Earthworm ecology

SECOND EDITION Earthworm Ecology © 2004 by CRC Press LLC SECOND EDITION Earthworm Ecology Edited by Clive A. Edwar...

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SECOND EDITION

Earthworm Ecology

© 2004 by CRC Press LLC

SECOND EDITION

Earthworm Ecology Edited by

Clive A. Edwards

CRC PR E S S Boca Raton London New York Washington, D.C.


1819_C00.fm Page 4 Monday, February 23, 2004 12:23 PM

Library of Congress Cataloging-in-Publication Data Earthworm ecology / edited by Clive A. Edwards. -- 2nd ed. p. cm. Rev. ed. of: Earthworm ecology / edited by Clive A. Edwards. 1994. Includes bibliographical references and index. ISBN 0-8493-1819-X (alk. paper) 1. Earthworms--Ecology--Congresses. I. Edwards, C. A. (Clive Arthur), 1925- II. Earthworm ecology. III. Title. QL391.A6E25 2004 592′.64—dc22 2003070024 This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts have been made to publish reliable data and information, but the author and the publisher cannot assume responsibility for the validity of all materials or for the consequences of their use. Neither this book nor any part may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, microfilming, and recording, or by any information storage or retrieval system, without prior permission in writing from the publisher. All rights reserved. Authorization to photocopy items for internal or personal use, or the personal or internal use of specific clients, may be granted by CRC Press LLC, provided that $.50 per page photocopied is paid directly to Copyright clearance Center, 222 Rosewood Drive, Danvers, MA 01923 USA. The fee code for users of the Transactional Reporting Service is ISBN 0-8493-1819-X/04/$1.00+$.50. The fee is subject to change without notice. For organizations that have been granted a photocopy license by the CCC, a separate system of payment has been arranged. The consent of CRC Press LLC does not extend to copying for general distribution, for promotion, for creating new works, or for resale. Specific permission must be obtained in writing from CRC Press LLC for such copying. Direct all inquiries to CRC Press LLC, 2000 N.W. Corporate Blvd., Boca Raton, Florida 33431. Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation, without intent to infringe.

Visit the CRC Press Web site at www.crcpress.com © 2004 by CRC Press LLC No claim to original U.S. Government works International Standard Book Number 0-8493-1819-X Library of Congress Card Number 2003070024 Printed in the United States of America 1 2 3 4 5 6 7 8 9 0 Printed on acid-free paper



Preface Charles Darwin was the first scientist to bring earthworms to the attention of scientists and the general public, more than a century ago. Darwin noted the importance of earthworms in breaking down dead plant materials, recycling the nutrients they contain, and turning over soil. His book The Formation of Vegetable Mould through the Action of Worms (1881) summarized his conclusions on earthworms, which he reached after 40 years of observation and experimental work. In this book, he expressed the opinion that “earthworms have played a most important part in the history of the world.” The importance of his personal contributions to our knowledge of the roles and biology of earthworms cannot be stressed enough and led to a great upsurge in research into the morphology, histology, and taxonomy of earthworms in the late 19th and early 20th centuries. However, it was only in the last 25 years that interest in and research into the ecology and biology of earthworms has peaked. Much of this work was summarized by Edwards and his coauthors in their book The Biology and Ecology of Earthworms (first edition 1972, second edition 1977, third edition 1996) and by Lee in his book Earthworms: Their Ecology and Relationships with Soil and Land Use (1985). Interest in earthworm ecology and the importance of earthworms to soil formation and fertility has been increasing at an extremely rapid rate and so has research into the subject. This is evidenced by the increases in the number of references cited by the authors of The Biology and Ecology of Earthworms in its three editions. In 1972, they cited 565 references; in the second edition (1977), they cited 674; but in the third edition (1996), they cited more than 1500. This probably represented only a third of scientific papers published up to that time. The first edition of Earthworm Ecology (1998) owed its origin to the Fifth International Symposium on Earthworm Ecology, which was held in Columbus, Ohio, in July 1994. At this Symposium, attended by more than 220 scientists from 38 countries, 165 research presentations were made, many of which are published in a special volume of the journal Soil Biology and Biochemistry. In the eight sessions that were held at the Columbus Symposium, each opened with an invited review paper of a key topic by a distinguished earthworm scientist and concluded with a final overview of the subject and conclusions by another well-known earthworm scientist. The 16 invited papers were edited to form the eight sections in the first edition of Earthworm Ecology, which covered all the major aspects of earthworm ecology, including earthworm diversity, behavior, physiology and general ecology, and the roles of earthworms in nutrient cycling, soil maintenance, plant growth, ecotoxicology, and waste management, with two chapters summarizing research on each topic. Since the first edition of Earthworm Ecology was published in 1998, there have been two further Symposia on Earthworm Ecology, in Vigo, Spain, in 1998 and in Cardiff, Wales, in 2002; the number of publications on earthworms has continued to increase rapidly. The first edition was extremely well received by scientists, students, and the general public. In view of the rapidly expanding developments and discoveries in earthworm biology and ecology, it seemed appropriate to update, and revise extensively, the first edition of the book and add new chapters that address the most rapidly developing areas of earthworm research. This second edition includes extensive revisions of the original chapters as well as additional chapters on the history of earthworm research, mechanisms by which earthworms increase soil fertility and promote plant growth, and the importance of invasions of exotic species of earthworms in North America and other regions of the world; there is a new chapter on vermiculture and vermicomposting in Europe. These changes make this book an even more valuable addition to the



publications that summarize the increasing importance of earthworms in natural ecosystems and crop production. It also addresses key issues in earthworm biology and ecology and is an essential key reference work for soil scientists and agronomists as well as those people with a great interest in earthworms. Clive A. Edwards The Ohio State University, Columbus



