiini contains nine genera, but we shall only mention a few species of whitefly predators belonging to three: Catana, Delphastus, and Serangium. Catana clauseni Chapin (as a Cryptognatha sp.) was collected in Malaysia feeding on citrus blackfly, Aleurcanthus woglumi Ashby, and sent to Cuba in 1930 against that same species. It became established and was still in Cuba in 1936 but declined in effect and numbers because of the great reduction of the blackfly by introduced parasitoids (Clausen & Berry, 1932; Clausen, 1978; Cock, 1985). Rees (1948) describes the larvae of C. clauseni and how to distinguish it from the larvae of Delphastus pusillus (LeConte). Delphastus pusillus was successfully imported into the Hawaiian Islands from Trinidad in 1980 as a predator of whiteflies, including the spiraling whitefly, Aleurodicus dispersus Russell, and from there to American Samoa in 1984, where it also became established against A. dispersus (Funasaki et al., 1988; Waterhouse & Norris, 1989). Delphastus pusillus naturally occurs across the southern half of the United States (Gordon, 1985). In Florida, it is a common predator of whiteflies attacking citrus trees (Muma, 1956). Adult females live 60.5 days at 28~ and development time from

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oviposition to adult emergence is 21.0 days with the consumption of 977.5 eggs of Bemisia tabaci (Hoelmer et al., 1993). In California, it is being cultured and released against the recent invading silverleaf whitefly, Bemisia argentifolii Bellows & Perring; D. pusillus is considered effective because it has a voracious feeding capacity, a high reproductive potential, a positive response to olfactory cues from whitefly-infested leaves, and the ability to discriminate and avoid feeding on parasitized whitefly nymphs (Parrella et al., 1992: Hoelmer et al., 1994; Heinz & Nelson, 1996). Serangium maculigerum Blackburn was introduced into Hawaii by Koebele in 1894 and now is found attacking several introduced whiteflies in Oahu (Leeper, 1976; Funasaki et al., 1988). Serangium parcesetosum Sicard was first found in India, where it is a predator of citrus whitefly. Timofeyeva and Hoang (1978) were unable to find any specific natural enemies of the whitefly in citrus plantations along the Caucasian coast of the Black Sea, so they imported the predator from India for study and release. The coccinellid produced four generations per year, destroyed up to 90% of the citrus whitefly population, and spread to other plantations; it overwintered successfully in the (former) USSR for at least 2 years. Serangium parcesetosum has been studied as a potential biological control agent of the silverleaf whitefly in the United States. This species is more voracious than D. pusillus, with a lifetime consumption of whitefly eggs and immatures estimated at just over 2500 at 30~ and nearly 5000 at 20~ (Legaspi et al., 1996). The impact of natural enemies on control of whiteflies is reviewed by Onillon (1990). The tribe Sticholotidini has 30 genera but only 2 concern us today, Pharoscymnus and Sticholotis, though there are apparently many new species to be described and studied in the tribe (many of which are distinguished by their reduced hind wings). The few feeding records of the species of this tribe indicate that diaspids and eriococcids are prey. Pharoscymnus is an Old World genus. Pharoscymnus horni Weise, a Ceylonese species, was cultured along with Sticholotis madagassa (Weise) and Chilocorus nigritus from Mauritius and was released at a rate of 800 adults per acre of sugarcane in Karnataka, India, for the control of the sugarcane scale, Melanaspis glomerata Green; the predators became established and the scale populations were reduced by 10 to 48% (Ansari et al., 1989). Pharoscymnus numidicus (Pic) is endemic to North Africa and the Middle East and is one of the most important predators of the date scale, Parlatoria blanchardi Targioni-Tozzetti, in Israel (Kehat, 1967). In Morocco, P. numidicus, P. setulosus Chevrolet, and P. ovoideus Sicard are predators of the date scale on palms (Smirnoff, 1957). Because of the near eradication of these predators due to insecticide use, interest in them was rekindled, with the aim of reestablishing them by releasing imported predators. Pharoseymnus numidicus was reestablished in all the date plantations in the Arava area of

al.

Israel (Kehat et al., 1974). Thus, whenever well-adapted predators are introduced under favorable climatic conditions, scale populations can be reduced to tolerable levels if no, or selective, pesticides are used (Benassy, 1990). Sticholotis madagassa Weise is not an important predator of Aulacaspis tegalensis (Zehntner) on sugarcane in Mauritius but is in Tanzania and Rrunion Island (Williams & Greathead, 1990). Sticholotis ruficeps Weise, an Asian species, somehow invaded Hawaii, where it feeds on Eriococcus araucariae Maskell and Pinnaspis buxi (Bouch~) (Leeper, 1976). Derodontidae This is another small family of beetles that would have remained obscure if it were not for one species, Laricobius erichsonii Rosenhaur, which was introduced from Europe to Canada and the United States to control a European invader, the balsam woolly aphid, Adelges piceae (Ratzeburg) (Franz, 1958). The biology of the other two genera in Derodontidae is unknown, but a few species have been reported to live in slime molds under bark and in shelf fungi. Among the seven predaceous insects that have been introduced and established against A. piceae in North America, L. erichsonii appears to be the only one exerting some control in certain areas in Canada (Franz, 1958) and it is considered the major controlling agent in Central Europe. Histeridae The biology of only a dozen of the nearly 4000 described species in this family is known in detail. However, some species have been utilized in biological control programs (Rao et al., 1971; Clausen, 1978; Waterhouse & Norris, 1987). It appears that histerids are carnivorous in both their adult and larval stages. Many genera are associated with carrion and dung, where they prey mainly on immature stages of Diptera and other coprophagous and sarcophagous insects that often occur in burrows and nests. There are genera that contain species associated with trees and rotting vegetation and prey on xylophagous insects such as bark beetles, weevils, and some immature scarabs. Species in the subfamily Hetarinae live in ant or termite nests. Eggs are usually deposited singly. The species associated with manure place them in the soil beneath cattle dung. There are three instars and pupation is in the soil or in manure within a pupal "cocoon," but the histerids in rotten wood do not make a cocoon. In temperate climates there is usually one generation a year, but some species can complete their development in about 1 month and usually overwinter as an adult (Balduf, 1935; Hinton, 1944; Nikitskiy, 1976; Morgan et al., 1983; Summerlin et al., 1989). A few histerid species have been imported to control filth flies. In 1909, Atholus bimaculatus (Linnaeus) (= Hister) was established in the Hawaiian Islands when nine individuals were imported from Germany for control of the

Chapter 16 TerrestrialArthropod Predators of Insect and Mite Pests horn fly (Legner, 1978). It also attacks houseflies in manure (Legner, 1978). Later, mostly in the 1950s, eight more histerid species were imported into Hawaii to attack the horn fly, of which four became established, including Pachylister caffer (Erichson) (Legner, 1978; Funasaki et al, 1988). A P. caffer first-instar larva can consume over 40 horn fly puparia, and a second-instar larva, over 325 (Summerlin et al., 1989). Hister nomas Erichson and P. caffer were introduced into California against houseflies and stable flies in 1969 but apparently did not become established (Legner, 1978). Pachylister chinensis Quensel, the most active predator of filth flies in manure in the South Pacific, became established in Fiji in 1936. It came from Indonesia and was credited for reducing housefly populations by Simmonds (1958), but Bornemissza (1968) believed other factors explain the reduction of flies in Fiji. Pachylister chinensis also became established in New Britain, New Hebrides, Samoa, and the Solomon Islands, but not in several other Pacific islands including the Hawaiian Islands. In California, Legner and Olton (1968) estimate that more than 95% of the destruction of fly populations in manure is caused by parasitoids and predators that attack immature stages of flies. Carcinops pumilio (Erichson) is a major predator of fly eggs and larvae in poultry manure in the United States (Geden & Axtell, 1988; Rueda & Axtell, 1997) and a simulation model of its predation on housefly immature stages was developed by Wilhoit et al. (1991). Plasius javanus Erichson was introduced from Java to Fiji in 1913 and 1914 to control the banana weevil, Cosmopolites sordidus, where the histerid reduced the weevil damage on one island. It was also introduced into the Cook Islands, Guam, Palau, and Tahiti, where it became established and reduced the damage on some islands. The histerid larvae can devour 30 or more weevil larvae per day over a 4- to 6-week period (Jepson, 1914; Rao et al., 1971; Clausen, 1978). Another species, Oxysternus maximus (Linnaeus), was found to be useful in the control of the palm weevil Rhynchophorus palmarum (Linnaeus), according to Hinton (1944). Teretriosoma nigrescens Lewis was introduced from Mexico to west Africa in 1991 for control of the greater grain borer, Prostephanus truncatus (Horn) in maize stores. The adult predators respond to the male-produced aggregation pheromone of P. truncatus and their seasonal flight patterns follow that of the host both in Mexico (Tigar et al., 1994) and in Togo (Borgemeister et al., 1997). In comparative before and after release studies in Togo, Richter et al. (1997) document a reduction in grain damage from 63% before the release of T. nigrescens to 21% following release. Among the many natural enemies associated with Oryctes rhinoceros, there are 11 histerid species in four genera in various tropical countries. Of the few histerid species introduced into eight different countries in the Pacific re-

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gion, only Pachylister chinensis became established (in four islands) while the many introductions of various Hololepta spp. failed completely (Waterhouse & Norris, 1987).

Nitidulidae Nitidulids have one of the largest feeding repertories among the Coleoptera (Lawrence, 1991b). Species of Epuraea, Glischrochilus, and Pityaphagus have been recorded as predators of scolytid eggs and larvae, but Lawrence (199 l b) thinks it is doubtful that any of these are obligate predators. However, species in the Cybocephalinae are predaceous on diaspine scales (Drea, 1990b) and whiteflies (Kirejtshuk et al., 1997). Some 150 species in the subfamily have been described, and some systematists considered them to constitute a family (Blumberg, 1973). Drea (1990b) lists 29 genera of diaspine scales that have been recorded as hosts of cybocephalines, so prey specificity needs to be determined before introducing any cybocephaline against this group (Blumberg & Swirski, 1974). The adults will feed on various arthropods other than diaspine scales such as moth, lecanine, and tetranychid eggs, but no oviposition occurs and survival is variable [oviposition did occur on Bemisia tabaci (Gennadius)]; the cybocephaline larvae were even more discriminating (Blumberg & Swirski, 1974). A few species have been imported to control diaspine scales. Heavy infestations of the date palm scale, Parlatoria blanchardi (Targioni-Tozzetti), were killing date palms in Algeria; a coccinellid and Cybocephalus nigriceps palmarium Peyrerimhoff from southern Oran (Algeria) were imported in the early 1920s, became established, and controlled the scale (Balachowsky, 1928). During the early 1940s, date palms in Moroccan oases were being killed by the date palm scale, and again the introduction of a coccinellid and the cybocephaline gave control where the predators became established (Smirnoff, 1954, 1957). During the early 1930s, a Cybocephalus sp. was introduced into California from China against California red scale; 10 years later it was found to be established in southern California (Rosen & DeBach, 1978). A Cybocephalus sp. from Trinidad was established in Bermuda by 1955 and contributes to the control of Pseudaulacaspis pentagona (Bennett & Hughes, 1959). Cybocephalus nipponicus EndrodyYounga, or a closely related species, was introduced from South Korea into the eastern United States for use against Unaspis euonymi (Comstock) infesting euonymus. It appears to be established but its impact on the scale is not evident (Drea, 1990b). Drea (1990b) concluded from reviewing the literature that in general Cybocephalus spp. alone do not appear to be important in the control of diaspine scales. Rhizophagidae The biology of this small family is poorly known. Worldwide there are 51 described species (Bousquet, 1990). It appears that both larval and adult Rhi-

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zophagus spp. are monophagous predators on certain species of bark beetles, both larval and adult. Several species in the genus Rhizophagus have been recorded or used in biological control of certain bark beetles. The Russians first observed R. grandis Gyllenhal to be an important predator of Dendroctonus micans (Kugelann), which attacks spruce and some other conifers (Kobakhidze, 1965). In old spruce stands, the bark beetle is not an important pest, but as spruce stands expanded to the West, serious D. micans outbreaks occurred in new plantations (Kobakhidze, 1965). Because R. grandis is considered the main factor for regulating bark beetle populations, Belgian, English, and French entomologists have developed a mass-rearing method for the predator and made inoculative releases of R. grandis in England and France to prevent outbreaks of D. micans (Grrgoire et. al., 1985; Gr6goire, 1988; Evans & King, 1989; Evans & Fielding, 1996). Orientation and oviposition of R. grandis are linked by simple oxygenated monoterpenes to its prey, D. micans (Grrgoire et al., 1992; Wyatt et al., 1993). Rhizophagus grandis was introduced into the United States, where inoculative releases have been made against D. terebrans Oliver (Moser, 1989). Two species of Rhizophagus were introduced from Europe into Canada and New Zealand against bark beetles in the 1930s but apparently never became established (Clausen, 1978). Staphylinidae There are about 27,000 species of rove beetles in 1,500 genera (Frank & Curtis, 1979), but the biologies of only a relatively few species of Staphylinidae are known. Larvae live in the same habitat as adults, mostly concealed in soil, decaying plant material, animal dung, or ant and termite nests; a few species are arboreal. Rove beetles are fungivorous, algivorous, saprophagous, predaceous, or parasitic (either insect parasitoids or external parasitoids on vertebrates). Most species have three larval instars, and pupation usually occurs in cells in the larval substrate; Steninae, some Paederinae, and Aleocharinae spin silken cocoons (Balduf, 1935; Frank, 1991). Predaceous species are found in Aleocharinae, Omaliinae, Osoriinae, Oxyporinae, Oxytelinae, Quediinae, Paederinae, Staphylininae, Tachyporinae, and Xantholininae. Many of the predaceous species are found associated with animal dung. Among 100 staphylinid species found in cattle dung in South Africa, the 79 predaceous species were from five subfamilies (Aleocharinae, Oxytelinae, Paederinae, Staphylininae, and Xantholininae) and the 19 coprophagous species were in the Oxytelinae (Davis et al., 1988). Hunter et al. (1991) found 21 species in 11 genera in the same five subfamilies (except for Xantholininae) associated with dung in Texas; Tachyporinae was represented in Texas but not in the South Africa dung study. Some staphylinids in the preceding subfamilies have been utilized in applied biological control. Aleocharinae is a huge subfamily that is poorly known

taxonomically and biologically. At least 72 genera of the Aleocharinae are predaceous on ants (Seevers, 1965); however, species in several genera have been used as biological control agents. All Aleochara spp., where biologies have been studied, are solitary ectoparasitoids of cyclorraphous dipteran pupae as larvae, but predators of eggs and larvae of the latter as adults (Balduf, 1935; Moore & Legner, 1971; Peschke & Fuldner, 1977; Klimaszewski, 1984). Klimaszewski (1984) recognizes seven subgenera in Aleochara. Several Aleochara spp. were introduced into North America from Europe, and some species have been masscultured and periodically released against dipteran rootworms. Aleochara (Coprochara) bilineata Gyllenhal is a Palearctic species that was apparently accidentally introduced into North America with its rootworm host puparia, Delia (= Hylemya) spp., and was reintroduced intentionally into Canada in the 1940s because it was thought that the Aleochara already present was an endemic species (Clausen, 1978; Muona, 1984). Aleochara bilineata attacks the pupae of the cabbage, onion, seed corn, and turnip (Delia) rootworms as well as on the spinach leaf miner and housefly (Anderson et al., 1983; Klimaszewski, 1984). Although parasitism of cabbage root fly in Canada is density dependent and can be as high as 94%, the introduction of A. bilineata is not considered to be sufficiently effective in reducing the abundance of this pest (Turnock et al., 1995). The insect growth inhibitor diflubenzuron will kill D. radicum (Linnaeus) but is not toxic to A. bilineata eggs or larvae (Gordon & Cornect, 1986). This species can be mass-cultured (Whistlecraft et al., 1985), and the Russians use mass culturing for releasing 20,000 to 40,000 beetles per hectare at the beginning of the egg-laying period of D. radicum and obtain full protection from the cabbage maggot (Beglyarov & Smetnik, 1977). Only 3% of marked A. bilineata were recovered in a release garden (Tomlin et al., 1992). Aleochara (Xenochara) tristis Gravenhorst is a Palearctic species introduced to North America from France as a natural enemy of the face fly, Musca autumnalis DeGeer (Drea, 1966). It was released in New Jersey, Pennsylvania, Maryland, and Nebraska, with no recoveries by 1969 (Legner, 1978). However, in a revision of North American Aleochara, Klimaszewski (1984) found specimens from Quebec, Canada, and Del Norte County of California; thus, it appears to be established in North America. Aleochara (X.) taeniata Erichson was introduced into the United States from Jamaica as a natural enemy of the housefly (White & Legner, 1966) and is now in California and Arizona (Legner, 1978; Klimaszewski, 1984). Aleochara (A.) curtula (Goeze), a rootworm and housefly predator-parasitoid, was introduced to North America from Europe. It now occurs in the eastern United States and Canada, while its presence in British Columbia may have resulted from a second introduction (Peschke & Fuldner, 1977; Klimaszewski, 1984). Oligota, another aleocharine genus, contains species that

Chapter 16

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are predaceous as adults and larvae on tiny arboreal arthropods, but apparently pupate in the soil; at least O. oviformis (Casey), a Holarctic species that preys on spider mites infesting avocado and citrus trees in California, would not pupate until exposed to soil (Badgley & Fleschner, 1956; Moore et al., 1975). It also is an important predator of tetranychid mites on citrus, pear, tea, and mulberry in Taiwan (Lo et al., 1990), and preys on Oligonychus mite on maize in Mexico; temperature threshold for the predator development is 12.5 and 15.4~ for the prey (Quinones et al., 1987). In European apple orchards, O. flavicornis Boisduval not only preys on tetranychid mites, but also feeds on thrips, whiteflies, and aphid eggs (Steiner, 1974). Oligota minuta Cameron, a common predator of cassava green mite in the Neotropics, was sent from Trinidad to Kenya in 1977 and 1983 but did not become established; in 1983, it was sent to West Africa (Cock, 1985). In Japan, Shimoda et al. (1993, 1994a, 1994b, 1997) have studied the biology and seasonal abundance of O. kashmirica benefica Naomi, an important predator of Tetranychus urticae. Atheta, another aleocharine genus of over 100 subgenera, has to be mentioned because the biology of at least one species is known in some detail. Atheta coriaria (Kraatz) adults and larvae consume eggs and early larval instars of several nitidulid beetles and houseflies (Miller & Williams, 1983). Paederinae is a fairly large subfamily composed of species found under bark, under stones, near water, and in agricultural habitats. Paederus fuscipes Curtis, an Old World species, is found with 18 other staphylinids in croplands of eastern China (Lu & Zhu, 1984). It is an important predator of several major rice pests, consuming up to 49 first-instar paddy stem borers and up to 20 first- or secondinstar plant hoppers per day; its functional response was determined as type II (Luo et al., 1989). Its importance in controlling leafhopper population densities in Malaysian rice fields is considered to be underestimated (Manley, 1977). Paederus fuscipes in sugarcane fields showed an aggregated distribution pattern based on eight different types of measurement (Lin & Gu, 1987). However, Paederus species are unlikely to be used in biological control as almost all species in all life stages contain pederin, a hemolymph toxin that causes blistering dermatitis (Morsy et al., 1996). Subfamily Staphylininae includes the largest species of the family. Several genera (including Ocypus) are placed in the genus Staphylinus by some taxonomists. In this broad interpretation, seven European Staphylinus species have been introduced inadvertently into North America (Newton, 1987). Most of these species were first collected near coastal port cities, indicating they (as well as many European carabids) were brought in the dirt used as ship's ballast from Europe. Ocypus olens Miiller, one of these introduced staphylinids, now occurs from southern California north to Oregon, and it is considered a potential agent for

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biological control of the brown garden snail, Helix aspersa Mtiller, in Califomia (Orth et al., 1975). In gardens where O. olens is found, there are fewer snails than in gardens where the staphylinid is absent (Fisher et al. 1976). In Europe it was one of the first predaceous insects to be manipulated, and around 1840 Boisgirand destroyed earwigs by placing O. olens in his own garden (Howard & Fiske, 1911). Nield (1976) studied the biology and searching behavior in the laboratory and in the field. He described the eggs of O. olens as hard shelled (as are other Staphylinus, Philonthus, and Quedius spp.), and thus differ from the soft-shelled carabid eggs; larvae ate earthworms, blowfly puparia, and Tenebrio larvae but not blowfly maggots or slugs. Like other predaceous insects, O. olens responds to prey on contact (Wheater, 1989), were more active when starved, and showed a greater rate of tuming when fed (Wheater, 1991). The genus Creophilus is considered to be in the subfamily Xanthopyginae by some taxonomists. Among the 14 widely distributed Creophilus spp. in the world (Moore & Legner, 1971), C. erythocephalus (Linnaeus) was successfully introduced from Australia into the Hawaiian Islands in 1921 to prey on the homily, Siphona irritans (Linnaeus), and houseflies and stable flies (Pemberton, 1948). Greene (1996) provides details of laboratory-rearing methods for C. maxillosus (Linnaeus), a predator of filth flies. Philonthus is a large, cosmopolitan genus in the Staphylininae and includes species having a variety of different habitats and prey. Fox and MacLellan (1956) did a precipitin test to determine that some Philonthus prey on wireworms, Agriotes sputator (Linnaeus), in Canada. Adults of P. theveneti Hom were observed to feed on houseflies and stable fly eggs in a New Brunswick feedlot by Campbell and Hermanussen (1974). They exposed the staphylinid to populations of three filth fly species in the laboratory. Stable flies were reduced by 76% and houseflies, by 37 to 41%, but no reduction was obtained in the face fly populations; thus, repeating releases of P. theveneti was considered as a possible regulating technique against stable flies. Philonthus politus Linnaeus and P. sordidus Gravenhorst in Califomia (Legner & Olten, 1968), P. cruentatus Guelin and P. flavolimbatus Erichson in Texas (Hunter et al., 1989), and P. americanus Erichson in Nebraska (Seymour & Campbell, 1993), are all common predators of houseflies and stable flies. Harris and Oliver (1979), using a ratio of 1 adult P. flavolimbatus to 10 hom fly eggs, obtained over 99% elimination of producing hom fly adults in the laboratory, but simulated field tests using the same ratio gave only a 72% reduction. Philonthus cognatus (Stephens) showed a preference for grain aphids over fungal food (Dennis et al., 1991), but only climbs wheat plants for flight (Dennis & Sotherton, 1994). Subfamily Tachyporinae contains some genera that are mainly mycetophagous. Little is known about the biology of Tachyporus, but the adults and larvae of all species are

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almost certainly predaceous (Campbell, 1979). However, within the genus there are different degrees of entomophagy and mycophagy. When Dennis et al. (1991) dissected guts and made field observations of foraging behavior of T. hypornum (Fabricius), T. chrysomelinus (Linnaeus), and T. obtusus (Linnaeus)mall known to prey on the grain aphid Sitobion avenae (Fabricius)mthey found differences in mycophagy between species. Tachyporus hypornum showed a preference for mildew conidia over aphids, while T. obtusus preferred aphids over mildew. Of the species that were abundant in cereals, T. chrysomelinus females showed a greater preference for aphids than males did. All species consumed mildew conidia, but in choice experiments, aphid consumption increased for female T. chrysomelinus and third-instar Tachyporus larvae and decreased for T. hypornum adults and first- and second-instar larvae; thus, mycophagy can limit aphid predation and influence numerical response (Dennis et al., 1991). Gut dissection should accompany the use of enzyme-linked immunosorbent assay (ELISA) in determining prey spectra and relative quantities of food eaten by polyphagous predators (Sunderland et al., 1987). Thomas et al. (1992) and Dennis et al. (1994) believe that field boundary habitats could be exploited to provide suitable overwintering sites. Subfamily Xantholininae has common species and plays an important role as predators in a wide range of habitats (Smetana, 1982), but only a few have been studied in any detail. The genus Nudobius is Holarctic and Ethiopian in its distribution, and apparently all species live under bark of dead or dying coniferous trees (Smetana, 1982). Nudobius pugetances Casey, a western North American species, preys wholly on secondary insects under the bark, which limits its usefulness as a biological control agent (Struble, 1930). Thyreocephalus albertsi (Fauvel) was collected in the Philippine Islands and was introduced into the Hawaiian Islands as a predator of the Oriental fruit fly, Dacus dorsalis Hendel. The adult staphylinids search fallen rotting fruit for fruit fly larvae, and a female can destroy 500 to 600 larvae during its life (Marucci & Clancy, 1952). There is no record of its establishment in Hawaii.

Order Diptera The Diptera order is divided into three suborders: Nematocera, Brachycera and Cyclorrhapha. A large number of dipteran families (about 30%) are predaceous at some stage during their life cycle (Hagen, 1987). Of the 21 nematoceran families, 4 include at least some predators, as do 10 of the 15 brachyceran families and 15 of the 62 cyclorrhaphan families. Some, such as Empidae, Asilidae, and Scatophagidae, are notable predators as adults but are either scavengers or carnivores in the soil during the larval stage. In other families, such as Cecidomyiidae, Syrphidae, and Chamaemyiidae, the larval stage is actively predatory while the adult stage feeds on pollen, nectar, or honeydew. There are only a few families in which both adult and larval stages

are predatory, such as Dolichopodidae, and in these cases the prey used by adults and larvae are notably different. The prey of larval dipteran predators include aquatic invertebrates, soil invertebrates, Homoptera and other small arthropods, wood-boring beetles, Orthoptera eggs, and mollusks, while the prey of adults include a wide variety of small arthropods. Although many of the predaceous Diptera may play an important role in the natural regulation of prey populations, only those that have been more actively considered as biological control agents will be discussed here.

Cecidomyiidae Cecidomyiidae is a large family of very small, fragile insects that are readily recognized by their long, hairy, beadlike antennae and reduced wing venation. The majority of these gall midges are true gallforming species, some of which are notorious pests; however, the family also includes some important predators of spider mites, Homoptera, and other Cecidomyiidae (Nijveldt, 1969). A number of cecidomyiid genera, including Coccodiplosis, Dicrodiplosis, and Vincentodiplosis, appear to have specialized on coccoid prey (Harris, 1968, 1990). There is little detailed information on their biology and impact on prey populations, but preliminary observations (Harris, 1968) indicate that they are likely to be of importance as natural controls. The genera Arthrocnodax, Feltiella [revised by Gagne (1995)] and Therodiplosis contain a number of species that are predatory on spider mites (Chazeau, 1985), and Lestodiplosis contains species predatory on a wide range of prey, including other cecidomyiids. McMurtry et al. (1970) reported A. occidentalis Felt to be a good predator, consuming 380 mites over a period of 17 days. The aphid predators are the most well-known group of predatory midges and have received the greatest attention in biological control. The genera Aphidoletes (three species) and Monobremia (one species) feed exclusively on aphids (Harris, 1973). Aphidoletes aphidimyza (Rondani) is the best known species of the group with a distribution throughout the Northern Hemisphere. There are many accounts of its biology (e.g., Harris, 1973; Markkula et al., 1979; Nijveldt, 1988). Adults emerge from pupae in the soil and are nocturnal in habit, living for up to 14 days, with a fecundity of up to 100 eggs. The orange eggs (0.3 X 0.1 mm) are laid singly or in clusters on plants near aphid colonies. The eggs hatch in 3 to 4 days and the firstinstar larvae immediately attack aphids, paralyzing them with an injected venom (Laurema et al., 1986). Larval development is completed in 7 to 14 days during which time they can kill from 5 to 10 large aphids or up to 40 to 80 small aphids. Pupation occurs in silken cocoons in the soil. Adults emerge after 1 to 3 weeks, depending on temperature, and the life cycle is often completed in about 3 weeks [280.2 degree days above a threshold temperature of 6.2~

Chapter 16 TerrestrialArthropod Predators of Insect and Mite Pests (Havelka, 1980) and 284 degree days above 9.2~ (Raworth, 1984)]. Aphidoletes aphidimyza appears able to distinguish between different aphid densities, laying eggs in proportion to the density of Myzus persicae on brussels sprouts (E1Titi, 1973) and Aphis pomi, on apples (Stewart & Walde, 1997). Aphid honeydew is used as a food by females (Uygun, 1971) and may also be used in prey location (Havelka & Syrovatka, 1991). Honeydew is also attractive to the newly hatched larvae (Wilbert, 1977) and this may help them to find the aphid colony. Adult females can distinguish different host plants. Mansour (1975) reported that after rearing three generations on M. persicae on turnip root cabbage, more eggs were laid on this host plant than on brussels sprouts. There are several features of the biology of A. aphidimyza that enhance its potential as a biological control agent. E1-Titi (1973) has demonstrated that oviposition is density dependent, although only weakly so under field conditions (Stewart & Walde, 1997). It also tends to kill more aphid prey than it consumes (Uygun, 1971), which could result in density-dependent prey mortality. The range of aphid prey accepted is broad (Harris, 1973) and covers all greenhouse aphid pests (Markkula et al., 1979), enabling it to be used against a variety of aphid pests on different greenhouse crops. Of the aphid predators, A. aphidimyza is the only one that can maintain populations throughout the season under glass (Ramakers, 1988). The midge is very easy to rear (Markkula & Tiittanen, 1976, 1985) and has been produced commercially both in Europe and in Canada since the early 1980s. The pupae in cocoons are very resilient and provide an ideal stage for transportation and release in the crop. The ability of A. aphidimyza to withstand cold storage at 5~ for up to 8 months has been demonstrated (Gilkeson, 1990). Cold storage is an important attribute for the commercialization of a biological control agent and this advancement is likely to lead to more widespread use of A. aphidimyza for the biological control of aphids, not only under glass but also in small-scale plantings of high-density field or orchard crops (e.g., Bouchard et al., 1988). There has been considerable interest in the potential of A. aphidimyza as a biological control agent for aphids in greenhouses in the former USSR (Ushchekov, 1975; Storozhkov et al., 1981), Europe (Markkula & Tiittanen, 1980; van Lenteren & Woets, 1988), China (Cheng et al., 1992), and North America (Meadow et al., 1985; Gilkeson & Hill, 1987). Two to three applications of pupae at 7- to 10-day intervals, using release rates of 1 predator to 200 aphids, kept Aphis gossypii in check on cucumber in the former USSR (Ushchekov, 1975). In contrast, in Finland (Markkula & Tiittanen, 1980) and in the United States (Meadow et al., 1985) release rates of one predator to three aphids at 14-day intervals were required to control M. persicae on peppers and tomatoes. A comparison of release rates for control of M. persicae on peppers was made by Gilkeson

451

and Hill (1987), who found that a ratio of 1 predator to 10 aphids gave the best results. It seems likely that both hostplant characteristics including size and surface morphology and the degree of aggregation of the target aphid could affect the performance of Aphidoletes aphidimyza in different greenhouse crops and could necessitate further examination of required release rates. Syrphidae Syrphidae, or hover fly, is a large family of Diptera particularly well known for striking mimicry of bees and wasps. The feeding habits of the family are diverse but the subfamily Syrphinae are important predators of aphids and other Homoptera (Gilbert, 1981; Chambers, 1988), and occasionally of chrysomelid leaf beetles (Rank & Smiley, 1994); and the tribe Pipizini of the Eristalinae are important predators of gall-forming aphids (Rojo & Marcos-Garcia, 1997). The predaceous syrphids can be divided into two groups, obligate predators and facultative predators (Chandler, 1968a; Rotheray, 1983). The majority of species belong to the former group, while some Melanostoma species and perhaps almost all Platycheirus species are facultative predators and have the ability to make use of rotting plant material to complete their development. Adult females emerge with an undeveloped reproductive system and require a protein source to mature eggs. The principal food of adult syrphids includes pollen and nectar (Gilbert, 1981; Hickman et al., 1995). Mating has rarely been observed in syrphids and often takes place on the wing. A few species such as Syrphus ribesii (Linnaeus) form male swarms. The fecundity of Epistrophe nitidicollis (Meigen) was estimated to be 126 (Tinkeu, 1995), but that of other syrphids can be as large as 500 to 1500 eggs, as for Metasyrphus corollae (Fabricius) (Benestad, 1970; Scott & Barlow, 1984). The white eggs (1.0 X 0.5 mm) are generally laid singly on the underside of leaves supporting aphid colonies. The identity of the eggs of some species can be determined from their surface sculpture (Chandler, 1968b). The duration of the egg stage is about 5 days. The hover fly larvae are active between dusk and dawn; their nocturnal habits make them less conspicuous than other aphid predators. They have sucking mouthparts and often lift the aphid prey from the plant surface while feeding. Prey consumption rates in the laboratory vary from a low of 135 aphids for Platycheirus clypeatus (Meigen) (Bankowska et al., 1978) to as many as 550 for Scaeva pyrastri (Linnaeus) (Wnuk & Fuchs, 1977). Larval development in Episyrphus balteatus (DeGeer) can be completed in as little as 10 days but more frequently extends to about 40 days under field conditions (Ankersmit et al. 1986). Pupation occurs on the plant or in the leaf litter and adults emerge after 1 to 3 weeks. The majority of syrphid predators are multivoltine, although some are univoltine, and overwinter as final instar larvae, pupae, or adults. The range of prey consumed by

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predaceous syrphid larvae can be extensive. Ruzicka (1975) reported that the polyphagous M. corollae can successfully develop on 12 different aphids but that the development rate and adult size [which can affect subsequent fecundity (Scott & Barlow 1984)] vary between prey species. One species, Cavariella theobaldi (Bragg), was found to be toxic to the syrphid. Syrphids are also attacked by a wide range of parasitoids (Rotheray, 1984). The oviposition behavior of aphidophagous syrphids is influenced by a number of olfactory, visual, and mechanical cues (Chandler, 1968a; Chambers, 1988). In M. corollae, oviposition is stimulated by olfactory cues originating from honeydew or from aphid comicle secretions (Bombosch & Volk, 1966; Hagen et al., 1970a; Ben Saad & Bishop, 1976; Budenberg & Powell, 1992). The ovipositor appears to have sensilla responding to honeydew components (Hood Henderson, 1982), whereas antennal sensilla respond to green leaf volatiles (Hood Henderson & Wellington, 1982). For E. balteatus, females land on ears of wheat more frequently if contaminated with honeydew and the number of eggs laid increased with honeydew concentration (Budenberg & Powell, 1992). Metasyrphus corollae also appears to prefer vertical surfaces (Sanders, 1980) and darker surfaces (Sanders, 1981) for oviposition. Cannibalism of eggs by third-instar larvae of E. balteatus is common under laboratory conditions (Branquart et al., 1997), but the extent of cannibalism in the field is unknown. Oviposition by Platycheirus and some Melanostoma species, the facultative predators, differs from that of the obligate predators in that eggs are frequently laid away from aphid colonies (Chandler, 1968b). These eggs are laid in small groups in a row and there is some evidence that the young larvae are cannibalistic. Syrphids have occasionally been used in classical biological control but to date all have failed to establish in the target regions, perhaps due to a lack of mating [see Waage et al. (1984)] in released material. The impact of syrphids in the context of natural control has seldom been assessed in detail and their role may have been underestimated as a result of their nocturnal activity. Bugg (1993) concludes that it is difficult to demonstrate the effect of field margins and flowers, as adult food sources, on the effectiveness of syrphid predation. However, observations on E. balteatus suggest that it selectively feeds on noncrop plants around the margins of cereal fields in England (Cowgill et al., 1993a) and that natural control of cereal aphids could be enhanced by modified management of field boundaries (Cowgill et al., 1993b), particularly using Phacelia tanacetifolia as a border plant (Hickman & Wratten, 1996) Three different techniques have been used to study syrphids: field cages for predator exclusion, laboratory cage studies, and modeling. Predator exclusion studies (Tamaki & Weeks, 1973; Chambers et al., 1983; Hopper et al., 1995) indicate the value of the aphidophagous predator complex as a whole but do not permit the separation of the

effects of syrphid from coccinellid predation. Laboratory cages were used by Wnuk (1977) to demonstrate that E. balteatus can eliminate colonies of Aphis pomi within a few days with predator to prey ratios of from 1:50 to 1:200. Predation within cages is undoubtedly greater than under field conditions and may indicate the potential of syrphids for use in greenhouses. Some preliminary experiments using M. corollae for the control of A. gossypii on cucumber in greenhouses (Chambers, 1986) have demonstrated promise but currently the cecidomyiid Aphidoletes aphidimyza is favored due to its ability to produce self-perpetuating populations and its ease of rearing (see earlier). Bombosch (1963) first suggested that the impact of syrphids could be evaluated by modeling the predator feeding potential. This approach has been extended by Tamaki et al. (1974) and Chambers and Adams (1986) but these models remain dependent on how applicable laboratory data on predator feeding potential relate to predator power in the field. For example, Tenhumberg (1995) estimated the feeding potential of E. balteatus in field cages to be only half that found in laboratory studies.

Chamaemyiidae Chamaemyiidae is a small family of predatory silver-colored flies specializing on coccoid and aphidoid prey. Several species have been successfully used for the classical biological control of adelgid pests. It is surprising, therefore, that the biology and the range of prey attacked by this group of predators are in general poorly known. Detailed information is restricted to only a few species. Of some 12 genera worldwide (McAlpine, 1960; Tanasijtschuk, 1993), the majority of species belong to the rather large genus Leucopis. The subgenus Neoleucopis contains species that are predators of adelgids (McAlpine, 1971; McLean, 1992), especially Adelges, Pineus, and Sacciphantes. The subgenus Leucopis also contains some adelgid specialists (e.g., L. argenticollis Zetterstedt and L. astonea McAlpine) as well as the genera Cremifania (Brown & Clark, 1956) and Lipoleucopis (Wilson, 1938). Other species in the subgenus Leucopis are predators of aphids (Tawilk, 1965; Sandhu & Kaushal, 1975; Tracewski, 1983; Tanasijtschuk, 1996), phylloxerids (Stevenson, 1967), mealy-bugs (Sluss & Foote, 1971, 1973), or soft scales (N. J. Mills, unpublished). The adelgid predators can be univoltine, such as Lipoleucopis praecox (Meigen) (Wilson, 1938), but are more typically bivoltine, such as Leucopis tapiae B lanchard (Eichhom et al., 1972), L. pinicola Malloch (Sluss & Foote, 1973), and L. obscura Haliday (Brown & Clark, 1956). In contrast, the aphid and scale predators appear to be multivoltine, as is L. verticalis Malloch (Sluss & Foote, 1971), L. conciliata McAlpine & Tanasijtschuk (Tanasijtschuk, 1959), and Chamaemyia polystigma Meigen (Sluss & Foote, 1973). The life cycle is similar for all species and is represented here by L. pinicola (Sluss & Foote, 1973). The

Chapter 16 TerrestrialArthropod Predators of Insect and Mite Pests adults emerge from puparia in the bark or soil and have a preoviposition period of about 18 days and a fecundity of about 40 eggs. Adults live about 25 to 30 days and lay small groups of white eggs (0.4 • 0.1 mm) in association with colonies of their prey. Eggs hatch after 8 to 10 days and the duration of the three larval instars is about 3 weeks under laboratory conditions. The larvae move away from the prey colonies to pupate and the pupal period lasts about 2 weeks in the laboratory. Methods for rearing Leucopis species have been developed by Gaimari and Turner (1996a). These chamaemyiid predators appear to be relatively restricted in the range of prey that they attack. The subgenus Neoleucopis is restricted to adelgids and within this group there are species specializing on Adelges, Pineus, or Sacciphantes prey (McAlpine, 1971). Greathead (1995) considers the Palearctic species L. obscura and L. atratula (Ratzeburg) to be associated with Adelges on fir, whereas L. tapiae, L. atrifacies Aldrich, L. nigraluna McAlpine, and L. manii McAlpine are asoociated with Pineus on pine. Among the aphid and coccid specialists, Leucopis conciliata and L. verticalis are known only in association with a few closely related prey species (Sluss & Foote, 1971; McAlpine & Tanasijtschuk, 1972). The larvae of the aphid predators L. gaimarii Tanasijtshuk and L. ninae Tanasijtshuk are voracious predators consuming about 100 aphids before completing their development (Gaimari & Turner, 1996b). The prey location mechanisms of Chamaemyiidae have not been studied. Several Leucopis species and Cremifania nigrocellulata Czerny have been used in the classical biological control of Adelges piceae in North America; Pineus pini (Macquart) in Hawaii; and P. laevis (Maskell) in Australia, New Zealand, and Chile (Mills, 1990). Three Leucopis species and C. nigrocellulata have been established against A. piceae in North America but control has not been achieved (Clark et al., 1971). In contrast, L. tapiae in New Zealand (Zondag & Nuttall, 1989), L. obscura in Chile (Zuniga, 1985), and both L. tapiae (originally misidentified as L. obscura) and L. nigraluna in Hawaii (Culliney et al., 1988; Greathead, 1995) have provided successful control of Pineus species. In addition, the Palearctic aphid predator L. ninae has been introduced to the western United States against the Russian wheat aphid (Tanasijtschuk, 1996).

Dolichopodidae This is a large family comprising more than 2000 species of small, bristly flies that are often metallic green or blue. The adults are predatory on small, soft-bodied insects and mites, and the larvae are probably all carnivorous. Dolichopodid species are found in a wide variety of habitats but the best known predators are those of the Medetera genus that prey on the larvae and pupae of wood-boring insects. Medetera is a distinctive genus of more than 250 described species and their association with bark beetles has

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attracted attention in both the Nearctic and Palearctic regions (Bickel, 1985). Most Medetera larvae are subcortical predators where they have been recorded preying on scolytids (DeLeon, 1935; Nuorteva, 1959; Beaver, 1966; Nicolai, 1995), Pissodes weevils (Deyrup, 1978), and other bark-inhabiting insects. Medetera aldrichii Wheeler has been studied in the most detail (DeLeon, 1935; Schmid, 1971; Nagel & Fitzgerald, 1975). Eggs are laid under bark scales and the hatching larvae enter the bark beetle galleries to feed on the prey. Full-grown larvae overwinter before pupation and adult emergence occurs in the spring. Although Kishi (1969) reported Medetera larvae to be scavengers instead of predators, other studies (DeLeon, 1935; Beaver, 1966; Schmid, 1971; Nagel & Fitzgerald, 1975) demonstrate that they are voracious predators consuming from 6 to 15 prey during their larval development. Medetera species appear to be able to make use of the aggregation pheromones of their bark beetle prey to locate suitable host trees for the development of their progeny. Various Medetera species have been attracted both to naturally infested tree bolts and to traps baited with synthetic aggregation pheromones (Williamson, 1971; Fitzgerald & Nagel, 1972; Borden, 1982; Mills & Schlup, 1989). Nagel and Fitzgerald (1975) also found that the orientation of the newly hatched larvae of M. aldrichii to scolytid entrance holes was stimulated both by the host tree volatile D-apinene and an extract of the frass of Dendroctonus pseudotsugae Hopkins. Medetera species appear not to be particularly specialized in relation to their bark beetle prey and have never been used in a biological control program. Moeck and Safranyik (1984), however, considered that the observed abundance and predation potential of Medetera species would make them good candidates for augmentative biological control of bark beetle pests.

Lonchaeidae Little is known of this moderately sized family of flies though in many cases the larval stages are considered to be scavengers on rotting vegetation or dung. A notable exception, however, is Lonchaea corticis Taylor, an active predator of the prepupae and pupae of the subcortical weevil, Pissodes strobi (Peck), that attacks the leading shoots of young pines and Sitka spruce (Alfaro & Borden, 1980; Hulme, 1989). The young larvae develop as scavengers in the larval galleries of the weevil, becoming predatory only when the prey have completed their larval development and formed a pupal cell under the bark. Each L. corticis larva can then consume about three pupae (Alfaro & Border, 1980), which results in a significant reduction in overwintering populations of the weevil (Hulme, 1990). One of the most effective means of controlling the weevil is to remove attacked leaders during winter, and techniques have been developed to use cold hardiness as a means of conserving the natural enemies from cut leaders (Hulme et al., 1986).

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Sciornyzidae The sciomyzid, or marsh fly, family is composed of about 600 species living in all zoogeographic regions of the world. It was not until 1953 that Berg (1953) first reported an association of sciomyzids with snails and other mollusks. Since then, the family has become one of the better known biologically, in view of its importance in natural and biological control (Knutson, 1976). The feeding behavior of the sciomyzids varies from parasitism, through predation to saprophagy, with many intermediate forms. Most of the predaceous larvae are aquatic and feed on freshwater snails occurring at or near the water surface. Slugs and terrestrial or semiaquatic snails are the hosts of the parasitic species. Dictya species provide an example of the biology of predaceous sciomyzids (Valley & Berg, 1977). Adults live for up to 100 days and generally have a preoviposition period of less than 3 weeks. The fecundity of females extends to several hundred eggs (white, 0.7 X 0.2 mm); these tend to be laid in rows on vegetation and the larvae hatch after 2 to 4 days. The prey include a variety of aquatic pulmonate snails. Larvae may feed for over an hour on a single prey but are seldom found in the field in contact with their prey. The larvae are able to swim across the surface of water and attack their prey by crawling between the shell and mantle. From 12 to 53 snails are killed by a single larva during its development. Puparia are formed on the water surface and adults emerge after 7 to 9 days. The biology of Nearctic Tetanocera species that are predators of semi-aqautic snails is provided by Foote (1996a, 1996b). Vala et al. (1995) describe the life history and larval biology of the Afrotropical Sepedon trichrooscelis Speiser. Gormally (1988) examines the influence of temperature on snail predation in Illione albiseta (Scopoli), and McLaughlin and Dame (1989) provide notes on rearing D. floridensis Steyskal. There are relatively few sciomyzids that are known to attack slugs (Reidenbach et al., 1989). Trelka and Foote (1970) provide details of the biology of three Nearctic Tetanocera species that spend the first two instars as parasitoids and the final instar as predators of slugs. The univoltine Euthycera cribrata (Rondani) is a European species that lays 400 to 600 eggs after a preoviposition period of several months (Reidenbach et al., 1989). Larvae sit and wait for a passing slug or snail and then burrow into the host, feeding first as a parasitoid and then as a predator or saprophage once the host dies. Each host is used for 4 to 11 days and the larvae attack 15 to 25 slugs over a period of 2 to 3 months of larval development. In a survey of sciomyzids attacking terrestrial helicid snails in the Mediterranean, Coupland (1996a) found six species. The majority of species were univoltine, with a preoviposition period as long as 72 days and a larval development period of up to 6 months. Most species were associated with forest and scrubland, although the multivoltine

Pherbellia cinerella (Fallen) is associated with pastures (Coupland & Baker, 1995). The predators of aquatic pulmonate snails appear to have a broad host range. In contrast, the parasitoid species are more restricted in host range, the Tetanocera species being confined to a single genus of slugs or even to a single species of Deroceras slugs in the case of T. plebeia (Loew) and T. valida (Loew) (Trelka & Foote, 1970). Prey specificity among the predators and saprophages of terrestrial snails appears to vary from being very broad to quite specific (Coupland et al., 1994; Foote, 1996a). Little is known of the prey location mechanisms in the Sciomyzidae, but Coupland (1996b) demonstrated that the feces of terrestrial snails induced oviposition by Pherbellia cinerella, and both feces and mucus stimulated the search of first-instar larvae. Sciomyzids have been used several times as potential biological control agents of aquatic snails (Mead, 1979; Godan, 1983). For example, in 1959 the Nicaraguan Sepedon macropus Walker was imported into Hawaii (previously devoid of Sciomyzidae) against Lymnaea ollula Gould, the principle vector of the giant liver fluke. The flies established and became abundant but their impact on the snail vector has not been adequately studied, although the incidence of the liver fluke has declined (Chock et al., 1961; Knutson, 1976). Marharaj et al. (1992) have considered the potential of S. jonesi Barraclough (= scapularis Adams) for biological control of Bulinus africanus (Krauss), an important vector of bilharzia blood flukes in Africa. There have been no introductions of sciomyzids for the biological control of terrestrial snails. However, there has been considerable interest in the potential of European species for the control of four exotic species of helicid snails in Australia (Coupland et al., 1994; Coupland & Baker, 1995; Coupland, 1996a). Order Hymenoptera The Hymenoptera constitute one of the largest and oldest orders of holometabolous insects. More than 120,000 species have been described, but the actual number of species is considerably higher. In terms of geologic age, the Hymenoptera have a fossil record referable to the Triassic. Taxonomically, the Hymenoptera are divided into the suborders Symphyta and Apocrita. The Apocrita are divided into the divisions Parasitica and Aculeata. Collectively, Symphyta, Parasitica, and Aculeata represent well-recognized lineages whose relationships to one another are not clearly established. Hymenoptera are important for understanding entomophagous habits because they are numerically large and biologically diverse, with all forms of phytophagy, predation, and parasitism expressed within each lineage. Traditional definitions of parasitism and predation are provided elsewhere in this book. These definitions fail when examining details of the biology of many Hymenoptera because

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we see complex life histories with some species utilizing different feeding strategies between the larval and adult stages. For instance, the larva may express characteristics of a parasitoid while the adult shows signs of predation. Indeed, this problem is reflected in numerous articles that cover "host records" and "prey selection" in discussing a species. Hagen (1987) lists the families of Hymenoptera in which predation has been reported. A modification of that list is provided in Table 1. From the standpoint of feeding behavior, predaceous Hymenoptera adults also consume pollen and take nutrition from floral and extrafloral nectaries. Much of the information concerning predation by Hymenoptera is anecdotal and the role of plant food is not clear. Nevertheless, at the family level trends in the evolution of predation are apparent. The impact of predatory behavior by Hymenoptera on economic pests has not been appreciated because it is difficult to measure. Many species feed casually on other insects and the magnitude of the impact of this predation has not been appreciated in terms of biological control. However, Hagen et al. (1976a) discuss the biology of predators as it relates to biological control. Anatomical features that have been adapted for predation are important in understanding the position of Hymenoptera as predaceous insects. Mandibulate mouthparts and an appendicular ovipositor are anatomical features common to many Hymenoptera, and are essential for the implementation of predatory behavior. Mandibles are used by many insects to consume prey, but careful observation must be exercised to distinguish between malaxation and feeding. For instance, many reports of adult parasitoids host feeding exist but these must be confirmed to establish genuine predation. Predaceous Hymenoptera feed on all stages of development, but most often they attack the immature stages of their victims. The egg stage is vulnerable to attack by predators and sometimes species that are usually classified as parasitic behave as predators. For instance, many groups of Parasitica attack the egg stage. When a developing larva consumes one egg, it is generally regarded as parasitic; when a developing larva consumes more than one egg, it is generally regarded as an egg predator. We see this in some Pteromalidae (Scutellista), Scelionidae (Baeus), and Eurytomidae (Desantisca spp.). Larvae, nymphs, and adults may have methods of defense that are somewhat helpful in deterring predation by Hymenoptera. The pupae of some insects have gin traps, which may help deter predation or parasitism. However, the pupa is generally more vulnerable than the nymph, larva, or adult.

Syrnphyta The Symphyta (wood wasps, horntails, and sawflies) are cosmopolitan in distribution with about 10,000

TABLE 1

Families of H y m e n o p t e r a with Predatory Behavior

Family

Predaceous Stage

Taxa of Prey

Symphyta Tenthredinidae

Adult

Coleoptera, Diptera, Homoptera

Ichneumonidae

Parasitica Adult, larva Spider eggs, bee eggs, larvae

Braconidae

Adult, larva

Diptera, Lepidoptera

Evaniidae

Larva

Dictyoptera eggs

Gasteruptiidae

Larva

Hymenoptera larvae

Aphelinidae

Adult

Scale insects

Encyrtidae

Adult, larva

Scale insect eggs

Eulophidae

Adult, larva

Lepidoptera and Coleoptera larvae, eggs of many insects and some spiders

Eupelmidae

Adult, larva

Eggs of many insects

Eurytomidae

Larva

Orthoptera, Homoptera eggs

Pteromalidae

Adult, larva

Coccidoidea eggs

Scelionidae

Adult

Mantid adult

Torymidae

Larva

Mantid eggs

Trichogrammatidae

Adult

Lepidoptera eggs

Chrysididae

Aculeata Adult, larva

Hymenoptera and their prey

Bethylidae

Adult

Coleoptera, Lepidoptera

Dryinidae

Adult

Homoptera

Mutillidae

Adult

Hymenoptera larvae

Tiphiidae

Adult

Scarabaeidae larvae

Thynnidae

Adult

Scarabaeidae larvae

Pompilidae

Adult

Spiders

Formicidae

Adult, larva

Many arthropods, including insects

Eumenidae

Adult, larva

Lepidoptera, Coleoptera larvae

Masaridae

Adult, larva

Vespidae

Adult, larva

Lepidoptera, Coleoptera larvae

Sphecidae

Adult, larva

Many insects

After Hagen, K. S. (1987). In F. Slansky, Jr. & J. G. Rodriguez (Eds.). Nutritional ecology of insects, mites, and spiders. (pp. 533-577). New York: John Wiley & Sons.

nominal species. Symphyta are the most primitive Hymenoptera based on adult and larval morphology. Xyelidae are among the earliest fossils and possess features not present in other Hymenoptera (Rasnitsyn, 1980). Some contemporary taxonomists believe that the Symphyta are a paraphyletic group because they possess anatomical features common to all Hymenoptera. Hymenopterists have not

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thoroughly explored the relationship between taxonomic characters and biological characteristics. Thus, we cannot infer that biological features observed in closely related groups did not evolve more than once. The most conspicuous adult feature that separates most Symphyta from Apocrita is the broadly attached, sessile metasoma (gaster) to the mesosoma, though some groups of Parasitica also display a relatively broadly attached mesosoma and metasoma. The appendicular ovipositor is welldeveloped in Symphyta and Apocrita. In sawflies it is used to saw plant tissue, but in the more highly evolved Hymenoptera it serves several additional functions that are discussed elsewhere. Larval Symphyta differ from Apocrita in that the former displays a well-developed head capsule with strong mandibles and resembles caterpillars. The larval thorax of most sawflies has three pairs of legs and the abdomen holds six to eight pairs of prolegs, providing the larva feeds externally. There are no crochets on the prolegs of sawflies as seen in caterpillars. Conventional wisdom views the Symphyta as phytophagous. The larval stages of most Symphyta are phytophagous but a few (Orussidae) are parasitic. Clausen (1940) reports that the adults of some tenthredinids are predaceous.

Parasitica Aspects of predation among so-called parasitic Hymenoptera (division Parasitica) have been discussed by Jervis and Kidd (1986) and Heimpel and Collier (1996). The consumption of host body tissues or fluids by an adult parasitoid is an aspect of biology that may be viewed as a form of predation. For lack of a better term, this phenomenon has been called "host feeding" by entomologists. Bartlett (1964a) provided the first comprehensive review of the phenomenon in parasitic Hymenoptera. Among parasitic Hymenoptera both sexes typically take food as adults, but host feeding seems restricted to adult females. The victim is not necessarily killed, and the role that moribund hosts play in population dynamics has not been examined. In a different context, victims may not be used as a host for progeny development. That is, many adult parasitic Hymenoptera feed on body fluids of potential hosts without laying eggs in or upon these potential hosts. Host feeding appears widespread among the Apocrita. Jervis and Kidd (1986) report that more than 140 species in 17 families of Hymenoptera engage in host feeding. Host feeding can affect the female wasp in several ways, including physical maintenance, longevity, and fecundity. The relationship between physical maintenance and longevity is intimate and difficult to separate and few studies have attempted to do this. From the female parasitoid's perspective, host feeding many be an alternative to starvation. During the process of starvation some wasps, such as the

ichneumonid Pimpla turionellae (Linnaeus), may undergo the loss of flight musculature (Sandlan, 1979). Several studies of parasitic Hymenoptera in many families have shown that fecundity is highest in females that have been provided host hemolymph. Flanders (1950) called neonate parasitic Hymenoptera females synovigenic when they did not possess a full complement of eggs ready for oviposition. Flanders contrasted this condition with socalled proovigenic parasitoids that emerge as adults with a full complement of eggs ready for oviposition. Flanders hypothesized that synovigenic female parasitoids must consume nutrients that are necessary for the development of their eggs. Feeding on host body fluids is one source of nutrition that may provide necessary nutrients for egg development in synovigenic parasitoids. While this characterization is conceptually appealing, we should observe that there are few rigorous data that could be used to support this dichotomy of reproductive capacity or physiology. However, one study of host feeding in Aphytis melinus DeBach clearly shows that while host hemolymph does not support the longevity of parasitoid adults, the typical hostfeeding pattern of one host per day contributes nearly four eggs per host feed to their fecundity (Heimpel et al., 1997). Female parasitoids use various anatomical techniques to feed on an insect that can be viewed as a potential host. To feed upon a host, some species use the ovipositor to inflict a wound from which hemolymph wells. The fluid is imbibed by the female parasitoid. Other species construct a feeding tube with the ovipositor. The parasitoid thrusts the ovipositor into the body of the host and hemolymph coagulates around the ovipositor, thereby forming a tube. When the tube is completed, the female parasitoid applies her mouthparts to the apex of the tube and feeds on host fluids via capillary action (Fulton, 1933). Some species of parasitoids use their mandibles to mutilate the host and feed on host body fluids at the wound. Other species consume host tissues in addition to body fluids (Waloff, 1974). Several types of host-feeding behavior have been outlined by Jervis and Kidd (1986). Concurrent host feeding involves females that oviposit and host feed on the same individual; nonconcurrent host feeding involves females that do not oviposit on the same individual used for host feeding. Destructive host feeding involves the death of the victim on which the parasitoid feeds; nondestructive host feeding relates to victims that survive the host-feeding process. Destructive feeding is usually nonconcurrent because the victim is not suitable as an ovipositional resource (a host). The impact of nondestructive host feeding may be even more difficult to document under field conditions, and thus more difficult to assess in terms of usefulness in biological control. Nondestructive feeding may be nonconcurrent or concurrent. During the lifetime of an adult parasitoid we can see autogenous and anautogenous host-feeding behavior. Autogenous species are capable of laying a comple-

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ment of eggs without host feeding. In such species, host feeding may be facultative. Anautogenous species must host feed to provide nutrition for the egg that is otherwise unavailable; in such species, host feeding is obligatory. Host feeding may be related to egg resorption. Many parasitic wasps resorb eggs that are not passed from the ovariole in a timely manner. Studies by Antolin and Williams (1989) on Muscidifurax zaraptor Kogan & Legner, a synovigenic pupal parasitoid of houseflies, and by Collier (1995) on A. melinus, a synovigenic nympal ectoparasitoid of California red scale, report that both parasitoids resorb eggs when starved and that host feeding is necessary for continued egg maturation. Early specialists in biological control apparently regarded host feeding as an ancillary aspect of parasitoid behavior. Nevertheless, a few studies suggest that host feeding can result in a significant level of mortality (DeBach, 1943). Gadd and Fonseka (1945) note that Neoplectrus maculatus Ferriere kills and consumes one nettle grub for each three that are used as hosts. Gadd et al. (1946) suggest that Platyplectrus natadae Ferriere kills one nettle grub for each four that are used as hosts and P. taprobanes (Gadd) kills one nettle grub for each six that are used as hosts. However, theoretical evidence suggests that the inclusion of host feeding in a host-parasitoid model leads to an increase in the equilibrium density of a host population (Mills & Getz, 1996). In an effort to resolve the conflict of between conventional wisdom and theory, Jervis et al. (1996) analyzed the biological control record of parasitoid introductions against Homoptera. They found that destructive host feeders were superior in both rates of establishment and success, suggesting that other attributes, such as searching ability, may be linked to host feeding in parasitoids.

Aculeata Predation by adult aculeates represents a very different phenomenon than the host feeding observed within the parasitic Hymenoptera. A feature almost universally present in aculeates is the sting, with its attendant glandular secretions. Only females possess the sting. A few groups of Aculeata, such as some bees and ants, have lost the sting. However, for the bulk of the Hymenoptera, the sting represents an obvious anatomical adaptation that enables the bee, wasp, or ant to defend itself from predation and/or to immobilize prey.

Chrysidoidea are regarded as the most primitive aculeate Hymenoptera. Six families are members of the Chrysidoidea: Bethylidae, Chrysididae, Dryinidae, Embolemidae, Sclerogibbidae, and Scolebythidae. The Sierolomorphidae have sometimes been placed within the Chrysidoidea in some classifications, but their true affinities lie with the Scolioidea. All families of Chrysidoidea are viewed as

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parasitic, but adults of some groups show predaceous characteristics. For instance, adult Dryinidae commonly feed on hosts, which may be nonconcurrent (Waloff, 1974; Chua et al., 1984). Dryinidae are remarkable among parasitic Hymenoptera in that the adults are larger than the hosts that they parasitize. This fact may be attributed to the prolonged feeding time without apparent harm to the host. A consequence of this feeding behavior is that smaller species of hosts can be utilized by relatively large-bodied dryinids (Ponomarenko, 1975). Bethylidae host feeding by adult females is more sporadic. Epyrinae, such as Laelius pedatus (Say), Holepyris glabratus (Fabricius), and Sclerodermus spp., often host feed (Bridwell, 1919, 1920). Sclerodermus species do not pierce the integument of the host, but feed on hemolymph exuded through the cuticle during malaxation (Bridwell, 1920). Female Sclerodermus also feed on hosts on which parasitoid larvae are developing and will feed on their own eggs and larvae; Bridwell also reports larvae feeding on their sibling larvae, but indicates that he has observed no maternal behavior toward larval progeny. Reports of host feeding have been made for some Bethylidae of the genus Goniozus. Many species of Goniozus malaxate their hosts but do not host feed (G. Gordh, personal observation). The account by Ranaweera (1950) leaves little doubt that host feeding was observed in a wasp he called G. montanus, and numerous reports of host feeding by G. nephatidis make it unlikely that the phenomenon does not occur in that species (Rao & Cherian, 1928; Jayaratnam, 1941).

Formicoidea are regarded as among the most highly evolved Hymenoptera, in part because they display sociality. Sociality combined with predatory habits can represent a quantum leap above the impact expressed by conventional predation. Predation by ants is expressed in most subfamilies of ants. Hrlldobler and Wilson (1990) summarized the genera of ants involved in prey specialization. Specialized prey include arthropod eggs, centipedes, millipedes, apterygotes, termites, beetles, moth larvae, and other Hymenoptera. Some ants are generalist perdators. As a consequence of interspecific fights, some species of ants carry other species of ants (enemies) back to the nest to be used as food for the colony. In other ants the predator-prey relationship is more intimate and cannibalism occurs (Driessen et al., 1984). Ants are behaviorally and biologically complex, and they express predatory behavior in many ways. Adaptations for predatory behavior are more apparent in ants than in other insects. Ants possess a sting that provides an effective weapon for the injection of offensive chemicals that neutralize prey. Mandibles are well-adapted structures that can be used to dismember prey. Behavior in ants is complex and workers frequently cooperate in the retrieval of prey. The importance of ants in biological control is often

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complex and sometimes contradictory (Way, 1992). To accurately assess the impact of ants in biological control, we must correctly identify the ants involved. Next, we must determine whether the ant species is endemic, adventive, or introduced. We must also determine whether the ant apecies is herbivorous, predaceous, or omnivorous. Finally, we must determine whether the ant is operating under natural or applied biological control. Ants apparently exert significant natural biological control in some forest habitats (Finnegan, 1974). Some of the general attributes that contribute to the effectiveness of ants as predators includes long-term colony existence, long hunting seasons, large populations of workers in a colony, large areas covered by workers, elaborate behaviors involving worker recruitment, and nonspecificity with regard to prey life stage. Red wood ants of the Formica rufa group include 8 species in Europe and 15 species in North America. In Europe, red wood ants have been noted as effective in the control of forest pests (G6sswald, 1951; Ruppertshofen, 1955). The usefulness of red wood ants is not universally accepted and some reservations have been expressed concerning their efficacy in forested habitats (Adlung, 1966). Inaccurate taxonomic identifications have contributed to the failure to appreciate the role of some species in the F. rufa group (Finnegan, 1971). Three species (Formica lugubris Zetterstedt, F. polyctena [F6rster], and F. aquilonia Yarrow) are effective in Europe. One species, F. lugubris, was successfully imported into Canada from Italy for control of forest pests in Quebec (Finnegan, 1975). Another species, F. obscuripes Forel, was successfully moved from Manitoba to Quebec (Finnegan, 1977). The overall effectiveness of these insects in Canada remains to be established, but introduction and exclusion studies of F. neoclara (Emery) in pear orchards showed the importance of this ant as a predator of pear psylla (Paulson & Akre, 1992a, 1992b). Formica yessensis Forrel has been demonstrated to be an important natural enemy of the pine caterpillar Dendrolimus spectabilis Butler in Korea (Kim & Kim, 1973; Kim & Choi, 1976; Kim & Murakami, 1978), and the potential of Formica species as predators of gypsy moth has been evaluated in the United States (Weseloh, 1996). Ants are not universally recognized as effective applied biological control agents in orchards, forests, and ornamental trees. Haney (1988) provides a world survey of the role of ants in citrus pest management. The citrus ant, Oecophylla smaragdina (Fabricius), is an effective predator for the control of insect pests. Huang and Yang (1987) document the use of citrus ants in China and note that the earliest written record of their application dates from 304 A.D. Leston (1973) discusses the use of citrus ants on other crops outside China. Oecophylla smaragdina is a so-called weaver ant, a species that bind leaves and twigs together with silk (H611dobler & Wilson, 1977). The ants inhabit their arboreal nests during the night and feed on insects on

the tree during the day. Ants colonize adjacent trees with the aid of bamboo bridges placed between the canopies of the trees by farmers. The effectiveness of these ants in the control of pests such as soft scales and mealybugs has been questioned (Groff & Howard, 1924; Hoffman, 1936; Chen, 1962). However, improved cultural practices and fostering of other natural enemies improve the effectiveness of O. smaragdina in the control of orchard pests (Yang, 1982, 1984; Yang et al., 1983, 1984; Dejean, 1991). The negative effect of pesticides on the action of O. smaragdina on citrus in China has been observed (Chen, 1985), and the elimination of chemicals in orchards further improves the effectiveness of O. smaragdina. Studies also indicate the potential of O. smaragdina in the control of Helopeltis pernicialis Stonedahl, Malipatil and Houston, a new pest of cashew in Australia (Peng et al., 1997). Other species of predatory ants may also exert a positive or negative impact on applied biological control of tree pests. The Argentine ant, Iridomyrmex humilis (Mayr), has been observed to remove 98% of the eggs of the chrysopid Chrysoperla carnea that were placed in street trees to control the tulip tree aphid Illinoia liriodendri (Dreistadt et al., 1986). In contrast, foraging F. hemorrohoidalis Emery ants were believed to kill 95% of the pupae of western spruce budworm, Choristoneura occidentalis Freeman, in north central Washington (Campbell & Torgersen, 1982), but carpenter ants are of limited importance as predators against spruce budworm in northwest Ontario (Sanders & Pang, 1992). Ants may act as predators of pests in annual field crops. Some studies in the United States show that the red imported fire ant, Solenopsis invicta, attacks pests of cotton including cotton fleahopper (Breene et al., 1990), boll weevil (Sterling et al., 1984), and tobacco budworm (McDaniel & Sterling, 1982; Nuessly & Sterling, 1994). This ant is an introduced predator from South America that is currently widespread in the cotton-growing region of the southeastern United States. While S. invicta may be beneficial for some pests of cotton (Breene, 1991), it may not be suitable against aphids on cotton because the ant protects aphids from other predators (Showier & Reagan, 1987), takes honeydew from aphids, and is predaceous on aphids that have been parasitized (Vinson & Scarborough, 1991). The red imported fire ant is also regarded as a significant predator of the sugarcane borer, Diatraea saccharalis, in Louisiana (Reagan et al., 1972, Ali & Reagan, 1985) and of the fall armyworm in sweet sorghum (Fuller et al., 1997). In general, this species of ant is regarded as highly noxious and millions of dollars a year are spent on its control in the United States. Kirk (1981) noted that Lasius neoniger Emery may be an effective predator of corn rootworm larvae (Diabrotica spp.) in South Dakota. A few studies in tropical regions show the potential for ants as biological control agents. Way et al. (1989) found that a complex of ant species in Sri Lanka contribute to the

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Terrestrial Arthropod Predators of Insect and Mite Pests

control of coconut caterpillar, Opisina arenosella Walker, through egg predation, and Lrhr (1992) correlated decrease of coreid bug damage to coconuts with an increase in ants. Eskafi and Kolbe (1990) note that S. geminata (Fabricius) can eliminate up to 25% of the medfly larvae, Ceratitis capitata (Wiedemann), falling from coffee and citrus in Guatemala. Wong et al. (1984) show that Iridomyrmex humilis serves a similar role in controlling medfly larvae, pupae, and teneral adults in Hawaii. Perfecto (1991) provides data that suggest S. geminata and Pheidole radowszkoskii Mayr may be helpful in the control of fall armyworm Spodoptera frugiperda, feeding on corn grown in Nicaragua. Endemic ants in Ghana can reduce the effectiveness of an introduced parasitoid of the cassava mealybug (Cudjoe et al., 1993).

Pompiloidea are considered by some taxonomists as transitional between sphecoids and scolioids. All three superfamilies are fossorial and are active burrowers. The superfamily includes the Pompilidae and Rhopalosomatidae. The Rhopalosomatidae are sometimes placed in the Scolioidea, but are considered within the Pompiloidea here. The Rhopalosomatidae are parasitoids of Gryllidae, but little is known of their biology (Gurney, 1953). The larva apparently forms a thalacium on the lateral aspect of the abdomen of crickets. Pompilidae are biologically distinctive in that the larvae all use spiders as food. The female wasp stings a spider and transports it to the nest. The adult female provisions a cell with one spider. After the nest has been provisioned, the female uses the apex of the gaster to tamp earth or mud over the entrance. Some Dipogon, Priocnemis, and Ageniellini construct the cell before hunting. This is probably a derived condition. Most female pompilids prepare the nest after the spider has been located and paralyzed, while other aculeates prepare the nest before searching for hosts. Predation, if it may be regarded as such, is restricted to adult pompilids. Williams (1956) reports that species of Pepsis feed on hemolymph of spiders that have been paralyzed and subsequently will be used as hosts for larval development. Concurrent feeding may be common in pompilids. Scolioidea consists of several families, including Mutillidae, Sapygidae, Scoliidae, Sierolomorphidae, and Tiphiidae. Predation among adult Mutillidae does not occur. Gregarious parasitism is unusual by Mutillidae larvae because they are voracious, and consume all available food. Presumably cannibalism, a form of predation, occurs in Mutillidae when more than one mutillid larva attempts to develop on a host (Brothers, 1984). Sapygids are all parasitic on other aculeate Hymenoptera; we know of no records of predation. Scoliids are exclusively solitary parasitoids of Coleoptera larvae. We know nothing of the biology of Sierolomorphidae. Tiphiidae adults are fossorial wasps and the larvae develop as parasitoids of some families of

459

Coleoptera, usually Scarabaeidae, Tenebrionidae, and Cicindelidae or sometimes Curculionidae. One genus, Diamma, attacks mole crickets. Tiphiids are also regarded as parasitic.

Sphecoidea includes the Sphecidae, which is recognized here in the sense of Bohart and Menke (1976) containing 11 subfamilies of solitary wasps that provision their nests with other insects and are considered beneficial. Prey specificity is not at the subfamily level, but is more at the tribal level. Feeding habits represent a continuum ranging from predation to parasitism. The larger sphecids, like Ampulicinae that capture cockroaches and Sphecinae that capture spiders or Orthoptera, are actually external parasitoids because they completely develop feeding on a single victim, while the sphecids that provision each cell with several small prey are indeed predators. Pemphredoninae insects provision their nests with Homoptera or, in a few cases, with Thysanoptera or Collembola. Astatinae provides Hemiptera for its larvae. In Larrinae, the tribe Larrini provisions nests chiefly with crickets and the tribe Tachytini, chiefly with grasshoppers. Crabroninae provides flies as prey. Nyssoninae is a large subfamily with six tribes, each having their own prey spectra but mostly Homoptera (chiefly leafhoppers) and flies. However, Sphecius speciosus (Drury), in the tribe Gorytini, is the cicada killer whose larvae are external parasitoids of cicadas, while other nyssonines are cleptoparasitoids of other sphecids. Philanthinae is ground nesting and provides aculeate Hymenoptera or Coleoptera as prey (Evans & Eberhard, 1970; Bohart & Menke, 1976). The best known Philanthinae are the bee wolves. Philanthus spp. provision their larvae with bees and wasps; thus, they are not beneficial but have a fascinating foraging behavior (Evans & O'Neil, 1988). In an intensive field study of several British pemphredonine species in the genus Passaloecus that provision their nests with aphids, Corbet and Backhouse (1975) concluded that solitary aculeates would not make good biological control agents for use in British field crops. These wasps have several disadvantages that preclude them from being effective natural enemies: they require high temperatures to be active, and have a slow numerical response to changes in prey density due to low fecundity and long generation time coupled with the emigration time from infested crops to their nests; finding and developing suitable nesting sites also require time and energy. Perhaps these disadvantages extend to all predaceous solitary aculeates. Corbet and Backhouse (1975), however, suggest possible use of pemphredonids in greenhouses. Vespoidea is considered to have only the family Vespidae, which comprises some 30 genera, seven tribes, and six subfamilies: Euparaguinae, Masarinae, Eumeninae, Stenogastrinae, Vespinae, and Polistinae (Carpenter, 1982). The primitive subfamilies Masarinae and Eumeninae

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are solitary; the former store pollen and nectar as food for their larvae and the latter provide their larvae with paralyzed or dismembered arthropods. The Stenogastrinae are subsocial because a feedball (evidently produced in the gut of the female) is placed in the cell before the egg hatches and later the larva is fed progressively with masticated insects and spiders. The other subfamilies are social wasps and their larvae are fed masticated arthropods and often also nectar (Evans & Eberhard, 1970; Ross & Matthews, 1991). Among the social vespoid wasps, the Polistinae subfamily has received the most attention by biological control workers--Polistes has been the main genus involved. Most of the more than 150 Polistes spp. known live in the tropics and are mainly caterpillar hunters (Evans & Eberhard, 1970; Reeve, 1991). Polistes spp. adapt to using man-made structures to build their paper nests that allows relocation, higher density, and protection from spraying of pesticides. Rabb and Lawson (1957) found foraging of Polistes spp. in North Carolina to be influenced by caterpillar abundance in tobacco and soybean fields and the number of natural nesting sites. Fewer hornworms were killed in tobacco fields when there was an abundance of green clover worms in soybean fields. By erecting wooden structure shelters around tobacco fields, P. annularis (Linnaeus) were induced to nest in the shelters, and these wasps reduced hornworms 60% although they had no effect on tobacco budworms (Lawson et al., 1961). Rabb et al. (1976) and Gillaspy (1979) concluded from their own attempts and those in the literature that increasing Polistes numbers to control lepidopteran larvae was not practical. Gould and Jeanne (1984) obtained mixed results in the control of Pieris rapae (Linnaeus) infesting cabbage plants by transplanting P. fuscatus (Fabricius) colonies in wooden nesting boxes. An average nest of 5.6 wasps was sufficient to reduce Pieris populations by up to five larvae (44%) on each of approximately 210 cabbage plants per season, while the availability of alternate prey influenced the degree of control of a target pest (Gould & Jeanne, 1984). Morimoto (1960) obtained increased predation of Pieris larvae in cabbage fields where he placed artificial nests for Polistes. In the temperate zone, nesting sites placed in sun-warmed sites will encourage larger and faster developed broods (Jeanne & Morgan, 1992). By placing P. antennalis Perez nests in cotton fields at the rate of 100 wasps per mu (0.67 ha), Li et al. (1984) obtained effective control of noctuid larvae. In the tropics the jackspaniard wasp, Polistes cinctus cinctus Lepeletier [in literature, P. annularis (Linnaeus), P. canadensis (Linnaeus)] was highly regarded on St. Vincent Island because it allowed cotton to be grown without pesticides, while in other Caribbean islands there were great losses to the cotton leaf worm Alabama argillacea (Hiibner) and this led to the exportation of P. c. cinctus to many of the Caribbean islands. Also on St. Vincent, the farmers

erected sheds in the fields for the wasp to nest in (Myers, 1931). The jackspaniard wasp also readily utilized the arrowroot leaf roller as an alternate host on St. Vincent Island (Cock, 1985). In Brazil and Peru, even though two Polistes spp. are not deliberately manipulated for biological control of the coffee leaf miner, Perileucoptera coffeella (GuerinMeneville), they are recognized as important predators of this pest (Enriquez et al., 1976; Reis & Souza, 1996). In Brazil, Parra et al. (1977) and Tozatti and Gravena (1988) have reported that predation by vespids can control outbreaks of the coffee leaf miner. The Indians in Amazonia, who grow 10 different crops without pesticides in cleared areas of 2 to 4 ha in the forest, owe much of the insect pest control to 10 different social wasps, including four Polistes spp. that nest in forest edges (Raw, 1988). The large New World tropical genus Mischocyttarus has species with biologies similar to Polistes (Gadagkar, 1991) and workers have investigated the foraging behavior of M. flavitarsus (Saussere) in greenhouses (Cornelius, 1991). Even though considered a generalist predator, this wasp species was deterred by aposomatic prey species (Bernays, 1988). This genus is manipulatable and has a wide prey range, making it a good potential as an augmentable biological control agent.

CONCLUSIONS The broad ecological role of predation has been discussed by Huffaker (1970); and the potential of predators in pest control has been presented by Hagen et al. (1976a), Luff (1983), and Wratten (1987). The current review of the major taxa of arthropod predators makes it clear that there are a variety of examples in which predators play a decisive role in the dynamics of phytophagous arthropod populations, through importation, augmentation, or natural control. The introduction of the vedalia beetle into southern California against the cottony-cushion scale in 1888 provides the earliest and most spectacular example of the potential of using predators for the classical biological control of newly invading pests. Numerous other examples have been documented in the earlier sections of this chapter. The historical record indicates that while predators have been used far less frequently than parasitoids for the classical biological control of arthropod pests, their overall rates of establishment and success are equal to those of parasitoids (Hall & Ehler, 1979; Hall et al., 1980), and, in fact, they may perform better than parasitoids in field crops and on plantations (Hokkanen, 1985). Predators used in the classical biological control of arthropod pests have in most cases been specialists; there is little justification for the importation of more polyphagous predators. Preadapted guilds of polyphagous predators are indigenous to most regions of the world and their introduction to other target areas can

Chapter 16 Terrestrial Arthropod Predators of Insect and Mite Pests

only be justified in the absence of such guilds, such as depauperate island faunas or where indigenous predators fail to adapt successfully to exotic target crops. In both cases, such importations should be considered with the utmost caution and specialist predators should be used whenever possible. Predator augmentation dates back as far as 1916, when a commercial insectary was initiated for the rearing of Cryptolaemus montrouzieri for inoculative seasonal control of mealybugs in the citrus orchards of southern California (Hagen, 1974). Since then, many different predators have been successfully augmented for the control of pests in protected cropping (Hussey & Scopes, 1985), but there remain few examples of successful field augmentation. Augmentation of the predaceous mite Phytoseiulus persimilis has been widely adopted for the control of the twospotted mite in California and Florida strawberry fields (Grossman, 1989; Decou, 1994). This example illustrates the potential for increased integration of field augmentation of predators into pest management strategies in the future, particularly in row crops, but also highlights the necessity to place greater emphasis on the development of improved economically viable rearing techniques. As we move from an era of introduced pests to one of indigenous pests through the successful implementation of classical biological control and quarantine restrictions, augmentation is likely to become a more frequently practiced form of biological control (Mills, 1991; Parrella et al., 1992). Gilliatt (1935) was one of the first to appreciate the role of insect predators in the natural control of potential pests in a study of the European red mite in apple orchards in Nova Scotia. This work led to the development of the concept of integrated pest management (Pickett, 1959; Stern et al., 1959) and the wider acceptance of the importance of generalist, as well as specialist, predators as a major factor in the prevention of pest outbreaks (Luff, 1983; Whitcomb & Godfrey, 1991; Riechert, 1992). More than 1000 species of arthropods have been documented from alfalfa fields in California (Smith & van den Bosch, 1967) and over 1000 predaceous arthropods, in soybean fields in Florida (Whitcomb, 1974). The conservation of this tremendous diversity of predators in field crops is one of the most important challenges for the future and for the development of sustainable agriculture. However, we need a far greater understanding of how microclimate, plant spacing, alternative food sources, and integrated controls affect not only the abundance of predators in field crops but also their impact on potential pests, before conservation will achieve the degree of success seen with other strategies of biological control.

Acknowledgment The assistance of Robert Zuparko during the final draft preparation of this chapter is gratefully acknowledged.

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Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

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Chapter 16

Terrestrial Arthropod Predators of Insect and Mite Pests

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Zeleny, J. (1984). Chrysopid occurrence in west palearctic temperate forests and derived biotypes. In M. Canard et al. (Eds.) Biology of chrysopidae (pp. 151-160). The Hague: Dr. W. Junk. Zhao, D. X., Boivin, G., & Stewart, R. K. (1990). Consumption of carrot weevil. Listronotus oregonensis (Coleoptera: Curculionidae) by four species of carabids on host plants in the laboratory. Entomophaga, 35, 57-60. Zhavoronkova, T. N. (1969). Certain structural peculiarities of the Carabidae (Coleoptera) in relation to their feeding habits. Entomological Review, 48, 462-471. Zheng, Y., Hagen, K. S., Daane, K. M., & Mittler, T. E. (1993a). Influence of larval dietary supply on food consumption, food utilization efficiency, growth and development of the lacewing Chrysoperla carnea. Entomologia Experimentalis et Applicata, 67, 1-7. Zheng, Y., Daane, K. M., Hagen, K. S., & Mittler, T. E. (1993b). Influence of larval food consumption on fecundity of the lacewing, Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). Entomologia Experimentalis et Applicata, 67, 9-14. Zhou, W., & Wang, R. (1989). Rearing of Orius sauteri (Hem.: Anthocoridae) with natural and artificial diets. Chinese Journal of Biological Control 5, 9-12 (in Chinese). Zhou, W., Wang, R., & Qiu, S. (1991a). Use of soybean sprouts as the oviposition material in mass rearing of Orius sauteri (Het.: Anthocoridae). Chinese Journal of Biological Control, 7, 7-9 (in Chinese with English summary). Zhou, W., Wang, R., & Qui, S. (1991b). Field studies on survival of Chrysoperla sinica (Neu.: Chrysopidae) mass reared and inoculatively released in wheat fields in northern China. Chinese Journal of Biological Control, 7, 97-100. Zhou, W., Liu, Z., Cheng, W., & Qui, S. (1981). Study on cultivation of adult Chrysopa sinica with powder artificial diet. Acta Phytopathologica Sinica, 7, 2-3. Zimmerman, E. C. (1948). Insects of Hawaii: Vol. 3, Heteroptera. Honolulu: University of Hawaii Press. Zondag, R., & Nuttall, M. J. (1989). Pineus laevis Maskell, pine twig chermes or pine woolly aphid (Hemiptera: Adelgidae). In A review of invertebrate pests and weeds in New Zealand 1874 to 1987. CIBC Technical Communications, 10, 295- 297. Zuniga, E. (1985). Eighty years of biological control in Chile. Historical review and evaluation of projects undertaken (1903-1983). Agricultural Technology, 45, 175-183. Zuniga, E. (1990). Biological control of cereal aphids in the southern core of South America, In R. K. Campbell & R. D. Eikenbary (Eds.), Aphid-plant interactions (pp. 362-367). Amsterdam: Elsevier Science.

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[171 Arthropods and Vertebrates in Biological Control of Plants T. S. BELLOWS

D. H. HEADRICK

Department of Entomology University of California Riverside, California

Crop Science Department California Polytechnic State University San Luis Obispo, California

INTRODUCTION

of biological control of weeds with invertebrates thus involves three broad fields of endeavor: research into plant biology and ecology, herbivore biology and ecology, and herbivore-plant interactions. In this volume there are two additional chapters that address biological control of weedy plants. Chapter 34 reviews programs against both aquatic and terrestrial weeds from a programmatic viewpoint. Chapter 35 reviews the use of plant pathogens as agents against weedy plants. This chapter reviews the use of invertebrates and vertebrates in plant biological control programs and discusses the taxa that have been used in these programs. We touch briefly on ecological attributes of biological control agents, and review procedures for ensuring the ecological safety of candidate natural enemies.

Biological control of plants using insect and other metazoan herbivores has a long history of research and application throughout the world. Some of the world's worst weed pests, both terrestrial and aquatic, have been controlled biologically with herbivores. In many of these cases, biological control has been the only possible option, for example, in cases where weeds become naturalized over millions of hectares of native grasslands or colonize natural waterways. Although cultural and chemical control cannot address the presence of a huge, self-reproducing population over vast areas, the use of natural control agents has often proved beneficial and effective. In the context of "use" of herbivorous insects, mites, nematodes, and vertebrates, we are almost exclusively concerned with the introduction of a herbivore to control either an adventive or a native plant pest. In such work, herbivores become candidate "agents" for use against a particular target weed. As this field has developed, the majority of cases have involved the discovery and release of herbivores into the environment to become naturally reproducing populations; the use of large numbers of mass-reared individuals, as is sometimes done with parasitoids or predators against other insect pests, has found only very limited application in the control of weeds. Thus, we are concerned here with the ecological context of introducing new herbivore species (through the usual channels of strict quarantine and evaluation, see Chapters 5 and 6) into environments as permanent members of the new community, with the aim that their presence will reduce the damage caused by a weedy plant. In most cases, the target weed will be adventive, or introduced, into the target environment. The work

Handbookof BiologicalControl

EFFECTS OF HERBIVORY O N WEEDY PLANTS Herbivory is widely common among invertebrates, and most plants have a number of herbivores, both generalists and in some cases specialists, feeding on them (Strong et al., 1984). Plants are, quite clearly, capable of sustaining considerable herbivory without undue damage to their own survival and reproduction. How is it, then, that herbivorous insects can cause sufficient change in plant population dynamics that they can control a plant population? Biological control of plants differs in some important ways from control of invertebrate pests or pathogens. While predation and parasitism of invertebrate pests are direct causes of mortality in the target population, plant death rarely occurs from the attack of a single or a few herbivores. In contrast, a variety of mechanisms are involved in

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T.S. Bellows and D. H. Headrick

the interactions between invertebrate herbivores and the plants that they feed on. Together these processes can lead to the demise of a plant population; even when in isolation, they do not cause the death of individual plants. The effects of herbivorous arthropods on plants occur at two levels: changes in the growth and reproduction of individual plants, and changes in the dynamics of the target plant population. In a great deal of literature the effects of herbivory on individual plants have been explored, but the quantitative impact of herbivores on plant populations has been reported in very few studies (Crawley, 1989). In terms of practical biological control, the matters of interest are the overall impact of herbivores on the dynamics of plant populations. Nonetheless, an appreciation of the component effects on individual plants sheds important light on the ecological interplay between plants and their herbivores. We will consider here how five different impacts of herbivores on plants can lead to plant population suppression and control.

R e d u c e d R e p r o d u c t i o n or R e c r u i t m e n t to t h e Plant Population Seed- and flower-feeding insects are often used in introduction programs against weedy plants. Herbivory of the reproductive structures can reduce fruit and seed set, and can in some cases reduce recruitment to the seedling stage of the populations. However, the relationship between seed production and seedling recruitment is often not linear. While seed production might be limiting for some plant populations, for many plant populations, including annual, biennial, and long-lived woody species, seed production vastly outmatches seedling recruitment. Sites for seedling establishment are often the resource that limits this stage of population growth (Andersen, 1989). In ecological context, this is a situation where the impact of mortality in one stage (the seed) is reduced in significance if a mortality or resource limiting a subsequent stage (seedling establishment) is density dependent. The presence of a limited number of seedling establishment sites acts as a density-dependent buffer once the seed supply exceeds the supply of favorable germination sites. Nonetheless, seedling recruitment of some plant species has been reduced by the introduction of seed- or flowerfeeding insects. Seed production of the tree Sesbania punicea (Cavanille) Bentham was reduced by 98% following the introduction of the apionid Trichapon lativentre (Bequin Billecocq) (Hoffman & Moran, 1992). The addition of the weevil Rhyssomatus marginatus F~hraeus further destroyed 84% of the produced seeds, and the two agents together arrested nearly completely the reproduction of the weed (Hoffman & Moran, 1992). An in-depth discussion of

the significance of seed-attacking insects is given by Neser & Kluge (1986).

Direct Mortality of Plants Herbivorous arthropods may occasionally kill their host plants directly. Plant death in such cases is usually caused either by consumption of whole plants, often by an unusually large population of herbivores, or by extensive disruption of plant physiological systems such as water transport. Plant death can also occur through repeated defoliation accompanied by destruction of plant carbohydrate reserves (preventing regrowth). In other cases, effects of herbivory act together with additional agents or environmental stresses to cause plant death indirectly.

Indirect Mortality of Plants Herbivory can reduce existing plant biomass or cause redirection of resources in plant tissues through many mechanisms (including defoliation, removal of plant sap, destruction of roots, and galling of plant tissues). Such herbivory often leads to reduction in stored reserves in a plant, and reduces the rate of plant growth or regrowth in the presence of herbivory. The relationship between injury from herbivores and individual plant performance (such as total seed set or growth rate) is often linear (Crawley, 1989). At moderate levels of herbivory, however, many plants are able to compensate partially or fully for losses (Trumble et al., 1993), so the relationship between the proportion of plants actually dying and the amount of herbivorous injury may be nonlinear, and is governed by a damage threshold (Harris, 1986). This threshold is the level or amount of biomass that must be removed before the plants cannot compensate and consequently incur an increased risk of death. Many species of forage grasses, for example, remain healthy with annual losses to herbivory of 40% of their biomass, but when herbivory removes more than 50%, grass stands decline (Harris, 1986). Plant response to herbivory varies not only with the amount of biomass consumed or removed, but also with the season in which herbivory takes place. In addition, plant response will vary with the specific tissues that are attacked; particularly when the tissues attacked are also those used by the plant for storage of carbohydrate reserves. For plant species in which reserves are stored in foliage, defoliation is much more likely to result in plant death than for species in which storage occurs in other structures, such as the cambium or roots. Seasonal timing of herbivory also is important in determining the outcome of plant-herbivore interactions. Defoliation of musk thistle, Carduus thoermeri Weinmann, at the rosette stage caused mortality, but similar

Chapter 17 Arthropodsand Vertebrates in BiologicalControl of Plants levels of defoliation after development of the fruiting stalk had little effect on the plants (Cartwright & Kok, 1990). Galling of plant tissues has its greatest effect when tissues are attacked early in development (Harris, 1986). The plant reacts as if the resources used for gall formation had been used for normal tissue growth and little compensatory growth takes place. Extensive galling can act as a nutrient sink, reducing other vegetative growth and, if galling occurs in the reproductive tissues, reducing reproduction (Dennell, 1988). Interactions with O t h e r Stresses Because herbivory is fundamentally a loss of biomass or nutrients to a plant, the degree of herbivory that a plant can stand is often a function of what other factors are present, timing of the herbivory, and environmental conditions affecting the plant.

Multiple Herbivores A series of introduced herbivores that either act sequentially through the year, or that attack different plant tissues, can be valuable in suppressing plant growth and reproduction. In parts of Hawaii, for example, control of Lantana camara Linnaeus was achieved by the introduction of both a tingid (Teleonomia scrupulosa Sthl) that annually defoliated the plants and additional agents that attacked the plant during the winter months (Andres & Goeden, 1971). Seed production of S. punicea in South Africa was virtually eliminated by the combined action of two seed-feeding insects (Hoffman & Moran, 1992). Tansy ragwort (Senecio jacobaea Linnaeus) in the northwestern United States was controlled by the complimentary actions of two herbivores, cinnabar moth [Tyria jacobaeae (Linnaeus)] and a flea beetle [Longitarsus jacobaeae (Waterhouse)] (McEvoy et al., 1990).

Abiotic Stress Defoliated plants tend to respond to injury by regrowth, drawing on stored reserves of carbohydrates and other nutrients. New foliage is then used by the plant to rebuild carbohydrate reserves. Plants that have used stored reserves for regrowth can be more vulnerable to abiotic stresses, such as winter cold or summer drought, until reserves have been restored. If a defoliation-refoliation cycle occurs shortly before periods of drought or other stress, the impact of this environmental stress on the plant can be more severe than would ordinarily occur. Defoliation of tansy ragwort by the cinnabar moth reduces root reserves and makes the plants more susceptible to death caused by frost (Harris et al., 1978).

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Plant Disease Herbivory may increase plant susceptibility to disease. Limb death in Mimosa pigra Linnaeus in Australia, caused by the pathogen Botryodiplodia theobromae Patouillard, was apparently stimulated by a stem-boring moth introduced against this weed (Wilson & Pitkethley, 1992).

Plant Competition In nearly every community, plants compete for resources: light, water, nutrients, germination sites, or canopy growth space. Grasses are important competitors of the rangeland weed Centaurea maculosa Lamark, reducing survival of rosettes by 83% over control sites lacking grasses (Mtiller-Sch~irer, 1991). The competitive ability of wheat against the weed Amsinckia intermedia von Fischer and Meyer was sharply increased in the presence of the flower gall nematode Anguina amsinckiae (Steiner & Scott) Thorne. The ability of weeds to compensate for herbivory by increased growth is greatest when competition is absent and when nutrients and water are not limiting. As plant competition increases, weeds are less able to regrow following attack by herbivores. Competition may act over time such that areas left bare by weed plant death, if quickly filled by other more desirable plants, are not available as sites favorable for germination and establishment of weed seedlings.

TAXA USED IN BIOLOGICAL CONTROL Julien (1992) has provided a world catalog of agents imported and released in various countries for control of adventive weedy plants. Some 259 species of invertebrates have been employed, predominantly insects (254 species) and some mites (5 species). Releases of these species have resulted in establishment at one or more locations for 62% (161) of the species used. Control (at least partial, including cases in which the agent was part of the complex of herbivores that eventually resulted in control) of the target weed was achieved in at least one location by 65 species (25% of all species released). A large number of families and species have been employed, and a summary of their taxonomic groupings is presented in Tables 1 and 2. Care should be taken in interpreting the information in these tables as definitive concerning the relative merits of any particular group, because this table is only a historical record and not a test of hypotheses relating to the suitability of one or more natural-enemy groups. Included in Julien's (1992) review and in these tables are many species whose releases are relatively recent and still under evaluation. The taxa employed in such programs include insects,

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T.S. Bellows and D. H. Headrick TABLE 1

A Summary of Invertebrates Intentionally M o v e d b e t w e e n Countries for Biological Control of Adventive W e e d s

Order

No. of families employed

No. of species employed

Establishments (no. of species)

Successes (no. of species)

Coleoptera Lepidoptera Hemiptera Diptera Thysanoptera Hymenoptera Orthoptera Acarina Fungi Nematodes Overall

7 21 8 6 2 3 1 3 4 1 56

109 82 19 35 4 4 1 5 8 1 268

66 (61%) 46 (56%) 15 (79%) 25 (71%) 2 (50%) 3 (75 %) 1 (100%) 3 (60%) 8 (100%) 1 (100%) 170 (63%)

33 (30%) 15 (18%) 8 (42%) 4 (11%) 1 (25%) 2 (50%) 0 (0%) 2 (40%) 5 (63%) 0 (0%) 70 (26%)

Data from Julien, M. H. (Ed.) (1992). Biological control of weeds: A world catalogue of agents and their target weeds. Wallingford, United Kingdom: CAB International.

mites, nematodes, fish, and pathogens (see Chapter 35 for pathogens used in weed biological control). Among these taxa, which groups of herbivores emerge as important for weed control depends in large part on which plant species become pests, and which groups feed on those plants. For these reasons, the number of families or species recognized as important may increase with time if additional weeds become targets of such programs.

Invertebrates From the historical record, we note that of 65 species of herbivorous insects and mites that have provided control of their target weeds, 40 are included in six families of insects: three families of Coleoptera; two, of Lepidoptera; and one, of Homoptera. These include Chrysomelidae (12 species), Curculionidae (14), Cerambycidae (4), Pyralidae (3), Arctiidae (3), and Dactylopidae (4). Relatively few generalities about the biologies of these groups are possible at the family level because within most families of insects diverse biologies are exhibited by member species. Broader descriptions of herbivorous insect families are given by Arnett (1968), Borror et al. (1989), and CSIRO (1970). Insectplant interactions are discussed by Strong et al. (1984). Van Driesche and Bellows (1996) provide a slightly fuller overview of the biologies of the major families of herbivores used in biological control.

Coleoptera Chrysomelidae Members of this family feed on foliage and flowers as adults. Larvae feed on foliage, are leaf miners, or are stem

or root borers. Some 39 species of chrysomelids have been used for biological control and 12 have successfully controlled their target pests in at least one location. Agasicles hygrophila Selman and Vogt has been used successfully in Australia and other countries (Julien, 1981) for aquatic forms of alligator weed, Alternanthera philoxeroides (Martius) Grisebach, a plant native to South America. The beetle is multivoltine with as many as five generations per year in Argentina, and adults lay an average of more than 1100 eggs during their 7-week adult life span (Clausen, 1978). The terrestrial weed S. jacobaea was controlled by two herbivores, one of which was the chrysomelid L. jaco-

baeae. Curculionidae Larvae of this family either feed externally on foliage, or feed internally in fruits or stems. Of 36 species of curculionids that have been used in biological control programs, 14 have provided control of their target weeds. These include the weevil Rhinocyllus conicus (Fr61ich), which controlled nodding thistle, (Carduus nutans Linnaeus) in Canada (Harris, 1984); Neohydronomus affinis Hustache, which control water lettuce (Pistia stratiotes Linnaeus) in several locations including Florida (Dray et al., 1990); and Microlarinus lypriformis (Wollaston), which contributed to partial controlled of puncture vine (Tribulus terrestris Linnaeus) in the southwestern United States and Hawaii (Huffaker et al., 1983).

Cerambycidae and Buprestidae Larvae of these families typically bore in the stems of woody plants. Adults often feed on flowers. Seventeen species of cerambycids or buprestids have been used in biolog-

Chapter 17 TABLE 2

Arthropods and Vertebrates in Biological Control of Plants

509

A S u m m a r y of t h e Historical Record of M o v e m e n t of G r o u p s of I n v e r t e b r a t e s a n d Fungi b e t w e e n C o u n t r i e s for Control of A d v e n t i v e W e e d s

Order

No. of species employed

Establishments (no. of species)

Successes (no. of species)

Coleoptera Chrysomelidae Curculionidae Cerambycidae Apionidae Bruchidae Buprestidae Anthribidae Lepidoptera Pyralidae Noctuidae Tortricidae Gelechiidae Arctiidae Gracillariidae Pterophoridae Lyonetidae Cochylidae Geometridae Sesiidae Aegeriidae Coleophoridae Oecophoridae Pterolonchidae Carposinidae Heliodinidae Sphingidae Lycaenidae Dioptidae Hepialidae Hemiptera Dactylopiidae Tingidae Coreidae Pseudococcidae Miridae Aphidae Psyllidae Delphacidae Diptera Tephritidae Cecidomyiidae Agromyzidae Anthomyiidae Ephydridae Syrphidae Thysanoptera Phlaeothripidae Thripidae Hymenoptera Tenthredinidae Eurytomidae Pteromalidae Orthoptera Pauliniidae

109 39 36 14 9 7 3 1 82 23 10 9 5 4 4 3 3 3 3 3 2 2 1 1 1 1 1 1 1 1 19 6 5 3 1 1 1 1 1 35 17 6 5 4 2 1 4 3 1 4 2 1 1 1 1

66 (61%) 21 24 9 3 6 3 0 46 (56%) 11 4 5 3 3 3 3 2 2 2 1 0 2 1 0 1 1 1 1 0 0 15 (79%) 5 3 2 1 1 1 1 1 25 (71%) 11 5 4 3 2 0 2 (50%) 2 0 3 (75%) 1 1 1 1 (100%) 1

33 (30%) 12 14 4 1 2 1 0 15 (18%) 3 1 2 0 3 1 2 1 0 0 0 0 0 0 0 1 1 0 0 0 0 8 (42%) 4 1 1 1 0 0 1 0 4 (11%) 2 1 1 0 0 0 1 (25%) 1 0 2 (50%) 0 1 1 0 (0%) 0

(continues)

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T.S. Bellows and D. H. Headrick TABLE 2 Order

Acarina Eriophyidae Tetranychidae Galumnidae Fungi Uredinales Hyphomycetes Ustilaginales Coelomycetes Nematodes Anguinidae Overall

No. of species employed

5 3 1 1 8 5 1 1 1 1 1 56

(continued) Establishments (no. of species)

3 (60%) 2 1 0 8 (100%) 5 1 1 1 1 (100%) 1 268

Successes (no. of species)

2 (40%) 1 1 0 5 (63%) 3 0 1 1 0 (0%) 0 170 (63%)

After Van Driesche, R. G., & Bellows, T. S. (1996). Biological control. New York: Chapman & Hall; data from Julien, M. H. (Ed.). (1992). Biological control of weeds: A world catalogue of agents and target weeds. Wallingford, United Kingdom: CAB International.

ical control projects and four have provided some control of their target weed species. Bruchidae

The larvae of this family typically develop inside seeds, especially of legumes. While seven species of bruchids have been employed in biological control projects and some have caused dramatic reduction of seeds and seedlings, in only one case has this herbivory resulted in suppression of the target weed. In South Africa, two species of seedfeeding bruchids are important in biological control of Prosopis spp., a plant that has some desirable characteristics but has become an invasive weed. By limiting seed production through biological agents, the plant can be preserved but its reproduction severely restricted, reducing its invasiveness and pest status (Zimmerman, 1991).

Lepidoptera

Pyralidae

Species in this third largest lepidopteran family are usually small, with the adults appearing as small, delicate moths with a scaled proboscis. Larval feeding habits are quite varied and species may be foliage feeders, borers, or feeders on stored products, including beeswax. One of the most famous members of this family in the history of biological control is the Phycitinae species Cactoblastis cactorum (Bergroth), which successfully controlled prickly pear cacti (Opuntia spp.) in Australia. Of 23 pyralid species employed in biological control, three have suppressed their target weeds.

Noctuidae

This is the largest family in the Lepidoptera. The adults are heavy-bodied, night-flying moths; the larvae are usually smooth bodied and dull in color. Most feed on foliage, but some are stem borers or feed on fruits. Of the 10 species employed as biological control agents one has controlled its target weed. Tortricidae

This is one of the largest families of microlepidoptera. The larvae are foliage feeders, most often of perennial plants. They may tie or roll leaves and often bore into plant parts. Of the nine species employed in biological control, two have controlled their target weeds. Arctiidae

This is a moderate-sized family with four rather distinct subfamilies (the Pericopinae, Lithosiinae, Arctiinae, and Ctenuchinae), which are given family status by some authors. Subfamily Arctiinae, or tiger moths, comprise most of the species in the family. Of the four species that have been used as biological control agents, three have successfully suppressed their target weeds. Tyria jacobaeae was responsible in part for control of tansy ragwort, S. jacobaea, in Oregon (McEvoy et al., 1990). Gracillariidae

Members of this family are minute moths whose larvae are leaf miners. Mines are typically blotch in form and the leaf is often folded. Many mines may occur per leaf. Pupation often takes place in the mine or on the surface of the mined leaf. One of the four species employed for biological control suppressed its host.

Chapter 17 Arthropodsand Vertebrates in BiologicalControl of Plants

Hemiptera Dactylopiidae These insects resemble mealybugs (Pseudococcidae) in appearance and habits. Dactylopiids feed on cacti and while the number of species in the family is not large, the family has played an important role in successful biological control of several species of cacti. Four of the six species used have provided control of their target cacti (Goeden et al., 1967).

Tingidae Nymphs and adults feed together on the same host plant by sucking plant fluids from leaves and other tissues, causing the foliage to become bronzed; and, when bug densities are high, plants die. Some species are relatively specific in their choice of host plants, which may be either herbaceous or woody species. One species, Teleonemia scrupulosa, played an important role in the control of lantana (Lantana camara), a woody ornamental of great importance as a pasture pest in tropical areas around the world (Julien, 1992).

Coreidae Most coreids are phytophagous. Some species feed on seeds and others on foliage. Some species have enlarged hind tibia or femurs. Many species produce noticeable odors. One of the three species employed in biological control has controlled its host plant.

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and are found in most habitats. Of the five species employed for biological control, one has been successful.

Thysanoptera Phlaeothripidae Some species in this family are herbivorous. Of the three species employed for biological control, one has suppressed its target weed. Liothrips urichi Karmy controlled Clidemia hirta (Linnaeus) in some habitats in Fiji (Rao, 1971).

Hymenoptera Tenthredinidae This is the most common group of sawflies, and most species are small or moderate in size. The larvae are external feeders on foliage. Typically there is one generation a year. Most species feed on woody shrubs or trees. A few species are gall makers or leaf miners. Of the two species that have been employed, neither has been successful.

Eurytomidae These are minute, darkly-colored wasps. They vary in their biologies. Some species are parasitic, while others feed in seeds or make galls. The single species of this family that has been employed for biological control suppressed its target weed.

Pteromalidae

Diptera Cecidomyiidae These are small delicate flies with long legs and long antennae. About two-thirds of known species form galls and most of the remaining species feed on decaying vegetation. Galls are formed on all parts of plants, including buds, leaves, flowers, and stems. One of the six species employed for biological control has been proved successful.

Tephritidae The members of this family are small to medium-sized flies, usually with patterned wings. Larvae feed inside plant tissues, tunneling in seed heads, forming galls, or feeding in fruits. A few species are leaf miners. Seventeen species have been used in biological control projects, mainly species that feed in seed heads of thistles, knapweeds, and other plants, or species that form galls. Establishment has occurred in a substantial proportion of cases. Two species have successfully controlled their target weeds.

Agromyzidae The larvae of most species of Agromyzidae are leaf miners. Species in the family attack a wide range of plants

The Pteromalidae comprise a diverse group of Hymenoptera, which includes some gall formers. One of these, Trichilogaster acaciaelongifoliae Froggat, has been important in the biological control of Acacia longifolia (Andrews) Willdenow in South Africa (Dennill & Donnelly, 1991). The wasp is univoltine, and females oviposit in floral buds of the target plant, leading to galling of these tissues. Extensive attack can occur, and attacked buds do not produce inflorescences or seeds. Attack by the wasp has resulted in 30% mortality of adult trees in some locations. The final impact of this wasp is still under evaluation, but the insect appears promising as a control agent of A. longi-

folia.

Acarina Eriophyidae These are extremely small mites (about 0.15 mm in length) that feed on plant tissues. Some species cause galls, while others feed externally on plant tissues and thereby discolor fruits or other plant parts. The potential biological control uses of the family are reviewed by Gerson and Smiley (1990), who note that eriophyids, while slow acting, are often highly host specific. Of the three

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species that have been employed for biological control, one has suppressed its target weed.

Tetranychidae Spider mites, which are larger than eriophyids, feed on plant foliage but do not cause galls; many species produce visible webbing. Gerson and Smiley (1990) summarize past biological control uses of the family, which have been extremely limited. The only target weed against which a spider mite (Tetranychus lintearius Dufour) has been deliberately introduced has been gorse (Ulex europaeus Linnaeus) in New Zealand (Hill et al., 1991), and evaluation of this program is continuing. Nematodes

A number of plant-parasitic nematodes in the Tylenchina, especially the family Anguinidae, induce galls on plant foliage. The taxonomy of this group is reviewed by Siddiqi (1986). Some nematodes in this group are resistant to dehydration, a feature that enhances their survival. A number of species in the group have been considered for use in biological control through augmentation (Parker, 1991). One species has been introduced against an adventive plant (Julien, 1992). Vertebrates A variety of domestic animals such as goats, sheep, and geese are used to some degree for terrestrial weed control; such uses are usually in the context of cultural regimes, where intensive foraging is used to reduce unwanted vegetation, including weedy species. In the case of aquatic weeds, fish have been used to reduce and manage intermittent or perennial weed problems. A total of 11 fish species have been introduced into various countries to suppress aquatic vegetation (Julien, 1992). These occur in three families, Cyprinidae (which include various carp species), Cichlidae, and Osphronemidae (Table 3). All these species are generalist herbivores that suppress whole communities of aquatic macrophytes. As such, these species are limited in their application to enclosed water bodies, such as irrigation ditches or ponds, where total or near total weed suppression is desired; and the fish population can be contained, thus avoiding introduction of nonnative fish to waterways and other natural breeding grounds of native fish. The potential for such fish to affect natural systems, including both macrophytic and native fish communities, is high. Each introduction must be considered carefully, taking into account the potential for subsequent spread to other water bodies by flood or casual relocation by people. In some instances sterile hybrids or sterile triploids are used to minimize the risk of establishing breeding

TABLE 3 Species of Fish Introduced into O n e or More Countries for the Control of Aquatic Plants Cyprinidae Aristichthys nobilis (Richardson) (big head) Ctenopharyngodon idella (Cuvier & Valenciennes) (grass carp, white amur) Hypophthalmichthys molitrix (Cuvier & Valenciennes) (silver carp) Puntius javanicus (Bleeker) Cichlidae Oreochromis aureus (Steinbachner) O. mossambicus (Peters) O. niloticus (Linnaeus) Tilapia macrochir (Boulenger) T. melanopleura Dumeril T. zillii (Gervais) Osphronemidae Osphronemus goramy Lacepedes (giant gourami) Data from Julien, M. H. (Ed.). (1992). Biological control of weeds: A world catalogue of agents and their target weeds. Wallingford, United Kingdom: CAB International.

populations of introduced fish (Anderson, 1993; Van Driesche & Bellows, 1996).

ATrRIBUTES AND SAFETY OF CONTROL AGENTS The desirable attributes of weed biological control agents vary depending on the ecological situation into which the agents are placed. Our awareness of this diversity of desirable attributes has matured over the nearly 100 years that such work has taken place. While it is tempting to point to past programs and to analyze the suitability of agents in the light of today's ecological understandings, such critiques are less useful than might be surmised, because decisions made early in the development of this science might not be made in similar situations today. Instead, we turn to current, conservative practice in the conduct of biological control programs to define attributes desirable among natural enemies of weedy plants. Candidate natural enemies, when introduced into a new environment, face the usual challenges of colonizing that environment, securing resources for growth and development, locating mates, reproducing, and surviving seasonal weather patterns and attack by extant natural enemies. Having accomplished this, they are expected to disperse in the environment (preferably throughout the adventive range of the weed), persist, reproduce, and reduce the population density of the weed to a noneconomic status. In most cases, it is also desirable that in their new environment the herbivore has little or no impact on any nontarget species of plant. Weed biological control agents are sought to be eco-

Chapter 17 Arthropodsand Vertebrates in Biological Control of Plants logically widely benign to nontarget plants, while being sufficiently damaging to the target plant to be effective in controlling it. While at first this may seem a daunting prospect, in many cases the ecological setting of the target weed permits considerable flexibility in achieving these goals. For example, weeds may be taxonomically isolated in their new environment. In such settings, weed-feeding agents that might feed on a few related plants in their native home would, if introduced into the weed's new adventive range, find themselves with only a single host-plant species present in this new range. In such circumstances, these agents are highly specific to the target, because their other normal hosts are lacking. In other cases, adventive weeds may be related to extant plants in the new environment. In these cases, more work may be involved in finding herbivores sufficiently selective that their impact on native vegetation will be at acceptably low levels.

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and Harley and Forno (1992) discuss interpreting the results of host-specificity trials. Wapshere (1989) formalized an important and informative "reverse-order" testing procedure for evaluating host range of herbivores (Fig. 1). By reasoning that host-plant use by insects must involve two steps, both acceptance by the adult for oviposition and suitability for immature development, Wapshere (1989) proposed that host-range testing should start with forced feeding trials of immature stages of the candidate herbivore. Plants on which the immatures can successfully develop to fertile adults are then possible candidates for inclusion in the host range of the herbivore. These plants are further tested by isolating adults of the herbivore with them, and by determining whether oviposition occurs. If either larval maturation fails, or if adults refuse to oviposit on the plant species, then it is extremely

HERBIVORE HOST RANGE TESTING Host Specificity Issues concerning host specificity are always situation specific. Generalizations are not possible, because the setting in which each weedy plant is addressed will be unique. Nonetheless, we find throughout the work of plant biological control a generally high degree of conservatism concerning what natural enemies are released into an environment, with emphasis placed on herbivores sufficiently specific that risk of impact to nontarget species is minimized. By and large, this work has been successful in avoiding widespread nontarget impacts, and only in rare cases have nontarget impacts been recorded as significant (Van Driesche & Bellows, 1996). Clearly defining host specificity, as it might be realized in a natural setting, is a difficult undertaking, in part because laboratory research will rarely mimic field behavior of any particular herbivore. The best solution for evaluating the potential host range of a candidate natural enemy is to study it in detail in its native home, defining its ecologically realized host range, and determining the impact it has both on the target weed and on nontarget plants (Clement & Sobhian, 1991; Baudoin et al., 1993). When such work is not possible, then weed biological control agents are evaluated in special quarantine facilities, where their biology and host range can be tested against both target and nontarget plants, prior to any planned release into the environment. While evaluating the results of laboratory trials is difficult because the behavior of many herbivores is modified by confinement, it is usually the most conservative assessment of herbivore impact. When a candidate herbivore is shown not to feed on non-target plants in forced settings in the laboratory, there is a high likelihood that it will not feed on them in natural settings. Wapshere (1989)

Test I: I

Larval Feeding Test

(Under close confinement, I no choice setting)

I

Continue testing i (Under clo~B confinement, Test Ih I Adult Oviposition Test #1 I no choice setting)

|

Continue testing Test II1: I Adult Oviposition Test #2 1 (under field conditions or loose confinement, multiple choice setting)

|

|

FIGURE 1 "Reverse-order"testing sequence for estimating host ranges of herbivorous arthropods. [After Wapshere, A. J. (1989). Comparing methods of selecting effective biocontrol agents for weeds (pp. 557-560). In Anonymous, Proceedings of the First International Weed Control Congress, Melbourne, Australia.]

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unlikely that in natural settings the plant would ever be utilized in any significant way. If both larval development and oviposition in confinement take place, an additional adult oviposition test is conducted under field conditions or loose confinement with multiple species of plants. In some cases, an insect will oviposit on a plant in close confinement that it does not oviposit on when offered the same plant with other plant species (Buckingham et al., 1989; Thompson & Habeck, 1989; Wilson & Garcia, 1992). If the adult does locate and oviposit on the plant species in this mixed-species setting, the plant is likely to be in the ecological host range of this herbivore. If the plant is avoided or ignored in this "choice" test, then it likely is not in the herbivore's host range in natural settings. Once estimates of the host range have been made for a particular candidate herbivore, the degree of host specificity required for a particular situation must also be determined. While few herbivores are monophagous on a single plant species, many are oligophagous, feeding on only a few related species of plants. Such oligophagous agents may be judged suitable for a program if they do not attack any vital economic or native plants, or when it is clear that their impact on native and economic plants will be minimal. Polyphagous herbivores are not usually employed in biological control programs, but may be successful in some cases where the target weed is the only plant in the agent's host range present in the new environment. One setting in which polyphagous herbivores are used is in contained waterways, such as irrigation canals, where control of macrophytic aquatic weeds is affected by herbivorous fish. O t h e r Attributes While the degree of host specificity is a vital and often primary focus of the evaluation of candidate herbivores, several other features of herbivore ecology are likely important in the success of any particular agent. In reviewing biological programs against weedy plants, it has not been possible to identify specific characteristics that are closely correlated with success or establishment. However, some features of herbivore biology are more common among successful agents. Of all the released insect species that have resulted in successful establishment, in 60% of the cases species where both the immature stages and the adults damage the host have been involved; in 37%, organisms where only the immature stages damage the plant have been involved; and in 3%, insects where only the adult damages the plant have been involved. Hence, a close association between the plant and the entire life cycle appears to be a common feature of herbivores established against weed pests. Mobility and dispersal capabilities are clearly important in expanding an herbivore's geographic range to become coincident with the weed's range. Not all stages need be

motile, however, because there are examples of biological control agents that have successfully established, dispersed, and controlled weeds that have had sessile stages. Some degree of seasonal synchrony between the herbivore and the target weed is necessary, and diapause cues, if obligatory, must be present for such synchrony to be effective. Ecological similarity between the target region and the area of origin of the herbivore often can help ensure that such climatic and seasonal parameters will not be limiting. Finally, we often see introduced herbivores become attacked by existing parasites or predators; thus, the reproductive potential of the herbivore in its new home must be sufficient for it to overcome natural mortality factors to become an effective control agent. Additional characteristics have been proposed as likely to be important to a successful weed-feeding agent. A good agent should not be self-limiting, but should be tolerant of high densities of its own species so that it will be able to become sufficiently dense to damage its host. Species that are limited in their country of origin by natural enemies (parasitoids, predators, diseases) may be very effective in a new region provided that the natural enemies can be eliminated during the introduction process and that there are not species in the new location likely to take their place. A candidate agent should complement existing stresses placed on the weed by other herbivores in the system (unless it is expected to replace an existing, but ineffective agent). Thus, weed biological control programs often consider herbivores that feed on different portions of the plants as complementary to one another.

AGENT SELECTION Agent selection is both art and science, and requires a certain degree of synthesis of both agent biology and target plant biology. It has not been possible to accurately predict which agents, of any potential list of candidate species, comprise the set of herbivores that will provide control of a target weed (Van Driesche & Bellows, 1996). However, because of the intense scrutiny such agents undergo, it is often possible to place candidate agents into such categories as "possible" or "unlikely"; and because of the high costs of evaluating and screening potential agents, such sifting or sorting is highly desirable. Where possible, the clearest and simplest way of selecting herbivores is to use species that have controlled the target weed in other countries with similar climates. Thus, the use of Cyrtobagous salviniae Calders and Sands to control Salvinia molesta D.S. Mitchell in South Africa was an obvious choice following its successful use earlier in Australia and Papua New Guinea against this weed (Thomas & Room, 1986; Cilliers, 1991). In the absence of a prior program to draw from, there are three approaches to agent preliminary selection or

Chapter 17

Arthropods and Vertebrates in Biological Control of Plants

screening (Wapshere, 1992). These include studies in the weed's native range to identify herbivores having the greatest impact there (while making appropriate allowance for parasitoids and other factors that might be different in the new target area for the agent) (Wapshere, 1974). A second method is to study the historical record of past projects (Julien, 1992) and to identify agents or features of successful agents that have been used against related weeds. Finally, in the absence of direct information, agents might be scored based on possession of particular attributes they (or their plant hosts) possess that seem, based on theoretical considerations, to be important for successful biological control (Harris, 1973; Goeden, 1983). Caution must always be employed in such cases, however, because biological performance of herbivores can be both unexpected and unexplainable based on preliminary, laboratory, or solely theoretical considerations. While such concepts cannot comprise a detailed guide to selecting agents, these concepts, together with the biological attributes discussed earlier, may serve as a foundation for sorting agents into at least priority rankings for evaluation. The number of organisms that are obtained for evaluation as biological control agents against weeds is always greater than the number finally released, and these are greater than the number that become established. The filter of quarantine is a crucial part of this work, and the conservative approach that has been the standard of this science, to only release herbivores after careful scrutiny and review, has served widely to protect our environments from herbivores with undesirable attributes, while allowing effective control of weeds that had previously devastated natural and agronomic systems. The use of invertebrates and vertebrates as effective control agents has been and will continue to be a crucial component of our efforts to manage invasive and noxious weeds. References Andersen, A. N. (1989). How important is seed predation to recruitment in stable populations of long-lied perennials? Oecologia (Berlin), 81, 310-315. Anderson, L. W. J. (1993). Progress and promise in management of aquatic-site vegetation using biological and biotechological approaches. In R. D. Lumsden & J. L. Vaughn (Eds.), Pest management: Biologically based technologies (pp. 241-249). Washington, DC: American Chemical Society. Andres, L. A., & Goeden, R. D. (1971). The biological control of weeds by introduced natural enemies. In C. B. Huffaker (Ed.), Biological Control (pp. 143-164). New York: Plenum Press. Arnett, R. H. (1968). The beetles of the United States (a manual for identification). Ann Arbor, MI: American Entomological Institute. Baudoin, A. B. A. M., Abad, R. G., Kok, L. T., & Bruckart, W. L. (1993). Field evaluation of Puccinia carduorum for biological control of musk thistle. Biological Control, 3, 53-60. Borror, D. J., Triplehorn, C. A., & Johnson, N. F. (1989). An Introduction to the Study of Insects (6th ed.). Philadelphia: Saunders College. Buckingham, G. R., Okrah, E. A., & Thomas, M. C. (1989). Laboratory

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host range tests with Hydrellia pakistanae (Diptera: Ephydridae), an agent for biological control of Hydrilla verticillata (Hydrocharitaceae). Environmental Entomology, 18, 164-171. Cartwright, B., & Kok, L. T. (1990). Feeding by Cassida rubiginosa (Coleoptera: Chrysomelidae) and the effects of defoliation on growth of musk thistles. Journal of Entomological Science, 25, 538-547. Cilliers, C. J. (1991). Biolgical control of water fern, Salvina molesta (Salviniaceae), in South Africa. Agriculture, Ecosystems and Environment, 37, 219- 224. Clausen, C. P. (Ed.). (1978). Introduced parasites and predators of arthropod pests and weeds: A world review. Agricultural Handbook No. 480. Washington, DC: U.S. Department of Agriculture. Clement, S. L., & Sobhian, R. (1991). Host-use patterns of capitulum feeding insects of yellow starthistle: Results from a garden plot in Greece. Environmental Entomology, 20, 724-730. Crawley, M. J. (1989). Insect herbivores and plant population dynamics. Annual Review of Entomology, 34, 531-564. CSIRO. (1970). [Corporate author]. The insects of Australia. A textbook for students and research workers. Carlton, Victoria: Melbourne University Press. Dennill, G. B., & Donnelly, D. (1991). Biological control of Acacia longifolia and related weed species (Fabaceae) in South Africa. Agriculture, Ecosystems and Environment, 37, 115-135. Dennill, G. B. (1988). Why a gall former can be a good biocontrol agent: The gall wasp Trichilogaster acaciaelongifoliae and the weed Acacia longifolia. Ecological Entomology, 13, 1-9. Dray, F. A., Jr., Center, T. D., Habeck, D. H., Thompson, C. R., Cofrancesco, A. F., & Balciunas, J. K. (1990). Release and establishment in the southeastern United States of Neohydronomus affinis (Coleoptera: Curculionidae), an herbivore of water lettuce. Environmental Entomology, 19, 799-802. Gerson, U., & Smiley, R. L. (1990). Acarine biocontrol agents, an illustrated key and manual. New York: Chapman & Hall. Goeden, R. D., Fleshner, C. A., & Ricker, D. (1967). Biological control of prockly pear cacti on Santa Cruz Island, California. Hilgardia, 38, 579-606. Goeden, R. D. (1983). Critique and revision of Harris' scoring system for selection of insect agents in biological control of weeds. Protection Ecology, 5, 287- 301. Harley, K. L. S., & Forno, I. W. (1992). Biological control of weeds, a handbook for practitioners and students. Melbourne, Australia: Inkata Press. Harris, P. (1973). The selection of effective agents for the biological control of weeds. Canadian Entomologist, 105, 1495-1503. Harris, P. (1986). Biological control of weeds. In Franz, J. M. (Ed.), Biological plant and health protection, biological control of plant pests and of vectors of human and animal diseases (pp. 123-138). International symposium of the Akademie der Wissenschaften und der Literatur, Mainz, November 15-17, 1984, Mainz and Darmstadt, Germany. Harris, P. (1984). Carduus nutans L., nodding thistle and C. acanthoides L., plumeless thistle (Compositae). In J. S. Kelleher & M. A. Hulme (Eds.). Biological control programmes against insects and weeds in Canada 1969-1980 (pp. 115-126). London: CAB International. Harris, P., Wilkinson, A. T. S., Thompson, L. S., & Neary, M. (1978). Interaction between the cinnabar moth, Tyria jacobaeae L. (Lep.: Arctiidae) and ragwort Senecio jacobaea L. (Compositiae) in Canada (pp. 174-180). In Anonymous, Proceedings, Fourth International Symposium on Biological Control of Weeds, Gainesville, FL. Hill, R. L., Gindell, J. M., Winks, C. J., Sheat, J. J., & Hayes, L. M. (1991). Establishment of gorse spider mite as a control agent for gorse (pp. 31-34). Proceedings of the 44th New Zealand Weed and Pest Control Conference. Wellington, N.Z. Hoffmann, J. H., & Moran, V. C. (1992). Oviposition patterns and the supplementary role of a seed-feeding weevil, Rhyssomatus marginatus (Coleoptera: Curculionidae), in the biological control of a perennial

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leguminous weed, Sesbania punicea. Bulletin of Entomological Research, 82, 343-347. Huffaker, C. B., Hamai, J., & Nowierski, R. M. (1983). Biological conrol of puncturevine, Tribulus terrestris, in California after twenty years of activity of introduced weevils. Entomophaga, 28, 387-400. Julien, M. H. (1981). Control of aquatic Alternanthera philoxeroides in Australia; another success for Agasicles hygrophila (pp. 583-588). Proceedings of the Fifth International Symposium on Biological Control of Weeds. Julien, M. H. (Ed.). (1992). Biological control of weeds: A world catalogue of agents and their target weeds. Wallingford, United Kingdom: CAB International. McEvoy, P. B., Cox, C. S., James, R. R., & Rudd, N. T. (1990). Ecological mechanisms underlying successful biological weed control: Field experiments with ragweed Senecio jacobaea (pp. 55-66). In Delfosse E. (Ed.), Proceedings of the Seventh International Symposium on Biological Control of Weeds, Rome, Italy. Miiller-Scharer, H. (1991). The impact of root herbivory as a function of plant density and competition: Survival, growth and fecundity of Centaurea maculosa in field plots. Journal of Applied Ecology, 28, 759776. Neser, S., & Kluge, R. L. (1986). The importance of seed-attacking agents in the biological control of invasive alien plants. In I. A. Macdonald, W., F. J. Kruger, & A. A. Ferrar (Eds.), The Ecology and Management of Biological Invasions in Southern Africa (pp. 285-293). Cape Town, South Africa: Oxford University Press. Parker, P. E. (1991). Nematodes as biological control agents of weeds. In D. O. TeBeest, (Ed.), Microbial control of weeds (pp. 58-68). New York: Chapman & Hall. Rao, U. P. (1971). Biological control of pests in Fiji (Miscellaneous Publication 2). Slough, U.K.: Commonwealth Institute of Biological Control. Siddiqi, M. R. (1986). Tylenchida parasites of plants and insects. Slough, United Kingdom: CAB International, Commonwealth Institute of Parasitology.

Strong, D. R., Lawton, J. H., & Southwood, T. R. E. (1984). Insects on plants: Community patterns and mechanisms. Cambridge, MA: Harvard University Press. Thomas, P. A., & Room, P. M. (1986). Taxonomy and control of Salvinia molesta. Nature (London), 320, 581-584. Thompson, C. R., & Habeck, D. H. (1989). Host specificity and biology of the weevil Neohydronomus affiinis [Coleoptera: Curculionidae] a biological control agent of Pistia stratiotes. Entomophaga, 34, 299306. Trumble, J. T., Kolodny-Hirsch, D. M., & Ting, I. P. (1993). Plant compensation for arthropod herbivory. Annual Review of Entomology, 38, 93-119. Van Driesche, R. G., & Bellows, T. S. (1996). Biological control. New York: Chapman & Hall. Wapshere, A. J. (1974). Towards a science of biological control of weeds (pp. 3-12). In Anonymous, Proceedings of the Third International Symposium on Biological Control of Weeds, Montpellier, France, 1973. Wapshere, A. J. (1989). A testing sequence for reducing the rejection of potential biological control agents for weeds. Annals of Applied Biology, 114, 515-526. Wapshere, A. J. (1992). Comparing methods of selecting effective biocontrol agents for weeds (pp. 557-560). In Anonymous, Proceedings of the First International Weed Control Congress, Melbourne, Australia: Wilson, B. W., & Garcia, C. A. (1992). Host specificity and biology of Heteropsylla spinulosa [Hom.: Psyllidae] introduced into Australia and Western Samoa for the biological control of Mimosa invisa. Entomophaga, 37, 293-299. Wilson, C. G., & Pitkethley, R. N. (1992). Botryodiplodia die-back of Mimosa pigra, a noxious weed in northern Australia. Plant Pathology, 41,777-779. Zimmermann, H. G. (1991). Biological control of mesquite, Prosopis spp. (Fabaceae), in South Africa. Agriculture, Ecosystems and Environment, 37, 175-186.

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[18[ A Perspective on Pathogens as Biological Control Agents for Insect Pests B. A. FEDERICi Department of Entomology University of California Riverside, California

ical agents and tactics into integrated pest management (IPM) programs. Like all other organisms, insects are susceptible to a variety of diseases caused by pathogens. Many of these pathogens cause diseases that are acute and fatal, and therefore can be important short-term regulators of insect populations. As a result, insect pathogens are currently the subject of a considerable research effort aimed at developing the most effective pathogens as biological control agents for insects. There has been interest in using pathogens to control insects for well over 100 years, and several are currently used quite successfully, but interest in their further development is now greater than ever due to the search for more environmentally friendly alternatives to chemical insecticides. The pathogens that cause disease in insects fall into four main groups: viruses, bacteria, fungi, and protozoa. In the present chapter, after a brief historical review and a preliminary description of strategies for using pathogens in control programs, each of these groups will be described in terms of the biological properties that determine their utility as agents for controlling insects. In addition to the pathogens, insect-parasitic nematodes will also be treated in this chapter because many of the same principles apply to the use of these organisms as biological control agents. A great deal has been written about the biology of insect pathogens and their use as control agents, including many excellent reviews, but few are actually used on a widespread basis as operational control agents. Thus, instead of reviewing this literature again, the intent is to summarize for nonspecialists (i.e., those outside the fields of insect pathology and microbial control) the key biological features of the major pathogens developed or considered for development as control agents and to provide a critical evaluation

INTRODUCTION Synthetic chemical insecticides have been the principal component of most insect control programs since the discovery of the insecticidal properties of DDT just prior to World War II. They continue to be used extensively due primarily to their high efficacy and relatively low cost, but also because most are easy to produce and use, are persistent, and have a broad spectrum of activity that includes many different types of insects. This combination of properties led to widespread and heavy use soon after discovery throughout the world to control agricultural insect pests and insect vectors of human and animal diseases. There can be little doubt that chemical insecticides have been of great value in reducing economic damage caused by insects and by the prevalence of many plant and animal diseases transmitted by insects. However, their extensive use has resulted in a variety of problems, the most important of which include the development of resistance in many pest populations, the elevation to major pest status of relatively minor insect pests resulting from increased use of insecticides to control resistant pests, the elimination of natural enemies and disruption of natural ecosystems, and the fear on the part of the public that continued use of chemical insecticides will further contaminate the environmentmparticu larly the food and water supplym with persistent and harmful chemicals. New chemical insecticides are much more expensive to develop, and this, plus pressures to reduce the use of chemicals in insect control programs, has led to increased emphasis on the development of alternatives control agents and strategies. These include biological control agents, cultural control (also referred to as environmental management), use of pheromones, increased development of insect-resistant plants, and better integration of nonchem-

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of why these agents are not more widely used in insect control. The emphasis will be on a description and an assessment of the attributes and limitations of the different pathogen types based on the numerous studies conducted in this field over the past three decades. The most appropriate uses for each type will be identified as well as the obstacles that must be overcome to have these agents used more widely in insect control. In addition, it will be shown how knowledge of the molecular biology of certain insect pathogens, particularly nuclear polyhedrosis viruses (NPVs) and Bacillus thuringiensis (B.t.), and the techniques of recombinant DNA technology are being employed to improve the insecticidal properties of these pathogens. References to the primary literature and reviews will be given where pertinent for those interested in a wider range of examples and more detailed information. The principal pathogens and nematodes that will be discussed in this chapter are listed in Table 1 along with references to more specialized articles.

als were important to the development of insect pathology and microbial control [see Cameron (1973)], the modern era of these two closely intertwined disciplines is due largely to the extraordinary vision, scholarship, and energy of Steinhaus. Steinhaus resurrected bacterium Bacillus thuringiensis Berliner as a potential control agent, and his studies along with those of Hannay (1953) and Angus (1954) were pivotal points in its ultimate commercialization and successful use as a microbial insecticide. In addition, through his early studies of the NPV of the alfalfa caterpillar, Colias eurytheme Boisduval, Steinhaus did much to focus attention on the potential of viruses as microbial insecticides. His studies of viral and bacterial diseases of insects and other pioneering efforts in the field of insect pathology reinvigorated studies of fungi and protozoa as control agents, and were important to the development of the international fields of insect pathology and microbial control as we know them today.

Historical B a c k g r o u n d

Current U s a g e in P e r s p e c t i v e

Serious interest in using pathogens to control insect pests can be traced back well over 100 years. According to Steinhaus (1975), several workers during the last century, including A. Bassi in Italy, V. Auduoin in France, and later J. LeConte in the United States and E. Metchnikoff in Russia, suggested that pathogens might prove to be effective agents for controlling crop pests. However, none of these early suggestions led to the successful use of pathogens to control insects. In the present century, renewed interest in using pathogens for insect control followed the successful use of other natural enemies such as predaceous beetles and parasitic wasps. Control of the cottony-cushion scale, Icerya purchasi Maskell, by the vedalia beetle, Rodolia cardinalis (Mulsant), in the United States led to the establishment of permanent research programs by governmental agencies in this and several other countries aimed at using natural enemies, including pathogens, as pest control agents (Paillot, 1933; Steinhaus, 1975). Two notable early successes emerged from these programs: the development of Bacillus popilliae Dutky as a control agent for the Japanese beetle, Popillia japonica Newman, in the United States (White & Dutky, 1942), and the use of the NPV of the European spruce sawfly, Gilpinia hercyniae (Hartig), as a classical biological control agent in Canada (Balch & Bird, 1944). As part of an expanded research effort in the United States, Professor Hma3, S. Smith at the University of California hired E. A. Steinhaus shortly after the end of World War II to develop pathogens of insects as biological control agents (Steinhaus, 1963, 1975). Steinhaus, who had been trained as a bacteriologist, was well aware of the success attained with Bacillus popilliae and the G. hercyniae NPV; and soon after his appointment he began research in earnest aimed at using insect pathogens, particularly bacteria and viruses, as control agents. Though certainly other individu-

Despite the rather extensive body of literature on insect pathogens and microbial control, only one pathogen, (B.t.), is used routinely in a variety of control programs and has proved to be a commercial success in industrialized countries. This is also the pathogen in which current interest concerning further development and use is the highest. Before discussing the different pathogen types, it is worthwhile to consider why this is so. Such an assessment identifies the key features required for a pathogen to be successful as an insect control agent. To do this requires a few definitions concerning the different ways in which pathogens are used or considered for use in insect control programs, and a preliminary view (to be expanded on later) of the performance expectations by which the potential of insect pathogens and their degree of success are evaluated. In general, the guiding principle here is one of economics; the pathogens that will be developed and used are those that are the most cost-effective, in either the short or long term. Though this may be obvious, it is all too often overlooked in much of the literature on the use of pathogens as control agents. The effectiveness of a control strategy based on an individual pathogen will always be compared with that obtained with other available control strategies, including those based on other pathogens and chemical insecticides. Also of importance, cost-effectiveness can vary with such important factors as crop, season, species complex to be controlled, geographic location, governmental regulations affecting registration and use, and status of economic development in the country where the pathogen is used. The latter two are particularly important because the costs of development and the use of a pathogen in developing countries, especially for viruses and fungi, are much less than in highly industrialized countries. This is because the costs of material and labor for production are low, many of

Chapter 18 TABLE 1

A Perspective on Pathogens as Biological Control Agents for Insect Pests

Principal Pathogens and N e m a t o d e s D e v e l o p e d or Considered for Use as Biological Control A g e n t s for Insect Pests and Vectors of Disease

Pathogen

Major targets

References ~

Viruses

Baculoviruses Nuclear polyhedrosis viruses

Granulosis viruses Nonoccluded (Oryctes virus)

Caterpillars, sawfly larvae

Caterpillars Scarab larvae

Federici, 1998 Granados & Federici, 1986 Adams & Bonami, 1991 Hunter-Fujita et al., 1998 Miller, 1997; Treacy, 1998 Tweeten et al., 1981 Bedford, 1981 Zelazny et al., 1992 Aruga & Tanada, 1971; Katigitri, 1981

Cytoplasmic polyhedrosis viruses

Caterpillars

Entomopoxviruses

Grasshoppers, scarab larvae

Granados, 1981; Arif, 1984

Iridoviruses

Mosquitoes

Anthony & Comps, 1991

Bacillus popilliae B. thuringiensis

Bacteria Scarab larvae Caterpillars

Mosquito and blackfly larvae

B. sphaericus

Bettle larvae Mosquito larvae

Klein, 1981; Klein, 1997 Navon, 1993 Baum et al., 1998 de Barjac & Sutherland, 1990; Becker & Margalit, 1993 Jenkins, 1998 Keller & Langenbruch, 1990 de Barjac & Sutherland, 1990 Baumann et al., 1991 Charles et al., 1996

Fungi

Mastigomycotina Coelomomyces species

Mosquito larvae

Lagenidium giganteum

Mosquito larvae

Federici, 1981; Couch & Bland, 1985 Federici, 1981

Aphids, caterpillars, beetles, grasshoppers

Wilding, 1981 Humber, 1989

Bettle larvae, caterpillars, grasshoppers Beetle larvae, leafhoppers, spittlebugs, cockroaches Aphids, whiteflies

McCoy et al., 1988 Wraight and Carruthers, 1998 McCoy et al., 1988

Zygomycotina Entomophthoraceous fungi Deuteromycotina Beauveria bassiana Metarhizium anisopliae Verticillium lecani

Nosema species Vairimorpha necatrix

Mermithids Steinernematids, Heterorhabditids

Microsporidia Grasshoppers, mosquito larvae, beetles Caterpillars

Nematodes Mosquito larvae Caterpillars, beetle larvae, mole crickets

Hall, 1981; Hall & Paperiok, 1982

Brooks, 1988; Henry, 1991 Maddox et al., 1981; Brooks, 1988

Petersen, 1982 Gaugler & Kaya, 1990 Kaya & Gaugler, 1993 Grewal and Georgis, 1998

a Review articles and books that provide extensive coverage of the biology, use, and control potential of pathogens and nematodes along with references to relevant primary literature. The textbook Insect Pathology by Tanada and Kaya (1993), and Manual of Techniques in Insect Pathology edited by Lacey (1997) also provide useful information and numerous references to the primary literature on insect pathogens and nematodes.

5| 9

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B . A . Federici

the farms are smaller and less mechanized, and the registration process is cheaper and less cumbersome. For these reasons, caution must be be exercised in drawing conclusions about the cost-effectiveness of a pathogen based on studies carried out in developing countries and then applying these results to prospective use in developed countries. Alternatively, experience gained from the greater use of pathogens in developing countries may provide valuable insights into how to integrate pathogens into IPM programs in developed countries. Nevertheless, though pathogens (especially viruses) are used more widely in developing countries such as China and India, even in these, usage is marginal in comparison to chemical insecticides. In most cropping systems, pest populations contain individuals infected with pathogens capable of causing both acute (e.g., nuclear polyhedrosis viruses) and chronic (e.g., microsporidia) diseases. The periodic spread of these pathogens throughout the pest population, especially when the population becomes large and economically important, often leads to devastating epizootics that reduce the pest population to below economic thresholds for years afterwards (Fuxa & Tanada, 1987). Typically, however, the pest population does not crash until there has been substantial economic damage. This point is well illustrated by the outbreaks and declines of many lepidopteran forest pests such as those of the gypsy moth, Lymantria dispar, and the spruce budworm, Choristoneura fumiferana. Because modeling of these epizootics is not sufficiently precise at present to predict accurately their occurrence and extent (Anderson, 1982), monitoring pathogens within the population is not considered a reliable method of using pathogens as control agents. Thus, programs aimed at using pathogens for pest control generally involve strategies in which pathogens are deliberately introduced against pest populations for shortor long-term control. In view of the preceding considerations, the most costeffective use of a pathogen, as with other biological control agents, is as a classical biological control agent (DeBach & Rosen, 1991). In such cases, introduction leads to largescale outbreaks of disease (epizootics) and establishment of the pathogen in the target population. Within a few years, the pest population is reduced below the economic threshold on a permanent basis. Unfortunately, though pathogens may establish and become endemic in a target population within a few years of introduction, there are very few examples where establishment has resulted in a classical biological control success. The best example in insects is the use of an NPV to control the European spruce sawfly in Canada, as noted earlier (Balch & Bird, 1944). Seasonal introduction is another way in which pathogens can be used. For this type of use, the pathogen is released into the pest population at the beginning of the season or early in the development of the pest population. The pathogen reduces the population below the economic threshold, but

typically only for one or a few seasons. The protozoan

Nosema locustae Canning has been used in such a strategy to reduce grasshopper populations over a period of several weeks (Henry, 1990). Again, however, this tactic has been of only limited utility. The most common strategy is to use pathogens as microbial insecticides, and because this strategy has been quite successful with bacteria and viruses, it will likely be of greater use in the future. In this case, a formulation of the pathogen is applied against a target pest on a periodic basis, as needed, much as in the case of chemical insecticides (Federici, 1991; Moscardi, 1999). Depending on the target pest, applications may often be fewer than those required with a chemical insecticide because the pathogens are quite specific and typically do not kill predatory and parasitic insects. Thus, these natural enemies remain in the ecosystem to slow the increase in the pest population after the initial mortality caused by the microbial insecticide. Moreover, the reproduction of the pathogen in the target insect, as in the cases of viruses, adds to the amount of the pathogen in the crop environment, and this can extend control and improve cost-effectiveness. In pests with only one or a few generations per season, a single application can yield effective season-long control where a combination of these factors is in operation. Another important issue affecting the use of pathogens is performance expectations. In most cases, a successful pathogen is one that can reduce the pest or vector population to below an economic or transmission threshold routinely and reliably at a cost that is economical in proportion to the value of the crop or impact of the disease. Clearly, pathogens that are effective as classical biological control agents, or on a seasonal introduction basis, would be the most cost-effective. However, few pathogens have been used successfully in these strategies. Often where there are claims of success, cost-effectiveness has not been clearly demonstrated. As a result, the efficacy of most pathogens is evaluated in terms of their utility as microbial insecticides. Since World War II, expectations for the efficacy of any control strategy have been very high, having been set largely by the performance of chemical insecticides. Traditionally, these have been fast-acting, broad-spectrum control agents with substantial residual activity that are relatively inexpensive, in addition to bring easy to produce, formulate, and use. Thus, under most circumstances pathogens are evaluated on the basis of how they compare with chemical insecticides, in particular, with how quickly they kill the target insect and what the cost is. This leads to what might be called the microbial control agent paradox--the advantages of microbial insecticides can also be disadvant a g e s m a paradox that is important because of its economic consequences. Ironically, it is now generally agreed that the two properties of many chemical insecticides originally considered their best attributes (i.e., a broad spectrum of

Chapter 18 A Perspective on Pathogens as Biological Control Agents for Insect Pests activity and significant residual activity) are actually detrimental. These properties are largely responsible for the destruction of natural-enemy populations and the development of insecticide resistance, and if such environmental costs are calculated, the cost-effectiveness of chemical insecticides is lower than calculated (Higley & Wintersteen, 1992). On the other hand, insect pathogens typically have a narrow spectrum of activity and relatively poor residual activity. Though these are now considered beneficial properties, they have discouraged interest by industry in the development of many potentially useful pathogens because of the relatively high costs of development and registration in comparison with the likely return on investment. This is a relative argument. The costs for development and registration of a microbial insecticide are actually much cheaper in developed countries than for a chemical insecticide (e.g., approximately a million dollars for a microbial compared with at least several million dollars for most chemicals in the United States, Europe, and Japan). This is because many pathogens with potential for development as microbial insecticides have already been identified. Nevertheless, a company still must see the potential for making its investment pay off within a few years. For many pathogens that are highly specific in their host range, this is simply not possible given the current regulatory environment and market size in most industrialized countries. Whether on a small or a large scale, industrial interest is extremely important because industry will be the source of pathogens to be used as microbial insecticides. This is particularly true in developed countries where the farms tend to be large. In fact, most farmers, whether large or small, want a reliable supply of control agents. Though they are willing to change cultural practices, because of numerous other responsibilities, farmers are generally unwilling to serve as the manufacturers of their own microbial insecticides. In light of the economics of pesticide development, it is easy to see why B.t. has been the most widely developed and used insect pathogen. In essence, it compares favorably with chemical insecticides in many crop and forest systems where lepidopterous insects are the key or major pests. It is fast acting; is relatively inexpensive; and is easy to produce, formulate, and use. Its residual activity is low, and none of the subspecies have a broad host range in comparison with most chemical insecticides. Yet the range of insects it controis provided, and continues to provide, a market large enough to justify commercial development. Overall, in most pest control situations the prospects for the use of pathogens is best where they will be used as microbial insecticides, to be used one or more times as needed during the pest season. Under these circumstances, the availability, reliability, and cost-effectiveness of microbial insecticides become paramount. These issues will be returned to again at the close of this chapter, but should be

52 |

kept in mind as the properties of the various pathogen groups and our ability to improve their efficacy are discussed.

VIRUSES All viruses are obligate intracellular parasites, and as such must be grown in living hosts. With insect viruses, this means either in insects (i.e., in vivo) or in cultured insect cells (in vitro); no methods exist for growing viruses on "artificial" media. Most of the viruses that occur in insects belong to one of the major taxonomic groups listed in Table 1. In general, these viruses are divided into two broad non-taxonomic categories, occluded viruses and nonoccluded viruses (Payne & Kelly, 1981; Tanada & Kaya, 1993; Hunter-Fujita et al., 1998). Occluded viruses are so named because after formation in infected cells, the mature virus particles (virions) are occluded within a protein matrix, forming paracrystalline bodies that are genetically referred to as either inclusion or occlusion bodies (Fig. 1). In nonoccluded viruses, the virions occur freely or occasionally form paracrystalline arrays of virions that are also known as inclusion bodies; these, however, have no occlusion body protein interspersed among the virions. More detailed information on the biological properties of insect viruses can be found in works by Adams and Bonami (1991), Tanada and Kaya (1993), and Miller (1997).

Biological Properties Related to Insect Control A short description of the most important biological properties is given here for the four most common virus types to set the stage for a more detailed discussion of occluded baculoviruses, which as a group have received the most attention as control agents.

Iridoviruses Iridoviruses are nonoccluded viruses with a linear double-stranded DNA genome that produce large, icosahedral virions (125 to 200 nm) that replicate in the cytoplasm of a wide range of tissues in infected hosts, causing disease that is generally fatal. Virions can form paracrystalline arrays in infected tissues, imparting an iridescent hue to infected hosts, from which the name of this virus group is derived. Over 30 types are known, and all have been extremely difficult to transmit per os. The host range of each type appears to be quite narrow based on natural occurrence in host field populations. Prevalence and mortality rates in natural populations of host insects are typically less than 1% (Kelly & Robertson,1973; Tanada & Kaya,1993).

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B.A. Federici

have been studied in any detail are generally easy to transmit p e r os to the original host and other species of the same order, and thus the host range of this virus type is probably the broadest among the insect viruses (Aruga & Tanada, 1971; Katagiri, 1981; Tanada & Kaya, 1993).

Entomopoxviruses Entomopoxviruses are occluded double-stranded DNA viruses that produce large virions (150 • 300 nm) that replicate in the cytoplasm of a wide range of tissues in most hosts, causing an acute fatal disease. Occlusion bodies, depending on the isolate, vary from being ovoidal to spindle shaped and generally occlude 100 or more virions. These viruses have been most commonly reported from coleopterous insects, from which there are over 20 isolates, but are also known from lepidopterous, dipterous (midges), and orthopterous (grasshoppers) insects. This virus type is easily transmitted p e r os, though the experimental host range of individual isolates, where tested, is relatively narrow, generally being restricted to closely related species (Granados, 1981; Arif, 1984).

Occluded Baculoviruses

FIGURE 1 Nuclear polyhedrosis virus polyhedra. (A) A wet mount preparation viewed with phase microscopy showing refractile polyhedra in two infected nuclei. (B) Electron micrograph through a single polyhedron showing the enveloped rod-shaped virions, characteristic of NPVs, occluded within the polyhedral matrix. On ingestion, this matrix dissolves in the insect midgut, and the virions invade the host via midgut microvilli.

Cytoplasmic Polyhedrosis Viruses Cytoplasmic polyhedrosis viruses (CPVs) are occluded double-stranded RNA viruses with a multipartite genome that replicate and form large (ca 0.5 to 2/xm) polyhedral to spherical occlusion bodies in the cytoplasm of midgut epithelial cells, causing a chronic disease. Infection in early instars retards growth and development, extending the larval phase by several weeks, and in many cases is ultimately fatal. This virus type is relatively common among lepidopterous insects and dipterous insects of the suborder Nematocera (e.g., mosquitoes, blackflies, midges). Isolates that

There are two types of occluded baculoviruses, NPVs and granulosis viruses (GVs). Both NPVs and GVs are highly infectious p e r os, and in some insect species these viruses cause widespread epizootics periodically that result in significant (>90%) declines in larval populations. NPVs are known from a wide range of insect orders as well as from Crustacea (shrimp), but by far have been most commonly reported from lepidopterous insects, from which well over a 500 isolates are known (Tanada & Kaya, 1993; Volkman et al., 1995). Many of these are different viruses (i.e., viral species). NPVs replicate in the nuclei of cells, generally causing an acute fatal disease (see Fig. 1). The virions are large (80 to 200 • 280 nm) and consist of one or more rod-shaped nucleocapsids with a double-stranded circular DNA genome enclosed in an envelope. The occlusion bodies of NPVs are referred to commonly as polyhedra because they are typically polyhedral in shape. Polyhedra are large (ca 0.5 to 2/xm), and form in the nuclei, where each occludes as many as several hundred virions. NPVs of lepidopterous insects infect a range of host tissues, but those of other orders are typically restricted to the midgut epithelium (Federici, 1993, 1997). Some NPVs have a very narrow host range, and may only replicate efficiently in a single species, whereas others, such as the AcMNPV [i.e., the NPV of the alfalfa looper, Autographa californica (Speyer)] have a relatively broad host range and are capable of infecting species from different genera (Granados & Federici, 1986; Blissard & Rohrmann, 1990). GVs, of which there are now over 100 isolates, are

Chapter 18

A Perspective on Pathogens as Biological Control Agents for Insect Pests

closely related to NPVs but differ from the latter in several important respects (Tweeten et al., 1981; Federici, 1997; Volkman et al., 1995). The virions of GVs are similar to those of NPVs but contain only one nucelocapsid per envelope. GVs are only known from lepidopterous insects. Like NPVs, they initially replicate in the cell nucleus, but replication involves early lysis of the nucleus (as virions begin to assemble), which in NPVs only occurs after most polyhedra have formed. After the nucleus lyses, GV replication continues throughout the cell, which now consists of a mixture of cytoplasm and nucleoplasm. When completely assembled, the virions are occluded individually in small (200 X 600 nm) occlusion bodies referred as granules. Many GVs primarily infect the fat body, whereas others have a broader tissue tropism and replicate throughout the epidermis, tracheal matrix, and fat body. One, the GV of the grape leaf skeletonizer, Harrisina brillians Barnes & McDonnough, is unusual in that it only replicates in the midgut epithelium (Federici & Stem, 1990). Use of Viruses as Insect Control A g e n t s The best example of the use of a virus as an insect control agent is the NPV of the European spruce sawfly, G. hercyniae, as a classical biological control agent to control this important forest pest (Balch & Bird, 1944; Cunningham & Entwistle, 1981). The European spruce sawfly was introduced into eastern Canada from northern Europe around the turn of the century and was a severe forest pest by the 1930s. Hymenopteran parasites were introduced from Europe in the mid-1930s as part of a biological control effort, and inadvertently along with these came the NPV, which was first detected in 1936. Natural epizootics caused by the virus began in 1938, by which time the sawfly had spread over 31,000 km 2. Most sawfly populations were reduced to below economic threshold levels by 1943, and remain under natural control today, the control being effected by a combination of the NPV (which accounts for more than 90% of the control) and the parasites. While viruses, particularly NPVs, are frequently associated with rapid declines in the populations of important lepidopterous and hymenopterous (sawfly) pests, the G. hercyniae NPV is the only true example of a virus that has been effective as a classical biological control agent. Another baculovirus, the "nonoccluded" baculovirus of the palm rhinoceros beetle (Oryctes rhinoceros) has been a quasi-classical biological control success in that once introduced into populations it can yield control for several years, but ultimately it dissipates and must be reapplied against the pest population (Bedford, 1981; Zelazny et al., 1992). Moreover, aumentative seasonal introductions, though possibly effective, have only rarely been effective and are not well documented. Thus, the control potential of most viruses is best evaluated by assessing their utility as microbial

523

insecticides. From this standpoint, iridoviruses are essentially useless because of their poor infectivity per os. CPVs are not much better because, though highly infectious per os, the disease they cause is chronic (Aruga & Tanada, 1971; Payne, 1981; Tanada & Kaya, 1993; Kunimi, 1998). CPVs have, however, been useful in some situations, such as for suppression of the pine caterpillar, Dendrolimus spectabilis, in Japan. The interested reader is referred to Katagiri (1981) for a review of these viruses as control agents. Entomopoxviruses have not yet been developed as control agents for any insect. The control potential and procedures for development of these viruses are similar to those described earlier for entomopoxviruses, and later below for NPVs; therefore, they will not be discussed here in any detail. The interested reader is referred to the publications by Granados (1981) and Arif (1984) for additional information about entomopoxviruses. Nuclear Polyhedrosis Viruses as Conventional Microbial Insecticides

The viruses most commonly used or considered for development as microbial insecticides in industrialized as well as less developed countries are the NPVs. The reasons for this are that NPVs are often common in, and easily isolated from, pest populations, production in their hosts is straightforward and inexpensive, and technology for formulation and application is relatively simple and adaptable to standard pesticide application methods. Most NPVs, however, are narrow in their host range, infecting only a few closely related species. Furthermore, though several can be grown in vitro in small to moderate volumes (ca. 20 to 300-liter cell cultures), no fermentation technology currently exists for their mass production on a commercial scale that would permit repeated applications to hundreds of thousands of acres, which is possible with B.t. and chemical insecticides. These two key limitations have been significant disincentives for the commercial development of NPVs, especially in industrialized countries. The large chemical and pharmaceutical companies that might be expected to take an interest in NPVs have, with rare exception, demonstrated little interest in producing a product that must be grown in living caterpillars or sawfly larvae, and that in most cases has a small market. The production technology is more suitable for "cottage industries" in either industrialized or developing countries. However, in industrialized countries, where all pathogens used as insecticides must be registered by one or more governmental agencies, the regulatory procedures and associated costs of developmentmconserva tively estimated at $1,000,000mimpede development by smaller companies such as those involved in the production of predators and parasites. Despite these drawbacks, several NPVs have been registered as microbial insecticides though the market size for

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B.A. Federici

TABLE 2 Target pest

Major Viruses Used or under Development for Control of Insect Pests a Virus

Crop or habitat

Product name

Producer

Registered or in use

Caterpillars Anticarsia gemmatalis

NPV

Soybeans

None

Adoxophyes orana

GV

Fruit orchards

Capex

Cydia pomonella Helicoverpa zea

GV NPV

Apples, walnuts Cotton, vegetables

Madex Gemstar

Lymantria dispar

NPV

Decidous forests

Mamestra brassicae

NPV

Vegetables

Gypcheck Disparvirus Mamestrin

Orgyia pseudotsugata Spodoptera littoralis S. exigua

NPV NPV NPV

Douglas fir forests Cotton Vegetables

TM Biocontrol-1 Spodopterin Spod-X

Various/local (Brazil) Andermatt Biocontrol (Switzerland) Andermatt Biocontrol Thermo-Trilogy (United States) Thermo-Trilogy Canadian Forest Service Caliope (France) Thermo-Trilogy Caliope Thermo-Trilogy

NPV NPV

Spruce forests Pine forests

NPV

Pine forests

Neocheck-S Sentifervirus Lecontivirus

Canadian Forest Service

Sawfly larvae Gilpinia hercyniae Neodiprion sertifer

N. lecontei

Under development

Caterpillars Autographa californica S. exigua Cydia pomonella Plodia interpunctella

NPV NPV GV GV

Vegetables Vegetables Apples, walnuts Stored nuts

Gusano Spod-X CYD-X None

Thermo-Trilogy Thermo-Trilogy Thermo-Trilogy U.S. Department of Agriculture

aSee Shah and Goettel (1998) or the website "www.sipweb.org" for a recent list of pathogen products.

m o s t is quite small (Table 2). W h e t h e r registered or not, several are used in m a n y less developed countries, particularly for control of lepidopteran pests of field and vegetable crops (Entwistle, 1998). M o r e o v e r , over the past decade there has been r e n e w e d interest in developing N P V s because r e c o m b i n a n t D N A technology offers potential for i m p r o v i n g the efficacy of these viruses. For e c o n o m i c reasons, as in the past, this interest is still restricted largely to

TABLE 3

N P V s of major lepidopteran pests and a few key sawflies. The high host specificity of N P V s makes t h e m of m o s t use where a single insect species is the only pest or at least a key one of a particular crop. Utility is increased if the target insect is not very sensitive to B.t., and is resistant to chemicals; or if the latter are too costly, e n v i r o n m e n t a l l y unacceptable, or unavailable. The viruses listed in Tables 2 and 3 all meet, or at one time met, these criteria. Before dis-

Comparative Efficacy of Representative Occluded Viruses a

Virus

Occlusion body yield per larva

Anticarsia gemmatalis NPV Helicoverpa zea NPV Lymantria dispar NPV Orgyiapseudotsugata NPV Spodoptera exigua NPV Neodiprion sertifer NPV Cydia pomonella GV

2 X 10 9 1 X 1010 2 X 109 2 X 10 9 2 x 109 1 X 109 1 X 1013

Occlusion body application rate per hectare 1.5 X

1X 5X 3X 1X 1X 2X

1011 1012 1011 1011 1012 1011 1015

aAmount needed to reduce crop loss or pest populations by approximately 80 to 95%.

LEs per hectare a

50 100 250 125 500 200 300

Chapter 18 A Perspective on Pathogens as BiologicalControl Agents for Insect Pests cussing the possibilities for improvement through genetic engineering, it is worthwhile to summarize with a few examples the use of conventional (i.e., unengineered) NPVs and GVs as microbial insecticides and to consider further their advantages and limitations.

Production and Formulation The NPVs are mass-produced in larval hosts grown on an artificial diet or vegetation from natural host plants, and in the latter case can be done in the field (Ignoffo, 1973; Moscardi, 1999). All viruses currently used in control programs are produced in larvae. To maximize production, larvae are infected per os at an advanced stage of development, such as during the late fourth instar, and are reared either as groups, or as individuals for species that are cannibalistic. After ingesting the virus, occlusion bodies dissolve in the alkaline midgut, releasing virions. In lepidopterans, the virus first invades midgut epithelial cells where, during the first 24 h of infection, it undergoes an initial colonizing phase of replication in the nuclei of these cells. No occlusion bodies are produced in these nuclei, but instead progeny virions migrate through the basement membrane, and invade and colonize almost all other tissues of the host. In these, virus replication results in virions that are occluded in polyhedra. Maximum production of polyhedra occurs in tissues that are the most nutrient rich and metabolically active such as the fat body, epidermis, and tracheal matrix. This definitive phase of viral disease occurs over a period of 5 to 10 days, and represents several cycles of replication as the virus spreads throughout the tissues and invades most host cells. The actual length of the disease depends on several factors including the host and viral species, the larval instar at the time of infection, the amount of inoculum, and the temperature. Near the end of the disease, after most polyhedra have formed, the nuclei lyse. As more and more nuclei lyse, the larva eventually dies; after this the body "liquefies," releasing literally billions of polyhedra. In commercial production, larvae may be harvested prior to liquefaction to keep bacteria, which quickly colonize dead larvae, at a low level in the final product. Alternatively, antibiotics can be added to the diet to keep bacterial counts low. After the larval production phase is complete, the larvae are collected and formulated. Formulation varies considerably, and depends on how the virus will be used, but both liquid concentrates and wettable powders have been developed that usually can be applied with conventional equipment (Ignoffo, 1973; Shapiro, 1986; Moscardi, 1999). The production of lepidopteran GVs and sawfly NPVs is similar to that described for lepidopteran NPVs [see Cunningham and Entwistle (1981) and Shapiro (1986)]. As noted previously, however, the sawfly NPVs differ from the lepidopteran NPVs in that the former only replicate and form polyhedra in midgut epithelial cells. Polyhedral yields

52.5

therefore are lower than those obtained with lepidopteran NPVs.

Use of NPVs and GVs The extent to which conventional NPVs can be useful as microbial insecticides depends on several factors that include the relative importance of the target pest in the pest complex attacking a crop, the amount of virus that must be used to control the pest in both the short term and long term (persistence and carryover), the value of the crop, and the cost and availability of alternative control measures (Federici, 1998). NPVs are ideal candidates for use where a single lepidopteran species is the major pest for most of the growing season on a crop with a high cash value where other available pest control methods are not cost-effective. Thus, NPVs that have been developed and used are those effective against species of Helicoverpa, Heliothis, and Spodoptera on such crops as cotton, corn, and sorghum; and even more so on tomatoes, strawberries, and flowers such as chrysanthemums, and Anticarsia gemmatalis in soybeans. The cost-effectiveness of these viruses is determined by the amount of virus that must be applied and the frequency of application necessary to keep the pest below an economic threshold. As noted earlier, this will vary with the virus, pest, and crop; and more importantly, among different countries. The amount of virus required is best assessed in terms of larval equivalents (LEs) (Ignoffo, 1973) necessary to achieve effective control. Illustrative examples are given in Table 3. The number of LEs required to obtain effective control is a critical component in the determination of cost-effectiveness due to the cost of labor and materials that go into virus production. This can range from 50 LEs per hectare per treatment using the A. gemmatalis NPV (AgNPV) to control the velvet bean caterpillar on soybeans to 500 LEs for the S. exigua multiple nucleocapsids per virion envelope (SeMNPV) on lettuce and chrysanthemums. Moreover, the number of LEs required to control a specific pest can vary with the crop due to differences in insect feeding behavior and in crop characteristics (such as phenology, leaf chemistry, and plant structure). For example, whereas 500 LEs per hectare may be required to control S. exigua on lettuce, the value may be as high as 1000 LEs on alfalfa or as low as 200 LEs on tomatoes. Clearly, the use of the SeMNPV to control the beet armyworm on tomatoes is much more cost-effective than its use would be on alfalfa. This type of economic evaluation is essential for determining if a specific NPV merits commercial development as well as for determining if it will be useful against a specific insect on a particular crop. Because the actual use of NPVs and GVs as microbial insecticides in insect control programs is very limited in developed countries and is not well documented in most developing countries with the exception of Brazil, it is not

526

B. A. Federici

possible to know the amount of hectares treated. The largest documented program in the world is the use of the AgNPV against this pest on soybeans in Brazil, where the hectares treated exceed 1 million (2.2 million acres) annually (Moscardi, 1999). Based on estimates collated by Entwistle (1998) and Moscardi (1999), this single program probably exceeds the total area currently treated worldwide with all other NPVs and GVs. These viruses may be more widely used than indicated here, but this information is not readily available in the published literature. The AgNPVhoybean program and a few others are briefly described here to provide examples of viruses used in control programs. A wider range of examples is provided in reviews by Hunter-Fujita et al. (1998) and Moscardi (1999), as well as in earlier reviews by Fuxa (1990), Shapiro (1986), Shapiro and Robertson (1992), Payne (1982, 1988), and Pinnock (1975), which remain worthy reading. AgNPV for Control of A. gemmatalis on Soybeans The use of the AgNPV to control the velvet bean caterpillar, A. gemmatalis, was initiated in the early 1980s and grew by the mid-1990s to a program of approximately 1 million hectares (2.2 million acres) of soybeans (Moscardi, 1999). The virus is applied at a rate of 50 LEs per hectare (1.5 X 10" polyhedra) when populations are in the first three instars, and when there are 20 or fewer larvae per row-meter of plants. Only one application is made per growing season. The cost to the farmer is about $1.50 per hectare, which is cheaper than chemical insecticides, and the level of control is comparable. The program is coordinated by the state agency, Embrapa, which awards contracts for the production of virus to five private companies. Most of the virus is produced in field plots, where yields of AgNPV-infected larvae have grown to 35 metric tons per year (Moscardi, 1999). The success of this program is due to several factors, a primary one being that the virus only has to be applied once per season. In addition, soybeans can tolerate a significant amount of defoliation without affects on yield, and labor costs for the production of the virus are quite low.

Helicoverpa zea NPV (HzNPV) for Control of the Heliothis and Helicovelpa Species The HzNPV was the first virus commercialized for use on a large scale (Ignoffo, 1973), and was sold originally by Sandoz, Inc. (which has merged with Ciba-Geigy to become Novartis) as Elcar. It was was developed for use against Heliothis virescens and Helicoverpa zea in cotton, but was not a commecial success due to the advent of the synthetic pyrethroids, which were cheaper and highly effective. This virus is still used in many countries such as China and India to control various members of the Heliothis/Helicoverpa complex on crops such as cotton, corn, and sorghum. Total usage worldwide

is probably in the range of 200,000 to 300,000 ha, and the rates of application are in the range of 100 to 200 LE per hectare. Typically, several applications are required per growing season, with the rate and frequency depending on the crop and size of the pest population. Though one of the most effective NPVs, this virus has not been used much in developed countries because it was not being produced commercially on a large scale. Novartis has sold its microbial insecticide business to Thermo-Trilogy, and the HzNPV is now again available under the product name Gemstar.

Spodoptera NPVs for Control of Spodoptera Species The Spodoptera complex consists of important species that attack a wide variety of field and vegetable crops. The most improtant pests include S. exigua, S. frugiperda, S. litura, and S. littoralis. Each of these is attacked by an NPV that is fairly specific, and isolates of several of these have been developed in different regions of the world for Spodoptera control. For vegetable crops, the SeNPV has been developed for control of S. exigua on vegetable and ornamental crops. Thermo-Triology currently produces this virus under the trade name Spod-X, and the product is used to control S. exigua on chrysanthemumns in greenhouses in the Netherlands, and on vegetable crops in Thailand, with application rates typically ranging from 100 to 300 LE per hectare depending on the crop and insect pressure. It is also being evaluated for use on cotton in the United States. Total area treated at present is quite small, amounting to less than 10,000 ha worldwide. The S. frugiperda NPV (SfNPV) has been developed for control of this pest in maize in Latin America, where annual usage is currently in the range of 20,000 ha (Moscardi, 1999). The S. litura and S. littoralis NPVs (Entwistle, 1998) are primarily used for control of these pests on cotton in Middle Eastern countries and Asia, but accurate figures on their use are not available. GVs for Insect Control The granulosis viruses of codling moth, Cydia pomonella (CpGV), the potato tuberworm, Phthorimaea operculella (PoGV), and the cabbageworm, Pieris rapae (PrGV), are used to varying degrees to control these pests. The CpGV is registered for use against codling moth larvae on apples in Canada, the United States, and several European countires including Switzerland and Germany. The virus is applied at rates varying from 1 to 2.5 X 1013granules per hectare, at a cost of $50 to $80 per application (see Table 3). In cool areas at high altitudes such as in Switzerland, the moth has only one or two generations per year, and thus the virus is cost-effective. In California, however, populations may have to be treated once a week, thereby decreasing the cost-effectiveness of the virus (Cunningham, 1998). Commerical preparations

Chapter 18 A Perspective on Pathogens as BiologicalControl Agents for Insect Pests currently on the market include Carpovirusine (France), Madex (Switzerland), and Granusal (Germany), with sales worldwide scheduled to reach 60,000 ha in 1998 (Moscardi, 1998). The PoGV is used in many developing countries to protect potatoes that are stored aboveground after harvest. Under direction of Center International for Potato Research (CIP, Lima, Peru), the virus is produced by "cottage industries" in countries such as Peru, Morroco, Libya, China, and Indonesia; and is typically applied to potatoes as a dust. The PrGV has been used for many years in mainland China to control P. rapae on vegetable crops (Entwistle, 1998). The virus, for use in either dusts or wettable powders, is produced in larvae in field plots of cabbage and lettuce, and then is harvested as the infected larvae begin to die. The area treated with the virus is not known, but probably is at least several tens of thousands of hectares per year. Limitations Viruses are not widely used at present in industrialized countries because products based on them are of very limited availability. Moreover, effective and competitively priced alternatives are readily available. Among these are new and more specific chemical insecticides such as the pyrroles, Fipronil and Imidocloprid, and existing and new products based on B.t., including transgenic plants. Furthermore, viruses still have what are considered key limitations. These include relatively slow speed of kill, narrow spectrum of activity (host range), little residual activity, and lack of a cost-effective system for mass production in vitro. On the other hand, these limitations have not inhibited the development and use of viruses in developing countries where NPVs and even a few GVs are used, especially on field and vegetable crops, in China, India, and Brazil, as well as in many smaller countries in Latin America, Africa, and Southeast Asia (Hunter-Fujita et al., 1998; Zhang, 1981; Peng er al., 1988, 1991; McKinley et al., 1989, Moscardi, 1989, 1990, 1999). The reasons for this are that chemical insecticides in many of these countries are expensive, their widespread and heavy use has resulted in resistance, labor costs for virus production in vivo are low, production technology is simple, and registration for use of viruses either is not required or is easily obtained. If pressure continues to reduce the use of synthetic chemical insecticides, viruses will receive increased attention, particularly for the control of lepidopterous insects for which no other effective control agents such as B.t. and parasites exist. This should lead to increased efforts to develop and use conventional viruses in IPM programs in both industrialized and developing countries. In addition to conventional viruses, the development of recombinant DNA technology (i.e., genetic engineering) offers promise

527

for improving viral efficacy by reducing or eliminating some of their major disadvantages. Use of R e c o m b i n a n t DNA T e c h n o l o g y to I m p r o v e N u c l e a r P o l y h e d r o s i s Viruses The two most significant limitations of conventional viral insecticides are the relatively slow speed of kill and the narrow host range. Recombinant DNA technology is being used to overcome both of these limitations (Miller, 1988; Maeda, 1989; Hawtin & Possee, 1992; Black et al., 1997; Treacy, 1998). When a conventional virus is used against an insect population (e.g., against noctuid larvae), the population typically consists of a mixture of instars and may contain more than one economically important species. A virulent NPV sprayed at an appropriate rate will kill the first and second, and in some cases the third instars, within 2 to 4 days. However, the more advanced instars may live for a week or more, causing further damage to the crop. Thus, current approaches to improving the efficacy of viral insecticides are aimed at developing broad-spectrum viruses that will cause a cessation of larval feeding within 24 to 48 h of infection, either by death or by paralysis. This is being done by deleting genes that delay death from viruses, and by engineering viruses to express genes encoding enzymes or peptide hormones that disrupt larval metabolism, or peptide neurotoxins that paralyze or kill the insect directly. Because it already has a broader host range than most occluded baculoviruses and can be genetically manipulated with ease in several cell lines, the Autographa Californica MNPV (AcMNPV) is the virus that has been the subject of most of the engineering studies to date. The virus is engineered by deleting the gene encoding EGT (ecdysteroid UDP-glucosyltransferase) and/or by adding one or two genes encoding toxins under the control of strong viral promoters. By using this strategy, genes for juvenile hormone esterase (Hammock et al., 1990), B.t. endotoxins (Martin et al., 1990; Merryweather et al., 1990; Pang et al., 1992), insecticidal neurotoxins from the straw itch mite (Pyemotes tritici), scorpions (Androctonus australis, Buthus epeus, and Leirus quinquestriatus lebraeus), and spiders (Agelenopsis aperta, Diguetia canites, Tegenaria agnestis) have been engineered into the AcMNPV (McCutchen et al., 1991; Tomalski & Miller, 1991; Black et al., 1997; Treacy, 1998). Of these, the most promising results have been obtained with viruses producing neurotoxins, where the time between feeding and paralysis has been reduced by as much as 40% in comparison to wildtype AcMNPV (Treacy, 1998). Engineering viruses to express insecticidal proteins in many cases could also result in an expanded host range. This is because in many lepidopteran host species that do not develop a patent disease when infected by conventional

52,8

B.A. Federici

viruses, there can be limited viral replication, with these less susceptible hosts developing a mild disease and surviving infection. However, the same hosts infected by an engineered virus that expresses a potent insecticidal protein will likely succumb because the virus does not need to replicate extensively to paralyze or kill the larva.

BACTERIA Bacteria are relatively simple unicellular microorganisms that lack internal organelles such as a nucleus and mitochondria and which reproduce by binary fission. With a few exceptions, most of those used as microbial insecticides grow readily on a wide variety of inexpensive substrates, a characteristic that greatly facilitates their mass production. The overwhelming majority of the bacteria currently used or under development as microbial control agents for insects are spore-forming members of the bacterial family Bacillaceae, and belong to the genus Bacillus. These insect-pathogenic bacilli occur in healthy and diseased insects, but also occur in, and can be isolated from, many other habitats including insect frass, soil, plants, granaries, and aquatic environments. Biological Properties in Relation to Insect Control Bacteria, especially the various subspecies of Bacillus thuringiensis Berliner, have been and will continue for the foreseeable future to be the insect pathogens used most widely and successfully in insect control. The reasons for this are that they are easy to mass-produce, formulate, and use in large-scale operational control programs; kill target insects quickly (- 1 0 were less common (24%) as were cases where the maximum LCso exceeded the field rate (25%). Notable cases of resistance in Hymenoptera include > 10-fold resistance of Diglyphus begini (Ashmead) to both carbamates and pyrethroids (Rathman et al., 1990), 66-fold resistance to methidathion in Comperiella bifasciata Howard (Schoonees & Giliomee, 1982), and >1200-fold resistance to malathion in Anisopteromalus calandrae (Howard) (Baker & Weaver, 1993). The set of cases reviewed here suggests that statistically significant variation in susceptibility to pesticides among conspecific populations is common in natural enemies. Resistance that may be high enough to confer survival at field application rates appears to be about twice as common in predatory phytoseiid mites compared with that of hymenopteran parasitoids. Phytoseiids may evolve resistance readily because they are exposed to pesticides in all life stages,

Chapter 24

Evolution of Pesticide Resistance in Natural Enemies

have limited dispersal, and can subsist on plant materials when prey density is low (Georghiou, 1972; Croft & Brown, 1975). These and other traits of phytoseiids will be discussed in relation to specific hypotheses described later. Hoy (1985) and Croft and van de Baan (1988) consider pesticide resistance in phytoseiids in greater detail. In summary, available evidence is not sufficient to conclusively refute or support the documentation bias hypothesis. Our review of recent field surveys shows that substantial resistance was found commonly in phytoseiid mites, but was less common in most of the other natural enemies tested. Results from a survey of fruit entomologists suggest that among insects and mites from apple orchards, resistance to azinphosmethyl was nearly as frequent in natural enemies as in pests (Croft, 1982). However, because of the unusually prolonged use of azinphosmethyl and other factors, resistance to azinphosmethyl in apple arthropods may not be indicative of broader trends (Tabashnik & Croft, 1985). Bioassays of several pest and natural-enemy species from two or more populations representing variation in insecticide exposure for a particular crop and region could help to assess the extent of bias in documentation.

Differential P r e a d a p t a t i o n The differential preadaptation hypothesis states that resistance to pesticides evolves more readily in pests than in natural enemies due to differences in responses to pesticides between pests and natural enemies that existed before selection for pesticide resistance. Several specific hypotheses fall under the general category of differential preadaptation: 1. Pests evolve resistance more readily because they have better intrinsic detoxification capabilities than natural enemies have (Gordon, 1961; Croft & Morse, 1979; Croft & Strickler, 1983). 2. Pests evolve resistance more readily because they have greater intrinsic tolerance to pesticides than natural enemies have (Rosenheim & Hoy, 1986). 3. Pests evolve resistance more readily because they have more genetic variation in tolerance to pesticides than natural enemies have (Georghiou, 1972). 4. Pests evolve resistance more readily because the fitness cost associated with resistance is lower for pests than for natural enemies. These four hypotheses are not mutually exclusive. Each hypothesis has two parts: (1) an intrinsic (before pesticide exposure) difference between pests and natural enemies in response to pesticides, which (2) enables pests to evolve resistance more readily than natural enemies evolve it. A test of any preadaptation hypothesis must examine both components. Tests of part (1) require comparisons between susceptible populations of pests and natural enemies. Ide-

675

ally, such tests should compare populations that have had little or no exposure to pesticides, but such populations may be rare. Thus, attempts to measure intrinsic differences between pests and natural enemies can be confounded by the history of insecticide exposure (Croft & Strickler, 1983). Tests of part (2) are more difficult because they require examination of how a particular intrinsic difference will influence evolution of resistance. Direct tests would need to determine if the measured intrinsic difference caused differences in rates of evolution. For example, an ideal comparison would contrast the rate of evolution of resistance in two populations of a natural-enemy species that differed only in initial detoxification capability. The preadaptation hypothesis would be supported if the natural-enemy strain with higher initial detoxification capability evolved resistance faster than the other strain evolved it. Further, if intrinsic detoxification capacity is a primary determinant of the rate of resistance evolution, then a natural-enemy strain with initial detoxification capability comparable to that of a pest would be expected to evolve resistance at a rate comparable to the pest. Indirect tests could compare rates of evolution of resistance between pest and natural-enemy species that had intrinsic differences, but such tests could not restrict the cause of a difference in evolutionary rates to any particular factor. In other words, species differ in many ways and interspecific comparisons do not allow one to determine if a given factor is responsible for differences in the rate of resistance evolution between species. Another type of investigation involves theoretical models. This approach attempts to measure the potential impact of intrinsic differences by comparing projected rates of resistance evolution under various assumptions about initial conditions. In the following section we consider empirical and theoretical evidence relevant to specific preadaptation hypotheses.

Detoxification Enzymes The origins of this hypothesis are reviewed by Croft and Strickler (1983) and Rosenheim et al. (1996). The principal idea is that herbivorous pest insects have evolved enzymes to detoxify plant secondary compounds and thus are better preadapted to detoxify pesticides than are entomophagous natural enemies, which do not eat plants. We review available evidence to determine (1) whether herbivorous pests have higher intrinsic levels of detoxification enzymes than natural enemies have, and (2) whether such differences cause natural enemies to evolve resistance more slowly than pests evolve it. In the broadest survey to date, Brattsten and Metcalf (1970) used the synergistic ratio of carbaryl with piperonyl butoxide to compare levels of mixed function oxidase (MFO) detoxification enzymes in 53 insect species from

TABLE 2

P e s t i c i d e S u s c e p t i b i l i t y o f Field a n d S t o r e d Grain P o p u l a t i o n s of N a t u r a l E n e m i e s , 1 9 7 9 t o 1 9 9 5 O'x

Species (family)

Location

Habitat

Maximum resistance ratio at

No. of populations tested

Pesticide

LCso

Maximum LCs0 > field rate

References

Acarina

Amblyseius fallacis (Phytoseiidae)

Michigan, New York

Apple, soybean

12 12 2 2 2 2 4 8 5

Azinphosmethyl Permethrin SD 57706 b NCI 85913 b Fluvalinate ZR 3903 b Carbaryl DDT Methoxychlor

34 a 15~ 46' 2a 5a 8° 3C > 43 a 13

Yes No ----Yes Yes --

Strickler & Croft, 1981 Croft & Wagner, 1981

Croft et al., 1982 Scow etaL, 1983

Euseius (=Amblyseius) hibisci (Phytoseiidae)

California

Citrus

2

Dimethoate

22

No

Tanigoshi & Congdon, 1983

Metaseiulus (= Typholodromus) occidentalis

California

Grape

14 6

Dimethoate Methomyl

11" 3a

Yes No

Hoy etal., 1979

Pear,

11 11 2

Azinphosmethyl Diazinon Dimethoate

5" 4~ 1c

D'I

(Phytoseiidae) wild blackberry

Typhlodromus arboreus

Oregon

Apple

2

Azinphosmethyl Carbaryl

7 2

England, the Netherlands, New Zealand

Apple

10 10 7

Azinphosmethyl Carbaryl Permethrin

6 > 62 2

Israel

Citrus, cotton

2

South Carolina

Stored grain

2

Michigan

Apple

South Carolina

Stored grain

(Phytoseiidae)

T. pyri (Phytoseiidae)

--__ a

H o y & K n o p , 1979 r~

No No

Croft & Aliniazee, 1983

Yes Yes No

Kapentanakis & Cranham, 1983 O

Araneae

Chiracanthium mildei

Malathion

3

Malathion

33"

Mansour, 1984

(Clubionidae)

Coleoptera

Xylocoris flavipes

Baker & Arbogast, 1995

(Anthocoridae)

Diptera

Aphidoletes aphidimyza ~

14

Azinphosmethyl

3"

Yes

5a > 1200 7~ 2" 2"

Yes ----

Warner & Cro~,1982

(Cecidomyiidae)

Hymenoptera

Anisopteromalus calandrae (Pteromalidae)

Aphytis africanus (Aphelinidae)

South Africa

Citrus

2 2 2 2 2

Chlorpyrifos-methyl Malathion Pirimiphos-methyl Cyfluthrin deltamethrin

2

Methidathion

6"

-

-

No

B a k e r & W e a v e r , 1993

Baker, 1994 Schoones&Giliomee, 1982

A. holoxanthus (Aphelinidae)

Israel

Citrus

7

A. melinus (Aphelinidae)

Califomia

Citrus

7 8 11 12 9

Malathion

3a

No

Havron, 1983

Carbaryl Chlorpyrifos Dimethoate Malathion Methidathion

2a

No

Rosenheim & Hoy, 1986

2~ 3"

No No No No

8~

88-

Bracon hebetor (Braconidae)

Georgia, South Carolina

Stored grain

3

Malathion

Comperiella bifasciata (Encyrtidae)

South Africa

Citrus

2

Methidathion

Diaretiella rapae (Aphidiidae)

California

Cauliflower, wild mustard

2

Methomyl

Diglyphus begini (Eulophidae)

Hawaii, California

Bean, tomato

5 5 5 5

Fenvalerate Methomyl Oxamyl Permethrin

17a 21 ~ 20 13a

No No Yes

Ganaspidium utilis (Ecucoilidae)

Hawaii, California

Bean, tomato

5 5 5 5 5

Fenvalerate Malathion Methomyl Oxamyl Permethrin

3~ 93~ 2~ 12~

Yes No No No Yes

Pholetesor ornigis (Braconidae)

Ontario (Canada)

Apple

3 2 2 2

Azinphosmethyl Fenvalerate Methomyl Permethrin

2~ 2~ 4~ 3-

Trioxys pallidus (Aphidiidae)

California

Walnut

5

Azinphosmethyl

5

66 a

Baker et al., 1995 No

Schoonees & Giliomee, 1982

No

Hsieh, 1984

Yes

Rathman et al., 1990

Rathman et al., 1995

O O

Trimble & Pree, 1987I

.-n

No

Hoy & Cave, 1988

5" Z

Neuroptera

Chrysoperla carnea (Chrysopidae)g

California

Alfalfa

4 4 4 4 4 4

e-

Carbaryl Diazinon Fenvalerate Methomyl Permethrin Phosmet

3~/2~ 2q4 2/2~ 3~/3c 5/11 2q16

No/No No/No Yes/Yes No/No Yes/Yes No, Yes

Grafton-Cardwell & Hoy, 1985

Inn

3

a Statistically significant difference is between LCs0's of at least one pair of populations (by nonoverlap of 95% fiducial limits). bThis is an experimental pyrethroid; see reference for details. CNo significant differences are among LCs0's. dpear populations are not treated with dimethoate. ~Bioassays are of eggs. fA subsequent survey detected no decrease in susceptibility from 1987 to 1989 (Trimble et al., 1990). gBioassays are of adults/first-instar larvae.

G~

678

B.E. Tabashnik and M. W. Johnson

TABLE 3 Summary of Pesticide Susceptibility of Field and Stored Grain Populations of Natural Enemies, 1979 to 1995

Group

Phytoseiid mites Phytoseiid mites (field-used pesticides only) C Nonphytoseiids Hymenoptera Chrysoperla carnea Totals Totals (field-used pesticides only) c

No. of species

Significant variation a (%)b

Maximum resistance ratio > I0 (%)b

Maximum LCso > field rate (%)b

5 5

77(10/13) 88(7/8)

40(8/20) 50(7/14)

50(6/12) 55(6/11 )

15 11 1 20 20

83(29/35) 93(25/27) 29(2/7) 81(39/48) 84(36/43)

23(10/44) 24(1/13) 17(2/12) 28(18/64) 24(17/58)

41(11/27) 25(5/20) 42(5/12) 44(17/39) 45(17/38)

aNonoverlap of 95% fiducial limits occurs for LCs0's of at least one pair of populations. bNumbers show the percentage of cases that meet each criterion (numbers of cases are in parentheses). CThis excludes cases in which populations were tested versus compounds that had not been applied to them in the field (i.e., pyrethroids tested before field use and dimethoate versus M. occidentalis in grapes).

eight orders. Piperonyl butoxide inhibits MFO enzymes that detoxify carbaryl. Thus, the ratio of the LDs0 (or LCs0) of carbaryl alone to the LDso (or LCs0) of carbaryl plus piperonyl butoxide (synergistic ratio) is an indicator of MFO activity. Brattsten and Metcalf (1970) found that a few of the phytophagous species had extraordinarily high synergistic ratios [most notably Pogonomyrmex barbatus (F. Smith), the red harvester ant, synergistic ratio >223], but the median synergistic ratio for 25 herbivores (3.6) was less than half the median for 15 entomophagous species (8.4). The proportion of species with low synergistic ratios (i.e., below the overall median of 4.8) was significantly greater for herbivores (17/25) than for predators and parasites (3/15) (p < 0.01, median test; Fig. 1). The median synergistic ratios for 13 crop pests (2.3) and 27 herbivorous and non-herbivorous pests (4.2) were also significantly lower than the median for entomophagous species (p < 0.01 and p < 0.05, respectively). These findings contradict part (1) of the preadaptation hypothesis. Consideration of part (2) of the hypothesis shows that natural enemies that have not been reported as resistant to insecticides had greater synergistic ratios than did several pests that are notorious for their ability to evolve insecticide resistance. For example, the synergistic ratios for six of seven species of parasitic Hymenoptera studied were higher than the ratios for the German cockroach [Blattella germanica (Linnaeus)], the corn earworm [Helicoverpa zea (Boddie)], the fall armyworm (Spodoptera frugiperda J. E.

FIGURE 1 Synergistic ratio of carbaryl with piperonyl butoxide as an indicator of mixed function oxidase (MFO) activity in entomophagous and herbivorous insects [Adapted from Brattsten, L. B., & Metcalf, R. L. (1970). Journal of Economic Entomology, 63, 1347-1348.]

Smith), and the southern house mosquito (Culex pipiens

quinquefasciatus Say). In conclusion, the data of Brattsten and Metcalf (1970) do not support the idea that phytophagous pests have higher levels of detoxification enzymes than natural enemies have. Further, their data suggest that low MFO activity, as indicated by the synergistic ratio of carbaryl to piperonyl butoxide, does not necessarily slow evolution of pesticide resistance. Some pests with low synergistic ratios have evolved resistance whereas some natural enemies with relatively high ratios have not. The preceding conclusions were later confirmed by findings that piperonyl butoxide affected a predatory mite (Amblyseius fallacis Garman) more than it affected its herbivorous prey mite (Tetranychus urticae Koch) (Strickler & Croft, 1985). In addition, the synergistic ratios of piperonyl butoxide with propoxur for adults of the ectoparasitic braconid Oncophanes americanus (Weed) (14.0) were 8-, 2-, and 12-fold greater than the synergistic ratios for adults, large larvae, and medium larvae, respectively, of its herbiv-

Chapter 24 Evolutionof Pesticide Resistance in Natural Enemies orous tortricid host, Argyrotaenia citrana (Fernald) (Croft & Mullin, 1984). The synergistic ratio for large larvae of the ectoparasite (5.5) was more than triple the synergistic ratio for adults or medium larvae of the host, but it was slightly less than the synergistic ratio of large larvae of the host (6.0). Croft and Mullin (1984) stated that "synergist tests are useful in qualitatively estimating the availability of an MFO detoxification pathway," but they questioned the value of piperonyl butoxide synergist tests as an indicator of MFO activity across diverse arthropod species. Thus, it is important to consider other measures of enzyme activity, such as results from in vitro assays. In vitro inhibition studies and hydrolysis assays showed that predatory lacewing larvae, C. carnea, have unusually active esterases that detoxify pyrethroids (Ishaaya & Casida, 1981). Although direct comparative tests were not done, preparations of whole lacewing larvae were more active than larval gut or integument preparations from an herbivore, the cabbage looper, Trichoplusia ni (Htibner). Lacewing larvae were chosen for enzymatic tests because they have high natural tolerance to pyrethroids and thus were suspected to have high esterase activity (Plapp & Bull, 1978). Therefore, the lacewing esterase activity data are a biased sample of natural-enemy detoxification enzyme capacity. Mullin et al. (1982) found differences in in vitro detoxification enzyme activity between susceptible populations of a predatory mite (Amblyseius fallacis) and its herbivorous prey mite (Tetranychus urticae). MFO and trans-epoxide hydrolase had greater activity in the prey than in the predator, but the opposite was observed for cis-epoxide hydrolase and glutathione transferase. Esterase activity was similar in susceptible populations of the two species. Although the herbivorous mite had greater activity than the predatory mite had for an MFO enzyme (aldrin epoxidase) and for trans-epoxide hydrolase, neither of these two enzymes was more active in resistant than in susceptible populations of the herbivore. These data suggest that resistance in the herbivore is not due to elevated levels of aldrin epoxidase or trans-epoxide hydrolase. Thus, it appears that intrinsically greater levels of these two enzymes were not responsible for the ability of the herbivorous pest to evolve resistance more readily than its predator evolved it. Conversely, of the five types of enzyme activity measured, only glutathione transferase was greater in resistant prey than in susceptible prey, suggesting that this enzyme could be partly responsible for resistance in the prey species. Contrary to the expectation of the preadaptation hypothesis, however, susceptible predators had more than 10-fold higher activity for this enzyme than susceptible pests had. The evidence suggests that the detoxification enzyme differences between A. fallacis and T. urticae reported by

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Mullin et al. (1982) do not support part (2) of the preadaptation hypothesis. It may be inappropriate to generalize from this case because predatory phytoseiid mites are the only group of natural enemies that has readily evolved pesticide resistance. Intrinsic disadvantages that slow evolution of resistance in other natural enemies may be absent or diminished in phytoseiids. Van de Baan and Croft (1990) compared in vitro enzyme activities between the mirid predator Deraeocoris brevis Knight and susceptible and resistant strains of its prey Psylla pyricola Foerster. They found that the pest had significantly higher esterase activity than did the predator. Further, elevated esterase activity was associated with resistance in the pest. However, glutathione S-transferase and P-450 monooxygenase activities were higher in the predator than in the susceptible strain of the pest. The results with esterase are consistent with the preadaptation hypothesis, but the results with the latter two enzyme activities are not. In a related study of in vitro enzyme activity, Croft and Mullin (1984) compared various life stages of a braconid ectoparasite Oncophanes americanus (Weed) and its tortricid host, Argyrotaenia citrana (Femald). Based on data from whole-body preparations averaged across life stages, none of the five assays conducted showed significantly lower enzyme activity in the parasitoid compared with that of the host. The parasitoid had three-fold higher cis-epoxide hydrolase activity (p < 0.001) and aldrin epoxidase activity (p = 0.06) than its host had. No significant differences were found between species in trans-epoxide hydrolase, glutathione transferase, or esterase activities. Enzyme activities from midgut tissue of late larvae of the host were much higher than the activities of whole-body preparations from any life stage of either species. Midgut tissue of the parasitoid was not assayed, so interspecific comparisons of midgut tissue enzyme activity were not possible. In summary, the data from this parasite-host system do not support part (1) of the preadaptation hypothesis and they do not address part (2) of the hypothesis. Another in vitro study compared adult midgut levels of three types of enzyme between an herbivorous coccinellid, Epilachna varivestis Mulsant, and a predatory coccinellid, Hippodamia convergens Guerin-Meneville (Mullin, 1985). Trans-epoxide hydrolase was virtually identical in the two species ( 5800/xg/g) and P. californicus estebanius Pergande (LCs0 = 450 ~g/cm2)]. However, median LD50 values did not differ significantly between 22 pests (35.5/~g/g) and 8 entomophagous species (28.8/xg/g). Similarly, medians for carbaryl LCs0 did not differ significantly between five pests (13.5/xg/cm 2) and seven parasites (14.5/xg/cm2). Surveys of studies that compare the LCs0 or LD5o values within complexes of natural enemies and pests also do not support the hypothesis that natural enemies are intrinsically more susceptible to pesticides than their prey or hosts are (Croft & Brown, 1975; Theiling & Croft, 1988). Croft and Brown (1975) found that natural enemies were more tolerant than their prey or hosts were in 67 of 92 cases in which the same bioassay method was used to compare species. Although predators were usually more tolerant than their prey were (63 of 77 cases), parasitoids were usually less tolerant than their hosts were (11 of 15 cases). Theiling and Croft (1988) calculated LCs0 or LDs0 ratios for 870 cases in which a natural enemy was compared with its prey or host. Ratios ranged widely, yet natural enemies were more tolerant than their prey or hosts were in 57% of the cases. Predators were more tolerant than their prey were, but parasitoids were less tolerant than their hosts were. For 10 of 12 families of natural enemies, including

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Braconidae and Aphelinidae, the average ratio for the family showed greater tolerance in the natural enemy. Phytoseiidae natural enemies were as tolerant as their prey were and only Ichneumonidae were less tolerant than their hosts were. The average ratio for 18 of 24 compounds including diazinon, permethrin, parathion, and carbaryl showed that natural enemies were more tolerant than their prey or hosts were. The preceding results contradict the differential intrinsic tolerance hypothesis. Theiling and Croft (1988) suggest some reasons why their survey may make natural enemies appear more tolerant than they really are. They note that LCs0 or LDso comparisons between pest and natural-enemy pairs are available for only a small subset of the studies of pesticide impact on natural enemies (fewer than 7% of the cases surveyed by Theiling & Croft, 1988). Natural enemies suspected to be tolerant to pesticides may be more likely to be compared with their prey or hosts in bioassays. Similarly, compounds thought to be more toxic to pests than to natural enemies may be more likely to be tested in comparative studies. Although some surveys suggest that natural enemies are not always less tolerant to pesticides than pests are, they are less tolerant in many cases (Theiling & Croft, 1988). Therefore, it is useful to consider how reduced intrinsic tolerance might affect evolution of insecticide resistance. If ability to survive field rates of pesticide is a criterion for resistance, then a natural enemy with lower intrinsic tolerance would have to increase its tolerance more substantially to be considered resistant. Simulations by Tabashnik and Croft (1985) suggest that, under certain conditions, reduced intrinsic tolerance could also slow evolution of resistance as measured by changes in the frequency of a resistance (R) allele. Simulations based on a one-locus model showed that 10- or 100-fold reduction in the LCso of homozygous susceptible (SS) individuals had little impact on projected times for resistance evolution in natural enemies of apple pests. In contrast, however, reducing the LCso of all three presumed genotypes (SS, RS, RR) by 10- or 100-fold greatly slowed resistance evolution in nearly all cases. When the LCs0's of all three genotypes were reduced, heterozygous individuals were rendered functionally recessive, which slowed evolution of resistance (see Curtis et al., 1978; Taylor & Georghiou, 1979; Tabashnik & Croft, 1982). The assumption of lower LCso'S for all three genotypes implies that an R allele increases the LCs0 by a fixed multiple. Thus, if the SS individuals are less tolerant, then so are RS and RR individuals. Lowering the LCso of SS individuals without altering the LCs0' s of RS or RR individuals assumes that an R allele provides a fixed level of tolerance, regardless of the tolerance of SS individuals. We do not know if either assumption is widely applicable. In summary, surveys of comparative bioassay studies

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suggest that, on average, natural enemies are not intrinsically less tolerant to pesticides than are pests. Such surveys may be biased, however; and there are at least 371 documented cases in which pests are more tolerant than their natural enemies are (Theiling & Croft, 1988). Reduced intrinsic tolerance could retard evolution of resistance in some natural enemies if resistance is defined as ability to survive field concentrations of a pesticide or if R alleles confer a fixed multiple of increased tolerance relative to susceptible individuals. The finding that Phytoseiidae species, which have been frequently recorded as evolving resistance, had low selectivity ratios (LCs0 of natural enemy divided by LCs0 of its prey or host) compared with other natural enemies (Theiling & Croft, 1988) suggests that low intrinsic tolerance relative to pests is not a major impediment to evolution of resistance in natural enemies. The idea that natural enemies are not generally less tolerant to pesticides than pests are differs from widely held perceptions. Such perceptions may be based partly on observations that field applications of pesticides affect natural enemies more than they affect pests. However, disruption of natural-enemy populations by field applications of pesticides may be due to reduction of host or prey populations in addition to direct toxic effects (see food limitation later in this chapter, and Johnson and Tabashnik in Chapter 13). Mathematical models show that if a pest and its natural enemy are equally susceptible to a pesticide, the pesticide will have a more severe impact on the natural-enemy population than on the pest population (Wilson & Bossert, 1971; Tabashnik, 1986). Therefore, pesticide applications can be extremely detrimental to natural-enemy populations, even if the natural enemy's tolerance is similar to that of the pest. Genetic Variation The genetic variation hypothesis says that natural enemies evolve resistance more slowly because natural-enemy populations have less genetic variation than pest populations have (Huffaker, 1971; Georghiou, 1972). Surveys of electrophoretic data show that hymenopterans have less variation in allozymes than most other insects have (Hedrick and Parker, 1997). In particular, the expected heterozygosity or average gene diversity (Hexp) for 13 species of wasps (0.044 ___ 0.006 SE) was less than half the Hexp for 158 species of Orthoptera, Homoptera, Coleoptera, Lepidoptera, and Diptera (0.120 ___ 0.006 SE) (Graur, 1985). These data are consistent with the idea that hymenopteran parasites have less genetic variation than do herbivorous insects. Although hymenopteran parasites may have less allozymic variation than most other insects, including many pests, this measure of genetic variation may be unrelated to the ability to evolve insecticide resistance. Some pests known for their resistance evolution had high expected het-

erozygosity (Heliothis virescens = 0.389, H. zea = 0.327, Lygus hesperus = 0.256) but others had very low values (B. germanica = 0.015, M. persicae = 0.000). The ability of some pests to readily evolve pesticide resistance, even though they display little or no electrophoretic heterozygosity, shows that this type of genetic variation is not a prerequisite for resistance evolution. Genetic variation in tolerance to pesticides is required for evolution of resistance, but it has rarely been measured (Roush & McKenzie, 1987; Tabashnik & Cushing, 1989; Tabashnik, 1995). Could intrinsic differences in genetic variation influence resistance evolution? Single-locus population genetics theory predicts that the rate of evolution of resistance increases approximately linearly with the logarithm of initial frequency of an R allele (May & Dobson, 1986). Large differences in initial frequency of an R allele have relatively small effects on rates; a 1000-fold difference between initial frequencies of an R allele in a pest (10 -3) and a natural enemy (10 -6) would lead to rates of resistance evolution twice as fast in the pest as in the natural enemy. Reducing the initial R allele frequency from 10 -3 to 10 -4 or 10 -5 in simulations of a one-locus model had little effect on projected rates of resistance evolution for most of the species of natural enemies of apple pests that were considered (Tabashnik & Croft, 1985). Most economically significant cases of pesticide resistance are thought to be under monogenic control, but there are also many examples of polygenic resistance (Roush & McKenzie, 1987; Tabashnik & Cushing, 1989). According to quantitative genetic theory, the rate of increase in pesticide tolerance would be directly proportional to the additive genetic variance (Via, 1986). Therefore, large differences in additive genetic variance would have a major impact on resistance evolution. In laboratory selection for resistance, natural enemies often do not respond readily (Hoy, 1990; Johnson & Tabashnik, 1994), which provides indirect support for the hypothesis that insufficient genetic variation limits resistance evolution in natural enemies. Laboratory selection programs achieved resistance levels sufficient to enable survival at recommended field rates of pesticide in only 22% of studies with parasitoids and in 68% of studies with predators (Johnson & Tabashnik, 1994). Estimates of heritability, which is the proportion of total phenotypic variance accounted for by additive genetic variance, are available for only a tiny fraction of the pesticide selection experiments reported. In this meager sample, the mean realized heritability of resistance for six pests (0.30, n = 14 cases; Omer et al., 1993) was greater than the maximum value reported for three natural enemies (range = -0.002 to 0.27, mean = 0.11, n = 13 cases; Johnson & Tabashnik, 1994). To summarize, natural enemies (particularly parasitic hymenopterans) may have less allozymic heterozygosity than pests have, but among herbivores this index of genetic

Chapter 24 Evolutionof Pesticide Resistance in Natural Enemies variation is not well correlated with the ability to evolve pesticide resistance. The extent of genetic variation in pesticide susceptibility in pest and in natural-enemy populations has not been characterized in a way that enables rigorous comparison between the two groups. However, relatively slow responses of natural enemies to laboratory selection for resistance in some cases suggest that limited genetic variation may sometimes contribute to the failure of natural enemies to evolve resistance in the field. Fitness Cost It is often presumed that in the absence of pesticides, a resistant individual is less fit than a susceptible individual is. If this fitness cost of resistance were substantially greater for natural enemies than for pests, it might retard evolution of resistance in natural enemies. Review of data available for pests suggests that the fitness cost is not generally large, but it may depend on the nature of the resistance mechanism (Roush & McKenzie, 1987). Studies of the predators Metaseiulus occidentalis and C. carnea and the parasitoid Anisopteromalus calandrae show little or no fitness cost associated with resistance (Roush & Hoy, 1981; Roush & Plapp, 1982; Grafton-Cardwell & Hoy, 1986; Baker et al., 1998). Likewise, Baker (1995) found that in two hymenopteran parasitoids, resistance to malathion was stable in the absence of exposure to insecticides. Stability of fenvalerate resistance in the leafminer parasitoid Diglyphus begini was not less than that in its leafminer host (Spollen et al., 1995). Additional data are needed to evaluate this hypothesis more thoroughly. Population Ecology The concept underlying the population ecology hypothesis is that pesticide resistance evolves more readily in pests than in natural enemies because of differences in population ecology. There are several specific hypotheses under the general category of differences in population ecology: 1. Pests evolve resistance more readily because natural enemies suffer from food limitation following insecticide treatments (Huffaker, 1971; Georghiou, 1972) 2. Pests evolve resistance more readily because of differences between pests and natural enemies in life history traits (Croft, 1982; Tabashnik & Croft, 1985) 3. Pests evolve resistance more readily because they are more exposed to pesticides than natural enemies are (Croft & Brown, 1975) 4. Pests evolve resistance more readily because of differences between pests and natural enemies in their genetic systems (e.g., ploidy level) As with preadaptation hypotheses, each hypothesis has two parts: (1) there is some difference in population ecol-

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ogy between pests and natural enemies, and (2) the difference enables pests to evolve resistance more readily than do natural enemies.

Food Limitation The food limitation hypothesis is based on the population dynamics of interactions between natural enemies and pests (Huffaker, 1971; Georghiou, 1972; Croft & Brown, 1975; Tabashnik, 1986). The idea is that the few resistant pests surviving an initial pesticide treatment will have an abundant food supply (the crop). In contrast, resistant natural enemies surviving treatment will find their food supply (prey or host) severely reduced. Thus, resistance evolves more slowly in natural enemies because they starve, emigrate, or have reduced reproduction following treatments that eliminate much of their food supply (Tabashnik, 1986). Pesticide treatments can reduce the food supply of natural enemies while leaving the pests' food supply intact. Thus, there is little question that pests and natural enemies differ in the way in which their food supply is affected by pesticides. It is difficult to determine, however, the extent to which natural-enemy populations are limited by the availability of prey or hosts after pesticide treatments. Pesticide applications reduce natural-enemy populations, but in most cases, direct effects of the pesticides on a natural enemy are confounded with indirect effects of the pesticides on the natural enemy's food supply. Further, the effect of food limitation on a natural enemy's ability to evolve resistance cannot be determined easily in the field. The food limitation hypothesis could be tested directly by contrasting responses to pesticide treatments in a natural-enemy population feeding on a susceptible strain of a pest versus a population of the same natural-enemy feeding on a resistant strain of the pest. The food limitation hypothesis predicts that pesticide resistance will evolve in the latter case, but not in the former. To our knowledge, this type of experiment has not been performed. Here we review other experimental, historical, and theoretical evidence to evaluate the food limitation hypothesis. If food limitation is a major factor slowing evolution of resistance in natural enemies, then one could predict that 1. Natural enemies will evolve resistance readily when provided with abundant food in artificial selection programs. 2. Natural enemies that use food sources not reduced by pesticides will evolve resistance more readily than do natural enemies that specialize on susceptible pests killed by pesticides. Food sources not reduced by pesticides include plants and pests that are not killed because they are protected from pesticide exposure, naturally tolerant, or resistant.