About the Editor Clive Edwards, Ph.D., is recognized as a world authority on earthworms, and his book Ecology and Biology of Earthworms is now in its third edition. After graduating from Bristol University and then earning a M.S. and Ph.D. at the University of Wisconsin, U.S.A., Dr. Edwards was appointed to the U.K. Ministry of Agriculture. In 1960 he joined Rothamsted Experimental Station as a Senior Principal Scientific Officer where his work focused on research into the effects of agricultural chemicals on the soil environment. From 1966 to 1968 he was visiting professor at Purdue University, U.S.A. He was appointed as Chair of the Department of Entomology at The Ohio State University, U.S.A. in 1985. Dr. Edwards has published extensively on soil ecology, environmental toxicology, and sustainable agriculture, and he is currently recognized as a world authority on earthworms. His book Ecology and Biology of Earthworms is the first comprehensive book on earthworms since Charles Darwin’s The Formation of Vegetable Mould Through the Action of Worms, which was published in 1881. In 1996, Professor Edwards’ book Ecology of Earthworms won a Presidential Citation from the U.S. Soil & Water Conservation Society. In 2001, Dr. Edwards presented The Ohio State University Distinguished Lecture The Future of Human Populations; Energy, Food and Water Availability in the 21st Century — one of the university’s highest honors for a faculty member. His involvement with the British Crop Protection Council has been an outstanding contribution to all the Pests & Diseases Conferences.



Contributors Jean Andre Université de Savoie Chambery, France Norman Q. Arancon Soil Ecology Laboratory The Ohio State University Columbus, Ohio, U.S.A. Geoff H. Baker CSIRO Entomology Canberra, Australia Nicolas Bernier Université de Savoie Chambery, France John M. Blair Division of Biology Kansas State University Manhattan, Kansas, U.S.A. Patrick J. Bohlen Archbold Biological Station Lake Placid, Florida, U.S.A. George G. Brown Embrapa Soya Londrina, Brazil Lijbert Brussaard Soil Quality Section Wageningen University Wageningen, The Netherlands Fabienne Charpentier Laboratoire d’Ecologie des Sols Tropicaux Bondy, France


James P. Curry Department of Environmental Resource Management University College, Belfield Dublin, Ireland Laurent Derouard Laboratoire d’Ecologie des Sols Tropicaux Bondy, France Jorge Domínguez Departamento de Ecoloxía e Bioloxía Animal Universidade de Vigo Vigo, Spain Bernard M. Doube Wood Duck Cellars Bridgewater, South Australia, Australia Clive A. Edwards Soil Ecology Laboratory The Ohio State University Columbus, Ohio, U.S.A. Herman Eijsackers Alterra, Wageningen University and Research Centre Institute of Ecological Sciences Vrije Universiteit Amsterdam, The Netherlands Cécile Gilot Yurimaguas, Loreto, Peru Paul F. Hendrix Institute of Ecology University of Georgia Athens, Georgia, U.S.A.


Samuel W. James Department of Life Sciences Maharishi University of Management Fairfield, Iowa, U.S.A. Radha D. Kale Department of Zoology University of Agricultural Sciences Bangalore, India André Kretzschmar INRA-Biometrié Avignon, France

Adriana Antonia Pop Institute of Biological Research Cluj-Napoca, Romania Victor V. Pop Institute of Biological Research Cluj-Napoca, Romania Adriaan J. Reinecke Department of Zoology University of Stellenbosch Stellenbosch, South Africa

Patrick Lavelle Laboratoire d’Ecologie des Sols Tropicaux Bondy, France

Sophié A. Reinecke Department of Zoology University of Stellenbosch Stellenbosch, South Africa

Renée-Claire Le Bayon Department of Plant Ecology Neuchâtel University Neuchâtel, Switzerland

John W. Reynolds Oligochaetology Laboratory Kitchener, Ontario, Canada

Mary Ann McLean Department of Biology Indiana State University Terre Haute, Indiana, U.S.A.

Jean-Pierre Rossi Laboratoire d’Ecologie des Sols Tropicaux Bondy, France

Dennis Parkinson Department of Biological Sciences University of Calgary Calgary, Alberta, Canada

Stefan Scheu Institute of Zoology Darmstadt University of Technology Darmstadt, Germany

Robert W. Parmelee Yucca Valley, California, U.S.A.

Martin J. Shipitalo North Appalachian Experimental Watershed U.S. Department of Agriculture Agricultural Research Service Coshocton, Ohio, U.S.A.

Beto Pashanasi Estacion Experimental San Ramon INIAA Yurimaguas, Loreto, Peru Jean-François Ponge MNHN Brunoy, France


Cécile Villenave Laboratoire d’Ecologie des Sols Tropicaux Bondy, France


Table of Contents Part I Introduction ......................................................................................................................................1 Chapter 1 The Importance of Earthworms as Key Representatives of the Soil Fauna.....................................3 Clive A. Edwards Chapter 2 How Earthworms Affect Plant Growth: Burrowing into the Mechanisms.....................................13 George G. Brown, Clive A. Edwards, and Lijbert Brussaard Part II Earthworm Taxonomy, Diversity, and Biogeography.................................................................51 Chapter 3 Planetary Processes and Their Interactions with Earthworm Distributions and Ecology......................................................................................................................................53 Samuel W. James Chapter 4 The Status of Earthworm Biogeography, Diversity, and Taxonomy in North America Revisited with Glimpses into the Future ...............................................................63 John W. Reynolds Chapter 5 Invasion of Exotic Earthworms into North America and Other Regions.......................................75 Samuel W. James and Paul F. Hendrix Part III Earthworm Biology, Ecology, Behavior, and Physiology............................................................89 Chapter 6 Factors Affecting the Abundance of Earthworms in Soils..............................................................91 James P. Curry Chapter 7 A Comprehensive Study of the Taxonomy and Ecology of the Lumbricid Earthworm Genus Octodrilus from the Carpathians.....................................................................115 Victor V. Pop and Adriana Antonia Pop