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Successful laboratory selection for pesticide resistance in natural enemies (Croft & Strickler, 1983; Hoy, 1985, 1990; Croft, 1990; Johnson & Tabashnik, 1994) provides some support for the food limitation hypothesis. However, as noted above earlier, laboratory selection may not produce high levels of resistance in natural enemies as readily as in pests. Such differences in the level of resistance achieved in pest and natural-enemy species may be due to intrinsic limitations of natural enemies (see earlier section on differential preadaptation); or to technical problems associated with sampling, rearing, and selecting large numbers of natural enemies. We are aware of only one study that directly compared evolution of pesticide resistance in a pest and its natural enemy in the laboratory. Morse and Croft (1981) compared responses to selection for resistance to azinphosmethyl in predatory mite Amblyseius fallacis and its prey Tetranychus urticae. A susceptible strain of the predator initiated from only a few individuals did not evolve resistance after seven selections. In contrast, a composite susceptible strain, initiated with 600 adult females from three predator strains, evolved 80-fold resistance in 22 selections. In a separate, but parallel experiment, a susceptible noncomposite strain of the pest showed a 20-fold increase in LCs0 in 22 selections. In the only experiment to compare resistance evolution in the predator and in the prey with susceptible strains of both species in contact, the composite strain of the predator evolved 80-fold resistance whereas the pest strain evolved only 5-fold resistance. These results suggest that the pest did not evolve resistance more readily than its predator, but interpretations are complicated by several factors. First, a noncomposite pest strain evolved resistance more readily than a noncomposite predator strain. Second, even though the proportional increase in LCs0 was higher for the predator than for the pest in some experiments, the final LCs0 after selection was always higher for the pest because of the pest's initially higher LCso. Third, the food limitation hypothesis was not tested directly because predators fed on leaf nectaries and survived even in the absence of prey. Thus, it was not possible to determine if lack of food would retard the evolution of resistance in the predator. The ability of phytoseiid mites to subsist on plant materials and their ability to evolve resistance in the field (Georghiou, 1972; Croft & Brown, 1975) is consistent with the second prediction from the food limitation hypothesis. Also consistent with this prediction is the general pattem that natural enemies usually become resistant only after their prey or host evolves resistance (Georghiou, 1972; Croft & Brown, 1975; Tabashnik & Croft, 1985). Rosenheim and Hoy (1986) concluded that food limitation was not a key factor affecting resistance evolution in Aphytis melinus, an aphelinid parasite of the Califomia red

scale [Aonidiella aurantii (Maskell)]. They noted that a nonresistant host population can survive pesticide applications if it is not contacted by treatments or if it is naturally tolerant. Thus, treating the periphery of citrus trees with dimethoate to control citrus thrips or with chlorpyrifos to control lepidopteran pests should not severely reduce populations of Califomia red scale, which are distributed throughout the tree. In addition, California red scale populations are normally tolerant of the relatively low concentrations of dimethoate used to suppress citrus thrips. Therefore, food limitation should not restrict the evolution of resistance to dimethoate or chlorpyrifos in Aphytis melinus. Conversely, food limitation should slow evolution of resistance in A. melinus to carbaryl, malathion, and methidathion because these insecticides are used to control scales. Analysis of ranges in LCs0 values showed that resistance in A. melinus to dimethoate and chlorpyrifos was not consistently greater than resistance to carbaryl, malathion, and methidathion. These results support the conclusion that food limitation was not a major determinant of rates of resistance evolution in A. melinus. Rosenheim and Hoy (1986) note that this is not a strong test of the hypothesis because many factors other than food limitation (e.g., crossresistance and variation among insecticides in the duration and extent of use) could have affected the outcome. The extremely high resistance to malathion found in the parasitoid Anisopteromalus calandrae is consistent with the food limitation hypothesis because in this case, the host [Sitophilus oryzae (L.)] is protected from exposure to malathion by feeding inside grain kernels during its immature stages (Baker & Weaver, 1993; Baker & Throne, 1995). Substantial resistance to malathion in the warehouse pirate bug, Xylocoris flavipes (Reuter), also fits the food limitation hypothesis, because this predator's prey are highly resistant to malathion (Baker & Arbogast, 1995). Mathematical models have been used to project the potential impact of food limitation on population dynamics and ability to evolve pesticide resistance of natural enemies. According to the Lotka-Volterra equations of predatorprey population growth, equivalent pesticide-caused mortality will suppress a predator population more than that of its prey (Wilson & Bossert, 1971). This occurs because the predator's birth rate and the prey's death rate are proportional to the product of the population sizes of both species. In contrast, the predator's death rate and the prey's birth rate are not affected by the population size of the other species. Thus, a pesticide treatment that kills 90% of predator and prey populations reduces the predator's birth rate and the prey's death rate by a factor of 100, but reduces the predator's death rate and the prey's birth rate only by a factor of 10. More refined models also show that naturalenemy populations are more severely suppressed by pesti-

Chapter 24

Evolution of Pesticide Resistance in Natural Enemies

cides than are pest populations, even though the immediate mortality is similar for both populations (Waage et al., 1985). Does suppression of natural-enemy populations affect their ability to evolve resistance? May and Dobson (1986) emphasized the general distinction between overcompensating and undercompensating density dependence. Pests generally rebound above their long-term average or equilibrium levels following pesticide treatments and thus show overcompensating density dependence. In contrast, natural enemies recover slowly, showing undercompensating density dependence. Undercompensating density dependence reduces the average population size, thereby increasing the extent to which immigration of susceptible individuals is expected to slow evolution of resistance (Comins, 1977; Taylor & Georghiou, 1979; Tabashnik & Croft, 1982). So, in the presence of immigration by susceptibles, pests with overcompensating density dependence will evolve resistance faster than natural enemies with undercompensating density dependence (May & Dobson, 1986). Simulation studies of 12 natural enemies of apple orchard pests showed that incorporation of a simplified version of the food limitation hypothesis substantially improved the correspondence between predicted and reported times for resistance evolution (Tabashnik & Croft, 1985). In this analysis, natural enemies were assumed to begin evolving resistance only after their prey or host had become resistant. Although results supported the food limitation hypothesis, this approach oversimplified dynamic ecological and evolutionary processes. Other simulation studies included the evolutionary potential for resistance in both predator and in prey, as well as coupled predator-prey population dynamics (Tabashnik, 1986). The key assumption of these simulations was that low prey density reduced the predator's rates of consumption, survival, and fecundity. Predator functional response and the effects of food shortage on predator survival and fecundity were based, in part, on experimental data from mites (Dover et al., 1979). The predator and prey were assumed to have equal intrinsic tolerance and equal genetic potential for evolving resistance. However, intensive pesticide use caused rapid resistance evolution in the pest (prey), but suppressed resistance evolution or caused local extinction of the predator. These theoretical results imply that food limitation is sufficient to account for pests' ability to evolve pesticide resistance more readily than natural enemies evolve resistance. In summary, pesticide treatments reduce the food supply of natural enemies more than that of pests. Severe reductions in food supply can slow resistance evolution in natural enemies. Indirect support for the food limitation hypothesis is provided by the success of laboratory selection programs in which natural enemies are provided abundant food, by

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the general trend that natural enemies evolve resistance in the field only when their prey or hosts are resistant or are protected from pesticide exposure, and by theoretical models. Food limitation, however, does not appear to explain resistance evolution in Aphytis melinus. Direct tests of this hypothesis are needed.

Life History Traits Life history traits include number of generations per year, rate and timing of reproduction, survival, developmental rate, and sex ratio. Theoretical work and historical patterns suggested that the rate of resistance evolution increases as reproductive capacity, particularly the number of generations per year, increases (Tabashnik & Croft, 1982, 1985; Georghiou & Taylor, 1986; May & Dobson, 1986). If the number of generations per year is consistently higher for pests than for natural enemies, then this might explain why pests evolve resistance more readily than do natural enemies. The median number of generations per year, however, is less for pests than for natural enemies (Stiling, 1990). Further, analysis of extensive databases and re-evaluation of relevant theory suggest that there is no simple relationship between generations per year and rate of resistance evolution (Rosenheim & Tabashnik, 1990; 1991, 1993). Thus, available evidence refutes the idea that pests become resistant faster because they have more generations per year than natural enemies have. Differences between pests and natural enemies in other life history traits may affect resistance evolution. For example, pests generally have higher fecundity (Stiling, 1990) and may maintain larger populations in treated habitats (Croft & Tabashnik, 1990) compared with natural enemies.

Exposure The rate of resistance evolution is a function of selection intensity, which is determined in part by extent of exposure to pesticides. Croft and Brown (1975) speculated that natural enemies are often less intensively selected than pests are because pesticides are directed at pests; natural enemies contact pesticides only insofar as they occupy the same habitat as their prey or host. However, mobile predators and parasites might pick up more toxicant and thus suffer greater mortality from residual deposits than would sedentary pests in the same habitat (Croft & Brown, 1975; see also Johnson & Tabashnik in Chapter 13). Evaluation of these hypotheses requires detailed information about exposure to pesticides in the field (e.g., the proportion of the population exposed, levels and duration of exposure in treated habitats, and gene flow between treated and untreated habitats). Because most of this infor-

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mation is not available, much empirical work is needed to assess the effects of pesticide exposure on resistance evolution in pests versus natural enemies.

occurs. Although compelling, this hypothesis is completely untestable.

SUMMARY AND IMPLICATIONS

Genetic Systems Most evolutionary considerations about pesticide resistance are based on the assumption that organisms are diploid and sexually reproducing, but a variety of genetic systems occur among insects and mites. Differences in genetic systems between pests and natural enemies could influence their relative ability to evolve resistance. For example, hymenopteran insects are haplodiploid. In one modeling study, however, resistance evolved faster under haplodiploidy than under diplodiploidy (Horn & Wadleigh, 1988), which suggests that haplodiploidy does not slow evolution of resistance in hymenopteran parasitoids. Phytoseiid predatory mites have various genetic systems including thelytoky (females only), parahaploidy (embryos of both sexes are diploid, but males lose one chromosome set during embryonic development), and perhaps true arrhenotoky (unfertilized eggs produce haploid males and fertilized eggs produce diploid females) (Hoy, 1985). Parahaploid phytoseiids such as Typhlodromus occidentalis and Phytoseiulus persimilis Athias-Henriot may have some advantages of haploidy (exposing haploid individuals to selection) and diploidy (recombination) (Hoy, 1985). This could help to explain why phytoseiids evolve resistance to pesticides more readily than do other natural enemies, but it does not support the idea that the genetic systems of natural enemies retard their resistance evolution. Related factors that could affect evolution of resistance in pests and in natural enemies are the extent of sexual versus asexual reproduction, inbreeding, and sociality. Social insects would not be expected to evolve resistance readily because they have small effective population size (few reproductives) and their reproducing individuals usually have limited exposure to pesticides. These factors may explain the paucity of documented cases of resistance in social Hymenoptera and Isoptera insects (Georghiou, 1981), many of which are pests. They do not help to explain the lack of resistance in parasitic hymenopterans. In summary, genetic systems and related factors may influence resistance evolution in pests and natural enemies. It does not appear, however, that there are consistent differences in these traits that would favor resistance evolution in pests compared with that of natural enemies. Perversity of Nature The perversity of nature hypothesis states that the worst possible outcome is for pests to evolve resistance more readily than natural enemies do; therefore, this is what

The hypotheses proposed to explain the scarcity of documented cases of resistance in natural enemies are not mutually exclusive. The relative importance of each factor may vary among species and pesticides. Several factors may act jointly in some cases. Thus, there may be no single, general explanation. Nonetheless, review of the available evidence casts doubt on some hypotheses, supports others, and indicates potentially productive avenues for further research. Resistance to pesticides in pest populations is probably more likely to be documented than is natural-enemy resistance, but the magnitude of this effect is difficult to measure. Bioassays comparing interpopulation variation for several pests and natural enemies from a given crop and region could help to assess the influence of bias in documentation. Available data show that natural enemies possess the detoxification enzyme systems found in pests. The intrinsic levels of detoxification enzymes are not consistently higher for pests than for natural enemies. When pests have higher intrinsic levels of detoxification enzymes than natural enemies have there is little evidence showing that this difference contributed to faster evolution of resistance in the pest. Versions of the preadaptation hypothesis based on intrinsic differences in detoxification ability thus appear to have limited power to explain differences between pests and natural enemies. Differences in intrinsic pesticide tolerance between pests and natural enemies are difficult to assess. Surveys suggest that intrinsic pesticide tolerance is not consistently higher for pests than for natural enemies, but comparative data are limited and may be biased. Higher intrinsic tolerance in pests could account in part for more documented cases of resistance in pests, particularly if the criteria for resistance include the ability to survive field applications of pesticides. Lack of genetic variation for pesticide tolerance in natural enemies could also retard their evolution of resistance. This facet of the preadaptation hypothesis needs investigation. Similarly, more data are needed to determine whether fitness costs associated with resistance are substantially lower for pests than for natural enemies. Indirect evidence suggests that differences in population ecology are important in slowing resistance evolution in natural enemies relative to pests. Experiments are needed to assess the extent to which natural-enemy populations are suppressed by food limitation, and how such suppression affects their ability to evolve resistance. Experiments are needed also to measure exposure to pesticides in pests and in natural enemies. Differences between pests and natural

Chapter 24

Evolution of Pesticide Resistance in Natural Enemies

enemies in number of generations per year do not explain the relative scarcity of resistance in natural enemies, but differences in other life history traits may be important. Differences in genetic systems and related factors are not likely to explain why pests evolve resistance more readily than do natural enemies. We think that food limitation due to reduction in host or prey populations by pesticides is a major factor influencing natural-enemy populations. If this is true, then there are some important implications for management. First, many natural enemies should evolve resistance when provided abundant food in artificial selection programs (Hoy, 1985, 1990; Croft, 1990; Johnson & Tabashnik, 1994). Second, intensive pesticide use may disrupt biological control, even if the natural enemies are not susceptible m either because of natural tolerance or resistance (Tabashnik, 1986; see also Johnson and Tabashnik in Chapter 13). Thus, to maintain effective biological control, use of selective pesticides should be sparing and judicious.

Acknowledgments We are grateful to K. Theiling and B. Croft for providing a preprint of their review paper and references from their extensive natural-enemy database, and to J. Baker for providing reprints and preprints of his exciting work. The thoughtful comments of J. Rosenheim, B. Croft, K. Theiling, H. van de Baan, C. Bach, M. Caprio, A. Moore, and L. Yudin improved the manuscript. We thank N. Finson, D. Horn, T. Sparks, and S. Toba for their assistance. We also thank our colleagues for faithfully citing this chapter during its long dormancy. This work was supported by several USDA grants (USDA grant HAW00947H and grants from the following USDA programs: Special Grants in Tropical and Subtropical Agriculture, Western Regional Pesticide Impact Assessment Program and Integrated Pest Management) and a Fujio Matsuda Scholar Award from the University of Hawaii Foundation.

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1251 Hypovirulence to Control Fungal Pathogenesis DENNIS W. FULBRIGHT Department of Botany and Plant Pathology Michigan State University East Lansing, Michigan

INTRODUCTION

quarantine laws that certainly must have prevented other biological invaders from moving to new islands and continents, but the laws did not stop all invaders as witnessed by the development of other major disease epidemics throughout the world (Scheffer, 1997). However, another maybe even more important lesson has developed from the chestnut blight epidemic. This lesson is about the natural biological constraints that even the most destructive pathogen must endure to maintain its longterm predominance on a particular host. Not long after the dissemination of chestnut blight into Europe, just prior to World War II, European chestnut trees also began dying rapidly of chestnut blight. However, about 20 years after the pathogen's introduction, sucker sprouts were observed to survive infection; chestnut trees, from these surviving sprouts, began to reclaim the landscape, and once again, chestnut products (wood and nuts) became an important commodity in the Mediterranean region of Europe (Heiniger & Rigling, 1994). To understand how these European chestnut trees survived meant that more information was needed if we were to understand the constraints faced by the pathogen. Yet, little work was being done on chestnut blight because it was such a devastating disease; many government agencies and researchers had given up on research as a being waste of time and money in the United States and elsewhere. Full credit must be given to early French researchers, including Jean Grente and co-workers who were able to determine the overall mechanism of the European chestnut tree's recovery (Grente & Berthelay-Sauret, 1978). The researchers applied fungal genetic techniques and concepts to the system to understand what might be happening on the surviving trees while pursuing applied biological control experi-

Nearly a century ago chestnut blight struck the Eastern forests of North America initiating the most destructive forest epidemic in recorded history (Anagnostakis, 1982). The pathogen, earlier known as Endothia parastica and later called Cryphonectria parasitica, was unleashed in New York City, having hitchhiked to North America on Japanese chestnut trees, Castanea crenata, a species more resistant to infection by the fungal pathogen than North America's native species the American chestnut tree, Castanea dentata (Milgroom et al., 1997). The pathogen is a wound-infecting, stem-cankering ascomycete that produces masses of sticky asexual conidia throughout the summer and light, airborne ascospores in the late summer each year until the stem is girdled and the bark is killed (Fig. 1). Because it is not a good saprophyte, where or how Cryphonectria parasitica survives after it has killed most of the chestnut trees in a localized area is not entirely clear. It is known to reinfect young sucker sprouts emerging from the root collar of infected or dying individuals and it can be found on certain oak species in some areas (Schwadron, 1995). It is well known that some chestnut trees will sucker from the root collar rapidly producing new shoots that can become reinfected and if they attain much size; the pathogen initiates continuous rounds of infection on the sprouts. The introduction of chestnut blight through the reckless importation of foreign species from one continent to another taught us early about the accidental importation of harmful species and the biological disaster that can develop if the biological lessons of competition and host-pathogen interactions are ignored. The chestnut blight disaster led to

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FIGURE 1 Naturally occurring lethal-type chestnut blight canker expanding through the bark. (A) Before outer bark removed and (B) outer bark removed. Canker probably initiated at the branch scar.

ments to determine if the system could be exploited at nonrecovering blighted locations. They discovered that the chestnut blight pathogen on infected but surviving trees was reduced in aggressiveness, and it appeared that the natural defense mechanisms of the tree were able to stop or slow the infection to the point where the tree could compartmentalize the infection to just the outer bark. This caused scaring and some cambial damage, with the subsequent development of wound tissue and callus; however, overall, the trees remained healthy and productive. This remarkable research, in terms of deciphering the the biological puzzle presented to the researchers, should be a highlight in biological control treatises. The chestnut blight pathogen in this state of reduced aggression was morphologically distinct from the aggressive form of the pathogen; in culture it was white instead of displaying its usual diagnostic orange pigmentation, was reduced in sporulation, and had a slower growth rate. That Grente and Berthelay-Sauret recognized this new form of the pathogen

as Endothia parasitica and not another canker-inducing species or a weak, secondary pathogen infecting stressed trees was a great achievement in itself, but not as great as the next. Subsequently, it was soon discovered that when this less aggressive, morphologically altered strain came into hyphal contact with aggressive strains of the chestnut blight fungus, the traits characteristic of the less aggressive strain transferred to the aggressive strain effectively reducing its virulence in the tree. These strains were not avirulent and did not become nonpathogenic on the chestnut; it was clear that they were still capable of recognizing and infecting the host, but where defense mechanisms of the tree species had earlier been ineffective, they were now effective in reducing canker expansion on the tree. Grente termed this natural control of chestnut blight "hypovirulence" and he proposed that a genetic factor in the cytoplasm of the hypovirulent strain was responsible for the hypovirulent phenotype (Grente & Berthelay-Sauret, 1969). He theorized that this cytoplasmic factor, when transferred to virulent strains from hypovirulent strains during hyphal anastomosis, was responsible for the transmissible nature of the genetic traits associated with hypovirulent strains. In North America, hypovirulence did not develop 20 years after the pathogen was introduced, or if it did it was not biologically successful and therefore not recognized. By the 1950s, it was estimated that over 3 billion chestnut trees were destroyed by the pathogen or prematurely harvested before blight infection destroyed the trees' value. While initial research in the early part of the century had provided great detail as to the life cycle and movement of the fungus, it did little to save trees. Breeding programs designed to capture the natural resistance in the Asian species' background initially failed to provide a disease-resistant tree with the important characteristics of the American species, such as girth and height. Forest management strategies such as eradication also failed. Except for uninfected trees that had been planted outside of the natural range of the native species, mature, nut-beating chestnut trees were becoming extremely rare in North America. By the 1960s, the Eastern forests only harbored remnant sprouts growing from the root collars of blight-killed trees, offering hope that one day the tree could be brought back as a co-dominant forest species. In the United States, research on and scientific interest in chestnut and chestnut blight waned for decades until two events occurred in the 1970s, one growing out of the other. Researchers at the Connecticut Agricultural Experiment Station, a research institute that had maintained an active chestnut tree breeding/research program, discovered Grente's work and began to investigate the cytoplasmic factor and its potential for controlling chestnut blight of American chestnut in North America. Van Alfen et al. (1975) soon discovered that the European hypovirulent strains could transfer the hypovirulent phenotype to North

Chapter 25

Hypovirulence to Control Fungal Pathogenesis

American virulent isolates infecting American chestnut. The American tree responded similarly to the European tree in presenting a defense reaction to the invading hypovirulent strain. This was followed by an astute observation. Newspaper coverage of the Connecticut research was read by a nature center volunteer near Grand Rapids, Michigan, who, while cross-country skiing, found diseased American chestnut trees with callusing cankers similar to those shown in the newspaper article. She sent the cankers to Connecticut and soon it was confirmed that hypovirulent strains were present in Michigan (Fulbright et al., 1983). The hypovirulent isolates recovered from the callused cankers on the Michigan trees were not typical of the hypovirulent strains isolated in Europe; they were orange instead of white and produced more spores in culture than did European hypovirulent strains (Elliston, 1978). Since then, hypovirulent strains have been found in other regions of North America, including New Jersey (Hillman et al., 1992) Ontario (McKeen, 1995), and other isolated locations (Jaynes & Elliston, 1982), but none are associated with as much chestnut survival or are as geographically widespread as in Michigan.

SEARCHING FOR THE CAUSE OF HYPOVIRULENCE The cytoplasmic factor associated with hypovirulence in chestnut blight was determined by Day et al. (1977) to be double-stranded RNA (dsRNA) molecules. This was not too surprising because the genetic component of nearly all fungal viruses is dsRNA. What was surprising was that there were no virions, icosehedral or other virus-like particles present in the hypovirulent strains. Instead, dsRNA was associated with pleiomorphic vesicles presumably of fungal origin (Dodds, 1980). At first there seemed to be a perfect correlation between the presence of dsRNA in the cytoplasm and the hypovirulent phenotype. Whether dsRNA was moved into a new strain via hyphal fusion or removed by curing agents, the characteristics of hypovirulent strains were gained or lost, respectively. It became apparent that the simple presence of dsRNA could not account for the dramatic culturable and pathogenic differences observed among dsRNA-containing strains. For example, C. parasitica strains would lose pigmentation when infected with various dsRNA genomes from Europe, but never lost pigmentation when infected with isolates of Michigan origin. Some hypovirulent strains grew almost as fast as nondsRNA infected strains, yet still retained a reduction in the ability to establish cankers on the tree host. A few strains regardless of origin were so debilitated in culture that it was a wonder the isolate could have existed in nature at all (Elliston, 1978).

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Elliston (1985) was the first to attempt to ascribe some of the obvious cultural differences to the dsRNA infection status of the isolates. He postulated that one of the reasons for phenotypic variation existing in the hypovirulent strains could be due to E. parasitica strains being infected with more than one dsRNA genome. Mixed virus infections in one fungal thallus can be difficult to detect. While most of the dsRNA molecules are of different size classes, there is enough overlap in the dsRNA genome size that one dsRNA molecule could easily mask the presence of another on agarose or polyacrylamide gels. Elliston determined through single-conidial isolation techniques that one of the first Michigan hypovirulent strains isolated was, in fact, doubly infected. By effectively segregating the cytoplasm through asexual spore cultures, he was able to detect the singular effect of each dsRNA molecule on the fungal host. One dsRNA genome had a greater effect on the fungal culture morphology than the other had, leading to speculation that different dsRNA genomes have separate, unequal effects, that were responsible for different outcomes of fungal infection on trees. In a similar experiment, where two dsRNAs were both transferred into the same genetic background, Smart and Fulbright (1995) found that these coinfected strains were markedly more reduced in virulence when compared with strains infected with each virus separately. This indicates that if two viruses are released separately in a stand of trees, the fungal strains that become infected with both dsRNA molecules may result in a third type of effect on the pathogen. Other studies (Fulbright, 1985) suggested that a cytoplasmic genetic factor in addition to dsRNA might be involved in the generation of the hypovirulent phenotype. Another type of hypovirulence first described in Michigan did not appear to be associated with dsRNA (Mahanti et al., 1993). Additional studies indicated that mitochondria dysfunction may play a role in the hypovirulent phenotype of some hypovirulent strains. Transmissible from strain to strain via hyphal fusion, the mitochondrial hypovirulent phenotype is maternally inherited, which delineates it from dsRNA-associated hypovirulence. The only dsRNA known to be maternally inherited in C. parasitica has been a dsRNA associated with the mitochondria (Polashock & Hillman, 1994) and genetically engineered transgenic hypovirulent strains (Anagnostakis et al., 1998). In the dsRNA-free hypovirulent strains, most of the respiratory activity is through the alternative oxidase pathway whereby the fungal thallus is cyanide resistant. Many of the strains showing these traits began to deteriorate on subculturing to fresh medium. This process has been observed before in other fungi and is described as senescence. It was speculated that mitochondrial DNA (mtDNA) mutations might be involved in this form of hypovirulence. To explore this possibility, mutations that cause respiratory defects were induced and selected in Ep155, a stable viru-

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lent strain used in most laboratories studying chestnut blight. The study found that a cytoplasmically transmissible, hypovirulent phenotype could be selected (MonteiroVitorello, 1995). If such mutants can be selected in C. parasitica, it is possible that they might be selected in other fungal pathogen species giving rise to the possibility of inducing a hypovirulent phenotype where dsRNAs are lacking.

HYPOVIRUSES While mitochondrial hypovirulence appears to play a role in the biological control of chestnut blight in specific stands of American chestnut trees in Michigan and Ontario (McKeen, 1995), the preponderance of hypovirulent strains found in surviving chestnut stands in Europe and North America appears to be dsRNA associated. Much is now known about these naked dsRNA genomes in terms of their structure, function, and genetic relatedness. Studies were initiated on three dsRNA genomes, one from Europe (CHV1-Ep713) (Choi & Nuss, 1902), the second from New Jersey (CHV2-NB58) (Hillman et al., 1992), and a third from Michigan (CHV3-GH2) (Fulbright, 1990). The result was the establishment of the first virus family without structural proteins, Hypoviridae (Hillman et al., 1995). Those dsRNA genomes that (1) reduced virulence, (2) were not associated with viral-encoded coat proteins, and (3) showed some nucleic acid or enzymatic protein motiff related to the type dsRNA of the Hypoviridae family were called hypoviruses. The dsRNA from isolates that are obviously hypovirulent but not well characterized are usually referred to as hypovirus-like dsRNAs to separate them from the dsRNAs that have been given species names such as CHV1-Ep713. This is the type species for the virus family and the designation indicates it is Cryphonectria hypovirus number 1 from the fungal isolate Ep713. Hypovirus CHV 1-Ep713 has been instrumental in developing our understanding of hypovirulence and the symptoms associated with hypovirulence, that is, how fungal viruses may interfere with important functions of the pathogen such as sporulation, growth rate, and virulence. It was intuitive to believe that a substance that the fungus normally produced was now lacking; and, in fact, studies showed that many potential pathogenicity or virulence compounds including cutinase (Varley et al., 1992), laccase (Rigling, 1995), oxalic acid (Vannini et al., 1993), polygalacturonase (Gao et al. 1996), and others (Kazmierczak et al., 1996) were down regulated or lacking altogether. So far, none of these interesting enzymes or compounds has proved to be an obvious pathogenicity factor in the C. parasitica/Castanea pathosystem and the search for such a fungal product continues. As part of that continuing process, Nuss (1996) and

coworkers concentrated their studies on G proteins (guanine nucleotide binding proteins), a group of regulatory proteins that play an essential role in cellular response to environmental stimuli (Gao & Nuss, 1996). One such protein, CPG-1, was found to be reduced in accumulation during hypovirus infection, and strains genetically disrupted for this protein also shared many of the characteristics of hypovirus infection. This work suggested that hypoviruses may suppress or interfere with virulence by way of disrupting one or more of the fungal-signaling components of the G protein pathway.

BIOLOGICAL CONTROL The most exciting aspect of the natural development of hypovirulence is that it has allowed researchers to focus on the biological constraints fungal pathogens may confront in a living substrate. Hypovirulence, initially found as a naturally occurring biological control of chestnut blight, has now been part of experimental and practical application for almost 40 years. In Europe, chestnut farmers can purchase a tube of "hypovirulence paste" that can be applied to trees displaying the types of cankers usually associated with virulent strains (Heinger & Rigling, 1994). It even can be applied to grafting wounds to prevent virulent strain infection of the healing graft union. Introducing any biological control into an environment managed toward crop production means that conditions at the introduction foci are generally manipulated toward plant production and away from pathogen or microorganism enhancement. Introducing hypovirulence, a form of the pathogen (weakened albeit, but a pathogen nonetheless), means that certain conditions must be manipulated in favor of the pathogen. The colonization of the hypovirulent fungus must be maintained or sustained in such a way that the pathogen ultimately supports itself and disseminates by natural means. After observing Michigan's American chestnut tree stands for 20 years, I am still surprised to see how well hypovirulence has maintained itself (personal observation). Even in extreme drought (1988 and 1998) and extreme winters (1993 and 1994), hypovirulent strains have not disadvantaged their host trees and have not allowed the trees to escape infection. Signs of the fungus can still be found on most trees in a blighted, surviving chestnut stand. The sustainable nature of naturally occurring hypovirulence is the goal of chestnut blight researchers, a goal that has elluded North American researchers to this point. The factors limiting successful establishment of hypovirulent strains are not well enumerated or understood. Concerns usually center around the vegetative compatibility with virulent strains presently in the stand or in the surrounding area. It is widely believed that hypovirus transmission is inhibited among strains heteroallelic for veg-

Chapter 25 Hypovirulenceto Control Fungal Pathogenesis

FIGURE 2 Instrumentsused to make holes in bark around the margin of the virulent cankers have included cordless electric drills, leather punches, and cork borers.

etative incompatibility loci, and these incompatible interactions are responsible for curtailing the rapid dispersal of hypovirulent strains in the natural range of chestnut in Eastern North America (Liu & Milgroom, 1996). These loci appear to have direct roles in blocking nuclear transmission and establishing heterokaryon formation. It appears that only certain vegetative incompatibility loci block hypovirus dispersal while others have no measurable effect. To bypass this potential problem, at least three different strategies have been employed. First, multiple hypovirulent strains have been introduced to a nonrecovering stand, hopefully representing all or most of the various vegetative compatibility groups in the area (Anagnostakis, 1990). A second strategy is to isolate a representative sample of the Cryphonectria parasitica population that is to be treated (Cummings-Carlson et al., 1998). These strains can be tested to determine the number and type of vegetative compatibility groups that are found at the site. Hypoviruses can then be introduced into these strains through hyphal fusion. The newly infected strains can then be reintroduced back to the location from which the strains were recovered. The third strategy used to bypass vegetative compatibility problems involves recombinant DNA techniques whereby integrated full-length complementary DNA (cDNA) could be found in ascospore progeny that included vegetative compatibility groups of the parental types and the recombinant types (Anagnostakis et al., 1998). Generally, dsRNA genomes are excluded from the ascospore, but the integration event allows virus heritability through the ascospore. Integrated full-length cDNA will generate infectious hypovirus in the cytoplasm, allowing the hypovirus access to new vegetative compatibility groups. Chestnut stands treated using the first two traditional approaches listed earlier are still currently monitored and enough success has been documented at each location that

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these strategies are still recommended when deploying hypovirulence (Anagnostakis, 1990; Cummings-Carlson, 1998). The nontraditional genetically engineered strain was also successfully deployed in a test limited by size and time. One isolate, however, was recovered from a superficial canker that represented a different vegetative compatibility type from that of either transgenic parent. This indicates that the dsRNA was able to appear in a new vegetative compatibility type as predicted by the model. The dsRNA was cytoplasmic and was originally generated from the integrated, full-length hypovirus clone (Anagnostakis et al., 1998). Another important consideration when releasing hypoviruses in chestnut stands involves choosing the proper hypovirus or hypovirus-like dsRNA. If too debilitated, it may reduce the ability of the host fungus to infect the bark of the tree, thereby causing the strain to be lost. The inability of the fungus to sporulate asexually may reduce dissemination of hypovirulence. In a treated stand of American chestnut trees, one particular debilitating dsRNA genome was introduced for three consecutive years, after which it could only be found in 36% of the bark samples assayed. Another hypovirus, one that could be found in a majority of its asexual spores, was released and after 2 years was found in the isolates recovered from 38% of the bark samples tested. The first debilitating hypovirus is still present in the pathogen population but at a reduced frequency (Cummings-Carlson et al., 1998).

TREATING CHESTNUT TREES WITH HYPOVIRULENT STRAINS To treat chestnut trees, hypovirulent strains traditionally have been placed around the margins of cankers caused by virulent strains. A hole is made with a cork borer or leather punch in the bark down to the cambium at the canker edge (Fig. 2). The hypovirulent inoculum is placed in the hole and taped to prevent the rapid desiccation of the introduced strain. If the hypovirus or mitochondria transfer to the thallus of the virulent strain inciting the canker, a layer of wound periderm or callus will develop at the margins, walling off the fungus (Fig. 3A to C). Effective treatments generally lead to the eventual closing of the canker when periderm completely covers the exposed wood within 2 or 3 years. The fate of the hypovirulent strain placed around the canker, as well as the fate of the original virulent strain-now hypovirulent, has not been well studied. What appears to be most important is the fate of the hypovirulent-inducing factor, the hypovirus or the mitochondrion. Dissemination through asexual spores requires the development of stroma, which means the hypovirulent strain must maintain enough virulence to continue to grow in the bark (Shain &

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FIGURE 3 Hyprovirulent-treated canker. (A) Swelling canker with older infected rhytidome attached; (B) loosebark removed exposing the callus tissue, (C) slices through the callus layer exposing the living tissue at the edge of the canker, and (D) removal of outer bark shows a "break out" where the fungal thallus has broken through the callus layer. Treatment holes around edge of the canker are still visible.

Miller, 1992). If the strain is too debilitated, it will be lost, if it is too virulent, the strain will be ineffective in stopping the girdling of the stem (Taylor et al., 1998). Many treated cankers end up with "break overs" where at some point around the callus the canker fungus grows over the callus and into healthy tissue (see Fig. 3 D). This is an area that needs to be followed up, because it could be a hypovirulent strain that is continuing to grow, which will mean more hypovirus dissemination through stroma development and asexual spore production. However, it could also mean that parts of the canker-inciting strain did not become infected with the hypovirulent factor, indicating that the current infection may still girdle the stem if not treated again. By using these techniques, the largest stand of mature (>2000 stems) American chestnut trees left in North America near West Salem, Wisconsin, was continually treated for 6 y e a r s - - from 1992 to 1997 (Cummings-Carlson et al.,

1998). Two different hypovirus-like dsRNAs were used in the treatment. Every canker that could be treated was treated using leather punches and the hypovirulent strain made up in an agar slurry. At the beginning of the treatment, the virulent strain in the stand represented a single compatibility group (another was found later). Many of the cankers at this site are producing callus and it appears that some of the trees have cankers in remission. However, many trees are still dying each year. In 1998, treatment was stopped and the fate of the stand will be left to natural hypovirus dissemination.

References Anagnostakis, S. L. (1982). Biological control of chestnut blight. Science, 215, 466-471. Anagnostakis, S. L. (1990). Improved tree condition maintained in two

Chapter 25

Hypovirulence to Control Fungal Pathogenesis

Connecticut plots after treatments with hypovirulent strains of the chestnut blight fungus. Forest Sciences, 36, 113-124. Anagnostakis, S. L., Chen, B., Geletka, L. M. & Nuss, D. L. (1998). Field release of transgenic hypovirulent Cryphonectria parasitica strains demonstrates hypovirus transmission to ascospore progeny, persistance and limited dissemintion. Phytopathology, 88, 598-604. Bissegger, M., Rigling, D, & Heiniger, (1997). Population structure and disease development of Cryphonectria parasitica in European chestnut forests in the presence of natural hypovirulence. Phytopathology, 87, 50-59. Chen, B., Choi, G. H., & Nuss, D. L. (1994). Attenuation of fungal virulence by synthetic infectious hypovirus transcripts. Science, 26, 1762-1764. Choi, G. H., & Nuss, D. L. (1992). Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA. Science, 257, 800803. Cummings-Carlson, J., Fulbright, D., MacDonald, W. L., & Milgroom, M. G. (1998). West Salem: A research update. Journal of American Chestnut Foundation, 12, 24- 26 Day, P. R., Dodds, J. A., Elliston, J. E., Jaynes, R. A., & Anagnostakis, S. L. (1977). Double-stranded RNA in Endothia parasitica. Phytopathology, 67, 1393-1396. Dodds, J. A. (1980). Association of type I viral-like dsRNA with clubshaped particles in hypovirulent strains of Endothia parasitica. Virology, 107, 1-12. Elliston, J. E. (1978). Pathogenicity and sporulation of normal and diseased strains of Endothia parasitica in American chestnut. In W. L. MacDonald, F. C., Cech, & H. C. Smith, (Eds.) Proceedings of the American Chestnut Symposium (pp. 95-100). Morgantown, WV: West Virginia University Books. Elliston, J. E. (1985). Characteristics of dsRNA-free and dsRNA-containing strains of Endothia parasitica in relation to hypovirulence. Phytopathology, 75, 151-158. Elliston, J. E. (1985). Further evidence for two cytoplasmic hypovirulence agents in a strain of Endothia parasitica from western Michigan. Phytopathology, 75, 1405-1413. Fulbright, D. W. (1985). A cytoplasmic hypovirulent strain of Endothia parasitica without double-stranded RNA. Phytopathology (Abstract), 75, 1328. Fulbright, D. W. (1990). Molecular basis for hypovirulence and its ecological relationships. In R. Baker & P. Dunn (Eds.), New directions in biological control (pp. 693-702). New York: Alan R. Liss. Fulbright, D. W., Weidlich, W. H., Haufler, K. Z., Thomas, C. S., & Paul, C. P. (1983). Chestnut blight and recovering American chestnut trees in Michigan. Canadian Journal of Botany, 61, 3164- 3171. Gao, S., Choi, G. H., Shain, L., & Nuss, D. L. (1996). Cloning and targeted disruption of enpg-l, encoding of the major in vitro extracellular endopolygalacturonase of the chestnut blight fungus, Cryphonectria parasitica. Applied and Environmental Microbiology, 62, 19841990. Gao, S., & Nuss, D. L. (1996). Distinct roles for two G protein subunits in fungal virulence, morphology, and reproduction revealed by targeted gene disruption. Proceedings of the National Academy of Sciences, USA, 93, 14122-14127. Grente, J., & Berthelay-Sauret, S. (1969). Pathologie vegetale m L'hypoviruence exclusive, phenomene original en pathologie vegetale. Comptes Rendus de l' Academie Sciences Paris, 268, 2347-2350. Grente, J., & Berthelay-Sauret, S. (1978). Biological control of chestnut blight in France. In W. L. MacDonald, F. C. Cech, & H. C. Smith (Eds.), Proceedings of the American Chestnut Symposium (pp. 3034). Morgantown, WV: West Virginia University Books.

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Heiniger, U., & Rigling, D. (1994). Biological control of chestnut blight in Europe. Annual Review of Phytopathology, 32, 581-599. Hillman, B. I., Tian, Y., Bedker, P. J., & Brown, M. P. (1992). A North American hypovirulent isolate of the chestnut blight fungus with a European isolate-related dsRNA. Journal of General Virology, 73, 681-686. Hillman, B. I., Fulbright, D. W., Nuss, D. L., & Van Alfen, N. K. (1995). Hypoviridae. In F. A. Murphy, et al. (Eds.), Virus taxonomy: Classification and nomenclature of viruses, sixth report of the International Committee on Taxonomy of Viruses. New York: Springer-Verlag. Jaynes, R. A., & Elliston, J. E.(1982). Hypovirulent isolates of Endothia parasitica associated with large American chestnut trees. Plant Disease, 66, 679-772. Kazmierczak, P., Pfeiffer, P., Zhang, L., & Van Alfen, N. K. (1996). Transcriptional repression of specific host genes by the mycrovirus Cryphonectria hypovirus 1. Journal of Virology, 70, 1137-1142. Liu, Y.-C., & Milgroom, M. G. (1996). Correlation between hypovirus transmission and the number of vegetative incompatibility (vic) genes different among isolates from a natural population of Cryphonectria parasitica. Phytopathology, 86, 79-86. Mahanti, N., Bertrand, H., Monteiro-Vitorello, C., & Fulbright, D. W. (1993). Elevated mitochondrial alternative oxidase activity in dsRNAfree, hypovirulent isolates of Cryphonectria parasitica. Physiology and Molecular Plant Pathology, 42, 455-463. McKeen, C. D. (1995). Chestnut blight in Ontario: Past and present status. Canadian Journal of Plant Pathology, 17, 295-304. Milgroom, M. G., Wang, K., Zhou, Y., Lipari, S. E., & Kaneko, S. (1997). Intercontinental population structure of the chestnut blight fungus, Cryphonectria parasitica. Mycologia, 88, 179-190. Monteiro-Vitorello, C. B., Bell, J. A., Fulbright, D. W., & Bertrand, H. (1995). A cytoplasmically-transmissible hypovirulence phenotype associated with mitochondrial DNA mutations in the chestnut blight fungus Cryphonectria parasitica. Proceedings of the National Academy of Sciences, USA, 92, 5935-5939. Nuss, D. L. (1996). Using hypoviruses to probe and perturb signal transduction processes underlying fungal pathogenesis. The Plant Cell, 8, 1845-1853. Polashock, J. J., & Hillman, B. I. (1994). A small mitochondrial doublestranded (ds) RNA element associated with a hypovirulent strain of the chestnut blight fungus and ancestrally related to yeast cytoplasmic T and W dsRNAs. Proceedings of the National Academy of Sciences, USA, 91, 8680-8684. Rigling, D. (1995). Isolation and characterization of Cryphonectria parasitica mutants that mimic a specific effect of hypovirulence-associated dsRNA on laccase activity. Canadian Journal of Botony, 73, 1655-1661. Scheffer, R. P. (1997). Natural history of some destructive diseases: Native plants, alien pathogens. In The nature of plant diseases (pp. 8189). Cambridge University Press. Schwadron, B. A. (1995). Distribution and persistence of American chestnut sprouts, Castanea dentata [Marsh.] Borkh., in Northeastern Ohio woodlands. Ohio Journal of Science, 95, 281-288. Shain, L., & Miller, J. B. (1992). Movement of cytoplasmic hypovirulence agents in chestnut blight cankers. Canadian Journal of Botony, 70, 557-561. Smart, C. D., & Fulbright, D. W. (1995). Characterization of a strain of Cryphonectria parasitica doubly infected with hypovirulence-associated dsRNA viruses. Phytopathology, 85, 491-494. Taylor, D., Jarosz, A. M., Lenski, R. E, & Fulbright, D. W. (in press). Acquisition of hypovirulence in host-pathogen systems with three trophic levels. American Naturalist. Vannini, A., Smart, C. D., & Fulbright, D. W. (1993). The comparison of

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oxalic acid production in vivo and in vitro by virulent and hypovirulent Cryphonectria (Endothia) parasitica. Physiology and Molecular Plant Pathology, 43,443-451. Van Alfen, N. K., Jaynes, R. A., Anagnostakis, S. L., & Day, P. R. (1975). Chestnut blight: Biological control by transmissible hypovirulence in Endothia parasitica. Science, 189, 890-891.

Varley, D. A., Podila, G. K., & Hiremath, S. T., (1992). Cutinase in Cryphonectria parasitica, the chestnut blight fungus: Suppression of cutinase gene expression in isogenic hypovirulent strains containing double-stranded RNAs. Molecular and Cellular Biology, 12, 5394544.

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[261 Controlling Soil-Borne Plant Pathogens T. S. BELLOWS Department of Entomology University of California Riverside, California

INTRODUCTION

ROOT PATHOGENS AND THEIR BIOLOGICAL CONTROL AGENTS

Biological control of soil-dwelling plant pathogens has been the focus of numerous studies, and has been treated in several texts and reviews. As in the case of pathogens of aboveground plant parts, management of soil-borne pathogens occurs at the microbial level (Andrews, 1992). Agents used against these pathogens include both competitive antagonists as well as predators and microbial hyperparasites. Biological control agents for pathogens and nematodes function either by destroying the pest organisms (predaceous and mycoparasitic antagonists), or through competitive exclusion. Competitive exclusion takes place when an antagonist occupies or uses resources in a nonpathogenic manner and in so doing excludes pathogenic organisms, thus preventing the disease. Diseases of roots and subterranean stems are caused by a variety of pathogens. Because of this diversity, the species antagonist to plant pathogens and the mechanisms by which they accomplish their beneficial action are also quite varied. The taxonomic diversity, biology, and use of these antagonists are covered in some detail in several texts and reviews, including Cook and Baker (1983), Parker et al. (1985), Lynch (1987), Campbell (1989), Adams (1990), Hornby (1990), Sayre and Walter (1991), Stirling (1991), Tjamos et al. (1992), and Cook (1993). This chapter introduces briefly some of the antagonists of soil-borne pathogens as representative of the broad taxa that are useful in this field, and then discusses ways in which these antagonists can be employed to bring about biological control of soil-borne plant pathogens.

Handbookof BiologicalControl

Microbial P a t h o g e n s a n d A n t a g o n i s t s Root diseases are caused by a wide variety of fungi and by some bacteria in many crops and plant systems. Biological control agents recognized as significant in suppression of microbial root diseases are largely antagonists that can occupy niches similar to the pathogens and either by natural means or through manipulation outcompete the pathogens in these niches. Antibiotic production is also important in a few cases, as are mycoparasitism and induced resistance. Antagonists are known among bacteria and fungi. Streptomyces scabies, the causative organism of potato scab, is suppressed by naturally occurring populations of Bacillus subtilis (Ehrenberg) Cohn and saprotrophic Streptomyces spp. Other microorganisms recognized as suppressing fungal diseases include species of Pseudomonas and Bacillus. Saprotrophic Fusarium fungi are able to suppress populations of pathogenic Fusarium spp. through competition for nutrients. There are few well-documented cases of induced resistance for soilborne pathogens, and these are mostly of wilt diseases. Examples of organisms that induce resistance in plants include nonpathogenic strains of Fusarium spp., Verticillium spp., and Gaeumannomyces spp. Mycoparasitic flora such as Trichoderma spp., Coniothyrium minitans Campbell, and Sporidesmium sclerotivorum Uecker et al. can be added to soil against fungal diseases. Bacillus spp. and especially Pseudomonas spp. are among

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bacteria that have properties particularly suited to effective suppression of root-infecting pathogens in soil, such as antibiotic production and competition for Fe 3§ ions. Mycetophagous soil amoebae have also been noted feeding on pathogenic fungi. These amoebae generally require moist conditions in which to function, and may be important in natural control of some fungi. Mycorrhizae are nonpathogenic fungi associated with roots in some temperate forest trees (and are often essential symbionts for coniferous tree species). Ectomycorrhizae are mostly basidiomycetes that form a sheath over the root, and hyphae spread out into the soil. These fungi have been studied in relation to nutrient uptake, but they also affect root disease. As they completely enclose the root, they change the quantity and quality of exudates reaching the soil, and consequently roots with mycorrhizae have a rhizosphere flora different from roots lacking these these symbionts (Campbell, 1985). In at least one case, the mycorrhizal fungus Pisolithus tinctorius (Persoon) Coker & Couch, the symbiont sheath is sufficiently thick that it forms a barrier to infection by such pathogens as Phytophthora cinnamomi Rands attacking eucalyptus trees. Other mycorrhizal fungi produce antibiotics effective against P. cinnamomi in plate tests. The intentional manipulation of mycorrhizal fungi for disease control has not been widely implemented, but opportunities for selected uses may be possible (Campbell, 1989).

Plant-Parasitic N e m a t o d e s Plant-parasitic nematodes inhabit many soils and attack the roots of plants. They are affected by a range of natural enemies, including bacteria, nematophagous fungi, and predaceous nematodes and arthropods. There is some limited evidence for virus association with nematodes (Loewenberg et al., 1959), but the etiology of these viruses is not well known (Stirling, 1991). The biologies of natural enemies of nematodes have been reviewed by Sayre and Walter (1991) and Stirling (1991).

Bacteria Affecting Plant-Parasitic Nematodes Several bacterial diseases of nematodes have been reported (Saxena & Mukerji, 1988); other bacteria produce compounds that are detrimental to plant-parasitic nematodes (Stirling, 1991). The most widely studied bacterial pathogen of nematodes are in the genus Pasteuria. Early work was focused on P. penetrans (Thorne) Sayre & Starr sensu stricto Starr & Sayre. This taxon represents an assemblage of numerous pathotypes and morphotypes, and may represent a complex of species (Starr & Sayre, 1988). This bacterium has been found infecting a large number of nematode species (more than 200 in about 100 genera, Sayre &

Starr, 1988; Stirling, 1991), does not attack other soil organisms, and is the most specific obligate parasite of nematodes known. Its spores attach to and penetrate the nematode cuticle. Most attention has been centered on populations of P. penetrans sensu stricto (Starr & Sayre, 1988) that attack root knot nematodes (Meloidogyne spp.). The spores of P. penetrans germinate a few days after a contaminated nematode begins feeding on a root (Sayre & Wergin, 1977). The bacterium reproduces throughout the entire female body, and the female either may be killed or may mature but produce no eggs. Bacterial spores (about 2 million from each infected nematode, Mankau, 1975) are released when the nematode body decomposes, and they remain free in the soil until contacted by another nematode. They tolerate dry conditions and a wide range of temperatures, and may remain viable in the soil for more than 6 months. Because P. penetrans is an obligate parasite, it has not yet been possible to develop in vitro culturing techniques for this bacterium. Different populations of the bacterium show varying degrees of specificity to small numbers of nematode species, but the mechanisms and degree of specificity remain to be elucidated (Stirling, 1991). Pasteuria penetrans appears responsible for some cases of natural regulation of nematode populations (Sayre & Walter, 1991). Variation in susceptibility of Meloidogyne spp. biotypes to P. penetrans may contribute to variation in effectiveness (Tzortzakakis et al., 1997). A few strains of Bacillus thuringiensis Berliner are also known to have activity against nematodes, including plantparasitic species. Zuckerman et al. (1993) report efficacy of a strain against M. incognita (Kofoid & White) Chitwood, Rotylenchus reniformis Linford & Oliveira, and Pratylenchus penetrans Cobb in field and in greenhouse trials. The body openings of these nematodes are too small to permit the ingestion or other ingress of the bacterium, and Zucherman et al. (1993) suggest that the mode of action is either a fl-exotoxin (Prasad et al., 1972; Ignoffo & Dropkin, 1977) or a t~-endotoxin released following bacterial cell lysis. A strain of B. thuringiensis with a nematotoxic 6endotoxin is the subject of a European patent application by Mycogen Corporation of San Diego, California (Zuckerman et al., 1993).

Fungi Affecting Plant-Parasitic Nematodes A large group of fungi attack nematodes in the soil (Barron, 1977; Stirling, 1991; Galper et al., 1991). Numerous species have been reported from all types of soils. The taxonomy of the group has been subject to revision, and we use the genetic names recognized in Stirling (1991) in this chapter. Some nematophagous fungi are endoparasitic in nematodes. Among these are genera that reproduce through motile zoospores (e.g., Catenaria anguillulae Sorokin, Lagen-

Chapter 26

Controlling Soil-Borne Plant Pathogens

idium caudatum Barron, and Aphanomyces sp.), which generally appear only weakly pathogenic in healthy nematodes (Stirling, 1991). Other endoparasitic fungi possess adhesive conidia, and the infection process begins when conidia adhere to a nematode's cuticle (e.g., the genera Verticillium, Drechmeria, Hirsutella, and Nematoctonus). In Nematoctonus spp., the germinating spores secrete a nematotoxic compound that causes rapid immobilization and death of nematodes (Giuma et al., 1973). A few species [Catenaria auxilaris (Kuhn) Tribe, Nematophthora gynophila Kerry & Crump] parasitize adult females or nematode eggs instead of juveniles. Other fungi capture nematodes through use of special trapping structures, and have been termed "predatory." Among the more common of these fungi are species in such genera as Monacrosporium, Arthrobotrys, and Nematoctonus. These fungi consist of a sparse mycelium, modified to form organs capable of capturing nematodes. These organs include adhesive structures, such as adhesive hyphae, branches, knobs, or nets (Stirling, 1991). There are also nonadhesive tings, the cells of which expand when touched on their inner surface, constricting the interior of the ring, and trapping nematodes. Most of these fungi are not specific and attack a wide range of nematode species. They are widely distributed (Gray, 1987, 1988) and most are capable of saprotrophic growth, but often appear limited in this phase in the soil. Many soils suppress the growth of these fungi (a condition called soil fungistasis or mycostasis). This is possibly due to two different causes. Mankau (1962) concluded that a water-diffusible substance was responsible for inhibited germination in tests of southern Californian soil. Other studies have indicated increased activity following soil amendments with nutrients (Olthof & Estey, 1966) or organic material (Cooke, 1968), which implies fungistasis may be a result of resource limitation. Following saprotrophic growth, formation of trapping structures occurs, and is apparently stimulated by nematodes (Nordbring-Hertz, 1973; Jansson & Nordbring-Hertz, 1980). Stirling (1991) suggested that this phase of predaceous activity is followed by diversion of resources to reproduction, followed by a relatively dormant phase. Several species of fungi are facultatively parasitic on nematodes. Of the few of these fungi that are significant pathogens of root knot and cyst nematodes, Verticillium spp. are among the most important. These fungi can parasitize nematode eggs, and V. chlamydosporium Goddard plays a major role in limiting multiplication of Heterodera avenae Wollenweber in English cereal fields (Kerry et al., 1982a, 1982b). Paecilomyces lilacinus (Thom) Samson parasitizes eggs of Meloidogyne incognita (Jatala et al., 1979) and Heterodera zeae Koshy, Swarup & Sethi (Dunn, 1983; Godoy et al., 1983). Dactylella oviparasitica Stirling & Mankau, a parasite of Meloidogyne eggs, is thought to be at least partly responsible for natural decline of root knot

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nematodes in California peach orchards (Stirling et al., 1979).

Predacious Nematodes

Predatory nematodes are found in four main taxonomic groups (Monochilidae, Dorylaimidae, Aphelenchidae, and Diplogasteridae), each with a distinct feeding mechanism and food preferences (Stirling, 1991). The monochilids have a large buccal cavity that bears a large dorsal tooth; all species are predaceous, feeding on protozoa, nematodes, rotifers, and other prey, which may be swallowed whole or pierced and the body contents removed. The dorylaimids are typically larger than their prey and possess a hollow spear that is used either to pierce the body of the prey or to inject enzymes into the food source and to then remove the predigested contents. The group is considered omnivorous, but the feeding habits are known for only a few species (Ferris & Ferris, 1989). Almost all the predatory aphelenchids are in the genus Seinura. Although small, they can feed on nematodes larger than themselves by injecting the prey with a rapidly paralyzing toxin via their stylet. The diplogasterids, typically a bacteria-feeding group, have a stoma armed with teeth, and the species with large teeth prey on other nematodes. Species in all these groups are generally omnivorous, feeding on free-living as well as plant-parasitic nematodes. The role of individual species in the population dynamics of plant-parasitic nematodes in the soil has been difficult to quantify, but it is possible that a number of species may act together to produce a significant impact (Stirling, 1991).

Insects and Mite Predators

Several microarthropods in the soil, including mites and Collembola, prey on nematodes, and high predation rates have been recorded in vitro (Stirling, 1991). A few genera are obligate predators of nematodes, while other genera are more omnivorous and consume nematodes as well as other foods (Moore et al., 1988; Walter et al., 1988; Sayre & Walter, 1991). The information available suggests that, as a group, microarthropods are probably significant predators on nematodes in some soils and habitats. Limited information about predation rates in soil is available, however, and more work will be necessary to assess the impact of this group on nematode populations.

MICROBIAL AND HABITAT CHARACTERISTICS Pathogens and Antagonists Competition for resources in soil environments is vital to the ability of any particular organism to increase in

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numbers and consequently to reduce the numbers or activity of other organisms, including plant pathogens (Campbell, 1989; Andrews, 1992). As discussed in Chapter 32, microbial competition can be important at two main stages of growth of pathogen populations. First, there may be competition during initial establishment on a fresh resource that previously was not colonized by microorganisms, as is typical for ruderal or r-selected species. Second, after initial establishment, there is further competition to secure enough of the limited resources present to permit survival and eventual reproduction. This later competition after population establishment is typical of K-selected species. Microorganisms show many traits that may characterize them as particularly adept at either the colonization (r-strategist) phase or the subsequent (K-strategist) phases of competition (Begon et al., 1986). These concepts represent the endpoints of a continuum, and there are varying degrees of r- and Krelated characteristics in different microbes in various habitats; see Andrews and Harris (1986) for further discussion on these concepts in microbial ecology. Plant pathogens are spread across this r - K range of characteristics, and also vary in other biological characteristics. Opportunistic pathogens are able to attack young, weakened, or predisposed plants, but may be poor competitors (Botrytis, Pythium, and Rhizoctonia). Other pathogens tolerate environmental stresses well. These organisms often live in situations with few competitors, because few species are able to exist in some stressful environments. Pathogens, such as the Penicillium species that cause postharvest rots, produce antibiotics that inhibit competitors. Other species have a very high competitive ability [Fusarium culmorum (Smith) Saccardo]. Knowledge of the ecology of a pathogen can be important in determining what biological control strategy might be most effective. Stress-tolerant and competitive species, for example, would require different biological control strategies and agents than would ruderal ones. Just as plant pathogens vary in r - K and other characteristics, antagonists of these pathogens have varied biological attributes. The properties of an effective biological control agent will depend on the setting in which it is intended to function. In many agricultural settings, disturbance makes new resources available to microbes through crop residue burial, cultivation, or planting. A frequent need, therefore, is a control agent that has the characteristics of an r-strategist (Campbell, 1989), which can grow quickly and colonize new resources rapidly when faced with minimal nutrient and environmental restrictions. It should function well in disturbed environments and have some means (such as spores) of surviving in the soil, or on the plant near the pathogen inoculum, or near the source or site of infection. Biological control agents that are r-strategists are an approximate equivalent of a protectant fungicide, being in place before the pathogen infection cycle can begin. In

other programs, such as those directed against a pathogen that has already invaded the plant host, a more competitive species will be required. Finally, a biological control agent may have to be tolerant of abiotic stresses, particularly for use in dry climates. Soil a n d t h e Rhizosphere Although there is much variation in soil types in different locations, soils are typically rich in microflora, with propagules numbering in the hundreds of thousands per gram of soil (Campbell, 1989). In most soils, growth of microorganisms is carbon limited (Campbell, 1989), either because what carbon is available is not physically accessible or because the microbes do not possess the enzymes necessary to degrade the carbon-containing molecules that are present. An exception to this general limitation is the rhizosphere, the roots and the regions immediately adjacent to them. The rhizosphere contains easily metabolized carbon and nitrogen sources such as amino acids, simple sugars, and other compounds exuded by the roots. Consequently, this region is more favorable than surrounding soil for the support of microflora. While root pathogens and plant-parasitic nematodes may be found growing on or in roots, many microbes in the soil may be dormant because of resource limitations. Because there are many dormant organisms in the ~soil prepared to take advantage of any favorable period or opportunity, competition for resources in the soil may be significant and may limit the ability to augment beneficial organisms and have them flourish, unless soils are first sterilized to eliminate potential competitors. Consequently, much research surrounding biological control of root diseases and nematodes has centered around identifying soils that are naturally suppressive to particular disease organisms and investigating the microbial components of the soil responsible for the suppression.

CONTROL OF SOIL BORNE PLANT PATHOGENS Organisms for biological control of soil bome diseases can be used primarily in two ways, either through conservation or through augmentation. Among the diversity of nonpathogenic microbes usually associated with plants, there is substantial opportunity for development of resident species as competitors of, or antagonists to, pathogenic organisms. Management of such antagonistic organisms for biological control can range from treatment of soil to favor the desirable organisms (conservation) through inoculation of soils or plants with specific beneficial microorganisms (augmentation). Substantial work has been done in characterizing the role of microorganisms in biological control of plant diseases

Chapter 26 ControllingSoil-Borne Plant Pathogens (Elad, 1986). The biological mechanisms underlying the success of these antagonists may include initial competition for occupancy of inoculation sites, competition for limiting nutrients or minerals, parasitism, and induction of plant defenses. Conservation Biological control of plant pathogens through conservation is accomplished either by preserving existing microbes that attack or compete with pathogens or by enhancing conditions for their survival and reproduction at the expense of pathogenic organisms. Conservation is applicable in situations where microorganisms important in limiting disease-causing organisms already occur, primarily in the soil and in plant residues. Microorganisms may be conserved by avoiding practices that negatively affect them (such as soil treatments with fungicides). The soil environment may be enhanced for some beneficial organisms through adding organic matter (including such soil amendments as composted organic matter, manures, cover crops, or crop residue). Root Diseases In the case of soil microflora, species employed for biological control of plant pathogens are often competitive antagonists. Adding amendments to soil is one way in which soil microorganisms may be managed to enhance populations of these beneficial organisms. Addition of or-

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ganic matter to soils for control of Streptomyces scabies, the causative organism of potato scab, is one example. Addition of carbon sources to soil increases general microbial activity that leads to reductions in S. scabies. Specifically, Bacillus subtilis and saprotrophic species of Streptomyces were encouraged by barley, alfalfa or soy meal (Campbell, 1989). Soy meal was also a substrate for antibiotic production against S. scabies. A general rise in soil organic matter also gave control of Phytophthora cinnamomi in avocado in Australia (Malajczuk, 1979). The addition of more than 10 tons of organic matter per hectare per year led to general increases in numbers of bacteria. Lysis of the hyphae and sporangia of the pathogen were attributed to species of Pseudomonas, Bacillus, and Streptomyces. Some soils appear to suppress disease naturally, and may contain antagonistic or antibiotic floras that flourish without the need for amendments. One example of such suppressive soils is the Fusarium-suppressive soil in the Chateaurenard District of the Rhone Valley in France (Fig. 1). Here, Fusarium oxysporum f. sp. melonis Snyder & Hansen is present, but no disease develops when susceptible melon varieties are grown. These soils are suppressive for several other types of F. oxysporum, but not to other species or genera of pathogens. The suppressive nature of the soils is clearly biotic, because the soils lose their suppressive ability when steam sterilized, and the suppressive ability can be transferred to other soils. The antagonists principally responsible for this suppression are nonpathogenic strains of F. oxysporum and F. solani (Martius) Saccardo. The sup-

FIGURE 1 The suppressive nature of soil from the Chateaurenard District (Rhone Valley, France) against Fusarium oxysporum f. sp. melonis Snyder & Hansen is caused by the presence of other nonpathogenic fungi in the soil. Untreated soil and steamed soil with a mixture of the fungi present completely suppress the disease. The species of fungi present vary in their individual ability to suppress the disease, with a nonpathogenic form of F. oxysporum Schlechtendal playing an importantrole. (After Alabouvette et al. (1979).

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pression appears to be due to fungistasis induced by nutrient limitation. The competing fungi appear to have nearly the same ecological niche as the pathogenic forms, and the saprotrophic forms outcompete the pathogens for limiting resources so that dormant chlamydospores of the pathogen do not germinate in the presence of host root exudates. It may be possible to develop systems for other areas using the antagonists from the Chateaurenard area (Campbell, 1989), although additional research may be necessary to permit their effective operation in different soils. Other soils suppressive to Fusarium wilts are also known. There are numerous other examples of suppressive soils (Larkin et al., 1996), although some soils or combinations appear to give somewhat variable results. Plant-Parasitic Nematodes

There are several reports of substantial natural control (control by natural enemies without intentional manipulation) of plant-parasitic nematodes. Stirling (1991) and Sayre and Walter (1991) review several of these. The natural suppression of the cereal cyst nematode Heterodera avenae in cereal cultivation in England (Gair et al., 1969) is one example of such suppression. In this case, populations of the nematode initially increased for the first 2 to 3 years of cultivation and then declined continually during 13 years of continuous cultivation of both oats and barley (a more susceptible crop) (Fig. 2). Four species of nematophagous fungi were present in the soil. The two species principally responsible for nematode suppression were Nematophthora gynophila and Verticillium chlamydosporium. Both fungi attacked female nematodes, either destroying them or reducing their fecundity. The activity of both fungi during laboratory trials was greatest i n w e t soils (Kerry et al.,

1980). Although natural suppression of the nematode population takes some time to develop in these soils, once established it maintains the population below the economic threshold (Stifling, 1991). Conserving nematode antagonists (as opposed to directly enhancing their numbers, as discussed later) in soils is a matter that has received relatively little attention. The application of toxins (e.g., insecticides and fungicides) to aerial portions of crops or directly to soils often leads to pesticide activity in the soil. All nematicides are nonselective in their action and hence will kill predatory nematodes (Stirling, 1991). In addition, herbicides have well-documented effects on soil microorganisms (Anderson, 1978) and may well exert some influence on microbial antagonists of nematodes. Insecticides may negatively affect soil microarthropods. Many fungicides are known to be detrimental to nematophagous fungi (Mankau, 1968; Canto-Saenz & Kaltenbach, 1984; Jaffee & McInnis, 1990), but at levels higher than would be expected under normal field practice. Among the fumigant nematicides, ethylene dibromide (EDB) and dibromo-chloro-propene (DBCP) appear nontoxic to the nematode-trapping fungi (Mankau, 1968), and several herbicides were not harmful to Arthrobotrys sp. (Cayrol, 1983). Despite these potentially significant effects on beneficial microfloras and faunas, and the possibility of conserving these organisms by appropriate choice of pesticide, little has emerged to integrate these ideas into normal farming practice. Perhaps because there has been no serious emergence of nematode problems associated with the use of these materials, the status quo is justified. Nonetheless, the opportunities for conserving biologically important agents should be considered in the development of future integrated management programs for plant-parasitic nematodes.

FIGURE 2 Postcroppinglevels of Heterodera avenae Wollenweberand crop yields under continuous grain [oats (Avena sativa Linnaeus) 1955 to 1962 and barley (Hordeum vulgare Linnaeus) 1963 to 1968] culture in the United Kingdom. [After Gair, R., et al. (1969). Annals of Applied Biology, 63, 503-512.]

Chapter 26 ControllingSoil-Borne Plant Pathogens Cultivation practices may also be selected to favor natural enemies of nematodes. Among these are minimal or conservation tillage, which reduced the number of cysts of H. a v e n a e on roots and the amount of damage caused by the nematode on wheat in Australia (Roget & Rovira, 1987). Other practices that may affect populations of natural enemies include normal tillage (which adds crop residue to the soil and thus may favor certain beneficial organisms) and crop rotation sequences (Stirling, 1991). The knowledge that some soils are naturally suppressive to nematodes prompts the question of whether or not the features of these soils can be used to improve biological control. In all documented instances where they have been studied, the suppressive properties of these soils appear to result primarily from the action of one or two specific biological control agents (Stirling, 1991). The suppressiveness requires substantial time to develop, and considerable economic loss might be incurred during the initial seasons of cropping before the suppressive nature has fully developed. Some risk is involved also, because the suppressive nature of the soil may not develop to suitable levels. Careful management of crop variety, particularly concerning susceptibility to nematode damage, during the initial phases of land usage for cropping, is an important part of taking advantage of the potential of these resident natural enemies (Stirling, 1991). Where soils are not naturally suppressive to nematode populations, they may be manipulated to enhance what natural control agents are present. Most attention in this arena has been given to the addition of organic matter to the soils. Much of the information concerning the effects of these amendments is circumstantial, but the beneficial effects appear widespread. Many different soil amendments have been considered and evaluated, and it is clear that the reduction of plant damage from nematodes following such amendments may occur through a variety of mechanisms (Stirling, 1991). One of these mechanisms is through general improvement of soil structure and fertility. Addition of crop residue or animal manures increases ion exchange capacity of the soil, chelates micronutrients to make them accessible by the plant, and adds available nitrogen. Grown under such improved conditions, healthy plants are better able than stressed plants to tolerate damage from nematodes. In a second mechanism, certain amendments may directly improve plant resistance to nematodes (Sitaramaiah & Singh, 1974). Populations of some nematophagous and antagonistic organisms respond directly to soil amendments. Spores of many of fungi fail to germinate in otherwise suitable but nonamended soils (Dobbs & Hinson, 1953) and this soil mycostasis can affect both spores and mycelia (Duddington et al., 1956a, b, 1956b, 1961; Cooke & Satchuthananthavale, 1968) (Table 1). Before predation on nematodes by

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TABLE 1 Results of a Field Microplot Experiment with Schmidt on Sugar Beets Showing the Effects of Soil Amendments and Nematode-Tapping Fungi on Nematode Populations and Yield Heteroclera s c h a c h t i i

Final nematode population/ 100 g soil Treatment

1. Untreated 2. Bran (20 ton/ha) (Drechsler) de Hoog & van Oorschot mycelium (6.8 ton/ha) at planting 4. Treatment2 + treatment 3 5. Treatment4 + M. thaumasia mycelium (6.8 ton/ha) in midseason 3. Monacrosporium thaumasia

Cysts

Eggs

Yield (ton/ha)

467 383 488

114 103 144

45.4 56.3 56.3

333 363

94 128

59.2 60.1

After Duddington, C.L., et al. (1956a). Nematologica, 1, 341-343. these fungi can take place, mycelial growth and trap formation must occur. The addition of organic matter provides a substrate that may stimulate spore germination. Organic amendments stimulate a broad range of soil microorganisms; thus, the effects of amendments on populations of these organisms are complex. There is a general increase in microbial population growth immediately following the addition of organic matter; subsequently as part of the community succession, there is an increase in populations of nematode-trapping fungi (Stirling, 1991). Speigel et al. (1988, 1989) concluded that the beneficial effects of chitin amendments resulted from the action of specialized microorganisms. Augmentation Biological control of plant pathogens through augmentation is based on mass-culturing antagonistic species and adding them to the cropping system. This is considered augmentation because the organisms used are usually present in the system, but at lower numbers or in locations different from those desired. The purpose of augmentation is to increase the numbers or to modify the distribution of the antagonisist in the system. In some cases such organisms are taken from one habitat (e.g., the soil) and augmented in another (e.g., the phyllosphere). There are several examples where such organisms, when moved to a new habitat (e.g., from the soil to the aboveground part of a plant) colonize and serve as successful agents of biological control (Andrews, 1992; Cook, 1993). The activity of augmenting microbial agents is sometimes termed "introduction" in the plant pathology literature, in the sense of "adding" them to the system (Andrews, 1992; Cook, 1993).

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Augmentation of antagonists may suppress disease through two different types of mechanisms. The first is when the antagonistic organisms compete, at potential infection sites or zones, with the pathogens themselves. In this approach, the antagonist population is directly responsible for disease suppression. A second approach is inoculation of plants with nonpathogenic organisms that prompt general plant defenses against infection by pathogens (induced resistance, discussed later), and control is achieved through greater resistance of the plant to infection. Parasitism is another mechanism by which beneficial microorganisms suppress plant pathogens. Some species of Trichoderma, for example, attack pathogenic fungi, leading to the lysis of the pathogen. Natural enemies of plantparasitic nematodes include bacterial diseases and nematophagous and nematopathogenic fungi. These organisms can also be augmented into soil environments to suppress pathogenic organisms. Augmentation of antagonists and parasites of plant disease organisms can generally be of two types, inoculation and inundation (also see Chapter 32). Inoculative releases consist of small amounts of inoculum, with the intention that the organisms in this inoculum will establish populations of the antagonist that, following subsequent population growth, will then limit the pathogen population. In inundative releases, a large amount of inoculum is applied, with the expectation that control will result directly from this large initial population with limited reliance on subsequent population growth. Biological control of plant pathogens may also rely on a hybrid of these two concepts. A large amount of inoculum may be applied, both to increase the population of the antagonist and to improve its distribution to favor biological control, and antagonism can result from both these applied organisms and the increased population of antagonists resulting from their reproduction. In some cases, augmentation of an antagonist will result in more than one season of control (Junqueira & Gasparotto, 1991; Cook, 1993). More generally, beneficial microorganisms are added seasonally or more frequently.

Root Diseases

The floras with demonstrated antagonistic properties under field conditions include fungi, principally Trichoderma spp., and, among bacteria, Bacillus spp. and Pseudomonas spp. Among bacteria, species of Bacillus are regularly used for biological control of root diseases. Members of the genus have advantages, particularly because they form spores that permit simple storage and long shelf life, and they are relatively easy to inoculate into the soil. The consequence of this biology is, however, that although the inoculum may be present in the soil, it may be in a dormant

or resting stage. Species of Bacillus have provided good control on some occasions. Capper and Campbell (1986) showed a doubling of wheat yield over wheat plants naturally infected with take-all disease by those also inoculated with B. pumilus Meyer & Gottheil. Bacillus pumilus and B. subtilis were also used to protect wheat from diseases caused by species of Rhizoctonia (Merriman et al., 1974). A major difficulty with the use of Bacillus spp. is that the control provided is often very variable, with very different results in different locations, or even in different parts of a season in the same location (Campbell, 1989). Bacillus subtilis is used as a seed inoculant on cotton and peanuts (Arachis hypogaea Linnaeus). Treatment promotes increased root mass, nodulation, and early emergence; and suppression of diseases caused by species of Rhizoctonia and Fusarium. Of substantially more promise as antagonists of root diseases are species of Pseudomonas, particularly the P. fluorescens Migula and P. putida (Trevisan) Migula groups (Campbell, 1989). These fluorescent bacteria are easy to grow in the laboratory, are normal inhabitants of the soil, and colonize and grow well when inoculated artificially. They produce a number of antibiotics as well as siderophores. Several have received patents and are marketed commercially for control of root rot in cotton (Campbell, 1989). One example is the use of isolates of a species of Pseudomonas as an antagonist of take-all disease of wheat (Weller, 1985). Isolates of P. fluorescens from soils showing control of take-all can be applied as seed coats and inoculated into fields suffering from the disease. Such treatments give 10 to 27% yield increases compared with untreated, infected control groups. Evidence points to both siderophore and antibiotic production as important. Species of the fungal genus Trichoderma can be saprotrophic and mycoparasitic and have been used against wilt diseases of tomatoes, melons, cotton, wheat, and chrysanthemums. The antagonists were applied to seeds or incorporated into the planting mix at transplanting in a bran mixture. Although disease did develop, it did so much more slowly than it did in untreated soils, giving from 60 to 83% reduction in disease (Siven & Chet, 1986). The mode of action against Verticillium albo-atrum Reinke & Berthier wilt of tomatoes appeared to be antibiosis. Mycoparasitic Trichoderma spp. have also been used successfully against diseases caused by Rhizoctonia and Sclerotium pathogens. Sclerotium rolfsii attacks many crop plants and survives unfavorable periods by forming sclerotia in the soil. Strains of T. harzanium that have r - l - 3 glucanases, chitinases, and proteases have been isolated. These enzymes permit T. harzanium to parasitize the hyphae and sclerotia of the pathogen, invading and causing lysis of the cells. Trichoderma harzanium is grown on autoclaved bran or seed, and this material is then mixed with the surface soil (Chet & Henis, 1985). Two other fungi known to parasitize sclerotia are Coniothyrium minitans

Chapter 26 ControllingSoil-Borne Plant Pathogens Campbell and Sporidesmium sclerotivorum (Ayers & Adams, 1981). Sporidesmium sclerotivorum is a hyphomycete that in nature behaves as an obligate parasite of sclerotia of Botrytis cinerea and several species of Sclerotium (Adams, 1990). This hyphomycete has been studied as an agent against botrytis rot in lettuce, where it shows considerable potential. It can be grown in vitro on various carbon sources, and is efficient in converting glucose into mycelium. Spores produced in mass culture are collected, processed, and applied to infected soil; and field tests are promising (Adams, 1990). Plant-Parasitic Nematodes

Organisms most often considered for augmentation against plant parasitic nematodes are nematophagous or parasitic fungi and bacteria. The bacterial pathogen of nematodes most studied is Pasteuria penetrans sensu stricto Starr & Sayre (Starr & Sayre, 1988), which is an obligate parasite of root knot nematodes (Meloidogyne spp.) and has not been successfully cultured in vitro. This restriction in mass-culturing has limited attempts to test the bacterium's effectiveness (Stirling, 1991). In experimental trials this pathogen has demonstrated potential for controlling Meloidogyne spp. (Mankau, 1972; Stirling et al., 1990; Fig. 3), infesting a high proportion of nematodes in soil to which bacterial spores had been added, and in other trials (USDA, 1978) reducing damage to plants in plots containing the bacterium. Observations by Mankau (1975) indicated that populations of the bacterium did not increase rapidly in field soil. The development of a mass production method in which roots containing large numbers of infected Meloidogyne spp. females were air-dried and finely ground to

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produce an easily handled powder enabled more extensive testing (Stirling & Watchel, 1980). When dried root preparations laden with spores were incorporated into field soil at rates of 212 to 600 mg/kg of soil, the number of juvenile Meloidogyne javanica (Treub) Chitwood in the soil and the degree of galling was substantially reduced (Stirling, 1984); other authors have reported similar results (Stifling, 1991). Effective use of such a bacterium through such inundative release would require spore concentrations on the order of 105 spores per gram of soil (Stifling et al., 1990). Such quantities could only be produced on a large scale with an efficient in vitro culturing method, a problem that has received attention but has not yet yielded a solution (Stifling, 1991). Use in inoculative releases, where smaller numbers of spores are applied, and subsequently a crop tolerant of nematode damage is grown to permit the increase of both nematode and bacterial populations has been suggested (Stifling, 1991). Conserving the bacterium in the presence of nematicides appears possible. Of seven tested nematicides only one showed slight toxicity to the bacterium (USDA, 1978). The use of Bacillus thuringiensis strains with activity against nematodes is also possible. Because these bacteria may be cultured in fermentation media, their mass culture is much simpler than that of P. penetrans. Suppression of nematodes was possible through drench applications and through incorporating the bacterium into a methylcellulose seed coat (Zuckerman et al., 1993). Considerable attention has been given to the nematodetrapping fungi as possible augmentative agents. Mass culture on nutrient media is possible for these fungi. Two cultures of nematophagous Arthrobotrys fungi have been developed and tested for addition to soil for specific target environments. Cayrol et al. (1978) reported the successful

FIGURE 3 Numberof galls caused by Meloidogynejavanica (Treub) Chitwood [and percentage of females infected with Pasteuria penetrans (Thorne) Sayre & Starr sensu stricto Starr & Sayre] after movement as juveniles through 4 cm of soil infested at various densities with P. penetrans spores. [After Stifling, G. R. et al., (1990). Nematologica, 36, 246-252.]

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use of A. robusta Cooke & Ellis var. antipolis, commercially formulated as Royal 300 | against the mycetophagous nematode Ditylenchus myceliophagus Goodey in commercial production of the mushroom Agaricus bisporus (Lange) Singer. The nematophagous fungus was seeded simultaneously with A. bisporus into mushroom compost, which led to 28% increases in harvest and reduced nematode populations by 40%. The results justified the commercial use of the fungus for nematode control in mushroom culture. Cayrol and Frankowski (1979) reported the use of Arthrobotrys superba Corda (Royal 350 | in tomato fields, applied to the soil at a rate of 140 g/m 2, resulting in protection of the tomatoes and colonization of the soil by the fungus. Other reports have indicated little efficacy of fungal preparations when added alone to soil (Barron, 1977; Sayre, 1980; Rhoades, 1985). In general, there has been limited success in the use of these agents; see Stirling (1991) for a summary. The fungistatic nature of soil (Mankau, 1962; Cooke & Satchuthananthavale, 1968) may limit the ability of these fungi to grow even when added in substantial numbers to soil. Many of the predaceous fungi may be unsuited for control of root knot nematodes, Meloidogyne spp. Stirling (1991) suggested that Monacrosporium lysipagum (Drechsler) Subramanian and M. ellipsosporum (Grove) Cooke & Dickinson, which can invade egg masses, may warrant further investigation. The nematode-trapping fungi are likely to be more effective against ectoparasitic nematodes and such species as Tylenchus semipenetrans Cobb, where juvenile stages migrate through the rhizosphere. Little attention has been given to testing predaceous fungi against such nematodes. Fungi that are internal parasites of nematodes have been difficult to culture on nutrient media, and consequently there have been few attempts to use them for augmentative control of nematodes. Alternative mass-culturing techniques may hold some promise (Stirling, 1991). Lackey et al. (1993) report the production and formulation on alginate pellets [see also Fravel et al. (1985)] of Hirsutella rhossiliensis Minter et Brady that, when added to soil, led to transmission to the nematode Heterodera schachtii Schmidt and suppressed nematode invasion of roots. Among the facultatively parasitic fungi that attack nematodes, Paecilomyces lilacinus and V. chlamydosporium have received the most attention as possible augmentative agents. The results of studies with P. lilacinus have been variable, with some studies showing some positive effect of the fungus, while others show little or no effect (Stirling, 1991). The mechanisms leading to the beneficial effect are not clearly elucidated, but may be from metabolic products or effects other than direct parasitism of eggs. Studies have generally involved the addition of fungal preparations to the soil at the rate of 1 to 20 ton/ha, which is likely too great for widespread commercial use. Additions at lower

rates (0.4 ton/ha) in a variety of carriers (alginate pellets, diatomaceous earth, wheat granules) also have resulted in limited beneficial effects (Cabanillas et al., 1989; Stirling, 1991). Tribe (1980) suggested the direct addition of V. chlamydosporium to the soil. Kerry (1988) added hyphae and conidia, formulated in sodium alginate pellets or in wheat bran, to soil, and the fungus proliferated in the soil only from granules containing bran. When chlamydospores were used as inoculum, the fungus was able to establish without a food base (De Leij & Kerry, 1991). Of three isolates studied, only one successfully colonized tomato root surfaces. This species apparently has considerable promise, but screening programs will be necessary to identify isolates with characteristics suitable for biological control (Stirling, 1991). Predaceous microarthropods and predaceous nematodes have evoked considerable interest. Most research has been done in simple microcosms, and there have been no attempts to evaluate augmentative release of these organisms in a field setting. In one experiment, Sharma (1971) found nematode numbers reduced by 50% or more in glass jars inoculated with mites and springtails compared with similar jars containing no predators, but the author pointed out possible causes for the reduction other than simple predation. Experiments with predaceous nematodes have in general failed to demonstrate a measurable impact of the predator (Stirling, 1991). One exception was the reduction of galling by Meloidogyne incognita on tomato by predaceous nematodes (Small, 1979). The general suitability of these groups of organisms for inundative release is questionable, because of the potential difficulties in developing technologies for their rearing, packaging, transport, and delivery beneath the soil in a viable state (Stifling, 1991). I n d u c e d Resistance Induced resistance is a form of disease control that uses the natural defense responses of the plant, which may include production of phytoalexins, additional lignification of cells, and other mechanisms (Horsfall & Cowling, 1980; Bailey, 1986), to defend the plant against pathogenic infection. These plant defenses are induced, or promoted, in the plant prior to exposure to the pathogen by challenging the plant with a nonpathogenic microbe. The plant defenses then limit later infection by the pathogen. The challenging organism employed may be an avirulent strain of the pathogen, a different forma specialis, or even a different species. Induced resistance and cross-protection are treated more fully in Chapter 19. Root Diseases

There are few well-documented cases of induced resistance for soil-borne pathogens, and these are mostly of wilt diseases. Dipping tomato roots in a suspension of F. oxy-

Chapter 26

709

Controlling Soil-Borne Plant Pathogens

FIGURE 4 Induced resistance with a reduced virulence strain (SS-4) of Verticillium albo-atrum Reinke & Berthier in a field of cotton (Gossipium hirsutum Linnaeus) infested with a virulent strain (T-1) of the pathogen. [After Schnathorst, W. C., & Mathre, D. E. (1966). Phytopathology, 56, 1204-1209.]

grows on grass roots and also has been found on wheat, where it occupies a niche similar to that of the pathogen G. graminis var. tritici Walker. The antagonist invades the root cortex but not the stele, and is halted by the lignification and suberization of the cortex and stele. Root cells with these chemically changed walls are less susceptible to invasion by the pathogen. Although this interaction produced yield increases in Europe, the strains or species present in the United States did not appear to confer resistance and in Australia there were only slight yield increases (Campbell, 1989). These variable results, while somewhat common for biological control of soil borne pathogens, do not reduce the value of the antagonists where they do work, but instead serve to outline some of the potential challenges in defining the taxonomy, biology, and host-plant relations in this group of organisms.

DEVELOPING AND USING BENEFICIAL SPECIES sporum f. sp. dianthi a few days before likely exposure to the pathogen F. oxysporum f. sp. lycopersici (Saccardo) Snyder & Hansen conferred protection that lasts a few weeks. Cotton may be protected for 3 months or longer by spraying the roots at transplanting with a mildly pathogenic strain of the disease-causing pathogen V. albo-atrum (Schnathorst & Mathre, 1966) (Fig. 4). The role of some fungi against take-all disease of wheat includes some elements of induced resistance. Gaeumannomyces graminis (Saccardo) Arx & Olivier var. graminis

TABLE 2

Since the first experimental reports of biological control of plant pathogens (Hartley, 1921; Sanford, 1926; Millard & Taylor, 1927; Henry, 1931), substantial potential for microbial control of pathogens has been demonstrated. A number of products or programs have reached the stage of commercial development or availability (Table 2). Products in current use include both those aimed at specialty markets such as control of nematodes on mushroom production and at large-scale markets such as seed treatments for cotton and soybeans.

S o m e C o m m e r c i a l l y Available A n t a g o n i s t s or Products for Soil Plant P a t h o g e n s a n d Plant-Parasitic N e m a t o d e s

Organism

Trade name

Target

Targeted against Pathogens Bacillus subtilis (Ehrenberg) Cohn

Kodiak, Epic

Pseudomonas cepacia (Burkholder) Palleroni and Holmes

Blue Circle; Intercept

P. fluorescens Migula

Dagger G

Fusarium oxysporum Schlechtendal (nonpathogenic strains) Gliocladium virens Millers, Giddens & Foster

Fusaclean; Biofox C GlioGard

Mycorrhyzae Streptomyces griseovirides Anderson et al. Trichoderma harzanium/polysporum (Link) Rifai

Vaminoc Mycostop BINAB

T. harzianum Rifai

F-Stop; Trichodex; Supravit; T-35; TY Trichodermin-3

T. lignorum (Tode) Harz

Seed treatment against Rhizoctonia spp., Pythium spp., and Fusarium spp. root diseases Rhizoctonia spp. Pythium spp., and Fusarium spp. diseases of seedlings Rhizoctonia spp. and Pythium spp. diseases of seedlings Diseases from pathogenic strains of F. oxysporum Rhizoctonia spp. and Pythium spp. diseases of seedings and bedding plants Botrytis spp. and Pythium sp. diseases Alternaria sp. and Fusarium spp. diseases Wood-rot fungi; Verticillium malthousei Ware in mushrooms Heterobasidion annosum; diseases caused by Rhizoctonia spp., Pythium spp., Fusarium spp. B. cinerea Persoon: Fries, and Sclerotium rolfsii Saccardo Rhizoctonia spp. and Fusarium spp. diseases

Targeted against Nematodes Arthrobotrys robusta Cooke & Ellis var. antipolis A.~superba Corda Chitin-based amendment

Royal 300 | Royal 350 | Clandosan |

Ditylenchus myceliophagus Goodey Meloidogyne spp. Plant-parasitic nematodes

710

T.S. Bellows

Research and development of antagonists of plant pathogens is composed of several steps, as discussed in Chapter 32. These include initial discovery of candidate agents; refinement of our knowledge of their biology, ecology, and mode of action; microcosm and field trials of their efficacy; and large-scale development for commercial production. The adoption of any biological control agent in commercial agriculture is dependent on its reliability and its availability. Limitations to development of any particular agent include cost of development and size of potential market. Many pesticides for control of plant diseases have a broad spectrum of activity; are applicable in a variety of crops and settings; and may act either prophylactically, therapeutically, or both. Biological controls, in contrast, may have narrow ranges of activity and may work in only a few crops or soil types. While they can often act both prophylactically and therapeutically, their action may take some time to develop. Microorganisms intended for use as biological control agents must be viewed in a biological instead of a chemical paradigm (Cook, 1993). Although an effective pesticide may work in many places, each place may have unique soil, edaphic, and biological features that limit or enhance the effectiveness of microbial antagonists of pathogens. Consequently, each microbial biological control system may have to make use of locally adapted strains, taking advantage of resident antagonistic floras and faunas and augmenting their effectiveness with additional species or strains, or enhancing resident populations through soil amendments. Although the different strains may use common mechanisms to achieve biological control, competitive abilities adapted to local conditions may be vital to permit the organisms to compete for resources and effectively control pathogens. Hence, antagonists to plant pathogens may have a much narrower market than a chemical pesticide has, and be unattractive for development by major corporations (Andrews, 1992). In this context, it may be appropriate for public institutions such as government experiment stations to undertake the development of such biological controls, in the same way that they take the responsibility for development of new plant varieties (Cook, 1993).

References Adams, P. B. (1990). The potential of mycoparasites for biological control of plant diseases. Annual Review of Phytopathology, 28, 59-72. Alabouvette, C., Rouxel, F., & Louvet, J. (1979). Characteristics of Fusarium wilt-suppressive soils and proposals for their utilization in biological control. In B. Schippers & W. Gams (eds.), Soil-borne plant pathogens (pp. 165-182). London: Academic Press. Anderson, J. R. (1978). Pesticide effects on non-target soil microorganisms. In I. R. Hill & S. J. L. Wright (Eds.), Pesticide microbiology (pp. 313-533). London: Academic Press. Andrews, J. H. (1992). Biological control in the phyllosphere. Annual Review of Phytopathology, 30, 603-635.

Andrews, J. H., & Harris, R. F. (1986): r- and K- selection and microbial ecology. Advances in Microbial Ecology, 9, 99-147. Ayers, W. A., & Adams, P. B. (1981). Mycoparasitism and its application to biological control of plant diseases. In G. C. Papavizas (Ed.). Biological control in crop production. Beltesville Symposium in Agricultural Research 5 (pp. 91-105) Granada: Allenheld, Osmum Publishing. Bailey, J. A. (1986). Biology and molecular biology of plant-pathogen interactions. Berlin: Springer-Verlag. Barron, G. L. (1977). The nematode-destroying fungi. Topics in mycobiology Vol. I Guelph, Ontario, Canada: Canadian Biological Publications. Begon, M., Harper, J. L., & Townsend, C. R. (1986). Ecology: Individuals, populations and communities. Oxford, United Kingdom: Blackwell Scientific Publications. Cabanillas, E., Barker, K. R., & Nelson, L. A. (1989). Survival of Paecilomyces lilacinus in selected carders and related effects on Meloidogyne incognita on tomato. Journal of Nematology, 21,164-172. Campbell, R. (1985). Plant microbiology. London: Edward Arnold. Campbell, R. (1989). Biological control of microbial plant pathogens. Cambridge, United Kingdom: Cambridge University Press. Canto-Saenz, M., & Kaltenbach, R. (1984). Effect of some fungicides on Paecilomyces lilacinus (Thom) Samson. Proceedings of the First International Congress of Nematology, Guelph, Canada, 1, 13-14. Capper, A. L., & Campbell, R. (1986). The effect of artificially inoculated antagonist bacteria on the prevalence of take-all disease of wheat in field experiments. Journal of Applied Bacteriology, 60, 155160. Cayrol, J. C. (1983). Lutte biologique contre les Meloidogyne au moyen d' Arthrobotrys irregularis. Revenue de Nrmatologie, 6, 265-73. Cayrol, J. C., & Frankowski, J. P. (1979). Une methode de lutte biologique contre les nematodes a galles des racines appartenant au genre Meloidogyne. Revue Horticole, 193, 15-23. Cayrol, J. C., Frankowski, J. P., Laniece, A., d'Hardemare, G., & Talon, J. P. (1978). Contre les nematodes en champigonniere. Mise au point d'une methode de lutte bologique a l'aide d'un hyphomycete predateur: Arthobotrys robusta souche antipolis (Royal 300). Revue Horticole, 184, 23- 30. Chet, I., & Henis, Y. (1985). Trichoderma as a biocontrol agent against soilborne root pathogens. In C. A. Parker, et al. (Eds.) Ecology and management of soilborne plant pathogens (pp. 110-112) St. Paul, M N: American Phytopathological Society. Cook, R. J. (1993). Making greater use of introduced microorganisms for biological control of plant pathogens. Annual Review of Phytopathology, 31, 53- 80. Cook, R. J., & Baker, K. F. (1983). The nature and practice of biological control of plant pathogens. St. Paul, MN: American Phytopathological Society. Cooke, R. C. (1968). Relationships between nematode-destroying fungi and soil-borne phytonematodes. Phytopathology, 58, 909- 913. Cooke, R. C., & Satchuthananthavale, V. E. (1968). Sensitivity to mycostasis of nematode-trapping Hyphomycetes. Transactions of the British Mycological Society, 51,555-561. De Leij, F., & Kerry, B. R. (1991). The nematophagous fungus, Verticillium chlamydosporium, as a potential biological control agent for Meloidogyne arenaria. Revue de Nrmatologie, 14, 157-164. Dobbs, C. G., & Hinson, W. H. (1953). A widespread fungistasis in soil. Nature (London), 172, 197-199. Duddington, C. L. Everard, C. O. R., & Duthoit, C. M. G. (1961). Effect of green manuring and a predaceous fungus on cereal root eelworm on oats. Plant Pathology, 10, 108-109. Duddington, C. L., Jones, F. G. W., & Moriarty, F. (1956a). The effect of predaceous fungus and organic matter upon the soil population of beet eelworm Heterodera schachtii Schm. Nematologica, 1,344-348.

Chapter 26

Controlling Soil-Borne Plant Pathogens

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71 1

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C

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[271 Biological Control in Subtropical and Tropical Crops C. E. KENNETI"

J. A. MCMURTRY

J. w . BEARDSLEY

Division of Biological Control

Department of Entomology University of California Riverside, California

Department of Entomology University of Hawaii at Manoa Honolulu, Hawaii

University of California Albany, California

This undertaking, which resulted in the complete subjugation of the scale, was the first outstanding success in the field of classical biological control. This success generated much interest in the biological method of pest control and, as a consequence, similar efforts against other citrus pests in southern California were soon undertaken. Although few of the many biological control projects in citrus during the succeeding 100 years have been as spectacularly successful as that with the cottony-cushion scale, the number of successful projects far exceeds that on any other crop. Much of the methodology and theory of biological control has been derived from the work on citrus.

INTRODUCTION A comprehensive review of biological control efforts against all tropical and subtropical perennial crops would require an entire volume and is obviously beyond the scope of this chapter. What is presented here reflects, to a considerable extent, the research interests and experience of the authors. We have attempted to review biological control efforts against pests of seven commercially important crops, particularly those in which there has been substantial biological control activity during the past 10 to 15 years: citrus, olive, avocado, tea, coffee, coconut, and banana. Citrus, because of its commercial importance worldwide, as well as the long history of biological control efforts against citrus pests, is treated in more detail than are other crops.

A r m o r e d Scales: Diaspididae

California Red Scale, Aonidiella aurantii (Maskell) According to Ebeling (1959), California red scale is probably the most important citrus pest in the world. It is less widely distributed than the purple scale, but causes greater damage and is more difficult to control. Of oriental origin, it is the most important pest of citrus in California, South Africa, Australia, New Zealand, and northwestern Mexico, and is a major pest in the eastern Mediterranean Basin, North Africa, and parts of South America (Quayle, 1938). Between 1889 and 1947, a great variety of exotic natural enemies was introduced into California for control of the red scale. The earliest efforts emphasized introduction of coccinellid predators, of which more than 40 species were imported between 1889 and 1892 (Compere, 1961). Failure of nearly all these to become established resulted in a greater emphasis on parasitoid introductions. Between 1900

CITRUS Worldwide, some 70 species of insects are considered to be major pests of citrus (Ebeling, 1959). Of these, more than one-third belong to the Homoptera order. Among others, this includes armored scales (Diaspididae), soft scales (Coccidae), fluted scales (Margarodidae), mealybugs (Pseudococcidae), and whiteflies (Aleyrodidae). The most successful biological control projects in citrus have been conducted with examples of these families. In 1888, the vedalia lady beetle, Rodolia (= Novius) cardinalis (Mulsant), was introduced into California from Australia for control of the cottony-cushion scale, Icerya purchasi Maskell, an introduced species that was devastating the citrus industry in southern California (Doutt, 1958).

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and 1908, several species including Aspidiotiphagus citrinus (Crawford), Comperiella bifasciata Howard, and Pteroptrix (= Casca) chinensis (Howard) were imported from southern China. None of these, however, became established (Compere, 1961; Flanders et al., 1958). During and prior to these efforts, an aphelinid parasitoid of unknown origin had been found to parasitize the red scale in southern California. This species, later identified as Aphytis chrysomphali (Mercet), was extensively propagated between 1902 and 1904 and was distributed to orchardists on request, but the early optimism for control of red scale with this parasitoid was not realized (Compere, 1961). Thus, Aphytis material encountered during foreign explorations either was disregarded or, if shipped to California, was identified as A.

chrysomphali. Further introductions of C. bifasciata (all from Japan) were made during 1916 and 1917, 1922, and 1924 (Compere, 1961). In California, the parasitoid failed to reproduce on red scale in the laboratory but was successfully propagated on Chrysomphalus bifasciculatus Ferris in 1924. It again failed to become established on red scale, but was later found to reproduce on the yellow scale, Aonidiella citrina (Coquillett), and was established on this scale in 1931 (Smith, 1942). It was later determined that the host scales in Japan were A. taxus Leonardi and C. bifasciculatus, not A. aurantii and C. aonidum (Linnaeus) as believed. Between 1918 and 1934, various coccinellid predators were imported from South Africa, China, Australia, and South America but none became established (Compere, 1961). In 1924, an Aphytis sp. (presumably A. lingnanensis DeBach but misidentified as A. chrysomphali) was imported from southern China but did not become established. In 1937, Habrolepis rouxi Compere, an encyrtid internal parasitoid of red scale, was imported from South Africa. Widely colonized in southern California, H. rouxi became established only in a very limited area (Flanders, 1944a). Though of little value, this species holds the distinction of being the first intentionally introduced parasitoid to become established on red scale in California. In 1940, Comperiella bifasciata was again imported, this time on red scale collected in southern China (Smith, 1942), and for the first time was successfully propagated on it in California (Flanders, 1943a). Although establishment remained questionable for several years, C. bifasciata eventually spread throughout all but the coastal areas of southern California (DeBach, 1948, DeBach et al., 1955). Studies by Flanders (1944b) and Teran and DeBach (1963) showed that the C. bifasciata from Aonidiella aurantii in China and that from A. taxus and Chrysomphalus bifasciculatus in Japan were distinct biological races, each being limited to its preferred host in the field. Between 1947 and 1949, many shipments of parasitized red scale were sent to California from southern China and Taiwan. From this material only Aphytis lingnanensis from

southern China and Encarsia (= Prospaltella) perniciosi (Tower) (a red scale race) from Taiwan became established (DeBach et al., 1950; DeBach 1953; Rosen & DeBach, 1978). Encarsia perniciosi was relatively common at first, but its eventual range was limited to the coastal areas whereas A. lingnanensis quickly gained dominance and by 1958 had displaced the long-established A. chrysomphali except at a few coastal sites (DeBach & Sundby, 1963). Although A. lingnanensis alone gave good control of red scale in coastal areas, it was ineffective in interior areas. Further exploration for new parasitoids during 1956 and 1957 resulted in the importation of several new species (DeBach, 1959), but of these only A. melinus DeBach from India and Pakistan became established. The other Aphytis species, A. fisheri DeBach and A. proclia (Walker), as well as Coccobius (= Physcus) debachi (Compere & Annecke) and Aspidiotiphagus citrinus, failed to become established. Subsequent importations made between 1960 and 1964 included A. coheni DeBach, A. holoxanthus DeBach (ex Israel, 1960), and A. africanus Quednau (ex South Africa, 1961), all of which failed to become established (Rosen & DeBach, 1978). Following colonization in 1958, Aphytis melinus quickly displaced A. lingnanensis at the original release sites and by 1964 had become dominant on red scale in southern California and had further displaced A. lingnanensis although the latter species remained common or even dominant in some coastal areas (DeBach, 1966, 1969). The general decline in red scale abundance in southern California after 1962 was attributed to A. melinus and A. lingnanensis, with the former being complemented by Comperiella bifasciata in the interior and intermediate areas and the latter, by E. perniciosi in coastal areas (DeBach, 1965a, 1969). Although substantial to complete control has been attained in many districts, only partial control is provided in others (Rosen & DeBach, 1978). DeBach (1962, 1965b) attributed this variability to the different climatic conditions that occur within the citrus belts of southern California. Kfir and Luck (1979) concluded that the negative effects of extreme temperatures on sex ratios and progeny production in A. melinus and A. lingnanensis not only contribute to their ineffectiveness in the more extreme climates of southern California but also may partially explain the displacement of A. lingnanensis by A. melinus. In the more climatically extreme citrus districts of central and northern California, where only A. melinus and C. bifasciata have been established, biological control of red scale is, at best, only partially effective, even though both parasitoids have been present for more than 30 years. Aphytis riyahdi DeBach, introduced from Saudi Arabia (DeBach, 1977), was colonized in central California, but failed to become established. In Australia, attempts to develop biological control of red scale have closely paralleled those in California. Begin-

Chapter 27 BiologicalControl in Subtropical and Tropical Crops ning about 1902, various indeterminate natural enemies were imported but only one parasitoid, thought to be A. chrysomphali, was reported as established in Western Australia (Wilson, 1960). By the 1940s, only one additional species, Comperiella bifasciata, had been established. Subsequent importation of A. melinus (1961) and E. perniciosi (1970) resulted in establishment, but introduction of A. lingnanensis, A. coheni, A. riyahdi, and Habrolepis sp., sometime after 1977, was unsuccessful (Furness et al., 1983). In the Lower Murray Valley (Victoria and South Australia), the long-established A. chrysomphali was found to have been displaced by A. melinus about 1972 to 1974 (Furness et al., 1983). Campbell (1976) documented the decline in red scale abundance following colonization of A. melinus and Furness et al. (1983) credited A. melinus and C. bifasciata with substantial to complete control of the scale. In Queensland, fully effective control was attributed to A. lingnanensis and C. brifasciata (Smith, 1978a). While C. bifasciata had been introduced into Queensland in 1948, the presence of A. lingnanensis apparently was due to natural ecesis, possibly from Victoria, where it had been introduced earlier. Since 1960, introduction of one or more red scale parasitoids has also been undertaken in France, Cyprus, Greece, Sicily, Israel, Morocco, and South Africa. In Mediterranean Basin countries where A. melinus has been established, the parasitoid has, as in Australia, displaced A. chrysomphali within a short period of time (DeBach & Argyriou, 1967; Rosen, 1967; Orphanides, 1984). However, displacement of native or introduced congeners by A. melinus has not always been the rule. Although A. melinus displaced A. chrysomphali in Israel, it did not displace the earlier, accidentally introduced A. coheni (Rosen, 1967) whereas in South Africa the native A. africanus has retained its dominant position despite establishment of A. melinus, A. lingnanensis, and A. coheni (Bedford, 1968; Annecke & Moran, 1982). In addition to California, Australia, and South Africa, partial to complete control has been reported in Chile (Gonzalez, 1969), Cyprus (Orphanides, 1984), Greece (DeBach & Argyriou, 1967), France (Benassy & Bianchi, 1974), and Argentina (Crouzel et al., 1973). In most cases the improved level of control was due to A. melinus but in France C. bifasciata alone was responsible.

Florida Red Scale, Chrysomphalus aonidum (Linnaeus) A polyphagous species of oriental origin, Florida red scale is scattered throughout the tropical and subtropical regions of North, Central, and South America; the Mediterranean Basin; South Africa; Australia; Asia; and the Pacific Islands. It has been reported as particularly damaging to citrus in Israel, Egypt, Lebanon, Brazil, Mexico, Texas, and Florida (Quayle, 1938; Bodenheimer, 1951; Ebeling, 1959). The first attempt to introduce exotic natural enemies of

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C. aonidum took place in Israel from 1945 to 1947 when Comperiella bifasciata was imported from California. This resulted in failure, but renewed attempts in 1956 and 1957 resulted in the importation of Aphytis holoxanthus and Pteroptrix (= Casca) smithi (Compere) from Hong Kong (Rivnay, 1968). Direct colonization of these parasitoids (fewer than 150 A. holoxanthus and ca. 120 P. smithi) resulted in establishment although P. smithi was not recovered in the field until 1960. The rapid natural dispersal of A. holoxanthus, aided by human transfer of parasitized scales, resulted in complete control of Chrysomphalus aonidum throughout the coastal plain citrus districts within 2 to 3 years (Rivnay, 1968; DeBach et al., 1971). Pteroptrix smithi was later found to have dispersed along the coastal plain and while its activity was judged complementary to that of A. holoxanthus, studies by Steinberg et al. (1986) indicate it is now the dominant species. According to Harpaz and Rosen (1971), biological control of what was previously the most serious pest of citrus in Israel permitted the development of an effective integrated control program in citrus. Further introductions and establishment of A. holoxanthus in Mexico, Florida, South Africa, Australia, and Texas have all met with complete subjugation of C. aonidum (Maltby et al., 1968; Selhime et al., 1969; Cilliers, 1971; Smith, 1978b; Annecke & Moran, 1982; Dean, 1982; Bedford, 1989).

Purple Scale, Cornuaspis (= Lepidosaphes) beckii (Newman) This scale has long been recognized as one of the most destructive scale pests of citrus. Considered indigenous to the Far East, it has been a major pest of citrus in parts of Central and South America, Australia, various Mediterranean countries, South Africa, Hawaii, Florida, Texas, and California (DeBach & Landi, 1961). It is highly specific to citrus, rarely being found on other plants. In California, where it gained entry in 1889, purple scale became a major pest in the coastal citrus districts. Efforts toward biological control were initiated as early as 1891 when two coccinellid predators, Orcus chalybeus (Boisduval) and Rhizobius setelles Blackburn [= lophanthae (Blaisdell)], were introduced. Both became established, but only Rhizobius remains common although it is of no importance in purple scale control (Rosen & DeBach, 1978). Many years later, and within a short period of time (1948 to 1950), two new species of parasitoids, later described as Aphytis lepidosaphes Compere and Coccobius (= Physcus)fulvus (Compere & Annecke), were introduced from the Orient (DeBach & Landi, 1961). Following a lengthy colonization program. A. lepidosaphes was found to be established throughout the infested areas. A colonization program for C. fulvus, however, resulted in establishment only at one locality (Rosen & DeBach, 1978). A1-

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though A. lepidosaphes provided only partial control, the rate of scale population increase was greatly reduced (DeBach & Landi, 1961). This degree of control, coupled with a periodic, alternating strip treatment program of oil sprays, provided satisfactory control without disrupting the natural enemies of other citrus pests. Between 1952 and 1968, A. lepidosaphes was shipped to 13 other countries or states, with substantial to complete control of purple scale occurring in most cases (DeBach, 1971). These included Texas (Dean, 1961), Mexico (Maltby et al., 1968), Peru (Herrara, 1964), Chile (Gonzalez, 1969), Greece (DeBach & Argyriou, 1967), France (Benassy et al., 1974), and South Africa (Bedford, 1973; Annecke & Moran, 1982). Concurrent with these efforts, surveys for natural enemies of diaspine scales in many parts of the world (DeBach, 1971) showed that not only was C. beckii more widely dispersed outside the Orient than was previously known but also the highly host-specific A. lepidosaphes had dispersed to as many, or more, countries (13) than it had been deliberately introduced to by man. According to DeBach, A. lepidosaphes appears to be responsible for substantial to complete control in nearly every country where accidental colonization (ecesis) has occurred; see also Rosen (1965) and Fabres (1974). Fortuitous biological control via ecesis has also occurred in other species of Aphytis (DeBach, 1971), but the best documentation is that concerning A. lepidosaphes.

Yellow Scale, Aonidiella citrina (Coquillett) Like the California red scale, this species is also of oriental origin. Its distribution, however, is less extensive than that of California red scale. In addition to California, Florida, and Texas, it also occurs in Mexico, Australia, New Guinea, Japan, China, India, Pakistan, Afghanistan, Iran, Russia, Turkey, Ethiopia, and Argentina. In California, A. citrina had become a serious pest of citrus by the 1880s. At that time and for many years afterward, it was thought to be a strain of California red scale until McKenzie (1937) discovered the morphological characters that separate the two species. Prior to 1900, several species of parasitoids were found to attack the yellow scale in California. These included Encarsia (= Prospaltella) aurantii (Howard), Aspidiotiphagus citrinus, and Aphytis citrinus Compere [= aonidiae (Mercet)]. These were thought to have been accidentally introduced from Japan; and although the near annihilation of yellow scale in the San Gabriel Valley in 1889 was attributed to two of them (Craw, 1891), a similar decline did not occur in other areas of the state (Flanders, 1956). Following the discovery that the Japanese race of Comperiella bifasciata (imported earlier for control of California red scale) reproduced in yellow scale in the laboratory,

mass propagation and colonization were undertaken (Smith, 1942). In southern California, C. bifasciata was credited with effective control within 1 to 3 years following colonization whereas in the more northerly San Joaquin Valley, it did not exert a similar control (Flanders, 1956). In 1948 and 1949, the Chinese race of C. bifasciata was colonized in the San Joaquin Valley and was credited with temporary control in at least one orchard (Flanders, 1956). Later, however, DeBach (1955) and Kennett (1973) found that the Japanese race was capable of effective control in the San Joaquin Valley in the absence of disruptive pesticide treatments. That this control was due to the Japanese race and not the Chinese race was indicated by laboratory tests showing that C. bifasciata reared from field-collected yellow scale did not reproduce in California red scale (Rosen & DeBach, 1978). Many other parasitoids, including several that attack California red scale or other diaspine scales, were released on yellow scale in California between 1953 and 1967, but of these only Aphytis melinus became established on this scale in one county. According to DeBach et al. (1978) the yellow scale had become extinct throughout southern California by 1970. They attributed this to displacement by California red scale, aided by the action of C. bifasciata.

Yanone Scale, Unaspis yanonensis (Kuwana) The yanone, or arrowhead, scale is considered indigenous to China (Ebeling, 1959). In Japan, where it was first found to occur in 1907, it became the most serious insect pest of citrus (Clausen, 1927). In 1964, it was reported to be established in southern France (Commeau & Sola, 1964), where it has become a major pest of citrus (Panis, 1982). Although 18 species of predators and 4 species of parasitoids were recorded as natural enemies of Unaspis yanonensis in Japan, none provided economic control (Murakami, 1975). Attempts to introduce natural enemies of yanone scale began in 1955 when A. lingnanensis was imported from California. This parasitoid, however, failed to become permanently established (Nishida & Yanai, 1965). Subsequent efforts with A. lingnanensis, imported from Hong Kong [where it occurred on U. citri (Comstock)], resulted in temporary establishment, but the parasitoid was unable to overwinter (Tanaka & Inoue, 1977). In 1975, a shipment of U. yanonensis from Hong Kong (derived from citrus fruits exported from China) yielded several specimens of a new Aphytis sp. after receipt in Japan (Tanaka & Inoue, 1977). However, the single live female obtained from this material failed to reproduce on U. yanonensis. In 1980, foreign exploration in China resulted in the introduction of two new parasitoids (Nishino & Takagi, 1981). Both of these, A. yanonensis DeBach & Rosen and

Chapter 27

Biological Control in Subtropical and Tropical Crops

Coccobius fulvus became established at various localities on Kyushu, Shikoku, and Honshu. Preliminary studies (Furuhashi & Nishino, 1983; Yukinari & Kagawa, 1985; Takagi & Ujiye, 1986; Furuhashi & Ohkubo, 1990) of these parasitoids have indicated a potential for highly effective control of U. yanonensis. As with the Florida red scale in Israel, complete control of yanone scale could be the key to development of an integrated control program for citrus pests in Japan. Preliminary field studies with A. yanonensis in France, following introduction in 1984, have given promising resuits (Benassy & Pinet, 1987).

Dictyospermum Scale, Chrysomphalus dictyospermi (Morgan) This highly polyphagous species, widely distributed in subtropical regions, is the most serious insect pest of citrus in the western Mediterranean Basin (Quayle, 1938). It is a major pest in Greece and Iran but a minor pest in Florida, California, Mexico, and South America. In Greece, the dictyospermum or Spanish red scale is considered to be a more serious pest of citrus than either California red scale or purple scale is. Although locally existing parasitoids, including A. chrysomphali, had long been known to be ineffective, apparently no attempts to introduce exotic species had been made prior to 1962 (DeBach & Argyriou, 1967). In 1962 and 1963, A. lingnanensis, A. coheni, and A. melinus were imported from California for control of both C. dictyospermi and Aonidiella aurantii. By 1963, Aphytis melinus was established on both scales (DeBach & Argyriou, 1967) whereas A. lingnanensis and A. coheni, although recovered in low numbers, failed to persist. Within 2 years A. melinus had displaced A. chrysomphali at all original release sites. According to DeBach and Argyriou, the effective rate of dispersal for A. melinus was 75 to 100 km/year. By 1968, only occasional specimens of C. dictyospermi could be found on the previously scale-encrusted trees at the original release sites (DeBach, 1974). Efforts to develop biological control of C. dictyospermi in Italy were begun in 1908 and in France (Corsica) in 1923 (Greathead, 1976). However, it was only after A. melinus was introduced in 1964 (Italy) and 1972 (France) that substantial to complete control was forthcoming (Greathead, 1976; Benassy, 1977; Rosen & DeBach, 1978). In Morocco, complete control was attained following the introduction of A. melinus in 1966 (Benassy & Euverte, 1970) whereas natural ecesis of the parasitoid from Greece has given good control in Turkey (Tuncyureck & Oncuer, 1974). The biological control of dictyospermum scale is most remarkable in that highly successful results have been attained with a parasitoid that had never been found with

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certainty to occur on this scale in the field prior to its colonization in California and Greece (DeBach, 1974).

Rufous Scale, Selenaspidis articulatus (Morgan) The rufous or West Indies scale is widely distributed in tropical and subtropical regions of the world. Its status as a major pest is, however, generally restricted to citrus in the West Indies and northem South America (Talhouk, 1975). In Peru, where S. articulatus was reported as more damaging to citrus than California red scale was (Wille, 1952; Beingolea, 1969), early investigations indicated little or no control by the resident parasitoid-predator complex. Introduction of A. lingnanensis was attempted in 1962 but the parasitoid failed to become established (Beingolea, 1969). However, the conclusion that rufous scale was native to Africa (Ebeling, 1959) led to exploration in Uganda, from which parasitized S. articulatus was shipped to Peru. This material yielded a new species of Aphytis, later described as A. roseni DeBach & Gordh, which was successfully colonized and established (Bartra, 1974). Complete control of rufous scale in the coastal citrus districts was reported by 1975 (Rosen & DeBach, 1978).

U n a r m o r e d or Soft Scales: C o c c i d a e

Black Scale, Saissetia oleae (Olivier) The black scale, a highly polyphagous, cosmopolitan species, is of economic importance mainly on citrus and olive. Though believed native to South Africa (DeLotto, 1976), S. oleae rarely is found on citrus there or in East Africa, central California, and parts of Mexico. It is most important as a pest of citrus in Australia, southern California, Chile, and numerous countries of the Mediterranean Basin. In southern California, where S. oleae became a major pest prior to 1880, attempts at biological control began in 1891 and 1892 with the introduction of various coccinellid predators from Australia. Of these, only Rhizobius ventralis Erichson and Orcus chalybeus became established (Essig, 1931). Additional species of Rhizobius, Orcus, and Leis were introduced from Australia between 1892 and 1902 but none became established (Bartlett, 1978). Introduction of hymenopterous parasitoids began with the introduction of the egg "predator" Scutellista caerulea (Fonscolombe) (= S. cyanea Motschulsky) from South Africa in 1901. This was followed by the introduction of some 30 species of parasitoids and about 10 species of coccinellids over the next six decades (Bartlett, 1969, 1978; Luck, 1981). Of the nine parasitoids that became permanently established, the most important are Metaphycus helvolus (Compete), M. bartletti Annecke & Mynhardt, M. lounsburyi (Howard), Diversi

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nervus elegans Silvestri, and S. caerulea. Metaphycus lounsburyi showed promise following establishment in 1918 (Smith 1921), but it was not until 1940, following the introduction of M. helvolus, that substantial control of S. oleae was attained (Bartlett, 1978). Various facets of the campaign against S. oleae that are of particular interest include the emphasis placed on introduction of coccinellid predators following the earlier success with the vedalia beetle against the cottony-cushion scale, and their failure to become established; the apparent displacement of Moranila californica (Howard), another chalcidoid egg predator, by S. caerulea (Flanders, 1958); failure of the introduced Coccophagus species to attack S. oleae on citrus, their being confined in most cases to the scale on other host plants (Clausen, 1956); the mistaken introduction of the hyperparasitoid Quaylea whittieri Girault, which became notorious for its attack on M. lounsburyi but essentially disappeared in later years (Flanders, 1943); the differing degrees of control achieved on univoltine (inland) and bivoltine (coastal) scale populations; the role of host feeding by M. helvolus in reducing S. oleae populations (DeBach, 1943); the fortuitous near eradication of the nigra scale, Saissetia nigra Nietner, by M. helvolus (Smith, 1944); and the complete elimination of Eucalymnatus tesselatus (Signoret) prior to reaching pest status, also by M. helvolus (Bartlett, 1969). Although the appearance of S. oleae as a pest of citrus in Australia was coincidental to that in California, much of the early (1897 to 1905) efforts to develop biological control was centered on movement of native natural enemies, particularly coccinellid predators, among the several states (Wilson, 1960). During this period, numerous parasitoids were introduced from various countries, including Metaphycus lounsburyi from South Africa and Moranila californica (1902) and Scutellista caerulea from California. Together, these were credited with excellent control of S. oleae in Western Australia (Wilson, 1960). In 1942, Metaphycus helvolus was introduced from California and became established in South Australia. According to Wilson, the general status of S. oleae as a minor pest in Australia is due to both presumably native as well as exotic natural enemies, a quite different result from that in California. In Chile, biological control of S. oleae was initiated in 1903 with the introduction of Rhizobius ventralis, but major efforts were not undertaken until the 1930s when eight species of parasitoids, including Metaphycus lounsburyi, were introduced from California and Peru (Graf Matin & Cortes, 1939; Bartlett, 1978). Of these, only S. caerulea became established. Introduction of M. helvolus, first undertaken in 1943, was unsuccessful, but a later attempt in 1951 resulted in establishment. Duran (1944) reported that the appearance of M. lounsburyi in Chile about 1944 was by ecesis from Peru, where it had been introduced for control of S. oleae on olive. Gonzalez (1969) reported that

M. helvolus and M. lounsburyi were highly effective against S. oleae in areas where the scale is bivoltine but much less so in univoltine areas. Scutellista caerulea, Metaphycusflavus (Howard) and Coccophagus caridei (Brethes) were also credited with aiding in control. Attempts to develop biological control of S. oleae on citrus in the Mediterranean Basin are of more recent origin. As suggested by Greathead (1976), the increase in severity of S. oleae infestations following the advent of synthetic insecticides was possibly responsible for these efforts (see also Rivnay, 1968). Beginning in 1953, with the introduction of several parasitoid species in France, efforts against S. oleae have been undertaken in Italy (1960, 1971), Corsica (1971), Iran (1960), Greece (1962, 1968) and Israel (1963, 1972-1978). The early introductions in France were unsuccessful (Wilson, 1976) but later efforts resulted in establishment of M. helvolus in 1969 and M. lounsburyi in 1976 (Panis, 1979, 1983). The early efforts in Israel also failed to result in establishment of parasitoids (Bartlett, 1978) but subsequent introductions, mostly from South Africa during 1972 to 1977, resulted in establishment of M. helvolus, M. lounsburyi, M. bartletti, and S. caerulea (Wysoki, 1979). Red Wax Scale, Ceroplastes rubens Maskell This coccid is an important pest of many economic plants, including citrus, in southern Asia, Japan, Australasia, and numerous islands in the Pacific Ocean. It also occurs in Kenya and the Seychelles Islands. In Japan, where it was first found in 1897, it soon became a serious pest of citrus in Kyushu and later spread to Honshu and Shikoku. Early attempts to establish natural enemies imported from California (1924) and Hawaii (1932-1938) were unsuccessful (Yasumatsu & Tachikawa, 1949). In 1946, however, surveys of parasitoids attacking C. rubens revealed the presence of a new, highly effective parasitoid in western Kyushu (Yasumatsu, 1951). This parasitoid, first thought to be Anicetus annulatus Timberlake, was later considered to be A. ceroplastis Ishii and finally described as a new species, A. beneficus Ishii and Yasumatsu, in 1957. Beginning in 1948, Anicetus beneficus was colonized throughout the citrus districts of Honshu and Shikoku, where it gave full economic control within three to four host generations (Yasumatsu, 1953). In Korea, significant reductions in densities of C. rubens were achieved within the same time span following introduction of A. beneficus in 1975 (Kim et al., 1979). This case of biological control is of particular interest in that it was suggested (Yasumatsu, 1958) that A. beneficus was native to Japan and possibly arose as a mutation from A. ceroplastis, a closely related species which attacks another species of Ceroplastes in Japan. Although such a phenomenon had not been demonstrated in biological control, an alternative hypothesis that

Chapter 27 BiologicalControl in Subtropical and Tropical Crops

A. beneficus was an accidental introduction also seemed questionable as the parasitoid had not been found to occur naturally outside of Japan. However, the discovery of A. beneficus attacking C. rubens in China (Jiang & Gu, 1983) appears to indicate that the parasitoid came to Japan from China.

White Wax Scale, Ceroplastes destructor Newstead This wax scale is an important pest of citrus in Australia. It has also been reported from citrus in New Zealand, and occurs over much of East and South Africa, where it is thought to have originated. In Australia, the earliest attempt at biological control was undertaken during the 1930s when some 25 species of parasitoids (collected from indeterminate species of Ceroplastes in Kenya and Uganda) were imported (Wilson, 1960). Three of these, Diversinervus elegans, Bothriophryne ceroplastae Compere, and Scutellista caerulea, were reared successfully on C. destructor but only the latter two were released. Neither species, however, became established. Renewed attempts between 1968 and 1973 resulted in the introduction of six parasitoids from South Africa. Four of these became established, of which Anicetus communis Annecke and Paraceraptocerus nyasicus Compere contributed most to the control of C. destructor (Sands et al., 1986). Earlier, Milne (1981) reported a case of complete suppression of C. destructor, principally by A. communis. The eventual outcome of this project further demonstrates that successful biological control most often lies in obtaining natural enemies that attack the target pest in its known or presumed area of origin.

Citricola Scale, Coccus pseudomagnoliarum (Kuwana) This soft scale became a major pest of citrus in southem Califomia following its discovery there about 1907 (Quayle, 1938). Prior to 1951, the scale was known to occur only in Japan, Califomia, and Arizona. Since then, it has been reported from the former Soviet Union (1951), Iran (1963), Turkey (1971), Greece (1972), Sicily (1973), Italy (1976), and Australia (1978). Attempts to develop classical biological control of citricola scale have, to date, been limited to Califomia. While none of these efforts have been successful, the results are of particular interest in that this scale is one of the few citrus pests in Califomia where no progress has been made (Flanders & Bartlett, 1964; Kennett, 1988). Between 1922 and 1985, several attempts with both monophagous and oligophagous parasitoids from Japan failed to result in establishment of any of the six species liberated (Gressitt et al., 1954). In southern California, however, citricola scale eventually was controlled by a complex of parasitoids, in-

71 9

cluding native, cosmopolitan, and exotic species, the latter having been introduced for control of the black scale, Saissetia oleae (Bartlett, 1953; 1969). In central and northern California, where citrus is grown under greater climatic extremes, these same parasitoids have proved to be ineffective, and the scale continues to be an important pest. Failure of the Japanese parasitoids to become established, particularly the host-specific Metaphycus orientalis (Compere) and Microterys okitsuensis Compere, appears to be due to their inability to bridge the hot summer period, at which time the univoltine, even-brooded host scale are too small for parasitoid reproduction (Compere, 1924; Flanders & Bartlett, 1964; Kennett, 1988). The recent appearance of citricola scale in countries other than Japan and the United States suggests that classical biological control may yet be possible in central California through introduction of oligophagous parasitoids found to attack the scale in those countries (Oncuer, 1974; Kennett, 1988). Brown Soft Scale, Coccus hesperidum Linnaeus This soft scale is the most cosmopolitan of the many different coccids that attack citrus. This scale is rarely a major pest of citrus but is prone to quickly reach outbreak status when its natural enemies are disrupted by chemical treatments against other pests. Typical of observations in this regard are those of Beingolea (1969), who stated that while the rarity of C. hesperidum in Peruvian citrus orchards was due to its natural enemies (Metaphycus luteolus Timberlake and Coccophagous quaestor Girault), its potential to become a severe pest became evident following the advent of synthetic pesticides. Many natural enemies are known to attack C. hesperidum throughout the world. In South Africa, for example, this scale is attacked by more than 25 species of chalcidoid wasps (Prinsloo, 1984). Because of its status as a minor pest of citrus, few efforts have been made to develop classical biological control of C. hesperidum. Apparently, the earliest attempts were made during the early 1900s when various, mostly indeterminate, species of parasitoids were introduced into Westem Australia (Wilson, 1960). Records of establishment are lacking for most of these, but the scale is generally kept under substantial control by native and cosmopolitan species. In Texas, where C. hesperidum became an economic pest during the 1950s, various exotic parasitoids were introduced in 1954 and again during the 1960s but none of the five species involved became established (Dean, 1955; Hart et al., 1969). Failure of resident parasitoids and predators to provide control was attributed to interference by ants (Dean, 1955), but later studies indicated drift of pesticides from adjoining crops as the causative factor because few of the resident parasitoids observed earlier could be found (Hart et al., 1969).

720

c . E . Kennett eta/.

This example of natural biological control is an exception to the usual experience where native or cosmopolitan natural enemies tend to be ineffective against exotic pests.

Fluted Scales: Margarodidae

Cottony-Cushion Scale, Icerya purchasi Maskell Native to Australia, this scale has spread throughout most of the subtropical, tropical, and warmer temperate regions of the world. It has a wide host range and is notorious for its ability to severely debilitate or even kill mature trees. This scale is adapted to a wide range of climates and is a pest of many fruit and shade trees, the most important being citrus, mango, and guava. Following its discovery on Acacia in northern California about 1868, the cottony-cushion scale spread rapidly and by 1886 was devastating the citrus industry in southern California. Chemical controls were generally ineffective and damage was so great that many orchardists destroyed their trees. This dire situation led state and federal horticultural officials to consider the importation of insect natural enemies as a possible solution to the problem (Doutt, 1958). Consequently, a search for natural enemies of cottony-cushion scale was conducted in Australia in 1888 and 1889. This resulted in the shipment to California of dipterous parasitoid Cryptochaetum (= Lestophonus) iceryae (Williston), and a coccinellid predator Rodolia (= Vedalia, = Novius) cardinalis (Mulsant). Both readily became established, and while C. iceryae was considered the more promising, its activity was quickly surpassed by the highly voracious R. cardinalis. A second lady beetle, Rodolia koebelei (Horn), was also introduced from Australia in 1892 and although it became established and persisted for many years, it was eventually displaced by R. cardinalis. By late 1889, the scale had been so decimated by the vedalia lady beetle that it was no longer considered even a minor threat to the California citrus industry (Quayle, 1938; Doutt, 1958; DeBach, 1974). While the spectacular control of I. purchasi was credited to R. cardinalis, the eventual role of C. iceryae, as suggested by Smith and Compere (1916), was not recognized until much later. Studies by Quezada and DeBach (1973) showed that Rodolia and Cryptochaetum acted in concert, with the lady beetle tending to displace the fly in the desert areas and the reverse being the case along the coast, whereas in the intermediate (interior) areas, both tended to be commonly present, with their seasonal relative abundances fluctuating according to the prevailing environmental conditions. Since the complete suppression of cottony-cushion scale in California, R. cardinalis has been introduced into some 57 countries, with successful establishment and good control reported in 55 (DeBach, 1964; Bartlett, 1978). In colder

regions, however, the vedalia beetle is often eliminated during winter and recolonization is required to maintain control (Greathead, 1976). In spite of such exceptions, the vedalia beetle has demonstrated an adaptability to a greater range of climatic conditions than any other natural-enemy introduction (Clausen, 1978b). Attempts to introduce C. iceryae into other countries have been more limited and less successful, with only 5 of the 10 cases resulting in establishment (Bartlett, 1978).

Other Fluted Scales: Icerya seychellarum (Westwood), L aegyptiaca (Douglas), and L montserratensis Riley & Howard Introductions of R. cardinalis in various countries for control of these fluted scales have resulted in their control either by the vedalia beetle alone or in conjunction with other native or introduced species such as R. pumila Weise, R. limbatus Motschulsky, R. chermisina Mulsant, Cryptochaetum monophlebi (Skuse), and C. grandicorne Rondini (Kuwana, 1922; Rodriguez-Lopez, 1942; Vesey-Fitzgerald, 1953; Beardsley, 1955; Bedford, 1965).

Mealybugs: Pseudococcidae

Citrophilus Mealybug, Pseudococcus calceolariae (Maskell) Presumably native to Australia, P. calceolariae first appeared as a pest of citrus in California in 1913. It has since been found in New Zealand, Chile, Italy, southern Russia, South Africa, Sardinia, and the Canary Islands. In California, the citrophilus mealybug rapidly reached major pest status in the coastal citrus districts, the infestations far surpassing those of the citrus mealybug (Clausen, 1978b). Periodic colonization of the coccinellid, Cryptolaemus montrouzieri Mulsant, earlier employed for control of the citrus mealybug, was used extensively against P. calceolariae for some years; and, while it provided measurable relief, the need for additional natural enemies became apparent as the mealybug continued to extend its range and increase in severity (Bartlett, 1978). Although the origin of P. calceolariae was unknown, it was deduced by Smith and Compere (1929) to have come from Australia. Foreign exploration, conducted there in 1927 and 1928, resulted in importation of two parasitoids, Coccophagus gurneyi Compere and Hungariella pretiosa (Timberlake), and several predators. Following colonization of the parasitoids in 1928 and 1929, complete control of P. calceolariae was attained within 2 years (Compere & Smith, 1932). Later, Bartlett and Lloyd (1958) found P. calceolariae to be extensively attacked by another parasitoid, Pauridea (= Tetracnemoidea) peregrina (Timberlake), which had been introduced in 1934 for control of the

Chapter 27

Biological Control in Subtropical and Tropical Crops

long-tailed mealybug. The extremely effective control of P. calceolariae in California has been consistently born out not only by the extreme rarity of the mealybug but also by the complete absence of outbreaks following synthetic insecticide applications for other pests (DeBach, 1974; Bartlett, 1978; Clausen, 1978b). According to these authors, the consistency and completeness of this control rivals that of the cottony-cushion scale by Rodolia cardinalis and Cryptochaetum iceryae. Effective control of P. calceolariae on citrus also has been attained in the former Soviet Union (Prokopenko & Mokrousova, 1963) and Chile (Gonzalez, 1969).

Green's Mealybug, Pseudococcus citriculus Green This mealybug, of widespread distribution in East Asia, is also known from Israel, Hawaii, Brazil, and Paraguay. In Israel, where it was first found in 1937, P. citriculus quickly became a serious pest of citrus (Rivnay, 1968). Initially, it was thought to be a closely related species, P. comstocki (Kuwana), but concern as to its identity led to extensive studies (taxonomic, host preference), which indicated that it was not P. comstocki but instead P. citriculus (Bodenheimer, 1951). Surveys during 1939 and 1940 (Rivnay, 1968) showed that while P. citriculus was attacked by many native predators and parasitoids, the degree of control was unsatisfactory. In 1939, while the mealybug's identity was yet unresolved, shipments of P. comstocki from Japan produced several species of parasitoids, among which Clausenia purpurea Ishii and Allotropa burrelli Muesbeck were the most abundant (Rivnay, 1942). The latter species failed to reproduce on P. citriculus, but C. purpurea was readily propagated and colonized. Following this, Rivnay (1946) reported that while resident parasitoids were highly competitive, once C. purpurea was introduced it always became the dominant species. Both Bodenheimer (1951) and Gruenberg [see Bodenheimer (1951)] concluded that none of the natural enemies (i.e., species of Scymnus, Clausenia, Leptomastidea, Leptomastix, and Anagyrus) had become dominant and that effective control would have ensued without the introduction of C. purpurea. However, it was subsequently reported (Rosen, 1967) that C. purpurea alone was responsible for the complete control of P. citriculus, see also DeBach (1974).

Citrus Mealybug, Planococcus citri (Risso) This highly polyphagous mealybug is an important pest of citrus in many parts of the world. In California, it became a serious pest in the coastal citrus districts following its introduction about 1880 (Clausen, 1915). Efforts at biological control began with the introduction of a coccinellid predator Cryptolaemus montrouzieri from eastern Australia in 1892. While the beetle at first often decimated heavy

721

infestations of P. citri, it was generally ineffective and later was found to persist only in milder climates of the immediate coastal areas (Smith & Armitage, 1920). Attempts to utilize hymenopterous parasitoids for control of P. citri began with the introduction of Leptomastidea abnormis (Girault) from Sicily in 1914 (Smith, 1917). This species became established but it was only partially effective (Clausen, 1956, 1978b). A second phase in the campaign against P. cirri began with the development of a method for mass-rearing P. citri on etiolated potato sprouts (Smith & Armitage, 1920, 1931). Utilized at first for the mass culture of Leptomastidea abnormis, this technique was so successful that it was then applied to the mass culture of Cryptolaemus. Between 1916 and 1930, 16 insectaries for Cryptolaemus production were established in the citrus-producing areas (Fisher, 1963). Though this program resulted in the colonization of many millions of Cryptolaemus each year, and was highly successful, the number of insectaries declined to only four by 1963. To a great extent, this was due to the successful biological control of the more serious citrophilus mealybug in 1930. Further attempts to obtain new parasitoids of P. citri resulted in the introduction of Leptomastix dactylopii Howard from Brazil in 1934 (Compere, 1939) and Pauridia peregrina Timberlake from south China in 1950 (Flanders, 1951), but neither of these persisted (Clausen, 1956) in the field. Pauridia peregrina has persisted as an insectary pest, often virtually halting the mealybug production program as a result of its attack on first-instar mealybugs. However, mass culture and periodic colonization of these two parasitoids, in addition to Cryptolaemus, have been credited, along with the earlier established L. abnormis, with reducing the frequency of P. citri outbreaks (DeBach & Hagen, 1964). Subsequent introductions of various mealybug parasitoids, including Anagyrus pseudococci (Girault), were made between 1950 and 1956 (Bartlett & Lloyd, 1958) but all were unsuccessful. Results of biological control campaigns against P. citri in other countries have been quite variable. In Western Australia, where mealybugs (including P. citri) were serious pests of citrus, highly successful control was obtained simply by transference of Cryptolaemus montrouzieri from New South Wales (Wilson, 1960). Elsewhere, results following the introduction of C. montrouzieri have, in most instances, paralleled those in California, with failure of the beetle to become permanently established being due to its inability to survive winter conditions (Wood, 1963; Rosen, 1967; Argyriou, 1969; Beingolea, 1969; Greathead, 1976). Establishment has, in general, been limited to more tropical regions such as Florida and Hawaii and limited areas in several Mediterranean countries (Greathead, 1976). Mass production and periodic colonization of Cryptolaemus have also been practiced with some degree

722

c . E . K e n n e t t e t al.

of success in several Mediterranean countries, including Spain (Gomez-Clemente, 1954) and Italy (Mineo, 1967). In Queensland, mass releases of Leptomastix dactylopii have been used to augment natural populations during periods of scarcity (Smith et al., 1988). Between 1984 and 1987, this program resulted in the reduction of P. cirri-infested fruits to an acceptable level by harvest. Extensive introductions of citrus mealybug parasitoids also have been attempted elsewhere, most often with limited success (Zinna, 1960; Bartlett, 1978; Luck, 1981). However, Beingolea (1969) reported that Pauridea peregrina (an accidental introduction) effectively controlled P. citri in Peru; and Gonzalez (1969) rated the introduced parasitoids L. abrnomis, A. pseudococci, and L. dactylopii as the most important natural enemies in controlling P. citri in Chile. Although the many and varied efforts to obtain complete biological control of P. citri rarely have succeeded, the program of periodic colonization (augmentation) of natural enemies for control of P. citri stands as a landmark in the development of this method of biological pest suppression.

Long-Tailed Mealybug, Pseudococcus longispinus (Targioni-Tozzetti) Cosmopolitan species P. longispinus generally occurs throughout tropical and subtropical climates where it attacks a great variety of plants, including citrus, avocado, and mango. Although its origin is unknown, Flanders (1940) suggested, on the basis of extreme scarcity and high parasitism, that P. longispinus is native to Australia. Following a major outbreak of P. longispinus on citrus in southern California, a parasitoid introduction program was undertaken in 1933. This was facilitated by previously, but recently acquired knowledge concerning parasitoids of P. longispinus in other countries (Flanders, 1940). Consequently, Anarhopus sydneyensis Timberlake was introduced from Australia in 1934; Hungariella peregrina (Compere), from Brazil in 1935; and Anagyrus fusciventris Girault, from Hawaii in 1936. Each of these in turn became established, it later being stated (Flanders, 1940) that A. sydneyensis was the dominant species. Subsequent outbreaks of P. longispinus between 1943 and 1945 led to studies (DeBach, 1949; DeBach et al., 1949) showing the mealybug was attacked by six primary parasitoids and eight predators. Of the parasitoids, Anarhopus sydneyensis was by far the most abundant, followed by Hungariella pretiosa, Coccophagus gurneyi, and H. peregrina. Anagyrus fusciventris, however, was not present. Most abundant among the predators were the brown lacewing (Sympherobius californica Banks), Cryptolaemus montrouzieri, and the green lacewing [Chrysoperla californica (Coquillett)]. From these studies it was concluded that

while the parasitoids were possibly more important than the predators during the spring, predators were the major factor in subjugating the mealybug. Although not unique, this example is unusual in that both exotic and native predators and parasitoids contributed to the suppression of P. longispinus, the native predators perhaps being most important overall. Fortuitously, A. sydneyensis and H. peregrina have provided complete control of P. longispinus on avocado in California (Flanders, 1944c). Similar efforts against P. longispinus on citrus in Israel were initiated in 1953 with the introduction of A. sydneyensis and H. peregrina, but only the latter species became established (Rivnay, 1968).

Whiteflies: A l e y r o d i d a e Citrus Blackfly, Aleurocanthus woglumi Ashby According to Clausen (1978c) the citrus blackfly is endemic to tropical and subtropical Asia, whence it has spread to East Africa, South Africa, the Seychelles Islands, the West Indies, Central America, northern South America, and the United States (Texas and Florida). Although A. woglumi was found in Jamaica in 1913 and quickly spread to Cuba, Panama, and Costa Rica, the initial impetus for biological control did not occur until the late 1920s, following Silvestri's (1926, 1928) publications on aleyrodid parasitoids in Asia. This led to exploration in southern Asia from 1929 to 1931, during which time several parasitoids and predators were sent from Malaya to Cuba (Clausen & Berry, 1932). The first species to be introduced, Eretmocerus serius Silvestri, readily became established whereas later attempts with Encarsia (= Prospaltella) divergens (Silvestri) and E. smithi (Silvestri) met with failure. The coccinellid predators Catana clauseni Chapin and Scymnus smithianus Clausen & Berry, both obtained in Sumatra, were colonized and established in 1930; and although the former species at times nearly eradicated the blackfly, it was unable to persist at low prey densities and was eventually supplanted by Eretmocerus serius. By 1951, C. clauseni could no longer be found in Cuba (Clausen, 1978c). Following the successful control of A. woglumi in Cuba, E. serius was introduced into Jamaica, the Bahamas, Haiti, Costa Rica, Barbados, the Seychelles, Kenya, and South Africa at various times between 1931 and 1959 with generally outstanding results. In Mexico, attempts at biological control began in 1938 when E. serius was introduced from the Canal Zone. Following its failure to become established, E. serius was reintroduced in 1943, this time successfully (Smith et al., 1964). The degree of control, however, was not comparable with that in Cuba and elsewhere in the West Indies, except in areas having continuously high humidity. This led to

Chapter 27

Biological Control in Subtropical and Tropical Crops

further exploration in Asia from 1948 to 1950. The first introductions, Encarsia divergens and E. smithi, sent from Malaya in 1948, failed to become established. Exploration was then moved to India and Pakistan (1949 and 1950), resulting in the shipment of eight parasitoid and two predator species (Smith et al., 1964). Of these, E. smithi, E. clypealis (Silvestri), E. opulenta (Silvestri), and Amitus hesperidum Silvestri became established. Each of these parasitoids demonstrated a capability to control the blackfly under suitable climatic conditions (Clausen, 1978c). While E. smithi appeared to be the most promising species and became dominant over Eretocerus serius, it subsequently came to be dominated by the other three species. Of these, A. hesperidum was found to be adapted to most of the varied climates of Mexico and was the most capable in quickly reducing blackfly infestations. However, as the general abundance of Aleurocanthus woglumi declined over time, Amitus hesperidum came to be dominated by Encarsia clypealis and E. opulenta. Flanders (1969) explained the order of dominance on the basis of the parasitoids' reproductive strategies (as they influenced interspecific competition). The spatial distribution of the three dominant species was also found to be influenced by climatic conditions. Thus, E. opulenta is the overall most effective species, particularly in the more arid regions, whereas E. clypealis is most effective in humid areas and A. hesperidum is the least effective, particularly in hot, dry areas. This example provides support for the general practice of multiple species introductions instead of preselection and introduction of a presumed single "best" species. It seems highly unlikely that the degree of control obtained would have occurred if only one species been introduced on the basis of its distribution and apparent effectiveness in India-Pakistan. Subsequent establishment of E. opulenta or Eretmocerus serius in other countries, either alone, as in E1 Salvador (Quezada, 1974), Kenya (Wheatley, 1964), South Africa (Bedford & Thomas, 1965) and Venezuela (Anonymous, 1978); with another species, as in Barbados (PschornWalcher & Bennett, 1967) and Florida (Dowell et al., 1979); or with two other species, as in Texas (Summy et al., 1983), have all resulted in excellent control. In those cases where multiple species were introduced, Encarsia opulenta became dominant and some degree of displacement of the other species (Eretmocerus serius, A. hesperidum, or Encarsia clypealis) followed. In Jamaica, the introduction of E. opulenta resulted not only in better control but also in displacement of the long-established Eretmocerus serius (van Whervin, 1968).

723

America, the woolly whitefly rarely had been found outside these regions until 1966 when it was simultaneously reported from southern California, the Cote d'Azur in southern France, and the environs of Malaga in Spain. By the 1970s, it had spread to Portugal, Corsica, Italy (including Sicily), Morocco, and Reunion. More recently it has been reported from Hawaii, Texas, Sardinia, and Egypt. In 1967, Amitus spiniferus Brethes, Eretmocerus paulistus Hempel, and an Encarsia sp. were introduced into California from Mexico but only A. spiniferus became established (DeBach & Warner, 1969). Reintroduction of Eretmocerus paulistus from Mexico and Florida in 1968, however, resulted in establishment. Although early results were promising, the work was moved to Baja California, Mexico, in 1970 when a chemical eradication program was undertaken in California. Following the failure of eradication efforts, A. spiniferus and E. paulistus were reintroduced from Baja California in 1971 along with Cales noacki Howard, which had been introduced from Chile in 1970. By 1975, these parasitoids, with C. noacki and A. spiniferus predominating, had effected complete control of Aleurothrixus floccosus in the original area of invasion (San Diego County) and in Baja California (DeBach & Rose, 1976). Surveys in 1983 and 1984 have indicated a good level of control throughout the infested areas of California with only 38% of 566 survey sites showing infestations, most of which were light or spotty (S. C. Warner, personal communication). In 1970, these parasitoids were introduced at Malaga, Spain. While only C. noacki became established, A. floccosus came under complete control throughout the province by 1974 (Greathead, 1976). Similar results have occurred following introduction of C. noacki in France (1971), Reunion (1976), Portugal (1978), and Sicily (1983); and in Hawaii (1981) and Italy (1982), where both C. noacki and Amitus spiniferus were introduced. A possible case of natural ecesis may have occurred with C. noacki in Morocco, where both the parasitoid and A. floccosus were reported to be established in 1973. This example of classical biological control clearly demonstrates the advantages to be gained through a priori knowledge of the natural enemies that attack potentially invasive pest species in their native land or lands. In this case, the many earlier records of parasitoids of A. floccosus in North and South America were of inestimable value in expediting natural-enemy introductions shortly after the invasive trend of this pest became apparent.

Woolly Whitefly, Aleurothrixus floccosus (Maskell)

Orange Spiny Whitefly, Aleurocanthus spiniferus (Quaintance)

Long known as a more or less serious pest of citrus in tropical North America, the Caribbean Islands, and South

Of Asian origin, this whitefly is widely distributed throughout much of that region and is at times a serious

724

c.E. Kennett et aL

pest of citrus in certain areas (Clausen, 1978c). As yet, however, it has not exhibited the same degree of invasiveness as have the other major citrus whiteflies although it is now known to occur in East Africa, Mauritius, Guam, and Hawaii. The first effort to develop biological control of A. spiniferus was conducted in Japan, where it had become a serious pest in Kyushu during the early 1920s. In 1925, Encarsia smithi and a coccinellid predator Cryptognatha sp. were imported from China (Kuwana & Ishii, 1927). Although only E. smithi was established, it quickly provided a complete and lasting control (DeBach, 1974). In Guam, where A. spiniferus was first recorded in 1951, attempts at biological control were initiated in 1952 with the importation of E. smithi, E. clypealis, E. opulenta Silvestri), Eretmocerus serius, and Amitus hesperidum from Mexico (Peterson, 1955). Of these, only Encarsia smithi and A. hesperidum became established, but complete control was obtained with E. smithi predominating. In Hawaii, discovery of Aleurocanthus spiniferus infestations in 1974 was quickly followed by introduction during the same year of Amitus hesperidum from Mexico and E. smithi from Japan. Both of these parasitoids became established (Nakao & Funasaki, 1976), but the degree of control has not been reported.

Citrus Whitefly, Dialeurodes citri (Ashmead) Of Asian origin, the citrus whitefly has, rather sporadically and over a long period of time, invaded various citrusproducing regions in both hemispheres. In the United States, it was known to be a serious pest of citrus in Florida before 1880 and later became of great concern in other Gulf Coast states. In California, where D. citri first appeared in 1907, it has never become a major pest although sporadic minor outbreaks have been observed. In Europe, D. cirri was first found in France about 1945 or 1946. Its subsequent spread throughout much of the Mediterranean Basin has, to a great extent, coincided with that of the woolly whitefly. It is now also known to occur in Sardinia, Italy, Corsica, Corfu, Turkey, Israel, the former Soviet Union, Japan, India, Pakistan, and Taiwan. The earliest attempt to use biological control against D. citri was undertaken in 1910 when the U.S. Department of Agriculture (USDA) sent R. S. Woglum to Asia in search of natural enemies (Woglum, 1913). Some 16 months later, Woglum returned to Florida with cultures of Encarsia (= Prospaltella) lahorensis (Howard) and coccinellid predator Serangium flavescens (Motschulsky), both of which were obtained in what is now Pakistan. Unfortunately, host stages suitable for reproduction were lacking and the stocks were lost. No further attempts to import natural enemies of D. citri were made until 1968 when E. lahorensis was introduced into California (DeBach & Warner, 1969). Further introductions from India, Japan, Hong Kong, and Flor-

ida resulted in the establishment of an Encarsia sp. from India and a coccinellid Delphastus pusillus (LeConte) from Florida (Rose & DeBach, 1981). Studies in California by Rose and DeBach showed that while E. lahorensis was capable of rapid suppression of Dialeurodes cirri and was an efficient searcher at low host densities, it was slow to disperse whereas the Encarsia sp. from India, although less responsive to host population increase, had superior dispersal abilities. Following the establishment of E. lahorensis in Florida in 1977 (some 66 years after the initial attempt), a massive colonization program was conducted throughout the state (Sailer et al., 1984). Within several years the parasitoid had become established in 59 of the state's 67 counties. The generally marked reductions in D. citri abundance, as reported in both Florida and California, suggest a successful conclusion to these biological control campaigns. Substantial results also have been obtained in Italy, where E. lahorensis was established in 1975 (Viggiani & Battaglia, 1983). This parasitoid has also been established in Sardinia, Corfu (1977) and Israel (1980), but the results have not been reported. In the former Soviet Union, where E. lahorensis failed to become established, some success has been reported with introduced parasitic fungi (Aschersonia spp.) and coccinellid Serangium parcesetosa Sicard introduced from India (Shenderovskaya, 1976).

Bayberry Whitefly, Parabemisia myricae (Kuwana) This whitefly appears to be the latest in a series of citrus aleyrodids that have spread into various regions of the world in recent decades. Its discovery in California during the 1970s led the introduction of several aleyrodid parasitoids between 1979 and 1980 (Rose & DeBach, 1992). While an Encarsia sp. and an Eretmocerus sp. were established, and good control was obtained within 4 years, an unintroduced (native ?) species, Eretmocerus debachi (Rose & Rosen), became the overall dominant parasitoid. Psyllids: Psyllidae Although only two species of psyllids have been reported as pests of citrus, both are of major economic importance in that they transmit greening (likubin) disease in citrus. The first species, Diaphorina citri (Kuwayama), is generally distributed over much of Asia and is also known from Brazil, Saudi Arabia, and the islands of Reunion and Mauritius; while on the contrary, the second species, Trioza erythreae (Del Guernica), occurs throughout most of eastern Africa, extending from Sudan to South Africa as well as the islands of Madagascar, Mauritius, Reunion, and St. Helena. In Reunion, where D. citri and T. erythreae occur together, the former generally is restricted to the low eleva-

Chapter 27

Biological Control in Subtropical and Tropical Crops

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I

J J A S O N D J

FIGURE 1 The importance of conserving fungi as biological control agents can be demonstrated by the use of fungicides, as in the case of fungicide treatment effects on incidence of rust (Hemileia vastatrix Berkeley & Broome) on coffee (CoffeR arabica Linnaeus) leaves. The untreated control has seasonally variable incidence with maxima of approximately 50%, whereas plots treated in both years have very low incidence. Plots treated only in the first year have low incidence in that year but subsequently have incidences much higher than the untreated control, indicating the presence of microorganisms important in limiting the disease (after Mulinge & Griffiths, 1974).

Conservation of existing flora may be important in limiting the extent of a number of leaf diseases (Campbell, 1989). These effects are often revealed through the use of fungicides which deplete extant fungi, permitting the development of previously unimportant diseases. Fokkema and de Nooij (1981), for example, evaluated the effects of various fungicides on leaf surface saprotrophs that have been used in biological control. Wide-spectrum fungicides permitted almost no growth of saprotrophs, whereas more selective agents permitted some growth of several genera of saprotrophs. In cases where these saprotroph populations play an important role in limiting disease organisms, the application of fungicides would eliminate their contribution to pathogen suppression. One such case is illustrated by Fokkema and de Nooij (1981). Plants treated with benomyl (a systemic fungicide) had fewer saprotrophs and developed more necrotic leaf area when inoculated with Cochliobolus sativus (Ito & Kuribayashi) Drechsler ex Dastur than nontreated plants (C. sativus is insensitive to benomyl). Another example (Mulinge & Griffiths, 1974) is leaf rust of coffee (Coffea arabica Linnaeus), caused by Hemileia vastatrix Berkeley & Broome. The disease can be controlled by proper application of fungicide. However, if fungicides are applied in one year and not in the next, the disease is worse on the treated plants than on those which did not receive treatments either year (Fig. 1). The elimination of the saprotrophic flora by the fungicide removes their natural suppressing influence on the disease organisms, resulting in greater disease incidence. Here, careful use of selective fungicides will be crucial to conserving the important antagonistic flora and permitting their beneficial action.

Augmentation Biological control of plant pathogens through augmentation is based on mass-culturing antagonistic species and adding them to the cropping system. This is considered augmentation of natural enemy populations, because the organisms used are usually present in the system, but at lower numbers or in locations different from those desired. The purpose of augmentation is to increase the numbers or modify the distribution of the antagonist in the system. In some cases such organisms are taken from one habitat (e.g., the soil) and augmented in another (e.g., the phyllosphere). Augmentation of microbial agents is sometimes termed "introduction" in the plant pathology literature, in the sense of "adding" the microbes to the system (Andrews, 1992; Cook, 1993). The organisms introduced, however, are usually found in a local ecosystem and are not "introduced" from another region of the world (in the sense of Chapter 5). There are several examples where such organisms, when moved to a new habitat (e.g., from the soil to the aboveground part of a plant), colonize and serve as successful biological control agents (Andrews, 1992; Cook, 1993). Augmentation of antagonists of plant disease organisms can generally be of two types, inoculation and inundation. Inoculative releases consist of small amounts of inoculum, with the intention that the organisms in this inoculum will establish populations of the antagonist which will then increase and limit the pathogen population. In inundative releases, a large amount of inoculum is applied, with the expectation that control will result directly from this large initial population, with limited reliance on subsequent population growth. Biological control of plant pathogens may

846

T.S. Bellows

also rely on a hybrid of these two concepts. A large amount of inoculum may be applied, both to increase the population of the antagonist and to improve its distribution to favor biological control, and antagonism can result from both these applied organisms and the increased population of antagonists resulting from their reproduction. Biological control of black-crust (Phyllachora huberi) on rubber tree foliage by the hyperparasites Cylindrosporium concentricum and Dicyma pulvinata (Junqueira & Gasparotto, 1991) is one example of long-term control of a plant pathogen by a single augmentation in an agricultural system (Cook, 1993). In this case, rubber trees were treated with spore suspensions of the antagonists (inundatively), which resuited in control over more than one season. More generally, beneficial microorganisms are added seasonally or more frequently. Stem Diseases

The control of Heterobasidion annosum (Fries) Brefeld, the causative agent of butt rot in conifer stumps, by Phanerochaete gigantea (Fries:Fries) Rattan et al. was one of the first commercially available agents for biological control of a plant pathogen (Campbell, 1989). The disease caused by H. annosum is primarily a disease of managed plantations. The fungus colonizes freshly cut stumps, invades the dying root system, and can then infect nearby trees through natural root grafts, causing death of the trees. Heterobasidion annosum, however, is a poor competitor, and when a stump is intentionally inoculated with Ph. gigantea (and usually with chemical nitrogen sources which encourage the growth of the antagonist), the antagonist rapidly colonizes the resource, excluding future attack by the pathogen and even eliminating existing pathogen infection. (Table 1). Very little inoculum is needed on a freshly cut stump, and the shelf life of the pellet formulation is about 2 months at 22~ The antagonist is able to outcompete H. annosum even when the initial inoculum favors the pathogen by as much as 15:1 (Rishbeth, 1963)

The ascomycete fungi Eutypa armeniaceae Hansford & Carter and Nectria galligena Bresadola in Strass infect apricots and apples, respectively, and cause stem cankers and eventual death of the trees. Pruning wounds in apricots are treated with Fusarium laterium Nees:Fries through specially adapted pruning cutters. Fusarium laterium produces an antibiotic which inhibits germination and growth of E. armeniaceae. When applied, the concentration of the antagonist must be greater than 106 conidia/ml. Integrated application which includes a benzimidazole fungicide gives better control than either fungicide or antagonist alone. Nectria galligena infection can be reduced through sprays of suspensions of Bacillus subtilis or of Cladosporium cladosporioides (Fresenius) de Vries. These are not in current commercial use because apples are currently sprayed for Venturia inaequalis (Cooke) G. Winter (apple scab) so frequently that N. galligena is controlled by those sprays. Crown gall is a stem disease caused by the bacterium Agrobacterium tumefaciens (Smith & Townsend) Conn. It affects both woody and herbaceous plants in 93 families. Infection is typically from the soil, rhizosphere, or pruning tools. Control can be effected by treating plants with a suspension of a related saprotrophic bacterium, Agrobacterium radiobacter (Beijerink & van Delden) Conn strain K84. This strain of the bacterium produces an antibiotic which is taken up by a specific transport system in the pathogen bacterium, which is then killed. The commercially available formulations of this agent are effective primarily against pathogen strains which attack stone fruits, but other bacteria are under investigation for use against strains pathogenic in other crops. This agent has been altered by genemodifying technology to produce a new strain (strain 1024) which lacks the ability to transfer antibiotic resistance to the target bacterium. The fungus Chondrostereum purpureum (Persoon:Fries) Pouzar infects stems of fruit trees and produces a toxin which leads to a condition known as silverleaf disease. Stems can be inoculated with a species of Trichoderma

TABLE 1 Colonization of Scots Pine Stumps (Pinus sylvestris Linnaeus) after Inoculation with Various Fungi as Antagonists to Heterobasidion annosum (Fries) Brefeld (Which Was Inoculated into All Stumps) (after Rishbeth, 1963) Percentage of mean area of stump section colonized after 10 weeks

6 months Ha

Inoculated Antagonist

Antagonist

pga

Ha b

Antagonist

Pg

None Botrytis cinerea Persoon:Fries Trichoderma viride Persoon:Fries Leptographium lundbergii Lagerberg & Melin Phanerochaete gigantea (Fries:Fries) Rattan et al.

28 5 10 9 80

38 55 65 5 Trace

--

80

7

5 0 95 80

0 0 37 75

0 43 47 75

25 40 0 0

gigantes (Fries:Fries) Rattan et al. bHeterobasidion annosum (Fries) Brefeld. aphanerochaete

Chapter 32 Foliar, Flower, and Fruit Pathogens grown on wooden dowels or prepared as pellets which are inserted into holes bored in the affected stem. Treated stems recover from the disease more rapidly than untreated stems. The Trichoderma sp. can be applied to pruning wounds to prevent initial establishment of C. purpureum.

Leaf Diseases

Control of leaf diseases at the time of pathogen germination has been shown in the laboratory. This control occurs in the presence of competitive organisms, which may include fungi, yeast, or bacteria. The mode of action in some cases is competition for nutrients which, together with water, are necessary for successful germination and invasion of many pathogens. The germination of Botrytis sp., for example, is inhibited by certain bacteria and yeasts (Blakeman & Brodie, 1977). This inhibition is less pronounced when additional nutrients are supplied, indicating that the mechanism is, at least in part, resource competition. Studies on control of botrytis rot in lettuce (Wood, 1951) indicated that several organisms were successful in suppressing the disease when sprayed on lettuce plants, among them species of Pseudomonas, Streptomyces, Trichoderma viride, and Fusarium. Peng and Sutton (1991) evaluated 230 isolates of mycelial fungi, yeasts, and bacteria and tested them as antagonists of B. cinerea in strawberry in both laboratory and field trials. Several organisms (including members of each taxonomic group tested) were effec-

TABLE 2

847

tive, some as effective as captan (a commercial fungicide) (Table 2). Sutton and Peng (1993b) further evaluated Gliocladium roseum and determined that the suppression of B. cinera by this antagonist was probably a result of competition for leaf substrate. The fungi Gliocladium roseum and Myrothecium verrucaria (Albertini & Schweinitz) Ditmar were also effective in suppressing B. cinerea in black spruce (Picea mariana [Miller] Britton Steams Poggenburg) seedlings (Zhang et al., 1994). Bacteria may also be used to limit frost damage to leaves and blossoms of plants. Certain bacterial species such as Pseudomonas syringae and Erwinia herbicola serve as nucleation sites on leaves for the formation of ice, and in their presence ice forms soon after temperatures fall below freezing. If these ice-nucleating bacteria are replaced by competitive antagonists (such as certain strains of Ps. syringae) that lack the protein that causes ice nucleation, frost is prevented even at temperatures from - 2 to - 5 ~ (Lindow, 1985). The protective bacteria, after being applied to the leaves, colonize them for up to 2 months, an interval suitable to protect from frost during the limited season that low temperatures are likely. A naturally occurring, non-ice-nucleating strain of Ps. fluorescens is registered in the United States as a commercial product (Frostban B) for suppression of frost damage (Wilson & Lindow, 1994). Spraying suspensions of propagules, generally at high concentrations, is the principal method for applying biological control agents to foliage (and to flowers), and dusts

Effects of Various Microorganisms and Captan on Incidence of Botrytis cinerea Persoon:Fries in Stamens and Fruits of Strawberry in Field Plots a Incidence of B. cinerea (%) Cambridge plots

Arkell plots

Treatment

Stamens

Fruits

Stamens

Fruits

Water check Botrytis cinerea Fries:Persoon check Captan Bacillus sp. Cryptococcus laurentii (Kufferath) Skinner Rhodotorula glutinis (Fresenius) Harrison Alternaria alternata (Fries) Kessler Myrothecium verrucaria (Albertini & Schweinitz) Ditmar Fusarium graminearum Schwabe Fusarium sp. Drechslera sp. Trichoderma roseum (Persoon) Link Epicoccum purpurascens Ehrenberg ex Schlechtendal Colletotrichum gloeosporioides Penzig Trichoderma viride Persoon:Fries Penicillium sp. Gliocladium roseum Link:Bainer

4b 19 a 5b 15 a 17 a 6b 9b 15 a 18 a 17 a

35 c 59 a 40b 56 a 43 b 33 c 51 a 48 b 47 b 46 b

2b 16 a 3b 12 a 11 a 12 a 3b 13 a 16 a 16 a

59 b 71 a 56b 74 a 72 a 48 c 52c 60 b 65 a 64 a

16 a

26 c

9 a

56 b

12 a 6b 4b 5b 4b 4b

27 c 43b 44b 38 b 14d 25c

13 a 4b 6b 2b 1b 3b

41 c 51 c 41 c 37 c 38c 43c

a All plots were treated with suspensions of conidia of B. cinerea. Several antagonists were as effective as captan in reducing incidence of the pathogen (after Peng & Sutton, 1991) (values in columns followed by the same letter did not differ significantly).

848

T.S. Bellows

(such as lyophilized bacterial preparations) are also used. Spray methodology has yet to be refined in terms of sprayer characteristics, droplet size, pressures, etc., and other methods of application with greater efficiency may be necessary to effectively target certain plant parts (Sutton & Peng, 1993a). Flower Diseases

One of the principal diseases of flowers of rosaceous plants is fire blight, which is particularly severe on pear (Campbell, 1989). The causal bacterium, Erwinia amylovora, also occurs on leaves and may cause stem cankers. The bacterium is transferred by insects to flowers in the spring from overwintering sites on stem cankers and subsequently from flower to flower. Infection enters the pedicel and from there the stem. Infected flowers and small stems die, and cankers form on other stems. Chemical control is difficult and expensive and is sometimes ineffective because of resistance to copper compounds and streptomycin. Biological control has been effective using Erwinia herbicola, sometimes in combination with Pseudomonas syringae (Wilson & Lindow, 1993). Suspensions of E. herbicola are sprayed onto the flowers just prior to the period of potential infection. The antagonist occupies the same niche as the pathogen, reducing the numbers of E. amylovora by competition, and there is also evidence for the production of bacteriocins (chemicals which suppress population growth of related bacteria) by some strains. Control can be good, comparable to that achieved by commercial bactericides, though repeated application of the bacterium is necessary (Isenbeck & Schultz, 1986). Another approach to control is to reduce secondary infections on leaves, which leads to reductions in the overwintering population of the pathogen. This control is achieved by treatment with the antagonists Ps. syringae and other bacteria (Lindow, 1985). A novel approach to dissemination of the antagonistic bacteria has been evaluated by Thomson et al. (1992). These workers mixed E. herbicola and Ps. fluorescens with pollen in a special apparatus at the entrance to honeybee (Apis mellifera Linnaeus) hives. Bees emerging from these hives through the mixtures transmitted the antagonists to the flowers efficiently, although disease control was not evaluated because of absence of disease in the test orchards. Johnson et al. (1993) report efffective control of E. amylovora using Ps. fluorescens strain A506 and E. herbicola strain C9-1. Crab apple has been proposed as a model system to further explore the possibilities of biological control of fire blight (Pusey, 1997). Fruit Diseases

Fruits are subject to attack both by general pathogens (Botrytis, Rhizopus, and Penicillium) and by a few more

specialist pathogens such as Colletotrichum coffeanum Noack, the causative agent of coffee berry disease, and Monilinia spp. brown rots of rosaceous fruits. Although many of these are controlled by fungicides, Trichoderma viride has been shown to limit disease from Monilinia spp. Various Bacillus spp. also are antagonistic to these fungi through production of antibiotics and by reducing the longevity and germination of spores. Both the bacteria and culture filtrates have been used with some success against these pathogenic fungi, but there has been no commercial development, probably because fungicides used routinely in orchards for control of other diseases give some control of brown rot (Campbell, 1989). Among the most serious diseases of soft fruits are postharvest rots (Dennis, 1983), especially those caused by Botrytis cinerea. Potential for biological control of postharvest diseases has been reviewed by Wilson and Wisniewski (1989). In strawberries, the B. cinerea grows saprotrophically on crop debris, and from there infects flowers or fruit. Various species of Trichoderma have been evaluated and were as effective as standard fungicides (Tronsmo & Dennis, 1977). The antagonists Cladosporium herbarum and Penicillium sp. gave excellent results in controlling botrytis rot on tomato (Newhook, 1957). Honeybees have been used to distribute Gliocladium roseum to strawberry flowers (Peng et al., 1992) and raspberry (Sutton & Peng, 1993a) to suppress botrytis rot. Selected isolates of Aureobasidium pullulans (de Bary) G. Arnaud, Rhodotorula glutinis (Fresen.) F. C. Harrison, and Bacilis subtilis reduced size and number of postharvest lesions on apple fruit when applied to apple trees in the field late in the growing season (Leibinger et al., 1997).

I n d u c e d Resistance Leaf and Stem Diseases

Induced resistance can control anthracnose diseases caused by Colletotrichum spp. (Ktic, 1981; Dean & Ktic, 1986). Colletotrichum lindemuthianum (Saccardo & Magnus) Lamson-Scribner causes anthracnose of beans, Colletotrichum lagenarium (Passerine) Saccardo causes cucumber anthracnose, and Cladosporium cucumerinum Ellis & Arthur causes scab in cucumbers. Inoculation of cucumbers with Colletotrichum linclemuthianum (which does not cause disease in cucumbers) makes the plants resistant to both Colletotrichum lagenarium and Cladosporium cucumerinure. Treatment may be applied to an early leaf and protection subsequently appears in later leaves, even if the initially inoculated leaf is removed. The factor causing resistance travels systemically through the plant. Variations on this approach include inoculating an early leaf with a pathogen, inducing resistance throughout the plant, and then removing the infected leaf. Induced resistance also

Chapter 32

Foliar, Flower, and Fruit Pathogens

849

FIGURE 2 Example of hypovirulence in American chestnut (Castanea dentata [Marsham] Borkjauser) inoculated with normal (control) and hypovirulent strains of Cryphonectria parasitica (Murrill) Barr. "8 around" is eight individual strains placed around a canker (after Jaynes & Elliston, 1980).

occurs in some virus diseases (Thomson, 1958) and may last for years, as in the case of healthy citrus seedlings being inoculated with an avirulent strain of citrus tristeza virus. Stem rot in carnations, caused by Fusarium roseum Link:Fries 'Avenaceum', can be prevented by inoculating wounds inflicted during propagation with the nonpathogenic F. roseum 'Gibbosum'. This inoculation produced a germination inhibitor and also reduced the time needed for the stems to develop resistance to the pathogen. This hastening of resistance was caused by activation of the host's

defense mechanisms and is another example of induced resistance. Induction of resistance is discussed more fully in Chapter 19. Hypovirulence Chestnut blight, caused by Cryphonectria parasitica, is controlled by employing naturally occurring hypovirulent strains of the disease pathogen. A number of hypovirulent strains are known, and natural spread of hypovirulent strains in Europe helps to limit damage there (Heiniger & Rigling, 1994). Inoculation of infected trees with a hypovirulent strain leads to reduced canker size and greater stem survival (Fig. 2). In applied programs hypovirulent strains are inoculated into infected trees at the rate of 10 inoculated trees/ha. The hypovirulent strain spreads from these locations and, on contacting more virulent strains, fuses with these strains and exchanges a dsRNA viral element present in the hypovirulent strain (Jaynes & Elliston, 1980; Heiniger & Rigling, 1994; see also Chapter 25). The dsRNA element, which causes hypovirulence, is transferred to the virulent strains and attenuates their effects. Active cankers are eliminated in 10 years (van Alfen, 1982). Parasitism of P a t h o g e n s

FIGURE 3 Percentage of soybean (Glycine max [Linnaeus]) plants showing symptoms of systemic blight after leaves were inoculated with different strains of Bdellovibrio bacteriovorus Stolp & Starr mixed in varying ratios with the pathogen Pseudomonas syringae pv. glycinae (Coeper) Young, Dye & Wilkie (after Scherff, 1973).

Leaf Diseases

Some plant pathogens, including fungi and some bacteria, are known to be attacked by other pathogens. Bdellovibrio bacteriovorus is a bacterium that can attack other bac-

850

T.S. Bellows

teria by penetrating the cell wall and lysing the host bacterium, subsequently reproducing inside the host. Different strains of Bd. bacteriovorus have been examined for virulence against Pseudomonas syringae pv. glycinae (Coeper) Young, Dye & Wilkie, the cause of soybean blight. By applying Bd. bacteriovorus at sufficiently high rates, disease symptoms were reduced more than 95% (Scherff, 1973) (Fig. 3). Parasites of fungi pathogenic on leaves are numerous (Kranz, 1981), but only a few have been studied in much detail, such as Sphaerellopsis filum, Verticillium lecanii, and Ampelomyces quisqualis. The mycoparasitic fungus typically penetrates the host hypha or spore and kills it. Some of the control may be from the antagonist overgrowing the sporulating pustules of the pathogen and preventing spore release, thus reducing inoculum in the environment, even if the spores are not killed. A typical problem with implementation of these mycoparasitic fungi is that they often do not affect a large proportion of the pathogens unless humidity and temperature are high. Consequently, although much reduction of spore production may take place, there is still sufficient inoculum of the pathogen remaining to cause disease. These mycoparasites often are seen naturally only at high incidences of disease, which is unsuitable for general economic control of the target pathogens. They may have some use as augmented agents in particular systems, either in the tropics or in greenhouses, where environmental conditions are more favorable.

DEVELOPING AND USING BENEFICIAL SPECIES Growth of our knowledge about biological control of plant diseases has been extensive since the first experimental reports (Hartley, 1921; Sanford, 1926; Millard & Taylor, 1927; Henry, 1931), and substantial potential for microbial control of pathogens has been demonstrated. A number of products or programs have reached the stage of commercial development or availability (Table 3). Products in current use include both those aimed at specialty markets, such as control of certain stem or flower diseases for which chemical control is either unavailable or expensive, and other products aimed at larger scale markets such as seed treatments for cotton and soybeans. The cycle for research, development, and implementation of antagonists of plant pathogens is composed of several steps. These include initial discovery of candidate agents; refinement of our knowledge of their biology, ecology, and mode of action; microcosm and field trials of their efficacy; and large-scale development for commercial production. The first challenge in the development of a biological control program is the discovery process. Many microorganisms show potential as antagonists of particular patho-

gens. Protocols have been proposed to make the process of screening these candidates more efficient (Andrews, 1992; Cook, 1993). The principal difficulties are screening out candidates that are effective only during in vitro (agar plate) trials but are not effective in natural settings, and in selecting candidates that can be successfully cultured in large quantities. Following discovery of suitable candidates, research focuses on their mode of action and on factors which may enhance or limit their efficacy in targeted settings (greenhouses, field plots). In addition, experimental fermentation and formulations must be developed for production of materials suitable for use in agricultural settings. Finally, issues of large-scale production and delivery must be addressed. Products for use must be effective on an economical basis, and economies of scale may play an important role in the eventual availability of any organisms or product. Products must have a satisfactory shelf life, and safe and effective methods for application must be discovered or developed (Cook, 1993; Sutton & Peng, 1993a). Such application methods might include sprays of suspensions or dusts, contact application, bee vectoring, and production of antagonists in a crop environment (Sutton & Peng, 1993a). The adoption of any biological control agent in commercial agriculture is dependent on its reliability and its availability. Limitations to the process of eventual adoption therefore include cost of development and size of potential market. Many pesticides for control of plant diseases have a broad spectrum of activity, are applicable in a variety of crops and settings, and may act either prophylactically, therapeutically, or both. Biological controls, in contrast, often have narrow ranges of activity because of their biology and may work in only a few crops or field settings because of their ecology. Although they can often act both prophylactically and therapeutically, their action may take some time to develop. Hence they may have a much narrower market than a chemical pesticide and be unattractive for development by major corporations (Andrews, 1992). In this context, it may be appropriate for public institutions such as government experiment stations to undertake the development of such biological controls, in the same way that they take the responsibility for development of new plant varieties (Cook, 1993). Microorganisms intended for use as biological control agents must be viewed in a biological rather than a chemical paradigm (Cook, 1993). Where an effective pesticide may work in many places, each place may have unique soil, edaphic, and biological features which limit or enhance the effectiveness of microbial antagonists of pathogens. Consequently, each microbial biological control system may have to make use of locally adapted strains, taking advantage of resident antagonistic flora and fauna and augmenting their effectiveness with additional species or strains or enhancing resident populations (as through soil amendments or other modifications to the environment or crop).

Chapter 32 TABLE 3

Foliar, Flower, and Fruit Pathogens

85 |

S o m e Commercially Available A n t a g o n i s t s or Products for Control of Foliar-, Flower-, and Fruit-Infecting Plant P a t h o g e n s Organism

Trade name

Target

Agrobacterium radiobacter (Beijerink & van Delden) Conn strain K-84

Agtrol; Galltrol; Norbac 84-C

Agrobacterium tumefaciens (Smith & Townsend) Conn (crown gall)

Pseudomonas cepacia (Burkholder) Palleroni and Holmes

Blue Circle; Intercept

Rhizoctonia spp., Pythium spp., and Fusarium spp. diseases of seedlings

Pseudomonas fluorescens Migula

Dagger G

Rhizoctonia spp. and Pythium spp. diseases of seedlings

Coniothyrium minitans Campbell

Coniothyrin

Sclerotinia sclerotiorum (Libert) de Bary in sunflower

Fusarium oxysporum Schlechtendal (nonpathogenic strains)

Fusaclean; Biofox C

Diseases froom pathogenic strains of Fusarium oxysporum

Gliocladium virens Millers, Giddens & Foster

GlioGard

Rhizoctonia spp. and Pythium spp. diseases of seedlings and bedding plants

Phanerochaete gigantea (Fries:Fries) Rattan et al.

Heterobasidion annosum (Fries) Brefeld (butt rot)

Pythium oligandrum Drechsler Streptomyces griseovirides Anderson et al. Trichoderma harzianum polysporum (Link) Rifai

Polygandron Mycostop BINAB

Pythium ultimum Trow in sugar beet Alternaria sp. and Fusarium spp. diseases Wood rot fungi; Verticillium malthousei Ware in mushrooms

Trichoderma harzianum Rifai

F-Stop; Trichodex; Supravit; T-35; TY

Heterobasidion annosum; diseases caused by Rhizoctonia spp., Pythium spp., Fusarium spp., Botrytis cinerea Persoon:Fries, and Scleotium rolfsii Saccardo

Trichoderma lignorum (Tode) Harz

Trichodermin-3

Rhizoctonia spp. and Fusarium spp. diseases

A l t h o u g h d i f f e r e n t strains m a y use c o m m o n m e c h a n i s m s to a c h i e v e b i o l o g i c a l c o n t r o l (such as p r o d u c t i o n o f antibiotics), c o m p e t i t i v e abilities a d a p t e d to l o c a l c o n d i t i o n s m a y be vital to p e r m i t the o r g a n i s m s to c o m p e t e for r e s o u r c e s and effectively control pathogens.

References Adams, P. B. (1990). The potential of mycoparasites for biological control of plant diseases. Annual Review of Phytopathology, 28, 59-72. Andrews, J. H. (1992). Biological control in the phyllosphere. Annual Review of Phytopathology, 30, 603-635. Andrews, J. H., & Harris, R. F. (1986). r- and K-selection and microbial ecology. Advances in Microbial Ecology, 9, 99-147. Bailey, J. A., Ed. (1986). "Biology and Molecular Biology of PlantPathogen Interactions." Springer-Verlag, Berlin; New York. Beer, S. V., Rundle, J. R., & Norielli, J. L. (1984). Recent progress in the development of biological control for fire blight. Acta Horticulturae, 151, 195-201. Begon, M., Harper, J. L., & Townsend, C. R. (1986). "Ecology: Individuals, Populations and Communities." Blackwell Sci., Oxford. Blakeman, J. P., & Brodie, I. D. S. (1977). Competition for nutrients between epiphytic microorganisms and germination of spores of plant pathogens on beetroot leaves. Physiological Plant Pathology, 10, 29-42. Campbell, R. (1989). "Biological Control of Microbial Plant Pathogens." Cambridge Univ. Press, Cambridge, U.K. Cook, R. J. (1993). Making greater use of introduced microorganisms for biological control of plant pathogens. Annual Review of Phytopatholo~y, 31, 53-80. Cook, R. J., & Baker, K. F. (1983). "The Nature and Practice of Biological Control of Plant Pathogens." American Phytopathological Society, St. Paul, MN.

Dean, R. A., & Kfic, J. (1986). Induced systemic protection in cucumber: Time of production and movement of the signal. Phytopathology, 76, 966-970. Dennis, C., Ed. (1983). "Post-Harvest Pathology of Fruits and Vegetables." Academic Press, London. E1-Ghaouth, A., Wilson, C. L., & Wisniewski, M. (1998). Ultrastructural and cytochemical aspects of the biological control of Botrytis cinerea by Candida saitoana in apple fruit. Phytopathology, 88, 282-291. Elad, Y. (1986). Mechanisms of interactions between rhizosphere microorganisms and soil-borne plant pathogens. In "Microbial Communities in Soil" (V. Jensen, A. Kjoller, & L. H. Sorensen, Eds.), pp. 49-60. Elsevier, New York. Fokkema, N. J., & de Nooij, M. P. (1981). The effect of fungicides on the microbial balance in the phyllosphere. European and Mediterranean Plant Protection Organization Bulletin, 11,303- 310. Fokkema, N. J., & van den Heuval, J. (1986). "Microbiology of the Phyllosphere." Cambridge Univ. Press, Cambridge, U.K. Hartley, C. (1921). Damping off in forest nurseries. USDA Bulletin 934, 1-99. Heiniger, U., & Rigling, D. (1994). Biological control of chestnut blight in Europe. Annual Review of Phytopathology, 32, 581-599. Henry, A. W. (1931). The natural microflora of the soil in relation to the foot rot problem of wheat. Canadian Journal of Research, 4, 69-77. Isenbeck, M., & Schultz, F. A. (1986). Biological control of fireblight (Erwinia amylovora [Burr.] Winslow et al.) on ornamentals. II. Investigation about the mode of action of the antagonistic bacteria. Journal of Phytopathology, 116, 308- 314. Jaynes, R. A., & Elliston, J. E. (1980). Pathogenicity and canker control by mixtures of hypovirulent strains of Endothia parasitica in American chestnut. Phytopathology, 70, 453-456. Jeffries, P., & Jeger, M. J. (1990). The biological control of postharvest diseases of fruit. Biocontrol News and Information, 11,333-336. Johnson, K. B., Stockwell, V. O., McLaughlin, R. J., Sugar, D., Loper, J. E., & Roberts, R. G. (1993). Effect of antagonistic bacteria on estab-

85Z

T.S. Bellows

lishment of honey bee-disperesed Erwinia amylovora in pear blossoms and on fire blight control. Phytopathology, 83, 995-1002. Junqueira, N. T. V., & Gasparotto, L. (1991). Controle biol6gico de fungos estrom~iticos causadores de doenqas foliares em Seringueira. In "Controle Biol6gico de Doenqas de Plantas," pp. 307-331. Org. W. Bettiol., Brasilia, DF: EMBRAPA. Kranz, J. (1981). Hyperparasitism of biotrophic fungi. In "Microbial Ecology of the Phylloplane" (J. P. Blakeman, Ed.), pp. 327-352. Academic Press, London. Kfic, J. (1981). Multiple mechanisms, reaction rates and induced resistance in plants. In "Plant Disease Control" (R. C. Staples & G. H. Toenniessen, Eds.), pp. 259-284. Wiley, New York. Leibinger, W., Breuder, B., Hahn, M., & Mendgen, K. (1997). Control of postharvest pathogens and colonization of the apple surface by antagonistic microorganisms in the field. Phytopathology, 87, 1103-1110. Lindow, S. E. (1985). Integrated control and the role of antibiosis in biological control of fireblight and frost injury. In "Biological Control on the Phylloplane" (C. E. Windels & S. E. Lindow, Eds.), pp. 83115. American Phytopathological Society, St. Paul, MN. Lynch, J. M. (1987). Biological control within microbial communities of the rhizosphere. In "Ecology of Microbial Communities" (M. Fletcher, T. R. G. Gray, & J. G. Jones, Eds.), pp. 55-82 [Society of General Microbiology Symposium 41]. Cambridge Univ. Press, Cambridge, U.K. Millard, W. A., & Taylor, C. B. (1927). Antagonism of microorganisms as the controlling factor in the inhibition of scab by green manuring. Annals of Applied Biology, 14, 202-216. Mulinge, S. K., & Griffiths, E. (1974). Effects of fungicides on leaf rust, berry disease, foliation and yield of coffee. Transactions of the British Mycological Society, 62, 495-507. Newhook, F. J. (1957). The relationship of saprophytic antagonism to control Botrytis cinerea Pers. on tomatoes. New Zealand Journal of Science and Technology, Series A, 38, 473-481. Parker, C. A., Rovira, A. D., Moore, K. J., Wong, P. T. W., & Kollmorgen, J. F., Eds. (1985). "Ecology and Management of Soilborne Plant Pathogens." American Phytopathological Society, St. Paul, MN. Peng, G., & Sutton, J. C. (1991). Evaluation of microorganisms for biocontrol of Botrytis cinerea in strawberry. Canadian Journal of Plant Pathology, 13, 247-257. Peng, G., Sutton, J. C., & Kevan, P. G. (1992). Effectiveness of honey bees for applying the biocontrol agent Gliocladium roseum to strawberry flowers to suppress Botrytis cinerea. Canadian Journal of Plant Pathology, 14, 117-129. Pusey, P. L. (1997). Crab apple blossoms as a model for research on biological control of fire blight. Phytopathology, 87, 1096-1102.

Rishbeth, J. (1963). Stump protection against Fomes annosus. III. Inoculation with Peniophora gigantea. Annals of Applied Biology 52, 6377. Sanford, G. B. (1926). Some factors affecting the pathogenicity of Actinomyces scabies. Phytopathology, 16, 525-547. Scherff, R. H. (1973). Control of bacterial blight of soybean by Bdellovibrio bacteriovorus. Phytopathology, 63,400-402. Sutton, J. C., & Peng, G. (1993a). Manipulation and vectoring of biocontrol organisms to manage foliage and fruit diseases in cropping systems. Annual Review of Phytopathology, 31,473-493. Sutton, J. C., & Peng, G. (1993b). Biocontrol of Botrytis cinerea in strawberry leaves. Phytopathology, 83, 615-621. Thomson, A. D. (1958). Interference between plant viruses. Nature, 181, 1547-1548. Thomson, S. V., Hanson, D. R., Flint, K. M., & Vandenberg, J. D. (1992). Dissemination of bacteria antagonistic to Erwinia amulovora by honey bees. Plant Disease, 76, 1052-1056. Tjamos, E. C., Papavizas, G. C., & Cook, R. J., Eds. (1992). "Biological Control of Plant Disease." Plenum, New York. Tronsmo, A., & Dennis, C. (1977). The use of [antagonistic] Trichoderma species to control strawberry fruit rots [caused by Botrytis cinerea, Mucor mucedo]. Netherlands Journal of Plant Pathology, 83 (Suppl. 1), 449-455. van Alfen, N. K. (1982). Biology and potential for disease control of hypovirulence of Endothia parasitica. Annual Review of Phytopathology, 20, 349-362. Wilson, C. L., & Wisniewski, M. E. (1989). Biological control of postharvest diseases of fruits and vegetables: An emerging technology. Annual Review of Phytopathology, 27, 425-441. Wilson, M., & Lindow, S. E. (1993). Interactions between the biological control agent Pseudomonas fluorescens A506 and Erwinia amylovora in pear blossoms. Ecology and Epidemiology, 83, 117-123. Wilson, M., & Lindow, S. E. (1994). Ecological similarity and coexistence of epiphytic ice-nucleating (ice +) Pseudomonas syringae strains and a non-ice-nucleating (ice-) biological control agent. Applied and Environmental Microbiology, 60, 3128-3137. Wood, R. K. S. (1951). The control of diseases of lettuce by use of antagonistic organisms. 1. Control of Botrytis cinerea Pers. Annals of Applied Biology, 38, 203-216. Zhang, P. G., Sutton, J. C., & Hopkin, A. A. (1994). Evaluation of microorganisms for biocontrol of Botrytis-cinerea in container-grown black spruce seedlings. Canadian Journal of Forest Research, 24, 1312-1316.

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133I Biological Control of Insects and Mites on Grapes D. L. FLAHERTY

L. T. WILSON

Cooperative Extension, University of California County Civic Center Visalia, California

Department of Entomology Texas A &M University College Station, Texas

INTRODUCTION

soil conditions in all the continents (Gonzalez, 1983). Diverse viticulture practices modify vine microclimates, which favor or inhibit pests indigenous to the ecosystem into which the grape has been introduced. Hence the ecological niches offered by the biocenosis of the vine have been occupied in each grape-growing region by different pest species (Bournier, 1976). Less commonly, pests from other Vitis species have been transported on plant samples and infested V. vinifera as was the case for phylloxera (Bournier, 1976). We would add that the diversity of growing conditions and pest species have likely given rise to a wealth of natural enemy species and biotypes which can be used to enhance biological control and pest management programs. Interest in biological control has increased with the development of integrated pest management (IPM) systems for vineyards. This move was generally brought about by pest resistance to synthetic organic pesticides and the accompanying serious biological outbreaks (Flaherty et al., 1985). In this chapter we present a general review of biological control of insects and mites in various grape-growing regions of the world, with emphasis on California.

The grape has been cultivated since antiquity, beginning in the region between and to the south of the Black and Caspian seas in Asia Minor. Winkler et al. (1974) state "That region, most botanists agree, is the home of Vitis vinifera L., the species from which all cultivated varieties of grapes were derived before the discovery of North America. From Asia Minor culture of the grape spread both west and east. Before 600 B.C. the Phoenicians probably carried wine varieties to Greece, thence to Rome, and on to southern France. No later than the second century A.D. the Romans took the vine to Germany. Probably at even an earlier date, raisin and table grapes were moving around the eastern end of the Mediterranean Sea to the countries of North Africa. The lines of spread of wine varieties differed from those of raisin and table varieties because of differences in custom and religion between the peoples of the northern and southern shores of the Mediterranean. Grapes spread to the Far East by way of Persia and India. Many years later, when Europeans colonized new lands, the grape was always among the plants taken along."

From the middle ages to the 14th century, viticulture reached its major expression in France, Italy, and central Europe, a flourishing period that terminated with the phylloxera disaster that devastated primarily the vineyards of France. Grape phylloxera, Daktulosphaira vitifoliae (Fitch), was introduced into France from North America circa 1886 and spread to the Black Sea area of the former Soviet Union within 10 years. The renewal of devastated vineyards marked an important stage in improvement of cultural practices, especially with the production of hybrids and resistant rootstocks (Gonzalez, 1983). About 10 million hectares of grapes are cultivated worldwide. Hundreds of clonal selections and hybrids have been produced for adapting the species to local climatic and

Handbookof BiologicalControl

BIOLOGICAL CONTROL OF INSECT A N D MITE PESTS Homoptera Cicadellidae

Bournier (1976) lists nine species of cicadellids (leafhoppers) which are recorded on grapes worldwide. In California Erythroneura elegantula Osborn, grape leafhopper,

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Copyright 9 1999by AcademicPress. All rights of reproductionin any form reserved.

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D.L. Flahertyand L. T. Wilson

is the most common pest of grapes. Economic damage is caused by leaf chlorophyll reduction, vine defoliation, marring of the surface of table grapes with excrement, and leafhoppers annoying pickers at harvest (Wilson et al., 1992b). Doutt and Nakata (1965, 1973) reported that large acreage of grapes planted near streams and rivers, where wild blackberries (Rubus ursinus Chamisso and Schlecht and R. procerus Mueller) flourish, seldom require control for grape leafhopper. This is because of the activity of a minute mymarid wasp, Anagrus epos Girault, which parasitizes the eggs of grape leafhopper and blackberry leafhopper, Dikrella californica (Lawson), a noneconomic species whose eggs are present throughout the year on wild blackberries. Williams (1984) verified the synchrony of blackberry leafhopper, grape leafhopper, and A. epos phenology reported by Doutt and Nakata (1973). Efforts to establish effective blackberry refuges near commercial vineyards have not been successful. Flaherty et al. (1985) indicated that overwintering numbers of A. epos were few and insufficient due to inadequate D. californica egg production during a critical winter period. It was previously thought that effective overwintering of A. epos in blackberries necessitated continuous production of eggs by D. californica. Williams (1984) reported on a period of reproductive diapause of D. californica females during the winter. Species of leafhoppers which overwinter as diapausing eggs on other host plants in natural systems also need consideration as important hosts of A. epos (Flaherty et al., 1985). Studies by McKenzie and Beirne (1972) in Canada and by Kido et al. (1984) in the San Joaquin Valley (California), who reported on the overwintering of A. epos on leafhopper eggs on wild rose, apple, and French prune, lend credence to the importance of other winter hosts of A. epos. For development of productive commercial refuges, studies in the San Joaquin Valley now place emphasis on a prune leafhopper species, Edwardsiana prunicola (Edwards), as a major overwintering host of A. epos (Flaherty et al., 1985). Wilson et al. (1989) reported that French prune planted adjacent to vineyards resulted in A. epos invading the vineyards 4 weeks earlier than for vineyards without French prunes. The authors also showed that the establishment and buildup of A. epos on the prune trees were greatly affected by whether a tree was directly exposed to prevailing winds (windbreak trees) or sheltered downwind by the windbreak trees. Murphy et al. (1996) reported that a significant amount of variation in A. epos trap captures in vineyards was explained by A. epos densities in prune trees surrounding the vineyards. Corbett and Rosenheim (1996a, 1996b), using rubidium marking, concluded that vineyard colonization by A. epos was related to the distance of overwintering habitats to the vineyards. Pickett et al. (1990) provide a thorough review of the use of refuges in agroecosystem

management and how they affect the efficacy of biological control agents. Typhlocyba pomaria McAtee, a leafhopper on apples, is also being considered as an overwintering host. Dependence on A. epos activity by grape growers is influenced by the grape cultivar and its intended use (Wilson et al., 1992b). For example, high populations of grape !eafhopper can be tolerated on Thompson Seedless vines destined for raisin or wine production and frequently A. epos provides sufficient control of the grape leafhopper. However, only low populations of leafhoppers are tolerated on Thompson Seedless vines and other grapes grown for fresh market consumption, making it more difficult to depend upon A. epos instead of applying insecticides for control of the leafhoppers. Excessive spotting (leafhopper droppings) determines the economic damage level on table grapes and this occurs long before any reduction in sugar or yield can be measured. Nonetheless, A. epos is highly effective on Thompson Seedless and its activity increases the possibility that grape leafhopper populations remain within tolerance limits, even in table grape vineyards (Wilson et al., 1992b). Anagrus epos is considerably less effective on Emperor and Ribier table grapes, particularly the latter. By late season, grape leafhopper populations increase to enormous numbers on these and some wine grape cultivars despite the presence of A. epos. Reasons for its effectiveness on Thompson Seedless, a cultivar harvested midseason, are not clear, but observations indicate that the smooth leaf surface of Thompson Seedless vines does not interfere with searching and oviposition by the parasitoid. Early maturing cultivars also produce fewer newly mature leaves, structures that are favored by grape leafhopper for egg deposition. In comparison, late cultivars such as Emperor and Ribier have hairy (tomentose) leaves that may interfere with the efficiency of the parasitoid. Development of newly matured leaves late into the season on these cultivars also favors grape leafhopper oviposition. Later season irrigation in such vineyards also favors grape leafhopper populations (Trichilo et al., 1990). A dryinid parasitoid, Aphelopus albopictus Ashmead (=A. comesi Fenton), attacks and oviposits in all instars of the grape leafhopper (Cate, 1975). This parasitoid places its egg between the nymph's second and third abdominal segments, where it remains undeveloped until the leafhopper nymph molts to the adult stage. During the parasitoid's larval development, the host appears normal, except for an elongating larval sack (thylacium) that increasingly protrudes from the abdomen with each parasitoid molt. By its fifth instar the parasitoid has developed mandibles and eviscerates the adult leafhopper. Prior to evisceration, the adult leafhopper is functionally nonreproductive since gonads fail to develop in parasitized adults. Usually A. comesi parasit-

Chapter 33

Biological Control of Insects and Mites on Grapes

ism is between 10 and 40% (Cate, 1975; Wilson et al., 1991a). Cate (1975) reported in one instance 77% parasitism. He speculated that vineyard cultural practice can be altered to favor parasitism and survival of the parasitoids. In a recent survey of leafhoppers and sharpshooters inhabiting grape vines and associated vegetation across most of western Texas, Wilson et al. (unpublished data) found dryinid parasitizing leafhoppers in each of the 13 vineyards that were studied. Erythroneura variabilis Beamer, variegated grape leafhopper, is the principal vineyard pest in the desert areas of southern California, Arizona, and Mexico. Infestations are especially severe in the Coachella Valley in California, where high temperatures allow rapid development and up to six generations per year (Wilson et al., 1992a). The low activity of A. epos in the Coachella Valley reportedly aggravates the problem. On the other hand, A. epos is active in the San Bernardino area of southern California where wild grapes and blackberries grow near commercial vineyards. Wilson et al. (1992a) reported parasitism as high as 90% in late summer. Until recently, grape growers in the San Joaquin Valley had to contend only with grape leafhopper. Now, however, they also deal with the variegated grape leafhopper, which was first detected in the Valley about 1980, and populations have since increased and rapidly spread. Defoliation now occurs in many Thompson Seedless vineyards where grape leafhopper historically had been under good control by A. epos. It is evident that A. epos is not an effective parasitoid of variegated grape leafhopper. Adding to the problem is the fact that the dryinid parasitoid A. comesi does not attack variegated grape leafhopper (Wilson et al., 1991a). Necessary chemical control causes serious outbreaks of secondary pests, such as spider mites and mealybugs. Annual costs for control of variegated grape leafhopper alone are projected to exceed $ 5 - 1 0 million, with yield and quality losses potentially reaching twice this amount (Wilson et al., 1986, 1987). Grape IPM in the San Joaquin Valley has been dealt a serious setback and adjustments must be made (Flaherty et al., 1985). Reasons for the ineffectiveness of A. epos in controlling variegated grape leafhopper on Thompson Seedless in the San Joaquin Valley are not entirely clear, but Settle et al. (1986) stated "Variegated leafhopper is a more serious pest than the grape leafhopper, in part because of differences in egg-laying behavior. Variegated leafhopper eggs are deeply buried within the leaf tissue, and are less likely to be detected by A. epos than grape leafhopper eggs, which stand out as blisters on the leaf surface." Settle et al. (personal communication) also recorded over 90% parasitism of grape leafhopper eggs and less than 20% parasitism of variegated grape leafhopper eggs in San Joaquin Valley Thompson Seedless vineyards. Settle and Wilson (1990a,

855

1990b) developed a model of host preference by A. epos which verifies that the eggs of E. variabilis are probably more difficult to detect by A. epos than those of E. elegantula.

In 1985, a search was initiated for parasitoids of variegated grape leafhopper in southern California, Mexico, Arizona, Colorado, New Mexico, and Texas, with the object of collecting and introducing into the San Joaquin Valley many species and biotypes of leafhopper parasitoids collected from diverse climatic zones and different times of the season (Gonzalez et al., 1988). Preliminary studies (Wilson et al., unpublished) indicate that A. epos has evolved a wide range of biotypes, differing in relative preference for the grape leafhopper and variegated grape leafhopper. For example, studies by Pickett et al. (1987, 1989) indicated that the native, or San Joaquin Valley biotype, has a 6.9-fold preference for grape leafhopper than for variegated grape leafhopper. Moreover, on the basis of preference, biotypes from Coachella Valley in southern California and in Colorado would respectively choose, provided equal numbers of eggs of both leafhopper species, 2.0 and 4.3 times more variegated grape leafhopper eggs. The data suggest that prospects are good for introducing a more effective parasitoid of variegated grape leafhopper into the San Joaquin Valley. However, data are presently not available on the preference of these biotypes for overwintering hosts such as prune leafhopper and to determine their effectiveness if established in the San Joaquin Valley. This issue is made even more complex by studies which suggest that the collections from diverse climatic zones by Gonzalez et al. (1988) were actually a mixture of different species of Anagrus and not A. epos biotypes (Trjapitzin & Chiappini, 1994). Further studies are showing that different species of Anagrus exist in various grape-growing areas of California (Trjapitzin, 1995). A pressing need of biological control specialists is a quantitative tool that can be used to easily differentiate between closely related parasitoids, but which differ greatly in their ability to control pest species. In the Okanagan Valley, British Columbia, Canada, Erythroneura ziczac Walsh is the most important insect on grape (McKenzie & Beirne, 1972). In their study to develop ways for preventing damaging leafhopper populations, they reported on two cultural procedures which would tend to keep E. ziczac populations below damaging levels: (1) destroy overwintering sites in and near the vineyards and (2) provide A. epos with overwintering leafhopper host eggs (Edwardsiana rosae (Linnaeus) and T. pomaria) by growing wild rose and apple in or near vineyards. Wells et al. (1988) found that A. epos is the main source of egg mortality for E. elegantula and E. ziczac in southcentral Washington and suggested that plum trees could be infested with nonpestiferous host species to provide a winter refuge for A. epos. Yigit and Erkilic (1987) reported that in southern

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FIGURE 1 Impact of weedcover crop on (a) mean number of spiders per shoot (Settle et al., unpublished) and (b) mean number of leafhopper nymphs per leaf (Settle et al., 1986).

Turkey the egg parasites Anagrus atomus (Linnaeus) and the trichogrammatid Oligosita pallida Kryger appeared to control the grape leafhopper, Arboridia adanae (Dlabola). Blackberry (Rubus sp.) and dog rose (Rosa sp.), infested by the cicadellid E. rosae, were found to be winter refuges for the parasitoids. Pavan and Picotti (1994) reported higher levels of parasitism of Empoasca vitis (Gothe) in grape vineyards by A. atomus than in adjoining kiwi vineyards. Based on host oviposition studies and results from the parasitism studies, the authors concluded that A. atomus was responsible for suppressing E. vitis populations in the grape vineyards. Pinto and Viggiani (1987) reported two new Trichogrammatidae species emerged from eggs of grapevine cicadellids in Mexico and Arizona. Small releases

FIGURE 2 Impact of rootstock on leafhopper nymphal abundance (Settle et al., 1986).

were made in the San Joaquin Valley without recovery (D. Gonzalez, personal communication). Observations by Settle et al. (1986) indicated that generalist predators (primarily the theridiid spider Theridion sp.) might play a significant role in suppressing leafhoppers in vineyards having cover crops. In studies conducted in the San Joaquin Valley, approximately twice as many spiders were recorded in a vineyard with a weed cover crop. Correspondingly, only half as many leafhoppers were found compared to the numbers in the plots without cover crops (Fig. 1). Costello and Daane (1995) in a two-year study reported 27 species of spiders, representing 14 families inhabiting San Joaquin Valley vineyards. Polesny (1987) also discussed the importance of spiders as predators on insect pests in vineyards in Austria. In San Joaquin Valley vineyards, augmentative releases of the generalist predator Chrysoperla species suppressed variegated grape leafhopper, however, effectiveness varied greatly (Daane et al., 1993, 1996). Settle et al. (1986), when examining the effect of grape rootstock on leafhopper abundance, found that Thompson Seedless grapes grown on their own roots showed greatly reduced attractiveness of vines. This resulted in a nearly 8fold reduction in leafhopper numbers compared with the more vigorous vines on Saltcreek rootstock (Fig. 2). Trichilo et al. (1990) reported an inverse linear relationship between the amount of water stress and leafhopper population growth, with longer season irrigation programs increasing late-season leafhopper densities in California. They suggested that the late-season leafhoppper densities could be controlled by timing the last irrigation for mid- to late-July. The reduced leafhopper pressures afforded by cultural practices suggest considerable potential for enabling biological

Chapter 33

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Biological Control of Insects and Mites on Grapes

control programs to be incorporated more readily in grape management systems. However, cultural controls aimed at increasing the control of one pest species may have no effect or potentially a negative effect on the control of a second species. Buccholz and Schruft (1994) in a four-year study of generalist predators in two vineyards concluded that increased understory vegetation generally did not promote the abundance and effectiveness of generalist predators which control Eupoecilia ambiguella populations in vineyards in Germany.

TABLE 1 Parasitoids of Grape Mealybug, Pseudococcus maritimus (Ehrhorn)a Parasitoids

Total reared

Number of hosts

Average per host

614

78

7.9

350 280

350 280

t.0 1.0

40

40

1.0

1 1285

1 749

1.0

Acerophagus notativentris (Girault)

Zarhopalus corvinus (Girault) Anagyrus subalbicornis (Girault)

Pseudoleptomastix squammulata Girault

Anagyrus clauseni Timberlake

Pseudococcidae

In California two mealybug species are known to infest vineyards. Pseudococcus maritimus (Ehrhorn), the grape mealybug, is primarily a pest of table grape cultivars whose bunches make contact with vine bark and become infested (Flaherty et al., 1992a). Flaherty et al. (1992a) report that before the late 1940s occasional losses occurred in table grapes, and even though bothersome, infestations were mostly spotty and frequently disappeared the following year. Increasing and more persistent populations were noted in the late 1940s. Extensive use of DDT and other synthetic pesticides to control grape leafhoppers apparently had disrupted natural enemies of P. maritimus. The second species, Pseudococcus affinis (Mackell) (=P. obscurus Essig), the obscure mealybug, which has been recorded on a wide number of hosts, was recently found causing severe damage in unsprayed vineyards in San Luis Obispo County, on California's central south coast. The presence of a second species was suspected because native parasitoids would likely control the grape mealybug in unsprayed vineyards. Evidently, obscure mealybug has adapted to vineyards in this area. The absence of effective parasitoids attacking obscure mealybug has also been observed on other host plants, suggesting that it is an introduced species that will require importation of natural enemies for its control. Releases of the parasitoid Pseudophycus flavidulus (Brethes) are considered an important ingredient for the successful management of P. affinis in Chile (Ripa & Rojas, 1990). In 1993 P. flavidulus was introduced and recovered in coastal vineyards in California (K. M. Daane, personal communication). Little work has been done to document the effectiveness of natural enemies of grape mealybug. Clausen (1924) reported rearing five primary endoparasitic encyrtid wasps from grape mealybugs in the Fresno area of the San Joaquin Valley. He also reported that in the late summer and fall of 1919 parasitism exceeded 90%. It is not clear, however, whether he considered mealybug populations to be effectively controlled by parasitoids. From 1084 grape mealybugs, Clausen (1924) reared nine species of parasitoids, five primary (one of which was gregarious) and four secondary (hyperparasites). In numbers of individuals, there were

Total aSummarized from Clausen (1924)

1285 of the former and 515 of the latter. Zarhopalus corvinus (Girault) parasitized the most hosts in his samples (Table 1). Flaherty et al. (1976) reported that in the late 1960s, ranking of host parasitism from samples of Doutt and Nakata (unpublished data) differed from those given in Table 1. They showed that host parasitism by Acerophagus notativentris (Girault) clearly dominated; Anagyrus subalbicornis (Girault) was found occasionally, Z. corvinus was uncommon, and other species were rare. Studies in 1988 revealed Pseudophycus angelicus (Howard) commonly parasitizing grape mealybug in San Joaquin Valley vineyards (E. F. Legner, personal communication). This encrytid species was previously reared from P. maritimus in southern California (Clausen, 1924). Flaherty et al. (1982) reported that parasitoids were not reared from mealybug samples collected from an Emperor vineyard with a history of heavy treatments in which over 25% of the bunches were badly infested, whereas in another Emperor vineyard that had a minimal insecticide program, parasitism was 46%, with mealybug activity below the acceptable economic level of 2% infested bunches. Parasitism by A. notativentris clearly dominated. Serious outbreaks of the mealybug Maconellicoccus hirsutus (Green) have recently occurred on grapevines in India (Manjunath, 1985). It attacks different cultivars, including Thompson Seedless, Anab-e-Shahi, and Bangalore Blue. In severe attacks, up to 90% of the clusters are destroyed. Chemical control has not been effective. An encyrtid wasp, Anagyrus dactylopii Howard, reared from M. hirsutus, a new record from India, appears to offer promise as a biological control measure. In late-season (mid-March/April) samples at Bangalore, parasitization ranged from 60 to 70%, although these fields had been regularly sprayed with insecticides. Manjunath (1985) also recommended introduction of two encyrtid wasps, Anagyrus kamali Moursi and Prochiloneurus sp., which, according to Kamal (1951), ef-

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D.L. Flahertyand L. T. Wilson

fected complete control of M. hirsutus after being introduced into Egypt from Java. Grasswitz and Burts (1995), in studies conducted in apple and pear orchards in the United Kingdom, reported that Pseudococcus maritimus was controlled by a complex of natural enemies including encrytid parasitoids (Pseudophycus websteri Timberlake and Mayridia spp.), a coccinellid beetle (Hyperaspis lateralis Mulsant), and a chamae myiid fly (Leucopis verticalis Malloch) in orchards that had not received pesticide controls during the previous 1 - 2 years. In the former Soviet Union, Planococcus cirri (Risso) is injurious to over 20 species of plants, including grapes (Niyazov, 1969). The main parasitoid of P. citri is Anagyrus pseudococci (Girault), which occurs in the south of European Russia and Soviet Central Asia. It destroys up to 75% of the host population in areas not treated with insecticides. The platygasterid Allotropa mecrida (Walker) was responsible for 20% parasitism of P. cirri in Turkmenia and Georgia. In 1960, two encyrtid wasps, Leptomastidea abnormis (Girault) and Leptomastix dactylopii Howard, were introduced into Georgia and Turkmenia from the United States, but native hyperparasites were reported to greatly reduce their effectiveness. In Transcaucasia and Soviet Central Asia, the signiphorid Thysanus (Chartocerus) subaeneus Frrster is responsible for up to 20% hyperparasitism of A. mecrida. Rzaeva (1985) reported that L. abnormis had successfully established on Planococcus ficus Signoret, a mealybug pest of grapes in eastern Transcaucasus, USSR. Niyazov (1969) advocated the introduction of Clausenia josefi Rosen, an encyrtid, from the Mediterranean area. Russian entomologists also advocated the introduction of A. notativentris from California (K. S. Hagen, personal communication). In California, little is known about the effectiveness of predators of mealybugs in vineyards. Cecidomyiid fly larvae were observed attacking mealybug egg masses in the above-mentioned lightly treated Emperor vineyard but not in the heavily treated vineyard (Flaherty et al., 1982). Charles (1985) reported that the cecidomyiid Diadiplosis koebelei Koebele was recorded for the first time in New Zealand, with larvae feeding on adults of Pseudococcus longispinus (Targioni-Tozzetti) on grapevines. About 30% of adult female mealybugs in unsprayed fruit bunches at harvest were killed by the cecidomyiid. Adults of Chrysoperla (=Chrysopa) spp. frequently are abundant on grapevines harboring mealybugs in California. Chrysopid adults are attracted to the mealybug honeydew, but it is not known to what extent their egg laying and subsequent control of mealybugs is influenced by the presence of honeydew. Laboratory studies in India showed that the green lacewing Mallada boninensis (Okamoto) consumed 237.9 M. hirsutus nymphs during its larval development (Mani & Krishnamoorthy, 1989).

The coccinellid Cryptolaemus montrouzieri Mulsant, the mealybug destroyer, is rarely observed in California vineyards and the feasibility of mass releases for control of the grape mealybug has not been studied. The use of C. montrouzieri for the control of mealybugs on a range of crops, including grapes, in Georgia, USSR, is reviewed by Yasnosh and Mjavanadze (1983). Best control was achieved by releasing adult beetles; immature beetles apparently suffer high mortality during transportation. Niyazov (1969) reports that one of the most effective predators of mealybugs on grapevines in the former Soviet Union is C. montrouzieri, which was introduced into the Black Sea coastal area from Egypt in 1932. Other coccinellids noted in Turkmenia were Coccinella septempunctata Linnaeus, Hyperaspis polita Weise, Scymnus apetzi Mulsant, S. subvileosus (Goeze), Nephus bipunctatus Kugelann, and S. biguttatus Mulsant. The larvae of Leucopis (Leucopomya) alticeps Czerny (Diptera: Ochthiphilidae) and Chrysoperla carnea (Stephens) were observed to destroy all stages of P. citri. The coccinellids were parasitized by the encyrtid Homalotylus sp. and the chrysopids by the scelionid Telenomus acrobates Girard. Mani (1988) reported that the coccinellid S. coccivora Rumakrishna and the parasitoid A. dactylopii are of considerable importance in the control of M. hirsutus in India. It was also reported that C. montrouzieri was observed 6 weeks after the initial release, with 64.3% control of M. hirsutus when 10 predators were released per vine (Srinivasan & Babu, 1989). Orlinskii et al. (1989) suggested that the coccinellid N. reunioni Ftirsch, introduced into the former Soviet Union in 1978, is a promising entomophage of P. ficus and P. citri and possesses certain advantages over C. montrouzieri. Initial controlled tests on effectiveness have given good results. The voracious appetite of mealybug-consuming coccinellids is illustrated by results from Padmaja et al. (1995), who showed that adult and immature Scymnus coccivora Aiyar consumed an average of 864 and 314 grape mealybug eggs, respectively, during their lifetime. Because the grape mealybug problem in California is probably caused by the application of chemical insecticides to control grape leafhopper and variegated grape leafhopper in table grape vineyards, Flaherty et al. (1985) suggested developing treatment programs which leave untreated or minimally treated areas to encourage the activity and spread of natural enemies. Coccidae

In Chile, Gonzalez (1983) reports that grape quality can be affected by copious amounts of honeydew produced by Parthenolecanium persicae (Fabricius). However, natural enemies play an important role in maintaining populations below economic levels. The principal enemies are two en-

Chapter 33 BiologyControl of Insects and Mites on Grapes crytid wasps, Coccophagus caridei (Brethes) and Metaphycus flavus (Howard). These and other parasitoids are common natural enemies of various lecanium coccids on other plant hosts, including P. corni (Bouchr), which is also a pest of grapes in Chile. Therefore, it was important to maintain untreated reservoirs of those scales on ornamentals or natural vegetation to ensure a source from which natural enemies may move to nearby vineyards, particularly in the event that treatments for other pests severely reduced parasitoid activity.