Part IV Influence of Earthworms on Soil Organic Matter Dynamics, Nutrient Dynamics, and Microbial Ecology .................................................................................................................143 Chapter 8 Effects of Earthworms on Soil Organic Matter and Nutrient Dynamics at a Landscape Scale over Decades......................................................................................................145 Patrick Lavelle, Beto Pashanasi, Fabienne Charpentier, Cécile Gilot, Jean-Pierre Rossi, Laurent Derouard, Jean Andre, Jean-François Ponge, and Nicolas Bernier Chapter 9 Integrating the Effects of Earthworms on Nutrient Cycling across Spatial and Temporal Scales..........................................................................................................161 Patrick J. Bohlen, Robert W. Parmelee, and John M. Blair Part V Effects of Earthworms on Soil Physical Properties and Function..........................................181 Chapter 10 Quantifying the Effects of Earthworms on Soil Aggregation and Porosity .................................183 Martin J. Shipitalo and Reneé-Claire Le Bayon Chapter 11 Effects of Earthworms on Soil Organization ................................................................................201 André Kretzschmar Part VI Interactions of Earthworms with Microorganisms, Invertebrates, and Plants......................211 Chapter 12 Functional Interactions between Earthworms, Microorganisms, Organic Matter, and Plants .......................................................................................................................................213 George G. Brown and Bernard M. Doube Chapter 13 Impacts of Earthworms on Other Biota in Forest Soils, with Some Emphasis on Cool Temperate Montane Forests ..................................................................................................241 Dennis Parkinson, Mary Ann McLean, and Stefan Scheu Part VII Earthworms in Agroecosystems..................................................................................................261 Chapter 14 Managing Earthworms as a Resource in Australian Pastures.......................................................263 Geoff H. Baker



Chapter 15 Earthworms in Agroecosystems: Research Approaches ...............................................................287 Paul F. Hendrix and Clive A. Edwards Part VIII Earthworms and Environmental Pollution ...............................................................................297 Chapter 16 Earthworms as Test Organisms in Ecotoxicological Assessment of Toxicant Impacts on Ecosystems...................................................................................................299 Adriaan J. Reinecke and Sophié A. Reinecke Chapter 17 Earthworms in Environmental Research .......................................................................................321 Herman Eijsackers Part IX Earthworms in Waste Management ...........................................................................................343 Chapter 18 The Use of Earthworms in the Breakdown of Organic Wastes to Produce Vermicomposts and Animal Feed Protein .....................................................................................345 Clive A. Edwards and Norman Q. Arancon Chapter 19 The Use of Earthworms: Nature’s Gift for Utilization of Organic Wastes in Asia .....................381 Radha D. Kale Chapter 20 State-of-the-Art and New Perspectives on Vermicomposting Research .......................................401 Jorge Domínguez


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Part I Introduction


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Importance of 1 The Earthworms as Key Representatives of the Soil Fauna Clive A. Edwards Soil Ecology Laboratory, The Ohio State University, Columbus, Ohio, U.S.A.

CONTENTS History ................................................................................................................................................3 Earthworm Taxonomy........................................................................................................................4 Earthworm Ecology ...........................................................................................................................4 Earthworms and Soil Fertility............................................................................................................5 Soil Formation ............................................................................................................................5 Turnover of Soil..........................................................................................................................6 Soil Aeration and Drainage ........................................................................................................6 Organic Matter Breakdown and Incorporation into Soil ...........................................................6 Nutrient Availability....................................................................................................................7 Effects of Agriculture on Earthworms...............................................................................................7 Earthworms as Indicators of Soil Quality and Health ......................................................................8 Earthworms and Soil Pollution..........................................................................................................8 Earthworm Immigrations ...................................................................................................................9 Need for Earthworm Research ..........................................................................................................9 Conclusions ........................................................................................................................................9 References ..........................................................................................................................................9

HISTORY The great importance of the soil biota in soil pedogenesis and in the maintenance of structure and fertility is not always fully appreciated by physical and chemical soil scientists. Earthworms are arguably the most important components of the soil biota in terms of soil formation and maintenance of soil structure and fertility. Although not numerically dominant, their large size makes them one of the major contributors to invertebrate biomass in soils. Their activities are important for maintaining soil fertility in a variety of ways in forests, grasslands, and agroecosystems. Aristotle was one of the first people to draw attention to the role of earthworms in turning over the soil; he aptly called them “the Intestines of the Earth.” However, it was not until the late 1800s that Charles Darwin, in his definitive work The Formation of Vegetable Mould through the Action of Worms (1881), really brought attention to the extreme importance of earthworms in the breakdown of dead plant and animal matter that reaches soils and in the continued turnover and maintenance of 3 © 2004 by CRC Press LLC


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Earthworm Ecology, Second Edition

soil structure, aeration, drainage, and fertility. Before Darwin’s book was published, earthworms were commonly considered soil-inhabiting crop pests. His views on the beneficial aspects of earthworms were supported and expanded subsequently by other contemporary scientists such as Muller (1878), Urquhart (1887), and many others. The observations Darwin described were so advanced that it was half a century before many of them were confirmed (see Chapter 2, this volume).

EARTHWORM TAXONOMY Earthworms belong to the order Oligochaeta, which includes more than 8000 species from about 800 genera. Earthworms are common all over the world in natural forests and grasslands as well as agroecosystems. However, many oligochaetes have an aquatic habit, and there is considerable controversy over earthworm systematics (see Chapters 3 to 5, this volume). Earthworms are found in most regions of the world, except those with extreme climates, such as deserts and areas that are under constant snow and ice. Some genera and species of earthworms, particularly those belonging to the Lumbricidae, are extremely widely distributed and are termed peregrine; often, when these species are introduced to new areas, they become dominant over the endemic species. This situation applies to parts of the northern United States and Canada, particularly those areas close to major waterways (see Chapters 3 and 5, this volume). However, the indigenous earthworm fauna of North America has not been well studied other than by Gates and Reynolds and earlier workers (Chapter 4). Endemic species include those in the Acanthodrilidae, with its most abundant genus Diplocardia; members of the Sparganophilidae; and species in the Megascolecidae, of which the most common genus is Pheretima. There are very few earthworm taxonomists, which has an impact on earthworm research the world over (see Chapter 4, this volume).