Phylloxeridae Wheeler and Jubb (1979) summarized their observations on the coccinellid Scymnus cervicalis Mulsant as a predator of the leaf-feeding form of grape phylloxera, D. vitifoliae, on wild grapes in Erie Co., Pennsylvania. Wheeler and Jubb (1979) believe that S. cervicalis is a potentially useful predator of a pest that is becoming increasingly important on wine grapes in Pennsylvania.

Lepidoptera

Tortricidae Those species of tortricids that infest grape clusters are commonly severe pests in most grape-growing areas of the world. Argyrotaenia citrana (Fernald), orange tortrix, is a major pest in the cool, coastal regions of California. Larvae cause the primary damage by feeding in grape clusters and allowing rot-causing organisms to invade (Bettiga & Phillips, 1992). Kido et al. (1981) assessed the potential of its biological control. Orange tortrix populations were sampled on Gamay Beaujolais vines in two vineyards in the Salinas Valley. One, the Soledad vineyard, had a history of injurious infestations and required treatments. The other, the Greenfield vineyard, had very light infestations and no treatments. Samples of clusters from the Greenfield vineyard contained very few orange tortrix larvae and pupae, with 53.5% parasitism for the sampling period; the Soledad vineyard, with an extremely high orange tortrix population, had 16% parasitism for the sampling period. The ichneumonid Exochus nigripalpus subobscurus Townes was the dominant parasitoid in both vineyards, but the braconid Apanteles aristoteliae Viereck was also recovered, but much less frequently. Orange tortrix infestations also occurred on coyote brush, Baccharis pilularis De Candolle, a native composite shrub commonly found in the Salinas Valley and growing in large numbers near the Greenfield vineyard. Large numbers of another tortricid species, Aristoteliae argentifera Busck, were found on coyote brush near the Greenfield vineyard, and several parasitic species of wasps and flies,

859

including Exochus sp. and Apanteles sp., were recovered from larvae and pupae. Coyote brush was much less abundant near the Soledad vineyard and consisted mostly of young plants and no infestations of A. argentifera were found. Studies are needed to determine whether the relative difference of orange tortrix infestations in the two vineyards was related to differences in pesticide history and the influence of the coyote brush ecosystem. Since the 1960s the tortricid Platynota stultana Walsingham, the omnivorous leafroller, has become a major pest in the warmer inland valleys of California (Coviello et al., 1992). Its rot-causing damage is similar to that of orange tortrix. A number of insect parasitoids have been recorded attacking omnivorous leafroller larvae in vineyards. However, parasitoids seldom accounted for more than 10% mortality, even in the presence of very high larval populations. Fortunately, omnivorous leafroller is controlled with the use of selective pesticides. Flaherty et al. (1985) recommended the importation and augmentation of natural enemies of omnivorous leafroller for the improvement of grape IPM in the San Joaquin Valley. Mass release of Trichogramma spp. to augment biological control of omnivorous leafroller or orange tortrix has not been studied in California vineyards. Makhmudov et al. (1977) reported that releases of Trichogramma sp. gave good control of Lobesia botrana (Denis and Schiffermuller), a tortricid pest of grapes in the former Soviet Union. Marcelin (1985) reports on significant reductions of L. botrana and Eupoecilia ambiguella (Htibner) populations with Trichogramma sp. releases, but its use in vineyards was not suggested. No reasons were given. Sengonca and Leisse (1989) reported that when the native egg parasite Trichogramma semblidis (Aurivillius) was augmented in vineyards in Germany, infestations of E. ambiguella and L. botrana larvae were reduced about 25% in both generations. Recent studies in Europe have emphasized the selective control of tortricid pests of grapes with Bacillus thuringiensis Berliner treatment and mating disruption (G. A. Schruft, personal communication). Nasr et al. (1995) reported that endemic populations of Trichogramma evanescens Westwood in Egypt parasitized 22-64% on the eggs of L. botrana, and this species was considered to be an important biological control agent. Castaneda-Samayoa et al. (1993) in a four-year study in Guatemala on the effectiveness of four Trichogramma spp. reported that Trichogramma releases reduced damage by E. ambiguella and L. botrana from 23 to 83%, with T. cacoeciae the most efficient species. In Chile, Gonzalez (1983) reports that damage by Proeulia auraria (Clarke), a leaf- and fruit-damaging tortricid, increases when natural enemies are destroyed by pesticides. A complex of five species of egg and larval parasitoids was identified. An aphelinid wasp, Encarsia sp., was the egg

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parasitoid. The larval parasitoids included a eulophid wasp of the genus Elachertus or Bryopezus, a braconid wasp of the genus Apanteles, an unidentified ichneumonid, and a tachinid fly, Ollacheryphe aenea (Aldrich), which was the most abundant enemy of P. auraria larvae.

Zygaenidae Flaherty et al. (1985) report that westem grapeleaf skeletonizer, Harrisina brillians Barnes and McDunnough, was originally distributed throughout the southwestem United States (excluding Califomia) and Mexico's Sonora, Chihuahua, Coahuila, and Aguascalientes states. It was first found in California near San Diego in 1941, severely defoliating wild grapes, Vitis girdiana Munson, in canyon areas. In a short time it became a serious pest in commercial vineyards. The larvae are voracious feeders and may cause complete loss of crop by defoliating entire vineyards. In 1950, the Division of Biological Control at the University of California, Riverside, initiated a program to search for natural enemies of grapeleaf skeletonizer. A number of parasitoids were introduced but only two, the braconid Apanteles harrisinae Muesebeck and the tachinid Ametadoria miscella (Wulp) (=Sturmia harrisinae Coquillett), became established. An extremely virulent granulosis virus, which became an important component in the successful biological control of grapeleaf skeletonizer, was also accidentally introduced (Clausen, 1961). Flaherty et al. (1985) reported that surveys in San Diego County in 1982 and 1983 revealed that it was necessary to spray grapeleaf skeletonizer in commercial vineyards. Abandoned untreated vineyards and backyard vines were severely defoliated despite the activity of the introduced parasitoids. Symptoms of virus infection were not observed in the survey. Curiously, the survey revealed a total absence of grapeleaf skeletonizer in wild grapes, V. girdiana, except where they were in close proximity to heavily infested commercial V. vinifera vineyards. The first grapeleaf skeletonizer infestation in the San Joaquin Valley was found in June 1961 (Clausen, 1961). New infestations appeared thereafter throughout the Valley despite eradication attempts. It became a widespread and serious pest of commercial vineyards and backyard vines, as well as wild grapes, Vitis californica Bentham. Flaherty et al. (1985) reported that establishment of A. harrisinae and A. miscella was unsuccessful in the San Joaquin Valley. Only a few parasitoid recoveries were made at the release sites. Moreover, samples of larvae taken from three heavily infested and abandoned vineyards in San Diego County produced only 13% parasitism, which is far less than the percentage parasitism (42% in 1953 and 62% in 1954) reported by Clausen (1961). No evidence of the virus was present in these vineyards. Clausen (1961) com-

mented that the virus must be credited with the major role in reducing grapeleaf skeletonizer populations to low levels and exterminating many small infestations. Flaherty et al. (1985) commented that perhaps at that time the virus was more widespread and had reduced grapeleaf skeletonizer populations to levels that made it more manageable by the parasitoids. This may account for the greater parasitism reported by Clausen (1961) than that found by Flaherty et al. (1985). However, the absence of virus in the abandoned vineyards in San Diego County requires an explanation, as does the absence of observable grapeleaf skeletonizer in wild grapes that were once heavily infested. Studies in the San Joaquin Valley confirmed that the virus of grapeleaf skeletonizer is extremely virulent and has the potential to be incorporated into an areawide biological control program, including wild grapes, backyard vines, and commercial vineyards (Flaherty et al., 1985). Recent surveys by Califomia Department of Agriculture entomologists in the San Joaquin Valley revealed significantly lower skeletonizer populations and damage to wild grapes. The virus and parasitism by M. miscella are thought to be responsible (B. Villegas, personal communication). Apparently similar, but less dramatic, action has taken place in commercial vinifera vineyards (W. W. Barnett, personal communication). In Italy, Pucci and Dominici (1986) reported that the percentage parasitism of the zygaenid Theresimima ampelophaga Bayle-Barelle by six species of parasitoids was not high enough to control the pest. Perhaps the missing ingredient for control is a pathogen.

Pyralidae Desmia funeralis (Htibner), the grape leaffolder, is a pest of grapes in the central and southern San Joaquin Valley. Larvae cause injury by rolling and feeding on leaves, reducing photosynthesis. Under extreme population densities, it may feed on fruit, but economic damage usually occurs only with massive, late-season infestations (Jensen et al., 1992b). The most commonly observed natural enemy of grape leaffolder is a larval braconid parasitoid, Bracon cushmani (Muesebeck). Parasitism ordinarily is in the range of 30-40% but often is higher. Bracon cushmani usually increases in the summer and frequently reduces the size of the second and third brood to such small numbers that little increase in grape leaffolder populations is detectable. When necessary, grape leaffolder is effectively controlled with selective insecticides (Jensen et al., 1992b).

Sesiidae Vitacea polistiformis (Harris), grape root borer, is a pest of grapes east of the Rocky Mountains in North America. Larvae severely prune and girdle grape roots by excavating

Chapter 33 BiologyControl of Insects and Mites on Grapes irregular burrows (Jubb, 1982). Saunders and All (1985) showed an inverse correlation between the severity of V. polistiformis and the activity of entomophilic rhabditoid nematode fauna in vineyard soils. Laboratory and field bioassays determined the susceptibility of first-instar larvae to the nematode Steinernema feltiae Filipjev, and the insect-nematode interaction was posited as a mechanism of natural control of the larval populations. Augmentation of entomopathic rhabditoid nematode populations during the critical period of oviposition and eclosion (egg hatch) is suggested as a technique for the control of V. polistiformis (Saunders & All, 1985).

Heliozelidae Although leafminers are not a problem in California vineyards, recent research by Alma (1995) has shown the widespread subeconomic presence of Holocascista rivillei Stanton in northwestern vineyards in Italy. Alma reported the presence of eight eulophid parasitoids attacking this species, three of which had previously not been reported associated with this species. The author also reported the presence of a predaceous mirid and an anthocorid feeding on the leafminer. Mortality caused by the parasitoids was 37.5%, with pathogens responsible for an additional 16.4%.

Coleoptera

Curculionidae In Chile, adults of Naupactus xanthographus (Germar) voraciously consume grape buds and leaves (Gonzalez, 1983). Additional damage is caused by feces which adhere to foliage and fruit clusters. Combined damage by adult and larval feeding on roots may weaken vines. A complex of pathogens (bacteria and fungi), nematodes, and insects attack larvae and pupae in the soil. An undescribed nematode of the family Rhabditidae parasitizes fourth and fifth instars; however, it is unknown whether death is caused by the nematode or by septicemia. The same nematode attacks other coleopteran species and may be reared on larvae of the pyralid moth, Galleria melonella (Linnaeus). Gonzalez (1983) also reports that larvae are frequently attacked by nematodes transported in soils carried in irrigation water from the Maipo River. However, the degree of control produced by nematodes has not been evaluated. Of particular importance as a natural enemy of N. xanthographus is a platygastrid wasp Platystasius (= Fidiobia) sp. Up to 60% of the egg masses under the bark have been found attacked by this parasitoid. Gonzalez (1983) reports that its action in conjunction with the complex of other natural enemies is sufficient to maintain N. xanthographus below economically damaging levels.

86 |

The black vine weevil, Otiorhynchus sulcatus (Fabricius), is an important pest of a wide range of horticultural crops in Europe, the United States, Canada, Australia, and New Zealand. Serious damage to grapes by adults feeding on berry pedicels and cluster stems and larvae feeding on roots has been reported in Europe and central Washington (Bedding & Miller, 1981). Their studies showed that application of aqueous suspensions of infective juvenile Heterorhabditis heliothidis (Khan, Brooks, and Hirschmann) to the soil resulted in up to 100% parasitism of larvae of O. sulcatus in potted grapes in nurseries. Pupae and newly emerged adults were also parasitized. Steinernema bibionis (Bovien) was found to be less effective. The use of nematodes provides an effective method for controlling O. sulcatus on potted plants in glasshouses and nurseries.

Bostrichidae In California Melalgus confertus (LeConte), a branch and twig borer, is found associated with many species of cultivated and native trees and shrubs. In grapes both adult and larval stages cause injury to grapevines (Zalom et al., 1992). Little is known about the natural enemies of M. confertus; however, a neuropteran predator in the family Rhaphidiidae and two coleopterans in the families Carabidae and Ostomidae may assist in maintaining low population levels. Recent studies have shown that the entomophagous nematode Steinernema feltiae Filipjev can move through frass tubes to infect larvae. Field studies are being conducted to determine the potential of the nematode as an agent for control (F. G. Zalom, personal communication).

Thysanoptera

Thripidae Several thrips (including Frankliniella spp. and Drepanothrips reuteri Uzel) are serious pests on grapes worldwide (Flaherty & Wilson, 1988). Little is known about their biological control in California vineyards (Jensen et al., 1992a) and, based on the lack of published information, elsewhere as well. However, studies in citrus in California suggest that the phytoseiid mite Euseius tularensis Congdon can reduce citrus thrips Scirtothrips citri (Moulton) populations (Grafton-Cardwell & Ouyang, 1995). Moreover, Schwartz (1987) reported that Amblyseius cirri Van der Merwe and Ryke preys upon Scirtothrips aurantii Faure in South Africa. Schwartz (1987) also reported that Amblyseius addoensis Van der Merwe and Ryke probably preys upon Thrips tabaci Lindeman in table grapes in South Africa, although it did not show an ability to reduce midsummer population increases of T. tabaci.

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Acari

Tetranychidae Tetranychids (spider mites) became serious pests of grapes as well as other crops worldwide after World War II. Reasons for this development have not been fully documented, but it is believed that the use of synthetic organic insecticides has upset natural controls (Flaherty et al., 1985). In California, two spider mite species are commonly abundant on grapes, Pacific spider mite, Tetranychus pacificus McGregor, which deserves serious consideration, and Willamette spider mite, Eotetranychus willamettei (McGregor), whose populations only occasionally become large enough in San Joaquin Valley vineyards to cause concern (Flaherty et al., 1992b). However, recent studies have shown that Willamette spider mite can cause serious yield reductions in wine grapes grown in coastal valleys and in the foothills of northern California (Welter et al., 1991). Two-spotted spider mite, T. urticae Koch, is rarely found on grapes in California; however, it is reported as serious on grapes in other countries such as the former Soviet Union, South Africa, and Australia. In the eastern United States, European red mite, Panonychus ulmi (Koch), is the principal spider mite pest (Jubb et al., 1985). It is also a pest of grapes in Europe. Schruft (1986) lists E. carpini vitis Boisduval, T. urticae, T. mcdanieli McGregor, and T. turkestani Ugarov and Nikolski as other pest species in Europe. Oligonychus vitis Zaher & Shehata is reported as a serious pest of grapes in Egypt and Chile (Rizk et al., 1978; Gonzalez, 1983). A number of spider mites, including P. ulmi, E. pruni (Oudemans), T. turkestani, and Bryobia praetiosa Koch, are reported as infesting vineyards in the former Soviet Union (S. R. Tuganow, personal communication). Eotetranychus pruni is also reported as a pest in Bulgaria (Schruft, 1986). In India, four species of tetranychid mites, namely O. mangiferus (Rahman and Sapra), O. punicae (Hirst), T. urticae, and E. truncatus Estebanes and Baker, are known to attack grapevines (Schruft, 1986). Schruft (1986) also reports grapes as hosts for B. praetiosa, E. smithi Pritchard and Baker, T. kanzawai Kishida, and T. urticae in Japan, but we are uncertain if they are serious pests. The most important natural enemy of spider mites in San Joaquin Valley vineyards is the phytoseiid Metaseiulus occidentalis (Nesbitt) (Flaherty et al., 1992b). Other phytoseiid species observed in California vineyards include Amblyseius californicus (McGregor) in the Salinas Valley and M. mcgregori (Chant) in the San Joaquin and Sacramento valleys. Both species have been observed to prey upon Willamette spider mite but little is known about their effectiveness. In the eastern United States the most common predatory mites found on Concord grapes (Vitis labrusca Linnaeus) are the two phytoseiids Neoseiulus (=Ambly-

seius) fallacis (Garman) and Amblyseius andersoni (Chant) and the stigmaeid Zetzellia mali (Ewing). Neoseiulus fallacis and Z. mali may be potentially important in the natural control of P. ulmi (Jubb et al., 1985). In Europe, the most frequently encountered phytoseiids are Typhlodromus pyri Scheuten, Euseius (=Amblyseius) finlandicus (Oudemans), Amblyseius aberrans (Oudemans), and A. andersoni, but Schruft (1986) reports only T. pyri is of importance for biological control of phytophagous mites. Gambaro (1972) reported that A. aberrans in Italy is able to check and keep spider mite populations at low densities if not disrupted by pesticides. Duso (1992) reported that A. aberrans and T. pyri populations were more abundant on cultivars with hairy leaf undersurfaces. The author concluded that under conditions of prey scarcity, the preference for cultivars was largely independent of prey availability and appeared to be associated with favorable microclimate, improved protection from rain or predation, availability of oviposition sites and shelters, and "an increased capacity for retaining wind pollen." Camporese and Duso (1996) in an extensive five-year study evaluated the competitiveness of T. pyri, A. aberrans, and A. andersoni on three grape cultivars. The authors found that A. aberrans was able to displace the other phytoseiids on all cultivars and reached higher densities on cultivars with pubescent leaf undersurfaces. However, T. pyri and A. andersoni were able to persist in vineyards having low spider mite densities. James and Whitney (1993) in studies of mite populations in southeastern Australia recorded nine species of phytoseiids with Typhlodromus doreenae Schicha and Amblyseius victoriensis (Womersley) in vineyards on which insecticide was not used and on which sulfur and copper were used to control vine diseases. In a second study, in the Canberra district of Australia, James et al. (1995) recorded six phytoseiid species (Typhlodromus doreenae Schicha, T. dossei Schicha, T. australicus (Womersley), Amblyseius wattersi Schicha, A. elinae Schicha, and Phytoseius foiheringhamiae Denmark and Schicha). Typhlodromus doreenae was the dominant species in all monitored vineyards. The results of these authors have considerable implications for choosing which phytoseiids to use in inoculative release programs for different geographical regions and/or climate types. Karban et al. (1995) in a study of 20 North American species of grapes plus Vitis vinifera explained 25% of the variability in abundance of Typhlodromus caudiglans by leaf characteristics, including density of leaf hairs and the presence of leaf domatia. They also failed to find a significant correlation between spider mite abundance and phytoseiid abundance. However, the spider mite densities recorded in their studies were extremely low and probably not sufficient for the effect of prey abundance on phytoseiid abundance to be accurately measured. In contrast, Hanna and Wilson (1991) and Hanna et al. (1997a) working with

Chapter 33

Biology Control of Insects and Mites on Grapes

ingly higher predator-prey ratio was required. The utility of the predator-prey ratio concept obviously requires that the spider mite density be below economically damaging levels. An equally important constraint is that the monitoring procedure utilizing this information must be easy to

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863

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much higher populations of spider mites provide evidence that phytoseiid abundance is clearly associated with spider mite abundance and that increased phytoseiid abundance inevitably results in a rapid decrease in spider mite population size. Rizk et al. (1978) report that the stigmaeids Agistemus exsertus Gonzalez and Amblyseius gossipi E1-Badry and the tydeid Tydeus californicus (Banks) are the most abundant predatory mites found on grapevines in middle Egypt. In Chile, Amblyseius chilenensis (Dosse) is the most important predatory mite (Gonzalez, 1983). Gaponyuk and Asriev (1986) reported that since its introduction into the Crimea, USSR, in 1976, M. occidentalis has acclimatized and spread widely, exerting considerable influence on E. pruni populations in vineyards. Predicting Effectiveness of Predaceous Mites

The potential for spider mite control can be determined in part by the ratio of the number of predators to spider mites. For any system there exists a particular predatorprey ratio at which the pest population will be controlled. For example, Tanigoshi et al. (1983) reported that a 1:10 ratio of Neoseiulus fallacis to P. ulmi provided control in orchards of Red Delicious apples. In an orchard of another apple cultivar, they found that a 1:20 ratio was sufficient and indicated that relatively fewer predaceous mites were required to provide control as a result of reduced spider mite fecundity on this apple cultivar. Wilson et al. (1984) similarly reported that a 1:11 ratio of Metaseiulus occidentalis to Tetranychus spp. provided control in almonds within 2 weeks when the spider mites were at densities greater than 5 mites per leaf. At lower densities, an increas-

Estimating spider mite abundance and predator effectiveness using standard monitoring procedures is particularly tedious, since mites are extremely small, often numerous, and therefore difficult and time-consuming to count. Schruft (1986) reports that it is possible to estimate the risk of damage by P. ulmi or E. carpini vitis using a method developed by Baillod et at. (1979). Its principle is based on the relationship between the number of spider mites per leaf and the proportion of leaves in a sample occupied by mites; instead of counting the mites, the number of leaves with one or more mites is recorded. The same sampling procedure has been used to evaluate predaceous mites (Baillod & Venturi, 1980). Flaherty et al. (1992b) similarly addressed the problem of counting in determining the need to initiate control actions by using an infested leaf (binomial) predator-prey ratio, in conjunction with information on the relative level of spider mites in the vineyard. Based on observations over several years, they determined that a 1:2 (0.5) binomial ratio of predator to spider mite infested leaves was sufficient for control. This ratio is less conservative than the ratios derived using Eq. (1) of Wilson et al. (1984) for almonds. Figure 3 indicates that a binomial ratio near 1:1 is equivalent to a 1:10 count ratio at densities between 15 and 50 spider mites per leaf. A binomial ratio closer to that reported by Flaherty et al. (1992b) was calculated with a 1:20 count ratio. The lower ratio for grapes may indicate a lowered reproductive capacity for spider mites on grapes compared to that found on almonds or possibly for that found by Tanigoshi et al. (1983) on apples. Effect of Alternate Foods of Predaceous Mites on Predator-Prey Relations

Flaherty (1969) reported that M. occidentalis is better able to regulate low densities of Willamette mites in the presence of small numbers of T. urticae that moved from weeds onto grape leaves. Flaherty et al. (1992b) recommend that Willamette spider mite be considered as an important alternate prey since it is a much less serious pest of grapes than Pacific spider mite. Flaherty and Hoy (1971) found that tydeid mites were particularly important as a food source for M. occidentalis when spider mie prey were scarce. Karban et al. (1994) and Hanna et al. (1997a) showed that predatory mites were more effective at controlling Pacific spider mite when released in conjunction with low levels of Willamette spider mite. Metaseiulus occidentalis also preys upon other mites, such as eriophyids, tydeids, and possibly tarsonemids. In Europe, additional food for T. pyri includes eriophyids, tydeids, pollen, and pearls

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of the grape (Schruft, 1972). Flaherty and Hoy (1971) and Calvert and Huffaker (1974) speculated on possible benefits of augmenting pollen-feeding tydeids by pollen applications or planting cover crops that produce wind-borne pollen. Gambaro (1972) reported that the ability of A. aberrans to live and reproduce in the absence of prey enables it to keep spider mite populations at low densities. However, the altemate source of food was not clearly defined. Wiedner and Boller (1990) emphasized the need for supplying pollen for the survival of T. pyri in vineyards in eastem Switzerland. Corbett et al. (1991) showed that strip-planting of alfalfa within a cotton field, followed by releases of Tetranychus urticae as a food source and Metaseiulus occidentalis as a predator, resulted in spread of both mite species into the cotton and maintenance of spider mite populations at subeconomic levels. Influence of Viticulture Practices on P r e d a t o r - P r e y Relations

Flaherty et al. (1992b) point out that viticultural practices influence spider mite outbreaks. They place considerable emphasis on correcting problems concerned with low vine vigor, dusty conditions, and water stress, all of which greatly increase the chance of Pacific spider mite outbreaks if not corrected. They also discuss how insecticides applied for control of other vineyard pests may disturb natural control of spider mites. Flaherty and Huffaker (1970) collected 10 species of phytoseiid mites from commercial vineyards in the San Joaquin Valley but only M. occidentalis apparently played a significant role in the control of spider mites. However, observations in 1983 (Flaherty, unpublished data) suggested that the predaceous mite Amblyseius near hibisci, previously rare in commercial vineyards, was abundant in some vineyards where triadimefon replaced sulfur for control of powdery mildew, Uncinula necator Burrill. Amblyseius nr. hibisci is commonly found in wild grapes where sulfur is not applied (Flaherty et al., 1985). English-Loeb et al. (1986) showed that A. near hibisci was the dominant phytoseiid species where sulfur was not applied and maintained lower numbers of Willamette spider mites than M. occidentalis where sulfur was used. However, in the following two years, similar studies (Hanna et al., 1997b) did not detect A. nr. hibisci in significant numbers, underscoring the unpredictability and unreliability of A. nr. hibisci as a major predatory mite of spider mites in grapes. Another phytoseiid, Typhloseiopsis smithi (Schuster), was also recorded on the non-sulfur-treated vine foliage, but not in abundance (English-Loeb et al., 1986). Effectiveness of Insect Predators of Spider Mites

Flaherty et al. (1992b) reported that predaceous insects and spiders are generally considered as ineffective natural enemies of spider mites; it is assumed they appear too late in the season or increase too slowly. However, their contri-

bution to natural control in vineyards should not be discounted. Observers are often impressed with how quickly six-spotted thrips, Scolothrips sexmaculatus (Pergande), destroys Pacific spider mite populations. However, the appearance of this predator in vineyards is unpredictable. Its inconsistency is possibly related to periodic low prey densities. In Italy, anthocorids and coccinellids are considered more effective at high prey densities (Duso & Girolami, 1985). Schruft (1986) reports that various predaceous insects such as the coccinellid Scymnus sp., the staphylinid Oligota sp., Scolothrips longicornis Priesner, and the anthocorids Anthocoris nemorum (Linnaeus) and Orius minutus (Linnaeus) are found on grapevines infested with P. ulmi, but their importance for biological control of red spider mite populations is not evident. On the other hand, it is certain that some chrysopids, especially Chrysoperla carnea, are effective predators of red spider mites during summer and late autumn (Schruft, 1986). The amount of spider mite control by insect predators may be subtle as well as important. For example, observations in vineyards and studies in the laboratory revealed that westem flower thrips, Frankliniella occidentalis (Pergande), which is considered a pest of grapes, feeds on Pacific spider mite eggs and may actually affect the pest's population in vineyards (Flaherty et al., 1992b). The importance of predation by F. occidentalis of spider mites has also been observed and partially quantified by researchers in cotton (Gonzalez et al., 1982; Gonzalez & Wilson, 1982; Trichilo 1986; Trichilo & Wilson, 1993; Wilson et al., 1991a, 1991b). Augmentation of Predaceous Mites

Releases of predatory mites to control spider mites have been tried in several crops, with promising results. However, these releases were often designed to overwhelm or inundate the spider mite population to provide near-term control. An altemative to the use of inundative releases is augmentative releases where lower release rates are used, with the progeny of the released predators and not the released predators themselves being responsible for enhancing control to a level sufficient to prevent economic loss. Results from several horticultural and field crops strongly suggest that augmentative release of predatory mites will become economically viable once rates and timing of releases are perfected (Corbett et al., 1991; Flaherty et al., 1992b; Oatman 1970; Oatman et al., 1976, 1977a, 1977b; Schruft, 1972; Tanigoshi et al., 1983; Tijerina-Chavez, 1991; Wilson et al., 1984). Results with different predatory mite species indicate control of spider mites with phytoseiid: spider mite ratios ranging from 1:20 to 1:10 (Flaherty et al., 1992b; Tanigoshi et al., 1983; Wilson et al., 1984). Tijerina-Chavez (1991) reported that the spider mite population on cotton began to decrease when a treatment's phytoseiid: spider mite ratio reached a range of 1:20 to 1:10 (see Wilson et al., 1991c). Analysis of data presented in

Chapter 33

Biology Control of Insects and Mites on Grapes

Tijerina-Chavez (1991) showed that the monetary value of increased cotton yield in plots receiving predatory mite releases greatly exceeded the cost of the predatory mites (Wilson et al., 1991c). Predatory mite releases in field crops will become cost-effective if targeted to augment naturally occurring predation, with the number of predators released dependent on the abundance of the naturally occurring predators rather than dependent on prohibitively costly inundative releases or disruptive acaricides. Flaherty et al. (1985) concluded that there are too many problems to overcome in the development of timely mass releases of M. occidentalis for the control of increasing Pacific spider mites in early summer. They suggest that a fall release program may be more fruitful than early summer releases in correcting a Pacific spider mite imbalance. Flaherty and Huffaker (1970) showed that late-season predator activity in vineyards is an essential ingredient in spider mite balance. In their studies, a fall release of M. occidentalis resulted in excellent biological control of Willamette spider mite the following spring and summer. Hoy and Flaherty (1970, 1975) established the importance of lateseason diapause induction for successful overwintering of M. occidentalis populations. Flaherty et al. (1985) reason that a fall release of predators reared under diapausing conditions would minimize the timing and survivorship problems encountered in early summer releases because immediate control of Pacific spider mite in the fall is not a factor and diapausing predators require little food. Howe;ver, Hanna et al. (unpublished) found that the success of a fall release requires not only that the predatory mites are ready to diapause, but also that alternative prey (i.e., tydeid or Willamette mites) are present for successful overwintering of M. occidentalis. In Italy, Girolami and Duso (1985) report on the establishment of predator-prey equilibrium in pesticide-disturbed vineyards with reintroductions of A. aberrans. Baillod et al. (1982) describe methods for reintroduction of T. pyri into vineyards in Switzerland and recommend their use for biological control of phytophagous mites. Schruft (1986) also reports that artificial release of T. pyri by the introduction of infested canes or foliage has been successful. Duso et al. (1991) reported that releases of A. aberrans controlled P. ulmi at low densities and T. pyri was more efficient in controlling populations of P. ulmi than populations of E. carpini. Boiler et al. (1988) concluded that hedges can provide ecological refuges and sources of T. pyri in the vineyards of northern Switzerland. Amblyseius nr. hibisci is frequently found in high numbers in vineyards bordering natural vegetation of riparian systems in the San Joaquin Valley. Hoy (1982) reported on the aerial dispersal of M. occidentalis.

Tenuipalpidae Brevipalpus chilensis Baker is a serious pest of grapes in Chile. Gonzalez (1983) reports that the problem devel-

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oped as a consequence of the unnecessary use of pesticides. Selective pesticide programs which take advantage of natural and cultural control are recommended to avoid strict dependence on chemical control. An important factor of natural control and perhaps the only natural enemy of B. chilensis is the predaceous mite Amblyseius chilenensis (Dosse). In the Mildura district of Victoria, Australia, B. lewisi McGregor causes a superficial scarring of bunch and berry stems (Buchanan et al., 1980). A close numerical relation between B. lewisi and its most common phytoseiid predator, Amblyseius reticulatus (Oudemans), did not reveal regulation of B. lewisi numbers by A. reticulatus during the growing season (September to April). However, large numbers of A. reticulatus during April may reduce the number of B. lewisi that overwinter. The false spider mite Tenuipalpus granati Sayed has been recognized as a serious pest of grapes in Egypt (Rizk et al., 1978). It was suggested that certain pesticides were in part responsible for the problem. Agistemum exsertus, Amblyseius gossipi, and Tydeus californicus were observed in association with T. granati, but the data did not reveal that pesticides disrupted regulatory action by these predatory mites.

Eriophyidae Colomerus vitis (Pagenstecher) is an eriophyid mite that attacks various species and hybrids of grapes and is probably widely distributed. Different biotypes of C. vitis have been recognized in California by their characteristic injury (Barnes, 1992). The phytoseiid mite M. occidentalis was reported to be effective in reducing populations of C. vitis. Schruft (1972) reported that C. vitis and Calepitrimerus vitis (Nalepa), also eriophyid pests on grapes in Europe, are fed on by the tydeids Tydeus grtzi Schruft and Pronematus stiirki Schruft.

CONCLUSION It is apparent to us that this review documents a rather weak worldwide biological control research program for a crop of such importance as grape. Instead of a prior and continuing commitment to biological control, the review reveals an emphasis on studies concerned with disruptions of secondary pests by pesticides and a paucity of studies dealing with biological control of primary pests. The relatively large number of studies dealing with spider mites as secondary pests and little in the way of studies on the importation, augmentation, and evaluation of natural enemies of primary pests lends credence to a lack of commitment by grape entomologists and the viticulture industry to biological control research. Flaherty et al. (1985) recommended that grape IPM in the San Joaquin Valley of California would be improved by augmentation of biological control, including importa-

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tion of natural enemies of some primary pests. The initiation of studies on the importation and augmentation of natural enemies of cicadellid pests of grapes discussed earlier has been an important step in California. The increasing emphasis on the use of augmentative releases to control spider mites on a range of crops shows particular promise for management of spider mites in grapes as well. However, we further recommend a greatly expanded cooperative effort in biological control studies by grape entomologists throughout the world. The efforts expended by citrus entomologists worldwide would serve as a working model for accelerating the importation and augmentation of natural enemies of grape pests.

Acknowledgment The authors thank G. Gordh, K. Hagen, R. Hanna, H. Kaya, J. McMurtry, C. Pickett, and J. Smilanick for their generous assistance.

talis)-prey (Pronematus spp.) interactions under sulfur and cattail pollen applications in a non-commercial vineyard. Entomopha~a, 19, 361-369. Camporese, P., & Duso, C. (1996). Different colonization patterns of phytophagous and predatory mites (Acari: Tetranychidae, Phytoseiidae) on three grape varieties: A case study. Experimental & Applied Acarology, 20, 1- 22. Castaneda-Samayoa, O., Hoist, H., & Ohnesorge, B. (1993). Evaluation of some Trichogramma species with respect to biological control of Eupoecilia ambiguella Hb. and Lobesia botrana Schiff. (Lep., Tortricidae).Zeitschrift fuer Pflanzenkrankheiten und Pflanzenschutz, 100, 599-610. Cate, J. R. (1975). Ecology of Erythroneura etegantula Osborn (Homoptera: Cicadellidae) in grape agroecosystems in California, Ph.D. Thesis, Univ. of California, Berkeley. Charles, J. G. (1985). Diadiplosis koebelei Koebele (Diptera: Cecidomyiidae), a predator of Pseudococcus longispinus T.-T. (Homoptera: Pseudococcidae), newly recorded from New Zealand. New Zealand Journal of Zoology, 12, 331-333. Clausen, C. P. (1924). The parasites of Pseudococcus maritimus (Ehrhorn) in California (Hymenoptera, Chalciodoidea). Part II. Biological studies and life histories. University of California Publications in Entomology, 3, 253- 288. Clausen, C. P. (1961). Biological control of western grape leaf skeletonizer (Harrisina brillians B. & McD.) in California. Hilgardia, 31,613637. Corbett, A., & Rosenheim, J. A. (1996a). Impact of a natural enemy overwintering refuge and its interaction with the surrounding landscape. Ecological Entomology, 21, 155-164. Corbett, A., & Rosenheim, J. A. (1996b). Quantifying movement of a minute parasitoid, Anagrus epos (Hymenoptera: Mymaridae), using fluorescent dust marking and recapture. Biological Control, 6, 35-44. Corbett, A., Leigh, T. F., & Wilson, L. T. (1991). Evaluation of alfalfa interplantings as a source of Metaseiulus occidentalis (Acari: Phytoseiidae) for management of spider mites in cotton. Biological' Control, 1,188-196. Costello, M. J., & Daane, K. M. (1995). Spider (Aranaeae) species composition and seasonal abundance in San Joaquin Valley Grape vineyards. Environmental Entomology, 24, 823- 831. Coviello, R., Hirschfelt, D. J., & Barnett, W. W. (1992). Omnivorous leafroller. In "Grape Pest Management" (D. L. Flaherty, L. P. Christensen, W. T. Lanini, J. J. Marois, P. A. Phillips, & L. T. Wilson, Eds.), 2nd ed., pp. 166-173. Univ. of California, Berkeley, Agricultural Science Publication 3343. Daane, K. M., Yokota, G. Y., Zheng, Y., & Hagen, K. S. (1996). Inundative release of common green lacewings (Neuroptera: Chrysopidae) to suppress Erythroneura variabilis and E. elegantula (Homoptera: Cicadellidae) in vineyards. Environmental Entomology, 25, 1224-1234. Daane, K. M., Yokota, G. Y., Rasmussen, Y. D., Zheng, Y., & Hagen, K. S. (1993). Effectiveness of leafhopper control varies with lacewing release methods. California Agriculture, 47, 19-23. Doutt, R. L., & Nakata, J. (1965). Overwintering refuge of Anagrus epos (Hymenoptera: Mymaridae). Journal of Economic Entomology, 58, 586. Doutt, R. L., & Nakata, J. (1973). The Rubus leafhopper and its egg parasitoid: An endemic biotic system useful in grape-pest management. Environmental Entomology, 2, 381-386. Duso, C. (1992). Role of Amblyseius aberrans Oud., Typhlodromus pyri Scheuten and Amblyseius andersoni Chant (Acari: Phytoseiidae) in vineyards. III. Influence of variety characteristics on the success of Amblyseius aberrans and Typhlodromus pyri releases. Journal of Applied Entomology, 114, 455-462. Duso, C., & Girolami, V. (1985). Strategie di controllo biologico degli acari tetranichidi su vite. Atti XIV Cong. Naz. Ital. Entomol., Palermo, Erice, Bagheria, pp. 719-728. m

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Biology Control of Insects and Mites on Grapes

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on the population dynamics of the grape mealybug, Pseudococcus maritimus (Hom.: Pseudococcidae), in the apple and pear orchards. Entomophaga, 40, 105-117. Hanna, R., & Wilson, L. T. (1991). Prey preference by Metaseiulus occidentalis (Acari: Phytoseiidae) and the role of prey aggregation. Biological Control, 1, 51- 58. Hanna, R., Wilson, L. T., Zalom, F. G., & Flaherty, D. L. (1997a). Effects of predation and competition on population dynamics of Tetranychus pacificus on grapevines. Journal of Applied Ecology, 34, 878-888. Hanna, R., Zalom, F. G., Wilson, L. T., & Leavitt, G. M. (1997b). Sulfur can suppress mite predators in vineyards. California Agriculture, 51, 19-21. Hoy, M. A. (1982). Aerial dispersal and field efficacy of a genetically improved strain of the spider mite predator, M. occidentalis. Entomologica Experimentalis Applicata, 32, 205-212. Hoy, M. A., & Flaherty, D. L. (1970). Photoperiodic induction of diapause in a predaceous mite, Metaseiulus occidentalis. Annals of the Entomological Society of America, 63, 960-963. Hoy, M. A., & Flaherty, D. L. (1975). Diapause induction and duration in vineyard-collected Metaseiulus occidentalis. Environmental Entomology, 4, 262- 264. James, D. G., & Whitney, J. (1993). Mite populations on grapevines in south-eastern Australia: Implications for biological control of grapevine mites acarina tenuipalpidae eriophyidae. Experimental & Applied Acarology, 17, 259- 270. James, D. G., Whitney, J., & Rayner, M. (1995). Phytoseiids (Acari: Phytoseiidae) dominate the mite fauna on grapevines in Canberra district vineyards. Journal of the Australian Entomological Society, 34, 79-82. Jensen, F. L., Flaherty, D. L., & Luvisi, D. A. (1992a). Thrips. In "Grape Pest Management" (D. L. Flaherty, L. P. Christensen, W. T. Lanini, J. J. Marois, P. A. Phillips, & L. T. Wilson, Eds.), 2nd ed., pp. 193-201. Univ. of California, Berkeley, Agricultural Science Publication 3343. Jensen, F. L., Hirschfelt, D. J., & Flaherty, D. L. (1992b). Grape leaffolder. In "Grape Pest Management" (D. L. Flaherty, L. P. Christensen, W. T. Lanini, J. J. Marois, P. A. Phillips, & L. T. Wilson, Eds.), 2nd ed., pp. 133-139. Univ. of California, Berkeley, Agricultural Science Publication 3343. Jubb, G. L., Jr. (1982). Occurrence of the grape root borer Vitacea polistiformis, in Pennsylvania. Melsheimer Entomological Series, 32, 2024. Jubb, G. L., Jr., Masteller, E. C., & Lehman, R. D. (1985). Survey of arthropods in vineyards of Erie County, Pennsylvania. Acari. Int. J. Acarol., 11, 201- 208. Kamal, M. (1951). Biological control projects in Egypt, with a list of introduced parasites and predators. Bulletin de la Societe Fouad I d'Entomologie, 35, 205-220. Karban, R., English-Loeb, G., Walker, M. A., & Thaler, J. (1995). Abundance of phytoseiid mites on Vitis species: Effects of leaf hairs, domatia, prey abundance and plant phylogeny. Experimental & Applied Acarology, 19, 189-197. Karban, R., Hougen-Eitzmann, D., & English-Loeb, G. (1994). Predatormediated apparent competition between two herbivores that feed on grapevines. Oecologia, 97, 508- 511. Kido, H., Flaherty, D. L., Bosch, D. F., & Valero, K. A. (1984). French prune trees as overwintering sites for grape leafhopper egg parasite. American Journal of Enology and Viticulture, 35, 156-160. Kido, H., Flaherty, D. L., Kennett, C. E., McCalley, N. F., & Bosch, D. F. (1981). Seeking the reasons for differences in orange tortrix infestations. California Agriculture, 35, 27-28. Mani, M. (1988). "Bioecology and Management of Grapevine Mealybug." Indian Institute of Horticultural Research, Technical Bulletin 5. Mani, M., &. Krishnamoorthy, A. (1989). Feeding potential and development of green lacewing Mallada boninensis (Okamoto) on the grape mealybug, Maconellicoccus hirsutus (Green). Entomon, 14, 19- 20

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Makhmudov, D., Azimov, A., Abdulagatov, A. Z., & Ataev, K. G. (1977). Control of the grape moth. Zashchita Rastenii, 7, 24-25 (in Russian). Manjunath, T. M. (1985). IndiamMaconellicoccus hirsutus on grapevine. FAO Plant Protection Bulletin, 33, 74. Marcelin, H. (1985). La lutte contre les tordeuses de la grape. Phytoma, 370, 29-32. McKenzie, L. M., & Beirne, B. P. (1972). A grape leafhopper, Erythroneura ziczac (Homoptera: Cicadellidae) and its mymarid (Hymenoptera) egg-parasite in the Okanagan Valley, British Columbia. Canadian Entomologist, 104, 1229-1233. Murphy, B. C., Rosenheim, J. A., & Granett, J. (1996). Habitat diversification for improving biological control: Abundance of Anagrus epos (Hymenoptera: Mymaridae) in grape vineyards. Environmental Entomology, 25,495-504. Nasr, F. N., Korashy, M. A., & Rashed, F. F. M. (1995). Trichogramma evanescens West. (Hym., Trichogrammatidae) as an egg parasitoid of grape moth Lobesia botrana (Den. & Schiff.) (Lep., Tortricidae). Anzeiger fuer Schaedlingskunde Pflanzenschutz Umweltschutz, 68, 4445. Niyazov, O. D. (1969). The parasites and predators of grape mealybug. Zashchita Rastenii, 14, 38-40 (in Russian). Oatman, E. R. (1970). Integration of Phytoseiulus persimilis with native predators for control of the two-spotted spider mite on rhubarb. Journal of Economic Entomology, 63, 1177-1180. Oatman, E. R., Gilstrap, F. E., & Voth, V. (1976). Effect of different release rates of Phytoseiulus persimilis (Acari: Phytoseiidae) on the two-spotted spider mite on strawberry in southern California. Entomophaga, 21,269-273. Oatman, E. R., McMurtry, J. A., Gilstrap, F. E., & Voth, V. (1977a). Effect of releases of Amblyseius californicus on the two-spotted spider mite on strawberry in southern California. Journal of Economic Entomology, 70, 638-640. Oatman, E. R., McMurtry, J. A., Gilstrap, F. E., & Voth, V. (1977b). Effect of releases of Ambylseius californicus, Phytoseiulus persimilis, and Typhlodromus occidentalis on the two-spotted spider mite on strawberry in southern California. Journal of Economic Entomology, 70, 45-47. Orlinskii, A. D., Rzaeva, L. M., & Shakhramanov, I. K. (1989). A promising entomophage. Zashchita Rastenii, 11, 25-26 (in Russian). Padmaja, C., Babu, T. R., Reddy, D. D. R., & Sriramulu, M. (1995). Biology and predation potential of Scymnus coccivora Aiyar (Coleoptera: Coccinellidae) on mealybugs. Journal of Entomological Research, 19, 79-81. Pavan, F., & Picotti, P. (1994). Population dynamics of Empoasca vitis (Goethe) (Homoptera Cicadellidae) and Anagrus atomus (Linnaeus) (Hymenoptera Mymaridae) in vineyards and kiwifruit orchards. Memorie della Societa Entomologica Italiana, 72, 163-173. Pickett, C. H., Wilson, L. T., Gonzalez, D., & Flaherty, D. L. (1987). Biological control of variegated grape leafhopper. California Agriculture, 41, 14-16. Pickett, C. H., Wilson, L. W., Flaherty, D. L., & Gonzalez, D. (1989). Measuring the host preference of parasites: An aid in evaluating biotypes of Anagrus epos (Hym.: Mymaridae). Entomophaga, 34, 551558. Pickett, C. H., Wilson, L. T., & Flaherty, D. L. (1990). Role of refuges in crop protection, with reference to plantings of French prune trees in a grape agroecosystem. In "Monitoring and Integrated Management of Arthropod Pests of Small Fruit Crops" (N. J. Bostanian, L. T. Wilson, & T. J. Dennehy, Eds.), pp. 161-155. Intercept, Dorset, England. Pinto, J. D., & Viggiani, G. (1987). Two new Trichogrammatidae (Hymenoptera) from North America: Ittysella lagunera Pinto & Viggiani (n. gen., n. sp.) and Epoligosita mexicana Viggiani (n. sp.). Pan-Pacific Entomologist, 63, 371-376. Polesny, F. (1987). Die Bedeutung von Spinnen im Weinbau. Pflanzenschutz, 3, 9-10.

Pucci, C., & Dominici, M. (1986). Biological notes and cyclical outbreaks of Theresimima ampelophaga Bayle-Barelle (Lep., Zygaenidae). Journal of Applied Entomology, 101,479-491. Ripa, S. R., & Rojas, P. S. (1990). Manejo y control biol6gico del chanchito blanco de la vid. Revista Frutirola, 11, 82-87. Rizk, G. A., Sheta, I. B., & Ali, M. A. (1978). Chemical control of mites infesting grape-vine in middle Egypt. Bulletin of the Entomological Society of Egypt, Economic Series, 11, 105-111. Rzaeva, L. M. (1985). Parasites and predators of the grape mealybug (Planococcus ficus Signoret) and introduction of new natural enemies into the eastern Transcacaus. Biologicheskikh Nauk, 4, 34-39 (in Russian). Saunders, M. C., & All, J. N. (1985). Association of entomophilic rhabditoid nematode populations with natural control of first instar larvae of the grape root borer, Vitacea polistiformis, in concord grape vineyards. Journal of Invertebrate Pathology, 45, 147-151. Schruft, G. (1972). Les tydridrs (Acari) sur vigne. OEPP/EPPO Bulletin, 3,51-55. Schruft, G. (1986). Grape. In "Spider Mites: Their Biology, Natural Enemies and Control" (W. Helle & M. W. Sabelis, Eds.), Vol. 1B, pp. 359-366. Elsevier, Amsterdam. Schwartz, A. (1987). Seasonal occurrence of a predaceous mite Amblyseius addoensis Van der Merwe & Ryke (Acari: Phytoseiidae) on table grapes. South African Journal for Enology and Viticulture, 8, 78-79. Sengonca, C., & Leisse, N. (1989). Enhancement of the egg parasite Trichogramma semblidis (Auriv.) (Hym., Trichogrammatidae) for control of both grape vine moth species in the Ahr Valley. Journal of Applied Entomology, 107, 41-45. Settle, W. H., & Wilson, L. T. (1990a). Bahavioural factors affecting differential parasitism by Anagrus epos (Hymenoptera: Mymaridae), of two species of erythroneuran leafhoppers (Homoptera: Cicadellidae). Journal of Animal Ecology, 59, 877-891. Settle, W. H., & Wilson, L. T. (1990b). Variation by the variegated leafhopper and biotic interactions: Parasitism, competition, and apparent competition. Ecology, 71, 1461-1470. Settle, W. H., Wilson, L. T., Flaherty, D. L., & English-Loeb, G. M. (1986). The variegated leafhopper, an increasing pest of grapes. California Agriculture, 40, 30-32. Srinivasan, T. R., & Sundara Babu, P. C. (1989). Field evaluation of Cryptolaemus montrouzieri Mulsant, the coccinellid predator against grapevine mealybug, Maconellicoccus hirsutus (Green). So. Indian Hort., 37, 50-51. Tanigoshi, L. K., Hoyt, S. C., & Croft, B. A. (1983). Basic biological and management components for mite pests and their natural enemies. In "Integrated Management of Insect Pests of Pome and Stone Fruits" (B. A. Croft & S. A. Hoyt, Eds.), pp. 153-202. Wiley-Interscience, New York. Tijerina-Chavez. (1991). Biological control of spider mites (Acari: Tetranychidae) on cotton through inoculative release of predatory mites Metaseiulus occidentalis and Amblyseius californicus (Acari: Phytoseiidae) in the San Joaquin Valley of California, Ph.D. Thesis, Univ. of California, Davis. Trichilo, P. (1986). Influence of the host plant on the interaction of spider mites with their natural enemies in a cotton agroecosystem, Ph.D. Dissertation, Univ. of California, Davis. Trichilo, P. J., & Wilson, L. T. (1993). An ecosystem analysis of spider mite outbreaks: Nutritional stimulation or natural enemy suppression? Experimental & Applied Acarology, 17, 291- 314. Trichilo, P. J., Wilson, L. T., & Grimes, D. W. (1990). Influence of grapevine water deficit on distribution of leafhoppers (Homoptera: Cicadellidae) in San Joaquin Valley Vineyards. Environmental Entomology, 19, 1803-1809. Trjapitzin, S. V. (1995). The identities of Anagrus (Hymenoptera: Mymaridae) egg parasitoids of the grape and blackberry leafhoppers (Homm

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Biology Control of Insects and Mites on Grapes

optera: Cicadellidae) in California. Pan-Pacific Entomologist, 71,250251. Trjapitzin, S. V., & Chiappini, E. (1994). A new Anagrus (Hymenoptera: Mymaridae) egg parasitoid of Erythroneura spp. (Homoptera: Cicadellidae). Entomological News, 105, 137-140. Wells, J. D., Cone, W. W., & Conant, M. M. (1988). Chemical and biological control of Erythroneura leafhoppers on Vitis vinifera in southcentral Washington. Journal of the Entomological Society of British Columbia, 85, 45-52. Welter, S. C., Freeman, R., & Farnham, D. S. (1991). Recovery of 'Zinfandel' grapevines from feeding damage by Willamette mite (Acari: Tetranychidae): Implications for economic injury level studies in perennial crops. Environmental Entomology, 20, 104-109. Wheeler, A. G., Jr., & Jubb, G. L., Jr. (1979). Scymnus cervicalis Mulsant, a predator of grape phylloxera, with notes on S. brullei Mulsant as a predator of woolly aphids on Elm (Coleoptera: Coccinellidae). Coleop. Bull., 33, 199-204. Wiedner, U., & Boiler, E. (1990). Bltihende Rebberge in der Ostschweiz. 2. Zum Pollenangebot auf den Rebbl~ittern. Schweizerische Zeitschrift ftir Obst- und Weinbau, 126, 426-431. Williams, D. W. (1984). Ecology of a blackberry-leafhopper-parasite system and its relevance to California grape agroecosystems. Hilgardia, 51, 1-32. Wilson, L. T., Carmen, I., & Flaherty, D. L. (1991 a). Aphelopus albopictus Ashmead (Hymenoptera: Dryinidae): Abundance, parasitism, and distribution in relation to leafhopper hosts in grapes. Hilgardia, 59. Wilson, L. T., Flaherty, D. L., & Peacock, W. L. (1992b). Grape leafhopper. In "Grape Pest Management" (D. L. Flaherty, L. P. Christensen, W. T. Lanini, J. J. Marois, P. A. Phillips, & L. T. Wilson, Eds.), 2nd ed., pp. 140-152. Univ. of California, Berkeley, Agricultural Science Publication 3343. Wilson, L. T., Trichilo, P. J., & Gonzalez, D. (1991b). Natural enemies of spider mites (Acari: Tetranychidae) on cotton: Density regulation or casual association? Environmental Eology, 20, 849-856. Wilson, L. T., Hoy, M. A., Zalom, F. G., & Smilanick, J. M. (1984).

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Sampling mites in almonds: I. Within-tree distribution and clumping pattern of mites with comments on predator-prey interactions. Hilgardia, 51, 1-13. Wilson, L. T., Pickett, C. H., Flaherty, D. L., & Bates, T. A. (1989). French prune trees: Refuge for grape leafhopper parasite. California Agriculture, 43, 7-8. Wilson, L. T., Flaherty, D. L., Settle, W., Pickett, C., & Gonzalez, D. (1987). Managing the variegated leafhopper and grape leafhopper. 1987 Proceedings of the Table Grape Symposium, pp. 5-11. Wilson, L. T., Trichilo, P. J., Flaherty, D. L., Hanna, R., & Corbett, A. (1991c). Natural enemy-spider mite interactions: Comments on implications for population assessment. Modern Acarology, 1, 167-173. Wilson, L. T., Barnes, M. M., Flaherty, D. L., Andris, H. L., & Leavitt, G. M. (1992a). Variegated grape leafhopper. In "Grape Pest Management" (D. L. Flaherty, L. P. Christensen, W. T. Lanini, J. J. Marois, P. A. Phillips, & L. T. Wilson, Eds.), 2nd ed., pp. 202-213. Univ. of California, Berkeley, Agricultural Science Publication 3343. Wilson, L. T., Flaherty, D. L., Andris, H., Barnett, W. W., Gonzalez, D., & Settle, W. (1986). The variegated leafhopper: An increasing pest of grapes in the San Joaquin Valley. 1986 Proceedings of the San Joaquin Valley Grape Symposium, pp. 27-29. Winkler, A. J., Cook, J. A., Kliewer, W. M., & Lider, L. A. (1974). "General Viticulture." Univ. of Calif. Press, Berkeley. Yasnosh, V. A., & Mjavanadze, V. I. (1983). On the efficiency and rational use of Cryptolaemus montrouzieri against plant pests in the Georgia SSR. In "Proceedings, 10th International Congress of Plant Protection, 2." Yigit, A., & Erkilic, L. (1987). Studies on egg parasitoids of grape leafhopper, Arboridia adanae Dlab. (Hom., Cicadellidae) and their effects in the region of South Anatolia. Ttirkiye I. Entomoloji Kongresi Bildirileri, 13-16 (In Turkish). Zalom, F. G., Bettiga, L. J., & Donaldson, D. R. (1992). Branch and twig borer. In "Grape Pest Management" (D. L. Flaherty, L. P. Christensen, W. T. Lanini, J. J. Marois, P. A. Phillips, & L. T. Wilson, Eds.), 2nd ed., pp. 121-123. Univ. of California, Berkeley, Agricultural Science Publication 3343.

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[34[ Biological Control of Weeds in Terrestrial and Aquatic Environments IL D. GOEDEN

L. A. ANDI~S

Department of Entomology University of California Riverside, California

USDA-ARS, Western Research Center 800 Buchanan Street Albany, California

INTRODUCTION

weed's natural enemies cannot exist or would have little environmental impact in the absence of their host. In other words, coevolved natural enemies that have developed a high degree of host specificity have proven the safest to use, are least likely to damage nontarget plant species, and are most suitable for regulating weed abundance. Biological control scientists go to considerable effort to match natural enemies to their weedy host plants in problem environments, seeking combinations and devising manipulations most detrimental to the weeds. The natural enemies used in biological control are selfperpetuating only in the presence of their weed hosts and then only within the limits set by the environment. According to definitions for biological control offered by Smith (1919, 1948) and DeBach (1964), the ability of natural enemies to regulate weed or pest arthropod populations in a self-sustaining, density-dependent manner sets biological control apart from other methods of control. Polyphagous agents (plant-feeding fish, sheep, cattle, geese, and other grazing animals) are useful in removing weeds in some situations (see later), but their numbers and actions must be carefully regulated to avoid damage to nontarget plants. Although these vertebrate grazers remove unwanted foliage, their inability to selectively regulate weed numbers limits their use in biological control.

In the United States, 500 major species of weeds cause estimated annual losses of about $8 billion (Chandler, 1980). These weeds infest cropland, rangeland, recreational, and aquatic areas and vary in their economic importance and need for control. Cultural and chemical controls for weeds are effective, but relief is temporary at best and often uneconomical. In fact, the more effective the chemical control, the sooner other more herbicide-resistant or herbicidetolerant weeds may fill the vacant niches. Thus, improved weed control is no longer a matter of improved plant kill. Planning and ingenuity are required to minimize immediate losses without inviting incursions by replacement weed species. As Aldrich (1984) noted, weeds are part of dynamic ecosystems continually evolving in response to natural and cultural control pressures. Biological control is a proven method of weed control. An increasing volume of literature is devoted to this approach, including a quadrennial international symposium and proceedings which update and highlight current activities and thought. Biological control continues to offer promise and expanded application in reducing weed losses.

W H A T IS BIOLOGICAL CONTROL OF WEEDS? Methodology Definition

Developing a biological control program begins with a systematic assessment of the weed problem: (1) assuring proper identification of the target weed, (2) charting the weed's geographic range, (3) characterizing the habitats it infests, (4) ascertaining the losses caused by the weed, (5) determining the degree of control required, and (6) compiling a list of natural enemies already present or reported

Biological control is the study of relationships among weeds, their associated organisms, and the environment, followed by the manipulation of selected species of these organisms (natural enemies) to the detriment of a target weed species. Attention is focused on those weed-natural enemy relations that have coevolved to the degree that the

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elsewhere. Answers are sought to certain questions; e.g., why has the plant become a problem? If natural enemies are lacking, can they be introduced? Or, if natural enemies are already present, can their abundance be enhanced by conservation or augmentation?

Introducing New Natural Enemies Naturalized weeds often have few host-specific natural enemies capable of effectively regulating their abundance. To correct this, new natural enemies can be sought in the weed's native range and introduced into the problem areas. This approach has been followed in many countries, which has led to the introduction of numerous weed-feeding insects and mites and, more recently, plant pathogens and nematodes (Julien, 1982, 1987, 1992; see later). Although the concept of finding and introducing exotic phytophagous organisms is simple, it requires detailed prerelease studies to ensure that control is achieved and that economically and ecologically important plants will not be harmed. Guidelines for introducing natural enemies were described in detail by Zwrlfer and Harris (1971), Frick (1974), Andres et al. (1976), Klingman and Coulson (1983), Schroeder and Goeden (1986), and Harris (1991) and include the following steps: (1) Project selection. Once released, introduced natural enemies cannot be restricted to parts of the weed's geographic range. Before studies that may lead to natural enemy introduction are undertaken, there must be assurance that the weed has few, if any, redeeming virtues and that there is little or no public opposition to the project (Turner, 1984). (2) Search for natural enemies. A list of organisms recorded from the target weed is compiled from literature and museum records. This is followed by field surveys and studies of associated organisms in selected parts of the weed's native range. Organisms are collected and identified, and their names are checked against literature and museum records. Promising candidate species are selected for further study. (3) Tests and biological studies of host range. Behavioral and biological studies and choice-no-choice feeding and oviposition tests are conducted in the laboratory to determine the host range of each candidate. Plants tested include cultivated and ecologically important species, with special focus on close taxonomic relatives of the weed (Wapshere, 1974a). (4) Evaluation of host-range studies. A report summarizing the candidate biological control agent's taxonomy, behavior, biology, and host-plant relations is submitted to regulatory agencies for review. In the United States, the U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Technical Advisory Group (USDA, APHIS-TAG), Hyattsville, Maryland, plus the relevant state Departments of Agriculture, and, sometimes, state universities, e.g., University of California, perform these reviews

and recommend whether to provide the release clearances. (5) Importation and release. Organisms approved for release are collected from the same field populations from which the test material was obtained and are imported into a domestic quarantine facility. Species that are univoltine or difficult to culture are identified and examined to ensure that they are free from parasites and entomogenous pathogens and may then be released directly into the field. Species amenable to culture are reared for one generation before their release. The quarantine handling of individual candidate specimens is labor intensive and often limits the number of biological control agents released. Release sites are selected on the basis of climate, habitat, freedom from disturbance, and other factors that optimize establishment. (6) Evaluation. For biological control to be effective, the imported agents must establish, increase in number, and inflict meaningful damage at a time critical to the weed's development. The released agents are evaluated against each of these points. Detailed evaluations are important to refine and improve methods and guidelines, test ecological theory, and document results of projects on the biological control of weeds. Weeds may have dozens of associated natural enemies. Some species attack only the flowers and fruit, whereas others may attack the leaves, stems, branches, crowns, or roots. The guild of agents attacking the flower heads and achenes of an asteraceous thistle, for example, may include monophagous to oligophagous species which vary in their impact on the host (Zwrlfer, 1973, 1988). Prerelease studies help determine which species are sufficiently host specific for biological control purposes and suggest the best sequence for release. An agent's host-finding capability and its competitiveness with other flower head-infesting species can be important in this regard. The selection of natural enemies and determination of their order of release have received some attention but need further study (Zwrlfer & Harris, 1971; Harris, 1973, 1991; Goeden, 1983).

Conservation Methods in Biological Control Potentially effective indigenous or exotic natural enemies may feed and reproduce on a weed host, yet fail to provide effective biological control. In such instances, the abundance of an associated agent may be effectively enhanced to provide localized reduction of the weed. For example, a low-dosage application of DDT was used selectively to eliminate Exochomus sp., a coccinellid beetle predator restricting the potential of an introduced cochineal insect, Dactylopius opuntiae (Cockerell) (HemipteraHomoptera: Dactylopiidae), to control the pricey pear cacti Opuntia ficus-indica (Linnaeus) Miller and O. tardispina Griffiths (Cactaceae) in South Africa (Annecke et al., 1969; Moran & Zimmerman, 1984). Once the coccinellid predators were reduced, the cochineal insects increased in num-

Chapter 34 BiologicalControl of Weeds bers and the cacti were controlled. This method of natural enemy enhancement is called biological control through conservation. In contrast to naturalized weeds, many indigenous species have complements of natural enemies which themselves are held in check by parasites, predators, and other environmental factors. However, identifying the factors prompting these natural and often wide-ranging outbreaks, knowing how to manipulate them, and determining whether this manipulation is ecologically desirable, let alone economically feasible, so far remain unresolved, hypothetical, and untested (Wapshere et al., 1989). Implementing biological control through conservation of natural enemies can be complicated. It requires a thorough understanding of the weed-natural enemy-environment relationship, plus the technical ability to manipulate aspects of this relationship to increase agent impact. Conservation methods also can be labor intensive and costly, which limits their usefulness to weed problems that promise high economic return.

Augmentation Methods in Biological Control The abundance of a natural enemy and the timing of its impact may be altered by supplemental releases. Biological control through the conservation of natural enemies relies on enhancing the buildup of populations already present; augmentation utilizes large-scale releases or applications of natural enemies collected or reared elsewhere. The augmentation approach to biological control of weeds was not widely practiced until the discovery by Daniel et al. (1973) that the endemic fungal pathogen Colletotrichum gloeosporioides (Penz.) Sacc. (Melanconiales) could be cultured and sprayed on northern jointvetch, Aeschynomene virginica (Linnaeus) B. S. P. (Leguminosae), a weed of rice in Arkansas and nearby states. The sprays augmented the early seasonal, naturally occurring, low levels of the fungus and provided excellent biological control. This study sparked the search for indigenous pathogens associated with other weeds and assessments of their production and implementation potential (Templeton et al., 1978; Charudattan & Walker, 1982; Wapshere et al., 1989; also see later). Frick and Chandler (1978) augmented the impact of the moth Bactra verutana Zeller (Lepidoptera: Tortricidae) by supplementing existing field populations with large numbers of this insect against purple nutsedge, Cyperus rotundus Linnaeus (Cyperaceae), infesting cotton. They demonstrated experimental control of the weed, but the method proved too costly for practical implementation.

Advantages and Limitations of Biological Control Any person who has spent time hoeing or pulling weeds can appreciate the advantages and limitations of these time-

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tested methods. Unfortunately, shortcomings are inherent in all methods of weed control, making each method appropriate under one or more set of circumstances but inappropriate under others. Advantages of the biological method of weed control include the following: (1) the introduced agents can perpetuate and distribute themselves throughout the weed's range; (2) the impact of host-specific agents is focused on a single weed species without harm to other plants; (3) the cost of developing biological control is relatively inexpensive ($1.5 million) compared to much higher costs for other approaches (Andres, 1977; Harris, 1979); (4) the agents are nonpollutive, energy efficient, and biodegradable; and (5) the knowledge generated during prerelease and evaluation studies contributes to improved understanding of weed ecosystems and environmental factors regulating natural communities. Some of the shortcomings of biological control are that: (1) once established in an area, an introduced agent cannot be recalled or limited to parts of the target weed's range; (2) a host-specific agent will control only one species in a weed species complex; (3) agent impact is often slow and may require 3 - 4 years before local control is attained; (4) an agent may feed and reproduce on closely related nontarget plants; and (5) the establishment, buildup, and impact of a biological control agent is determined by the quality of the environment and the host and cannot be predicted. Fortunately, by combining the several methods of biological control with appropriate timing, many of these shortcomings can be minimized (Wapshere et al., 1989).

HISTORY OF BIOLOGICAL CONTROL OF WEEDS Much can be learned from analyses of case histories of projects on the biological control of weeds such as those reviewed in the section starting on page 880. Not apparent from these abbreviated case histories are the pulse and temper of the historical periods during which projects were initiated, the ebb and flow of individual and collective research efforts, the diverse personalities and research approaches involved, and the trumpeted successes and reluctant failures, all of which constitute a rich history for the biological control of weeds. In its rite of passage from an art to an accepted subdiscipline of applied ecology, biological control of weeds has grown at different rates and in different directions in various areas of the world. We provide a brief overview of biological control of weeds, one of three subdisciplines that, until recent times, comprised the field of biological control (DeBach, 1964). This account is largely taken from Goeden (1978, 1988, 1993). For most of its history, biological control of weeds was the domain of a rather small, dedicated group of broadly versed entomologists (DeBach, 1964), and, like

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certain other aspects of science, it began by accident. The earliest record of the biological control of a weed involved the intentional introduction of the cochineal insect Dactylopius ceylonicus (Green) (Hemiptera-Homoptera: Dactylopiidae) into northern India from Brazil in 1795 in the mistaken belief that it was D. coccus Costa, a species cultured commercially as a source of carmine dye. Instead of reproducing well on the cultivated, spineless prickly pear cactus, Opuntia ficusindica (Linnaeus) Miller, D. ceylonicus readily transferred to its natural host plant, O. vulgaris Miller, which had become a widespread, introduced weed in India when it escaped from cultivation in the absence of its South American natural enemies. Once the value of D. ceylonicus as a biological control agent was recognized, it was introduced from 1836 to 1838 into southern India, where it brought about the first successful, intentional use of an insect to control a weed. Shortly before 1865, D. ceylonicus also was transferred from India to Sri Lanka (then Ceylon), which again resulted in the successful control of O. vulgaris throughout that island and, accordingly, registered the first intentional transfer of a natural enemy between countries for the biological control of a weed (Goeden, 1978; Moran & Zimmerman, 1984). The historical scene next shifted to Hawaii, where Albert Koebele was hired as foreign explorer after helping to achieve the spectacularly successful biological control of the cottony cushion scale on citrus in California during the 1890s (Doutt, 1958, 1964). He explored the jungles of southcentral Mexico during 1902 for insects feeding on lantana (Lantana camara Linnaeus, Verbenaceae). Lantana was an ornamental plant of Central and South American origins that had escaped from cultivation to become a serious weed in Hawaii. Koebele shipped to Hawaii 23 species of insects that he considered important natural enemies of this plant in the parts of Mexico he had explored (Goeden, 1978). The published letters of Koebele describing his labors and hardships during this foreign exploration make adventurous reading (Perkins & Swezey, 1924). Extreme temperatures, unscheduled shipping delays, pathogens, and other contaminants took their toll of shipments. Upon their arrival by ship in 1903, the insects were liberated directly on lantana plants in the field without host-specificity testing. Eight species, including some of the most effective natural enemies of lantana, reportedly were established on this weed throughout the island group by 1905 (Andres & Goeden, 1971; Goeden, 1978; Julien, 1982). The procedure of foreign exploration for natural enemies of an alien weed in its country or countries of origin was pioneered in this early project on lantana. Also, the lantana seed fly, Ophiomyia lantanae (Froggatt) (Diptera: Agromyzidae), was transferred from Hawaii to New Caledonia in 1908-1909 and to Fiji in 1911 (Rao et al., 1971). These shipments marked the beginnings of a tradition of "transfer projects" (DeBach, 1964), involving transfers of biological

control agents of proven worth to other countries with the same weeds. For example, three more species of lantana insects were transferred from Hawaii to Fiji during 19221928 (Rao et al., 1971). This tradition of intemational cooperation in natural enemy transfers continues today. The introduction of D. ceylonicus to Australia from Ceylon and India was attempted again in 1903, but without establishment (Goeden, 1978; Moran & Zimmerman, 1984). Australian work on the biological control of pricey pear cacti (Opuntia spp.) began in earnest during the period 1913-1914, when the two-membered Prickly Pear Travelling Commission surveyed the insects and pathogens associated with these plants in Java, Ceylon, India, East Africa, South Africa, the Canary Islands, the Mediterranean littoral, the United States, Mexico and other parts of Central America, the West Indies, South America, and Hawaii (Johnston & Tryon, 1914). This feat of worldwide exploration for natural enemies of a group of weeds remains unequaled in scope of geographic coverage, though often since surpassed regionally in depth. The control of the prickly pear cacti Opuntia inermis deCandolle and O. stricta Haworth in Australia ranks as one of the most successful projects in biological control of weeds. This project followed the initial efforts of the Prickly Pear Travelling Commission, which first recognized the potential value of what was later to become the principal natural enemy, the cladode-mining moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae). The major entomological efforts in this biological control program occurred during the 1920s, when North and South America, particularly the southern United States, Mexico, and Argentina, were thoroughly explored for potentially useful, cactus-feeding insects. More than 150 species of cactus insects eventually were collected and studied, many of which were new to science. From 1921 to 1925, 48 species were imported into Australia, of which 19 were liberated and 11 became established. A single consignment of C. cactorum was imported from Argentina in 1925. Large-scale mass rearings and host-plant specificity testing with useful and weedy plant species were undertaken for the first time in a biological control program. Cactoblastis cactorum became widely established following the distribution of more than 2.7 billion mass-cultured and field-collected eggs between 1925 and 1933. About 90% of the original stands of O. inermis and O. stricta were destroyed by 1934 through larval feeding by this moth, supplemented by airborne, soft-rot bacteria for which the borers provided portals of entry into infested plants. Virtually complete control of these weeds was achieved in Queensland and northern New South Wales, involving 24 million hectares of formerly infested land that was restored to agricultural use (Dodd, 1940; Goeden, 1978; Moran & Zimmerman, 1984). The spectacular success of Cactoblastis cactorum tended

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Biological Control of Weeds

to eclipse the benefits derived from other cactus insects used in biological control, notably several species of cochineal insects (Moran & Zimmerman, 1984). For example, Dactylopius ceylonicus was successfully reintroduced into Australia during 1913-1915 and it virtually eliminated O. vulgaris as a rangeland weed in Queensland. "Nothing succeeds like success," and so C. cactorum and Dactylopius spp. were transferred during the mid-1920s and 1930s to countries where prickly pear cacti also were introduced weeds: Indonesia, Mauritius, New Caledonia, Reunion, and South Africa (Greathead, 1971; Rao et al., 1971; Goeden, 1978). In South Africa and Mauritius, these early, successful transfer projects led to the independent development of other successful research projects in the biological control of weeds (Greathead et al., 1971; Goeden, 1978; Julien, 1982, 1987, 1992). The biological control of Koster's curse, Clidemia hirta (Linnaeus) D. Don (Melastomataceae), was the next noteworthy success. This is a shrub native to the West Indies and tropical South and Central America that became a serious introduced weed on Fiji. After a preliminary survey of insects attacking C. hirta and allied Melastomataceae, Liothrips urichi Karny (Thysanoptera: Thripiidae) was selected as a promising biological control agent and its life history and host-plant specificities were intensively studied in Trinidad during 1927 and 1928. Potted C. hirta infested with the thrips were shipped under cold storage to Fiji in 1930. Upon arrival, the thrips were transferred directly to plants in the field. Field releases continued throughout 1930. By 1932-1933, several hundred hectares of thripstunted C. hirta had been overgrown by plant competitors of greater forage value. Shaded and greatly weakened by thrips attack, these weeds were soon defoliated and killed. Regrowth was readily located and attacked by L. urichi. By 1937, the competitive ability of the weeds was permanently impaired by continued thrips attack except in a few shaded and wet areas, and successful biological control was achieved (Simmonds, 1937; Rao et al., 1971; Goeden, 1978; Julien, 1982). During the 1920s, New Zealand joined the list of Commonwealth countries sponsoring original research on biological control of weeds. Studies of insects attacking gorse, Ulex europaeus Linnaeus (Leguminosae), were initiated in England in 1926 and the introduction and successful colonization of the seed weevil, Apion ulicis Forster (Coleoptera: Apionidae), was accomplished during 1929-1931. Surveys of insects attacking blackberries (Rubus spp., Rosaceae) in Europe and North America were conducted during the mid-1920s, but no species was thought safe enough for introduction and the project was abandoned. Beginning in 1927 and continuing into 1930, diapausing pupae of the cinnabar moth, Tyria jacobaeae (Linnaeus) (Lepidoptera: Arctiidae), a defoliator of tansy ragwort, Senecio jacobaea Linnaeus (Asteraceae), were introduced into New Zealand

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from England, but establishment was not achieved. Australia also received T. jacobaeae from New Zealand during 1929-1932, beginning a series of colonizations continued in the 1950s and 1960s. Efforts to establish this moth were thwarted by strong predation by native insects, mainly scorpion flies. All attempts to establish this moth were unsuccessful (Goeden, 1978; Julien, 1982, 1992). It was not until the USDA study and introduction in 1969 of the chrysomelid beetle, Longitarsus jacobaeae (Waterhouse), for the control of tansy ragwort in northern California and Oregon that efforts against this weed became successful (Frick, 1970; Hawkes & Johnson, 1978; McEvoy et al., 1991). In fact, the high degree of biological control attained rates it among the major successes (Julien, 1992). The success of the prickly pear program led Australia to undertake biological control of other widespread, introduced, rangeland weeds, including cocklebur (Xanthium strumarium Linnaeus, Asteraceae). Foreign exploration for Australia began in the United States during 1929. St. Johnswort (Hypericum perforatum Linnaeus, Hypericaceae) was another pest for which foreign exploration for Australia began in England during 1926. The former project yielded only a limited measure of biological control. The latter project produced varying results with different introduced insects in different situations, analyzed in part by careful, quantitative, ecological research (N. Clark, 1953; L. R. Clark, 1953). This type of research has come to characterize contemporary Australian projects in the biological control of weeds. The insect agents and technology transferred from the Hypericum project contributed greatly to the development of biological control of weeds in North America. Before World War II, groundwork was laid for the rapid expansion of biological control of weeds that occurred during the 1950s, 1960s, and 1970s. Professor H. S. Smith [who first coined the term "biological control" (DeBach, 1964)] initiated the first project in the biological control of weeds in the continental United States. This involved the introduction of insects to control the native prickly pear cacti, Opuntia littoralis (Engelmann) Cockerell and O. oricola Philbrick, and their hybrids on rangeland on Santa Cruz Island off the coast of southern California. Several insect species from the California mainland and Texas were introduced to the island beginning in 1940, but successful biological control was attained only after Dactylopius opuntiae, native to Mexico and the southern California coast, was introduced to the island in 1951 from Hawaii ex Australia ex Mexico (Goeden et al., 1967; Goeden, 1978; Goeden & Ricker, 1981)! During World War II, activities on the biological control of weeds were reduced to a few transfer projects. For example, the leaf beetle Chrysolina hyperici (Frrster) (Coleoptera: Chrysomelidae) was transferred from Australia to New Zealand in 1943 for the biological control of St. Johnswort. In 1944, J. K. Holloway of the USDA and

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H. S. Smith arranged the introduction of several insect species from Australia for specificity testing in California and release during 1945-1946 for the biological control of St. Johnswort, also known as Klamath weed. The successful biological control of Klamath weed, primarily caused by the defoliating leaf beetle Chrysolina quadrigemina (Suffrian) (Coleoptera: Chrysomelidae), rivaled the Australian success with prickly pear cacti. This success primarily was responsible for fostering the establishment and expansion of the subdiscipline of biological control of weeds in North America (Huffaker, 1957). Within a decade after the liberation of C. hyperici and C. quadrigemina, the Klamath weed had been reduced in status from an extremely important rangeland weed to that of an occasional roadside plant. It now occurs at less than 1% of its former density and has been removed from the list of noxious weeds in California (Holloway & Huffaker, 1949, 1951). In 1950, Canada made its first intentional introduction of an insect for weed control when it imported Chrysolina quadrigemina and C. hyperici from California for control of St. Johnswort (Smith, 1951). In 1945, Hawaii resumed an earlier interest in the biological control of Eupatorium adenophorum Sprengel (Asteraceae) and introduced the stem-gall-forming fly, Procecidochares utilis Stone (Diptera: Tephritidae), presumably one of those natural enemies recommended for introduction to Hawaii by Koebele 20 years earlier. This successful introduction was followed by a series of projects undertaken by the Entomology Division of the Hawaii Department of Agriculture, which made Hawaii a center of activity in biological control of weeds during the 1950s and 1960s. Among the weeds on which foreign exploration was initiated and insects were introduced and established for biological control during the 1950s were the Christmas berry (Schinus terebinthifolius Raddi; Anacardiaceae), elephant's foot (Elephantopus mollis Humboldt, Bonplaud & Kuth; Anacardiaceae), sourbush (Pluchea odorata (Linnaeus) Cassini; Asteraceae), melastoma (Melastoma malabathricum Linnaeus; Melastomataceae), firebush (Myrica faya Aiton; Myricaceae), and emex (Emex australis Steinheil and E. spinosa Campdera; Polygonaceae). Substantial to complete biological control of emex reportedly was achieved at 600-to 1200-m elevations with the weevil Apion antiquum (Gyllenhal) introduced from South Africa in 1957 (Davis, 1966). Otherwise, these six projects and several other contemporary transfer projects on biological control of weeds in Hawaii unfortunately are characterized by a paucity of published results (Goeden, 1978; Julien, 1982, 1987, 1992). Another successful project was initiated at this time on black sage, Cordia macrostachya (Jacquin) Roemer & Schultes (Boraginaceae), an introduced weed in sugarcane fields on the island of Mauritius. A preliminary survey of the insect fauna of black sage and related plant species was

conducted in the West Indies during 1944-1946. Following detailed life history studies and host-specifcity tests, the leaf beetle Metrogaleruca obscura DeGeer (Coleoptera: Chrysomelidae) was introduced to Mauritius from Trinidad in 1947 (Simmonds, 1950). The beetle populations multiplied explosively and by 1950 had spread islandwide, causing heavy defoliation which killed plants or weakened them so they were replaced by competing plant species. A seedfeeding wasp, Eurytoma attiva Burks (Hymenoptera: Eurytomidae), also was introduced in 1949 and 1950 (Williams, 1960). Defoliation and seed destruction by these introduced insects have continued to prevent the regeneration of black sage (Simmonds, 1967; Goeden, 1978; Julien, 1992). This also was one of the first projects that involved entomologists affiliated with what eventually became the CAB International Institute of Biological Control (IIBC), a major worldwide, contract research organization now headquartered at Silwood Park, U.K. Most weeds targeted for biological control up to this time were introduced, perennial weeds of relatively undisturbed rangeland. However, beginning in Australia, Canada, and the United States in the late 1950s and early 1960s, projects were initiated on aquatic and semiaquatic weeds, annuals and biennials, and cropland and ruderal weeds. For example, the first aquatic weed targeted for biological control with insects was alligatorweed, Alternanthera phylloxeroides (Martius) Grisebach (Amaranthaceae), a pest in the southeastern United States. The first annual weed targeted for biological control with insects in North America was puncturevine, Tribulus terrestris Linnaeus (Zygophyllaceae). Both projects are reviewed in Section IV. The classic CIBC study by Zwrlfer (1965) of the insect fauna of Canada thistle (Cirsium arvense [Linnaeus] Scopoli) and other wild Cynareae (Asteraceae) in Europe sponsored by the (then) Canada Department of Agriculture during the early 1960s formed the foundation for a number of biological control projects targeted on introduced thistles in Canada and the United States (Schrrder, 1980). These included annual, biennial, and perennial species of Carduus, Centaurea, Cirsium, and Silybum (Goeden et al., 1974a). These projects continue with mixed results. Especially noteworthy is the successful biological control of musk thistle, Carduus nutans Linnaeus, attained with the introduced seedhead weevil, Rhinocyllus conicus Linnaeus (Coleoptera: Curculionidae), in Canada (Harris, 1984a) and Virginia (Kok & Surles, 1975) and the crown-mining weevil, Trichosirocalus horridus (Panzer) (Coleoptera: Curculionidae) (Kok, 1986). A biological control program on introduced spurges (Euphorbia ssp., Euphorbiaceae) of Eurasian origins was initiated by Canada in the early 1960s, with the first introduction of the hawk moth, Hyles euphorbiae Linnaeus (Lepidoptera: Sphingidae), from Germany in 1965 (Harris, 1984b). One lesson from biological control of spurges (also

Chapter 34 BiologicalControl of Weeds demonstrated with salvinia) is the value of correctly identifying and matching the targeted weed with related populations in its native geographical range to facilitate the collection and establishment of coevolved natural enemies. This demonstrates the value of plant taxonomy and insect taxonomy to the biological control of weeds. The biological control of rush skeletonweed, Chondrilla juncea Linnaeus (Asteraceae), in Australia is another noteworthy milestone. This project, launched in 1971 with cooperation between Italy and Australia, was the first to involve the intentional international transfer of a phytopathogen, i.e., the rust fungus (Uredinales) Puccinia chondrillina Bubak & Sydenham, for the successful biological control of a weed. This project also was one of the first to target a weed of cropland (nonirrigated wheatland). It established procedures for testing phytopathogens for host specificity under quarantine conditions and involved the first intentional importation and release in 1971 of a phytophagous mite [Eriophyes chondrillae (Canestrini) (Acarina: Eriophyidae)] for biological control (Cullen, 1974, 1978). Other projects on biological control of weeds have been initiated, including more than 80 in the United States and Canada (Goeden et al., 1974a; Julien, 1987, 1992). Several could be singled out as representing additional "firsts." Programs in classical biological control of weeds, i.e., those involving the importation of exotic natural enemies, have become scientifically exacting and quantitatively precise, but more and more enmeshed in governmental regulation (Harris, 1991; Goeden, 1993). In part this is due to the increasing number of workers in this subdiscipline (19 attendees at the first biological control of weeds symposium in Switzerland in 1968 versus 134 attendees at the sixth symposium in Canada in 1984) and in part to records of several early-introduced natural enemies from nontargeted, indigenous plant species (Turner, 1984). Conflicts of interest between ranchers and beekeepers in Australia over the introduction of biological control agents for the control of Echium plantagineum Linnaeus (Boraginaceae) (called Paterson's curse or salvation Jane, respectively, by these contending parties) caused the enactment of the Biological Control Act of 1984. This Act details how weeds targeted for biological control are to be open to public review before the release of biological control agents, among other comprehensive regulations (Cullen & Delfosse, 1985).

SCOPE OF BIOLOGICAL CONTROL OF WEEDS Target W e e d s Julien (1982) and Julien et al. (1984), list 101 species of weeds that have been targeted for biological control. Thirtythree plant families are represented among these 101 weed species, 25 of which belong to the Asteraceae and 19 of

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which are Cactaceae; the other 31 families are represented by five or fewer species (Julien et al., 1984). Historically, biological control with introduced natural enemies has primarily been directed against perennial, terrestrial weeds of pastures and rangeland. Pemberton (1981) noted that only four (22%) of what Holm et al. (1977) considered to be 18 of the world's worst weed species have been targeted for biological control, i.e., Convolvulus arvensis Linnaeus (Convolvulaceae), Cyperus esculentus Linnaeus and C. rotundus (Cyperaceae), and Eichhornia crassipes (Martius) Solms-Laubach (Pontederiaceae). The successful biological control of the aquatic weed water hyacinth (E. crassipes) is reviewed here; projects on the other three species have been unsuccessful (Julien, 1982). Pemberton (1981) also noted "that biological control of weeds has not yet had a single project against a weedy grass . . . . " this despite grasses (Graminaceae) comprising 10 of the world's 18 worst weeds according to Holm et al. (1977). Two grasses, Digitaria sanguinalis (Linnaeus) Scopoli and Panicum dichotomiflorum Michaux, were included among the ca. 80 species or species groups of weeds listed by Goeden et al. (1974a) as targeted for biological control in the United States and Canada. Nothing resulted from these two projects, however, because as Schroeder and Goeden (1986) remarked, one of the first and easiest steps in any project on the biological control of weeds is to designate a weed as a target species. Weedy grasses traditionally have not been considered suitable for biological control because many are close relatives of important cultivars. The chances of finding arthropod natural enemies able to discriminate among such closely related, potential host plants were remote. However, phytopathogens offer promise for control of graminaceous weeds, as some are extremely host specific, e.g., rust fungi (Section 3). Weeds not amenable to biological control include (1) weeds of highly disturbed habitats, e.g., cropland, subject to host-plant removal by tillage and to pesticide applications, (2) submersed aquatic weeds, which apparently have few host-specific natural enemies, (3) highly toxic weeds for which tolerable densities are too low to be obtained by use of natural enemies, (4) minor weeds of limited distribution that do not threaten to invade other areas, and (5) weeds whose eradication is sought, because the goal of biological control is only the reduction of a pest's densities to tolerable levels, never its eradication (Harris, 1971; Frick, 1974; Goeden, 1977). Most weeds successfully controlled with introduced natural enemies were introduced plant species (Julien, 1982; Julien et al., 1984). Only four species of native weeds have been successfully controlled with intentionally introduced organisms: Opuntia dillenii (Ker-Gawler) Haworth (Cactaceae) on the island of Nevis in the West Indies (Simmonds & Bennett, 1966); O. littoralis and O. oricola on Santa Cruz Island off southern California (Goeden et al., 1967;

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Goeden & Ricker, 1981); and O. triacantha (Willdenow) Sweet on the islands of Antigua, Monserrat, and, again, Nevis in the West Indies (Simmonds & Bennett, 1966; Bennett, 1971). All four of these native weeds are prickly pear cacti (subgenus Platyopuntia), which along with other Cactaceae, as Moran and Zimmerman (1984) noted, are unusual among terrestrial weeds, e.g., as regards their insect relations. Before their biological control began, cacti were among the world's most economically important and troublesome pasture and rangeland weeds. Insect A g e n t s Used Unless otherwise indicated, the following characterizations were taken from Julien et al. (1984) (see Chapter 17). Julien (1982) lists 174 biological control projects directed against the 101 weed species discussed earlier. Of these 174 projects, 151 (87%) used exotic organisms introduced against 82 weed species, and 23 (13%) used native organisms against 26 weed species. One hundred seventy-one species of insects from 7 orders and 38 families comprised 98% of all releases of natural enemies and 96% of all species of natural enemies released for biological control of these 101 weeds. Most released species were Coleoptera, Lepidoptera, Diptera, and Hemiptera (Homoptera and Heteroptera) in this order of decreasing use. Few species of Orthoptera, Thysanoptera, and Hymenoptera have found use as agents for biological control of weeds. Among the 69 colonized species of Coleoptera, 60 colonized species of Lepidoptera, 20 colonized species of Diptera, and 16 colonized species of Hemiptera, 65, 55, 70, and 66% became established and 29, 20, 19, and 44% proved effective as agents for biological control of weeds, respectively. The 12 families of insects that contained the most species released for biological control of weeds, in decreasing order of magnitude, were Chrysomelidae (Coleoptera), Curculionidae (Coleoptera), Pyralidae (Lepidoptera), Dactylopiidae (Hemiptera-Homoptera), Tingidae (Hemiptera-Heteroptera), Tephritidae (Diptera), Cerambycidae (Coleoptera), Noctuidae (Lepidoptera), Apionidae (Coleoptera), Agromyzidae (Diptera), Gelechiidae (Lepidoptera), and Tortricidae (Lepidoptera). Moran and Zimmerman (1984) reported that 63 species of cactophagous insects were introduced worldwide for biological control of 22 species of Cactaceae. Nineteen (30%) of those species were successfully established. Australian entomologists introduced 54 species of insects for cactus control; South African entomologists introduced 24 species of insects for cactus control. P h y t o p a t h o g e n i c A g e n t s Used When the status of projects on the biological control of weeds in the United States and Canada was assessed for the

Weed Science Society of America by Goeden et al. (1974a), very few weed pathogens were in use as biological control agents. However, the decade of the 1970s saw a flurry of research efforts to use phytopathogens, especially fungi, for biological control of aquatic and terrestrial weeds (Charudattan, 1978; Freeman & Charudattan, 1981; Charudattan & Walker, 1982). Julien (1982) listed four phytopathogens as imported for biological control of weeds worldwide. Two of these pathogens were accidental introductions; however, the other two, both rust fungi, provide excellent examples of successful control of alien terrestrial weeds with intentionally introduced natural enemies. The historically significant introduction of Puccinia chondrillina into Australia in 1971 for the biological control of rush skeletonweed has already been noted. The high degree of host specificity exhibited by P. chondrillina prevented the direct transfer of the Australian material to control the two forms of rush skeletonweed found in the western United States. Surveys in Europe located a strain of P. chondrillina that attacked the predominant form of the weed in the United States (Emge et al., 1981). The second example was the successful biological control of the weedy blackberries Rubus constrictus Lefevre & Mueller and R. ulmifolius Schott (Rosaceae) with Phragmidium violaceum (Schultz) Winter introduced from Germany to Chile in 1973 (Oehrens, 1977). A more recently reported example of the successful use of an intentionally introduced pathogen in the biological control of Hamakua pamakani, Aegeratina riparia (Regel) King & Robinson (Asteraceae), was achieved by the Cercosporella sp. (Uredinales) imported from Mexico to Hawaii and released in 1975 (Trujillo, 1985). Charudattan (1984) discussed plant pathogens employed as "microbial herbicides." This strategy employs alien or native pathogens mass-cultured and applied as inundative inocula on target weeds. Successful examples involve (1) Colletotrichum gloeosporioides f. sp. aeschynomene, registered and sold as Collego | for control of northern jointvetch, Aeschynomene virginica, on rice and soybeans in Arkansas (Templeton et al., 1978); and (2) Phytophthora citrophthora (R. E. & E. H. Smith) Leonian (Peronosporales), registered and sold as DeVine | for control of milkweed vine, Morrenia odorata (Hook. and Am.) Lindle, in citrus in Florida (Ridings et al., 1978). O t h e r A g e n t s Used Two species of mites (Acarina) have been successful as agents for biological control of weeds. Tetranychus opuntiae Banks (Tetranychidae) was an accidental introduction on prickly pear cacti in Australia. The association resembles many examples of accidentally introduced phytophagous insects reported to feed on alien and native plants. Eriophyes chondrillae (see p. 877) was the first mite species

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intentionally transferred between continents for biological control of weeds (Cullen, 1974, 1978). As with the rust fungus, workers returned to Europe to obtain a biotype of E. chondrillae that would attack rush skeletonweed in the western United States; one was found in Italy by Sobhian and Andres (1978). Another eriophyid mite, E. boycei Keifer (Eriophyidae), was exported from California to the USSR in 1971 and 1972 for the biological control of ragweeds (Ambrosia spp., Asteraceae), but it was not released (Goeden et al., 1974b). Cromroy (1982) cited additional examples of native and introduced mites attacking weeds in an attempt to demonstrate their efficacy as biological control agents. Again, few substantive examples of accidental biological control are known. Nematodes are well known as plant pests, but few species are used as agents for biological control of weeds worldwide. Only Paranguina picridis Kirjanova & Ivanova (Nematoda: Tylenchidae) was cited as an introduced agent by Julien (1982) and Julien et al. (1984). In 1976, it was released in restricted field trials in Quebec and Saskatchewan, following its introduction from the USSR for the biological control of Russian knapweed, Centaurea repens Linnaeus (Asteraceae). Paranguina picridis was successfully moved from central Asia to the Crimea and reportedly yielded good control of Russian knapweed (Kovalev, 1973). Experimental field use was made of Nothanguina phyllobia Thorne (Nematoda: Neotylenchidae) by augmenting its naturally occurring populations with large numbers of infectious larvae to control silverleaf nightshade, Solanum elaeagnifolium Cavanilles (Solanaceae), its native weedy host plant in Texas (Orr, 1980). The introduction of N. phyllobia into Australia and South Africa, where silverleaf nightshade is an alien weed, has been considered. Other invertebrate natural enemies have limited use as nonselective grazers in biological control of aquatic weeds. These include crayfish, snails, and tadpole shrimp (Andres & Bennett, 1975; Takahashi, 1977). A vertebrate herbivore, the grass carp, Ctenopharyngodon idella (Curvier & Valenciennes) (Pisces: Cyprinidae), has yielded mixed results in different countries when introduced against mixes of aquatic weeds (Julien, 1982, 1992). Seven other fish species and the manatee complete the list of vertebrates that have limited use in aquatic weed control (Andres & Bennett, 1975; Julien, 1982). Geese, sheep, and goats have long been used as managed grazers of terrestrial weeds (King, 1966).

Countries More than 70 countries were involved in 499 releases of introduced natural enemies for the biological control of weeds (Julien, 1982; Julien et al., 1984). The principal countries involved through 1970 were mentioned earlier in this chapter. Julien et al. (1984) listed world regions by the number of direct and indirect (transfer projects) releases of natural enemies in the following descending order of activ-

ity: Australia, with 108 releases; North America, with 80; Hawaii, with 71; all other Pacific islands, with 69; Africa exclusive of the Republic of South Africa, with 48; South Africa, with 34; the Caribbean islands, with 32; the Indian Ocean islands, with 23; Asia, with 20; South America, with 7; the South China Sea islands, with 6; and Europe, with 1 release. Europe has long served as a source of natural enemies for biological control of weeds as well as a principal source of the target weeds themselves (Julien, 1982), reflecting patterns of world commerce and human immigration (Schroeder & Goeden, 1986). Pemberton (1981) developed a separate system of ranking world regions by the number of projects that resulted in releases of natural enemies. From greatest to least active, these regions were North America, the Pacific islands (including Hawaii), Africa, Asia, Australia, Europe, the Caribbean islands, South America, Central America, and the Middle East. In terms of countries targeting the most weeds against which natural enemies were released, Africa and Australia exchanged rankings, while the other countries retained their order. Perhaps it is only a coincidence that the first set of rankings was compiled by an Australian, and the second system by a North American. Or, indeed, it may reflect how projects are composed and priorities assigned by research administrators in the several countries. The focusing of research personnel and resources on fewer weeds could result in the importation of more agents per weed. Agencies Many of the agencies involved in the biological control of weeds were mentioned previously. Julien et al. (1984) ranked research organizations involved in biological control of weeds by the total numbers of releases of natural enemies (repeated releases excluded). Ranked accordingly, in descending order, along with percentages judged effective (established and successful) by Julien et al. (1984) in parentheses, these mainly nonprofit governmental or international agencies were as follows: the Commonwealth Institute of Biological Control (CIBC [now IIBC]), with 79 releases (11% effective); the Hawaii Department of Agriculture, with 69 (43%); the U.S. Department of Agriculture (USDA), with 41 (30%); the Commonwealth Scientific and Industrial Research Organization (CSIRO), Australia, with 40 (33%); the Commonwealth Prickly Pear Board, Australia, with 37 (24%); Agriculture Canada, with 35 (17%); the Department of Agriculture and Fisheries, South Africa, with 33 (35%); the Queensland Department of Lands, Australia, with 28 (15%); the Ministry of Agriculture and Fisheries, Fiji, with 16 (7%); the Department of Scientific and Industrial Research, New Zealand, with 12 (20%); plus unnamed miscellaneous agencies, with 80 (40%), and unknown agencies, with 34 (39%). Most domestic research by Agriculture Canada on bio-

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logical control of weeds with insects is conducted at the Regina, Saskatchewan, Research Station. Canadian universities and provincial agencies also actively collaborate with Agriculture Canada scientists on domestic phases of projects. Most overseas research for Agriculture Canada on candidate agents is conducted by IIBC entomologists in Europe. IIBC laboratories where research on biological control of weeds is conducted on a contract basis currently include those located at Rawalpindi, Pakistan, at Delrmont, Switzerland, and on Trinidad in the West Indies. The CSIRO maintains a European laboratory at Montpellier, France (Schroeder & Goeden, 1986). The Queensland, Australia, Department of Primary Lands has maintained a North American Field Station at Temple, Texas, in recent years. The United States effort on biological control of weeds through the introduction of new natural enemies centered around the USDA laboratory at Albany, California, from the late 1950s to 1988. With the release of control agents from the Albany quarantine throughout the United States, other USDA personnel or laboratories were assigned biological control responsibilities at Fort Lauderdale and Gainesville, Florida; Beltsville and Frederick, Maryland; Stoneville, Mississippi; Columbia, Missouri; Bozeman, Montana; Lincoln, Nebraska; and Lubbock and Temple, Texas. A European laboratory for research on biological control of weeds was located at Rome, Italy, in 1959, which was later moved to Montpellier, France, in the mid-1980s, with substations at Rome and Thessaloniki, Greece. Other USDA laboratories for weed research are located at Hurlingham, Argentina (Coulson, 1985), and Townsville, Queensland, Australia. State institutions in the United States that figured in the miscellaneous category of Julien et al. (1984) noted earlier and where at least one project on biological control of weeds was active during 1967-1987 were the University of Arkansas; the University of California, Berkeley, Davis, and Riverside; the California Department of Food and Agriculture, Sacramento; the University of Florida, Gainesville; the University of Idaho; Kansas State University, Manhattan; Montana State University; North Dakota State University, Fargo; Oregon State University; the Oregon State Department of Agriculture, Salem; Virginia Polytechnic Institute and State University; Washington State University; and the University of Wyoming, Laramie.

CASE HISTORIES OF RECENT SUCCESSES IN NORTH AMERICA AND OTHER PARTS OF THE WORLD A l l i g a t o r w e e d , Alternanthera phylloxeroides, in t h e S o u t h e a s t e r n United States a n d Australia Alligatorweed is an emersed, perennial, aquatic plant from South America whose hollow, segmented stems allow

it to form dense floating mats on the surface of rivers and other bodies of water. The floating mats block navigation, inhibit water use, and limit water flow. The rooted, segmented stems often break and allow the mats to float freely, spread, and root at new sites. The ability of the stems to root freely at the nodes renders mechanical removal of the mats ineffective, as the remaining fragments merely compound the problem. Stem segmentation also limits herbicide translocation and effectiveness. In fact, attempts to control alligatorweed with herbicides have often worsened the problem by killing neighboring plants and allowing the alligatorweed to flourish (Maddox et al., 1971; Coulson, 1977). In view of the difficulties encountered in controlling alligatorweed, and as part of their expanded aquatic weed control program, the U.S. Army Corps of Engineers sought the assistance of the USDA, Agricultural Research Service (ARS), in assessing the potential for controlling this pest by biological means. In 1960, G. B. Vogt traveled to Argentina and adjacent countries to the north in search of phytophagous arthropods and plant pathogens that could be used to control this weed. He recorded over 40 species of natural enemies attacking alligatorweed, 3 of which he singled out as particularly important: Agasicles hygrophila Selman & Vogt (Coleoptera: Chrysomelidae), Amynothrips andersoni O'Neill (Thysanoptera: Phlaeothripidae), and Vogtia malloi Pastrana (Lepidoptera: Phyctinae). In 1962, the USDA opened a laboratory near Buenos Aires, Argentina, to study the biologies and host-plant specificities of these candidate biological control agents (Coulson, 1977). Adults of the alligatorweed fleabeetle, Agasicles hygrophila, feed on the emersed leaves and stems of alligatorweed. The eggs are oviposited in clusters on the undersides of young leaves. The developing larvae feed on the leaves and stems; the third or last instar tunnels into the hollow stems to pupate. The imago later chews its way out through the stem wall and the life cycle begins again. Maddox (1968) reported as many as five generations per year in Argentina. Beetle feeding destroys both leaves and stems, and the latter become waterlogged after repeated perforations with adult emergence holes, causing the mats to sink. The small (2.2 mm), black, short-winged or macropterous adults of Amynothrips andersoni feed among the bracts of the young buds or in the leaf axils. The larvae are reddish and complete their development in about 30 days. There are three to five generations annually. The thrips overwinters mainly as adults. Thrips feeding scars the leaf surface and stunts and distorts the stem growth (Maddox et al., 1971). Vogtia malloi is nocturnal. Oviposition occurs on the terminal leaves. The neonate larvae tunnel into the stems. Larvae may exit periodically, reenter, and consequently damage a number of stems as they pass through five instars. Pupation occurs inside the hollow stem. There are three to five generations per year. Vogtia feeding causes extensive

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stem collapse and it develops well on both rooted and freefloating plants (O'Neill, 1968; Maddox et al., 1971). Alligatorweed fleabeetles were introduced into the United States from 1964 through 1970 from waterways near Buenos Aires (Coulson, 1977). The beetle is now established in Alabama, Florida, Georgia, Louisiana, Mississippi, South Carolina, and Texas but failed to establish in Arkansas, California, North Carolina, and Tennessee. Attempts were made to establish fleabeetles from a site south of Buenos Aires in hopes they would be better coldadapted to the more northern alligatorweed infestations. This proved unsuccessful. A laboratory colony of V. malloi established at Albany, California, from collections near Buenos Aires served as the source of North American colonies during 1971. A second laboratory colony originating from Neocochea, 156 km south of Buenos Aires, provided stock for releases through 1972 (Coulson, 1977). The moth is established in Arkansas, Florida, Louisiana, Mississippi, South Carolina, and Texas (Julien, 1987). Agasicles gave good initial control in many coastal areas of the southeastern United States, but it has recently exhibited sensitivity to hot, dry summers and cold winters. Earlyseason supplemental releases of adult fleabeetles have enhanced its impact in inland areas. No other types of alligatorweed control are now needed in Florida, Louisiana, and Texas. Although sizable populations of Amynothrips are active early in the season, their impact is uncertain. Vogtia malloi has reduced mats by 70-80% in coastal areas of Mississippi, but control is uneven and appears cyclical over a period of several years (Julien, 1987). Although insects had been used to control terrestrial weeds on numerous occasions, the introduction of Agasicles into the southeastern United States in 1964 marked the first use of an insect as an aquatic weed control agent. The relative success of this project reduced skepticism over whether insects associated with aquatic weeds were sufficiently monophagous to permit their use for biological control and focused increased attention on other species of emersed and floating weeds (Andres & Bennett, 1975). The initial buildup and control of alligatorweed on the St. Johns River, Florida, occurred within 15 months of initial release, while at other sites it took several years. The different rates of control may relate to the carbohydrate reserves in the stems composing the mats, the growth rate of the plant, the length of the growing season, and the percent of the mat renewed each season (Andres & Bennett, 1975; Coulson, 1977). Fleabeetles from U.S. colonies also were transferred to Australia in 1977, New Zealand in 1982, and Thailand in 1982. The beetle is established in all three countries. A fourth species, Disonycha argentinensis Jacoby (Coleoptera: Chrysomelidae), was introduced into Australia in 1980 and New Zealand in 1982 directly from Brazil, but it failed to establish. Agasicles spread quickly through the infesta-

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tions of alligatorweed in Australia and provided substantial control of the weed within 14 months. Vogtia impact on alligatorweed there is masked by Agasicles-caused plant injury. The moth is ineffective in terrestrial areas (Julien, 1987).