EARTHWORM ECOLOGY The size of earthworms ranges from a few millimeters to as much as 2 m in length, from 10 mg to nearly a kilogram in weight, and up to 40 mm in diameter. The record was a specimen believed to be a Microchaetus sp. that was 7 m long and 75 mm in diameter (Lungström and Reinecke 1969). The larger earthworms are usually found in southern latitudes, such as South America, South Africa, Southeast Asia, Australia, and New Zealand. No other terrestrial invertebrate has such a wide range of sizes between the smallest and the largest individuals (Lee 1985) Populations of earthworms vary greatly in terms of numbers or biomass and diversity. Populations range from only a few individuals per square meter to more than 1000 per square meter (Lee 1985; Edwards and Bohlen 1996; Lavelle et al. 1999). The size of populations depends on a wide range of factors, including soil type, pH, moisture-holding capacity of the soil, rainfall, and ambient temperatures, but most importantly, on the ready availability of organic matter. This is because interactions between organic matter and microorganisms provide food for earthworms. Earthworm populations in cultivated land usually do not exceed 100 per square meter or 400 per square meter in grassland, and similar populations to those in grassland are usually found in woodlands, where the availability of organic matter is seldom limiting. Numbers as high as 2000 per square meter have sometimes been recorded, although relatively few earthworms occur in the more acidic mor soils under coniferous forests. Usually, the largest earthworm populations are lumbricids, which seem to be able to survive adverse soil and litter conditions much better than species belonging to many of the other families. The earthworm biomass in most soils exceeds the biomass of all other soil-inhabiting invertebrates. It has been stated that earthworm biomass in a pasture may be ten times that of stock animals that graze on it (see Chapters 6 and 14, this volume). The diversity of species of earthworms varies greatly between sites and habitats, and there often tend to be species associations in different soil types and habitats. Earthworm communities



The Importance of Earthworms as Key Representatives of the Soil Fauna

5

in soils in temperate countries are dominated by lumbricids and tend to be considerably less diverse than in soils with other earthworm families in warmer latitudes (Lavelle et al. 1999). However, even in the most complex soil systems, the diversity of earthworm species does not seem to be very great, rarely exceeding ten, and there are usually only three to five species in any particular site. There is some evidence that species that fill the same ecological niche do not normally occur in the same degree of abundance at a particular site (Edwards and Lofty 1982a,b; Edwards and Bohlen 1996). The activity of earthworms differs greatly between seasons in temperate regions, where earthworms are active mainly in the spring and autumn. During the winter, they penetrate deeper into soil, where they are much more protected from the adverse winter cold temperatures. In dry summer periods, they also burrow deeper into soil and sometimes construct cells lined with mucus in which they estivate in a coiled position until environmental conditions become favorable again. Although cocoons may be produced at almost any time of the year, cocoon production is usually seasonal. In temperate regions, the most cocoons are produced in spring or early summer, with a second, much smaller peak in autumn. Numbers of cocoons range from 1 to 20 per mating, depending on species. The life cycles of many species of earthworms have not been well studied. There probably is adequate information on about 12 species of temperate lumbricid earthworms, 7 species from Africa (Lavelle et al. 1999), and 20 species of earthworms common in tropical agroecosystems (Barois et al. 1999). Earthworms have potential for very long life cycles of up to 10 to 12 years, although in the field, many species may live only 1 or 2 seasons because of their susceptibility to a wide range of predators (Edwards and Bohlen 1996). Indeed, their potential longevity, combined with their fecundity, means that very large populations could build up rapidly in the absence of predation or adverse environmental conditions. In addition, some species can produce cocoons parthenogenetically without mating, which increases their potential to spread to new sites. Their moisture and temperature relationships have major effects on their ability to populate new sites. Earthworms lose moisture through their cuticles, so they are very dependent on soil moisture, and their activities are linked closely with rainfall patterns in both temperate and tropical environments. However, for some reason, in periods of intense precipitation, some species may emerge from their burrows, and they are often found in large numbers on the soil surface, where they may die. Cocoon production and the growth of earthworms are correlated positively with temperature, but the cocoon incubation period, percentage hatching, and number of hatchlings produced per cocoon are correlated negatively with temperature (Edwards 1998). Many species cannot survive below 0°C, and most species cannot survive above 30 to 35°C (Edwards 1983). Nevertheless, they have behavioral patterns and resistant cocoons that enable them to survive adverse climate conditions.

EARTHWORMS AND SOIL FERTILITY SOIL FORMATION Earthworms are extremely important in soil formation, principally through activities in consuming organic matter, fragmenting it, and mixing it intimately with soil mineral particles to form waterstable aggregates. During feeding, earthworms promote microbial activity by an order of magnitude, which in turn also accelerates the rates of breakdown and stabilization of humic fractions of organic matter. Different species of earthworms do not affect soil formation in the same way because of very different behavior patterns. Some species consume mainly inorganic fractions of soil, whereas others feed almost exclusively on decaying organic matter (see Chapters 8 and 9, this volume). They can deposit their feces as casts either on the soil surface or in their burrows, depending on the species concerned, but all earthworm species contribute in different degrees to the comminution



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and mixing of the organic and inorganic components of soil and decrease the size of not only organic particles, but also mineral particles (Shrickhande and Pathak 1951; Joshi and Kelkar 1952). During passage through the earthworm gut, the different kinds of mineral particles become mixed intimately with organic matter and form aggregates, which improve both the drainage and moisture-loading capacity of the soil. These aggregates are usually very water stable and improve many of the desirable characteristics of soils. There have been various suggestions as to the possible ways in which earthworms form aggregates, such as by production of gums (Swaby 1950) or calcium humate (Meyer 1943), by plant residues (Ponomareva 1953), or by means of polysaccharide molecules (Parle 1963). Various authors have estimated that up to 50% of the aggregates in the surface layers of soil are formed by earthworms (Kubiena 1953). Earthworms also contribute in many ways to soil formation, structure, and physical characteristics (see Chapters 10 and 11, this volume).

TURNOVER

OF

SOIL

As Darwin first noted, earthworms move large amounts of soil from the deeper strata to the surface. The amounts moved in this way range from 2 to 250 tons per hectare per annum, equivalent to bringing a layer of soil between 1 mm and 5 cm thick to the surface every year, creating a stonefree layer on the soil surface. In temperate climates, all the upper 15 cm of soil may be turned over every 10 to 20 years (Edwards and Bohlen 1996). However, much larger turnovers have been reported from tropical agroecosystems (Lavelle et al. 1999).

SOIL AERATION

AND

DRAINAGE

Earthworms also affect soil structure in other ways. Some species make permanent burrows, whereas others move randomly through the soil, leaving cracks and crevices of different sizes. Both sorts of burrows are important in maintaining soil aeration, drainage, and porosity. Moreover, earthworm burrows are usually lined with a protein-based mucus that helps stabilize these channels, and many of the species with permanent burrows cast their feces around the lining of the burrows, with the cast material usually containing more plant nutrients in a readily available form than the surrounding soil. There is good evidence that earthworm activity increases both the porosity and the air-to-soil volume (Wollny 1890; Hopp 1974; Edwards and Lofty 1977). Burrows are also important in improving soil drainage, particularly because those of some species, such as Lumbricus terrestris L., penetrate deep into soil in permanent burrows (Edwards and Lofty 1978, 1982a,b) and can even pass through layers of clay. The burrows and pores also increase the infiltration rate greatly (Slater and Hopp 1947; Teotia et al. 1950; Carter et al. 1982), and there are numerous reports of water penetrating the surface soil between two and ten times faster when earthworms were present than when they were not (Stockdill 1966; Wilkinson 1975; Tisdall 1978). These effects on infiltration can be of two kinds. The first is the presence of large surface-opening holes that are not usually taken into account by soil scientists when conventional models of infiltration are developed (Edwards and Lofty 1982a). Second, the crevices also created by earthworms, but which are smaller, not only increase infiltration, but also aid in water retention (see Chapters 10 and 11, this volume). Finally, earthworm activity makes a significant contribution to soil aeration (Stockli 1928; Kretzschmar 1978) by creating channels, particularly in heavy soils, that allow air to penetrate into deeper layers of soil, minimizing the incidence of anaerobic layers.

ORGANIC MATTER BREAKDOWN

AND INCORPORATION INTO

SOIL

Although all species of earthworms contribute to the breakdown of plant-derived organic matter, they differ greatly in the ways in which they break down organic matter and incorporate it into the soil. Their activities can be of three kinds, each associated with a different group of species. Some © 2004 by CRC Press LLC



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species are limited mainly to the plant-litter layer on the soil surface, decaying organic matter or wood, and seldom penetrate soil more than superficially. The main role of these species seems to be comminution of the organic matter into fine particles, which facilitates microbial activity. Other species live just below the soil surface most of the year, except when the weather is very cold or very dry; do not have permanent burrows; and ingest both organic matter and inorganic materials. These species produce organically enriched soil materials in the form of casts, which they deposit either randomly in the surface layers of soil or as distinct casts on the soil surface. Finally, there are the truly soil-inhabiting species with permanent burrows that penetrate deep into the soil. These species feed primarily on organic matter but also ingest considerable quantities of inorganic materials and mix these thoroughly through the soil profile. These last species are of primary importance in pedogenesis. All species depend on consuming organic matter in some form and play an important role in the final stages of organic matter decomposition, which is humification into complex amorphous colloids containing phenolic materials, probably by promoting microbial activity. There is little doubt that, in many ecosystems, earthworms are the key organisms in the breakdown of plant organic matter. Populations of earthworms usually expand in relation to the availability of organic matter; in many temperate and even tropical forests, it seems that earthworms have the capacity to consume the total annual litter fall. Such a total turnover has been calculated for an English mixed woodland (Satchell 1967), an English apple orchard (Raw 1962), a tropical forest in Nigeria (Madge 1965), and an oak forest in Japan (Sugi and Tanaka 1978); it seems likely that similar calculations would be valid for other sites (Edwards and Bohlen 1996). There is current speculation that invasions of lumbricids into North American forests are changing them dramatically and having an impact on rates of organic matter turnover and soil cover (see Chapters 5, 8, 9, and 13, this volume).

NUTRIENT AVAILABILITY During feeding by earthworms, the carbon:nitrogen ratio in the organic matter falls progressively; moreover, most of the nitrogen is converted into the ammonium or nitrate form. At the same time, the other nutrients, phosphorus and potassium, are converted into a form available to plants. Soils that have poor populations of earthworms often develop a structure with a mat of decomposed organic matter at the soil surface (Kubiena 1953); this can also occur in grassland and is common on poor upland grasslands in temperate countries and in New Zealand in areas where earthworms have not yet been introduced (Stockdill 1966) (see Chapters 6 and 14, this volume).

EFFECTS OF AGRICULTURE ON EARTHWORMS Earthworm populations are affected greatly by many of the main agricultural practices; in particular, cultivations, fertilizers, pesticides, and crop rotations exert major effects on earthworm activities and communities. Cultivations have considerable effects on earthworm communities, particularly those species with deep burrows. A single cultivation does not have any drastic effects on earthworm populations other than by mechanical damage, destruction of permanent burrows, and exposure to bird predators. However, repeated heavy cultivations progressively diminish earthworm populations. No till (direct drill) and a variety of conservation tillage practices, such as ridge tillage and shallow plow, favor the buildup of larger earthworm populations that are limited only by the availability of food (Edwards and Lofty 1982a; Edwards and Bohlen 1996). Fertilizers can be either organic or inorganic, including a broad range of organic manures from sources such as cattle, pigs, poultry, sewage wastes, and wastes from industries such as those involving a brewery, paper pulp, or frozen potatoes. These materials are major factors in the buildup of large field earthworm populations; when such organic wastes are added to agricultural land, earthworm populations may double or triple in a single season. Some liquid manures that have not © 2004 by CRC Press LLC