Puncturevine, Tribulus terrestris, in the S o u t h w e s t e r n United States, Hawaii, a n d St. Kitts This cosmopolitan weed of Old World origins is a prostrate, annual herb that bears an abundance of small yellow flowers and troublesome spiny fruit. These fruit separate at maturity into five, boney, one- to four-seeded segments, each of which is studded with two or four, sharp, rigid, divergent spines. The seeds apparently survive burial in soils for 20 years. The spines penetrate and lodge in tires, shoes, and the feet and fur of animals, which aids seed dissemination (Johnson, 1932; Goeden & Ricker, 1973). The natural range of puncturevine includes the Mediterranean regions of Europe and Africa and drier parts of Asia (Andres & Angelet, 1963). It was accidentally introduced into the midwestem United States with livestock, especially sheep, imported from the Mediterranean area. Puncturevine now occurs from coast to coast, but is most common in the Southwest. It arrived in California about 1900, apparently as a railroad ballast contaminant, and spread rapidly along railroad and highway fights-of-way. As an agricultural weed, its spiny fruit interfere with hand harvesting, injure livestock, and contaminate seed, feed, and wool (Johnson, 1932). It also is a weed of disturbed residential and industrial land and, like crabgrass, is a weed that many city dwellers recognize. As an annual, nonwoody, nonrangeland weed, puncturevine represents a departure from the traditional perennial range and pasture weed targeted for biological control. The natural enemies of puncturevine were surveyed in India, southem France, and Italy during 1957-1959. The seed-feeding weevil Microlarinus lareynii (Jacquelin duVal) (Coleoptera: Curculionidae) and the stem- and crown-mining weevil M. lypriformis (Wollaston) were selected as the most promising candidates for use as biological control agents. Field and laboratory studies conducted in France, Italy, and Califomia during 1959-1961 demonstrated that the adults fed on a wide range of plant species, but reproduction was successful only on puncturevine, other species of Tribulus, and a few herbaceous annual Zygophyllaceae native to the southwestern United States (Kallstroemia sp.; Andres & Angelet, 1963). Although minor concern was expressed over its potential detrimental effect on the native plants, this conflict of interest was resolved by weighing the potential benefits of biological control of puncturevine against these potential losses. With the need for action recognized, both weevils were approved

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for release in compliance with less complicated federal regulatory procedures then in use. Since their release, the weevils have been recorded feeding on some nonhost plants but reproduce only on Tribulus or closely related Zygophyllaceae (Andres, 1978). The immature stages of both weevils were described by Kirkland and Goeden (1977). The biology of M. lareynii was described by Andres and Angelet (1963) and Kirkland and Goeden (1978a); that of M. lypriformis by Andres and Angelet (1963) and Kirkland and Goeden (1978b). The egg of M. lareynii is deposited in a pit chewed in the pericarp of an immature fruit or occasionally in a floral bud or flower and capped with an anal secretion, often stained dark with feces. The larva feeds on the seeds and surrounding tissues, destroying seeds directly by mastication or indirectly by inducing abortion. Pupation occurs in an open cell in the fruit. The adult chews an emergence hole between adjacent carpels. The eggs hatch in 2 - 3 days, and larval development lasts 13-16 days; the pupal stadium lasts 4 5 days in southern California. The biology of M. lypriformis is similar, only most oviposition occurs in the undersides of the central, older parts of the prostrate, spreading, matlike plants (i.e., root crowns, primary branches, and stem bases). The young larvae tunnel into the pith, where they largely confine their feeding, eventually pupating in open cells in the larval mine. The adults emerge from circular holes chewed mainly in the upper surfaces of stems, branches, and crowns. Both weevil species are multivoltine and produce a generation each month in the summer by reinfesting plants and attacking new plants as dispersed adults. Both species overwinter as adults in reproductive diapause among surface debris and plant litter and on or around associated nonhost plant species. The weevil adults were initially imported from Italy and released directly in the field in Arizona, California, Colorado, Nevada, Utah, and Washington in July and August 1961 (Huffaker et al., 1961; Andres & Angelet, 1963); establishment occurred in Arizona, California, and Nevada (Maddox, 1976). The weevils established readily in California and spread rapidly and widely, aided by extensive transfers of field-collected adults (Goeden & Ricker, 1967). Maddox (1976) reported the subsequent spread and establishment of both weevils in Kansas, New Mexico, Oklahoma, Texas, and Utah and of the stem weevil in Florida as well as the spread of both weevils into Mexico. Soon after both weevils were established in southern California, Goeden and Ricker (1967, 1970) reported substantial egg predation by native Heteroptera and larval and pupal parasitism by indigenous chalcidoid Hymenoptera. Goeden and Kirkland (1981) assessed this predation in irrigated and nonirrigated field plots and determined that about half the seed weevil eggs infesting puncturevine fruit were killed by egg predation that reduced fruit infestation rates from 50 to 25%. Maddox (1981) determined that seed

germination in infested fruit was drastically reduced. Kirkland and Goeden (1978c) used the insecticide check method to assess the effects of both weevils acting in concert on irrigated and nonirrigated plants in field plots. Their results showed that water stress was the principal cause of earlyseason plant mortality; however, weevil attack caused a 60% reduction of flower production on surviving plants in nonirrigated plots. Moreover, only half of these flowers on nonilTigated plants produced fruit late in the growing season. Maddox (1981) also used insecticidal check plots to demonstrate that the stem weevils had a greater impact than the seed weevils on puncturevine plants per se, as measured by stem growth rates, metered water stress, and whole-plant biomass. Maddox (1981) and Huffaker et al. (1983) reported that seed weevils, largely acting alone in experimental field plots, increased flower production by puncturevine, which they attributed to some vaguely described "survival strategy" of the weevil. Huffaker et al. (1983) reported that 15 years after introduction of the weevils, puncturevine coverage and seed production declined in more than 80% of 1200 field plots monitored in California. They attributed this decline to the actions of both species of weevils. The biological control of puncturevine in California generally is considered a partial success or a substantial success under field conditions where weevil attacks intensify moisture stress on nonirrigated plants (Kirkland & Goeden, 1978c; Maddox & Andres, 1979; Julien, 1982). Puncturevine also provides examples of successful transfer projects. Both species of weevils were transferred as field-collected adults in 1962 from California to Hawaii, where puncturevine and the perennial Tribulus cistoides Linnaeus were brought under complete biological control within a few years on all islands (Julien, 1982). Stem weevils subsequently were transferred to the island of St. Kitts in the West Indies from Hawaii in 1966, and seed weevils were transferred from southern California to St. Kitts in 1969. The latter species failed to establish, but the former species alone provided complete control of T. cistoides (Julien, 1982).

W a t e r Hyacinth, Eichhornia crassipes, in t h e S o u t h e a s t e r n United States Eichhornia crassipes, a floating plant native to the American tropics, has become a naturalized weed throughout tropical, subtropical, and temperate climatic areas of the world (Bock, 1969). The plant favors vegetative reproduction, daughter plants forming on stolons originating from the central rhizomes. Enormous mats can form quickly, the plant doubling in volume every 10-15 days under favorable conditions (Penfound & Earle, 1948). Water hyacinth's ability to completely cover lakes and slow-moving streams can cause major navigational, agricultural, and health-re-

Chapter 34 BiologicalControl of Weeds lated problems and otherwise disrupt the normal chains of events that occur in the aquatic habitat. Although herbicides can hold the plant in check, chemical control can be costly and only temporary at best. Interest in biological control of water hyacinth developed simultaneously between the U.S. Army Corps of Engineers and the British Ministry of Overseas Development (Bennett & Zwrlfer, 1968). Research developed along two lines. Surveys for natural enemies were carried out in Guyana, Surinam, the Amazon region of Brazil, Uruguay, the West Indies, and British Honduras (Bennett & Zwrlfer, 1968). Of several dozen phytophagous arthropods found on this aquatic weed, seven were thought to have some biological control potential. Of these, three were tested and cleared for importation to North America: Neochetina bruchi Hustache (Coleoptera: Curculionidae), N. eichhorniae Warner, and Sameodes albiguttalis, Warren (Lepidoptera: Pyralidae). A fourth insect, Acigona infusella (Walker) (Pyralidae), was eventually released in Australia (Julien, 1987). In the United States, research also involved the study and use of indigenous organisms attacking water hyacinth, i.e., Bellura densa (Walker) (Lepidoptera: Noctuidae), Cercospora rodmani Conway (Hyphomycetes), and Acremonium zonatum (Sawada) Gams (Hyphomycetes). Although the native host of B. densa is pickerelweed, Pontederia cordata Linnaeus (Pontederiaceae), a close relative of water hyacinth, the larvae can severely damage the latter weed at times. Biological studies were conducted and a diet on which to mass rear B. densa was developed, followed by the experimental release of many eggs and first instars to augment native populations. The moth had little impact in the United States (Julien, 1987). Cercospora rodmani is a fungus indigenous to Florida that causes leaf spot, leaf necrosis, and secondary root rot of hyacinth plants. It also causes plant death when sprayed on mats of water hyacinth. The fungus is being registered as a commercial mycoherbicide (Charudattan, 1986). Another fungus, Acremonium zonatum, damages water hyacinth in southern Florida and Louisiana but seems to have its greatest impact when associated with the mite Orthogalumna terebrantis Wallwork (Acarina: Galumnidae). This mite is native to South America and accidentally entered the United States after its host plant was intentionally introduced as an ornamental. The females of Neochetina eichhorniae and N. bruchi chew holes in the leaf petioles into which they insert one or several eggs, respectively (Center, 1982). The larvae tunnel beneath the epidermis and work their way down to the base of the petiole or the rhizome to which the leaf is attached, by which time they are in their third and final instar. The fully grown larvae chew their way out of the stems and move toward the surface of the water. They cut several lateral rootlets which are incorporated into an underwater pupal cocoon attached to the hyacinth roots. The

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emerging adults leave the water from emergent plant parts, where they feed, mate, and oviposit. The weevil overwinters as larvae, pupae, or adult. There is one generation per year (DeLoach & Cordo, 1976). Sameodes albiguttalis oviposits into the spongy leaf petioles, favoring areas with cuts in the epidermis or injuries made by other organisms. The young larvae feed under the epidermis, periodically exiting onto the petiole surface, crawling downward, and then reentering the globose area of the petiole to continue feeding. The fifth and final instar excavates a pupal cell in the petiole. DeLoach and Cordo (1978) estimated that there are five generations per year in Argentina. Larval feeding causes the petioles to break and die and results in heavy dieback the following winter. Neochetina eichhorniae was introduced into the United States in 1972 from the vicinity of Buenos Aires (Center, 1982). It has established throughout the range of water hyacinth in North America. This weevil also was subsequently transferred from the United States to several other countries, where it is now established: Australia, Fiji, India, Indonesia, New Guinea, South Africa, Sudan, and Thailand (Julien, 1987). Neochetina bruchi was introduced into the United States from Argentina in 1974 and is now established in California, Florida, Louisiana, and Texas. Establishment has also been confirmed in India and Sudan (Julien, 1987). Sameodes albiguttalis was released in the United States in 1977 (Center & Durden, 1981) and is established in California, Florida, Louisiana, and Mississippi. Establishment has also been confirmed in India and Sudan (Julien, 1987). Acigona infusella was introduced into Australia from Brazil but failed to establish. Orthogalumna terebrantis was introduced into Egypt and Zambia, but again establishment has not been confirmed (Julien, 1987). Neochetina eichhorniae has probably been the major contributor to the control of water hyacinth in the United States, Australia, and Sudan. Cofrancesco et al. (1985) documented the reduction of water hyacinth in Louisiana from about 445,000 ha in 1974 to 122,000 ha by 1980. Sameodes albiguttalis retards growth in the early stages of mat development, although its action may be sporadic and patchy (Center, 1985; Julien, 1987). When introduced from Buenos Aires, N. bruchi was observed successfully controlling water hyacinth in an isolated reservoir in La Rioja Province, Argentina, suggesting that its control potential should not be discounted (DeLoach & Cordo, 1983). The water hyacinth project was the second attempt at biological control of an aquatic weed with introduced arthropods. Although focus remained on the search and importation of natural enemies from the native South American range of the weed, the discovery of the indigenous Bellura densa and Cercospora rodmani added another dimension to the research on biological control of aquatic

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weeds in the United States. Despite the limited success of attempts to augment natural B. densa population levels in Florida, the moth may eventually prove useful as an introduced agent in other countries. Biological control of water hyacinth also differed from earlier projects on the biological control of weeds because the benefits realized were not confined to areas of low economic worth, e.g., rangeland, pastures, and waste areas, but rather involved the management of valuable water resources. As such, it offered one of the first real opportunities to develop a weed management program that could integrate imported natural enemies with other, more traditional and costly, weed control methods. On the other hand, the reduction of water hyacinth to low levels has also tempted weed control workers to "clean up" remaining pockets of plants with herbicides. Without proper integration, this action can upset the balance between the natural enemies and their weed host and has resulted in further hyacinth outbreaks (Center, 1982). Buckingham and Passoa (1985) studied flight muscle development in the water hyacinth weevils. They suggested that in an integrated weed control program when conservation of the weevils is desired, summer herbicide applications should be delayed until the greatest number of newly emerged weevils with well-developed wing muscles are present. These agents would then be better able to migrate to unsprayed areas. They also suggested that herbicides should not be applied in the spring until water temperatures have risen above 18~ the threshold for wing development. Unfortunately, herbicidal control is more efficient if begun early in the season.

Three Recent S u c c e s s e s O u t s i d e of North A m e r i c a Cuscuta spp. in the People's Republic of China

The following account is largely taken from a translation of Wang (1986) provided to us by the author. Two species of parasitic weeds called dodders, Cuscuta australis R. Brown and C. chinensis Lamarck (Convolvulaceae), are serious weeds of oilseed, peanut, potato, and soybean crops in Shandong, Anhui, Hubei, Jilin, Liaoning, and Helongjiang Provinces and the Xinjiang autonomous Region, PRC. The fungal pathogen Colleotrichum gloeosporioides was isolated from dodder in soybeans in Jinan, Shandong Province, in 1963. The biology and mass culture of the fungus were studied from 1963 to 1966, which led to the development of a mycoherbicide named Lubao No.1. From its initial use in soybean fields in five provinces in 1966, production and application of this mycoherbicide grew until by the late 1970s, ca. 670,000 ha of soybeans were treated in 30 provinces. Reportedly, 85% control of these weeds

was realized in all fields and soybean losses were reduced by 3 0 - 50%. During the 11 years of the "Cultural Revolution," the production of Lubao No. 1 was severely curtailed and problems were experienced with the mycoherbicide; e.g., it had a short shelf life and required high humidity for infection. An improved strain called Lubao No. 1 $22 is currently in mass production and is widely used. Microbial herbicides are expected to receive considerable attention in the future in the PRC.

Ragweeds, Ambrosia spp. (in the USSR) Three species of ragweeds, Ambrosia artemisiifolia Linnaeus, A. psilostachya deCandolle, and A. trifida Linnaeus (Asteraceae), were accidentally introduced into the USSR from their native North America sometime during the 1920s to 1940s. They fast became noxious weeds and by 1980 had spread into the southern part of European USSR, Transcaucasia, Kazakhstan, and the Maritime Territory. Ambrosia artemisiifolia apparently is the most important of the three ragweeds, as it infests most crops and is costly and difficult to control with chemicals or by cultural and mechanical means. These ragweeds also have become medically important hay fever plants (Kovalev, 1974, 1980). Thanks to an informal cooperative program involving Canadian, United States, and USSR scientists and begun in 1965, about 450 species of insects, mites, and fungi have been identified as natural enemies of 17 species of Ambrosia in North and South America (Harris & Piper, 1970; Kovalev, 1971, 1980; Goeden & Ricker, 1976). More than 30 species of natural enemies were introduced into the Soviet Union from 1967 to 1979 (Kovalev, 1971, 1980; Goeden et al., 1974b). The host-plant specificities of these candidate agents were tested in quarantine in the USSR, using eight varieties of sunflower, Helianthus anuus Linnaeus (Asteraceae), as the "critical test plant," 18 species of Helianthus, and 80 species of cultivars representing 46 genera and 18 families of plants (Kovalev, 1970), in accordance with the so-called "centrifugal testing method" (Wapshere, 1974a) in general use today (see earlier). By 1980, four species of insects obtained from the same species of weeds in their native North America had been released to establish a complex of natural enemies in the Soviet Union. These introduced ragweed insects included Tarachidia candefacta Htibner (Lepidoptera: Noctuidae), a defoliator obtained from Canada and California and released on A. artemisiifolia in 1969 and on A. psilostachya in 1972, respectively (Kovalev & Runeva, 1970; Kovalev & Samus, 1972; Gilstrap & Goeden, 1974; Goeden et al., 1974b); Brachytarsus tomentosus (Say) (Coleoptera: Anthribidae), a pollen-feeding beetle first released in the northern Caucasus in 1978; Euaresta bella Loew (Diptera: Teph-

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ritidae), a monophagous seed feeder apparently obtained from Canada and released in the northern Caucasus in the 1970s with unknown results; and Zygogramma suturalis (Fabricius) (Coleoptera: Chrysomelidae), another defoliator obtained from Canada and the United States and first released in 1978 (Kovalev, 1980; Julien, 1982). Tarachidia candefacta was the first natural enemy released for ragweed control in the USSR and the first natural enemy intentionally introduced into Europe from North America for biological control of a weed. In mass rearing T. candefacta, specially designed oviposition units were used to harvest large numbers of eggs deposited on hanging threads. Larvae were fed a prepared diet (Kovalev & Runeva, 1970; Kovalev & Nayanov, 1971). Although successfully established on both A. artemisiifolia and A. psilostachya, it apparently has been unsuccessful as a biological control agent, largely because of predation of the exposed larvae (O. V. Kovalev in lit.) The results obtained with Zygogramma suturalis have been spectacularly successful under certain conditions (Reznik, 1991; Julien, 1992). This beetle was mass reared at several laboratories beginning in 1979 following its initial winter's survival. It was released south of the European part of the USSR and Transcaucasia to the Far East (Kovalev & Medvedev, 1983; Kovalev & Vechernin, 1986). Larvae and adults feed on leaves and inflorescence throughout the growing season and range of A. artemisiifolia from April to mid-September. The beetle produces two complete and a partial third generation annually (Kovalev, 1980). Kovalev and Vechernin (1986) reported that seventh-generation Z. suturalis formed feeding fronts consisting of a stable nondeclining wave of beetles which moved at a constant rate and which they termed an "isolated population wave (IPW)." On one state farm at Stravropol, the insects were concentrated in a narrow band at 5000 individuals per m 3, which completely destroyed all the ragweeds as it moved across an infested field at a rate of 3 m per day. About 10 million beetles were concentrated in a circular feeding front with a length of 1.5 km and a breadth of ca. 10 m. The weed-controlling action of these feeding fronts sharply increased yields of lucerne, sainfoin, and maize by two- to threefold.

Salvinia, Salvinia molesta D. S. Mitchell, in Australia and New Guinea Unless otherwise indicated, the following account was summarized from the review of Thomas and Room (1986). The free-floating aquatic fern Salvinia molesta (Salviniaceae) is native to Brazil. It was spread as an aquarium plant and botanical curiosity to tropical and subtropical Africa, Asia, Australia, Fiji, and New Guinea, where it

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rapidly propagated vegetatively to become one of the world's most important aquatic weeds. In 1955, it first appeared in Lake Kariba, a huge reservoir on the Zambia-Zimbabwe border, and quickly spread and soon covered 1000 km 2 or 21% of the lake's surface. CIBC entomologists conducted foreign exploration in South America for Salvinia auricularia Aublet, also called Kariba weed. Three insect species, the moth Samea multiplicatus Guenee (Lepidoptera: Pyralidae), the grasshopper Paulinia acuminata (DeGeer) (Orthoptera: Acrididae), and the weevil Cyrtobagous singularis Hustache (Coleoptera: Curculionidae), were recommended as the most promising agents for biological control of this fern. During the 1960s and 1970s, all three species of insects were released on Lake Kariba, elsewhere in Africa, and in Fiji. Only P. acuminata became established on Lake Kariba and provided limited control of salvinia. By 1970, Kariba weed was cited as one of the best documented contemporary examples of the importance of taxonomy to biological control of weeds. However, a pressed specimen of Kariba weed collected in 1941 and preserved in the Rio de Janeiro Botanic Garden was not Salvinia auricularia but rather a new species described as S. molesta in 1972. By 1978, this weed was determined to be a sterile hybrid species that originated in southeastern Brazil. Exploration by CSIRO entomologists resulted in the detection, study, and recommendation of Samea multiplicatus, P. acuminata, and what then was thought to be a separate biotype of C. singularis as the most promising candidate biological control agents. The weevil was introduced into Australia in 1980, where it established readily, and in less than 2 years the weevil destroyed a 200-ha infestation on Lake Moondarra in northern Australia. After additional study, this weevil was described as Cyrtobagous salviniae Calder & Sands. These results support the concept that the best natural enemies are obtained from the target weed species origin. This concept was challenged by Hokkanen and Pimentel (1984), but supported by Goeden and Kok (1986) and Moran et al. (1986), and most recently discussed by Dennill and Hokkanen (1990). Cyrtobagous salviniae was transferred to Papua, New Guinea, from Australia in 1982 and established only after the novel manipulation of the weevil's environment in field-release cages. This involved regular applications of urea fertilizer to the caged weed, which increased its nitrogen content and enhanced its nutritional suitability such that the weevils multiplied explosively. The weevils continued to multiply in phenomenal numbers once the cages were opened and this critical mass of weevils was given access to the large volume of unfertilized weed that covered Sepik Lake to a depth of up to 1 m. Following a large-scale redistribution program in August 1985, salvinia had been reduced from coveting 250 km 2 of water surface on the

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lower floodplain of the Sepik River to 2 K1TI2. This represented the destruction of 2 million metric tons of salvinia in 2 years!

FUTURE DIRECTION OF BIOLOGICAL CONTROL OF WEEDS The direction of biological control depends upon how the problems, tasks, and priorities of this subdiscipline are perceived (Harris, 1991, Goeden, 1993). The pressures of a rapidly expanding human population, increased environmental pollution, scarcity of natural resources, and increasingly stringent regulations governing pesticide use will speed the movement to biological control and other safe alternative control methods. The search for new, coevolved foreign and domestic natural enemies will continue, as will the development and registration of new mycoherbicides. Current techniques for finding, testing, introducing, colonizing, and manipulating these new natural enemies will continue (Zwrlfer & Harris, 1971; Frick, 1974; Andres et al., 1976; Klingman & Coulson, 1983; Schroeder & Goeden, 1986; Harris, 1991) and be refined. However, even these techniques are not without problems. Increasing human presence in many of the areas (such as western Europe) where weeds originated adds to the difficulty of locating natural populations of the weeds and their natural enemies (Schroeder & Goeden, 1986). The inability to find suitable natural enemies will promote attempts to artificially alter the host selectivity and adaptability of existing natural enemies by selective breeding or genetic engineering. Present efforts at genetic improvement of natural enemies are costly, are time-consuming, and may be of limited practical value (Beckendorf & Hoy, 1985). Trial feeding in caged host-specificity studies, though limited in extent, may provide sufficient grounds for the rejection of a candidate natural enemy, even if there was no previous record of nontarget plant attack (Dunn, 1978). In the future, the interpretation of such laboratory studies will be balanced with the increased use of multiple-choice, open-field experiments in which potted test plants will be intermingled with populations of the target weed and its associated natural enemies. Despite the potential of new biochemical and physiological techniques for unraveling the myriad factors involved in host plant-natural enemy interactions, it is doubtful that these will ever replace field and laboratory organism-population studies. Perhaps, biological control of weeds, like the so-called "dismal science" of economics (Stein, 1987), is destined to remain an art for the foreseeable future (Harris, 1976; Goeden, 1993). However, standardizing data collection techniques among countries will strengthen the significance of future project comparisons and generalizations (Harris, 1991; Julien, 1992).

Biological control will expand to new countries and include the transfer of proven biological control agents from other areas. As in the past, the transfer and establishment of successful agents is followed by the development of new facilities, expertise, and the undertaking of new projects. In developed countries, the main challenge will be to provide new biological control successes that will engage the imagination and support of research administrators and a public increasingly oriented toward high-technology solutions. Attempts to develop weed project cost-benefit analyses will improve, although efforts to include ecological and aesthetic benefits will continue to pose difficulties. To optimize the benefits of biological control, changes in agricultural production, resource use, and perceptions of what constitutes damaging weed populations will be required.

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Oehrens, E. (1977). Biological control of the blackberry through the introduction of rust, Phragmidium violaceum, in Chile. FAO Plant Protection Bulletin, 25, 26-28. O'Neill, K. (1968). Amynothrips andersoni, a new genus and species injurious to alligatorweed. Proceedings of the Entomological Society of Washington, 70, 175-183. Orr, C. C. (1980). Nothanguina phyllobia, a nematode biocontrol of silverleaf nightshade. In "Proceedings of the V International Symposium on Biological Control of Weeds, 1980, Brisbane, Australia" (E. S. Delfosse, Ed.), pp. 389-391. Pemberton, R. W. (1981). International activity in biological control of weeds: Patterns, limitations and needs. In "Proceedings of the V International Symposium on Biological Control of Weeds, 1980, Brisbane, Australia" (E. S. Delfosse, Eds.), pp. 57-71. Penfound, W. T., & Earle, T. T. (1948). The biology of the waterhyacinth. Ecological Monographs, 18, 447-472. Perkins, R. C. L., & Swezey, O. H. (1924). "The Introduction into Hawaii of Insects That Attack Lantana." Bulletin of the Hawaiian Sugar Plantation Association Experimental Station No. 16. Rao, V. P., Ghani, M. A., Sankaran, T., & Mathur, K. C. (1971). "A Review of the Biological Control of Insects and Other Pests in Southeast Asia and the Pacific Region." Commonwealth Institute of Biological Control Technical Communication No. 6, pp. 1-149. Reznick, S. Ya. (1991). The effects of feeding damage in ragweed Ambrosia artemisiifolia (Asteraceae) on populations of Zygogramma suturalis (Coleoptera, Chyrsomelidae). Oecologia, 88, 204- 210. Ridings, W. H., Mitchell, D. J., Schoulties, C. L., & E1-Gholl, N. E. (1978). Biological control of milkweed vine in Florida citrus groves with a pathotype of Phytophthora citrophthora. In "Proceedings of the IV International Symposium on Biological Control of Weeds, 1976, Gainesville, FL" (T. E. Freeman, Ed.), pp. 224-240. Schrrder, D. (1980). The biological control of thistles. Biocontrol News & Information, 5, 297-320. Schroeder, D., & Goeden, R. D. (1986). The search for arthropod natural enemies of introduced weeds for biological control--In theory and practice. Biocontrol News & Information, 7, 147-155. Simmonds, F. J. (1950). Insects attacking Cordia macrostachya (Jacq.) Roem. and Schult. in the West Indies. II. Schematiza cordiae Barber (Coleoptera: Galerucidae). Canadian Entomologist, 81,275-282. Simmonds, F. J. (1967). Biological control of pests of veterinary importance. Veterinary Bulletin, 37, 71-85. Simmonds, F. J., & Bennett, F. D. (1966). Biological control of Opuntia spp. by Cactoblastis cactorum in the Leeward Islands (West Indies). Entomophaga, 11, 183-189. Simmonds, H. W. (1937). The biological control of the weed, Clidemia hirta, commonly known in Fiji as "the curse." Agricultural Journal (Suva, Fiji), 8, 37-39. Smith, H. S. (1919). On some phases of insect control by the biological method. Journal of Economic Entomology, 12, 288-292. Smith, H. S. (1948). Biological control of insect pests. In "Biological Control of Citrus Insects. The Citrus Industry" (W. E. Reuther, E. C. Calaran, & G. E. Carman, Eds.), Vol. IV, pp. 276-320. Univ. of California, Division of Agricultural Science, Berkeley. Smith, J. M. (1951). Biological control of weeds in Canada. Canadian National Weed Commission, East Sector Proceedings, 5, 95-97. Sobhian, R., & Andres, L. A. (1978). The response of the skeletonweed gall midge, Cystiphora schmidti (Diptera: Cecidomyiidae), and gall mite, Aceria chondrillae (Eriophyidae) to North American strains of rush skeletonweed (Chondrilla juncea). Environmental Entomology, 7, 506-508. Stein, H. (1987). Is the dismal science really a science? Discover (Nov.), pp. 96- 99. Takahashi, F. (1977). Triops spp. (Notostraca: Triopsidae) for the biological agents of weeds in rice paddies in Japan. Entomophaga, 22, 351357.

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Templeton, G. E., TeBeest, D. O., & Smith, R. J., Jr. (1978). Development of an endemic fungal pathogen as a mycoherbicide for control of northern jointvetch in rice. In "Proceedings of the IV International Symposium on Biological Control of Weeds, 1976, Gainesville, FL" (T. E. Freeman, Ed.), pp. 214- 216. Thomas, P. A., & Room, P. M. (1986). Taxonomy and control of Salvinia molesta. Nature, 320, 581-584. Trujillo, E. E. (1985). Biological control of Hamakua Pa-Makani with Cercosporella sp. in Hawaii. In "Proceedings of the VI International Symposium on Biological Control of Weeds, 1984, Vancouver, BC" (E. S. Delfosse, Ed.), pp. 661-671. Turner, C. E. (1984). Conflicting interests and biological control of weeds. In "Proceedings of the VI International Symposium on Biological Control of Weeds, 1984, Vancouver, BC" (E. S. Delfosse, Ed.), pp. 203-225. Wang, R. (1986). Current status and perspectives of biological weed control in China. Chinese Journal of Biological Control, 1, 173-177. Wapshere, A. J. (1974a). A strategy for evaluating the safety of organisms for biological weed control. Annals of Applied Biology, 77, 201-211. Wapshere, A. J., Delfosse, E. S., & Cullen, J. M. (1974b). Host specificity

of phytophagous organisms and the evolutionary centers of plant genera and subgenera. Entomophaga, 19, 301-309. Wapshere, A. J., Delfosse, E. S., & Cullen, J. M. (1989). Recent developments in biological control of weeds. Crop Protection, 8, 227-250. Williams, J. R. (1960). The control of black sage (Cordia macrostachya) in Mauritius: The introduction, biology and bionomics of a species of Eurytoma (Hymenoptera, Chalcidoidea). Bulletin of Entomological Research, 51, 123-132. Zwrlfer, H. (1965). Preliminary list of phytophagous insects attacking wild Cynareae (Compositae) in Europe. Commonwealth Institute of Biological Control Technical Communication No. 1, pp. 81-154. Zwrlfer, H. (1973). Competitive coexistence of phytophagous insects in the flower heads of Carduus nutans. In "Proceedings of the II International Symposium on Biological Control of Weeds, 1971, Rome, Italy" (P. H. Dunn, Ed.), pp. 74-81. Zwrlfer, H. (1988). Evolutionary and ecological relationships of the insect fauna of thistles. Annual Review of Entomology, 33, 103-122. Zwrlfer, H., & Harris, P. (1971). Host specificity determination of insects for biological control of weeds. Anual Review of Entomology, 16, 159-178.

C

H

A

P

T

E

R

[351 Use of Plant Pathogens in Weed Control E. N. ROSSKOPF

R. CHARUDATTAN

j. B. KADIR

USDA-ARS 2199 South Rock Road Fort Pierce, Florida

Plant Pathology Department University of Florida Gainesville, Florida

Department of Plant Protection Faculty of Agriculture Universiti Putra Malaysia Selangor, Malaysia

INTRODUCTION

and the necessity for nonchemical alternatives in environmentally sensitive areas, have further opened avenues for the use of plant pathogens as biological control agents for weeds.

The significant advances made in agricultural technology during the past 40 years have made it possible for U.S. farmers to produce surplus food for millions of people worldwide, despite only 2% of the American population being engaged in agriculture (Peeples, 1994). Weeds represent one of the most costly and limiting factors in crop production. Weeds can cause substantial losses in the form of yield reductions through competition with crop plants for light, water, nutrients, heat energy, carbon dioxide, and space. Reductions may also be caused by the production of growth-inhibiting compounds, a phenomenon referred to as allelopathy. Weeds can also cause losses by reducing food, feed, and fiber quality as well as increasing the cost of land preparation or harvesting. Over the past four decades, chemical herbicides have dominated weed management strategies in developing countries (Abernathy & Bridges, 1994; Wyse, 1992). In the United States, chemical herbicides have accounted for nearly 60% of the total amount of all agricultural pesticides applied (Aspelin, 1994). Although herbicides have proven to be an extremely effective means of vegetation control, their use has come with a number of direct and indirect costs that may now be considered as outweighing the benefits in many cases. Public concern has increased over the contamination of water sources as well as agronomic problems caused by the overapplication and soil persistence of many herbicides. Herbicide resistance, which has been noted in more than 100 weed species, continues to be of increasing concern (Holt, 1992). These factors, coupled with the banning of many chemical pesticides, more stringent and costly registration and regulation,

Handbookof BiologicalControl

BIOLOGICAL CONTROL STRATEGIES Microbial biocontrol agents may be introduced and used in one of three ways, based on the types and numbers of applications required. Strategies are grouped into the classical approach, which consists of a single, inoculative introduction; the augmentative approach, which consists of periodic releases; and the inundative, or biopesticide, tactic. Epidemiological, density-dependent relationships between the biological control target and the biological control agent can be used to describe and distinguish these strategies (Charudattan, 1989). The classical approach is primarily directed toward plants that are exotic introductions which have become weed problems as a result of their growing in the absence of natural enemies. The classical approach may also be appropriate where cost of weed control expense is a limiting factor, such as in pasture or rangelands. Organisms used in the classical approach are assumed to require little or no additional manipulation. Many of the most important and difficult-to-control weeds have been intentionally or accidentally introduced into the area in which they are now a major problem. Approximately half of the weeds in the United States and 13 of the top 15 weeds are introduced species (Watson, 1991). Exotic weed species are able to thrive in the new area, due, in part, to the absence of natural enemies. The search for biocontrol agents to be used

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Copyright 9 1999 by Academic Press. All rights of reproduction in any form reserved.

892.

E.N. Rosskopf et aL

in the classical approach is usually performed in the original geographical range of the weed. Potential agents are then screened for virulence and those with potential are introduced into the new region with the expectation that the organisms' population will establish itself to provide weed suppression without complete eradication. In this manner it is expected that the pathogen and weed populations will equilibrate (Watson, 1991). These agents must have adequate host specificity that is limited to the target weed or to a small, related group of plants which contains no economically important members. The host range can be established by using a variety of protocols. Wapshere (1974) outlined a strategy that utilizes a centrifugal phylogenetic scheme. This begins with the testing of the organism, under optimal conditions for disease development, on a group of closely related plant species. The group should include not only important, closely related crop plants but also additional weed and native plant species. The testing of organisms under optimal conditions may artificially expand the host range of the organism, thus eliminating some potential biological control agents due to the risk assumed to be associated with their release (Adams, 1988).

SUCCESSFUL EXAMPLES USING THE CLASSICAL APPROACH There are several outstanding examples of successful control achieved with this approach. One of the most commonly cited successes involves the use of Puccinia chondrillina BubS_k & Syd. for the control of skeletonweed, Chondrilla juncea Linnaeus. This weed was a major problem in wheat-growing areas of Australia (Hasan, 1988). Strains of the rust, found in the Mediterranean, were tested for their specificity by inoculation of important Australian crop plants as well as members of the Asteraceae that are closely related to skeletonweed. Tests were performed under a variety of environmental conditions and none of the plants were found to be infected with the rust. Thus, the rust fungus was considered adequately specific to skeletonweed (Hasan, 1988). It was subsequently learned that the single strain of the rust released into Australia was only capable of controlling the predominant narrow-leaf phenotype of the weed; thus, multiple strains were required for successful control of the broad- and intermediate-leaf phenotypes (Hasan, 1985b). The first strain of this fungus was released in Australia in 1971. Within several months, the density of narrow-leaved skeletonweed started to decline substantially and there were inoculated areas in which the weed was no longer considered a problem (Hasan, 1988). The decrease in the narrow-leaved population allowed for the increase of the intermediate- and broad-leaved types which were resistant to the introduced rust strain. Addi-

tional strains were subsequently released. The search for strains of the rust that are virulent to the broad-leaved form continues. Puccinia chondrillina has also been released in the western United States, where it has proved to be the most effective of the biocontrol agents released against this weed (Supkoff et al., 1988). The second successful example is the control of European blackberries that had become weed problems in Australia and Chile. The rust fungus Phragmidium violaceum (Schultz) Winter was successfully established in Chile in 1973 and has controlled Rubus constrictus Lefevre et R. J. Mueller effectively and R. ulmifolius Schott. to a lesser extent (Hasan, 1988). This pathogen is effective by causing the plants to be more sensitive to frost damage and allowing for the invasion of secondary pathogens. This fungus was also recently released into Australia (Bruzzese & Field, 1985; Bruzzese & Hasan, 1986a, 1986b, 1986c). Ageratina riparia (Regel) K. & R., also known as hamakua pamakani or mistflower, is a considerable problem on several Hawaiian Islands. This weed has been successfully controlled using Entyloma ageratinae Barreto and Evans, which was introduced to Hawaii in 1975. Greater than 95% control of the weed was achieved within the first year of release (Trujillo, 1985). An isolate Puccinia carduorum Jacky collected in Turkey was released in the United States to control Carduus theormeri Weinman, a problematic weed in pastures and rangelands (Bruckart and Dowler, 1986). Although the host range of this fungus was initially determined to include several important species in Carduus and related genera, these were found to be resistant when inoculated in restricted field trials (Bruckart et al., 1985). The fungus was tested for pathogenicity to 16 accessions of C. thoermeri, 10 accessions of related weedy Carduus spp., 22 native and 2 weedy Cirsium species, and Cynara scolymus (artichoke). It was determined that species outside the genus Carduus are unsuitable hosts for this rust fungus. This group of unsuitable hosts includes 25% of the Cirsium species from North America tested, artichoke, and representatives from two other genera, Saussurea and Silybum. Considering the host-range data and the very susceptible nature of C. thoermeri, a judgment was made that species other than C. thoermeri would not be threatened by the introduction of P. carduorum into North America to control musk thistle. Musk thistle plots were inoculated successfully in the fall and spring of each year in 1987-1989. Artichoke and selected Cirsium spp. (nontarget plants) were planted between plots of inoculated musk thistle in two of three years. Only one rust pustule was found on an artichoke plant in 1989; all other plants remained rust-free despite severe disease on surrounding musk thistle plants. This indicated that P. carduorum poses no threat to these to these nontarget plants. The rust overwintered on musk thistle. Its spread

893

Chapter 35 Use of Plant Pathogens in Weed Control TABLE 1 Weed Targets and Exotic Pathogens Intentionally Released for Biological Weed Control Projects (Watson, 1991 ) Pathogen

Country of introduction

Subanguina picridis (Kirj.)

Canada and U.S. (continental)

Watson, 1986a, 1986b

U.S. (Hawaii)

Target weed

Asteraceae Acroptilon repens (L.) DC

References

Brezeski

(Russian knapweed) Ageratina riparia (Regel) K. & R.

(hamakua pamakani) Carduus nutans L.

Phaeoramularia sp.

South Africa

Barreto & Evans, 1988; Trujillo, 1985; Trujillo et al., 1988 Bruckart & Dowler, 1986; Bruckart et al., 1985; Politis & Bruckart, 1986; Politis et al., 1984 Adams, 1988; Adams & Line, 1984a, 1984b; Blanchette & Lee, 1981; Burdon et al., 1984; Cullen, 1978; Emge et al., 1981; Hasan, 1972, 1981, 1985b; Hasan & Wapshere, 1973; Supkoff et al. 1988 Morris, 1991

Uromycladium tepperianum

South Africa

Morris, 1991, 1997

Chile

Oehrens & Gonz~iles, 1975

Chile

Oehrens, 1977; Oehrens & Gonz~iles, 1974

Entyloma ageratinae Barr.

& Evans Puccinia carduorum Jacky

U.S. (continental)

Puccinia chondrillina Bu-

Australia and U.S. (continental)

(musk thistle, nodding thistle) Chondrilla juncea L.

(skeletonweed)

Eupato rium adenopho rum

Spreng. (crofton weed) Fabaceae (Leguminosae) Acacia saligna (Labill.) Wendl. (Acacia) Galega officinalis L.

(galega, goat's rue) Rosaceae Rubus spp. (blackberry)

back & Syd.

(Sacc.) McAlp. Uromyces galegae (Opic)

Sacc. Phragmidium violaceum

(Schultz) Winter

was limited during the rosette stage, and the disease became severe only during the bolting stage (i.e., stem elongation). Senescence of rust-infected musk thistles was accelerated and seed production was reduced by 2 0 - 5 7 % . Thus, the results confirmed that P. c a r d u o r u m can contribute to the control of musk thistle (Baudoin et al., 1993). Accordingly, permission was granted in 1987 for a limited field release of the rust in Virginia. A c a c i a saligna (Labill.) Wendl. poses a significant weed problem in South Africa. A gall-forming rust fungus, Urom y c l a d i u m t e p p e r i a n u m (Sacc.) McAlp. was found in Australia and introduced into South Africa in 1987. Since then, the fungus has spread to nearly all areas in which the weed occurs and has decreased the density of this invasive tree by at least 80%. The rust fungus is reported to be successfully spreading and suppressing the weed populations (Morris, 1997). Projects leading to intentional release of exotic phytopathogens for weed control are listed in Table 1. In addition to the foregoing examples, there are a substantial number of projects aimed at developing classical biological control agents (Table 2) and this approach is becoming increasingly important as more and more exotic weeds are becoming

invasive pests and an economical alternative is sought to the costly chemical controls.

C O M M E R C I A L I Z A T I O N A N D THE BIOHERBICIDE A P P R O A C H The concept of using inundative inoculation with a pathogen for weed control has gained momentum and attention in recent years. Research in the late 1960s through the 1980s culminated in the successful registration of two plant pathogens as bioherbicides and their subsequent use in commercial agriculture for nearly two decades (Charudattan, 1991). Between 1980 and 1997, five bioherbicides were registered in the United States, Canada, and Japan. DeVine | composed of the pathogen P h y t o p h t h o r a p a l m i v o r a [Butler] Butler to control M o r r e n i a odorata (Hook. & Am.) Lindl. in Florida citrus, has been extremely successful in controlling that weed. This fungus was the first commercially available mycoherbicide (Charudattan, 1991; Kenney, 1986). It is applied as a liquid containing chlamydospores and can provide as high as 96% weed control within

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E.N. Rosskopf e t al. TABLE 2

W e e d Targets and Exotic Pathogens Considered or under Investigation in Classical Biological W e e d Control Programs (Watson, 1991)

Target weed

Pathogen

Intended country of introduction

Asclepiadaceae Cryptostegia grandiflora R. Br. Morrenia odorata (H. & A.) Lindle. (stranglervine, milkweed vine)

Maravalia cryptostegiae (Cumm.) Ono Aecidium asclepiadinum Speg.

Australia U.S. (continental)

Tomley, 1989 Charudattan et al., 1978b

Araujia mosaic virus Puccinia araujae Lrv.

U.S. (continental) U.S. (continental)

Charudattan et al., 1980 Charudattan et al., 1978a

Puccinia jaceae Otth

Canada

Puccinia centaureae DC

Canada

Hasan et al., 1989; Watson & Alkhoury, 1981; Watson & C16ment, 1986; Watson et al., 1981 Watson & C16ment, 1986

Puccinia jaceae Otth

U.S. (continental)

Erysiphe cichoracearum DC ex Marat Leveillula taurica (Lrv.) Amaud f. sp. chondrillae Puccinia abrupta Diet. & Holw. var. partheniicola (Jackson) Parmelee Puccinia expansa Link. (= P. glomerata Grev.) Puccinia xanthii Schw.

Australia Australia

Asteraceae Centaurea diffusa Lam. (diffuse knapweed) Centaurea maculosa Lam. (spotted knapweed) Centaurea solstitialis L. (yellow starthistle) Chondrilla juncea L. (skeletonweed)

Parthenium hysterophorus L. (parthenium) Senecio jacobaea L. (tansy ragwort) Xanthium spp. (cocklebur)

Boraginaceae Heliotropium europaeum L. (common heliotrope) Euphorbiaceae Euphorbia esula L. complex (leafy spurge) Hydrocharitaceae Hydrilla verticillata (L.f.) Royle (hydrilla) Liliaceae Asphodelus fistulosus L. (onion weed) Polygonaceae Emex spp. Rumex crispus L. (curly dock)

Pontederiaceae Eichhornia crassipes (Mart.) Solms-Laub. (waterhyacinth) Rosaceae Rubus fruticosus L. (European blackberry)

References

Bruckart, 1989; Bruckart & Dowler, 1986 Hasan, 1980, 1983 Hasan, 1980, 1983

Australia

Evans, 1986; McClay, 1985; Parker, 1989 Alber et al., 1986

Australia

Hasan, 1980, 1983

Cercospora sp. Uromyces heliotropii Sredinski

Australia Australia

Hasan, 1985a Hansan, 1985a

Melampsora euphorbiae (Schub.) Cast. Uromyces scutellatus (Pers.) Lrv.

U.S. (continental)

Bruckart et al., 1986

U.S. (continental)

Drfago et al., 1985

Fusarium roseum "Culmorum" (Link ex Fr.) Snyder & Hans.

U.S. (continental)

Charudattan et al., 1981; SmitherKopperl et al., 1998

Puccinia barbeyi (Roum.) P. Magn.

Australia

Anonymous, 1988

Cercospora tripolitana Sacc. et Trott. Peronospora rumicis Cda. Uromyces rumicis (Schum.) Winter

Australia Australia U.S. (continental)

Anonymous, 1988 Anonymous, 1988 Inman, 1971; Schubiger et al., 1985

Uredo eichhorniae Gonz-Frag. & Cif.

U.S. (continental)

Charudattan & Conway, 1975; Charudattan et al., 1978b

Phragmidium violaceum (Schultz) Winter

Australia

Bruzzese & Field, 1985; Bruzzese & Hasan, 1986a, 1986b, 1986c, 1987

10 weeks (Ridings, 1986). DeVine | is available by special order through Abbott Laboratories (Abbott Park, IL). Collego | composed of the fungus Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. f. sp. aeschynomene, is registered for the control of northern jointvetch (Aeschynomene virginica [L.] B. S. P.) in rice and soybeans

Australia

(TeBeest & Templeton, 1985). Collego | was developed by scientists at the University of Arkansas, the U.S. Department of Agriculture-Agricultural Research Service, and the Upjohn Company (Bowers, 1986). This fungus is formulated as a wettable powder and results generally in greater than 85% control (Smith, 1986). Collego | is now

Chapter 35

Use of Plant Pathogens in Weed Control

available from Encore Technologies (Minnetonka, MN). The host range of this fungus is more broad than was originally determined and risks posed to nontarget crop plants have been addressed through label restrictions (TeBeest & Templeton, 1985). Colletotrichum gloeosporioides f. sp. malvae was developed for control of round-leaved mallow (Malva pusilla Sm.) and was registered in Canada in 1992 for use in field crops (Makowski & Mortensen, 1992; Mortensen & Makowski, 1997). This product is not currently available, as the industrial partner, PhilomBios (Saskatoon, SK, Canada), has been unable to establish a viable market for this product (Boyetchko, 1998). Puccinia canaliculata (Schw.) Lagerh., a rust fungus, has been registered as the bioherbicide Dr. BioSedge | for the control of yellow nutsedge (Cyperus esculentus L.) (Greaves & MacQueen, 1992; S. C. Phatak, personal communication). Work on this system began in 1979 (Phatak et. al., 1981, 1983) and the bioherbicide was registered in 1994. This rust pathogen is reported to spread rapidly and can cause as high as 90% reduction in fresh weight of the weed when applied at the rate of 5 mg of uredospores per hectare. However, the strain of the rust fungus from the state of Georgia registered as Dr. BioSedge | does not infect purple nutsedge (Scheepens & Hoogerbrugge, 1991) or several yellow nutsedge biotypes that are naturally resistant to specialized strains of the fungus (Bruckhart et al., 1988). When applied in early spring, P. canaliculata inhibits flowering and reduces yellow nutsedge stand by as much as 46%. It is also reported to inhibit new tuber formation by as much as 66% (Phatak et al., 1983). The obligately parasitic nature of this fungus makes production of inoculum a problem and therefore Dr. BioSedge | is currently unavailable for commercial use. Another isolate of Colletotrichum gloeosporioides has been developed for use in China for the control of Cuscuta L. spp. (dodder). It is currently being marketed under the name Luboa No. 1 and provides control of 80% or more of the weed (Mortensen, 1998). Two different products based on the fungus Chondrostereum purpureum (Pers. ex Fr.) Pouzar, a wound-invading pathogen of broad-leaved trees, are currently in use or under development as bioherbicides. Biochon~ is used (not registered) for the control of Prunus serotina Ehrh. in Dutch forests and ECO-clear ~ is under development for North American registration and use as a stump application in Canadian forests (Dumas et al., 1997; Prasad, 1994; Shamoun & Hintz, 1998). Another tree pathogen, Cylindrobasidium laeve (Pers: Fr.) Chamuris, has been registered in South Africa and is commercially available for use for stump treatment to prevent regrowth of wattles, Acacia mearnsii de Wildman and A. pycnantha Benth., in the Cape Province (Morris et al., 1998). Methods for mass production of inoculum, based on

895

a laboratory-scale pilot plant, have been developed. Basidiospores of the pathogen are produced on solid substrate and a concentrated spore suspension in oil is packed in plastic sachets for marketing and use (Morris et al., 1998). This bioherbicide, named Stumpout | is now available for commercial use in wattle-clearing programs. The bacterial pathogen Xanthomonas campestris Migula pv. poae has recently been registered as a bioherbicide. Japan Tobacco, Inc., has registered this bacterial agent under the name Camperico | to control annual bluegrass (Poa annua L.) in bermudagrass (Cynodon dactylon [L.] Pers.), zoysia grass (Zoysia matrella MelT.), and Kentucky bluegrass (Poa pratensis L.) tufts and golf greens (Imaizumi et al., 1997). It is necessary to mow the turf prior to application to provide a means of host entry for the pathogen (Johnson, 1994). A second bacterium, Pseudomonas syringae van Hall pv. tagetis, has potential as a bioherbicide for the control of Canada thistle in soybean (Johnson et al., 1995). This pathogen causes apical chlorosis and is currently being tested for control of several members of the Asteraceae (Johnson et al., 1996). Encore Technologies has licensed P. syringae pv. tagetis from the University of Minnesota and is pursuing its commercial development (D. R. Johnson, Encore Technologies, personal communication). Among other agents under development for possible commercialization is Alternaria cassiae Jurair & Khan, which was researched extensively for possible use as a bioherbicide for Acacia Meamsii sicklepod [Senna obtusifolia (L.) H. S. Irwin & Bar.], coffee senna (Cassia occidentalis L.), and showy crotalaria (Crotalaria spectabilis Roth) (Walker & Boyette, 1985). It was initially developed under the trade name CASST by Mycogen Corp. (San Diego, CA) (Bannon, 1988). In regional field trials, conducted under the auspices of the USDA-CSREES Cooperative Regional Research Project S-136, this fungus provided control that was comparable to that of chemical herbicides (Charudattan et al., 1986). Mycogen has since relinquished the license to develop this fungus (Boyetchko, 1999). It is currently under investigation for use in Brazil (R. Charudattan, personal communication), possibly as a preemergent, soil-incorporated bioherbicide (Pitelli et al., 1998). Cercospora rodmanii Conway, a host-specific pathogen of waterhyacinth [Eichhornia crassipes (Mart.) Solms], was field tested between 1974 and 1984. The University of Florida patented the use of this pathogen and Abbott Laboratories was licensed to develop it as a bioherbicide. The pathogen was formulated as a wettable powder and was capable of reducing waterhyacinth growth by as much as 90% when used in combination with insect biological control agents (Charudattan et al., 1985). However, when used alone, the efficacy of this pathogen was inadequate when compared to the available chemical herbicides. This in-

896

E.N. Rosskopf et ai.

adequate efficacy, coupled with economic considerations, halted attempts at commercialization (Charudattan, 1990). Two fungi have recently been patented by the University of Florida for use as biological control agents of weeds. Phomopsis amaranthicola sp. nov. [U.S. Patents 5,393,728 and 5,510,316 (Charudattan et al., 1996b)] is a pathogen of pigweeds (Amaranthus spp.) that is effective against a number of species in the genus. This fungus has been tested in greenhouse and field trials and found to be highly promising (Rosskopf, 1997; Rosskopf et al., 1996). Symptoms produced by this fungus begin as leaf lesions, which coalesce (Fig. l a), causing premature leaf abscission. Lesions then develop on the stem (Fig. l b), which girdle the stem and cause the plant to topple. The second fungus, Dactylaria higginsii (Luttrell) M. B. Ellis [U.S. Patent 5,698,491 (Kadir & Charudattan, 1996)], is effective in controlling several Cyperus spp., including two of the worst agricultural weeds, yellow nutsedge and purple nutsedge (Cyperus esculentus L. and C. rotundus L.). The fungus not only kills

the above-ground shoots but also limits tuber production and the ability of the weed to compete with crops, such as tomato and pepper (Kadir, 1997). The pathogen produces a leaf blight (Fig. 2a), which has been successful in field trials (Fig. 2b.) Colletotrichum truncatum (Schwein) Andrus & W. D. Moore is under development for control of hemp sesbania (Sesbania exaltata (Raf.) Rydb. ex A. W. Hill) in cotton, rice, and soybean (Boyette, 1994; Boyette et al., 1993b; Egley et al., 1993; Jackson et al., 1996; Jackson & Slininger, 1993; Schisler et al., 1991, 1995; Schisler & Jackson, 1993). In small-scale plots hemp sesbania was effectively controlled in soybean and rice with a 1:3 (v:v) unrefined corn oil/Colletotrichum truncatum formulation containing 0.2% Silwet L-77. A dried formulation consisting of dextrose and hydrated silica gel suspended in experimental oil formulations was also effective in controlling hemp sesbania. Pesta formulations (explained later) containing conidia and microsclerotia provided some control when applied preemergence or when preplant incorporated but were

FIGURE 1 Leafspots (a) and stem lesions (b) caused on Amaranthus hybridus by Phomopsis amaranthicola, a biological control agent for pigweeds and amaranths.

Chapter 35

Use of Plant Pathogens in Weed Control

FIGURE 2 (a) Leaf blight on Cyperus esculentus (purple nutsedge) resulting from application of the potential biological control agent Dactylaria higginsii. (b) Control of purple nutsedge in miniplot field trials with application of Dactylaria higginsii. Two applications of the fungus resuited in complete control of the weed.

significantly less effective than postemergence application of fungus-oil formulations. Control of hemp sesbania in cotton was significantly reduced by fungicide seed treatments and in-furrow fungicide and insecticide treatments. Rice formulations of the fungus were tested for viability and virulence to hemp sesbania. The fungus was highly virulent to weed seedlings even after 8 years of storage at -20~ and only slightly less virulent at 4~ Survival of C. truncatum conidia in formulations stored at room temperature was significantly less than at the lower temperatures (C.D. Boyette, personal communication). An Alternaria sp. is undergoing evaluation as a bioherbicide for dodder (Cuscuta spp.) in cranberries. Results from field trials and greenhouse studies are promising. Plots that had been treated the previous year with Pesta formulation of the pathogen experienced no infestation of dodder the following year, suggesting a possible residual effect of the pathogen (Bewick et al., 1986; T. A. Bewick, Cranberry

897

Research Station, University of Massachusetts, personal communication). Exserohilum monoceras is undergoing evaluations for development as a bioherbicide to control barnyard grass (Echinochloa crus-galli (L.) Beauv. var. crus-galli) and other Echinochloa species (Echinochloa crus-galli var. formosensis, E. colona (L.) Link, and E. oryzicola (Ard.) Fritsch) in Japan (Tsukamoto et al., 1997). The same pathogen is being developed cooperatively by scientists from Australia, Canada, the Philippines, and Vietnam (Zhang et al., 1996; Tuat et al., 1998). The foliar fungal pathogen Ascochyta caulina appears to have good prospects of being developed as a bioherbicide to control common lambsquarters (Chenopodium album L.). The ability of this fungus to control common lambsquarters in corn and sugar beet was studied in Europe. Both preemergence soil incorporation and postemergence spray application of the fungus were studied. Application of A. caulina spores to soils resulted in diseased, stunted, and dead seedlings of the weed. Disease incidence and weed mortality were influenced by spore density, soil water content, and soil type but not by sowing depth. Spore densities of 109-101~ m -2 were required for 50% mortality of emerged common lambsquarters plants (Kempenaar, 1995; Kempenaar et al., 1996b). The postemergence application of the fungus caused necrosis and mortality of the weed seedlings. Up to 65% mortality of treated seedlings was obtained and sublethally diseased plants were reduced in growth. Maximum dry matter, number of fruits per plant, and seed weight of the weed were reduced as a result of fungal infection. Competitiveness of the weed was also reduced. Yield reduction was prevented by application of A. caulina in corn but not in sugar beet (Kempenaar et al., 1996a). Attempts are underway to integrate the use of A. caulina in weed management systems by making use of pre- and postemergent applications of the fungus to reduce the number of emerging seedlings of common lambsquarters, the number of surviving plants, and the number of seeds produced (Scheepens et al., 1998). A list of bioherbicides, including the presently registered agents, those that are said to be used as unregistered, localuse agents, and experimental candidates, is provided in Table 3.

DELETERIOUS RHIZOBACTERIA AND WEED CONTROL This group of microorganisms has been characterized as nonparasitic bacteria that colonize plant roots and cause decreases in plant growth. Many of these bacteria are specific in their growth-suppressive activity. The initial discovery of these bacteria was on crop plants. A weed association was first discovered on downy brome (Bromus tectorum L.)

898

E.N. Rosskopf et al. TABLE 3 Weed

List of Registered a n d U n r e g i s t e r e d Bioherbicides or A g e n t s u n d e r D e v e l o p m e n t Pathogen (registered or trade mark name)

Target crop(s)

Soybean Tree plantations Rice and soybean

Canada South Africa U.S., Arkansas

4* 5 5

Amaranthus spp. Chenopodium album Cuscuta spp. Cyperus spp. Cyperus esculentus Cyperus rotundus Cytisus scoparius

Colletotrichum coccodes Cylindrobasidium laeve (Stumpout | Colletotrichum gloeosporioides f. sp. aeschynomene (Collego| Phomopsis amaranthicola Ascochyta caulina Alternaria sp. Dactylaria higginsii Puccinia canaliculata (Dr. B ioSedge | Cercospora caricus Fusarium tumidum

Vegetables Various Cranberries Various Various Various Tree plantations

Echinochloa spp.

Exserohilum monoceras

Rice

Eichhornia crassipes

Cercospora rodmanii

Aquatic habitats

Euphorbia heterophylla Grass weeds

Helminthosporium sp. Drechslera spp. and Exserohilium spp.

Hakea sericea lmperata cylindrica Malva pusilla

Colletotrichum gloeosporioides Colletotrichum caudatum Colletotrichum gloeosporioides f. sp. malvae (BioMal | Cercospora mikaniicola Phytophthora palmivora (De Vine | Xanthomonas campestris pv. poae (Comperico | Ascochyta pteridis Sporisorium ophiuri Colletotrichum sp. nov. nr. graminicola Rhynchosporium alismatis Puccinia lagenophorae Alternaria cassiae Colletotrichum truncatum Pseudomonas solanacearum Colletrotrichum spp. Alternaria sp. Colletotrichum gloeosporioides Fusarium nygamai Fusarium oxysporum Fusarium semitectum var. majus Sclerotinia sclerotiorum Fusarium tumidum Myrothecium verrucaria Chondrostereum purpureum (Biochon ~ ) (ECO-clear~ ) Pseudomonas syringae pv. tagetis Colletotrichum orbiculare

Various Cereals Citrus Tree plantations Various Various

U.S., Florida Holland U.S., Florida U.S., Florida U.S., Georgia Brazil; Israel New Zealand Canada Australia; Japan Philippines-Canada c U.S., Florida; South Africa; Egypt; India; SE Asia Brazil Vietnam-Australia U.S., Florida South Africa Malaysia Canada

3 4 4 3 5* 3 3 3 3 3 4* 3 3 3 2 3 4 1 5"

Malaysia U.S., Florida Japan Scotland, U.K. Thailand-U.K. Thailand-U.K. Australia U.K.-Switzerland Brazil U.S., Mississippi U.S., Florida Brazil-U.S., Florida Philippines Malaysia Sudan-Germany West Africa-Canada Sudan-Germany Canada New Zealand U.S., Maryland Holland Canada U.S.; Canada Australia

2 5 4 3 3 3 2 4 3 4 3 2 2 2 3 3 3 4 3 3 5 4 4 4*

Abutilon theophrasti Acacia mearnsii Aeschynomene virginica

Mikania micrantha Morrenia odorata Poa annua Pteridium aquilinum Rottboellia chochinchinensis Sagittaria spp. Senecio vulgaris Senna obtusifolia Sesbania exaltata Solanum viarum Sphenoclea zeylanica Striga hermonthica

Taraxacum officinale Ulex europaeus Various annual weeds Various broad-leaved trees Various composite weeds Xanthium spp.

Plantation crops Citrus Turf grass Pastures Cereals Cereals Rice Various Soybean Soybean and rice Citrus and sod Rice Rice Various Cereals Sorghum Lawn and garden Plantation crops Various Tree plantations Various Various

Country a

Status b

Note: Compiled from unpublished and published reports. a,,_,,, cooperative work is in progress between the indicated countries; ";", the indicated countries are engaged in independent work. bStatus: 1, in exploratory phase; 2, laboratory and/or greenhouse testing underway; 3, field trials in progress; 4, under early commercial or practical development; 4", commercial development tried but registration uncertain; 5, available for commercial or practical use; 5", available registered as a microbial herbicide but currently unavailable for use due to economic reasons. CCountries joined by a hyphen are engaged in a cooperative project to develop the bioherbicide agent.

Chapter 35 TABLE 4

899

Use of Plant Pathogens in Weed Control

Biological W e e d Control Projects Based on Rhizobacteria (Kremer & Kennedy, 1994)

Investigator/location

Weeds a

Ecosystem b

Rhizobacteria

Status c

References

A. Caesar USDA-ARS Bozeman, MT

EPHES CENRE

Rangelands

Agrobacterium Pseudomonas Xanthomonas

A, B, C

Caesar, 1994 Caesar et al., 1992 Pers. comm.d

J. Clapperton & R. Blackshaw Agriculture Canada Lethbridge, AB

SETVI AVEFA

Cereal c r o p s Rangelands

Pseudomonas

A, B,

Pers. comm.

C. Dorworth, D. Macy, & R. Winder Canadian Forest Service Victoria, BC

CLMCD

Forest nursery

Pseudomonas

A

Pers. comm.

M. Dumas Canadian Forest Service Sault Ste. Marie, ON

Rubus spp.

Forest

Unidentified

A

Pers. comm.

L. Elliott USDA-ARS Corvallis, OR J. Frey Mankato State University Mankato, MN

POANN

Seed c r o p s Turf grass

Pseudomonas

A, B, C

Elliott et al., 1994

XANST

Row c r o p s

Pseudomonas

A, B,

Pers. comm.

P. Harris & P. Stahlman Kansas State University Hays, KS

BROTE, BROJA BROSE, AEGCY

Cereal c r o p s

Enterobacter Pseudomonas Xanthomonas

A, B, C, D

Harris & Stahlman, 1991, 1992, 1993a, 1993b

A. Kennedy USDA-ARS Pullman, WA

BROTE, BROJA AEGCY, SSYAL AMARE

Cereal c r o p s

Pseudomonas fluorescens

A, B, C, D

Johnson et al., 1993 Kennedy et al., 1991 Kennedy et al., 1989

R. Kremer USDA-ARS Columbia, MO

ABUTH, AMARE

Row c r o p s

Pseudomonas Enterobacter Erwinia herbicola Flavobacterium

A, B, C

lpomoea spp. Setaria spp.

Kremer, 1993 Kremer et al., 1990 Souissi & Kremer, 1994

EPHES

Rangelands

K. Mortensen & S. Boyetchko Agriculture Canada Saskatoon, SK

BROTE SETVI

Cereal c r o p s Pastures

Pseudomonas

A, B

Boyetchko & Mortensen, 1993

H. D. Skipper Clemson University Clemson, SC

BROTE

Cereal c r o p s

Pseudomonas

A

Skipper et al., 1996 Pers. comm.

a ABUTH, Abutilon theophrasti Medicus, velvetleaf; AEGCY, Aegilops cylindrica Host., joined gaotgrass; AMARE, Amaranthus retroflexus L., redroot pigweed; AVEFA, Avena fatua L., wild oat; BROJA, Bromus japonicus Thunb. ex Murr., Japanese brome; BROSE, Bromus secalinus L., cheat; BROTE, Bromus tectorium L., downy brome; CENRE, Acroptilon repens L., Russian knapweed; CLMCD, Calamagrostis canadensis var. canadensis Michaux, Canada reedgrass; EPHES, Euphorbia esula L., leafy spurge; POANN, Poa annua L., annual bluegrass; SETVI, Setaria viridis (L.) Beauv., green foxtail; SSYAL, Sisymbrium altissimum L., tumble mustard; XANST, Xanthium strumarium L., common cocklebur. bSituation in which target weed occurs. CStatus: A, laboratory screening; B, greenhouse/growth chamber screening; C, small-scale field testing; D, large-scale field testing. dpersonal communication by authors with original investigators, 1993-1994.

in winter wheat (Cherrington & Elliott, 1987). These bacteria are used similarly to the fungal bioherbicides in that they are applied inundatively, although the application is made to the soil prior to weed emergence. This method does not result in eradication of the target weed species but significantly depresses its competitive ability ( K r e m e r & Kennedy, 1996). Table 4 provides a partial listing of programs using rhizobacteria. A c c o m p l i s h m e n t s in this area, as listed by K r e m e r and K e n n e d y (1996) include control of d o w n y

b r o m e using P s e u d o m o n a s spp. This system has been successful under field conditions when bacteria were applied to the soil. Grain yields of the winter wheat in plots treated with the bacteria were significantly higher than in plots where the d o w n y b r o m e was not suppressed. Isolates Pp001 and Pf239 of another species of P s e u d o m o n a s were tested for their effects on velvetleaf seedling e m e r g e n c e and found to reduce seedling e m e r g e n c e to less than 55% in treated soil. In both of these examples, the bacterial isolates also reduced the numbers of seeds produced, thus potentially

900

E.N. Rosskopfet ai.

FIGURE 3 Bioassayof deleterious rhizobacteria effects on (a) downy brome (Bromus tectorum L.) and (b) green foxtail [Setaria viridis (L.) Beauv.] seed germination. Photographsprovidedby S. Boyetchko.

contributing to long-term weed control (Kremer & Kennedy, 1996). The use of these agents is also being pursued in Canada, where more than 2000 isolates of rhizobacteria obtained from prairie soils are under investigation (Boyetchko, 1999). Some isolates, tested in a variety of bioassays (Figs. 3a and 3b), have proven to be extremely successful in minimizing weed seed germination. Host-range tests of many of these isolates have shown little or no detrimental effects on nontarget hosts, including spring and winter cereal crops. In some cases, the bacteria had growth-promoting effects on the tested crops (Boyetchko, 1999).

DEVELOPMENTAL TESTING OF MYCOHERBICIDES The most commonly cited explanation for the failure of fungal plant pathogens used for biological control agents of weeds to cause severe disease is the requirement of an

extended dew period for adequate infection. Some pathogens, such as Sphacelotheca holci Jack (= S. cruenta [Kuhn.] Potter), long considered a potential biological control agent for johnsongrass (Sorghum halepense [L.] Pers.), do not have this as a major constraint. Researchers working with this pathogen have reported that, although initial greenhouse studies indicated a need for free moisture for infection, a 55% infection of plants occurred regardless of the availability of free moisture. Although this is a relatively low infection rate, the authors found it to be adequate to reduce the competitive ability of the weed (Massion & Lindow, 1986). Daniel and coworkers (1973), studying the use of a strain of Colletotrichum gloeosporioides (the Collego | pathogen) to control northern jointvetch (Aeschynomene virginica), found that infection was not limited by the absence of a dew period but that fastest onset of disease was achieved if the inoculated plants were exposed to 80% relative humidity overnight. This fungus was reported to be capable of causing infection at greenhouse temperatures ranging from 23 to 32~ The same organism was capable of infecting plants ranging from 5.0 to 30.5 cm tall, although the greatest percentage of mortality was achieved with the smallest-size class of plants. A species of Phomopsis (Sacc.) Bub~ik, P. convolvulus Ormeno, was evaluated for its potential for the control of field bindweed (Convolvulus arvensis L.) (Morin et al., 1990a; Ormeno-Nunez et al., 1988; Sparace et al., 1991; Vogelsang et al., 1994). This fungus caused the highest levels of plant mortality (55%) when the inoculated plants were exposed to a minimum of 18 h of dew and an inoculum concentration of 109 conidia/m 2. This treatment resulted in 55% plant mortality (Morin et al., 1990b). Isolates of Bipolaris setariae (Saw.) Shoemaker examined for the control of goosegrass (Eleusine indica [L.] Gartner) required a 48-h dew period for 100% infectivity. The optimal temperature for disease development in this system was 24~ The isolate was able to control goosegrass plants of the 2- and 4-week growth stages (Figliola et al., 1988). Similar results were obtained in studies involving the development of anthracnose of spiny cockleburr (Xanthium spinosum L.), caused by Colletotrichum orbiculare (Berk. et Mont.) v. Arx (Auld et al., 1988, 1996). The optimal temperatures for disease development by this organism were between 20 and 25~ with a dew period of 48 h. As with several other potential biological control organisms, if this dew period was split into 12-h exposures with 12 h separating dew exposure, the disease severity was decreased. A significant level of mortality of cockleburr was not achieved with any of the treatments, with disease ratings approaching five, which did not constitute plant death (McRae & Auld, 1988). Colletotrichum truncatum (Schw.) Andrus and Moore,

Chapter 35

Use of Plant Pathogens in Weed Control

used for the control of Florida beggarweed (Desmodium tortuosum [Sw.] DC), had optimal disease development with 14-16 h of dew at temperatures between 24 and 29~ Conidial suspensions with concentration of 10510 7 conidia/ml were most effective in controlling plants in the cotyledon stage of growth. The efficacy of the pathogen diminished as the plants matured (Cardina et al., 1988). The percentage of control obtained at 18~ was significantly lower. Microsphaeropsis amaranthi (Ell. and Barth.) Heiny and Mintz (= Aposphaeria amaranthi Ell. and Barth.), a pathogen of tumble pigweed (Amaranthus albus L.), was found to cause the most significant levels of pigweed mortality in a series of growth-chamber experiments when applied to plants of the four-leaf stage and exposed to a minimum of 8 h of dew. There were no significant differences in the mortality of inoculated plants exposed to 8, 12, and 24 h of dew. This dew period requirement is substantially lower than those for many of the potential biological control agents that have been evaluated. There were also no significant differences in mortality when conidial suspensions ranging from 10 4 to 107 were used for inoculation. In this case, there was no detrimental effect produced by delaying the onset of dew and therefore the disease resulted in 100% plant mortality (Mintz et al., 1992). Thus, it is clear that an understanding of the epidemiological parameters is essential for determining the real p o tential of biological control agents for weeds. Although many organisms that are effective at initial, small-scale testing do not prove to be efficacious in larger fields, determination of the basic environmental conditions necessary for disease development will assure some measure of success in field use.

FIELD ASSESSMENT Field evaluation is one of the most important components of a complete evaluation of the efficacies of pathogens as biological control agents for weeds. Although an organism may perform effectively in greenhouse or growthchamber experiments, the use of the fungus in the field is often characterized by variable activity against the target weed. Puccinia carduorum was evaluated in the field for the control of musk thistle (Carduus theormeri). Although this pathogen had performed effectively in the greenhouse, providing significant reductions in plant-matter accumulation after both single and multiple applications of the pathogen, field performance was limited to accelerated senescence and reductions in seed production (Baudoin et al., 1993). Colletotrichum orbiculare was tested in small-scale plots for the control of Xanthium spinosum, with promising resuits. It was further tested at four sites with variable envi-

90 |

ronmental conditions. At two sites with artificial dew periods of 18 h, the pathogen produced 100% plant mortality. In sites that were not treated with an artificial dew period, a maximum plant mortality of 50% was reached (Auld et al., 1990). The pathogen applied in oil emulsions proved to be more effective in the field (Klein et al., 1995a, 1995b, 1995c). This pathogen has also been tested in combination with the rust fungus Puccinia xanthi (Morin et al., 1993a, 1993b), with synergistic effects resulting. Field trials testing the effect of Colletotrichum truncatum (Schw.) Andrus and Moore on the growth of hemp sesbania (Sesbania exaltata [Rydb.] ex Hill) included the application of the pathogen to plots at two rates in either an aqueous suspension or an invert emulsion. The maximum level of weed mortality in plots treated with the aqueous suspension was 42%, whereas in invert emulsion suspensions of the pathogen there was 97% mortality in the plots treated with the higher application rate. This was comparable to the control with the herbicide acifluorfen. The effect of the invert emulsion applied without the fungus was statistically similar to the effect of the pathogen in the aqueous suspension (Boyette et al., 1993b). Alternaria crassa (Sacc.) Rands was evaluated for the control of jimsonweed (Datura stramonium L.). It was effective in one field-trial location using a mycelial preparation, whereas at the second site plant mortality reached a maximum of only 29% (Boyette et al., 1986). This system demonstrates a common phenomenon that of the reduced efficacy of many pathogens in the field, as well as the variability associated with site differences. The control of Amaranthus albus L. by the agent Microsphaeropsis amaranthi is an example of a successful transition from greenhouse to field use. This pathogen, which was extremely efficacious on the target weed in controlled growth-chamber studies, also performed well in the field, with 9 6 - 9 9 % mortality after applications of 1 x 106 and 6 • 106 conidia/ml (Mintz et al., 1992).

FORMULATION OF BIOLOGICAL CONTROL AGENTS The use of formulations for biological control agents is a relatively new application of technology that is well known to the chemical herbicide industry. Formulations or formulating agents are considered to be the crucial difference between the product being able to reach the general public and remaining in the laboratory. Most chemical herbicides could not be distributed without being combined with some other material. Thus, the active constituent is combined with a solvent, cattier, or surfactant in order to make its delivery and dispersal convenient, which is the broad definition of formulation (Anderson, 1983). Although this allows the user to spread a very small amount of active

902

E.N. Rosskopf et aL

ingredient over a wide area, this may not be the only advantage to a formulated chemical. Chemical herbicides may gain their activity or have enhanced phytotoxicity due to the agent with which they are mixed. The formulation may also allow the agent to have a prolonged shelf life or to be transported easily and without altering the effectiveness of the product. In some cases, the cartier may serve as the formulation. This is usually the case with dry pellet or powder formulations. In addition to the basic formulation, materials that act as surfactants may be added to the formulated product to further enhance the activity or usability of the product. The same basic principles underlie the use of formulations for the application of biological control agents. Formulations are used most frequently to enhance the activity of the organism (Boyette & Abbas, 1994; Green et al., 1998). The need for high levels of inoculum in the field and the normal requirement of an extended dew period for efficacy of fungal pathogens are two aspects of the development of a biological control agent that may be alleviated by the addition of a formulating agent. The formulation of biologicals is complicated by the need for the organism to remain alive and virulent through the processing. The convenience of application, which is so important for chemical formulation, is almost a secondary consideration when a biological control organism is the active ingredient. The more important focus in the formulation of biological control agent is improving the longevity and efficacy. In addition, the formulation of a biological may address the need for using combinations of biologicals and chemical pesticides. The most commonly used addition to a suspension containing a biological control agent, which for convenience and likelihood is assumed to be a conidial suspension in water, is that of surfactants. Since water is the most common carrier of biological control agents during the preliminary stages of development, the addition of a water-compatible agent is the most convenient next step. Surfactants may be of various forms that result in a variety of effects, but focus is on modifying the surface properties of a liquid (Anderson, 1983). This may facilitate the spreading, emulsifying, or sticking properties of an agent in a water solution. Surfactants may themselves have phytotoxic effects or may predispose the plant to infection as well as providing increased coverage. In some cases, products such as Tween 80 | or Tween 20 | may have detrimental effects on the biological control agent (Prasad, 1993). These are important characteristics to evaluate during the experimental phase of surfactant use, as they may enhance or inhibit the effect of the biocontrol agent. Surfactants can be classified into groups based on their ionization in water and this may give some clue as to how a new or untried surfactant will behave in a biological control setting. The commonly used surfactants, Tween

20 | Tween 80 | Triton X-100 | and Tergitol | are all nonionic surfactants. These have been the most commonly used surfactants for initial experimentation. Silwet L-77 | is an example of a new generation of surfactants which are organosilicones. These surfactants reduce the surface tension far more than other types of surfactants and may prove to be an important advancement for biological control agent applications, as they may allow for penetration of the cuticular area (Stevens, 1994; Zidack & Backman, 1996). One drawback with this type of nonionic surfactant is that in helping to breach the cuticle, it may cause the plant to produce resistance-inducing compounds or promote entry of microorganisms capable of inducing cross-protection, both of which can retard the growth of the pathogen (Zidack et al., 1992; Womack & Burge, 1993). Other surfactants that act as emulsifying agents, which are used with more complex formulations such as those that involve oilbased spore suspensions, are now more commonly used. In addition to the use of surfactants in water-carried systems, a number of other formulations are being explored. Material capable of forming aqueous gels when added to spore suspensions serves to stick the spores to the leaf surface, while providing a hydrophilic matrix in which the spores may germinate more readily in the absence of an adequate dew period (Shabana et al., 1997). This type of formulation appears to have lost much of its attraction, as the solution is viscous and difficult to apply as well as being relatively costly. Other simple adjuvants could include the addition of a water-soluble nutrient base that can be mixed with the water suspension prior to application. This is the case with Collego | (Encore Technologies), which consists of a dried spore preparation that is resuspended in water and a prepackaged amount of sugar as an osmoticum and nutrient source to allow for the gradual rehydration and germination of spores of Colletotrichum gloeosporioides f. sp. aeschynomene. Use of sugar also has been reported for control of spurred anoda (Anoda cristata [L.] Schlect.) with Alternaria macrospora Zimm. Control of Desmodium tortuosum (Florida beggarweed) was enhanced when sucrose was added to the Colletotrichum truncatum (Pers.) Grove spore suspension prior to application. Surfactants may increase the even distribution of fungal spores within an aqueous solution by overcoming their hydrophobic nature (Bannon et al., 1990). These are essentially cases where adjuvants or surfactants have been used to increase the efficacy of a pathogen, attributable to either the increase in germination or the more efficient application and adhesion of the biological control agent on the host plant. Within the past 5 or 10 years, there has been substantial progress in developing effective formulations for biological control agents (Boyette et al., 1996; Connick et al., 1991; Daigle & Connick, 1990; Daigle & Cotty, 1992; Saad et al., 1993; Smith, 1991). The first attempts were compli-

Chapter 35 Use of Plant Pathogens in Weed Control cated by the inability of many fungal propagules to endure a great deal of processing, but to increase the long-term viability and to facilitate long-distance transport, this aspect of the development of a biological control agent has had to be addressed. Two general approaches have been taken that are directly related to the way in which the biological control agent is envisioned to act, either in the biological control of weeds or in the biological control of diseases. If the target site is the foliage portion of the plant, formulation tactics have been directed at a fluid formulation or a formulation that is readily suspended in an aqueous solution. For organisms that act at the soil level or are incorporated into the soil, solid formulations have been developed (Connick et al., 1991). In some cases, the formulated product may be a solid, but the organism may multiply on this substrate and be disseminated into the foliage in this manner. One type of formulation used for biological control consists of encapsulation of the propagule in starch granules. This allows the biocontrol agent to be delivered in a conveniently applied form; however, adherence to the leaf surface requires that there be preapplication wetting, which is not realistic for large-scale commercial use (McGuire & Shasha, 1992). A second type of formulation that has been the focus of most workers in the field of biological control of weeds utilizes invert emulsion. This method involves the use of a variety of mixtures composed of combinations of paraffin wax, mineral oil, soybean oil, and lecithin. These combinations are mixed with a spore suspension and an emulsifying agent. The first application of this type of mixture was with spores of Alternaria cassiae to control sicklepod (Senna obtusifolia) (Daigle et al., 1990). The ability of the oils to significantly depress the rate of water evaporation facilitates germination of the applied spores when there is an inadequate dew period. The amendment of the invert emulsion with nutrients increased the germinability, as did establishing the optimal pH of the solution (Daigle & Cotty, 1991, 1992). Since this first development of invert emulsion based formulations, numerous potential biological control agents have been applied using this type of formulation with different combinations of components (Womack et al., 1996; Yang & Schaad, 1996). The knowledge gained from past experimentation in invert emulsion formulation has led to the extensive use of vegetable oils, and this treatment appears to cause no alteration to the cuticular layer of the leaf surfaces of the plants that have been examined (Auld, 1993; Egley & Boyette, 1995). Additional work with Alternaria Nees spp., A. crassa (Sacc.) Rands, and A. cassiae indicated that the formulation of these mycoherbicides as invert emulsions reduced the necessary inoculum threshold (Amsellam et al., 1990). The work with these two pathogens indicated that conidia were receiving additional benefits from the formulation ingredients beyond that provided by

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the prolonged availability of water. However, few experiments included adequate controls with the emulsion alone to determine what, if any, effects these oil and wax mixtures have on the plant. In the case of Alternaria spp., the assumption was that the fungus was enhanced in some way, rather than the plant being predisposed (Amsellam et al., 1990). The potential for phytotoxicity has been assessed in other studies and this has affected the choices of the components for the formulations. A great deal of work has been done in this area with Colletotrichum truncatum for the control of hemp sesbania (Sesbania exaltata [Raf.] Rydb. ex Hill) and Colletotrichum orbiculare for the control of Xanthium spinosum. Control of hemp sesbania was dramatically improved by the use of the invert emulsion in the absence of dew, again supporting the hypothesis that greater control is achieved through providing a prolonged period of water availability (Boyette, 1995). Additional work with the Colletotrichum spp. indicates that there is a direct effect on the plant from some types of oils (Auld, 1993; Klein et al., 1995c). Reports of host-range expansion through the use of the invert emulsion formulation further support the idea of the effect of oils on the plant contributing to disease progress. Although the use of oils to increase the host range of biological control agents that have extremely limited host ranges is a positive prospect, host ranges might also be altered to include crops in which the agent is applied. In the case of Alternaria crassa, a biological control agent for jimsonweed (Datura stramonium L.), the host-range expansion resulted in a number of crops being affected, including tomato (Lycopersicon esculentum Mill.), eggplant (Solanum melongena L.), potato (S. tuberosum L.), and tobacco (Nicotiana tabacum L.) (Yang et al., 1993). Two additional formulations that have become increasingly popular for biological control agents of weeds and diseases are alginate pellets and one referred to as Pesta. These solid formulations are easily adapted to a number of different fungi. Alginate pellets have been used to deliver a substantial number of biological control agents, including Alternaria macrospora, A. cassiae, Fusarium lateritium Nees:Fr, Colletotrichum malvarum (Braun. and Casp.) South., Fusarium solani (Mart.) Sacc. f. sp. cucurbitae Snyd. and Hans., Talaromyces flavus (K16cker) Stolk and Samson, Gliocladium virens Mill., Gold., and Foster (DeLucca et al., 1990), Penicillium oxalicum Currie and Thom., and Trichoderma viride Pers:Fr. (Daigle & Cotty, 1992). This formulation can be manipulated in a number of ways to optimize the development of the agent in the field, as well as increasing the ease of application. Organisms that have been formulated in this manner have excellent shelf life compared to the unformulated organisms, and the composition actually allows the formula to act as a sporeproduction system. This type of system optimizes the po-

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tential of the agent by providing high concentrations of freshest inoculum possible, and it can be manipulated to provide optimal conditions for sporulation. Rather than quantifying the inoculum at the time of application and introducing it into the environment, depending on that source to provide adequate infection, this system allows a new crop of fresh spores to be produced from the mycelium or spores that have been incorporated into the pellet. Nutritional amendments, such as sugars or corn, soy, or rice meal as a carbon source or amino acids, just as in a growing medium, may be incorporated into the formulation to provide a base for improved germination as well. This method of formulation appears to be relatively inexpensive and versatile and can produce inoculum to virtually any size or weight standard (Gemeiner et al., 1991). This also has the advantage that additional stickers may be added with an encapsulated biocontrol agent and allow the alginate to adhere to the surfaces of seeds to protect them against a pathogen (Andrews, 1992). The Pesta formulation is also a means of producing inoculum within the formulated material. This material consists of a wheat gluten mixed with the fungus to prepare sheets of material that are then dried and crumbled. This material, used with Fusarium oxysporum Schlecht.:Fr. to control sicklepod, was found to retain viability for 1 year, although at a reduced level (Boyette et al., 1993a). This formulation allows for a convenient means of delivery and results in the production of secondary cycles of conidia in the field. When agricultural byproducts, such as corn cobs or rice husks, are used to produce inoculum, the pathogen may be stored on this ground material and the material then applied directly to the field (Batson & Trevethan, 1988). This is a case of the medium of spore production acting as a carrier rather than a true formulation. This could also be said of the use of a liquid medium that is incorporated with Vermiculite or Perlite for field application. Although these methods may provide inexpensive means of producing inoculum for field use, prolonged storage of these types of materials does not seem feasible. Studies on the viability of the encapsulated pathogen after prolonged storage have not addressed the potential for contamination of this material or the degradation of nutrients in the mixture. These factors could result in not only a loss of viability but also a loss of infectivity. One interesting aspect that has been explored recently is the use of sunscreens to protect spores that are not melanized (Prasad, 1993). For instance, Chondrostereum purpureum formulated with an ultraviolet protectant was able to withstand a wider range of environmental conditions. Finally, there are a number of cases in which fungi tested as biocontrol agents were successful in greenhouse trials but failed to perform equally efficaciously in the field. Although the lack of an adequate dew period is most commonly cited as the explanation for this phenomenon, it is

possible that the propellant used to pressurize the sprayer may play a role. The most commonly used sprayer systems rely on CO2 as the spray propellent and the generation of carbonic acid in CO2-pressurized suspensions can lower the pH of the suspension. Rosskopf et al. (1997) studied the effect of CO2-induced changes in pH on spore germination or disease development with three bioherbicidal fungi. Germination of conidia of Phomopsis amaranthicola, a pathogen of pigweeds (Amaranthus spp.), and Alternaria cassiae, a pathogen of sicklepod (Senna obtusifolia), was significantly reduced when the suspensions were of pH 4.0-5.0 compared to pH 7.0. In the case of P. amaranthicola, the germination dropped from 93% at pH 7.0 to 73% at pH 4.0. The CO2 propellant had a significant effect on P. amaranthicola, causing as much as a 50% reduction in germination of conidia, but did not similarly affect conidia of A. cassiae. Disease severity, rated on a scale of 0-12, was significantly reduced when A. cassiae was applied to plants with CO2 rather than compressed air. In the case of P. amaranthicola, disease severity was reduced from 10.6 when the fungus was pressurized with air for 30 min to 5.5 when pressurized with CO2 for the same duration. The third fungus, Microsphaeropsis amaranthi, also a pathogen of pigweed, was not affected by changes in pH or CO2 pressurization. Six commonly used adjuvants and surfactants lowered the pH of pressurized solutions even more than CO2 alone, which may additionally compromise field efficacy of bioherbicide agents.

BIOHERBICIDES AND INTEGRATED WEED M A N A G E M E N T An important area of research that is beginning to receive more attention is the compatibility of biological control agents with multiple crop protection strategies in an integrated pest control program (Smith, 1982; Watson & Wymore, 1989). This may include the use of multiple biological control agents (Chandramohan & Charudattan, 1996) or the timing of applications of biological control agents with cultural management practices for diseases and weeds (TeBeest & Templeton, 1985). For an agent to be successfully incorporated into agricultural practices that are already established, such as the use of chemical fungicides or herbicides, it is important to determine what the effects of these practices might be on the biological agent. It has been found that chemical pesticides may serve as a nutritional base for some microorganisms or otherwise enhance the disease effects that plants incur from fungal plant pathogens (Altman & Campbell, 1977; Altman & Rovira, 1989; Cerkauska, 1988; Johal & Rahe, 1990). The primary goal of testing the effect of chemicals on potential biological control agents is to determine the incompatible reactions that may limit the use of the organism.

Chapter 35 Use of Plant Pathogens in Weed Control In the case of C. gloeosporioides f. sp. aeschynomene, or Collego | it was found that the fungus was compatible with tank-mixed applications of herbicides, such as bentazon (3-( 1-methylethyl)- 1H-2,1,3-benzothiadiazin-4(3H)-one 2,2-dioxide) or acifluorfen (5-(2-chloro-4-(trifluoromethyl) phenoxy)-2-nitrobenzoic acid). This organism was also found to be compatible with a number of insecticides and fungicides (Smith, 1991). The agent DeVine | on the other hand, was found to be detrimentally affected by the addition of any wetting agents, fertilizers, or chemical pesticides (Kannwischer et al., 1980). Charudattan (1993) and Hoagland (1996) provide reviews of the materials that have been tested with several biological control agents. Although fungal plant pathogens that are developed as biological control agents appear to be most commonly compatible with insecticides, there are few other generalizations that can be drawn. Thus, it is imperative that each individual agent be tested before it is tank-mixed or other combined use is recommended. It is possible that the efficacy of microbial weed control agents could be enhanced when used in combination with chemical herbicides (Smith, 1991) as well as in conjunction with other weed management practices. For example, soil solarization has been shown to provide good control of several weeds, including winter annual grasses and field bindweed, but only marginal control of nutsedge (Chellemi et al., 1997). Several weeds are not completely controlled by the heat produced, including bermudagrass (Cynodon dactylon [L.] Pers.), johnsongrass (Sorghum halepense [L.] Pers.), and common purslane (Portulaca oleracea L.) (Pullman et al., 1984). Biological control agents could be applied for control of the weeds that are less affected by soil solarization and tend to come through the plastic. Rhizobacteria also have the potential for use in combination with other control measures (Fernando et al., 1994) and may be enhanced by management practices. Boyetchko (1999) has suggested that reduced tillage practices could allow for increased populations of rhizobacteria, with crop residues providing excellent habitats and substrate for overwintering of these bacteria. The weed-suppressive activity of bacteria applied to winter annual grass weeds was enhanced by the application of reduced rates of herbicides (Harris & Stahlman, 1992). This was also true when deleterious bacteria were applied to downy brome in combination with diclofop and metribuzin (Stubbs & Kennedy, 1993). There is also the potential for combining different strains of rhizobacteria and rhizobacteria with other biocontrol agents. A synergistic effect was observed when Pseudomonas fluorescens Migula was combined with Flavobacterium balustinum Harrison and applied to soil containing seedlings of leafy spurge (Kremer & Kennedy, 1996). In situations where complete eradication of the target weed is not accomplished, biological agents may adequately affect the growth components of the weed, so that

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it is no longer a significant competitor (Kempenaar et al., 1996a). Kennedy et al. (1991) conducted laboratory and field studies to examine the effects of P. fluorescens strain D7 on downy brome (Bromus tectorum), which is a major pest in winter wheat in the northwestern United States. The application of this rhizosphere bacterium reduced germination, biomass production, and seed production of the target weed but had no effect on the growth of wheat. Paul and Ayres (1990) conducted field experimentation on the effect of common groundsel (Senecio vulgaris L.) competition on the growth and yield of lettuce (Lactuca sativa L.). The rust pathogen Puccinia lagenophorae Cooke, which infects groundsel, had a significant impact on the competitive ability of the weed when compared to noninoculated plants. Lettuce yields in plots containing diseased groundsel were between two and three times greater than in plots with noninfected plants. This rust fungus may have potential as a classical biocontrol agent for common groundsel in the United States (Wyss & Mtiller-Sch~irer, 1998). Sclerotinia sclerotiorum (Lib.) de Bary was able to effect a decrease in competition between spotted knapweed (Centaurea maculosa Lam.) and bluebunch wheatgrass [Agropyron spicatum (Pursh.) Scribn. and Smith]. Sclerotinia sclerotiorum reduced the spotted knapweed density by 68-80% without reducing the density of the wheatgrass (Jacobs et al., 1996). Colletotrichum coccodes (Wallr.) S. J. Hughes, which has limited efficacy on velvetleaf (Abutilon theophrasti Medik.) monocultures (Anderson & Walker, 1985), was found to significantly reduce the plant growth and competitive ability when used in soybean production fields (DiTommaso et al., 1996). Yield losses in soybean were significantly lower in plots in which the velvetleaf plants were treated with the pathogen.

BIOTECHNOLOGY AND BIOLOGICAL CONTROL Successful biological control using microbial agents requires several complex and often specific interactions between the biocontrol target and the agent. This complexity of interactions is one reason for the inconsistency and unpredictability of biological control systems. Understanding these interactions at the molecular and biochemical levels will render the biological control approach more predictable and less arbitrary. It will also help to facilitate the development of agents through characterization of the mechanisms of plant pathogenesis. It is hoped that these types of understandings will lead to genetic engineering of highly effective biological control agents, enable the selection of agents with desired traits, and help to determine environmental fate of biological control agents. Plant pathogens produce a variety of secondary metabo-

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lites capable of inflicting characteristic phytotoxic damage in their plant hosts. Two kinds of pathogen-produced phytotoxins are recognized: host-selective or host-specific toxins and host-nonselective or host-nonspecific toxins (Turgeon & Yoder, 1985; Yoder, 1983). Host-selective toxins are toxic only to the hosts that are normally attacked by the pathogen, and nonselective toxins are phytotoxins that affect a broader range of hosts than the toxin-producing pathogen does. Approximately 20 host-selective toxins have been identified and are often determinants of host range (Walton, 1996). A phytotoxin can be further classified on the basis of its biological role as a pathogenicity factor, a toxin that is essential for a pathogen to cause disease or a virulence factor, or a toxin that increases the level of disease once disease develops (Yoder, 1983). Finally, many pathogenic microorganisms are known to synthesize plant growth hormones. However, a growth hormone is different from a toxin; whereas a toxin is a pathogen-produced compound that the plant is unable to synthesize, many compounds with growth-hormonal activity are products of a plant's normal metabolism. Although such compounds are generally not toxic when the plant produces them, the physiological imbalance created by their synthesis during the disease process serves as a virulence factor of the pathogen. It should be possible to genetically engineer two important factors affecting bioherbicides, level of virulence and alteration in host range. Theoretically, it should be possible to engineer for increased virulence or host range or both, provided the following conditions can be met: (1) availability of a suitable pathogen for genetic engineering; (2) availability of suitable vectors and selectable markers; (3) availability of cloned toxin genes; (4) availability of a suitable gene-expression system for the toxin genes and for any genes necessary to confer resistance to the toxin to the transformed agent; (5) in the case of fungal pathogens, ability to produce and regenerate protoplasts or feasibility of direct injection of genes; and (6) availability of suitable containment facilities to conduct tests under safe conditions. Attempts to engineer bioherbicides have just begun, but several projects can serve as examples of the possibilities. In the first example, Charudattan et al. (1996a) attempted to alter the virulence and host range of the ubiquitous bacterial plant pathogen Xanthomonas campestris pv. campestris (Pammel) Dowson with genes encoding the production of bialaphos, which is a secondary metabolite and a hostnonselective phytotoxin produced by the soil saprophyte Streptomyces hygroscopicus (Jensen) Waksman & Henrici. Bialaphos and the active moiety phosphinothricin are registered as a new class of biologically derived herbicides. These biochemicals also have antimicrobial effect. A 33.5-kb Hind III-treated segment of a reconstructed plasmid (41 kb) containing bialaphos production genes was introduced into the genome of the bacterium, and the altered

and the parent bacteria were tested for alterations to their host range. The pathogenic host reaction was characterized by a typical black-rot disease caused by the parent and the transformed bacterium on its natural hosts, cabbage and broccoli, whereas the nonhost reaction caused by the parent was a necrotic hypersensitive reaction and a spreading, chlorotic, compatible host reaction caused by the transformed bacterium (Charudattan et al., 1996). The bioherbicide pathogen Colletotrichum gloeosporioides f. sp. aeschynomene (CGA) has been transformed with the bar gene, which confers resistance to bialaphos and phosphinothricin. This gene was also cloned from S. hygroscopicus, in which it serves to protect against the autocidal effects of bialaphos. In this case, the bar-gene-transformed fungus could be exposed to bialaphos without being affected and the bar-transformed biocontrol agent can then be coapplied with the chemical herbicide. This allows for the control of both northern jointvetch (Aeschynomene virginica), which is susceptible to CGA, and Indian jointvetch (A. indica), which is controlled by bialaphos, but not CGA (Brooker et al., 1996). In addition to the possibilities associated with the transformation of biological control agents for the purposes of increased virulence or host-range alteration, there is the application for monitoring introduced strains and for risk assessment. Characterization of isolates of Chondrostereum purpureum, used as a mycoherbicide for control of hardwood weed species, through the use of DNA fingerprinting has made it possible to differentiate between the isolate released as mycoherbicide and those that are naturally occurring (Gosselin et al., 1996; Ramsfield et al., 1996). This type of work has also been applied to the biological control agent Phomopsis subordinaria (Desmaz) Traverso, evaluated for the control of plantain (Plantago lanceolata L.). In addition to isozyme characterization of isolates to be used for biocontrol, randomly amplified polymorphic deoxyribonucleic acid (RAPD) analysis was used (de Nooij & van Damne, 1988; Meijer et al., 1994). In a recent study by Berthier et al. (1996), the internal transcribed spacer (ITS) polymorphic restriction patterns of the DNA of the biological control agent Puccinia carduorum Jacky were found to be distinct for P. carduorum strains from Carduus acanthoides L. and C. thoermeri compared to those of the same fungal species isolated from C. tenuiflorus Curtis and C. pycnocephalus L. DNA fingerprinting techniques and the development of reliable markers and tracking systems can greatly contribute to further success of bioherbicides as well as the general knowledge base related to the biology of these organisms. Molecular markers may be used to monitor specific strains of microbes using polymerase chain reaction (PCR) amplification to detect specific DNA sequences. Tools such as bioluminescence markers and green fluorescent protein can contribute to this process and have been applied success-

Chapter 35 Use of Plant Pathogens in Weed Control fully in several cases (Kennedy, 1996; Poppenborg et al., 1997). Although this technology has not been widely applied as a regular component in the selection and development of biological control agents, it is anticipated that utilization of this technology will facilitate the registration of plant pathogens as bioherbicides in the future.

LAWS GOVERNING BIOLOGICAL CONTROL AGENTS The Federal Plant Pest Act (FPPA) of 1957, as amended, and the Federal Plant Quarantine Act (FPQA) of 1912, as amended, grant the Secretary of Agriculture broad authority to carry out operations or measures to detect, eradicate, suppress, control, prevent, or retard the spread of plant pests (Charudattan & Browning, 1992). This authority gives the United States Department of Agriculture (USDA) the flexibility to respond appropriately to protect American agriculture against foreign pests. According to this Act, a plant pest is any organism or infectious agent which directly or indirectly injures plants or causes disease or damage to any plants or plant parts. The authority to administer the regulations and activities of controlling and eradicating plant pests rests with the Animal and Plant Health Inspection Service (APHIS) of the USDA. The Plant Protection and Quarantine (PPQ) branch under USDA-APHIS bears the primary responsibility for the control and eradication activities. Plant Protection and Quarantine also regulates the legitimate importation, interstate movement, and use of foreign plants and plant products as well as plant pests and potential plant pests used for research or commercial purposes. This is done under a permitting process with which APHIS grants what is commonly known as a quarantine permit. Microbial biological control agents used as pesticides are regulated under the Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA). FIFRA, in its revised form, was enacted in October of 1988. Under this Act, the Environmental Protection Agency (EPA) has been given the responsibility for ensuring that the distribution and use of pesticides are done in such a manner as to prevent unacceptable risks to human health and the environment. The EPA regulates the use of pesticides primarily through registration of pesticides, which it does after a thorough review of the health and safety data, and through prohibition of distribution and sale of unregistered pesticides, or pesticides that are improperly labeled, or have improper composition. In addition, it is illegal to use a pesticide in a manner inconsistent with its labeling. A coordinated framework for regulating products arising from biotechnology, including biocontrol agents, produced through genetic engineering was developed in 1986 under the authority of the executive Office of the President, Office

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of Science and Technology Policy. Under this framework, the authority to regulate recombinant technology products and recombinant biocontrol agents is given to the USDAAPHIS' Biotechnology, Biologics, and Environmental Protection (BBEP) division. The USDA policy on the regulation of biotechnology does not view genetically engineered biocontrol organisms as fundamentally different from those that have been isolated from nature and introduced into a new environment. The organisms and products produced through the new techniques of biotechnology are regulated under existing laws that have applied to naturally occurring organisms and products of traditional technologies. To address the need for specific information necessary for the assessment of the products of the new technologies, a few new regulations have been promulgated and some old ones have been updated. The USDA regulations consider the risks posed by an organism or a product under a specific use rather than on the process (i.e., genetic engineering) used in production. Permits are required for any introduction of organisms modified through genetic engineering. Under these regulations, "introduction" means to move a regulated article into or through the United States, to release into the environment, or to move between states. "Release into the environment" means the use of the regulated article outside the constraints of physical confinement of a laboratory, contained greenhouse, a fermentor, or other contained structure. A "regulated article" is any product which contains an unclassified organism and may be a plant pest or any organism which has been altered or produced through genetic engineering, if the donor organism, recipient organism, or vector or vector agent belongs to any genera or taxa designated by the USDA as meeting the definition of plant pest or if it is an organism whose classification is unknown. The regulations have been amended to include a specific exemption from the need for a permit for organisms that meet the definition of a regulated article. A limited permit is not required for interstate movement for genetic material from any plant pest contained in Escherichia coli (Migula) Castellani and Chalmers genotype K-12, sterile strains of Saccharomyces cerevisiae Hansen, or asporogenic strains of Bacillus subtilis (Ehrenberg) Cohn, provided all of the specific conditions recognized by the USDA list are met. As scientific knowledge with the products of biotechnology increases and we achieve familiarity with the interaction between modified organisms and their environment, additional amendments to the regulations are expected. These amendments will be added either by APHIS at the Agency's initiative or through a public petition process, which is an innovative feature of these regulations. This process is expected to be used by applicants and other members of the interested public to seek changes to the list of organisms on the USDA' s list or to obtain specific exclusions of genetically engineered organisms from regulation.