8


aged or composted can have temporary adverse effects on earthworm populations when applied to soils as slurries because of their ammonia and salt contents, but these effects are usually short term. Many inorganic fertilizers also contribute indirectly to the buildup of earthworm populations because of increased crop yields and hence increased amounts of crop residues added to the soil. However, earthworms are very sensitive to ammonia, and ammonia-based fertilizers often have adverse effects on earthworm populations, especially when these fertilizers are applied annually over several seasons (Edwards and Lofty 1982b). Pesticides, which include insecticides, herbicides, fungicides, and nematicides, are used extensively on agricultural land in developed countries. It is often assumed that many pesticides are toxic to earthworms or have harmful effects on them. However, most herbicides have few direct effects on earthworms, although the triazine herbicides are slightly toxic. However, herbicides have drastic indirect effects on earthworms through their influence on the availability of organic matter (Edwards and Thompson 1973). Most fungicides have few effects on earthworms, with the exception of the carbamate-based fungicides, such as benomyl, which are very toxic. Of the insecticides in current use, only the organophosphate, phorate, and most carbamate-based compounds such as carbaryl, carbofuran, and methiocarb, and the avermectins are toxic to earthworms (Edwards 1984a, b). Of more than 200 pesticides reviewed by Edwards and Bohlen (1992), fewer than 20 were seriously toxic to earthworms (see Chapters 16 and 17, this volume). Crop rotations have been progressively decreasing in industrialized agriculture. There has been relatively little work on the effects of crop rotations on earthworm problems. In general, the inclusion of crops such as cereals that leave considerable organic residues encourage the buildup of earthworm populations more than do legumes, which decompose quite rapidly. Root crops, for which most of the crop is removed, discourage the buildup of earthworm populations (Edwards and Bohlen 1996).

EARTHWORMS AS INDICATORS OF SOIL QUALITY AND HEALTH There has been considerable interest in the concept of maintaining soil quality and health. There has been considerable discussion on defining these terms and on identifying appropriate physical, chemical, and biological indicators of soil quality. One definition is “the ability of a soil to sustain biological productivity, maintain environmental quality and promote plant, animal and human health” (Doran and Parkin 1996). Soil is a heterogeneous mixture of abiotic and living components, including a very complex range of soil-inhabiting organisms. The basic functions of soils depend on their structural and functional integrity and the impacts of disturbances on management on these functions. A wide range of indicators of soil quality and health criteria has been suggested, but it is becoming increasingly clear that it is essential that the indicators must include biological components because soil is a dynamic entity (Blair et al. 1996). It is difficult to use microbial indicators of soil quality and health as much as desired because of a lack of simple methodologics that can be used in the field by relatively untrained workers. Soil microinvertebrates have been suggested as possible indicators of quality and health (Linden et al. 1994), but sampling microarthropod or nematode populations is difficult, so their identification and utility as suitable indicators is a complex problem. There is a consensus among soil ecologists and most farmers that earthworms may be one of the best indicators available of soil quality (Doube and Schmidt 1997). They are easy to sample and identify and, as the discussions in this book illustrate, are important indicators of both soil health and soil quality (see Chapters 2 and 6, this volume).

EARTHWORMS AND SOIL POLLUTION There has been increasing interest in the use of earthworms as organisms to assess the environmental effects of soil pollution. Three Conferences on Earthworm Ecotoxicology (1991, U.K.; 1997, the




9

Netherlands; 2001, Denmark) were each attended by more than 100 scientists and provide good evidence of this interest. Standardized testing protocols have been developed by such national and international organizations as the Organization for Economic Cooperation and Development and the European Union (Edwards 1983, 1984b). Many aspects of earthworm ecotoxicology are reviewed in Chapters 16 and 17 of this volume.

EARTHWORM IMMIGRATIONS Interest has increased greatly in migrations of earthworms across regions and continents. Peregrine earthworms, especially lumbricids, are invading soils across the world, particularly into agricultural soils, but more recently into forest soils. These issues are discussed extensively in Chapters 5 and 13 of this volume.

NEED FOR EARTHWORM RESEARCH Although the number of publications on earthworm biology and ecology is increasing rapidly, there still seems an urgent need for greatly expanded research, particularly on some aspects of earthworm activity. There still is inadequate knowledge of the basic biology and ecology of even some of the more common species of lumbricoids. Very few studies have addressed the problems of the detailed interrelationships among earthworms, microorganisms, and decaying organic matter and its incorporation into soil (see Chapters 2 and 12, this volume). There is good empirical evidence that introduction of earthworms together with organic matter into impoverished soil, with addition of organic matter and adjustment of pH, can increase soil fertility greatly, but there is little knowledge of the mechanism of such increases or even the best ways of introducing earthworms. Most important is the worldwide lack of knowledge of the geographic distribution of earthworms and populations of the different species. Until more is known of the fundamental biology and ecology and the activities of the many different species and their role in maintaining soil structure and fertility, it is impossible to assess their potential role in soil improvement. These problems are particularly acute in North America, where there are few earthworm specialists, and taxonomic research is extremely sparse.

CONCLUSIONS This second edition of Earthworm Ecology appears only 5 years after the first edition; it has been revised extensively, and four new chapters on important issues have been added. The reasons for creating a second edition so soon were partially because of rapid developments in earthworm biology and ecology and, to some extent, because of the great reception of the first edition by scientists and the public. It is hoped that this new edition will find a ready audience, and that it will encourage further interest in earthworms.

REFERENCES Barois, I., P. Lavelle, M. Brossand, L. Tondal, M. Martinez, J.P. Rossi, B.K. Senapati, A. Angeles, C. Fragoso, J.J. Jimienez, T. Decaens, C. Lattand, J. Kamyono, E. Blanchart, L. Chapius, G.E. Brown, and A. Monerno. 1999. Ecology of earthworms with large environmental tolerance and extended distribution, in Earthworm Management in Tropical Ecosystems, Lowell, P., L. Brussaard, and P. Hendrix, Eds., CABI Wallingford, Oxford, U.K., pp. 57–86.