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The petition to amend must contain a statement of grounds and supporting literature, data, or unpublished studies as well as opposing views or contradictory data. A petition that meets these requirements will be published in the Federal Register for comment. When a petition is approved, the changes to the regulation are published with a complete response to public comments. The National Environmental Policy Act (NEPA) was enacted in 1969 to protect against adverse environmental effects resulting from major actions implemented by federal agencies. Under this Act, all federal and federally supported agencies must consider the environmental impact of major actions, such as release of a foreign pathogen for weed control or a genetically engineered microbe into the environment, that may significantly affect the quality of the human environment in the United States. With certain exceptions, an Environmental Assessment (EA) is required for the initial field release of a foreign or engineered biocontrol agent into the United States or into the field. The necessary permits for importation or field release of the biocontrol agent will be granted only after the EA is approved. The reviewing scientist in APHIS prepares the EA, and the environmental assessment is subject to peer review by the APHIS scientific staff. When the environmental assessment results in a Finding of No Significant Impact (FONSI) on the environment, a notice of availability of the environmental assessment and FONSI is published in the Federal Register, and the permit to go ahead with the planned introduction or field release is issued. The permit may contain special conditions which must be met in addition to those specified in the protocol submitted as part of the application. As a condition of every permit for release to the environment, scientific data must be collected and submitted to APHIS. The EA document will contain information describing the purpose of the document, Departmental regulations, the conditions under which the permit is issued or denied, precautions against environmental risk, the background biology of the organisms, and the possible environmental consequences of the field test. The environment that could be affected by the field test is described and the precautions developed for protecting that environment, including field plot design, field inspection and monitoring, test plot security, and disposal plans, are analyzed. The environmental consequences of the test are examined from all possible perspectives. Consideration is given to the biology of the recipient, donor, and vector and to the potential for biological containment based on knowledge of this biology. Any possibility of risk to native flora or fauna is evaluated, with special consideration of organisms which are threatened or endangered. Any potential impact on human health is examined. A detailed report describing the effects of the proposed field release on the environment is called the Envi-

al.

ronmental Impact Statement (EIS). Requirement of an EIS is initiated if any adverse risk is perceived. The Endangered Species Act (ESA) of 1973 was enacted to protect the many threatened and endangered (T&E) species, both plants and animals, in the United States. The Fish and Wildlife Service (FWS) of the U.S. Department of the Interior (USDI) administers this Act. Under the authority of this act, the impact of federal actions on native and endangered plant and animal species must be determined by using a safety evaluation protocol developed under this Act. Comments on concerns and any test results developed to assess risk to T&E species should be included in the EA or EIS documents. The federal government has a legal means of designating weeds considered to be extremely harmful to the nation or a region. The Federal Noxious Weed List allows for such listing. Once a plant is designated as a noxious weed, certain regulatory actions can be enforced, such as banning the collection, use, and transport of such plants and the requirement of permits to collect and transport such plants for legitimate purposes. The federal Noxious Weed Act provides the authority for these regulations. In addition to federal laws, several states have laws and regulations regarding environmental policy and/or endangered species within their boundaries, similar to NEPA and ESA. Certain states have regulations requiring permits or approval prior to shipment or release of arthropod and nematode biological control agents within their borders or otherwise have formal requirement for notification prior to importations or releases. Some states have their own Noxious Weed Laws that enable them to designate and regulate weeds of local importance. In 1959, the USDA and the USDI established a joint committee that developed guidelines about kinds of data that would be necessary to assess insect species introduced into the United States for biological control of weeds. Later, plant pathogens considered for use as biological weed control agents were also evaluated by this group. The group, a voluntary assembly of scientists, formed a relationship with Canada and Mexico so decisions to release new organisms could be made on a continental basis. In 1966, this working group was put under APHIS-PPQ and it was reorganized in 1987 as the Technical Advisory Group on the Introduction of Biological Control Agents of Weeds (TAG) to make recommendations to scientists and to give assessments to regulating agencies. TAG membership includes representatives from 10 designated federal agencies and additional representatives invited to review applications to import and/ or release biocontrol agents (Coulson, 1992). TAG deals only with naturally occurring organisms, not those which have been genetically engineered. Its responsibilities are to (1) review research proposals on biological control of weeds involving introduction of exotic organisms into the United States to ensure that all aspects of safety of

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the potential introductions are considered in the research plan; (2) provide guidelines for researchers that must be met before an organism is considered for entry into or approved for release from quarantine in the United States; (3) review the documentation supporting proposals to release exotic organisms for biological control of weeds in the United States and to evaluate the adequacy of the data showing the safety of the proposed release; and (4) recommend actions to be considered by PPQ to release or not to release biological control organisms from quarantine. There are essentially three types of petitions to the TAG: (1) Proposals to conduct research on the classical biological control of a plant species not previously targeted for such research in the United states. It is at this point that conflicts of interest can be identified that may indicate to the researcher that approval for the introduction of exotic natural enemies of the plant would be unlikely or at most difficult to obtain, and consideration can thus be given to aborting the project before needless expenditure of research funds. (2) Proposals for the introduction of exotic organisms into quarantine in the United States for research purposes, review of which may be requested by PPQ. (3) Proposals for the field release of an exotic organism in the United States (or Canada or Mexico). In connection with the. first or second type of petition, a list of plants to be included in host specificity testing is provided for review by the TAG. The major issues evaluated by the TAG reviewers are (1) the adequacy of taxonomic information about both the biological control agent and its target weed, (2) the adequacy of the range of plants included in the host specificity tests, (3) the adequacy of the results of research on the host range of the agent proposed for field release, from both field and laboratory studies and literature search, and (4) the potential impact of the agent on nontarget plants. The TAG Chair evaluates the comments of TAG and other outside reviewers of the petition and, if a clear consensus is evident, prepares a recommendation on the petition. Recommendations concerning a new plant for biological control or test plant lists are made to the petitioner. Recommendations concerning quarantine importation or field release of organisms are made to the Deputy Administrator of APHIS-PPQ. Often the review comments indicate the need for additional information or additional testing, in which case this need is expressed to the petitioner, with copy to the PPQ Deputy Administrator. As stated previously, microbial biocontrol agents used as pesticides are regulated under the FIFRA by the EPA. According to FIFRA, biological control agents fall under the definition of a pesticide if they are intended for "preventing, destroying, repelling, or mitigating any pest" or are intended for "use as a plant regulator, defoliant, or desiccant." However, FIFRA provides authority to exempt from regulation any pesticide which is adequately regulated by another federal agency (such as USDA-APHIS) or which is

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otherwise of a nature not requiring oversight under FIFRA. Under this authority, EPA exempted all biological control agents from FIFRA oversight, with the exception of eukaryotic microorganisms, including protozoa, algae, and fungi; prokaryotic microorganisms, including bacteria; and viruses. However, EPA can revoke this exemption if it determines that a biocontrol agent or class of biocontrol agents is not adequately regulated by another federal agency and the agent(s) should not otherwise be exempt from FIFRA. EPA has recognized that regulatory oversight of microbial pesticides must consider ways in which these pesticides differ from chemical pesticides. Among microbial pesticides, those involving pathogenic, nonindigenous, or genetically modified microorganisms are considered to pose greater potential risks than indigenous, nonpathogenic, unmodified organisms. The use of biocontrol organisms that will result in the appearance of the organism (or any parts of the organism) in food or feed is regulated by the EPA under the Federal Food, Drug and Cosmetic Act (FFDCA). Any biocontrol agent that poses toxic hazard will fall under the Toxic Substances Control Act (TSCA). TSCA becomes involved when a living recombinant is being produced; however, this will not affect most researchers, as materials produced for research and development are exempted from this regulation. Finally, the Endangered Species Act may require that labeling warn users of potential adverse effects on endangered species. The DeVine | label, for example, specifically instructs that this bioherbicide is not to be used in areas where the endangered native azalea, Rhododendron chapmanii Gray, naturally occurs. In general, there are four kinds of applications which are processed by EPA under FIFRA. These are Registrations: Registration allows the unrestricted use and marketing of a pesticide product as long as the accepted labeling is followed. Registrations are handled under Section 3 of FIFRA. Experimental Use Permits: An experimental use permit (EUP) may be issued to a person, company, or institution for the purpose of obtaining the required data for registration. EUPs generally have a one- or two-year time limit, and the organism can only be used by cooperators of the experimental program. The organism can only be shipped to those states as stipulated in the program and the conditions of use are tightly controlled. EUPs are issued under Section 5 of FIFRA. Often researchers are confused as to whether the proposed work will require an EUP or a Notification. As a rule of thumb, applications to greater than 10 acres of land or 1 acre of water require an EUP. Also, if the use will result in residues of the pesticide in food or feed, an EUP is usually required. Smaller size experiments which are crop-destruct or designed for noncrop uses

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(such as forestry or ornamental plants) usually can be handled by a Notification. Emergency Exemptions: Emergency exemptions are issued in situations where there is insufficient time to process a registration or the data base for registration is incomplete and significant adverse effects (such as public health impacts) may occur if the use of the pesticide is prohibited. Emergency exemptions are regulated under Section 18 of FIFRA and are only issued to Federal and State Agencies. Special Local Needs: Section 24(c) provides that a State may register additional uses of registered pesticides for use and distribution within that State, provided that such use has not been previously denied, disapproved, or canceled.

Some simple rules to follow are

In addition to formal applications, the following are regulated by the EPA:

One of the important challenges facing the developers of biological control agents is to establish protocols by which the agents can be produced and utilized in a manner that is competitive or compatible with the tools that are currently available. The cost of producing large quantities of biomass can be inhibitory if there does not exist a rather substantial market. It was once thought that if an organism could not be produced using submerged fermentation, it would not have promise as a viable biocontrol agent. Through improvements in existing technologies, this is no longer the case, although the information base is more fully developed for liquid fermentation (Churchill, 1982). The majority of the information available on fungal nutrition and the conditions necessary for sporulation may apply to any production system, but most have been evaluated using liquid fermentation. Some examples of fungi that have been cultured on a large scale using submerged fermentation include C. gloeosporioides f. sp. aeschynomene (Collego | for the control of northern jointvetch and Phytophthora palmivora (DeVine | for the control of stranglervine (Churchill, 1982). In the submerged fermentation system, a high yield of biomass is produced and this biomass is easily separated from the culture medium. At the laboratory experimentation scale, shake flasks may be used to culture ample amounts of inoculum but may not allow for predicting how the organism will grow on a larger scale. A number of factors can contribute to the proper growth of the cultured organism and these may be difficult to monitor in a small, shake flask system. Laboratory fermentors are available that monitor parameters such as pH, temperature, dissolved oxygen, and the amount of agitation (Bannon et al., 1990). Some fungi require manipulation of one or more of these factors to induce sporulation in liquid culture. Spores are favored over mycelium for long-term storage (Churchill, 1982). Depending on the conditions, some fungi will produce a number of different types of propagules in a single liquid culture. This is the case with Colletotrichum gloeosporioi-

Notifications: A notification is essentially a request that EPA make a determination as to whether the proposed small-scale testing of a nonindigenous, genetically altered or genetically engineered organism is of such a nature that an EUP should be required prior to the initiation of the study. Notifications are handled by EPA under the Coordinated Framework for B iotechnology. Tolerances: EPA is responsible for regulating the residues of pesticides which may appear in food. This is done by establishing a tolerance level, which is the maximum permissible residue allowed. Because of their nature, microbial pesticides usually are regulated through an Exemption from the Requirement of a Tolerance. To qualify for the exemption, the applicant must provide data or information that indicates that the pesticide in any amount will be safe when used on food or feed crops. For EUPs where the microbial pesticide will be used on food or feed, a Temporary Exemption from the Requirement of a Tolerance may be issued, with somewhat less data. In general, microbial pesticides have been determined by EPA to be in the public interest (due to host specificity, low toxicity, and unique modes of action) and the tolerance fees for these submissions are often refunded. Subdivision M of the FIFRA Guidelines: Subdivision M of the FIFRA guidelines describes in detail the studies and data required for registration of a microbial pesticide. If a particular requirement is inappropriate, the applicant may request that the requirement be waived. Such waiver requests should be accompanied by the pertinent information that provides a basis for the waiver request. Subdivision M guidelines have been recently updated and replaced. For the latest information, see Environmental subset at Gopher.epa.gov.

1. Always strictly follow the rules and regulations that are in force. 2. Whenever applicable, obtain proper permits and institutional clearances before doing "controlled" or "regulated" type of activity. 3. Keep institutional, state, and federal agencies fully informed of progress and promptly report back to the agencies when the work is completed. 4. Always keep the public fully informed if your research might involve public sentiments.

PRODUCTION OF BIOHERBICIDE AGENTS

Chapter 35

Use of Plant Pathogens in Weed Control

des f. sp. aeschynomene, in which the majority of spores produced in liquid fermentation are yeast like spores, produced by budding (Churchill, 1982). Conidia and blastospores and arthrospores are also produced by this fungus, a phenomenon referred to as fungal dimorphism. Although in the case of Collego | all spore types are infective, it is possible in other cases, when dimorphism is induced, that the resulting propagules may not have the same efficacy. In some studies, the nutritional components of the culture media have been manipulated to induce sporulation in fungi that do not normally produce spores in liquid culture (Stowell, 1991). With some Fusarium species, it was found that potassium phosphate, magnesium sulfate, and potassium chloride were particularly important in inducing sporulation (Diarra et al., 1996; Hallsworth & Magan, 1994). In general, among the fungi tested, sporulation often occurs in the presence of various types of stress, most commonly nutritional (Mckoy & Trinci, 1987). This means of inducing sporulation may not be applicable for production of biological control agents because the postprocessing viability and efficacy can be detrimentally affected. To address this complication, many types of media may need to be tested to determine the optimal conditions for a large quantity of biomass that must also maintain viability and activity. The first aspect may be addressed in terms of the specific growth rate, which is a measure of the biomass increase over time. This can then be used to compare different compositions of media for optimal growth. The type of inoculum used to seed the fermentors may also affect the end product. In some cases, as much as a twofold increase in fermentation time is required when conidia are used for fermentor inoculation rather than mycelium (Churchill, 1982). The quantity of conidia produced, as well as their tolerance to the drying process, is affected by the carbonto-nitrogen ratio as well as the sources of those nutrients (Jackson & Bothast, 1990). Although a large portion of the work done in this area has been done with Colletotrichum species used for biological control of weeds, the foundation lies in the development of yeasts used in food preparation (D'Amore et al., 1991). It has been found that if a high carbon-to-nitrogen ratio is used, excessive availability of carbohydrates results in lipid accumulation. A high lipid concentration is associated with poor germination in many fungi (Griffin, 1994). The physiological role of the carbon source may be even more important than the ratio. For example, glucose is often used as a component of many types of media (Dhingra & Sinclair, 1995). Some fungi may cease to produce a number of inducible enzymes when they are in the presence of glucose (Griffin, 1994). These enzymes may be crucial to pathogenesis. The levels of specific minerals may be as important as the carbon source. Zinc and magnesium, for example, play an important role in the production of pathogenesis-related toxins in species of Alternaria (Griffin, 1994).

9 11

After a system is established that results in an adequate amount of the most desirable type of inoculum, it must be determined if the propagules will be tolerant to the drying process. This may be highly dependent upon the culturing conditions and the absence or presence of an osmoticum in the medium (Abbas et al., 1995b; Dillard, 1988; Harman et al., 1991). Several studies have been conducted to determine the medium components that might contribute to desiccation tolerance (Burleigh & Dawson, 1994). Some substances that have been used to influence the water potential and influence spore viability include polyethylene glycol, glycerol, sucrose, glucose, and maltose, as well as a variety of carbohydrate sources. An increase in tolerance to the drying process, as represented by increased viability and maintenance of efficacy, has been associated with an increase in the cellular concentration of trehalose (Burleigh & Dawson, 1994; D'Amore et al., 1991; Hallsworth & Magan, 1994). In addition to submerged fermentation, other methods have been used for large-scale production of inoculum, although the technology has not progressed as rapidly. Solid substrate fermentation utilizes materials such as cereal grains, straw, or other inexpensive agricultural wastes, such as corn cobs or rice sheaths. This material is used for growing the fungus and then is applied directly to the field with little or no additional processing. Although this may be the only alternative for fungi that will not produce easily dispersed propagules in any other system, this method has a number of drawbacks. Inoculum produced by this method is difficult to quantify because the fungus is not separated from the culturing material. It is often difficult to maintain sterility in these systems and storage of the resulting bulky material may be limiting. For some fungi, a combination of solid substrate and submerged fermentation is necessary to produce the desired inoculum. The potential mycoherbicidal agent Alternaria macrospora has been produced by first using liquid medium to generate mycelium that is then blended and combined with vermiculite (Walker, 1980). This mixture is then spread in a thin layer and exposed to cycling light. This method produces an ample amount of conidia but is considerably more labor intensive and expensive than liquid fermentation alone. The additional handling of the fungus also provides more opportunities for contamination. Regardless of the drawbacks of this system, it has been used for midscale production of several biological control agents (Churchill, 1982).

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Berthier, Y. T., Bruckart, W. L., Chaboudez, P., & Luster, D. G. (1996). Polymorphic restriction patterns of ribosomal transcribed spacers in the biocontrol fungus Puccinia carduorum correlates with weed host origin. Applied and Environmental Microbiology, 62, 3037-3041. Bewick, T. A., Binning, L. K., Stevenson, W. R., & Stewart, J. (1986). Development of biological control for swamp dodder. Proceedings of the North Central Weed Control Conference, 41, 24. Blanchette, B. L., & Lee, G. A. (1981). The influence of environmental factors on infection of rush skeleton weed (Chondrilla juncea) by Puccinia chondrillina. Weed Science, 29, 364-367. Bowers, R. C. (1986). Commercialization of Collego--An industrialist's view. Weed Science, 34 (Suppl. 1), 24-25. Boyetchko, S. M. (1999). Innovative applications of microbial agents for biological weed control. In "Biotechnological Approaches in Biocontrol of Plant Pathogens" (K. G. Mukerji, B. P. Chamola, & R. K. Upadhyay, Eds.), pp. 73-97. Plenum, London. Boyetchko, S. M., & Mortensen, K. (1993). Use of rhizobacteria as biological control agents of downy brome. In "Proceedings of the Soils and Crop Workshop, Saskatoon, Saskatchewan, Canada," pp. 443448. Boyette, C. D. (1994). Unrefined corn oil improves the mycoherbicidal activity of Colletotrichum truncatum for hemp sesbania (Sesbania exaltata) control. Weed Technology, 8, 526-529. Boyette, C. D. (1995). Improvement of mycoherbicidal activity of anthracnose pathogens with adjuvants and surfactants. Proceedings of the Southern Weed Science Society, 48, 167 (Abstract). Boyette, C. D., & Abbas, H. K. (1994). Host range alteration of the bioherbicidal fungus Alternaria crassa with fruit pectin and plant filtrates. Weed Science, 42, 487-491. Boyette, C. D., Abbas, H. K., & Connick, W. J. (1993a). Evaluation of Fusarium oxysporum as a potential bioherbicide for sicklepod (Cassia obtusifolia), coffee senna (C. occidentalis), and hemp sesbania (Sesbania exaltata). Weed Science, 41,678-681. Boyette, C. D., Quimby, P. C., Bryson, C. T., Egley, G. H., & Fulgham, F. E. (1993b). Biological control of hemp sesbania (Sesbania exaltata) under field conditions with Colletotrichum truncatum formulated in an invert emulsion. Weed Science, 41,497-500. Boyette, C. D., Quimby, P. C., Caesar, A. J., Birdsall, J. L., Connick, W. J., Daigle, D. J., Jackson, M. A., Egley, G. H., & Abbas, H. K. (1996). Adjuvants, formulations, and spraying systems for improvement of mycoherbicides. Weed Technology, 10, 637- 644. Boyette, C. D., Weidemann, G. J., TeBeest, D. O., & Turfitt, L. B. (1986). Biocontrol of jimsonweed in the field with Alternaria crassa. Proceedings of the Southern Weed Science Society, 39, 388. Brooker, N. L., Mischke, C. F., Patterson, C. L., Mischke, S., Bruckart, W. L., & Lydon, J. (1996). Pathogenicity of bar-transformed Colletotrichum gloeosporioides f. sp. aeschynomene. Biological Control, 7, 159-166. Bruckart, W. L. (1989). Host range determination of Puccinia jaceae from yellow starthistle. Plant Disease, 73, 155-160. Bruckart, W. L., & Dowler, W. M. (1986). Evaluation of exotic rust fungi in the United States for classical biological control of weeds. Weed Science, 34 (Suppl. 1), 11-14. Bruckart, W. L., Johnson, D. R., & Frank, R. J. (1988). Bentazon reduces rust-induced disease in yellow nutsedge (Cyperus esculentus). Weed Technology, 2, 299-303. Bruckart, W. L., Politis, D. J., & Sutker, E. M. (1985). Susceptibility of Cynara scolymus (artichoke) to Puccinia carduorum observed under greenhouse conditions. In "Proceedings of the VI International Symposium on Biological Control of Weeds, Vancouver, Aug. 19-25, 1984" (E. S. Delfosse, Ed.), pp. 603-607. Agriculture Canada, Ottawa.

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Chapter 35

Use of Plant Pathogens in Weed Control

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nia xanthii and Colletotrichum orbiculare on Xanthium occidentale. Biological Control, 3, 296-310. Morin, L., Watson, A. K., & Reeleder, R. D. (1990a). Effect of dew, inoculum density, and spray additives on infection of field bindweed by Phomopsis convolvulus. Canadian Journal of Plant Pathology, 12, 48-52. Morin, L., Watson, A. K., & Reeleder, R. D. (1990b). Production of conidia by Phomopsis convolvulus. Canadian Journal of Microbiology, 36, 86-91. Morris, M. J. (1991). The use of plant pathogens for biological weed control in South African Agriculture, Ecosystems and Environment, 37, 234-255. Morris, M. J. (1997). Impact of the gall-forming rust fungus Uromycladium tepperianum on the invasive tree Acacia saligna in South Africa. Biological Control, 10, 75-82. Morris, M. J., Wood, A. R., & Den Bre~yen, A. (1998). Development and registration of a fungal inoculant to prevent regrowth of cut wattle tree stump in South Africa, and a brief overview of other bioherbicide projects currently in progress. "IV International Bioherbicide Workshop Programme and Abstracts, 6 - 7 August 1998," p. 15. Univ. of Strathclyde, Glasgow, Scotland. Mortensen, K. (1998). Biological control of weeds using microorganisms. In "Plant-Microbe Interaction and Biological Control" (G. J. Boland & L. D. Kuykendall, Eds.), pp. 223-248. Dekker, New York. Mortensen, K., & Makowski, R. M. D. (1997). Effects of Colletotrichum gloeosporiodes f. sp. malvae on plant development and biomass of non-target field crops under controlled and field conditions. Weed Research, 37, 351-360. Oehrens, E. (1977). Biological control of the blackberry through the introduction of rust, Phragmidium violaceum in Chile. FAO Plant Protection Bulletin, 25, 26-28. Oehrens, E. B., & Gonzales, S. M. (1974). Introducci6n de Phragmidium violaceum (Schulz) Winter como factor de biologico de zarzamora (Rubus constrictus Lef. et M. y R. ulmifolius Schott.). Agro Sur, 2, 30-33. Oehrens, E. B., & Gonzales, S. M. (1975). Introducci6n de Uromyces galegae (Opiz) Saccardo como factor de control biologico de galega (Galega officinalis L.). Agro Sur, 3, 87-91. Ormeno-Nunez, J., Reeleder, R. D., & Watson, A. K. (1988). A foliar disease of field bindweed (Convolvulus arvensis) caused by Phomopsis convolvulus. Plant Disease, 72, 338-342. Parker, A. (1989). Biological control of parthenium weed using two rust fungi. In "Proceedings of the VII International Symposium on Biological Control of Weeds" (E. S. Delfosse, Ed.), pp. 531-538. Ist. Sper. Patol. Veg. (MAF). Paul, N. D., & Ayres, P. G. (1990). Effects of interactions between nutrient supply and rust infection of Senecio vulgaris L. on competition with Capsella bursa-pastoris (L.) Medic. New Phytologist, 114, 667674. Peeples, K. A. (1994). Agriculture's challenge to develop a vision for the future. Weed Technology, 8, 372-375. Phatak, S. C., Wells, H. D., Sumner, D. R., Bell, D. K., & Glaze, N. C. (1981). Observation of rust on yellow nutsedge (Cyperus esculentus L.). Phytopathology, 71: 899. Phatak, S. C., Wells, H. D., Sumner, D. R., Bell, D. K., & Glaze, N. C. (1983). Biological control of yellow nutsedge with the indigenous rust fungus Puccinia caniliculata. Science, 219, 1446-1447. Pitelli, R., Charudattan, R., & DeValerio, J. T. (1998). Effect of Alternaria cassiae, Pseudocercospora nigricans, and soybean (Glycine max) planting density on the biological control of sicklepod (Senna obtusifolia). Weed Technology, 12, 37-40. Politis, D. J., & Bruckart, W. L. (1986). Infection of musk thistle by Puccinia carduorum influenced by conditions of dew and plant age. Plant Disease, 70, 288-290. Politis, D. J., Watson, A. K., & Bruckart, W. L. (1984). Susceptibility of

musk thistle and related composites to Puccinia carduorum. Phytopathology, 74, 687-691. Poppenborg, L., Friehs, K., & Flaschel, E. (1997). The green fluorescent protein is a versatile reporter for bioprocess monitoring. Journal of Biotechnology, 58, 79-88. Prasad, R. (1993). Role of adjuvants in modifying the efficacy of a bioherbicide on forest species: Compatibility studies under laboratory conditions. Pesticide Science, 37, 427-433. Prasad, R. (1994). Influence of several pesticides and adjuvants on Chondrostereum purpureummA bioherbicide agent for control of forest weeds. Weed Technology, 8, 445-449. Pullman, G. S., DeVay, J. E., Elmore, C. L., & Hart, W. H. (1984). "Soil Solarization: A Nonchemical Method for Controlling Diseases and Pests." Univ. of California Cooperative Extension Leaflet 21377. Ramsfield, T. D., Becker, E. M., Rathlef, S. M., Tang, Y., Vrain, T. C., Shamoun, S. F., & Hintz, W. E. (1996). Geographic variation of Chondrostereum purpureum detected by polymorphisms in the ribosomal DNA. Canadian Journal of Botany, 74, 1919-1929. Ridings, W. H. (1986). Biological control of stranglervine in citrusmA researcher's view. Weed Science, 34 (Suppl. 1), 31-32. Rosskopf, E. N. (1997). Evaluation of Phomopsis amaranthicola sp. nov. as a biological control agent for Amaranthus spp. Ph.D. Thesis, Univ. of Florida, Gainesville, FL. Rosskopf, E. N., Charudattan, R., DeValerio, J. T., & Stall, W. B. (1996). Control of pigweeds and amaranths (Amaranthus spp.) with a fungus: Three years of field experimentation. WSSA Abstracts, 36, 49. Rosskopf, E. N., Gaffney, J. F., & Charudattan, R. (1997). The effect of spray propellant on the efficacy of bioherbicide candidates. WSSA Abstracts, 37, 62. Saad, F., Watson, A. K., Smith, J. P., & Sparace, S. (1993). Formulation of Colletotrichum coccodes as a bioherbicide. Abstracts, II International Bioherbicide Workshop: "Bioherbicides~Applying the Temperate Experience to the Tropics," July 31-Aug. 1, 1993, MacDonald College of McGill University, Quebec. Scheepens, P. C., & Hoogerbrugge, A. (1991). Host specificity of Puccinia caniliculata, a potential biocontrol agent for Cyperus esculentus. Netherlands Journal of Plant Pathology, 97, 245-250. Scheepens, P. C., Kempenaar, C., & Van der Zwerde, W. (1998). Integrating biological control of Chenopodium album in weed management systems. Abstracts, IV International Bioherbicide Workshop, Univ. of Strathclyde, Glasgow, Scotland. Schisler, D. A., & Jackson, M. A. (1993). Storage and efficacy of liquid culture produces microsclerotia of the bioherbicidal fungus, Colletotrichum truncatum. Abstracts, II International Bioherbicide Workshop: "Bioherbicides~Applying the Temperate Experience to the Tropics," July 31-Aug. 1, 1993, MacDonald College of McGill University, Quebec. Schisler, D. A., Jackson, M. A., & Bothast, R. J. (1991). Influence of nutrition during conidiation of Colletotrichum truncatum on conidial germination and efficacy in inciting disease in Sesbania exaltata. Phytopathology, 81,458-461. Schisler, D. A., Jackson, M. A., McGuire, M. R., & Bothast, R. J. (1995). Use of pregelatinized starch and casamino acids to improve the efficacy of Colletotrichum truncatum conidia produced in differing nutritional environments. In "Proceedings of the VIII International Symposium on Biological Control of Weeds, Feb. 2-7, 1992, Canterbury, New Zealand" (E. S. Delfosse and R. R. Scott, Eds.), pp. 659-664. DSIR/CSIRO, Melbourne. Schubiger, F. X., D6fago, G., Sedlar, L., & Kern, H. (1985). Host range of the haplontic phase of Uromyces rumicis. In "Proceedings of the VI International Symposium on Biological Control of Weeds, Vancouver, Aug. 19-25, 1984" (E. S. Delfosse, Ed.), pp. 653-659. Agriculture Canada, Ottawa.

Chapter 35

Use of Plant Pathogens in Weed Control

Shabana, Y. M., Charudattan, R., DeValerio, J. T., & Elwakil, M. A. (1997). An evaluation of hydrophilic polymers for formulating the bioherbicide agents Alternaria cassiae and A. eichhorniae. Weed Technology, 11, 212- 220. Shamoun, S. F., & Hintz, W. E. (1998). Development and registration of Chondrostereum purpureum as a mycoherbicide for hardwood weeds in conifer reforestation sites and utilities rights-of-way. "IV International Bioherbicide Workshop Programme and Abstracts, 6-7 Aug., 1998," p. 14. Univ. of Strathclyde, Glasgow, Scotland. Skipper, H. D., Ogg, A. G., Jr., & Kennedy, A. C. (1996). Root biology of grasses and ecology of rhizobacteria for biological control. Weed Technology, 10, 610-620. Smith, R. J. (1982). Integration of microbial herbicides with existing pest management programs. In "Biological Control of Weeds with Plant Pathogens" (R. Charudattan & H. L. Walker, Eds.), p. 189. Wiley, New York. Smith, R. J., Jr. (1986). Biological control of northern jointvetch in rice and soybeansmA researcher's view. Weed Science, 34 (Suppl. 1), 17-23. Smith, R. J., Jr. (1991) Integration of biological control agents with chemical pesticides. In "Microbial Control of Weeds" (D. O. TeBeest, Ed.), pp. 189-208. Chapman & Hall, New York. Smither-Kopperl, M. L., Charudattan, R., & Berger, R. D. (1998). Dispersal of spores of Fusarium culmorum in aquatic system. Phytopathology, 88, 382-388. Souissi, T., & Kremer, R. J. (1994). Leafy spurge (Euphorbia escula) cell cultures for screening deleterious rhizobacteria. Weed Science, 42, 310-315. Sparace, S. A., Wymore, L. A., Menassa, R., & Watson, A. K. (1991). Effects of the Phomopsis convolvulus conidial matrix on conidia germination and the leaf anthracnose disease of field bindweed (Convolvulus arvensis). Plant Disease, 75, 1175-1179. Stevens, P. J. G. (1994). Silwet L-77 organosilicone surfactant to maximize infection of weeds with pathogens. Regional Research Project $234 Annual Meeting. Stowell, L. J. (1991). Submerged fermentation of biological herbicides. In "Microbial Control of Weeds" (D. O. TeBeest, Ed.), pp. 225-261. Chapman & Hall, New York. Stubbs, T. L., & Kennedy, A. C. (1993). Effect of bacterial and chemical stresses in biological weed control systems. Agronomy Abstracts, 57, 261. Supkoff, D. M., Joley, D. B., & Marois, J. J. (1988). Effect of introduced biological control organisms on the density of Chondrilla juncea in California. Journal of Applied Ecology, 25, 1089-1095. TeBeest, D. O., & Templeton, G. E. (1985). Mycoherbicides: Progress in the biological control of weeds. Plant Disease, 69, 6-10. Tomley, A. J. (1989). The biological control program for Cryptostegia grandiflora in Australia. In "Proceedings of the VII International Symposium on Biological Control of Weeds" (E. S. Delfosse, Ed.), pp. 685-688. Ist. Sper. Patol. Veg. (MAF). Trujillo, E. E. (1985). Biological control of hamakua pa-makani with Cercosporella sp. in Hawaii. In "Proceedings of the VI International Symposium on Biological Control of Weeds, Vancouver, Aug. 19-25, 1984" (E. S. Delfosse, Ed.), pp. 661-671. Agriculture Canada, Ottawa. Trujillo, E. E., Aragaki, M., & Shoemaker, R. A. (1988). Infection, disease development, and axenic cultures of Entyloma compositarum, the cause of hamakua pamakani blight in Hawaii. Plant Disease, 72, 355357. Tsukamoto, H. Gohbara, M., Tsuda, M., & Fujimori, T. (1997). Evaluation of fungal pathogens as biological control agents for the paddy weed, Echinochloa species by drop inoculation. Annals of the Phytopathological Society of Japan, 63, 366-372.

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Tuat, N. A., Trung, H. A. M., Hetherington, S. D., & Auld, B. A. (1998). Potential bioherbicide for Echinochloa in Vietnam. Abstracts, IV International Bioherbicide Workshop, Univ. of Strathclyde, Glasgow, Scotland. Turgeon, G., & Yoder, O. C. (1985). Genetically engineered fungi for weed control. In "Biotechnology: Applications and Research" (P. N. Cheremisinoff & R. P. Ouellette, Eds.), pp. 221-230. Technomic, Lancaster, PA. Vogelgsang, S., Watson, A. K., & Hurle, K. (1994). The efficacy of Phomopsis convolvulus against field bindweed (Convolvulus arvensis) applied as a preemergence bioherbicide. Zeitschrift fuer Pflanzenkrankheiten Pflanzenschutz, 14, 253- 260. Walker, H. L. (1980). Alternaria macrospora as a potential biocontrol agent for spurred anoda: Production of spores for field studies. Advances in Agricultural Technology, AAT-S-12. USDA-SEA-AR, New Orleans, LA. Walker, H. L., & Boyette, C. D. (1985). Biocontrol of sicklepod (Cassia obtusifolia) in soybeans (Glycine max) with Alternaria cassiae. Weed Science, 33, 212-215. Walton, D. (1996). Host-selective toxins: Agents of compatibility. Plant Cell, 8, 1723-1733. Wapshere, A. J. (1974). A strategy for evaluating the safety of organisms for biological weed control. Annals of Applied Biology, 77, 201-211. Watson, A. K. (1986a). Biology of Subanguina picridis, a potential biological control agent of Russian knapweed. Journal of Nematology, 18, 149-154. Watson, A. K. (1986b). Host range of, and plant reaction to, Subanguina picridis. Journal of Nematology, 18, 112-120. Watson, A. K. (1991). The classical approach with plant pathogens. In "Microbial Control of Weeds" (D. O. TeBeest, Ed.), pp. 3-23. Chapman & Hall, New York. Watson, A. K., & Alkhoury, I. (1981). Response of safflower cultivars to Puccinia jaceae collected from diffuse knapweed in eastern Europe. In "Proceedings of the V International Symposium on Biological Control of Weeds, Brisbane, July 22-27, 1980" (E. S. Delfosse, Ed.), pp. 301- 305. CSIRO, Melbourne. Watson, A. K., & C16ment, M. (1986). Evaluation of rust fungi as biological control agents of weedy Centaurea in North America. Weed Science, 34 (Suppl. 1), 7-10. Watson, A. K., & Wymore, L. A. (1989). Biological control, a component of integrated weed management. In "Proceedings of the VII International Symposium on Biological Control of Weeds" (E. S. Delfosse, Ed.), pp. 101-106. Ist. Sper. Patol. Veg. (MAF). Watson, A. K., Schroeder, D., & Alkhoury, I. (1981). Collection of Puccinia species from diffuse knapweed in eastern Europe. Canadian Journal of Plant Pathology, 3, 6-8. Womack, J. G., & Burge, M. N. (1993). Mycoherbicide formulation and the potential for bracken control. Pesticide Science, 37, 337-341. Womack, J. G., Eccleston, G. M., & Burge, M. N. (1996). A vegetable oil-based invert emulsion for mycoherbicide delivery. Biological Control, 6, 23- 28. Wyse, D. L. (1992). Future of weed science research. Weed Technology, 6, 162-165. Wyss, G. S., & Mtiller-Sch~rer, H. (1998). Puccinia lagenophorae as a classical biocontrol agent for common groundsel (Senecio vulgaris) in the United States? Phytopathology, 88 (Suppl.), $99. Yang, S., & Schaad, N. W. (1996). Combined non- or low-virulent pathogens and special formulated carriers as broad-spectrum bioherbicides. "Biological Control of Weeds, IX International Symposium, 19-26 January 1996, Stellenbosch, South Africa" (V. C. Moran & J. H. Hoffmann, Eds.), p. 482 (Abstract). Univ. of Cape Town, Cape Town, South Africa. m

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ochloa species in rice (Oryza satira) to indigenous pathogenic fungi. Plant Disease, 80, 1053-1058. Zidack, N. K., & Backman, P. A. (1996). Biological control of kudzu (Pueraria lobata) with the plant pathogen Pseudomonas syringae pv. phaseolicola. Weed Science, 44, 645-649. Zidack, N. K., Backman, P. A., & Shaw, J. J. (1992). Promotion of bacterial infection of leaves by an organosilicone surfactant: Implication for biological weed control. Biological Control, 2, 111-117.

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I36I Biological Control of Insects in Urban Environments D. L. DAHLSTEN

R. W. HALL

Center for Biological Control University of California Berkeley, California

Department of Entomology Ohio State University Columbus, Ohio

INTRODUCTION

environments. Ebeling's (1975) book on urban entomology excluded pests of ornamental plants except for a treatment of house plant pests. The main emphasis was on structural, stored product, food, fabric and paper, veterinary, and vertebrate (rats and mice) pests. There is also a chapter on entomophobia, the cause for many calls to the pest control operator or urban pest manager. Emphasis on developing ecological approaches for urban insect pests has been with urban plant pests. Frankie and Ehler (1978) cited a dearth of ecological studies in urban environments. Olkowski et al. (1976, 1978)attempted to establish an ecological framework for control of urban tree pests. Three books (Frankie & Koehler, 1978, 1983; Bennett & Owens, 1986) have been published since Ebeling's 1975 work dealing with various aspects of urban entomology and urban pest management. The field of urban pest management can be divided into seven areas: medical, psychological, architectural, agricultural, floricultural, silvicultural, and horticultural (Olkowski et al., 1978). Several of these areas are treated in other sections of this volume. Medical and veterinary problems are traditionally dealt with by medical entomologists. We discuss biological control of cockroaches as an example of the diversity of insect pest problems in the urban environment. Also, the Mackinac Island outbreak of scale insects because of spraying for flies is a special example of a secondary outbreak due to disruption of natural enemies in an urban environment. Architectural pests include structural, fabric, paper, and other household pests. Little has been done on the biological control of these organisms. Agriculture and forest pests occur in urban environments and most of these are included in other chapters in this

The urban environment is perhaps the most complex with which the pest manager must deal. Although the pest categories--vertebrate, weed, pathogen, and arthropod-are the same as in agriculture, the habitat is extremely diverse and discontinuous. The urban environment provides special opportunities for pests and for pest control and specifically biological control. The management goals in the urban environment are almost impossible to define because of the subjectivity involved in determining economic value of aesthetic or nuisance pests. Although the principles of biology and ecology pertain to the diverse, human-structured environment, the diffuse management and economic goals have made it difficult for pest managers to apply ecological concepts to control problems in urban environments. Therefore, it is difficult to apply modem pest management philosophy to the urban environment. Urban pest management has only recently adopted (in the past 15 years) integrated pest management approaches. This is due in large part to the public's increased concern for pesticides in the environment. Because economic values are not easily defined, individuals either did nothing or contracted with pest control operators to apply prophylactic treatments on a yearly or quarterly basis. Since the 1940s, most pest control in urban environments has been essentially chemical. From 5.3 to 10.6 pounds of pesticide per acre are applied to urban gardens and lawns (National Research Council, 1980). These rates are higher than the average for agriculture or other managed lands. Because the fields of urban entomology and urban pest management are just beginning to develop, entomology departments have begun to hire specialists on insects in urban

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D.L. Dahlsten and 1~ W. Hall

volume. Urban forestry is developing rapidly and perhaps trees will be harvested for commercial timber in urban environments in the future. This would drastically change the management goals for urban trees and possibly pest management practices. Agricultural pests can become pests on backyard ornamental and fruit trees. For example, cottony cushion scale, Icerya purchasi Maskell, infests Citrus spp., Pittosporum spp., and Acacia spp. Biological control successes on ornamentals are often offshoots of biological control successes in nearby agriculture. Floriculture includes house plants and plants used for cut flowers. Biological control is gaining credibility as a highly useful tool in integrated control programs directed against certain pests in commercial glasshouses (see Chapter 31). However, there are few examples of biological control of pests of flowers in urban plantings. Most examples discussed herein fall into the ornamental horticulture area, which includes trees and other plants used in landscaping in yards, parks, cemeteries, botanical gardens, turf areas, streets, and highway right-of-ways. Finally, urban pest management also involves psychology. Entomophobia is a human problem rather than a pest problem. Education, rather than biological control, is an important step in eliminating entomophobia.

ECOLOGICAL ATTRIBUTES OF URBAN O U T D O O R ENVIRONMENTS The urban arthropod fauna is rich and diverse (Frankie & Ehler, 1978). One striking example comes from a small suburban yard near New York City where 1402 insect species were collected over several years (Lutz, 1941). Urbanization has provided unique opportunities for insects to exploit, which include construction of buildings, maintenance of environmental conditions favorable to year-round insect growth and development, storage of food products, generation of solid and liquid wastes, and planting of host plants. Since most of the biological control successes have been with outdoor plants, we focus on what humans have done to alter urban habitats with plants and how this influences the potential for biological control in urban environments. Frankie and Ehler (1978) conclude that arthropod communities in urban environments are similar to those in natural environments. However, there are a number of human influences that affect the distribution and abundance of arthropods in urban environments. One factor that complicates urban pest management is the size of the area managed, which may range from a backyard garden with one or two fruit trees to miles of highway fight-of-way planted with ground cover. The pest manager is confronted with a diverse habitat and clientele with multiple goals. It is difficult to organize diverse programs without involving public

agencies that take an interest in specific problems such as a department of transportation with roadside plants, a local tree commission, or a user group concerned with a particular habitat type such as turf grass. This may also explain why a number of the biological control examples were first tried or were a success in agricultural or forest environments before being used in urban areas. The native and introduced flora in urban environments is dramatically diverse. For example, there are 132 tree, 147 shrub, and 53 ground cover or vine species in Austin, Texas (Frankie & Ehler, 1978). In Berkeley, California, 10 tree species constituted the native tree flora; now 123 tree species exist in Berkeley (Olkowski, 1974; Frankie & Ehler, 1978) and there are nearly 300 species on the Berkeley campus of the University of California (Cockrell & Warnke, 1976). There is tremendous variability in the number of species, depending on where cities or towns are located. One example is the Siberian and English elms that were planted in many small towns and ranches in northeastern California, creating small islands of elms separated by 15-40 km. Two other examples are given by McBride and Jacobs (1986), who contrasted two California cities, Menlo Park, with a presettlement oak forest, and South Lake Tahoe, with a presettlement Jeffrey pine forest. Urbanization resulted in a change of the number of tree species from 5 to 145 at Menlo Park and from 1 to 6 at South Lake Tahoe. These examples represent three very different ecological situations: an open grass-oak woodland in northeastern California where elms are planted, an oak savanna woodland in Menlo Park, and an urban center in a large contiguous forest in South Lake Tahoe. The areas surrounding cities, either as natural ecosystems or as large areas of agricultural development, are extremely important to the type of insect problems that might be anticipated on the cities' trees. The physical environment within cities influences development, distribution, and abundance of insects and their natural enemies. Buildings and other structures such as fences can restrict movement or create wind fields and may also provide insect refuges. Buildings and paved areas such as streets, sidewalks, and parking lots can influence the ambient temperature. Runoff from rain is also increased in paved areas. Thus, in addition to modifying existing habitats, urbanization has also formed new ones.

POTENTIAL FOR URBAN BIOLOGICAL CONTROL Until recently, there has been little incentive for biological control projects in urban environments. However, public concerns about chemical pollutants in air and water may limit urban pesticide applications and provide incentives for initiation of urban biological control programs (Dahlsten et al., 1985).

Chapter 36 BiologicalControl of Insects in Urban Environments Most exotic pest introductions occur in the discontinuous, diverse urban environment, with many species of exotic plants (Dahlsten, 1986). Thus, urban environments may be well suited to the classical biological control importation approach. Augmentation through inoculative releases and relocation of natural enemies would also be a useful tactic for urban environments. Because of the potential for pesticide-induced disruption, plant diversity, multiple ownerships, and diverse objectives, conservation of natural enemies is as important or more so than in other environments. Many examples of successful biological control in urban environments are not well documented, but this lack of critical assessment is characteristic of most pest control tactics. Documentation, sound sampling and monitoring procedures, and quantification are as important in urban environments as they are in forestry and agriculture. Because of the diversity and the interrupted distribution of habitat type, the urban environment offers a unique opportunity for experimentation to address such questions in biological control as single vs multiple species introductions and predators vs parasites. A good example of this is provided in a series of studies evaluating three different strains of an egg parasitoid, Oomyzus gallerucae (Fonscolmbe) (Eulophidae), of the elm leaf beetle, Xantherogaleruca luteola (Mtiller), in northeastern California (Clair et al., 1987, 1988). Generally, the urban environment has received little attention with respect to classical biological control. The National Research Council (1980) reports 70 species of natural enemies released against 15 urban pests (excluding agricultural, medical/veterinary, forest, and greenhouse pests that also occur in urban environments), with an establishment rate of 34.3%. This is compared to 915 species of parasitoids and predators released against 106 agricultural, medical/veterinary, forest, and greenhouse pests, with an establishment rate of 29.4%. The determination of "success" is difficult (see Chapter 40), but most classical biological control successes in the urban environment have been against scale insects on perennial plants. This is true in agriculture as well (Flanders, 1986). Some degree of success has been reported for classical biological control with natural enemies against 43 urban and ornamental pests (Table 1). The importance of naturally occurring biological control should not be underestimated (Hagen et al., 1971). Often the importance of biological control agents is not realized until they are disrupted. Such was the case with the pine needle scale (Chionaspis pinifoliae [Fitch]) at South Lake Tahoe (discussed later). In other cases, the documentation of the importance of natural enemies was fortuitous. Such was the case with the elm spanworm, Ennomos subsignarius (Htibner), in Connecticut. The elm spanworm is occasionally a serious defoliator in the eastern hardwood forests. Like the gypsy moth, it is also a pest of shade trees in towns and cities and therefore an urban pest. Kaya and Anderson (1974) documented the importance of an undes-

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cribed encrytid egg parasitoid, Ooencyrtus sp., in the collapse of elm spanworm populations in the woodlands and towns of southwestern Connecticut. Shade tree pests may be the most fruitful area for biological control in the future. With the rapidly expanding concept of the urban forest, it may be possible to organize larger programs and generate public support for biological control attempts. The urban forest is loosely defined as trees as well as other vegetation growing in close association with people (Kielbaso & Kennedy, 1983). The amount of money spent on tree care programs in the United States is substantial, and in 1980 it amounted to $2.19 per capita or $10.78 per tree (Kielbaso & Kennedy, 1983). The value of street trees in 1974 in the United States was conservatively valued at $15 billion. The economic incentive appears present for the development of strong programs in biological control. Certain problems could be focused on regionally or nationally. Although many trees are planted in the urban environment, there has been a tendency to develop monocultures and there is concern over the low diversity of urban forest trees (Kielbaso & Kennedy, 1983). Six of the ten most important urban forest pests nationally are defoliators and the top two pests are aphids and scale insects (Kielbaso & Kennedy, 1983). The focus of developing biological control programs in the urban forests has therefore been on defoliators and homopterans (Olkowski et al., 1978; Dahlsten et al., 1985). Many of the examples given herein are for problems on woody plants or trees, either native or introduced. The trees may be part of the forest into which the towns have encroached, such as with the elm spanworm in the eastern hardwood forest or the pine needle scale in the western coniferous forest. In other cases, fruit or forest trees are planted and pests of agriculture or forestry become urban ornamental pests, such as the woolly whitefly, Aleurothrixus floccosus (Maskell), on citrus and the Nantucket pine tip moth, Rhyacionia frustana (Comstock), on pine in southern California. The brief case histories are examples of classical biological control, augmentation, and naturally occurring biological control. Although precise documentation is lacking in many cases, the available evidence strongly suggests that persistent, well-funded research on the use of natural enemies to control plant pests in the outdoor urban environment may lead to more successes.

BIOLOGICAL CONTROL CASE HISTORIES Blattaria: Blattidae a n d Blattellidae ( C o c k r o a c h e s ) Cockroaches are among the most important pests in urban environments (Ebeling, 1975). Most of the cockroaches that are household and structural pests in temperate regions are tropical or subtropical in origin and because they are

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D.L. Dahlsten and R. W. Hall TABLE 1

Pests Found in Urban Areas for Which S o m e Success Has Been Reported for Introduced Natural Enemies in Urban or Unspecified (*) Environments

Pest

C o m m o n name

Location

Some urban or ornamental success reported (reference)

Blattaria Periplaneta americana Periplaneta australasiae Supella longipalpa

American cockroach Australian cockroach Brownbanded cockroach

Hawaii Hawaii U.S.

DeBach, 1964; Luck, 1981 DeBach, 1964; Luck, 1981 Slater, 1984

Dermaptera Forficula auricularia

European earwig

Canada

Turnbull & Chant, 1961

Thysanoptera Gynaikothrips ficorum

Cuban laurel thrips

Hawaii

Rao et al., 1971

Hemiptera Nezara viridula

Southern green stink bug

Australia, Hawaii

*Luck, 1981

Homoptera Acizzia uncatoides Trioza eugeniae Ctenarytaina eucalypti Aleurothrixus floccosus Antonina graminis Aonidiella aurantii Aonidiella citrina Asterodiaspis variolosum Asterolecanium pustulans Chloropulvinaria psidii Chromaphis juglandicola Coccus hesperidum Cornuaspis beckii Eucallipterus tiliae Icerya purchasi Lecanium corni Maconellicoccus hirsutus Myzocallis annulata Nipaecoccus nipae Nipaecoccus viridis Orthezia insignis Parasaisetia nigra Parlatoria oleae Planococcus citri Planococcus kenyae Pseudaulacaspis pentagona Pseudococcus comstocki Pseudococcus fragilis Pseudococcus longispinus Pulvinaria delottoi Pulvinariella mesembryanthemi Quadraspidiotus pe rniciosus Saisettia coffeae Saisettia oleae Siphoninus phillyreae Tinocalis plantani Trialeurodes vaporariorum

Acacia psyllid Eugenia psyllid Blue gum psyllid Woolly white fly Rhodesgrass mealybug California red scale Yellow scale Golden oak scale Bamboo (pustule) scale Green guava mealybug Walnut aphid Soft brown scale Purple scale Linden aphid Cottony cushion scale European fruit lecanium Hisbiscus mealybug Oak aphid Coconut mealybug Lebbeck mealybug Greenhouse orthezia Nigra scale Olive scale Citrus mealybug Coffee mealybug White peach scale Comstock mealybug Citrophilis mealybug Long-tailed mealybug Ice plant scale Ice plant scale San Jose scale Hemispherical scale Black scale Ash whitefly Elm aphid Greenhouse whitefly

U.S. U.S. U.S. U.S. U.S. U.S. U.S. Tasmania, New Zealand Puerto Rico Puerto Rico, Bermuda U.S. New Zealand, USSR U.S. U.S. U.S. British Columbia Egypt Tasmania, New Zealand Hawaii Hawaii, Egypt Kenya U.S. U.S. U.S., Chile Kenya Bermuda U.S. U.S. U.S., Bermuda, Israel U.S. U.S. U.S., Europe Chile U.S., Australia U.S. U.S. Australia, Tasmania

Pinnock et al., 1978; Dreistadt & Hagen, 1994 Dahlsten et al., 1995 Dahlsten et al., 1998a, 1998b DeBach & Rose, 1976, 1977 Dean et al., 1979 *Luck, 1981 *Luck, 1981 Wilson, 1960; Ferguson, 1989 DeBach, 1964 DeBach, 1964; Simmonds, 1969 van den Bosch et al., 1970 Saakian-Baranova, 1966 DeBach, 1964; DeBach & Rose, 1977 Olkowski et al., 1982a; Zuparko, 1983 Quezada & DeBach, 1973 DeBach, 1964 Clausen, 1978 *Luck, 1981; Walker, 1989 *Luck, 1981 DeBach, 1964; Laing & Hamai, 1976 DeBach 1964 Flanders, 1959 DeBach, 1964 *Luck, 1981 *Luck, 1981 Bennett & Hughes, 1959 Meyerdirk et al., 1981 DeBach, 1964 *Luck, 1981 Frankie & Hagen, 1986 Frankie & Hagen, 1986 Sailer, 1972 Beingolea, 1969 *Luck, 1981 Bellows et al., 1992 Olkowski et al., 1982b *Luck, 1981

Coleoptera Adoretus sinicus Popillia japonica Xanthogaleruca luteola

Chinese rose beetle Japanese beetle Elm leaf beetle

Hawaii U.S. U.S.

Pemberton 1954 Fleming 1968 Luck & Scriven, 1976; Cranshaw et al., 1989

(continues)

Chapter 36

923

Biological Control of Insects in Urban Environments

TABLE 1 (continued) Pest

C o m m o n name

Location

Some urban or ornamental success reported (reference)

Lepidoptera

Cnidocampa flavescens Lithocolletis saniella Lymantria dispar Mygmia phaerorrhoea Operophtera brumata Rhyacionia frustrana Spodoptera mauritia acronyctoides Stilpnotia salicis

Oriental moth Oak leaf miner Gypsy moth Brown-tail moth Winter moth European pine shoot moth Lawn armyworm Stain moth

U.S. New Zealand U.S. U.S. Canada U.S. Hawaii U.S., Canada

DeBach, 1964; Laing & Hamai, 1976 Swan, 1973 DeBach, 1964 DeBach, 1964 Embree, 1971 Scriven & Luck, 1978 Clausen, 1978 Clausen, 1978

Holly leaf miner

Canada

Turnbull & Chant, 1961

Introduced pine sawfly

Canada

McGugan & Coppel, 1962

Diptera

Phytomyza ilicis Hymenoptera

Diprion similis

introduced, they seem to be ideal candidates for classical biological control. Cockroaches contaminate food, impart an unpleasant odor to residences, and may transmit disease. Also, some people are allergic to cockroaches and many exhibit reactions to whole-body extracts of cockroaches or cockroach feces (Ebeling, 1975). The major urban pest species in the United States include the German cockroach, Blatella germanica (Linnaeus), the American cockroach, Periplaneta americana (Linnaeus), the brownbanded cockroach, Supella longipalpa (Serville), the Oriental cockroach, Blatta orientalis Linnaeus, and the smokybrown cockroach, Periplaneta fuliginosa (Serville). Several authors have noted predation or parasitism of cockroaches (Ebeling, 1975), but little evidence exists to indicate that natural enemies can reduce or maintain cockroach densities beneath economic or aesthetic injury levels. However, the potential exists and there is need for serious consideration of the use of natural enemies for control of cockroach populations (Piper & Frankie, 1978). Hymenopteran egg parasitoids appear to offer the greatest potential for short- and long-term population regulation of cockroaches (Piper et al., 1978). Inundative releases have enormous potential for control of indoor and outdoor cockroach populations (Piper & Frankie, 1978). However, use of such techniques requires a knowledge of the patterns of distribution and abundance of the pest species involved. A complicating factor in use of natural enemies for cockroach control is that not all urbanites will be amenable to indoor parasitoid releases (Piper & Frankie, 1978). In fact, Edmunds (1957) noted that one family was more disturbed by the cockroach parasitoids in their home than by the infestation of Oriental cockroaches. Pemberton (1948) noted that two species of exotic ampulicid wasps, Ampulex compressa (Fabricius) and Dolicurus stantoni (Ashmead), played a significant role in control-

ling some species of cockroaches in Hawaii. The cockroach egg parasitoid Comperia merceti (Compere) has potential for use in urban cockroach biological control. Comperia merceti appears to have a substantial impact on brownbanded cockroach when densities of oothecae are high (Coler et al., 1984). At lower densities, parasitism rates are low. Thus, at such densities, inoculative or inundative releases may be necessary to achieve satisfactory levels of control. The use of C. merceti for brownbanded cockroach control has enjoyed great success at the University of California, Berkeley (Slater, 1984). Slater et al. (1980) note that in an institutional setting, workers were willing to tolerate C. merceti. Another species of egg parasitoid, Aprostocetus hagenowii (Ratzeburg), is thought to be an important natural enemy of cockroaches (Cameron, 1955). When released into a room with high densities of American cockroach oothecae, A. hagenowii parasitized 83% of the oothecae (Roth & Willis, 1954). Fleet and Frankie (1975) and Piper et al. (1978) found significant mortality of oothecae of American and smokybrown cockroaches due to parasitism by A. hagenowii.

D e r m a p t e r a : E u r o p e a n Earwig (For~cula auricularia Linnaeus) The European earwig is a nuisance in close proximity to homes and gardens. It feeds on fruits, vegetables, and flowering plants and may enter houses. Introductions of Bigonicheta spinipennis (Meigen) (Diptera: Tachinidae) were made in British Columbia from the United States (this material was originally from Europe). Bigonicheta spinipennis became established and contributed to mortality of the earwig. Turnbull and Chant (1961) rated this program as a

924

D.L. Dahlsten and !~ W. Hall

success. However, complete biological control of European earwig may be undesirable as it has value as a predator, consuming large numbers of aphids and scale insects (Clausen, 1978).

T h y s a n o p t e r a : C u b a n Laurel Thrips

( Gynaikothrips ficorum Marchal) Cuban laurel thrips infested Ficus retusa Linnaeus and Ficus benjamina Linnaeus in Hawaii and feeding by the thrips caused a heavy drop of young foliage. In addition, biting and swarming of the thrips made it a public nuisance (Rao et al., 1971). The anthocorid predator Montandoniola moraguesi Puton was introduced into Hawaii from the Philippines in 1964. The predator became established on Oahu and to date has been important in suppressing the thrips (Rao et al., 1971).

Homoptera

The Eugenia Psyllid (Trioza eugeniae Froggat) The eugenia psyllid was introduced into Califomia from Australia and was first observed in May of 1988 in Inglewood, which is near Los Angeles. It is a pest of eugenia (also called Australian brush cherry or lillypilly), Syzygium paniculatum, a widely planted ornamental shrub or small tree, oftentimes used as a hedge in the coastal counties of Califomia. The psyllid spread to neighboring counties by the end of 1988 and was a pest in northern California by 1989. Monitoring procedures were developed that were effective for both the psyllid and its primary parasitoid, a eulophid, Tamarixia n. sp., that was introduced from Australia in 1992 (Dahlsten et al., 1995). Initial results were spectacular but psyllid populations became fairly abundant again in 1996 and 1997, particularly in cool regions such as San Francisco. Although the parasitoid is very effective in most regions of the state, it appears that the psyllid populations become very abundant in some cool areas, but even in these areas populations are much lower than they were prior to the release of Tamarixia.

Psyllidae: The Acacia Psyllid (Acizzia uncatoides (Ferris & Klyver)) The acacia psyllid project is an example of a successful classical biological pest control project in roadside plantings. The psyllid was first found in California in 1955 and by 1971 became so abundant on the acacias along some highways that the California Department of Transportation contracted with the Division of Biological Control, University of California, Berkeley, for assistance (Pinnock et al., 1978). This led to exploration for natural enemies in Victoria, Australia, the native home of many acacias and apparently the acacia psyllid. Five predacious and two parasitoid species were initially collected and imported from 1972 to 1975, but only the predators were released and of these, only Diomus pumilio Weise was recovered (Pinnock et al., 1978). A subsequent study confirmed that D. pumilio was the only purposely introduced species established, but the most numerous predator attacking the psyllid was an unintentionally introduced species, Anthocoris nemoralis (Fabricius) (Dreistadt & Hagen, 1994). These researchers found that the combination of both introduced species provided acceptable biological control of the psyllid in the San Francisco Bay area. One interesting aspect of this project is that an exotic coccinellid species, Harmonia conformis (Boisduval), which failed to become established in California, successfully brought the acacia psyllid under control in koa tree forests when sent from Califomia to Hawaii (Pinnock et al., 1978). Diomus pumilio, which did so well in California, did not control the psyllid when introduced into Hawaii. This is a good example of matching a natural enemy to its hosts in different habitats.

The Blue Gum Psyllid (Ctenarytaina

eucalypti (Maskell)) The blue gum psyllid, native to Australia, was first discovered in North America in January of 1991 in Monterey County, California (Dahlsten et al., 1998a). The psyllid feeds on several species of Eucalyptus and in particular those with waxy blue foliage such as E. cinerea, E. glaucescens, E. viminalis, E. pulverulenta, and E. globulus. It was found on E. pulverulenta, which has waxy blue foliage on the mature as well as the juvenile leaves, and this species is known as silver-leaved mountain gum or baby blue gum in the foliage industry in California. Tasmanian blue gum, E. globulus, is planted as an ornamental throughout California and is a prominent feature of the landscape in the state, having been planted and distributed widely in California over 100 years ago (Dahlsten, 1996). Eucalyptus globulus has waxy blue foliage only on the juvenile leaves and new shoots and foliage, which, when heavily infested by the psyllid, may cause homeowners concern because of growth loss, honeydew, sooty mold, and waxy secretions from nymphs. The main concern was with growers producing E. pulverulenta, which accounted for $2.3 billion in sales in 1996 in California (Dahlsten et al., 1998b). Blue gum psyllid populations exploded and by the end of 1992 could be found everywhere in the state on E. globulus and E. pulverulenta. The Eucalyptus Growers Association raised money to finance a biological control program with the University of California Center for Biological Control in Berkeley. A single species of primary parasitoid, Psyllaephagous pilosus Noyes (Hymenoptera:

Chapter 36 BiologicalControl of Insects in Urban Environments Eucrytidae), was found in late 1991 in Southern Australia and in New Zealand and sent to the University of California quarantine facility in Albany, California. Six species of secondary or hyperparasitoids were reared in quarantine in low numbers. In the spring and summer of 1993, approximately 7000 parasitoids were released at eight locations in California from Alameda County in the north (San Francisco Bay Area) to San Diego County in the south. The parasitoids spread as rapidly as the psyllids had done earlier. Psyllid populations declined at most sites in 1993, and in 1994 the blue gum psyllid was no longer a problem (Dahlsten et al., 1998a). This highly successful biological control program has eliminated the need for chemical sprays for the psyllid in the E. pulverulenta plantations in California and has resulted in a benefit-cost ratio ranging from at least 9:1 to 24:1 based solely on the reduction of insecticide treatments (Dahlsten et al., 1998b).

Aleyrodidae: Woolly Whitefly (Aleurothrixus floccosus (Maskell)) The origin of the woolly whitefly is uncertain but it is widely distributed in the West Indies and in Central and South America (Clausen, 1978). It is a pest primarily of citrus. A platygasterid, Amitus spiniferus (Brethes), and two aphelinids, Eretmocerus paulistis Heimpel and Cales noacki De Santis, have been used successfully as biological control agents in Chile, Mexico, and France (Luck, 1981). In San Diego, California, citrus is planted as a garden and ornamental tree. The woolly whitefly was first discovered there in 1966 (DeBach & Rose, 1976). DeBach had observed the whitefly to be under good control in mainland Mexico and A. spiniferus, E. paulistis, and an Encarsia sp. were introduced in small numbers in San Diego in 1967 (DeBach & Rose, 1976). The first two parasitoids became well established and showed promise as biological control agents. In 1969, the California Department of Food and Agriculture decided to eradicate the whitefly with chemical insecticides. The biological control program was therefore halted in San Diego and shifted to Baja California Norte in Mexico, where the whitefly was also found shortly after its discovery in San Diego (DeBach & Rose, 1976). Thirty A. spiniferus and 169 E. paulistis were colonized in Tijuana in 1969. Two of the original colonized trees were used as nursery trees. In one year, by transferring twigs with parasitized whitefly, more than 27,000 of the two parasitoids were distributed around Tijuana (DeBach & Rose, 1976). A fourth parasitoid, C. noacki, from Chile was also released. By late 1970, these three parasitoids were well established and it appeared that the biological control program was a success. In San Diego, the biological control program was re-

925

sumed in 1971 when the failed eradication project was abandoned (DeBach & Rose, 1976). The area infested with woolly whitefly in California was about 200 square miles. The University of California at Riverside and the California Department of Food and Agriculture cooperated in releasing the parasitoids that were collected in Tijuana or imported from mainland Mexico, Chile, and Brazil. Parasitoids were colonized at all release sites in San Diego in 1971 and these sites provided nursery trees for further parasitoid releases in 1972. The woolly whitefly continued to increase in California but by 1973 the biological control program was a success in San Diego County and Tijuana (DeBach & Rose, 1976). In 1973, the Japanese beetle (Popillia japonica Newman) was found unexpectedly in San Diego and an eradication zone of about 100 city blocks was established. A study was set up to investigate the effects on the woolly whitefly natural enemies of the three chemicals (carbaryl, chlordane, and dicofol) that were to be used for the beetle eradication program (DeBach & Rose, 1977). Dicofol was used for mite control because of disruption caused by eradication treatments. In this study it was shown that the eradication efforts against the Japanese beetle disrupted the biological control of the woolly whitefly. Before the chemical treatments began the two whitefly parasitoids A. spiniferus and C. noacki were generally distributed and other citrus pests were also under good biological control. After treatment woolly whitefly populations increased dramatically and were up to 1200 times higher in treated areas than in untreated areas. Populations of citrus red mite, Panonychus citri (McGregor), and purple scale, Cornuapis (--Lepidosaphes) beckii (Newman), also increased (DeBach & Rose, 1977). After the eradication treatments ended, A. spiniferus and C. noacki began to return to the previously treated areas. The side effects of eradication programs have not been well documented. This is partly because most of these programs are in urban environments. Eradication projects employing broad-spectrum insecticides provide a unique opportunity to study biological control in urban environments. The 1980-1982 Mediterranean fruit fly, Ceratitis capitata (Wiedemann), eradication program employing malathion bait spray in northern California resulted in disruption of biological control of various insects in an urban area (Dreistadt & Dahlsten, 1986). Gardens in treated areas had more mites, aphids, and whiteflies than gardens in unsprayed areas (Troetschler, 1983). Decreased control of other insects in urban areas such as the walnut aphid, Chromaphis juglandicola (Kaltenbach), and black scale, Saissetia oleae (Bernard), was also attributed to the effects of the bait spray on their natural enemies (Ehler & Endicott, 1984). In another study, parasitoids of iris whitefly, Aleyrodes spiraeoides Quaintance, were significantly more susceptible to

926

D.L. Dahlsten and I~ W. Hall

malathion bait spray than were the whiteflies and parasitism was significantly lower on plants in the sprayed areas (Hoelmer & Dahlsten, 1993).

Ash Whitefly (Siphoninus phillyreae (Haliday)) The discovery of the Old World ash whitefly in California in 1988 led to the prompt inception of a biological control program. Foreign exploration was carried out in 1989 and 1990, leading to the successful importation and release of two species, Encarsia inaron (Walker) (= partenopea Masi) (Hymenoptera: Aphelinidae) and Clitostethus arcuatus Rossi (Coleoptera: Coccinellidae) (Bellows et al., 1992). Although both species became established, the aphelinid colonized a greater area and thus received greater attention (Bellows et al., 1992). Subsequent life-table analyses of field sites documented that E. inaron was playing a key role in the reduction of S. phillyreae populations (Gould et al., 1992a, 1992b). By 1992, whitefly populations had been reduced by the wasp to undetectable levels. The loss of aesthetic benefits due to ash whitefly damage was analyzed, and the total benefits of the biological control program ranged from $324 million at wholesale values to $412 million at retail. The direct cost of the program was around $1.2 million. The benefit to cost ratios were 270:1 and 344:1, respectively (Jetter et al., 1997).

Aphididae and Drepanosiphidae: Oak Aphid (MyzocaUis annulata (Hartig)) In Australia, the oak aphid causes damage to oaks (Quercus spp.) in Victoria and Tasmania. Aphelinus subflavescens (Westwood) (= flavus Nees) was imported from England and released in 1939. Shortly thereafter, A. subflavescens from an unknown source was recovered in Australia and Tasmania. Parasitism was heavy in Tasmania and the health of the oaks gradually improved (Wilson, 1960). The parasitoid was also introduced into New Zealand in 1939, although there was evidence that it had already been unintentionally imported (Walker, 1989). Here the aphid is considered strictly an aesthetic pest and has not been of any apparent importance since the establishment of A. subflavescens was documented, although no detailed studies have been published.

The linden aphid is common in Europe and has spread across the United States and Canada since its discovery in Washington, D.C., in 1886 (Olkowski et al., 1982a). In 1970, several species were introduced in Berkeley, but only Trioxys curvicaudus Mackauer became established (O1kowski et al., 1982a); it was subsequently established in San Jose, California (Zuparko, 1983). Since aphid populations, honeydew, and citizen complaints were reduced, this project was considered a biological control success (O1kowski et al., 1982a). However, this judgment may not be valid. Populations of the aphid were low in 1971, with 40% parasitization, but in 1972, aphid populations were higher, with parasitism fluctuating between 20 and 50%; populations were not sampled again until 1978, when parasitism did not exceed 30%, and about half of the aphid mummies yielded hyperparasitoids (Olkowski et al., 1982a). Additional research from 1991 to 1994 found that aphid populations and parasitism rates varied tremendously between different sites in the San Francisco Bay area (Zuparko & Dahlsten, 1995). Analysis of these results reveals the importance of host plant resistance against the linden aphid, with lower aphid populations correlated with linden species with relatively denser leaf pubescence that have T. curvicaudus present (Zuparko & Dahlsten, 1994). Although host plant resistance is considered to be the more important factor in limiting aphid populations, the parasitoid contributes a significant mortality factor and thus may be considered a partial biological control success. The controversy over the success of this program illustrates the importance of careful quantitative documentation of the release and efficacy of natural enemies. The elm aphid is monophagous on elms. It is known from Europe and Russia and has been introduced into western North America (Richards, 1967). In Berkeley the aphid reaches high densities and its honeydew creates a nuisance. Chemical insecticides were commonly used from 1945 to 1971, although with decreasing effectiveness (Olkowski et al., 1982b). In 1972, two parasitoids, Trioxys hortorum Stary and T. tenuicaudus Stary, were introduced from Czechoslovakia. Trioxys tenuicaudus became established and spread very slowly. Resident complaints of honeydew beneath elms diminished and this project was reported to be a successful classical biological control project (O1kowski et al., 1982b).

Linden and Elm Aphids (Eucallipterus tiliae Linnaeus and TinocaUis platani (Kaltenbach))

Diaspididae

Both lindens and elms are planted as street trees, and the linden aphid, E. tiliae, and elm aphid, T. platani, have been the targets of urban biological control projects in northern California.

The pine needle scale is a native insect with many coniferous hosts. The outbreak of this scale in 1968 in South Lake Tahoe, California, provided an opportunity to document the importance of naturally occurring biological con-

Pine Needle Scale (Chionaspis pinifoliae (Fitch))

Chapter 36

Biological Control of Insects in Urban Environments

trol in an urban environment. The city of South Lake Tahoe has encroached into the natural westside Sierra forests and both lodgepole pine, Pinus contorta Douglas, and Jeffrey pine, P. jeffreyi Greville & Balfour, are common along the streets and in the yards of homes. The scale normally occurs in low numbers on both pine species but in 1968, populations erupted in areas that had been fogged with malathion for control of a mosquito, Culex tarsalis Coquillett. The fogging program was halted and the subsequent decline of the scale population was documented (Luck & Dahlsten, 1975). The scale was found to have a uniparental population on lodgepole pine and a biparental population on Jeffrey pine (Luck & Dahlsten, 1974). Not only was the biology of the scale different but the parasitoids varied depending on the host tree species of the scale. The two scale parasitoids on lodgepole pine were the aphelinids Physcus howardi Compere and Prospaltella bella Gahan. The parasitoid on scale on Jeffrey pine was Achrysocharis phenacapsia Yoshimoto (Eulophidae) (Luck & Dahlsten, 1974). Two coccinellid predators, Chilocorus orbus Casey and Cryptoweisia atronitens (Casey), were the dominant biotic mortality factors on both pine species along with parasitism by P. bella on lodgepole pine (Luck & Dahlsten, 1975). Other scales, Nuculaspis californica (Coleman), Pineus sp., Physokermes sp., and Matsucoccus sp., two species of mites, Oligonychus sp. and Brevipalpus sp., and an aphid, Schizolachnus sp., were found to be very abundant in the fogged area as well (Dahlsten et al., 1969).

White Peach Scale (Pseudaulacaspis pentagona (Targ.)) The white peach scale was introduced into Bermuda in 1917. By 1920, the scale threatened oleander (Nerium oleander Linnaeus) with extinction (Bennett & Hughes, 1959). Several species of natural enemies were imported from Italy and the United States. Aphytis diaspidis (Howard) from Italy was an immediate success and brought P. pentagona under substantial control (Bennett & Hughes, 1959).

Asterolecaniidae

Golden Oak Scale (Asterodiaspis variolosa (Ratzeburg)) The golden oak scale is a pit-making species that became an important pest of oaks in New Zealand and Tasmania in the 1920s and in Australia in the 1930s. The principal problems were on the golden oak, Quercus pedunculata Ehr. Severely infested trees grow poorly and suffer dieback; young trees are sometimes killed (Johnson & Lyon, 1976). The parasitoid Habrolepis dalmanni (Westwood) (Encyrtidae) was introduced from the eastern United States into New Zealand in the 1920s. Later, H. dalmanni was introduced into Tasmania and Australia from New Zealand and

927

into Chile from the United States. Biological control was partially to substantially successful in Australia, Tasmania, and Chile (Clausen, 1978) and almost completely successful in New Zealand (Ferguson, 1989). Coecidae

European Fruit Lecanium (Lecanium corni (Bouch~)) In the 1970s the Lecanium corni (Bouchr) complex was causing serious injury to ornamental and fruit trees on Mackinac Island in Michigan. Trees with high L. corni population densities exhibited dieback and a decline in vigor. In addition, the trees, sidewalks, and park benches were aesthetically injured by honeydew deposition and growth of sooty mold. Merritt et al. (1983) attributed the scale infestation to destruction of natural enemies by weekly applications of dimethoate for fly control. When dimethoate treatments were reduced after initiation of an IPM program for flies, there was an immediate decline in L. corni densities. In the two years following the reduction in pesticide use, a dramatic decline in honeydew deposition was also noted (Merritt et al., 1983).

Green Guava Mealybug (Chloropulvinaria (=Pulvinaria) psidii (Maskell)) The green guava mealybug, also called the green shield scale, is a tropical species that is common in California, Southeast Asia, Hawaii, the West Indies, and Florida. It has a wide host list of tropical and subtropical plants; Ficus spp., guava, coffee, and oleander are favored hosts (Clausen, 1978). Following an increase of C. psidii on ornamentals in Bermuda, several species of natural enemies were introduced from Hawaii and California and four species became established (Bennett & Hughes, 1959). Microterys kotinskyi Fullaway (Encyrtidae) is thought to be important in control of the scale. Simmonds (1969) cited biological control of C. psidii as complete.

Ice Plant Scales (Pulvinariella mesembryanthemi (Vallot) and Pulvinaria delottoi Gill) Both of these ice plant scales originated in South Africa and attack plants in the families Aizoaceae and Crassulaceae. A scale was first detected in California in 1949 at the University of California Botanical Garden on ice plants, Carpobrotus spp., and several more reports of the scales were made in the Bay Area between 1949 and 1970 (Tassan et al., 1982). Ice plants are used widely in California as ornamental ground covers and the California Department of Transportation (Caltrans) alone maintains approximately 6000 acres of ice plants along highways (Frankie & Hagen, 1986). Pulvinariella mesembryanthemi has a wide distribution and has moved from its origin in South Africa to southern

928

D.L. Dahlsten and R. W. Hall

Europe along the Mediterranean, the Canary Islands, Germany, and several countries in South America. At present, P. delottoi has moved only into California (Frankie & Hagen, 1986). Under some circumstances the ice plants can become pests by encroaching on native vegetation and the scales could then be considered biological control agents. It was not until 1971 that dense populations of P. mesembryanthemi were discovered in Napa, California, damaging ice plants at private residences. In 1973, a survey of ice plants along highways in Alameda County was conducted by Caltrans with entomologists from the county, state, and federal government and the University of California, Berkeley (Tassan et al., 1982). It was discovered at that time that there were actually two scale species present. Biological studies showed that P. delottoi had one generation per year and colonized the mature lower portions of the plant, whereas P. mesembryanthemi had two generations per year and usually attacked the new terminal growth (Donaldson et al., 1978). By 1976, the scales were causing considerable damage to ice plants along highways. In 1978, the Division of Biological Control at the University of California, Berkeley, embarked on a three-year biological control program funded by Caltrans. As a result of this program, seven natural enemies of the scales were collected in South Africa and released in California. Two coccinellid species, Hyperaspis senegalensis hottentotta Mulsant and Exochomus flavipes (Thunberg), failed to establish (Frankie & Hagen, 1986). Five wasps were released: the encyrtids Metaphycus funicularis Annecke, M. stramineus Compere, Metaphycus spp., and Encyrtus saliens Prinsloo & Annecke and the aphelinid Coccophagus cowperi Girault. The first two have established throughout California and E. saliens is probably established in northern California (Frankie & Hagen, 1986). These three introduced natural enemies have largely eliminated the need for chemical sprays for ice plant scales along freeways in California (Frankie & Hagen, 1986). Native aphelinids (Coccophagus spp.), an exotic encyrtid (Metaphycus helvolus (Compere), introduced from South Africa in the 1930s for control of black scale on citrus), and an exotic coccinellid (Cryptolaemus montrouzieri Mulsant, released for control of mealybugs on citrus) also attack the ice plant scales in California. The Mediterranean fruit fly eradication program in California in 1980-1982 provided an opportunity to study the effect of malathion bait spray on the ice plant scales and their natural enemies in 1981-1982. A single insecticide application reduced the number of parasitoids, Coccophagus lycimnia (Walker), by 79% and M. stramineus by 90% (Washburn et al., 1983). The timing and number of applications of bait spray were critical as a number of applications would be detrimental to the parasites. Also, immature scale (crawlers) was affected by the bait spray (Washburn

et al., 1983). In the laboratory, malathion bait spray at very low concentrations produced sublethal effects on one of the ice plant scale parasitoids, E. saliens (Hoy & Dahlsten, 1984). The ice plant scale project demonstrates that classical biological control can be used for pests of roadside plantings of ground cover. It was also shown that secondary outbreaks of ice plant scale could occur due to the aerial application of bait sprays. Finally, the ice plant scales could be considered as agents of biological control in areas where ice plant is a pest.

Miscellaneous Scales

Several homopteran pests of ornamentals have been controlled by natural enemies introduced for biological control on agricultural crops. Natural enemies imported for control of cottony cushion scale, lcerya purchasi Maskell (Margarodidae), on citrus controlled it on ornamentals as well (Clausen, 1978). Another example is the nigra scale, Parasaissetia nigra (Nietner), which was controlled by Metaphycus helvolus (Compere), a parasitoid introduced against black scale, Saissetia oleae (Bernard), on citrus (Clausen, 1978).

Pseudococcidae

Rhodesgrass Mealybug (Antonina graminis (Maskell)) In the 1940s the rhodesgrass mealybug became a major pest of forage and lawn grasses in Texas. The mealybug is of Asiatic origin and infests at least 69 species of lawn and turf grasses (Dean et al., 1979). Several parasitoids were introduced as a part of a biological control program (Schuster et al., 1971). Complete control resulted from the action of Neodusmetia sangwani (Rao), an encyrtid from India. Dean et al. (1979) estimated that in 1976, the parasitoid saved nearly $17 million per year in turf grass management costs in Texas.

Comstock Mealybug (Pseudococcus comstocki (Kuwana)) Comstock mealybug was introduced into a residential area of the San Joaquin Valley of California and caused considerable damage to ornamentals. Three species of parasitoids were introduced from Japan and became established (Meyerdirk et al., 1981). These species, Pseudaphycus malinus Gahan (Encyrtidae), Allotropa burrelli Muesebeck (Platygasteridae), and Allotropa convexifrons Muesebeck (Platygasteridae), combined with Zarhopalus corvinus (Girault) (Encyrtidae) and the native predators Leucopsis ocellaris Malloch (Leucospididae) and Chrysopa spp. (Chrysopidae) to provide biological control. Population densities of the Comstock mealybug were reduced 6 8 73% by the natural enemy complex. After establishment of

Chapter 36 BiologicalControl of Insects in Urban Environments the natural enemies, mealybug population densities were below damage thresholds for omamentals in residential areas (Meyerdirk et al., 1981). The program is considered a success (Ervin et al., 1983)

Lebbeck Mealybug (Nipaecoccus virdis (Maskell)) The lebbeck mealybug infests several species of ornamental plants but was especially destructive to the lebbeck tree, Albizia lebbeck, in Cairo and other cities in Egypt. From 1933 to 1939, natural enemies were introduced from Java. Two encyrtid parasitoids, Anagyrus aegyptiacus Moursi and Leptomastix phenacocci Compere, were established and provided complete control of the mealybug. In some areas, parasitism reached 98% and in many localities the mealybug almost disappeared (Clausen, 1978).

Hibiscus Mealybug (Maconellicoccus hirsutus (Green)) The hibiscus mealybug is thought to be native to the Far East. It was introduced into Egypt and was considered to be the most injurious mealybug in Egypt. The mealybug severely infests Hibiscus spp., mulberry (Morus sp.), Albizia lebbeck (Linnaeus), Acacia arabica (Willdenow), Bauhinia spp., Grevillia spp., guava, Parkinsonia aculeatus Linnaeus, Robinia pseudacacia Linnaeus, and Cajanus cajan (Linnaeus) Millsp. After a severe outbreak in and around Cairo in 1920, several species of natural enemies of other mealybugs were introduced. The encyrtid Anagyrus kamali Moursi, imported from Java, became established and provided control (Clausen, 1978).

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overwinter well and parasitism rates early in the season are extremely low. In many areas it has not been recovered even late in the season. Aprostocetus brevistigma (Gahan), which is apparently native to the northeastern United States, has been reported as parasitizing 50-80% of elm leaf beetle pupae in the northeastem United States (Berry, 1938b). Aprostocetus brevistigma has been established in California but has little impact on elm leaf beetle populations (Luck & Scriven, 1976; Dreistadt & Dahlsten, 1990). Recent surveys in Ohio suggest that A. brevistigma is unimportant there as well (R. W. Hall, unpublished). Erynniopsis antennata Rondani (Diptera: Tachinidae) was imported from several European countries and established in central California in 1939. It is now well distributed throughout northern California, but parasitism rates do not exceed 40% and average under 5% (Dreistadt & Dahlsten, 1990). Luck and Scriven (1976) found that E. antennata parasitized a significant portion of the elm leaf beetle larval population late in the season. However, early season parasitism was insufficient to prevent aesthetically damaging levels of defoliation. A new strain ("San Diego") of Bacillus thuringiensis Berliner has been developed for use against Chrysomelidae; Cranshaw et al. (1989) report it appears to be highly effective against both larval and adult elm leaf beetles, and Dahlsten et al. (1998c) have found it to be effective with two applications per generation, timed 1 week apart, at first instar larval peak, at one location in California.

Scarabaeidae Coleoptera

Chrysomelidae Elm Leaf Beetle (Xanthogaleruca luteola (Miiller)) The elm leaf beetle was introduced into the United States from Europe in the 1830s (Howard, 1908). Since its introduction, elm leaf beetle has spread across the United States and now defoliates elms in urban and suburban plantings nearly everywhere they are grown. The eulophid egg parasitoid Oomyzus gallerucae (Fonscolombe) (=Tetrastichus xanthomelaenae Rondani) has been repeatedly introduced from Europe and the Middle East (Berry, 1938a; Clair et al., 1988). Oomyzus gallerucae is established in central Ohio, apparently as a result of an introduction made in 1932 (Hall & Johnson, 1983). Unfortunately, O. gallerucae does not prevent the elm leaf beetle from causing severe aesthetic injury to elms in central Ohio (Hamerski et al., 1990). Oomyzus gallerucae has also been introduced and recovered from northem and southern Califomia (Luck & Scriyen, 1976; Clair et al., 1988; Dahlsten et al., 1990). However, in Califomia, O. gallerucae apparently does not

Japanese Beetle (Popillia japonica Newman) The Japanese beetle is a major pest of turf grass on golf courses, recreation areas, and home lawns in the northeastem and midwestem United States (Tashiro, 1987). Prior to introduction into the United States, the Japanese beetle was known to occur only on the four main islands of Japan, where it was thought to be of little economic importance (Fleming, 1972). Damage to turf is caused by the larva (grub), which feeds on the roots of grasses. Turf injury depends on grub density and degree of maintenance of the lawn. Poorly maintained lawns may be damaged at densities of 4 - 5 grubs/ft 2 whereas on well-maintained tuff, damage is usually not apparent until densities exceed 10 grubs/ft 2. The most effective biological control agent of the Japanese beetle is Bacillus popilliae Dutky, which causes milky spore disease in the larva (Tashiro, 1987). Bacillus popilliae was first identified in central New Jersey in 1933 (White, 1941). The name milky spore disease refers to the milky color assumed by the hemolymph of the grub as sporulation of the bacteria occurs. When sufficient quantities of B. popilliae spores are ingested, grubs become infected. A1-

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D.L. Dahlsten and !~ W. Hall

though infected grubs may live and continue to feed for weeks or months after infection, eventually they become weakened and die. Upon death and decay of the grub, a high concentration of spores is released into the soil and other grubs ingesting the spores are subject to infection. Commercially available formulations of spore powder (marketed as "Milky Spore" and "Japanese Beetle Attack") are applied by depositing approximately 2 g of spore powder at intervals of 1.5-3 m on turf grass areas with high population densities of grubs (Tashiro, 1987). Strains NJ-43 and SI-12 of the nematode Steinernema glaseri Steiner are capable of reducing the Japanese beetle in turf grass by two-thirds if the nematodes are rinsed from the grass surface after application (Selvan et al., 1994).

ing has been published recently, but C. frustranae has continued to spread in southern California with the tip moth.

Miscellaneous Lepidoptera Applications of Bacillus thuringiensis have been shown to be an effective control for several species of lepidopteran defoliators in urban environments, including gypsy moth, Lymantria dispar (Linnaeus), fall cankerworm, Alsophila pometaria (Harris), spring cankerworm, Paleacrita vernata (Peck), fall webworm, Hyphantria cunea (Drury), bagworm, Thyridopteryx ephemeraeformis (Haworth), California oakworm, Phryganidia californica Packard, and red humped caterpillar, Schizura coccina (Smith).

Diptera Lepidoptera

Tortricidae Nantucket Pine Tip Moth (Rhyacionia frustrana ( Comstock)) The Nantucket pine tip moth is native to the eastern and southern United States. It is widely distributed and infests most native and exotic pines in that region. Its primary importance is in the south, where it is a pest in loblolly or shortleaf pine plantations. However, this moth is also a common pest of ornamentals and nursery stock. Usually infestations occur on seedlings and saplings less than 3 m in height. Although trees are rarely killed by this insect, the feeding on the terminal and lateral buds and stems causes discoloration and deformation of the branches and stem (Coulson & Witter, 1984). In 1971, the Nantucket pine tip moth was discovered on Monterey pine, Pinus radiata, on a golf course in San Diego County (Scriven & Luck, 1978). Eventually a major portion of southwestern San Diego County was infested. Other species of ornamental pine were attacked but Monterey pine was the most severely attacked. A native tachinid, Erynnia tortricis (Coquillett), and an ichneumonid, Scambus aplopappi (Ashmead), were found to parasitize the tip moth, but only at a rate of up to 10% (Scriven & Luck, 1978). Natural enemies were introduced from the eastern and southern United States and in 1979, an ichneumonid, Campoplex frustranae Cushman, and a tachinid, Lixophaga mediocris Aldrich, were introduced from the southeastern United States. The tachinid did not become established, but C. frustranae did and increased rapidly throughout 1976 and 1977 (Scriven & Luck, 1978). By the end of 1979, parasitism of overwintering tip moth had reached 50%. Many Monterey pines at the original parasite establishment site improved in appearance and vigor, indicating that the biological control program with C. frustranae was promising (Scriven & Luck, 1978). Noth-

Agromyzidae Holly Leafminer (Phytomyza ilicis Curtis) The holly leafminer was introduced into British Columbia and damaged leaves of English holly in commercial and urban plantings. Five species of parasitoids were released on Vancouver Island from 1936 to 1938 and on the mainland in 1939 (Clausen, 1978). Although four species became established, parasitism was primarily due to Chrysocharis gemma (Walker) (Eulophidae) and Opius ilicis Nixon (Braconidae). Chrysocharis gemma caused approximately 90% of the parasitism on Vancouver Island whereas O. ilicis was responsible for approximately 90% of the parasitism on the mainland. On English holly in ornamental plantings, the parasitoids usually prevent serious disfigurement of the plants and chemical controls are rarely needed. Therefore, Turnbull and Chant (1961) deemed biological control to be a complete success in these situations. However, on commercially produced holly, parasitoids did not ensure a blemish-free plant and pesticides are still used. Turnbull and Chant (1961) and Munroe (1971) consider biological control as partially to substantially successful in commercial plantings.

References Beingolea, G. O. (1969). Biological control of citrus pests in Peru. Proceedings of the 1st International Citrus Symposium, Riverside, California, 2, 827-838. Bellows, T. S., Paine, T. D., Gould, J. R., Bezark, L. G., & Ball, J. C. (1992). Biological control of ash whitefly: A success in progress. California Agriculture, 46(1), 24, 27- 28. Bennett, F. D., & Hughes, I. W. (1959). Biological control of insect pests in Bermuda. Bulletin of Entomological Research, 50, 423-436. Bennett, G. W., & Owens, J. M., Eds. (1986). "Advances in Urban Pest Management." Van Nostrand-Reinhold, New York. Berry, P. A. (1938a). Laboratory studies on Tetrastichus xanthomelaenae

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Rond. and Tetrastichus sp., two hymenopterous egg parasites of the elm leaf beetle. Journal of Agricultural Research, 57, 859-863. Berry, P. A. (1938b). "Tetrastichus brevistigma Gahan, a Pupal Parasite of the Elm Leaf Beetle." USDA Circular 485. Cameron, E. (1955). On the parasites and predators of the cockroach. I. Tetrastichus hagenowii (Ratz.). Bulletin of Entomological Research, 46, 137-147. Clair, D. J., Dahlsten, D. L., & Dreistadt, S. H. (1988). Biological control of the elm leaf beetle, Xanthogaleruca luteola, in CaliforniamA case study. In "Global Perspectives on Agroecology and Sustainable Agricultural Systems" (P. Allen & D. van Dusen, Eds.), Vol. 2, pp. 497504. Agroecology Program, Univ. of California, Santa Cruz. Clair, D. J., Dahlsten, D. L., & Hart, E. R. (1987). Rearing Tetrastichus gallerucae (Hymenoptera: Eulophidae) for biological control of the elm leaf beetle, Xanthogaleruca luteola. Entomophaga, 32, 457-461. Clausen, C. P., Ed. (1978). "Introduced Parasites and Predators of Arthropod Pests and Weeds: A World Review." USDA-ARS Agricultural Handbook No. 480. Cockrell, R. A., & Warnke, F. F. (1976). "Trees of the Berkeley Campus." Division of Agricultural Sciences, Univ. of California, Berkeley. Coler, R. R., Van Driesche, R. G., & Elkinton, J. S. (1984). Effect of an oothecal parasitoid Comperia merceti (Compere) (Hymenoptera: Encyrtidae) on a population of the brownbanded cockroach (Orthoptera: Blattellidae). Environmental Entomology, 13, 603-606. Coulson, R. N., & Witter, J. A. (1984). "Forest Entomology." Wiley, New York. Cranshaw, W. S., Day, S. J., Gritzmacher, T. J., & Zimmerman, R. J. (1989). Field and laboratory evaluation of Bacillus thuringiensis strains for control of elm leaf beetle. Journal of Aboriculture, 15, 3134. Dahlsten, D. L. (1986). Control of invaders. In "Ecological Studies: Ecology of Biological Invasions of North America and Hawaii" (H. A. Mooney & J. A. Drake, Eds.), Vol. 58, pp. 275-302. Springer-Verlag, New York. Dahlsten, D. L. (1996). Introduced Eucalyptus foliage feeders in California. In "Proceedings of the California Forest Pest Council 44th Annual Meeting, Nov. 15-16, 1995," pp. 32-35. Dahlsten, D. L., Dreistadt, S. H., Geiger, J. R., Tait, S. M., Rowney, D. L., Yokota, G. Y., & Copper, W. A. (1990). "Elm Leaf Beetle Biological Control and Management in Northern California." Final Report to the California Department of Forestry and Fire Protection. Dahlsten, D. L., Garcia, R., Prine, J. E., & Hunt, R. (1969). Insect problems in forest recreation areas. California Agriculture, 23(7), 4-6. Dahlsten, D. L., Hajek, A. E., Clair, D. J., Dreistadt, S. H., Rowney, D. L., & Lewis, V. R. (1985). Pest management in the urban forest. California Agriculture, 39(1-2), 21-22. Dahlsten, D. L., Hansen, E. P., Zuparko, R. L., & Norgaard, R. B. (1998b). Biological control of the blue gum psyllid proves economically beneficial. California Agriculture, 52(1), 35-40. Dahlsten, D. L., Kent, D. M., Rowney, D. L., Copper, W. A., Young, T. E., & Tassan, R. L. (1995). Parasitoid shows potential for biocontrol of eugenia psyllid. California Agriculture, 49(4), 36-40. Dahlsten, D. L., Rowney, D. L., Copper, W. A., Tassan, R. L., Chaney, W. E., Robb, K. L., Tjosvold, S., Bianchi, M., & Lane, P. (1998a). Parasitoid wasp controls blue gum psyllid. California Agriculture, 52(1), 31-34. Dahlsten, D. L., Rowney, D. L., & Lawson, A. B. (1998c). IPM helps control elm leaf beetle. California Agriculture, 52(2), 18-23. Dean, H. A., Schuster, M. F., Boling, J. C., & Riherd, P. T. (1979). Complete biological control of Antonina graminis in Texas with Neodusmetia sangwani (a classic example). Bulletin of the Entomological Society of America, 25, 262-267. DeBach, P. (1964). Successes, trends, and future possibilities. In "Biological Control of Insect Pests and Weeds" (P. DeBach, Ed.), pp. 673713. Reinhold, New York.

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DeBach, P., & Rose, M. (1976). Biological control of woolly whitefly. California Agriculture, 30(5), 4-7. DeBach, P., & Rose, M. (1977). Environmental upsets caused by chemical eradication. California Agriculture, 31 (7), 8-10. Donaldson, D. R., Moore, W. S., Koehler, C. S., & Joos, J. L. (1978). Scales threaten ice plant in Bay Area. California Agriculture, 32(10), 4,7. Dreistadt, S. H., & Dahlsten, D. L. (1986). Medfly eradication in CaliforniamLessons from the field. Environment, 28(6), 18-20, 41-44. Dreistadt, S. H., & Dahlsten, D. L. (1990). Distribution and abundance of Erynniopsis antennata (Dipt.: Tachinidae) and Tetrastichus brevistigma (Hym.: Eulophidae), two introduced elm leaf beetle parasites in northern California. Entomophaga, 35, 527-536. Dreistadt, S. H., & Hagen, K. S. (1994). Classical biological control of the acacia psyllid, Acizzia uncatoides (Homoptera: Psyllidae), and predator-prey-plant interactions in the San Francisco Bay area. Biological Control, 4, 319-327. Ebeling, W. (1975). "Urban Entomology." Univ. of California, Division of Agricultural Sciences, Richmond, CA. Edmunds, L. R. (1957). Observations on the biology and life history of the brown cockroach Periplaneta brunnea Burmeister. Proceedings of the Entomological Society of Washington, 59, 283-286. Ehler, L. E., & Endicott, P. C. (1984). Effect of malathion-bait sprays on biological control of insect pests of olive, citrus, and walnut. Hilgardia, 52(5), 1-47. Embree, D. G. (1971). Operophtera brumata (L.), winter moth (Lepidoptera: Geometridae). In "Biological Control Programmes against Insects and Weeds in Canada, 1959-1968," pp. 167-175. Commonwealth Institute of Biological Control Technical Communication No. 4. Ervin, R. T., Moffitt, L. J., & Meyerdirk, D. E. (1983). Comstock mealybug (Homoptera: Pseudococcidae): Cost analysis of a biological control program in California. Journal of Economic Entomology, 76, 605609. Ferguson, A. M. (1989). Asterodiospis spp., pit scales (Homoptera: Asterolecaniidae). In "A Review of Biological Control of Invertebrate Pests and Weeds in New Zealand, 1874-1987" (P. J. Cameron, R. L. Hill, J. Bain, & W. P. Thomas, Eds.), pp. 257-262. Commonwealth Institute of Biological Control Technical Communication No. 10. Flanders, R. V. (1986). Potential for biological control in urban environments. In "Advances in Urban Pest Management" (G. W. Bennett & J. M. Owens, Eds.), pp. 95-127. Van Nostrand-Reinhold, New York. Flanders, S. E. (1959). Biological control of Saissetia nigra (Nietn.) in California. Journal of Economic Entomology, 52, 596-600. Fleet, R. R., & Frankie, G. W. (1975). Behavioral and ecological characteristics of a eulophid egg parasite of two species of domiciliary cockroaches. Environmental Entomology, 4, 282-284. Fleming, W. E. (1968). "Biological Control of Japanese Beetle." USDA Technical Bulletin No. 1383. Fleming, W. E. (1972). "Biology of Japanese Beetle." USDA Technical Bulletin No. 1449. Frankie, G. W., & Ehler, L. E. (1978). Ecology of insects in urban environments. Annual Review of Entomology, 23, 367-387. Frankie, G. W., & Hagen, K. S. (1986). "Ecology and Biology of Iceplant Scales, Pulvinaria and Pulvinariella in California." California Department of Transportation, Division of Highway Maintenance, Sacramento, CA (Report No. FHWA-CA-HM-OZ). Frankie, G. W., & Koehler, C. S., Eds. (1978). "Perspectives in Urban Entomology." Academic Press, New York. Frankie, G. W., & Koehler, C. S., Eds. (1983). "Urban Entomology: Interdisciplinary Perspectives." Praeger, New York. Gould, J. R., Bellows, T. S., & Paine, T. D. (1992a). Population dynamics of Siphoninus phillyreae in California in the presence and absence of a parasitoid, Encarsia partenopea. Ecological Entomology, 17, 127134.

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Gould, J. R., Bellows, T. S., & Paine, T. D. (1992b). Evaluation of biological control of Siphoninus phillyreae (Haliday) by the parasitoid Encarsia partenopea (Walker), using life-table analysis. Biological Control, 2, 257-265. Hagen, K. S., van den Bosch, R., & Dahlsten, D. L. (1971). The importance of naturally occurring biological control in the western United States. In "Biological Control" (C. B. Huffaker, Ed.), pp. 253-293. Plenum, New York. Hall, R. W., & Johnson, N. F. (1983). Recovery of Tetrastichus gallerucae (Hymenoptera: Eulophidae), an introduced egg parasitoid of the elm leaf beetle (Pyrrhalta luteola) (Coleoptera: Chrysomelidae). Journal of the Kansas Entomological Society, 56, 297-298. Hamerski, M. R., Hall, R. W., & Keeney, G. D. (1990). Laboratory biology and rearing of Tetrastichus brevistigma (Hymenoptera: Eulophidae), a larval-pupal parasitoid of the elm leaf beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 83, 2196-2199. Hoelmer, K. A., & Dahlsten, D. L. (1993). Effects of malathion bait spray on Aleyrodes spiraeoides (Homoptera: Aleyrodidae) and its parasitoids in northern California. Environmental Entomology, 22, 49-56. Howard, L. O. (1908). The importation of Tetrastichus xanthomelaenae (Rond.). Journal of Economic Entomology, 1,281-289. Hoy, J. B., & Dahlsten, D. L. (1984). Effects of malathion and Staley's bait on the behavior and survival of parasitic Hymenoptera. Environmental Entomology, 13, 1483-1486. Jetter, K., Klonsky, K., & Pickett, C. H. (1997). A cost-benefit analysis of the ash whitefly biological control program in California. Journal of Arboriculture, 23, 65-72. Johnson, W. T., & Lyon, H. H. (1976). "Insects that Feed on Trees and Shrubs." Comstock Publ. Assoc., Cornell Univ. Press, Ithaca, NY. Kaya, H. K., & Anderson, J. F. (1974). Collapse of the elm spanworm outbreak in Connecticut: Role of Ooencyrtus. Environmental Entomology, 3, 659-663. Kielbaso, J. J., & Kennedy, M. K. (1983). Urban forestry and entomology: A current appraisal. In "Urban Entomology: Interdisciplinary Perspectives" (G. W. Frankie & C. S. Koehler, Eds.), pp. 423-440. Praeger, New York. Laing, J. E., & Hamai, J. (1976). Biological control of insect pests and weeds by imported parasites, predators and pathogens. In "Theory and Practice of Biological Control" (C. B. Huffaker & P. S. Messenger, Eds.), pp. 685-743. Academic Press, New York. Luck, R. F. (1981). Parasitic insects introduced as biological control agents for arthropod pests. In "CRC Handbook of Pest Management in Agriculture" (D. Pimentel, Ed.), Vol. II, pp. 125-284. CRC Press, Boca Raton, FL. Luck, R. F., & Dahlsten, D. L. (1974). Bionomics of the pine needle scale, Chionaspis pinifoliae (Fitch), and its natural enemies at South Lake Tahoe, California. Annals of the Entomological Society of America, 66, 309- 316. Luck, R. F., & Dahlsten, D. L. (1975). Natural decline of a pine needle scale (Chionaspas pinifoliae [Fitch]) outbreed at South Lake Tahoe, California, following cessation of adult mosquito control with malathion. Ecology, 56, 893-904. Luck, R. F., & Scriven, G. T. (1976). The elm leaf beetle, Pyrrhalta luteola in southern California: Its pattern of increase and its control by introduced parasites. Environmental Entomology, 5,409-416. Lutz, F. F. (1941). "A Lot of Insects (Entomology in a Suburban Garden)." Putnam, New York. McBride, J. R., & Jacobs, D. F. (1986). Presettlement forest structure as a factor in urban forest development. Urban Ecology, 9, 245-266. McGugan, B. M., & Coppel, H. C. (1962). A review of the biological control attempts against insects and weeds in Canada. In "Biological Control of Forest Insects, 1910-1958," pp. 35-216. CAB, Commonwealth Institute of Biological Control Technical Communication No. 2. Merritt, R. W., Kennedy, M. K., & Gersabeck, E. F. (1983). Integrated

pest management of nuisance and biting flies in a Michigan resort: Dealing with secondary pest outbreaks. In "Urban Entomology: Interdisciplinary Perspectives" (G. W. Frankie & C. S. Koehler, Eds.), pp. 277-299. Praeger, New York. Meyerdirk, D. E., Newell, I. M., & Warkentin, R. W. (1981). Biological control of Comstock mealybug. Journal of Economic Entomology, 74, 79-84. Munroe, E. G. (1971). Status and potential of biological control in Canada. In "Biological Control Programmes against Insects and Weeds in Canada," Chap. 48, pp. 213-255. Commonwealth Institute of Biological Control Technical Communication No. 4. National Research Council. (1980). "Urban Pest Management." Report by Committee on Urban Pest Management, Environmental Studies Board, Commission on National Resources. National Academy Press, Washington, DC. Olkowski, W. (1974). A model ecosystem management program. Proceedings of the Tall Timbers Conference, Ecology, Animal Control Habitat Management, 5, 103-117. Olkowski, W., Olkowski, H., Kaplan, A. I., & van den Bosch, R. (1978). The potential for biological control in urban areas: Shade tree insect pests. In "Perspectives in Urban Entomology" (G. W. Frankie & C. S. Koehler, Eds.), pp. 311-349. Academic Press, New York. Olkowski, W., Olkowski, H., & van den Bosch, R. (1982a). Linden aphid parasite establishment. Environmental Entomology, 11, 1023-1025. Olkowski, W., Olkowski, H., van den Bosch, R., & H o m , R. (1976). Ecosystem management: A framework for urban pest control. Bioscience, 26, 384-389. Olkowski, W., Olkowski, H., van den Bosch, R., Hom, R., Zuparko, R., & Klitz, W. (1982b). The parasitoid Trioxys tenuicaudus Stary (Hymenoptera: Aphidiidae) established on the elm aphid Tinocallis platani Kaltenbach (Homoptera: aphididae) in Berkeley, Califomia. Pan-Pacific Entomologist, 58, 59-63. Pemberton, C. E. (1948). History of the entomology department, experiment station, H.S.P.A., 1904-1945. Hawaii Planters' Record, 52, 5390. Pemberton, C. E. (1954). Invertebrate Consultants Committee for the Pacific. Pacific Science Board, National Academy of Sciences, National Research Council. Pinnock, D. E., Hagen, K. S., Cassidy, D. V., Brand, R. J., Milstead, J. E., & Tassan, R. L. (1978). Integrated pest management in highway landscapes. California Agriculture, 32(2), 33-34. Piper, G. L., & Frankie, G. W. (1978). Integrated management of urban cockroach populations. In "Perspectives in Urban Entomology" (G. W. Frankie & C. S. Koehler, Eds.), pp. 249-266. Academic Press, New York. Piper, G. L., Frankie, G. W., & Loehr, J. (1978). Incidence of cockroach egg parasitoids in urban environments in Texas and Louisiana. Environmental Entomology, 7, 289-293. Quezada, J. R., & DeBach, P. (1973). Bioecological and population studies of the cottony cushion scale, Icerya purchasi Mask., and its natural enemies, Rodalia cardinalis Muls. and Cryptochaetum iceryae Will., in southern California. Hilgardia, 41, 631-688. Rao, V. P., Ghani, M. A., Sankaran, T., & Mathur, K. C. (1971). "A Review of the Biological Control of Insects and Other Pests in the Southeast Asia and the Pacific Region." Commonwealth Institute of Biological Control Technical Communication No. 6. Richards, W. R. (1967). A review of the Tinocallis of the world (Homoptera: Aphididae). Canadian Entomologist, 99, 536-553. Roth, L. M., & Willis, E. R. (1954). The biology of the cockroach parasite Tetrastichus hagenowii (Ratzeburg), a chalcidoid egg parasite (Hymenoptera: Eulophidae). Transactions of the American Entomological Society, 80, 53-72. Saakian-Baranova, A. A. (1966). The life cycle of Metaphycus luteolus Timb. (Hymenoptera: Encyrtidae), parasite of Coccus hesperidum (Homoptera: Coccidae), and the attempt of its introduction into the USSR. Entomological Review, 45, 733-751 (in Russian).