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Blair, J.M., P.J. Bohlen, and D.W. Freckman. 1996. Soil invertebrates as indicators of soil quality, in Methods for Assessing Soil Quality, Doran, J.W. and Jones, A.J., Eds., Soil Science Society of America Special Publication 49, Madison, WI, pp. 273–291. Carter, A., J. Heinonen, and J. deVries. 1982. Earthworms and water movement, Pedobiologia, 23, 395–397. Darwin, C.R. 1881. The Formation of Vegetable Mould through the Action of Worms, with Observations on Their Habitats, Murray, London. Doran, J.W. and T.B. Parkin. 1996. Quantitative indicators of soil quality: a minimum data set, in Methods for Assessing Soil Quality, Soil Society of America Special Publication 49, Madison, WI, 25–38. Doube, B.M. and O. Schmidt. 1997. Can the abundance or activity of soil macrofauna be used to indicate the biological health of soils, in Biological Indicators of Soil Health, Pankhurst, C.E., B.M. Doube, and Gupta, Eds., USSR, CAB International, Wallingford, Oxford, U.K., pp. 265–296. Edwards, C.A. 1983. Development of a Standardized Laboratory Method Assessing the Toxicity of Chemical Substances to Earthworms, Report EUR 8714 EN, Environment and Quality of Life, Commission of the European Communities, Brussels, Belgium. Edwards, C.A. 1984a. Changes in agricultural practice and their impact upon soil organisms, in Proceedings of Symposium No. 13, The Impact of Agriculture on Wildlife, Agriculture and the Environment, Jenkins, D., Ed., N.E.R.C. U.K. pp. 46–65. Edwards, C.A. 1984b. Report of the Second Stage of a Standardized Laboratory Method Assessing the Toxicity of Chemical Substances to Earthworms, Report EUR 8714 EN, Environment and Quality of Life, Commission of the European Communities, Brussels, Belgium. Edwards, C.A. 1998. The use of earthworms in processing organic wastes into plant growth media and animal feed protein, in Earthworm Ecology, Edwards, C.A., Ed., CRC Press, Boca Raton, FL, pp. 327–354. Edwards, C.A. and P.J. Bohlen. 1992. The effects of toxic chemicals on earthworms, Rev. Environ. Contamination Toxicol., 125, 23–99. Edwards, C.A. and P.J. Bohlen. 1996. Earthworm Ecology and Biology, Chapman & Hall, London. Edwards, C.A. and J.R. Lofty. 1977. Biology of Earthworms, 2nd ed., Chapman & Hall, London. Edwards, C.A. and J.R. Lofty. 1978. The influence of arthropods and earthworms upon root growth of direct drilled cereals, J. Appl. Ecol., 15, 789–795. Edwards, C.A. and J.R. Lofty. 1982a. The effect of direct drilling and minimal cultivation on earthworm populations, J. Appl. Ecol., 19, 723–724. Edwards, C.A. and J.R. Lofty. 1982b. Nitrogenous fertilizers and earthworm populations in agricultural soils, Soil Biol. Biochem., 14, 515–521. Edwards, C.A. and A.R. Thompson. 1973. Pesticides and the soil fauna, Residue Rev., 45, 1–79. Edwards, W.M., R.R. Van der Ploeg, and W. Ehlers. 1979. A numerical study of noncapillary sized pores upon infiltration, J. Soil Sci. Soc. Am., 43, 851–856. Hopp, H. 1974. What Every Gardener Should Know About Earthworms, Garden Way Publishing, Charlotte, VT. Joshi, N.V. and B.V. Kelker. 1952. The role of earthworms in soil fertility, Indian J. Agric. Sci., 22, 189–196. Kretzchmar, A. 1978. Quantification ecologique des gaeeries de lombriciens. Techniques et premieres estimations, Pedobiologia, 18, 31–38. Kubiena, W.L. 1953. The Soils of Europe, Murray, London. Lavelle, P., L. Brussaard, and P. Hendrix. 1999. Earthworm Management in Tropical Agroecosystems, CABI Wallingford, Oxford, U.K. Lee, K.E. 1985. Earthworms: Their Ecology and Relationships with Soils and Land Use, Academic Press, Sydney, Australia. Linden, D.R., P.F. Hendrix, D.C. Coleman, and P.C.J. Van Vliet. 1994. Faunal Indicators of Soil Quality for a Sustainable Environment, Doran, J.W., D.C. Coleman, D.F. Bezolicek, and B.A. Stewart, Eds., Soil Science Society of America Special Publication 35, Madison, WI, pp. 91–10. Lungström, P.O. and Reinecke, A.J. 1969. Ecology and natural history of the microchaelid earthworms of South Africa 4. Studies on the influence of earthworms upon the soil and the parabiological question, Pedobiologia, 9(1–2), 152. Madge, D.S. 1965. Leaf fall and disappearance in a tropical forest, Pedobiologia, 5, 273–288. Meyer, L. 1943. Experimenteller Beiträge zu makrobiologischen Wirkungen auf Humus and Boden Bildung, Arch. Pflanzenerahrung Dungung Bodenkunde, 29, 119–140. Muller, P.E. 1878. Studier over Skovjord I. Om Bogemuld od Bogemor paa Sand og Ler, Tidsskrift Skogbruk, 3, 1–124.