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Biological Control of Insects in Urban Environments

Sailer, R. I. (1972). Concepts, principles and potentials of biological control: Parasites and predators. Proceedings of the North Central Entomological Society of America, 27, 35-39. Schuster, M. F., Boling, J. C., & Marony, J. J., Jr. (1971). Biological control of rhodesgrass scale by airplane releases of an introduced parasite of limited dispersing activity. In "Biological Control" (C. B. Huffaker, Ed.), pp. 227-250. Plenum, New York. Scriven, G. T., & Luck, R. F. (1978). Natural enemy promises control of Nantucket pine tip moth. California Agriculture, 32(10), 19-20. Selvan, S., Grewal, P. S., Gaugler, R., & Tomalak, M. (1994). Evaluation of Steinernematid nematodes against Popilla japonica (Coleoptera: Scarabaeidae) larvae: Species, strains and rinse after application. Journal of Economic Entomology, 87, 605-609. Simmonds, F. J. (1969). "Brief Resume of Activities and Recent Successes Achieved." Commonwealth Institute of Biological Control. Commonwealth Agricultural Bureaux Publications. 16 pp. Slater, A. J. (1984). Biological control of the brownbanded cockroach, Supella longipalpa (Serville) with an encyrtid wasp, Comperia merceti (Compere). Pest Management, 3(4), 14-17. Slater, A. J., Huflbert, M. J., & Lewis, V. R. (1980). Biological control of the brownbanded cockroaches. California Agriculture, 34(8), 16-18. Swan, D. I. (1973). Evaluation of biological control of the oak leaf miner, Phyllonorycter messeniella (Zell.) (Lepidoptera: Gracillariidae), in New England. Bulletin of Entomological Research, 63, 49-55. Tashiro, H. (1987). "Turfgrass Insects of the United States and Canada." Comstock Publ. Assoc., Comell Univ. Press, Ithaca, NY. Tassan, R. L., Hagen, K. S., & Cassidy, D. V. (1982). Imported natural enemies established against ice plant scales in Califomia. California Agriculture, 36(9-10), 16-17. Troetschler, R. G. (1983). Effects on nontarget arthropods of malathion bait sprays used in California to eradicate the Mediterranean fruit fly, Ceratis capitata (Wiedemann) (Diptera: Tephritidae). Environmental Entomology, 12, 1816-1822.

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Tumbull, A. L., & Chant, D. A. (1961). The practice and theory of biological control in Canada. Canadian Journal of Zoology, 39, 697753. van den Bosch, R., Frazer, B. D., Davis, C. S., Messenger, P. S., &Hom, R. (1970). Trioxys pallidus, an effective new walnut aphid parasite from Iran. California Agriculture, 24(11), 8-10. Walker, J. T. S. (1989). Tuberculatus annulatus (Hartig), oak aphid (Homoptera: Callaphididae). In "A Review of Biological Control of Invertebrate Pests and Weeds in New Zealand, 1874-1987" (P. J. Cameron, R. L. Hill, J. Bain, & W. P. Thomas, Eds.), pp. 307-308. Commonwealth Institute of Biological Control Technical Communication No. 10. Washburn, J. A., Tassan, R. L., Grace, K., Bellis, E., Hagen, K. S., & Frankie, G. W. (1983). Effects of malathion sprays on the ice plant insect system. California Agriculture, 37(1-2), 30-32. White, R. T. (1941). Development of milky disease on Japanese beetle larvae under field conditions. Journal of Economic Entomology, 34, 213-215. Wilson, F. (1960). "A Review of the Biological Control of Insects and Weeds in Australia and Australian New Guinea." Commonwealth Institute of Biological Control Technical Communication No. 1. Zuparko, R. L. (1983). Biological control of Eucallipterus tiliae [Hom.: Aphididae] in San Jose, Calif., through establishment of Trioxys curvicaudus [Hym.: Aphidiidae]. Entomophaga, 28, 325-330. Zuparko, R. L., & Dahlsten, D. L. (1994). Host plant resistance and biological control for linden aphids. Journal of Arboriculture, 20, 278281. Zuparko, R. L., & Dahlsten, D. L. (1995). Parasitoid complex of Eucallipterus tiliae (Homoptera: Drepanosiphidae) in northem California. Environmental Entomology, 24, 730-737.

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[37] Biological Control of Medical and Veterinary Pests IL GARCIA

E. F. LEGNER

Division of Biological Control University of California Albany, California

Department of Entomology

INTRODUCTION

agricultural situation, natural enemies can coexist with pests and thus may regulate the pest populations. Additionally, in many situations the habitat exploited by the medically important pests is only an undesirable extension of human activity. An example would be the cultivation of rice, where the production of pests such as mosquitoes is usually of little concern to the grower. Interest in biological control of medical pests and vectors had its modest beginning nearly 100 years ago (Lamborn, 1890). At that time, the possible use of dragonflies as natural enemies for the control of mosquitoes was clearly recognized. However, as is true even today, the enormous difficulties associated with the colonization and management of these insects quickly extinguished any idea for the practical use of these predators for mosquito control. Shortly after the turn of the century, the mosquitofish, Gambusia affinis (Baird & Girard), came to the forefront of biological control. This small fish, being much easier to deal with than dragonflies, was quickly utilized and transported throughout the world during the early decades of this century in attempts to control mosquitoes. The mosquitofish, G. affinis, and other naturalistic methods of control were employed with some vigor for about the first 40 years of the century. All these control measures were curtailed sharply with the introduction of synthetic organic insecticides after World War II. The convenience and quick killing power of these chemicals was so dramatic for mosquitoes, flies, and lice that other control tactics were quickly reduced to a minor role. Interest in biological control arose again when the succession of chemicals developed during the 1940s and 1950s began to fail due to the development of genetic resistance in vector and pest populations. The biological control of medically im-

University of California Riverside, California

The manipulative use of natural enemies for the control of medical and veterinary invertebrate pests has been restricted largely to various species of Diptera. Some work has been conducted on ants, cockroaches, wasps, ticks, and snails, but work on these animals has been limited. Here we review the biological control agents that can be manipulated, that have been used successfully, that are being researched, and that show at least some promise for successful application. Bay et al. (1976) indicate that medically important pests differ from agricultural pests in fundamental ways. First, pests that affect humans are usually in the adult stage while those that attack crops are usually in the immature stage. This is of some advantage for control of medically important pests because it allows the control action to be taken against the immatures, thus eliminating the adult before it can cause problems. A second difference, however, is not favorable as it relates to setting tolerance levels. Whereas an allowable number of pests (tolerance level) can be established for the biological control of a crop pest, such levels are far more difficult to establish for pests attacking humans. For example, an individual mosquito can be of great annoyance and can precipitate a reaction for control. In addition, low population levels of a vector may still transmit a disease and, therefore, cannot be tolerated (Service, 1983). However, setting tolerance levels for veterinary pests would be more in line with those for agricultural pests. A third difference, usually a distinct disadvantage for biological control, is that the habitat utilized by medically important pests is frequently temporary, as opposed to that of an agricultural crop, which is more permanent. In the

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portant pests and vectors has made slow progress since its revival and is still behind that which has occurred in agricultural systems (Service, 1983). This disparity is due to the problems of establishing pest tolerance levels and the temporary, unstable habitats exploited by medically important pests (Legner & Sjogren, 1984). While progress in the development of biological control agents has been substantial and work in progress appears promising, our overall evaluation at this point is that biological control will rarely be a panacea for medically important pests. However, with continued effort it can be a major component in the overall strategy for the control of some of these important pests (Legner & Sjogren, 1984). The literature reviewed in this chapter is organized by taxonomic groups because of the wide assemblage of different habitats occupied by medically important pests. The major groups where some success has been achieved or where work is currently being conducted are the mosquitoes, blackflies, synanthropic flies, intermediate host snails, and cockroaches. Most effort has been directed against mosquitoes because of the human disease agents they transmit. Consequently, much of this chapter is devoted to mosquitoes. The synanthropic flies and snails are also covered in this chapter, but the biological control of cockroaches is reviewed in the chapter on urban pests (Chapter 36).

MOSQUITOES The successful widespread use of biological control agents against mosquitoes requires a much better understanding of the ecology of predator-prey and pathogenhost relationships (Service, 1983). The opportunistic characteristics of many species (i.e., their ability to exploit temporary habitats, coupled with their short generation time, high natural mortality, great dispersal potential, and other R-strategist characteristics) pose difficult problems for any biotic regulatory mechanism. Mosquitoes typically exploit many aquatic habitats. Often a biological control agent has a much narrower range of environmental activity than the target mosquito has. Thus, in many situations, a number of different biological control agents and/or appropriate methods will be necessary to control even one species of mosquito across its range of exploitable breeding sources.

Fish Several species of fish are used for the biological control of mosquitoes, and these species together form the major successes in the field. Unfortunately, their usefulness is limited to more permanent bodies of water, and even under these situations, their impact on the target species has been only partially successful. Bay et al. (1976) point out that many species of fish consume mosquito larvae, but only a

few fish species have been manipulated to manage mosquito populations. The mosquitofish, G. affinis, is the best-known agent for mosquito control. This fish, which is native to the southern United States, Mexico, and the Caribbean area, was first used as an introduced agent for mosquito control when it was transported from North Carolina to New Jersey in 1905 (Lloyd, 1987). Shortly thereafter, it was introduced to the Hawaiian Islands to control mosquitoes that had been introduced during the nineteenth century. During the next 70 years, the mosquitofish was transported to over 50 countries and today stands as the most widely disseminated biological control agent (Bay, 1969; Lloyd, 1987). Many of these introductions were aimed at Anopheles species that were transmitting malaria. Hackett (1937) described its usefulness in malaria control programs in Europe. He commented that its effects were cumulative and not sufficient by themselves, but that the fish had a definite impact on the suppression of the disease. Tabibzadeh et al. (1970) reported a rather extensive release program in Iran and concluded that the fish was an important component in the malaria eradication program. Sasa and Kurihara (1981) and Service (1983) believed that the fish had little impact on the disease and that most evidence supporting these claims is circumstantial. However, Inci et al. (1992) reported a 50% reduction in malaria cases in southeast Turkey after releases of G. affinis. Gambusia is not recommended by the World Health Organization (WHO) for malaria control programs, primarily because of its impact on indigenous species of fish (Services, 1983; Lloyd, 1987). The biological attributes of G. affinis, namely, a high reproductive capability; high survivorship; small size; omnivorous foraging in shallow water; and relatively high tolerance to variations in temperature, salinity, and organic waste, would seemingly make this species an excellent biological control agent (Bay et al., 1976; Moyle, 1976). However, whether this fish leads to effective mosquito control at practical costs in many situations is still debated. Kligler's (1930) statement that . . . their usefulness as larvae destroyers under local conditions where vegetation is abundant and micro fauna rich enough to supply their needs without great trouble, is limited. In moderately clear canals, on the other hand, or in pools having a limited food supply, they yielded excellent results . . . . is probably one of the most accurate. In California, this fish has been used rather extensively over the years for control of mosquitoes in various habitats (Bay et al., 1976). Many mosquito abatement districts in this state have developed systems for culturing, harvesting, and winter storage of the mosquitofish to have enough available for planting early in the spring (Coykendall, 1980). This is particularly important in the rice growing areas of California where early stocking appears to be of critical importance for buildup of fish populations to control

Chapter 37

Biological Control of Medical and Veterinary Pests

mosquitoes during late summer. The results of the use of G. affinis in California rice fields will be summarized later as an illustrative example of the mixed successes achieved in the field. Rice cultivation continuously poses one of the most difficult control problems for Anopheles and Culex species. Hoy and Reed (1970) showed that good to very good control of C. tarsalis Coquillett could be achieved at stocking rates of about 480 or more females per hectare and Stewart et al. (1983) reported excellent control with a similar stocking rate against this species in the San Joaquin Valley. Although C. tarsalis appears to be controlled effectively by G. affinis, the control of its frequent companion in northern California rice fields, A. freeborni Aitken, is less apparent. Hoy et al. (1971) showed a reduction of A. freeborni populations at various stocking rates of about 120 to 720 fish per hectare, but the reduction was not nearly as striking as that for C. tarsalis. These workers surmised that improvement in control could be achieved by earlier season stocking, possibly multiple release points in fields and a reliable source of healthy fish for stocking. Despite an extensive research effort in mass culture, management, and storage for G. affinis by the state of California (Hoy & Reed, 1971), a mass production method has not been satisfactorily achieved (Downs et al., 1986; Cech & Linden, 1987). Studies of G. affinis for control of mosquitoes in wild rice show that relatively high stocking rates can effectively reduce A. freeborni and C. tarsalis populations within a 3month period (Kramer et al. 1987). The commercial production of wild rice, which is a more robust and taller plant than white rice and requires only 90 instead of 150 days to mature, has been increasing over the last few years in California (Kramer et al., 1987). In the preceding study, stocking rates of 1.7 kg/ha (ca. 2400 fish per kilogram) released in 1/10 ha wild rice plots failed to show a significant difference in reduction of mosquitoes from plots with no fish. A decrease in numbers of larvae was noted just prior to harvest, which suggested that the fish were beginning to have an impact on mosquito numbers (Kramer et al., 1987). Fish in these plots, based on recovery after drainage, was about 100,000 individuals per hectare (ca. 32 kg/ha) or a density of about 10 fish per square meter. However, significant control was not achieved. During 1987, this study was repeated at the rates of 1.7 and 3.4 kg/ha of fish. Results showed an average suppression of larvae (primarily A. freeborni) of < 1 and 0.5 per dip for the low and high rate, respectively, compared with control plots that averaged > 4.5 per dip. Fish densities in the 1987 study surpassed those of 1986 by about twofold at the 1.7 kg/ha rate and threefold at the 3.4 kg/ha rate. It is believed that these greater fish numbers accounted for the control differences observed in the second year, although mosquitoes were not eliminated. Differences be-

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tween test and control plots were first observed 8 weeks after the fish had been planted and mosquitoes remained under control until drainage of the fields (Kramer et al., 1988). Davey and Meisch (1977a, 1977b) showed that the mosquitofish, at inundative release rates of 4800 fish per hectare, was effective for control of Psorophora columbiae (Dyar & Knab) in Arkansas rice fields. Fish released at the water flow inlets dispersed quickly throughout the fields. This is an important attribute for controlling species of Psorophora and Aedes, whose hatch and larval development are completed within a few days. A combination of 1200 G. affinis and about 300 sunfish (Lepomis cyanellus Rafinesque) gave better control than either four times the amount of G. affinis or L. cyanellus used separately. This synergistic effect reduces logistic problems associated with having enough fish available at the times fields are inundated. B laustein (1986) found enhanced control of A. freeborni by mosquitofish in California rice fields after the addition of green sunfish. He speculated that the increased control was the result of the mosquitofish spending more time in protected areas where mosquitoes were more abundant and the green sunfish was avoided. The availability of fish for stocking fields either inundatively, such as in Arkansas, or for control later in the season, as practiced in California, has been a fundamental reason why fish have not been used more extensively in rice fields. A unique use of the mosquitofish by inundative release was reported by Farley and Caton (1982). These workers released fish in subterranean urban storm drains to control C. quinquefasciatus Say breeding in entrapped water at low points in the system. Fish releases were made following the last major rains to avoid having them flushed out of the system. Fish survived for more than 3 months during the summer and were found throughout the system. Gravid females produced progeny. However, no mating occurred, and after the initial increase in numbers, populations of fish diminished as summer progressed. Reduction of mosquitoes from 75 to 94% were observed for 3 months compared with untreated areas (Mulligan et al., 1983). This control practice is now conducted on a routine basis by the Fresno Mosquito Abatement District (J. R. Caton, personal communication 1987). Although G. affinis has been useful for control of mosquitoes in a number of situations, clearly there are drawbacks to its use. In fact, if today's environmental awareness existed at the turn of the century, this fish probably never would have been intentionally introduced into exotic areas (Pelzman, 1975; Lloyd, 1987). The major objection to this fish has been its direct impact on native fish through predation, or its indirect impact through competition (Bay et al., 1976; Schoenherr, 1981; Lloyd, 1987). More than 30 species of native fish have been adversely affected by the introduction of Gambusia (Schoenherr, 1981; Lloyd, 1987).

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Gambusia, a general predator, can also substantially reduce zooplankton and thus lead to algal blooms in certain situations (Hurlbert et al., 1972). Introductions of Gambusia have also reduced numbers of other aquatic invertebrates coinhabiting the same waters (Hoy et al., 1972; Farley & Younce, 1977; Rees, 1979; Waiters & Legner, 1980; Hurlbert & Mulla, 1981). The next most widely used fish for mosquito control is the common guppy, Poecilia reticulata (Peters). It has been deployed successfully in Asia for the control of wastewater mosquitoes, especially C. quinquefasciatus. Like its poeciliid relative, Gambusia, it is native to the Americas (tropical South America). However, instead of being intentionally introduced to control mosquitoes, it was taken to other parts of the world by tropical fish fanciers. Sasa et al. (1965) observed wild populations of this fish breeding in drains in Bangkok and concluded that it was controlling mosquitoes common to that habitat. The practical use of guppies is primarily restricted to subtropical climates because of an inability to tolerate temperate-zone water temperatures (Sasa & Kurihara, 1981). However, their most important attribute is a tolerance to relatively high levels of organic pollutants, which makes them ideal for urban water sources that are rich in organic wastes. In Sri Lanka, wild populations have been harvested and used for the control of mosquitoes in abandoned wells, coconut husk pits, and other sources rich in organics (Sasa & Kurihara, 1981). The fish occurs widely in India, Indonesia, and China and has been intentionally introduced for filariasis control into Rangoon and Burma (Sasa & Kurihara, 1981). On the Comoro Islands, it has shown good potential for the control of A. gambiae Giles in cisterns (Sabatinelli et al., 1990). Mian et al. (1985) evaluated its use for control of mosquitoes in sewage treatment facilities in southern California and concluded that guppies showed great potential for mosquito control in these situations. In Cuba, investigators have successfully controlled mosquitoes in polluted ditches and oxidation ponds with guppies (Koldenkova et al., 1988; Garcfa et al., 1991). Exotic fish have also been used for clearing aquatic vegetation from waterways, which has resulted in excellent mosquito control. In the irrigation systems of southeastern California, three species of subtropical cichlids, Tilapia zillii (Gervais), Oreochromis mossambica (Peters), and O. hornorum (Trewazas) were introduced and have become established over some 2000 ha of C. tarsalis breeding habitat (Legner & Sjogren, 1984). In this situation, mosquito populations are under control by a combination of direct predation and consumption of aquatic plants by these omnivorous fish (Legner & Medved, 1973; Legner 1978a, 1983; Legner & Fisher, 1980; Legner & Murray, 1981; Legner & Pelsue, 1980, 1983). As Legner and Sjogren (1984) indicate, this is a unique example of persistent biological control and is probably only applicable for relatively

sophisticated irrigation systems where a permanent water supply is assured, and water conditions are suitable to support the fish (Legner et al., 1980b). There is a threefold advantage in the use of these fish: (1) they clear vegetation to keep waterways open, (2) they control mosquitoes, and (3) they grow large enough to be caught for human consumption. Some sophistication is necessary when stocking these cichlids for aquatic weed control, which is often not understood by irrigation district personnel (Hauser et al., 1976, 1977; Legner, 1978b). Otherwise competitive displacement may eliminate T. zillii, the most efficient weedeating species (Legner, 1986). Household storage of water in open containers has frequently been the cause for outbreaks of human disease transmitted by Aedes aegypti (Linnaeus) in less developed parts of the word. While conducting A. aegypti surveys in Malaysia during the mid-1960s, one of us (Garcia) observed what were apparently P. reticulata guppies being utilized by town residents for the control of mosquitoes in bath and drinking water storage containers. The origin of this control technique was not clear, but it appeared to be a custom brought to the area by Chinese immigrants. Not all residents used fish, but those that did had no breeding populations of A. aegypti. Neng (1986) reported on the use of catfish of the Claris sp. for the control of A. aegypti in water storage tanks in coastal villages of southern China. This fish was considered appropriate because it was indigenous, edible, consumed large numbers of mosquito larvae; had a high tolerance for "adverse conditions"; and could be obtained from the local market. One fish was placed in each water source and later checked for its presence by larval survey teams about every 10 to 15 days. If fish were not found on inspection, the occupant was told to replace the fish or be fined. The investigation was conducted from 1981 to 1985, and surveys over this period showed a sharp initial reduction in A. aegypti followed by a low occurrence of the mosquito over the 4-year study period. Outbreaks of dengue were observed in neighboring provinces during this period, but not in the fishing villages under observation. The cost of the program was estimated to be about 1/15th that of indoor house spraying (Neng, 1986). Alio et al. (1985) described another use of a local species of fish for the control of a malaria vector similar to the method reported by Kligler (1930). Oreochromis sp., a tilapine, was introduced into man-made water catchment basins called "barkits" in this semiarid region of northern Somalia. These small scattered impoundments serve as the only sources of water during the dry season for the large pastoral population of the area. Anopheles arabiensis Patton, the vector of malaria in that area, is essentially restricted to these sites. Release of fish into the "barkits" dramatically reduced both the vector and nonvector populations of mosquitoes rather quickly. Treatment of the hu-

Chapter 37 BiologicalControl of Medical and Veterinary Pests

man population with antimalarial drugs during the initial phase of this 2-year study, combined with the lower vector population, reduced the transmission rate of malaria to insignificance over a 21-month period whereas the control villages remained above 10%. Alio et al. (1985) commented that the added benefits of reduced vegetation and insects in the water sources were also recognized by the local population. This resulted in community cooperation and was expected to further benefit the control strategy by providing assistance in fish distribution and maintenance as the program expanded to other areas. The last two examples involve the use of indigenous over exotic fish, where feasible, in vector control programs. There are other examples where native fish have been used in specialized circumstances or are being evaluated for such use (Kligler, 1930; Legner et al., 1974, 1975a, Menon & Rajagopalan, 1978; Walters & Legner, 1980; Ataur-Rahim, 1981, Luh, 1981, Koldenkova et al., 1988; Garcfa et al., 1991; Lounibos et al., 1992; Nelson & Keenan, 1992; Yaday et al., 1992; Fletcher et al., 1993). Lloyd (1987) argued that only indigenous fish should be employed for mosquito control because of the environmental disruption induced by exotics such as G. affinis. However, he suggested that native fish should be analyzed carefully for prey selectivity, reproductive potential, and effectiveness in suppressing pest populations before attempting their use. Lloyd (1987) also pointed out that a mulfidisciplinary approach involving fishery biologists and entomologists should be employed when developing indigenous fish for mosquito control. However, in California where native pup fish in the genus Cyprinodon may afford a greater potential for mosquito control under a wider range of environmental stresses than afforded by Gambusia (Waiters & Legner, 1980), the California Department of Fish and Game discourages their use on the basis that unknown harmful effects might result to other indigenous fish. There is also the concern that certain rare species of Cyprinodon might be lost through hybridization. Perhaps China' s example of a multipurpose use of native fish for mosquito control and human protein source is the most resourceful strategy. This application for mosquito control is not new. Kligler (1930) used a tilapine fish to control Anopheles sp. in citrus irrigation systems in old Palestine, where farmers cared for the fish, consuming the larger ones. According to Luh (1981), the culture of edible fish for the purpose of mosquito control and human food is now widely encouraged in China. The old Chinese peasant custom of raising edible fish in rice fields has received greater attention in recent times because of the benefits made possible through this practice. The common carp, Cyprinus carpio Linnaeus, and the grass carp, Ctenopharygodon idella Valenciennes, are most commonly used. Fish are released as fry at the time rice seedlings are planted. Fields are specially prepared with a central "fish pit" and radiating ditches for refuge when water levels are low.

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Pisciculture in rice fields, as noted by Luh (1981), has three major benefits: (1) there is a significant reduction in culicine and to a lesser extent anopheline larvae, (2) fish are harvested as food, and (3) rice yields are increased apparently by a reduction in competitors and possibly by fertilization of the plants by fish excreta. Another group of fish, the so-called "instant" or annual fish (Cyprinodontidae), which are native to South America and Africa, have been considered as possible biological control agents for mosquitoes (Vanderplank, 1941, 1967; Hildemann & Wolford, 1963; Bay, 1965, 1972; Markofsky & Matias, 1979). The relatively drought-resistant eggs of these cyprinodontids, which allow them to utilize temporary water sources as habitat, would seem to make them ideal candidates for mosquito control. There is also some evidence that they do impact mosquito populations in native areas (Vanderplank, 1941; Hildemann & Wolford, 1963; Markofsky & Matias, 1979). Research on the biology and ecology of several species has been conducted; however, there are no published accounts, to our knowledge, on the successful use of these fish in field situations. In California, the South American species Cynolebias nigripinnis Regan and C. bellottii (Steindachner) survived the summer in rice fields, but no reproduction was observed over a 3-year period (Coykendall, 1980). It was speculated that they may play a future role in California's mosquito control program in temporary pools and possibly in rice fields. Cynolebias bellottii was observed to reproduce repeatedly and to persist in small, intermittently dried ponds in Riverside, California, for 11 consecutive years, 1968 to 1979 (E. F. Legner, personal communication, 1999). Four drying and flooding operations over 2 months were required to eliminate this species from ponds that were to be used for native fish studies (Waiters & Legner, 1980). It seems logical, given the biological capability of surviving an annual dry period, that these fish could be successfully integrated into mosquito control programs, especially in newly created water sources in geographic areas where they naturally occur (Vaz-Ferreira et al., 1963; Anonymous, 1981; Gerberich, 1985). Arthropods

Numerous species of predatory arthropods have been observed preying on mosquitoes, and in some cases, are believed to be important in controlling mosquito populations (James, 1964; Service, 1977; Collins & Washino, 1979; McDonald & Buchanan, 1981). However, among the several hundred predatory species observed, only a few have been used in a manipulative way to control mosquitoes. Dragonflies, sometimes referred to as mosquito hawks, were one of the first arthropods to be examined before the turn of the century. Difficulties in colonization, production, and handling have restricted their use to experimental ob-

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servation. It is unlikely that they will be used extensively (Lamborn, 1890; Beesley, 1974; E1Rayah, 1975; Riviere et al., 1987a). There are a few cases where the difficulties associated with the manipulative use of arthropods have been at least partly overcome. More than 50 years ago, in a classic use of biological control, the mosquito Toxorhynchites, whose larvae are predators of other mosquitoes, was released on several Pacific Islands in an effort to control natural and artificial container breeding mosquitoes such as A. aegypti and A. albopictus (Skuse) (Paine, 1934; Bonnet & Hu, 1951; Peterson, 1956). The releases were not considered successful; however, the mosquitoes did establish in some areas (Steffan, 1975). Several reasons given to explain why these releases failed were low egg production, lack of synchrony between predator and prey life cycles, and selection of only a relatively small number of prey breeding sites (Muspratt, 1951; Nakagawa, 1963; Trpis, 1973; Bay, 1974; Riviere, 1985). Although not apparently a suitable predator in the classical sense, there is still interest in the use of various Toxorhynchites spp. for inundative release (Gerberg & Visser, 1978). Trpis (1981), working with T. brevipalpis (Theobald), showed that the high daily consumption rate and long survival of the larvae without prey made it a prime candidate for biological control use. Observations on adult females indicated a 50% survivorship over a 10-week period with a relatively high oviposition rate per female. All these preceding attributes suggest that this species would be useful for inundative release programs against container breeding mosquitoes. Studies by Focks et al. (1979) in Florida, working with T. r. rutilis Coquillett, showed that this species had a high success rate in artificial breeding containers. In a 12.6-ha residential area, about 70% of the available oviposition sites were located over a 14-day period by two releases of 175 females. Mass-culturing techniques have been developed for this species and T. amboinensis (Doleschall) (Focks & Boston, 1979; Riviere et al., 1987b). Focks et al. (1986), working with T. amboinensis, reported that release of 100 females per block for several weeks, combined with ultra low volume (ULV) application of malathion, reduced A. aegypti populations by about 96% in a residential area of New Orleans. The Toxorhynchites releases and not the insecticide treatment apparently accounted for most of the reduction. These workers noted that the procedure could be further refined by reducing both the number of predators and malathion applications without lowering efficacy. Mosquitoes such as A. aegypti and A. albopictus, which breed in and whose eggs are dispersed via artificial containers, pose major health hazards as vectors of human diseases throughout much of the warmer climates of the world. The massive quantities of containerized products and rubber tires that are discarded without care or are stockpiled, have given these mosquito species a

tremendous ecological advantage. The establishment and extensive spread of A. albopictus in the United States underline this point (Sprenger & Wuithironyagool, 1986). The apparent inability of governments to appropriately control disposal of these containers and difficulties in location once they are discarded makes inundative releases of Toxorhynchites, either alone or in combination with other control tactics, a much more plausible approach (Focks et al., 1986; Riviere et al., 1987a; Miyagi et al., 1992; Tikasingh, 1992; Tikasingh & Eustace, 1992; Toma & Miyagi, 1992). Notonectids are voracious predators of mosquito larvae under experimental conditions (Ellis & Borden, 1970; Garcia et al., 1974; Hazelrig, 1974). Notonecta undulata Say and N. unifasciata Guerin have been colonized in the laboratory. In addition, the collection of large numbers of eggs, nymphs, and adults is feasible from such breeding sites as sewage oxidation ponds (Ellis & Borden, 1969; Garcia, 1973; Sjogren & Legner, 1974; Hazelrig, 1975; Miura, 1986). Some studies have been conducted on storage of eggs at low temperatures; however, viability decreased rapidly with time (Sjogren & Legner, 1989). At present, the most feasible use of these predators appears to lie in the recovery of eggs from wild populations on artificial oviposition materials and their redistribution to mosquito breeding sites. Such investigations were conducted in central California rice fields by Miura (1986). Floating vegetation such as algal mats and sometimes duckweed (Lemna spp.) form protective refugia for mosquito larvae; and consequently, populations of mosquitoes can be high in the presence of notonectids (Garcia et al., 1974). It appears that colonization and mass production costs, coupled with the logistics of distribution, handling, and timing of release at the appropriate breeding site, are almost insurmountable problems for routine use of notonectids in mosquito control. In addition to insect predators, several crustaceans feed on mosquito larvae. Among these are the tadpole shrimp, Triops longicaudatus (LeConte), and several copepod species. Mulla et al. (1986) and Tietze and Mulla (1987, 1991), investigating the tadpole shrimp, showed that it was an effective predator under laboratory conditions and speculated that it may play an important role in the field against floodwater Aedes and Psorophora species in southern California. Drought resistance in predator eggs is an appealing attribute for egg production, storage, and manipulation in field situations against these mosquitoes. However, synchrony in hatch and development between the predator and the prey is crucial if this is to be a successful biological control agent for the rapidly developing Aedes and Psorophora spp. In addition, the tadpole shrimp is considered an important pest in commercial rice fields. Miura and Takahashi (1985) reported that Cyclops vernalis Fisher was an effective predator on early-instar Culex tarsalis larvae in the laboratory. These workers speculated

Chapter 37

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Biological Control of Medical and Veterinary Pests

that copepods could have an important role in suppressing mosquito populations in rice fields because of their feeding behavior and abundance. Another crustacean with promise for more extensive application is cyclopoid predator Mesocyclops aspericornis Daday (Riviere et al., 1987b; Lardeux et al., 1992). Work by Riviere and colleagues has indicated reductions of A. aegypti and A. polynesiensis Marks by more than 90% after inoculative release of this organism into artificial containers, wells, tree holes, and land crab burrows. Although not able to withstand desiccation, this small predator has persisted almost 2 1/2 years in crab holes and up to 5 years in wells, tires, and tree holes under subtropical conditions. This species can be mass-produced, but its occurrence in large numbers in local water sources allows for the inexpensive and widespread application to mosquito breeding sites in Polynesia (Riviere et al., 1987a,b). The species is also very tolerant of salinities greater than 50 parts per thousand. The benthic feeding behavior of Mesocyclops makes it an effective predator of the bottom-foraging Aedes, but limits effectiveness against surface-foraging mosquitoes. Riviere et al. (1987a, 1987b) believed that the effectiveness against Aedes is due to a combination of predation and competition for food. Perhaps the greatest utility of this Mesocyclops will lie in the control of crab hole breeding species, such as A. polynesiensis in the South Pacific. Further investigations may uncover additional cyclopods that can impact other mosquito species (Kay et al., 1992). The most important nonarthropod invertebrate predators to draw attention for mosquito control are the turbellarian flatworms and a coelenterate. Several flatworm species have been reported to be excellent predators of mosquito larvae in a variety of aquatic habitats (Legner & Medved, 1974; Yu & Legner, 1976; Legner, 1977, 1979; Collins & Washino, 1978; Case & Washino, 1979; Ali & Mulla, 1983; George et al., 1983). Several biological and ecological attributes of flatworms would seem to make them ideal candidates for manipulative use: these flatworms have ease of mass production, overwintering embryos, effective predatory behavior in shallow waters with emergent vegetation, on-site exponential reproduction following inoculation (Medved & Legner, 1974; Tsai & Legner, 1977; Legner & Tsai, 1978; Legner, 1979), and tolerance to environmental contaminants (Levy & Miller, 1978; Nelson, 1979). Collins and Washino (1978) and Case and Washino (1979) hypothesized that flatworms, particularly Mesostoma, may play an important role in the natural regulation of mosquitoes in some California rice fields because of their densities and their predatory attack on mosquito larvae in sentinel cages. Preliminary analysis showed a significant negative correlation between the presence of flatworms and population levels of C. tarsalis and Anopheles freeborni

(Case & Washino, 1979). However, these workers cautioned that an alternative hypothesis related to the ecology of these species may have accounted for the correlations. Later investigations by Palchick and Washino (1984) were not able to confirm the correlations between flatworms and mosquito populations. However, the enormity of the problem associated with sampling in California rice fields, coupled with the complexity of the prey and predator interactions, makes further studies necessary before the role of flatworms in rice fields can be clearly established. The important attributes for manipulative use of flatworms mentioned earlier raise the question of why they have not been developed further for use in mosquito control. Perhaps the contemporary development of Bacillus thuringiensis var. israelensis (B.t.i.) DeBarjac (H- 14)-- a highly selective, easily applied, microbial insecticidem may have been at least partially responsible for slowing further work and development of these predators. Their mass culture must be continuous and demands skilled technical assistants (Legner & Tsai, 1978). Their persistence in field habitats may also depend on the presence of other organisms such as ostracods that can be utilized for food during low mosquito abundance (Legner et al., 1976). The coelenterates, like the flatworms, showed great promise for further development and use in selected breeding habitats. Chlorohydra viridissima (Pallas) is efficient in suppressing culicine larvae in ponds with dense vegetation, and this species also can be mass-produced (Lenhoff & Brown, 1970; Yu et al., 1974a, 1974b, 1975). However, like the flatworms, work on these predators has waned, perhaps for reasons similar to those speculated for the flatworms. Microbial pesticides can be employed over an extensive range of different mosquitobreeding habitats.

Fungi The most promising fungal pathogen is a highly selective and environmentally safe oomycete, Lagenidium giganteum Couch. First tested for its pathogenicity to mosquitoes in the field by McCray et al. (1973), it has been applied by aircraft to rice fields (Kerwin & Washino, 1987). Lagenidium develops asexually and sexually in mosquito larvae and is capable of recycling in standing bodies of water. This creates the potential for prolonged infection in overlapping generations of mosquitoes. Lagenidium may also remain dormant after the water source has dried up and then may become active again when water returns. The sexually produced oospore offers the most promising stage for commercial production because of its resistance to desiccation and long-term stability. However, problems in production and activation of the oospores still remain (Axtell et al., 1982; Merriam & Axtell, 1982a, 1982b, 1983; Jaronski & Axtell, 1983a, 1983b; Jaronski et al., 1983; Kerwin

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~ Garcia and E. F. Legner

et al., 1986; Kerwin & Washino, 1987). Field trials with

the asexual oospore and the sexual zoospore indicate that this mosquito pathogen is near the goal of practical utilization. Kerwin et al. (1986) report that the asynchronous germination of the oospore is of particular advantage in breeding sources where larval populations of mosquitoes are relatively low, but recruitment of mosquitoes is continuous due to successive and overlapping generations, as in California rice fields. The germination of oospores over several months provides long-term control for these continuous low-level populations. In addition, the asexual zoospores arising from the oospore-infected mosquito are available every 2 to 3 days to respond in a density-dependent manner to suppress any resurging mosquito population. This stage survives about 48 hours after emerging from the infected host. Kerwin et al. (1986) indicate that laboratory fermentation production of the asexual stage of Lagenidium for controlling mosquitoes in the field is approaching the development requirements and costs for the production of B.t.i. A distinct advantage of this pathogen over B.t.i. is its potential to recycle through successive host generations. The disadvantage of the asexual stage is that it is relatively fragile, cannot be dried, and has a maximum storage life of only 8 weeks (Kerwin & Washino, 1987). Thus, the focus of attention for commercial production by Kerwin and colleagues is on the oospore, which is resistant to desiccation and can be easily stored. Axtell and Guzman (1987) have encapsulated both the sexual and asexual stages in calcium alginate and have reported activity against mosquito larvae after storage for up to 35 and 75 days, respectively. Further refinement in techniques of production and encapsulation might make this approach a viable option for future commercial production and application. Limitations on the use of this pathogen include intolerance to polluted water, salinity, and other environmental factors (Jaronski & Axtell, 1982; Lord & Roberts, 1985; Kerwin & Washino, 1987). However, there are numerous mosquito breeding sources where these limitations do not exist; therefore, we should expect to see this selective and persistent pathogen available for routine mosquito control in the future. The fungus Culicinomyces clavosporus Couch, Romney & Rao, first isolated from laboratory mosquito colonies and later from field habitats, has been under research and development for more than a decade (Sweeney et al., 1973; Couch et al., 1974; Russel et al., 1979; Frances et al., 1985). The fungus is active against a wide range of mosquito species and also causes infections in other aquatic Diptera (Knight, 1980; Sweeney, 1981). The ease of production with relatively inexpensive media in fermentation tanks is an extremely desirable trait. However, problems in storage must be overcome if this fungus is to be widely used. Perhaps a drying process, now being investigated,

will solve storage requirements (Sweeney, 1987). Although the fungus has high infection rates in field trials, dosage rates have been high and appreciable persistence at the site has not been demonstrated (Lacey & Undeen, 1986; Sweeney, 1987). For a more thorough review of this pathogen, see Sweeney et al. (1973), Lacey and Undeen (1986), and Sweeney (1983, 1987). Various species of Coelomomyces have been studied over the last two decades for use in mosquito control. Natural epizootics with infection rates in excess of 90% have been recorded. These fungi persist in certain habitats for long periods; however, factors triggering outbreaks in these situations are not well understood (Chapman, 1974). Some field testing has been done, but results have been highly variable (Federici, 1981). In general, difficulties associated with the complex life cycle of these fungi have encumbered research on them. Federici (1981) and Lacey and Undeen (1986) have reviewed the potential of these fungi for mosquito control. Nematodes Among the various nematodes pathogenic for mosquitoes, R o m a n o m e r m i s culicivorax Ross & Smith has received the most attention (Petersen & Willis, 1970, 1972a, 1972b, 1975; Brown & Platzer, 1977; Brown et al., 1977; Poinar, 1979; Petersen, 1980a, 1980b; Brown-Westerdahl et al., 1982; Kerwin & Washino, 1984). This mermithid, which is active against a wide range of mosquito species, has been mass-produced (Petersen & Willis, 1972a) and has been utilized in a number of field trials. The nematode was commercially produced and sold under the name Skeeter Doom| however, according to Service (1983), eggs showed reduced viability in transport and the product currently is no longer sold. However, the nematode's ability to recycle through multigenerations of mosquitoes and overwinter in various habitats, including drained, harvested, stubble-burned, cultivated, and replanted rice fields, are strong attributes favoring its further research and development for biological control (Petersen & Willis, 1975; Brown-Westerdahl et al., 1982). Several field applications have produced good results and have included both the preparasitic stage and post-parasitic stages, with the former being more applicable for the "quick kill" and the latter being more long-term for continuous control such as in California rice fields (Petersen et al., 1978a, 1978b; Levy et al., 1979; Brown-Westerdahl et al., 1982). Some drawbacks to its widespread use include intolerance to low levels of salinity, polluted water, and low oxygen levels; predation by aquatic organisms; and potential for development of resistance by the host (Petersen & Willis, 1970; Brown & Platzer, 1977; Brown et al., 1977; Petersen, 1978; Brown-Westerdahl, 1982). However, these environmental problems are not generally an issue for anopheline control.

Chapter 37 BiologicalControl of Medical and Veterinary Pests For control of these species the cost of in vivo mass production clearly stands as the major drawback for this pathogen. Perhaps its most plausible use will be in specialized habitats integrated with other control strategies (Brown-Westerdahl et al., 1982). Bacteria

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over the last few years as a potential biological control agent for container-breeding mosquitoes (Egeter et al., 1986; Washburn & Anderson, 1986). Desiccation-resistant cysts allow persistence of the ciliate from one year to the next. Currently, in vitro production methods are being developed and small field trials are being initiated to determine its efficacy and practicability for field use (Anderson et al., 1986a, 1986b).

The spore-forming bacterial pathogen B.t.i. (H-14) was isolated by Goldberg and Margalit (1977) and the produced toxin has been demonstrated by numerous studies to be an effective and environmentally sound microbial insecticide against mosquitoes and blackflies. Its high degree of specificity and toxicity, coupled with its relative ease of production, has made it the most widely used commercial product to date for mosquito and blackfly control. Several formulations are currently available from commercial firms throughout the world. Its efficacy under different environmental conditions and problems associated with its use have been reviewed by Garcia and Sweeney (1986), Lacey and Undeen (1986), Garcia (1987), de Barjac and Sutherland (1990), Priest (1992), and Becker and Margalit (1993). Another spore-forming bacterium, Bacillus sphaericus Neide, has also shown great promise as a larvicide against certain mosquito species (Mulla et al., 1984). In general, several strains of this pathogen show a much higher degree of toxic variability among species of mosquitoes. Culex spp. appear to be highly susceptible, whereas other species such as Aedes aegypti are highly refractory. Unlike the ephemeral larvacidal activity of B.t.i. toxin, some strains of B. sphaericus have shown persistence in certain habitats (Des Rochers & Garcia, 1984; Matanmi et al., 1990). For further detail, see reviews by Lacey and Undeen (1986), de Barjac and Sutherland (1990), and Priest (1992).

These flies, the most important of which are muscoid species, can be defined broadly as those most closely associated with human activities. Breeding habitats vary from the organic wastes of urban and rural settlements to those provided by various agricultural practices, particularly ones related to the management and care of domestic and range animals. Their degree of relationship to humans varies considerably with the ecology and behavior of the fly involved. Some are more often found inside dwellings (endophilic) while others remain mostly outdoors (exophilic). The discussion that follows separates these flies by their general endophilic and exophilic habits. This discussion is restricted to brief comments because the potential for biological control of these flies has been reviewed by Legner et al. (1974), Bay et al. (1976), and Legner (1986).

Protozoa

Endophilic Flies

A large number of protozoa have been isolated from mosquitoes and other medically important arthropods (Roberts et al., 1983; Lacey & Undeen, 1986). Of this assemblage, the microsporidians have been studied rather intensively. Because of their complex life cycle and the in vivo production methods necessary for maintaining them, research on their practical utility has been limited. However, as Lacey and Undeen (1986) point out, if more information is developed on their life cycle, it may be found that they could play a role in suppressing mosquitoes through inoculative and augmentative releases in certain habitats. Among other protozoa that show promise is endoparasitic ciliate Lambornella clarki Cofliss & Coats, a natural pathogen of the tree hole mosquito, Aedes sierrensis (Ludlow). This pathogen has received considerable attention

Povolny (1971) describes these flies as primarily dependent on human and domestic animal wastes. Musca domestica Linnaeus is by far the best known example; however, some Drosophila and Psychoda spp. also fall into this category. Certain Fannia spp. are more on the periphery but also are included here. The common housefly, M. domestica, has been a constant associate of humans over much of our modern history. Attempts to control its populations by biological means have been extensive and on occasion successful in special situations. More frequently, they have failed to reduce numbers to acceptable levels. It should be emphasized that control of M. domestica populations, as well as most other endophilic flies pestiferous to humans, would be largely unnecessary if waste products produced by human activities could be appropriately managed. Because this is not the

Viruses Numerous pathogenic viruses have been isolated from mosquitoes and blackflies. However, to date none look promising for practical use in control (Lacey & Undeen, 1986).

SYNANTHROPIC DIPTERA

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case, efforts toward the biological control of these species have continued. Starting around the turn of this century to approximately 1968, biological control of these flies was attempted by the introduction of a broad range of different natural enemies into areas where the flies presented problems. The Pacific Islands were a focus of much attention with the introduction of dung beetles, several parasitoids, and predators during this period. It was believed that the accidental introduction of the ant Pheidole megacephala Fabricius, combined with the introduction of the coprophagous dung beetle, Hister chinensis Quensel, caused significant fly reductions on the islands of Fiji and Samoa (Simmonds, 1958). The Hawaiian islands had 16 introductions from 1909 to 1967, of which 12 became established. However, the exact role of these natural enemies in overall regulation of flies on the islands is still not well understood (Legner et al., 1974; Legner, 1978c). Rodriguez and Riehl (1962), in California, used the novel and successful approach of chicken cockerels as direct predators of fly larvae in chicken and rabbit manure. However, this technique is utilized very little today because of the threat that roving birds pose to the spread of avian pathogens. Research over the last two decades has been centered on the more highly destructive parasitoid and predatory species. Examples, such as the encyrtid Tachinaephagus zealandicus Ashmead, five species of the pteromalid genus Muscidifurax, and Spalangia sp., were evaluated for their capabilities of attacking dipterous larvae and pupae in various breeding sources. They are believed to be capable of successful fly suppression if the fight species and strains are applied in the fight locality (Legner & Brydon, 1966; Legner & Dietrick, 1972, 1974; Morgan et al., 1975, 1977; Olton & Legner, 1975; Pickens et al., 1975; Morgan & Patterson, 1977; Rutz & Axtell, 1979; Gold & Dahlsten, 1981; Propp & Morgan, 1985; Axtell & Rutz, 1986; Legner, 1988b; Mandeville et al., 1988; Pawson & Petersen, 1988). Other approaches have included the use of pathogens and predatory mites, and inundative releases of parasitoids and predators (Ripa, 1986). Although partially successful, none of these strategies has become the sole method for fly control, and the wrong choice of a parasitoid strain may have detrimental results (Legner, 1988b). Instead, the focus is on integrated controls including other methods such as cultural, adult baiting, and aerosol treatments with short residual insecticides. However, it is generally agreed that existing predatory complexes exert great influences on fly densities (Legner et al., 1975b, 1980a; Geden, 1984; Geden et al., 1987, 1988; Geden & Axtell, 1988), that many biological control agents of endophilous flies have not been thoroughly surveyed, and that their potential has not been adequately assessed (Mullens, 1986; Mullens et al., 1986).

Exophilic Flies These species include flies that persist in nature in the absence of humans, but whose populations can increase dramatically as a result of certain human activities such as providing more breeding habitat. They include several species in the genera Calliphora, Hippelates, Musca, Muscina, Phaenicia, Stomoxys, and others. Some success has been recorded with the use of natural enemies against the calliphorid species in California and Hawaii, but attempts elsewhere in the world have not been effective (Bay et al., 1976). The braconid parasitoid Alysia ridibunda Say, indigenous to parts of the United States, was released into an area of Texas new to its range and did parasitize the blowflies, Phaenicia sericata (Meigen), and a Sarcophaga species. However, the parasitoid did not maintain control and became rare within a couple of years (Lindquist, 1940). The gregarious parasitoid. T. zealandicus, may have considerable potential for biological control of exophilic flies (Olton & Legner, 1975). The range of habitats utilized by this natural enemy is considered unparalleled by any other fly parasitoid. However, extensive field work with this genus has not been given much attention. However, one species, T. stomoxcida Subba-Rao, provides overall permanent reductions of Stomoxys in Mauritius (Greathead & Monty, 1982). The complex of problems that confronts field programs in biological control of exophilic flies has clearly had a dampening effect on research in this area. The unforeseen problems associated with attempts to biologically control the eye gnat, Hippelates collusor (Townsend), in California exemplify those problems. In the early 1960s, a concerted effort was mounted to control this gnat with the use of both indigenous and exotic parasitoids in orchards in southern California. About a dozen species and strains were evaluated for several years. Some of the exotics became established, but eye gnat reductions were obvious only where cultivation practices were curtailed (Legner et al., 1966; Legner, 1970). Cultivation of the orchards buried the larvae and pupae of the eye gnat below the search zone of the parasitoids and cultivation also removed vegetation that offered the parasitoids protection and possibly nutrients (Legner, 1968; Legner & Olton, 1969; Legner & Bay, 1970). Buried eye gnats emerged from several centimeters below the soil surface and thus continued to pose a serious problem (Bay et al., 1976). The discovery of a group of genes, tentatively called "wary genes," in parasitoids of synanthropic Diptera affords greater opportunities for biological control (Legner, 1987, 1988a, 1989, 1993). Inheritance of quantitative behavior associated with gregarious oviposition and fecundity in the South American parasitoid Muscidifurax raptorellus Kogan & Legner is accompanied by unique extranuclear influ-

Chapter 37

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ences that cause changes in the oviposition and larval survival phenotypes of females prior to the production of their progeny (Legner, 1989). Males can change a female's fecundity phenotype when mating, by transferring an unknown substance. Some genes in the female apparently have the phenotypic plasticity to change expression under the influence of substances in the male seminal fluid. The intensity of this response depends on the genetic composition of the male and female. Full expression occurs in the F1 virgin female (Legner, 1989). The mated female receives a message from the male after mating that expresses his genome for the presence or absence of polygenes governing quantitative behavior, such as fecundity. The discovery of this behavior in M. raptorellus has opened questions into the stability of polygenic loci (Legner, 1993). The ability of the male substance to apparently switch loci on or off in the female suggests active and inactive states for such loci. Polygenic loci generally are occupied by genes coded for a fixed kind of expression. Greater importance may be placed on liberated males during mass release strategies that seek seasonally to accelerate and increase the magnitude of parasitism, because it may be possible to convey directly to unmated females already resident in the environment certain desirable strain characteristics. In the process of hybridization, wary genes may serve to quicken the pace of evolution by allowing natural selection to begin to act in the parental generation (Legner, 1987, 1988a). Tabanidae, or horseflies, although widespread and on occasion serious pests and vectors of disease to livestock, have not received much attention. Only one successful inundative release of egg parasitoid Phanurus emersoni Girault has been recorded (Parman, 1928). Apparently, this effort was precipitated by a severe outbreak of anthrax at the time and because this disease diminished and other control tactics are available, interest in their biological control has not been fostered. Of the flies associated with cattle droppings, symbovine flies (Povolny, 1971) have received the most attention for biological control over the last two decades. The primary targets for control have been the bush fly, Musca vetustissima Walker; the horn fly, Haematobia irritans (Linnaeus); and the face fly, Musca autumnalis DeGeer (Wallace & Tyndale-Biscoe, 1983; Ridsdill-Smith et al., 1986; RidsdillSmith & Hayles, 1987). The primary emphasis of control has been on habitat destruction through the use of introduced dung-burying scarab beetles. Biological control through dung destruction has been reviewed by Legner (1986). Although the importation and introduction of dung beetles have clearly aided agriculture by reducing operating costs and increasing grazing areas through dung removal, they have not had a great impact on the densities of flies in any area. Because there are no practical nonbiological control methods to reduce fly numbers and because the addition

of more scarabs may actually exacerbate the problem, we believe that the most logical direction for research is to intensify worldwide search for more effective natural enemies, especially predators and pathogens. A number of pathogens have been isolated from various species of muscids and some studies have been conducted evaluating their role as control agents. For example, the exotoxin of B.t. Berliner has been reported to reduce fly production under certain conditions. However, only a few of these agents appear to show great promise for manipulative use (Daoust, 1983a, 1983b; Mullens, 1986; Mullens et al., 1987a, 1987b, 1987c.)

SNAILS Berg (1973), Bay et al. (1976), Garcia and Huffaker (1979), and McCullough (1981) have reviewed developments in biological control of mainly freshwater snails, especially as they relate to the transmission of trematode parasites of humans and their domestic animals. Discussion here is restricted to some pertinent points of those reviews and to some developments that have occurred since their completion.

Predators Many general predators, including species of fish, frogs, birds, and certain aquatic insects, consume freshwater snails. Domestic ducks have been used with some success in China by herding them through rice fields to forage for food. However, of all these general predators, only certain tilapine fish have been given research consideration as possible biological control agents. Fish in the genera Oreochromis, Sarotherodon, and Tilapia feed directly on snails during various stages of their life cycle. This occurs primarily because the feeding behavior of these fish is frequently in the vegetation/detrital zone that is also utilized for feeding by snails. Larger adult species of Oreochromis and Sarotherodon feed directly on adult snails but this predation has not been observed for Tilapia adults. Tilapia adults only consume snails incidentally during their normal foraging on plant materials (Roberts & Sampson, 1987). Possibly the greatest impact of these fish on snail populations is through competition for resources. Roberts and Sampson (1987) state that, in general, Tilapia spp. compete directly with the snails that feed on higher plants while Oreochromis competes with snails that feed on algae. In addition to competition for food, these fish alter the habitat, and therefore have a disruptive effect on the snails' life cycle (habitat modification); see Roberts & Sampson (1987) for details of culturing techniques and other biological and ecological attributes of the various tilapiine species.

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Certain species of sciomyzid flies are probably the most host-specific predators of snails. Several hundred species have been described, of which the larvae depend on mollusks for food. Of six species released in Hawaii primarily against Lymnaea ollula Gould, the intermediate host of cattle liver flukes (Fasciola spp.), twomSepedon sauteri Walker and S. macropus Hendel - - were partially successful as indicated by a reduction in liver infections at slaughterhouses (Bay et al., 1976; Garcia & Huffaker, 1979). Berg (1973) emphasized that because there are several hundred species in this family with a wide range of biological attributes, they offer great opportunity for matching a certain sciomyzid with the appropriate ecotype snail. Unfortunately, the scope of opportunities for use of these flies for snail control has not been given the attention it deserves.

Antagonists Another approach for control of snails has been through interspecific competition. The large predatory snail, Marisa cornuarietis Linnaeus, has been evaluated rather extensively in Puerto Rico and has demonstrated effectiveness for control of Biomphalaria glabrata Say, the intermediate host of human schistosomiasis, in certain habitats, especially ponds. Suppression of B. glabrata by Marisa is primarily due to competitive feeding and to incidental predation on the immature stages of this snail (McCullough, 1981; Madsen, 1990). Elsewhere in the Caribbean, the thiarid snails Melanoides tuberculata (Miiller) and Thiara granifera (Lamarck) have spread after introduction and have reduced B. glabrata populations in certain areas (Madsen, 1990). In Africa, M. cornuarietis eliminates three species of pulmonate snails (Biomphalaria sp., Bulinis sp., and Lymnaea sp.) in a water impoundment in northern Tanzania. Prior to release of M. cornuarietis, the three pulmonate species, in addition to a melaniid snail, Melanoides sp., existed in large, thriving populations. Two years after the introduction, only M. cornuarietis and the melaniid snail remained, the latter in population densities similar to preintroduction levels (Nguma et al., 1982; Madsen, 1990). No adverse environmental effect was recorded in this situation; however, the authors stressed that a careful examination of potential environmental risks should be made before introduction to a new area. Another competitor snail, Helisoma duryi (Wetherby), has promise for the control of B. glabrata. Christie et al. (1981) working with the ram's horn snail, H. duryi, showed that it controlled B. glabrata in artificial outdoor drains on the Caribbean Island of St. Lucia. The elimination of B. glabrata may have been due to inhibition of reproduction by adults and possibly to increased mortality of immature snails. The time required for elimination was related to environmental temperature and the number of H. duryi ini-

tially released. In Africa, Madsen (1983) surveyed H. duryi as an introduced species in an irrigation scheme in northern Tanzania and found it restricted to just a few drains 10 years after it had been established in the area. He noted that its failure to spread may have been related to the routine molluscacide applications to the irrigation canal system. Moens (1980, 1982) achieved successful biological control of L. truncatula Mtiller, an intermediate host of the trematode Fasciola hepatica Linneaus in watercress in Belgium, with the predatory snail Zonitoides nitidus Miiller. Predation was related to temperature, soil moisture, and cover. It is obvious from this review that the role of biological control of snails as intermediate hosts of human diseases is limited. McCullough (1981) believed it to be restricted to specific situations and not to have widespread applicability. We conclude that the natural-enemy component is to play a supportive role in almost all geographic areas where schistosomiasis and other snail-transmitted diseases exist, because any method that reduces transmission of a disease in a self-sustaining fashion is of major benefit to a community.

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Chapter 37

Biological Control of Medical and Veterinary Pests

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the biological control of Aedes and Culex vectors (Diptera: Culicidae) breeding in crab holes, tree holes, and artificial containers. Journal of Medical Entomology, 24, 425-430. Riviere, F., Sechan, Y., & Kay, B. H. (1987b). The evaluation of predators for mosquito control in French Polynesia. In T. D. St. George, B. H. Kay, & J. Blok (Eds.), Proceedings of the Fourth Symposium on Arbovirus Research in Australia (1986) (pp. 150-154). Brisbane, Australia: Q.I.M.R. Roberts, D. W., Daoust, R. A., & Wraight, S. P. (1983). Bibliography on pathogens of medically important arthropods (1981) (WHOVBC/83.1). Geneva: World Health Organization. Roberts, J., & Sampson, D. R. T. (1987). Data sheet on biological control agents: Tilapiine fish (WHO/VBC/945). Geneva: World Health Organization. Rodriguez, J. L., & Riehl, L. A. (1962). Control of flies in manure of chickens and rabbits by cockerels in southern California. Journal of Economic Entomology, 55,473-477. Russell, R. C., Debenham, M. L., & Lee, D. J. (1979). A natural habitat of the insect pathogenic fungus Culicimomyces in the Sidney area. Proceedings of the Linnean Society of New South Wales, 103, 71-73. Rutz, D. A., & Axtell, R. C. (1979). Sustained releases of Muscidifurax raptor (Hymenoptera: Pteromalidae) for house fly (Musca domestica) control in two types of caged layer poultry houses. Environmental Entomology, 8, 1105-1110. Sabatinelli, G., Majori, G., Blanchy, S., Fayaerts, P., & Papakay, M. (1990). Testing of the larvivorous fish, Poecillia reticulata in the control of malaria in the Islamic Federal Republic of the Comoros. World Health Organization WHO/MAL, 90, 1-10. Sasa, M., & Kurihara, T. (1981). The use of poeciliid fish in the control of mosquitoes. In M. Laird (Ed.), Biocontrol of medical and veterinary pests (pp. 36-53). New York: Praeger. Sasa, M., Harinasuta, C., Purived, Y., & Kurihara, T. (1965). Studies on mosquitoes and their natural enemies in Bangkok. III. Observations on a mosquito-eating fish "guppy," Lebistes reticulatus, breeding in polluted waters. Japanese Journal of Sanitation and Zoology, 23, 113127 (in Japanese). Schoenherr, A. A. (1981). The role of competition in the displacement of native fishes by introduced species. In R. J. Naiman & D. L. Stoltz (Eds.), Fishes in North American deserts (pp. 173-203). New York: Wiley Interscience. Service, M. W. (1977). Mortalities of the immature stages of species B of the Anopheles gambiae complex in Kenya: Comparison between rice fields and temporary pools, identification of predators and effects of insecticidal spraying. Journal of Medical Entomology, 13, 535-545. Service, M. W. (1983). Biological control of mosquitoes--has it a future? Mosquito News, 43, 113-120. Simmonds, H. W. (1958). The housefly problem in Fiji and Samoa. South Pacific Communications Quarterly Bulletin, 8, 29-30, 47. Sjogren, R. D., & Legner, E. F. (1974). Studies of insect predators as agents to control mosquito larvae, with emphasis on storage of Notonecta eggs. Proceedings of the California Mosquito Control Association, 42, 71-72. Sjogren, R. D., & Legner, E. F. (1989). Survival of the mosquito predator, Notonecta unifasciata (Hemiptera: Notonectidae) embryos at low thermal gradients. Entomophaga, 34(2), 201 - 208. Sprenger, D., & Wuithironyagool, T. (1986). The discovery and distribution of Aedes albopictus in Harris County, Texas. Journal of American Mosquito Control Association, 2, 217- 219. Steffan, W. A. (1975). Systematics and biological control potential of Toxorhynchites. Mosquito Systematics, 7, 59-67. Stewart, R. J., Schaefer, C. H., & Miura, T. (1983). Sampling Culex tarsalis immatures on rice fields treated with combinations of mosqui-

tofish and Bacillus thuringiensis H-14 toxin. Journal of Economic Entomology, 76, 91-95. Sweeney, A. W. (1981). Prospects for the use of Culicinomyces fungi for biocontrol of mosquitoes. In M. Laird (Ed.), Biocontrol of medical and veterinary pests (pp. 105-121). New York: Praeger. Sweeney, A. W. (1983). The time-mortality response of mosquito larvae infected with the fungus Culicinomyces. Journal of Invertebrate Pathology, 42, 162-166. Sweeney, A. W. (1987). Prospects of pathogens and parasites for vector control. In T. D. St. George, B. H. Kay, & J. Blok (Eds.), Proceedings, Fourth Symposium on Arbovirus Research in Australia (1986) (pp. 163-165). Brisbane, Australia: QTM.R. Sweeney, A. W., Lee, K. J., Panter, C., & Burgess, L. W. (1973). A fungal pathogen for mosquito larvae with potential as a microbial insecticide. Search, 4, 344-345. Tabibzadeh, I., Behbehani, C., & Nakhai, R. (1970). Use of Gambusia fish in the malaria eradication programme of Iran. Bulletin of the World Health Organization, 43, 623-626. Tietze, N. S., & Mulla M. S. (1987). Tadpole shrimp (Triops longicaudatus), new candidates as biological control agents for mosquitoes. California Mosquito Vector Control Association, Biological Briefs, 13(2), 1. Tietze, N. S. & Mulla, M. S. (1991). Biological control of Culex mosquitoes (Diptera: Culicidae) by the tadpole shrimp, Triops longicaudatus (Nostostraca: Tiopsidae). Journal of Medical Entomology, 28, 24-31. Tikasingh, E. S. (1992). Effects of Toxorhynchites moctezuma larval predation on Aedes aegypti populations: Experimental evaluation. Medical Veterinary Entomology 6, 266-271. Tikasingh, E. S., & Eustace, A. (1992). Suppression of Aedes aegypti by predatory Toxorhynchites moctezuma in an island habitat. Medical Veterinary Entomology 6, 272-280. Toma, T., & Miyagi, I. (1992). Laboratory evaluation of Toxorhynchites splendens (Diptera: Culicidae) for predation of Aedes albopictus mosquito larvae. Medical Veterinary Entomology 6, 281-289. Trpis, M. (1973). Interactions between the predator Toxorhynchites brevipalpus and its prey Aedes aegypti. Bulletin of the World Health Organization, 49, 359-365. Trpis, M. (1981). Survivorship and age specific fertility of Toxorhynchites brevipalpis females (Diptera: Culicidae). Journal of Medical Entomology, 18, 481-486. Tsai, S. C., & Legner, E. F. (1977). Exponential growth in culture of the planarian mosquito predator Dugesia dorotocephala (Woodworth). Mosquito News, 37, 474-478. Vanderplank, F. L. (1941). Nothobranchius and Barbus species: Indigenous antimalarial fish in East Africa. East African Medical Journal, 17, 431-436. Vanderplank, F. L. (1967). Why not "instant fish" farms? New Science, 33, 42. Vaz-Ferreira, R., Sierra, B., & Scaglia, S. (1963). Eco-etologia de la reproduccion en los peces del genera Cynolebias Steindachner. Aptdo. de los Archivos de la Sociedad de Biologia de Montevideo, 26, 4449. Wallace, M. M. H., & Tyndale-Biscoe, M. (1983). Attempts to measure the influence of dung beetles (Coleoptera: Scarabaeidae) on the field mortality of the bush fly Musca vetustissima Walker (Diptera: Muscidae) in south-eastern Australia. Bullettin of Entomolgical Research, 73, 33-44. Waiters, L. L., & Legner, E. F. (1980). Impact of the desert pupfish, Cyprinodon macularius, and Gambusia affinis affinis on fauna in pond ecosystems. Hilgardia, 48(3), 1-8. Washburn, J. O., & Anderson, J. R. (1986). Distribution of Lambornella clarki (Ciliophora: Tetrahymenidae) and other mosquito parasites

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in California treeholes. Journal of Invertebrate Pathology, 48, 296- 309. Yadav, R. S., Padhan, K., & Sharma, V. P. (1992). Fishes of the District Sundargarh, Orissa, with special reference to their potential in mosquito control. Indian Journal of Malariology, 29, 225-233. Yu, H.-S., & Legner, E. F. (1976). Regulation of aquatic Diptera by planaria. Entomophaga, 21, 3-12. Yu, H.-S., Legner, E. F., & Pelsue, F. (1975). Control of Culex mosquitoes in weedy lake habitats in Los Angeles with Chlorohydra viridissima. Proceedings of the California Mosquito Control Association, 43, 123126.

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Yu, H.-S., Legner E. F., & Sjogren, R. D. (1974a). Mosquito control with European green hydra in irrigated pastures, river seepage and duck club ponds in Kern County. Proceedings of the Mosquito Control Association, 42, 77-78. Yu, H.-S., Legner, E. F., & Sjogren, R. D. (1974b). Mass release effects of Chlorohydra viridissima (Coelenterata) on field populations of Aedes nigromaculis and Culex tarsalis in Kern County, California. Entomophaga, 19, 409-420.

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INTRODUCTION

naeus), and rats such as Rattus rattus Linnaeus and R. norvegicus Berkenhout)]. Some releases have been inten-

Several species of vertebrates, especially mammals, have been successful invaders and colonizers of new territories, in particular, insular island ecosystems. Others have exhibited high environmental tolerance and adaptability after careful and repeated introductions to new locales by humans. Following establishment, several vertebrate species have become important pests. These pests harm agricultural systems by damaging agricultural lands [e.g., rabbits (Oryctolagus cuniculus Linnaeus) in Australia and New Zealand], by attacking crops [e.g., European starlings (Sturnus vulgaris Linnaeus) in the United States], and by acting as sources for communicable diseases [e.g., brushtail possums, (Trichosurus vulpecula Kerr), are reservoirs for bovine tuberculosis (Mycobacterium bovis Karlson and Lessel) in New Zealand]. Other pest vertebrates damage natural systems by threatening the continued existence of endangered flora [e.g., goats (Capra hircus Linnaeus) on the Galapagos Islands] and fauna [e.g., brown tree snake (Boiga irregularis {Merrem }) on Guam], and by adversely affecting wilderness areas by changing ecosystem functions and diversity (Vitousek et al., 1996). The continued relocation of vertebrates exacerbates the ongoing problem of global homogenization of biota (Lodge, 1993). Movement of particular vertebrates into areas where they had not previously existed has, in some instances, occurred naturally without human intervention [e.g., the passerine bird (Zosterops lateralis {Latham }) arrived in New Zealand unassisted from Australia]. The vast majority of vertebrate translocations have been human assisted. Accidental introduction has occurred as a consequence of human transportation [e.g., brown tree snakes, mice (Mus musculus Lin-

tional (but illegal) to serve self-centered private interests [e.g., monk parakeets (Myiopsitta monachus {Boddaert }) in New York, Florida, and Texas]. Other species have been legitimately introduced to procure public benefit by providing: (1) new agricultural products [e.g., European wild boars (Sus scrofa Linnaeus); sheep (Ovis aries Linnaeus); cows (Bos taurus Linnaeus), goats and rabbits for meat, and brushtail possums for fur in New Zealand], (2) recreation [e.g., red deer (Cervus elaphus Linnaeus), fallow deer (Dama dama Linnaeus), and trout (Salmo trutta Linnaeus and S. gairdneri Richardson) in New Zealand]; (3) companionship [e.g., cats (Felis domesticus Linnaeus) and dogs (Canis familiaris Linnaeus)]; or (4) biological control agents [e.g., the European fox (Vulpes vulpes Linnaeus), stoats (Mustela erminea Linnaeus), weasels (M. nivalis Linnaeus), and ferrets (M. putorius furo Linnaeus) for the control of rabbits in Australia or New Zealand; cane toads (Bufo marinus Linnaeus) for control of gray-backed cane beetles (Dermolepida albohirtum {Waterhouse}) in sugarcane plantations in Australia; and the small Indian mongoose (Herpestes javanicus {Saint-Hilaire }, { = auropunctatus (Hodgson)}) for control of rats in Hawaii]. Chemical and cultural control of vertebrate pests is expensive and nonsustainable, and at best provides a temporary local solution to problems (Hone, 1994; Williams & Moore, 1995). Biological control of vertebrates, a potentially less expensive and self-sustaining method of population suppression, has focused primarily on mammalian pests. Predators, parasites, and pathogens specific to mammals with two notable exceptions (the myxoma and calici viruses that infect rabbits) have failed to provide satisfac-

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tory control (Shelford, 1942; Howard, 1967; Davis et al., 1976; Wood, 1985; Smith & Remington, 1996; Whisson, 1998). Historical records indicate that the majority of attempts at vertebrate biological control have been ad hoc efforts and not the product of careful studies designed to elucidate factors and conditions likely to affect the impact of natural enemy introductions on pest populations. Furthermore, failure of biological control of vertebrates by predatory vertebrates has compounded problems associated with exotic vertebrates because control attempts result in addition of new species that cause biological and conservation problems. The level of control achieved by natural enemies is dependent on ratios of natality to mortality of control agents and their host species (Davis et al., 1976). For vertebrates these ratios are affected by many factors: advanced learning; social, territorial, and breeding behaviors; chemical, physical, and immunological defenses; temporal and spatial escape strategies; and genetic selection in both natural enemy and host populations for persistent coexistence. These complex interrelated factors, coupled with opportunistic feeding habits, have made vertebrate pests difficult targets for biological control with natural enemies. Advances in understanding of mammalian fertilization biology have provided molecular biologists with necessary information to develop and investigate the concept of immunocontraception for vertebrate pest control. Immunocontraception utilizes genetically modified pathogens that express surface proteins from the target pest's egg or sperm to induce an immune response in the host. Antibodies then attack gametes in the host's reproductive tract causing sterilization (Tyndale-Biscoe, 1994b, 1995). Computer models indicate that immunocontraception may provide long-term control of vertebrate pests because genetically modified pathogens reduce net reproductive rates without killing hosts (Barlow, 1994, 1997). In this chapter, I discuss attributes that have aided vertebrate establishment; damage resulting from colonization and uncontrolled population growth; biological control of mammalian pest species with predators, parasites, and pathogens; and future directions that biological control research for vertebrates is taking with genetically engineered microorganisms.

FACTORS THAT FACILITATE VERTEBRATE ESTABLISHMENT

permissive to successful introductions of new species. E1ton's (1958) predictions have been substantiated in part by paleobiological reconstructions of invasions between newly joined communities (Vermeiji, 1991) and by mathematical modeling describing multi-species interactions in communities (MacArthur, 1955; Case, 1991). Isolated oceanic islands (e.g., New Zealand), and insular continents and habitats (e.g., Australia and lakes) often have a low diversity of native species. Such environments have typically experienced little immigration and are susceptible to invasion by vertebrates (Brown, 1989). Stable, speciose communities with high levels of interspecific competition appear to resist invasion by new species and are sources of successful colonists into less speciose or disturbed communities (MacArthur, 1955; Brown, 1989; Lodge 1993). This phenomenon has produced asymmetrical patterns of colonization, with successful vertebrate invaders usually being native to continents or extensive nonisolated habitats within continents with more diverse biotas (Brown, 1989; Vermeiji, 1991). Continental herbivores and predators have been very successful in establishing self-sustaining populations in insular habitats, in part because such habitats often lack large generalist vertebrates and essentially have just two trophic levels, producers and decomposers (if specialist herbivores and their predators are excluded) (Vitousek, 1990). Niches equivalent to those on the mainland are largely unoccupied (Brown, 1989). Insular ecosystems therefore often appear to readily accommodate generalist herbivores and predators, perhaps because of low levels of competition for resources that are often inadequately defended chemically or physically (Vitousek, 1990; Vermeij, 1991; Bowen & van Vuren, 1997). Organisms from insular habitats that have not coevolved closely with predators or herbivores lack life history features that deter attack or permit survival despite high mortality from predation or herbivory (Bowen & van Vuren, 1997). Lack of such biological attributes may increase the competitive advantage of exotics (Case, 1996; Coblentz, 1978; Vitousek, 1990). Introduced vertebrates can also be extremely disruptive in continental regions when habitat disturbance by urbanization or agriculture occurs. European wild boars have detrimental effects on gray beech forests in the Great Smoky Mountains in the southeast United States. Habitat disturbance-through pig rooting, trampling, and browsing-and human removal of predators (pumas and wolves) aided pig establishment and spread in this area (Bratton, 1975; Singer et al., 1984; Vitousek, 1990).

C o m m u n i t y Characteristics

Species Characteristics

Communities vary in their ability to accommodate the establishment and proliferation of new species (Primack, 1995). Elton (1958) suggested that species-poor communities (e.g., islands) or highly disturbed habitats are more

Although there are well-recognized exceptions to general rules that characterize successful vertebrate colonists (Ehrlick, 1989; Williamson & Fitter, 1996b), species that establish self-sustaining populations outside their native

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range typically exhibit some of the following general characters: (1) short generation times, (2) high dispersal rates, (3) high tolerance for varying geographic and climatic conditions, (4)polyphagy, (5) low attack rates from upper trophic level organisms, and (6) human commensalism (Ehrlich, 1986, 1989; Lodge, 1993; Williamson & Fitter, 1996a). The assumption of a high intrinsic rate of increase is generally unnecessary for establishment (Ehrlich, 1986; Lodge, 1993), although it is important for the establishment of some exotic bird species (Veltman et al., 1996). The spread of the European rabbit in Australia and New Zealand, countries that both historically lacked significant eutherian mammal fauna, illustrates some of the preceding points. The European rabbit originated in Spain and Portugal (Corbet, 1994) and spread through most of Europe over 3000 years ago following deforestation by humans for agriculture and overgrazing by livestock. Animals reared in captivity were carried through Europe in advance of naturally spreading populations (Flux, 1994). The spread of the European rabbit throughout Australia following its introduction in 1788 varied from 15 km/year to approximately 300 km/year. Rate of spread was fastest across dry savannas where conditions were most similar to Mediterranean climates and slowest through woodlands (Myers et al., 1994). In Australia, habitat alteration by humans such as conversion of land to pasture, overgrazing of rangelands, and predator eradication [e.g., dingos (Canis familiaris dingo Meyer)] aided rabbit survivorship and spread. Rabbits are polyphagous and feed on grasses and browse shrubs. During severe food and water shortages, bark, fallen leaves, seed pods, tree roots, and termites are consumed (Myers et al., 1994). Rabbits are highly fecund and exhibit rapid population growth under good conditions. Individual female rabbits 10 to 12 months of age can produce litters averaging 5 to 6 young, and with abundant food 23 to 48 offspring per year are produced (Gibb & Williams, 1994). Behavioral adaptability, sociality, and territoriality, in addition to use of elaborate underground warrens, have also aided rabbit proliferation in marginal habitats (Myers et al., 1994).

Relocation of V e r t e b r a t e s a n d H u m a n A s s i s t a n c e in E s t a b l i s h m e n t Some of the first introductions of exotic vertebrates were those commensal with humans as they colonized new areas. Among well-documented early human introductions are dingoes in Australia (Brown, 1989) and Polynesian rats [Rattus exulans (Peale)] on Pacific islands (Roberts et al., 1992). As early Europeans explored the planet, other commensal species such as R. rattus, R. norvegicus, and Mus

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musculus expanded their geographic range without deliberate human assistance and are now cosmopolitan in distribution (Brown, 1989). Not all vertebrate pests cohabitat with or are associated with human disturbance of the environment. Red deer and feral cats, for example, inhabit much of New Zealand's pristine habitats with no human management. Most vertebrate translocations fail even with human assistance. Failure of exotics to establish may depend on life history parameters, responses to abiotic factors, inability to outcompete native species for resources or enemy free space, or chance (Cornell & Hawkins, 1993). Deliberate releases of exotic birds have establishment rates of around 20 to 35% (Veltman et al., 1996). Establishment estimates for intentional vertebrate releases are biased because successes are more often recorded than failures (Ehrlich, 1989; Veltman et al., 1996). The amount of effort directed toward introduction is an important variable affecting successful colonization by vertebrates, and establishment rates increase with high levels of management and numbers of individuals released (Ehrlick, 1989; Griffith et al., 1989; Williamson & Fitter, 1996b; Veltman et al., 1996). In contrast, organisms that are casually introduced into new areas have much lower probabilities of establishing and proliferating. This phenomenon is expressed in the tens rule, a statistical characterization of probability outcomes for different levels of invasion success (Williamson & Fitter, 1996a, 1996b). For a variety of plants and animals, a general rule holds that 1 in 10 species imported (i.e., brought into new areas intentionally or accidentally) appear in the wild, 1 in 10 of those now found in the wild become established, and that 1 in 10 of those established with self-sustaining populations become pests (Williamson & Fitter, 1996b).

VERTEBRATE PEST MANAGEMENT Following establishment, proliferation, and rise to pest status, control of exotic vertebrates is often prompted by economic, environmental, or conservation concerns. Several control strategies may be pursued, the most common being chemical control (e.g., poisoning) and cultural control (e.g., trapping, fencing, and shooting). The least used option has been biological control. Chemical and cultural control of vertebrate pests has been covered by Hone (1994) and Williams and Moore (1995). Biological control is the intentional use of populations of upper trophic level organisms (e.g., predators, parasites, and pathogens) commonly referred to as natural enemies to suppress populations of pests to lower densities than would occur in the absence of natural enemies (DeBach, 1964; Van Driesche & Bellows, 1996). Biological control programs for vertebrates have employed all three classes of

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natural enemies: predators, parasites, and pathogens. In contrast to weeds and pestiferous arthropods, however, biological control as a population suppression tactic for management of vertebrate pests has historically received much less attention. Predators of vertebrates in the few instances they have been used have not been particularly successful. Some vertebrate predator introductions also had severe impacts on nontarget organisms. Consequently, early unpromising results discouraged intensive development of this technology (Howard, 1967; Davis et al., 1976; Wood, 1985). There is a need for increased effort using biological control agents against vertebrates, especially where resistance to toxins has developed, or behavior and terrain makes chemical and cultural control difficult and expensive (Wood, 1985; Bloomer & Bester, 1992). Biological control should be fostered internationally because many countries experience similar problems (e.g., rabbits are agricultural pests in Argentina, Australia, Chile, Europe, and New Zealand; rats, cats, and dogs attack endangered faunas on many oceanic islands; feral pigs and goats in New Zealand, Australia, and the United States degrade habitat and threaten endangered flora). Biological control can be aided by the establishment of institutions to help coordinate regional and international research activities. For example, in 1992, the Australian federal government supported the creation of the Cooperative Research Center for Biological Control of Vertebrate Pest Populations (also known as the Vertebrate Biocontrol Center), an unincorporated collaborative venture between state and federal organizations with international cooperators (Anonymous, 1997a). The principle research goal of this institution is population suppression of noxious vertebrate species by regulating reproductive rates (TyndaleBiscoe, 1994a). P r e d a t o r s as Biological Control A g e n t s A fundamental issue that has important implications for biological control is understanding the regulatory effects predators have on prey populations. Determining impact of introduced predators on pest and nontarget populations is becoming increasingly more important as public awareness of potential nontarget impacts increases and the impact of past introductions on nontarget organisms has become clearer (Howarth, 1983; Van Driesche & Hoddle, 1997). Introductions of vertebrate predators as biological control agents against vertebrates have in some instances had disastrous impacts on nontarget wildlife, especially insular communities that have lacked an evolutionary history with generalist predators (Case, 1996). An example is the impact the small Indian mongoose on native rail populations in Hawaii following its release in the 1880s for rat control

(Loope et al., 1988). The mongoose has little demonstrable effect on rats (Cagne, 1988) and mongoose populations are now poisoned to protect native birds (Loope et al., 1988). Exotic predators may enhance the success of introduced pest species by moderating the competitive impact of natives on introduced pests should predators reduce densities of native species (Case, 1996). On the other hand, there is very good evidence that under certain circumstances introduced exotic predators can regulate target vertebrate pests. In such cases, predator efficacy may be affected by ecosystem complexity; by influence of such extrinsic factors as weather, disease, or human intervention on pest population growth; and by the availability of alternative food sources to sustain predators when pest populations are low. In simple ecosystems such as islands, establishment of reproducing predator populations can result in the extinction of target pests. In the absence of alternative prey, releases of cats for rabbit control on Berlinger Island near Portugal by a lighthouse keeper resulted in the eradication of the rabbits, and subsequently cats died from starvation (Elton, 1927). In complex communities, alternate prey may be taken when primary prey populations are low for prolonged periods, as is the case for some microtine rodent species in Europe. European rodent populations exhibit fluctuations in size as a response to variation in food availability. These fluctuations are also influenced by predation. Population cycles are not observed in Southern Hemisphere countries where European pests and predators have been transferred (Korpim~iki & Krebs, 1996; Sinclair, 1996). Rabbit populations in Australia and New Zealand are maintained at low levels by introduced predators, but regulation only occurs after pest numbers have been reduced by other means. Poisoning programs in New Zealand in the 1950s and 1960s substantially reduced rabbit densities and populations were maintained at low levels by introduced predators, in particular, ferrets and cats (Newsome, 1990). Similarly in Australia, European foxes and cats maintain rabbit populations at low densities following population crashes caused by prolonged hot summers that reduce forage and browse (Newsome et al., 1989; Newsome, 1990). Mouse populations are regulated in a similar fashion by predators (raptors and foxes) in Australia (Sinclair et al., 1990). Introduction of two foxes Dusicyon culpaeus (Molina) and D. griseus (Gray) native to mainland Chile onto the Chilean side of Tierra del Fuego Island regulated rabbit populations after rabbit densities were substantially reduced by the myxoma virus (Jaksic & Yhfiez, 1983). The suppressive action of predators on rabbits in Australia has been demonstrated through predator removal experiments [referred to as perturbation experiments by Sinclair, (1996)] in which European foxes and cats were shot from four-wheel drive vehicles at night. Removal of predators

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Biological Control of Vertebrate Pests

resulted in rapid rabbit population growth compared with rabbit densities in control plots in which predators were not removed (Newsome et al., 1989). The "predator pit" first conceptualized by May (1977) describes rabbit regulation in Australia and New Zealand by generalist predators. The model suggests that once prey populations fall below certain densities (i.e., because of culling or disease) predators can prevent recovery to higher levels. Generalist predators achieve this by maintaining relatively high numbers by attacking alternate prey species, and low but persistent levels of predation on species in the pit prevents pest populations from outbreaking. For the rabbit-fox system in Australia, a predator pit operates at densities of 8 to 15 rabbits per kilometer of linear transect. Below these densities foxes utilize alternate food sources (e.g., native animals) and above this critical density rabbit populations escape regulation by predators (Newsome, 1990). In New Zealand, rabbits are contained in the pit by cats and ferrets when densities are 0.4 rabbits per hectare (Barlow & Wratten, 1996). The effect of predators on long-term population dynamics of alternate prey species is generally difficult to disentangle from confounding effects of habitat degradation and competition for food and breeding sites from other introduced species (Pech et al., 1995). Foxes regulate mice and rabbits through positive density dependence at low prey densities. Increasing pest densities during outbreaks results in inverse density-dependent predation and type III functional responses (Sinclair et al., 1990; Pech et al., 1992). Rabbit and mouse populations escape predator regulation when favorable weather provides good breeding conditions, or when predators are controlled by shooting or poisoning (Newsome, 1990; Sinclair et al., 1990; Pech et al., 1992). Predator control may be necessary for lifestock protection or for conservation of endangered wildlife and when implemented resurgence of pest populations occurs (Newsome et al., 1989; Newsome, 1990). Predator numbers may increase when primary prey (e.g., rabbits) are abundant. Predation by abundant predators on secondary prey (e.g., native animals) result, leading to declines in secondary prey density. Under such circumstances native prey species may only persist in refugia or in areas with artificially reduced predator pressure (Pech et al., 1995). Altematively, declining densities of a primary pest prey species (either through management or disease) can intensify predator attacks on nontarget organisms. Therefore, when conservation of endangered natives is a concern, culling of predators may be undertaken either concurrently with the decline in prey density or in anticipation of such a decline (Grant Norbury, personal communication, 1997). In such situations an integrated approach to managing vertebrate pests and their predators is necessary (Newsome, 1990).

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Predator efficacy can be enhanced either through habitat modification or resource provisioning. Cats can maintain rat and mouse populations around farm buildings below environmental carrying capacity as long as they are provisioned with additional food (e.g., milk). Dietary supplementation prevents rodent extermination and the subsequent extinction of cats. Sustaining a cat population prevents uncontrolled invasions by rodents and low pest densities are maintained (Elton, 1953). Provision of nesting boxes for barn owls (Tyto alba javanica) reduces crop damage by rats in Malaysian oil palm plantations; rodenticide use declined, and in some instances use was eliminated (Wahid et al., 1996). Changes in management practices can improve predator efficacy. Rodent control by Tyto alba (Scopoli) in Pinus radiata Don plantations in Chile was enhanced by clearing 4-m wide strips between trees (for owls to maneuver in while in flight) and construction of perches in forests (for resting and surveillance). Bam owl numbers and predation rates on rodents increased following habitat modification (Mufioz & Murfa, 1990). Under increased predation pressure, rodents will modify foraging behaviors by reducing activity when owls are flying or making hunger calls (Abramsky et al., 1996). Learning in this manner produces behavioral adaptations because of strong selection pressures to minimize predation risks on pest populations (Davis et al., 1976). Parasites as Biological Control A g e n t s Parasites or macroparasites (e.g., helminths, lice, ticks, fleas, and other metazoans) do not typically kill their hosts as a prerequisite for successful development as insect parasitoids do. They tend to be enzootic (i.e., remain at fairly constant levels through time) and usually must pass through a free-living stage to complete an entire life cycle (Anderson, 1979; McCallum, 1994). The potential of parasites to regulate vertebrate host populations was first proposed as early as 1911 (Lack, 1954) and later was demonstrated theoretically with Lotka-Voltera models in which parasites increased host mortality rates (Anderson & May, 1978; May & Anderson, 1978; May, 1980). Parasites act in a positive density-dependent manner by adversely affecting host survival or reproduction (Anderson & May, 1978; Dobson & Hudson, 1986; Scott & Dobson, 1989). Host parasite load also affects the ability of individual parasites to grow, reproduce, and survive in definitive hosts; and the severity of density dependence on host and parasite fitness is affected by patterns of parasite distribution in host populations (Scott & Lewis, 1987). Helminths, for example, tend to be aggregated within host populations so that few hosts are heavily burdened while most are lightly infected (Scott & Lewis, 1987). Density-dependent

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constraints on parasite survival and reproduction occur in the few heavily infected hosts, and under such conditions, helminth population stability is enhanced (Anderson & May, 1978; May & Anderson, 1978). Furthermore, parasites with low-to-moderate pathogenicity exert stronger regulatory actions on populations than highly pathogenic species that cause their own extinction by killing hosts before transmission (Anderson, 1979). Parasite regulation of vertebrate populations has been observed under field conditions. Botfly (Cuterebra grisea Coquillett) parasitism of voles [Microtus townsendii (Bachman)] in Vancouver Canada, is inversely density dependent; and botfly infestation significantly reduces vole survival, reproduction, and development (Boonstra et al., 1980). The parasitic helminth Trichostrongylus tenuis (Cobbold) is the primary agent responsible for long-term population cycles in red grouse [Lagopus lagopus scoticus (Latham)] inhabiting Scottish heathlands (Dobson & Hudson, 1994). The regulatory effect of T. tenuis has been demonstrated by reducing parasite infestations with helminthicides in experimental birds. Treated grouse showed increased overwintering survival, clutch sizes, and hatching rates when compared with untreated birds (Dobson & Hudson, 1994). In the laboratory, introduction of the nematode Heligmosomoides polygyrus Dujardin reduced mice densities by 94% in comparison with control populations. Reduction of nematode transmission rates and elimination of parasites with helminthicides allowed infested mouse populations to increase (Scott, 1987). Although host and parasite densities in this study were higher than those found in nature, the data showed that introduction of a parasite regulated host population abundance. The potential effectiveness of nematodes as biological control agents in field situations has been evaluated for control of the house mouse, an introduced pest in Australia (Singleton & McCallum, 1990; Spratt, 1990). Mouse (Mus domesticus) populations erupt every 7 to 9 years in cereal-growing regions of southeastern Australia (Singleton & McCallum, 1990; McCallum, 1993) and economic losses to mouse plagues exceed $50 million (Australian) (Beckman, 1988; Singleton, 1989). Outbreaks are associated with high autumn rainfalls following prolonged periods of drought that extend the growing season for grasses that set seeds. This high-quality food source increases high mouse survivorship and breeding throughout winter. Population crashes occur when food supplies are exhausted (Singleton, 1989). Saunders and Giles (1977) suggested that droughts are necessary to remove the regulating effects of natural enemies, and this removal combined with favorable weather conditions permitted mouse numbers to increase rapidly. Capillaria hepatica (Bancroft), a parasitic nematode that infests mice, is naturally occurring and widely distributed in pestiferous rodents in coastal areas of Australia. It is,

however, absent in mouse populations in cereal-growing areas (Singleton et al., 1991). This nematode is unique because it is the only known helminth with a direct life cycle that requires host death for transmission. Female nematodes deposit eggs in the host's liver; and these eggs are liberated by predation, cannibalism, or necrophagy with subsequent digestion of infected liver. Unembryonated nematode eggs voided after ingestion undergo embryonation to become infective and are probably consumed when mice preen their fur and feet (Singleton et al., 1991) (Fig. 1). Ground beetles (Carabidae) may vector C. hepatica eggs after they have been eaten (Mobedi & Arfaa, 1971). Firststage larvae emerge from ingested embryonated eggs and move into the liver through the hepatic portal system (Wright, 1961). Nematode infestation significantly reduces natality and numbers of young mice weaned by infected females (McCallum & Singleton, 1989; Singleton & McCallum, 1990; Singleton & Spratt, 1986; Spratt & Singleton, 1986). Capillaria hepatica is associated with introduced rat and mouse species in urban areas, and naturally occurring infections in native Australian mammals are rare probably because of the susceptibility of nematode eggs to ultraviolet radiation and desiccation (Spratt & Singleton, 1986; Singleton et al., 1991). Native Australian mice and marsupials are susceptible to experimental infection in laboratories (Spratt & Singleton, 1986). Rats (R. norvegicus and R. rattus) are major reservoirs for C. hepatica in urban areas and infestation rates range from 40 to 80% (Childs et al., 1988; Singleton et al., 1991). Infestation levels are lower in sympatric mice populations (0 to 40%, Singleton et al., 1991). Low rat numbers in cereal-growing regions of Australia may be a factor contributing to the nonpersistence of C. hepatica in these areas (Singleton et al., 1991). Infestation of nonrodent mammals by C. hepatica is rare (Singleton et al., 1991) but has occurred in rabbits (Gevrey & Chirol, 1978), dogs (LeBlanc & Fagin, 1983), horses (Munroe, 1984), and humans (Pannenbecker et al., 1990). Human infections can be treated successfully (Pereira & Franca, 1983). Exploratory models investigating the impact of C. hepatica on mouse populations indicated that the requirement of host death for parasite transmission is strongly destabilizing. In the absence of resource limitation mouse densities increase similarly to disease-free populations before parasites have an impact and infected populations decline in density (McCallum & Singleton, 1989). Slow regulation of mouse populations occurs because of the need for host death for transmission. Consequently, the nematode's life cycle operates on the same time scale as that of its host instead of being orders of magnitude faster, as is the case with other parasites that do not require host death for transmission (McCallum & Singleton, 1989; Singleton & McCallum, 1990). The destabilizing influence of C. hepatica on mouse

Chapter 38

Biological Control of Vertebrate Pests

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FIGURE 1 Life cycle of Capillaria hepatica (Nematoda) in the house mouse [Mus musculus (Rodentia: Muridae)] (artwork prepared by Vincent D'Amico, III). [After Singleton, G. R., & McCallum, H. I. (1990). Parasitology Today, 6, 190-193.]

populations may contribute to localized host and parasite extinctions. These extinctions, coupled with very low mouse densities in nonoutbreak years, result in population bottlenecks and may explain why nematodes do not persist in regions where mouse outbreaks occur. Soil type, temperature, and moisture content do not affect nematode egg survival and embryonation under favorable conditions in outbreak regions (Spratt & Singleton, 1987). Outbreak intensity can theoretically be reduced by C. hepatica if populations are inoculated early, preferably 1 year before an outbreak is expected (McCallum, 1993). Releases of high doses of nematode eggs in the summer or autumn when mouse densities are sufficient to enable high levels of transmission may offer the best chance for successful control (McCallum & Singleton, 1989; McCallum, 1993).

Field experiments in enclosures and with increasing populations of free-ranging mice have failed to demonstrate long-term regulation on mouse population growth with periodic inoculative releases of C. hepatica eggs. Unexpected declines in control populations (i.e., populations not treated with nematodes) have to some degree masked the effect of C. hepatica on mice populations (Barker et al., 1991; Singleton et al., 1995; Singleton & Chambers, 1996). Transmission of C. hepatica in treated populations is not density dependent and can occur at low levels for 12 to 18 months. Transmission rates show seasonal trends influenced by soil temperatures and increasing aridity (Barker et al., 1991; Singleton & Chambers, 1996). Improved understanding of the influence of factors (such as temperature and rainfall on nematode persistence, survival, and transmission in field

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situations) and timing of releases of parasite eggs may improve releases of C. hepatica for control of mouse outbreaks (Singleton et al., 1995; Singleton & Chambers, 1996). Vertebrate species that successfully colonize new habitats have reduced parasite loads in comparison with mother populations from which they originated (Dobson & May, 1986). Lower infestation levels probably occur because individuals that make up small founding populations either were uninfected or had only a limited subset of the total potential parasite species found in the area of origin, or intermediate hosts required for parasite persistence were absent in the new range. Sparrows and starlings, both successful colonizing species from Europe, have two to three times fewer parasites in North America compared with populations from which they originated. Populations established outside of Europe may have benefited from reduced parasite burdens, although there are no quantitative data to indicate that this aided establishment and proliferation (Dobson & May, 1986). Investigating the role of parasites on population dynamics of rabbits in Europe with the view for possible introduction into countries where rabbits are pests is also warranted (Boag, 1989). Introduced mammals such as rats, goats, and cats on oceanic islands exhibit depauperate parasite faunas (Dobson, 1988). Fewer parasites coupled with presumed low genetic diversity of small founding populations, and reduced selection pressures for parasite resistance may make these pest vertebrates vulnerable to introduced host-specific parasites. The ideal parasite introduced into a high-density pest population that originated from a small founding population should have low-to-intermediate pathogenicity, because such parasites establish and maintain themselves in populations at lower densities than more pathogenic species do (Anderson & May, 1978; May & Anderson, 1978). Macroparasites that reduce both host longevity and fecundity may have the potential to cause sustained reductions of host population densities (Dobson, 1988). Low genetic variability among target populations should theoretically enable introduced parasites to become more evenly distributed among hosts, and reduction in parasite aggregation would increase natural-enemy efficacy (Dobson & Hudson, 1986). The possibility of reassociating parasites with vertebrate pests is not limited to mammals and birds. Host-specific parasites may have the potential to reduce reproduction and longevity of pest reptile (Dobson, 1988) and amphibian species (Freeland, 1985). The brown tree snake is the proximate cause of 12 native bird extinctions on Guam following its accidental introduction after World War II on military equipment (Pimm, 1987; Savidge, 1987; Jaffe, 1994; Rodda et al., 1997). The snake also has caused declines of native reptile and small mammal populations, and enters houses and attacks sleeping human infants (Rodda et al., 1997). Additionally, the brown tree snake has caused eco-

nomic losses by adversely affecting domestic animals (e.g., chickens and pets), and high densities of snakes on power lines regularly cause short circuits that interrupt electrical supplies and necessitate repairs. Control of the brown tree snake has been attempted through trapping, but the snake's extreme preference for live bait over artificial lures has made this approach impractical (Rodda et al., 1997). The brown tree snake mnative to eastern Indonesia, the Solomon islands, New Guinea, and northeastern Australiambelongs to the family Colubridae. It is the only member of this family on Guam. There is one native species of snake on Guam, the blind snake, Rhamphotyphlopys braminus (Daudin), which belongs to the family Typhlopidae and is the only snake occurring on many islands in the central Pacific region (T. Fritts, personal communication, 1998). The brown tree snake has extended its range and is now established on the previously snake-free island of Saipan, and this snake has been intercepted in Hawaii; Corpus Christi, Texas, and Spain (Rodda et al., 1997). Given the propensity for the brown tree snake to be dispersed to new habitats within cargo loads on planes and ships, the major social, economic, and ecological problems that are caused on islands after colonization, in addition to its distant taxonomic relationship to snakes common to Pacific islands, make the brown tree snake an excellent target for biological control. The taxonomic relationship between colubrids and typhlopids may simplify the task and reduce the cost of finding natural enemies unique to the brown tree snake. Parasites or pathogens that are host specific just to the family (i.e., Colubridae) or genus (i.e., Boiga) level may be safe to nontarget snakes (e.g., typhlopids) because these organisms have not evolved the ability to cause disease in distantly related hosts. Extreme caution should be exercised when implementing a biological control program against vertebrate pests with parasites. Parasites and pathogens can pose major threats to populations of endangered animals (McCallum, 1994; McCallum & Dobson, 1995). The susceptibility of nontarget organisms, especially endemic species, to infection by candidate biological control agents should be investigated thoroughly prior to parasite releases. Reassociating parasites that preferentially infect a competitively dominant pest species may increase species diversity of invaded communities by reducing the pest's prevalence. In this instance, the natural enemy would assume the position of a keystone parasite (Marcogliese & Cone, 1997). P a t h o g e n s as Biological Control A g e n t s Pathogens or microparasites include viruses, bacteria, and protozoans. Pathogens tend to be unicellular and exhibit epizootic (i.e., boom or bust) life cycles due to rapid proliferation in hosts (Anderson, 1979; McCallum, 1994).

Chapter 38

Biological Control of Vertebrate Pests

The potential of pathogens to regulate vertebrate population densities by reducing the longevity and fecundity of infected hosts has been demonstrated theoretically with mathematical models and by perturbation experiments using vaccines (Smith, 1994). As with macroparasites, models indicate that microparasites of intermediate pathogenicity are more effective biological control agents (Anderson, 1982). Highly virulent pathogens kill themselves by destroying hosts before they can be transmitted and avirulent strains are not transmitted because they are removed by the immune system. The immune system is theorized as being responsible for maintaining the intermediate virulence of vertebrate microparasites (Anita et al., 1994). Pathogens that are readily transmitted (i.e., microparasites spread by water, air, and vectors) or have high-density host populations are more contagious than those with low transmission rates (i.e., spread is by host-to-host contact) or low host densities (Ebert & Herre, 1996). New associations between pathogens and novel hosts are generally not more harmful than those that have evolved closely with the host. Experimental evidence indicates that novel disease-causing organisms are on average less harmful, less infectious, and less fit than the same parasite strain infecting the host it is adapted to (Ebert & Herre, 1996). Also, a microparasite's ability to infect and exploit novel hosts decreases with increasing geographic and presumably genetic distance from the host to which the pathogen is adapted (Ebert, 1994). Exceptions do occur, however, and pathogens can have devastating impacts on hosts that have no evolutionary history with the disease organism. An example is the myxoma virus, the causative agent of myxomatosis in European rabbits. The use of this natural enemy against rabbits in Australia and Europe has been the most thorough biological control program against a vertebrate pest. The myxoma virus is a member of the genus Leporipoxvirus (Poxviridae) and originated from South America where it was first recognized as an emerging disease of European rabbits in laboratories in Montevideo, Uruguay, in 1896. Infected laboratory rabbits died of a fatal febrile disease that caused tumors on the head and ears. The tumors resembled myxomas (a benign tumor composed of connective tissue and mucous elements) and the disease was subsequently named infectious myxomatosis of rabbits (Fenner & Marshall, 1957; Fenner & Ratcliffe, 1965; Fenner, 1994). The indigenous host for myxoma virus in South America is the forest rabbit [Sylvilagus brasiliensis (Linnaeus)]. Unlike its effect on European rabbits, myxoma inoculum injected into forest rabbits caused benign fibromas at the site of inoculation that persisted for many months, although death did not occur. Mosquitoes were implicated in vectoring the disease from forest rabbits to European rabbits being bred in South American rabbitries. Another leporipox-

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virus has been isolated in California from the brush rabbit, Sylvilagus bachmani (Waterhouse), and is closely related to the myxoma virus (Fenner & Marshall, 1957; Fenner & Ratcliffe, 1965; Fenner, 1994; Fenner & Ross, 1994; Ross & Tittensor, 1986). Myxoma virus has been used in Australia, Europe, Chile, and Argentina for biological control of European rabbits. The virus was first imported into Australia from Brazil in 1919 and 1926 but was not released (Fenner & Ratcliffe, 1965). Work by Australians with the virus began again in the United Kingdom in 1934 and continued with caged rabbits on Wardang Island off the south coast of Australia. The virus was successfully established on mainland Australia in 1950 (Fenner, 1994) and within 2 years it had established itself over most of the rabbit's range (Fenn e r & Ratcliffe, 1965). The virus initially had a major impact on the estimated 600 million rabbits and on the damage they caused, reducing population density by 75 to 95%. Efficacy was dependent on climate and rabbit population susceptibility. Populations have subsequently increased and stabilized at around 300 million because of myxomatosis. Damage attributable to rabbits still amounts to $600 million (Australian) annually, including both lost agricultural production and cost of control applications (Robinson et al., 1997). In addition to agricultural losses, rabbits severely affect native flora by eating foliage and inducing wind and water erosion of soils by overgrazing. Native fauna are also affected as rabbits out-compete indigenous herbivores and dense rabbit populations sustain exotic predator populations that feed on native animals (Gibb & Williams, 1994; Myers et al., 1994; Robinson et al., 1997). Within a few years of the initial panzootic, field isolates of the virus showed less virulence when compared with the original strain that had been released. The original strain killed >99% of laboratory rabbits on average 10.8 days after infection, while circulating strains caused 90% mortality after 21.5 days. Genetic resistance in rabbits was also detected (Fenner & Marshall, 1957; Fenner & Ratcliffe, 1965). Dual natural selection had occurred, the virus had attenuated, and rabbits had increased in resistance to the disease. Mosquitoes have been responsible for vectoring myxoma virus in Australia. The European rabbit flea, Spilopsylus cuniculi (Dale), an important vector in Europe, was introduced into Australia in 1968 and increased the geographic distribution of the disease. This flea did not persist in areas with rainfall