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Parle, J.N. 1963. A microbiological study of earthworm casts, J. Gen. Microbiol., 31, 1–3. Ponomareva, S.I. 1953. The influence of the activity of earthworms on the creation of a stable structure in a sod-podzolised soil, Trudy Pochvenie Institut Dokuehaeve, 41, 304–318. Raw, F. 1962. Studies of earthworm populations in orchards. I. Leaf burial in apple orchards, Ann. Appl. Biol., 50, 389–404. Satchell, J.E. 1967. Lumbricidae, in Soil Biology, Burgess, A. and F. Raw, Eds., Academic Press, London, pp. 259–322. Shrickhande, J.E. and A.N. Pathak. 1951. A comparative study of the physico-chemical characters of the castings of different insects, Indian J. Agric. Sci., 21, 401–407. Slater, C.S. and H. Hopp. 1947. Relation of fall protection to earthworm populations and soil physical conditions, Proc. Soil Sci. Soc. Am., 12, 508–511. Stockdill, S.M.J. 1966. The effect of earthworms on pastures, Proc. N.Z. Ecol. Soc., 13, 68–75. Stockli, A. 1928. Studien über den Einfluss der Regenwurmer auf die Beschaffenheit des Bodens, Landwirtschaft Jahrbuch Schweiz, 42, I. Sugi, Y. and M. Tanaka. 1978. Number and biomass of earthworm populations, in Biological Production in a Warm Temperature Evergreen Oak Forest of Japan, Kira, T., Y. Ono, and T. Hosokawa, Eds., J.I.B.P. Synthesis 18, University of Tokyo Press, pp. 171–178. Swaby, R.J. 1950. The influence of earthworms on soil aggregation, J. Soil Sci., 1, 195–197. Teotia, S.P., F.L. Duley, and T.M. McCalla. 1950. Effect of stubble mulching on number and activity of earthworms, Neb. Agric. Exp. Stn. Bull., 165, 20. Tisdall, J.M. 1978. Ecology of earthworms in irrigated orchards, in Modification of Soil Structure, Emerson, W.W., R.R. Bond, and A.R. Dexter, Eds., Wiley, Chichester, U.K., pp. 297–303. Urquhart, A.T. 1887. On the work of earthworms in New Zealand, Trans. N.Z. Inst., 19, 119–123. Wilkinson, G.E. 1975. Effect of grass fallow rotations on the infiltration of water into a savanna zone soil of northern Nigeria, Trop. Agric. (Trinidad), 52, 97–103. Wollny, E. 1890. Untersuchungen über Beeinflussung der Fruchtbarkeit e der Ackerkrume durch die Tätigdeit der Regenwurmer, Forschungen Gebeit Agrik Physik Bodenkunde, 13, 381–395.


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Earthworms Affect Plant 2 How Growth: Burrowing into the Mechanisms George G. Brown Embrapa Soja, Londrina, Brazil

Clive A. Edwards Soil Ecology Laboratory, The Ohio State University, Columbus, OH, U.S.A.

Lijbert Brussaard Soil Quality Section, Wageningen University, Wageningen, The Netherlands

CONTENTS Effects of Earthworm on Plants: The History.................................................................................14 Earthworms and Plant Production in the Tropics ....................................................................15 The Mechanisms by Which Earthworms Affect Plant Growth: A Conceptual Background ...........................................................................................................17 Types and Modes of Interaction ...............................................................................................17 Spatial and Temporal Scales of Earthworm Action .................................................................17 Why Focus on Effects of Earthworms on Plant Roots? ..........................................................18 The Seven Main Mechanisms by Which Earthworms Affect Plants..............................................18 1. Dispersal and Changes in Populations and Activities of Beneficial Microorganisms........19 2. Changes in Populations and Impacts of Plant Pests, Parasites, and Pathogens..................23 Potential Role of Earthworms in the Reduction of Plant Disease and Pest Problems ..............................................................................................................23 Potential Role of Earthworms in Increasing Plant Disease or Pest Problems ..............25 3. Earthworms and Plant Growth-Regulating and Growth-Influencing Substances ...............25 4. Root Abrasion and Ingestion of Living Plant Parts by Earthworms...................................26 5. Interactions of Earthworms with Seeds ...............................................................................27 6. Changes in Soil Structure Caused by Earthworms..............................................................27 Earthworm Casts .............................................................................................................28 Earthworm Burrows ........................................................................................................30 7. Changes in Nutrient Spatiotemporal Availability Caused by Earthworms .........................31 Nutrients from Earthworms (Death, Excretion) .............................................................34 Crawling Forward: The Challenge of Identifying and Quantifying the Potential of Earthworms to Increase Plant Growth .........................................................................................34 “All-Minus-One” Tests and Field Trials...................................................................................35 The Earthworm Threshold Concept .........................................................................................36 Future Needs in Earthworm Research......................................................................................36

13 © 2004 by CRC Press LLC


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Acknowledgments ............................................................................................................................37 References ........................................................................................................................................37

EFFECTS OF EARTHWORM ON PLANTS: THE HISTORY The importance of earthworms for soils, plant growth, and society has undergone various phases, from profound recognition to utter ignorance and disdain. They were highly regarded as promoters of soil fertility during the Egyptian empire (Minnich 1977), and early philosophers such as Aristotle considered them beneficial animals, calling them the “earth’s entrails” (or intestines) (Kevan 1985). From antiquity to Darwin’s time, however, not much information is available on earthworms (see review by Kevan 1985); throughout much of the 17th up to the beginning of the 20th century, earthworms were considered garden pests that needed elimination from soils (Minnich 1977; Brown et al. 2004). Probably the earliest and best-known report of the potential benefits of earthworms to soils is the much-quoted letter of Rev. Gilbert White to the Hon. Daines Barrington, written on May 20, 1777. This letter also provided some first hints of the mechanisms by which earthworms affect plant growth. White (1789) wrote: Dear Sir — … Earthworms, though in appearance a small and despicable link in the chain of Nature, yet, if lost, would make a lamentable chasm. For to say nothing of half the birds, and some quadrupeds which are almost entirely supported by them, worms seem to be the great promoters of vegetation, which would proceed but lamely without them, by boring, perforating, and loosening the soil, and rendering it pervious to rains and the fibers of plants, by drawing straws and stalks of leaves and twigs into it; and most of all, by throwing up such infinite numbers of lumps of earth called worm-casts, which, being their excrement, is a fine manure for grain and grass … Gardeners and farmers express their detestation of worms; the former because they render their walks unsightly, and make them much work; and the latter because, as they think, worms eat their green corn. But these men would find that the earth without worms would soon become cold, hard-bound, and void of fermentation, and consequently sterile; and, besides, in favour of worms, it should be hinted that green corn, plants, and flowers, are not so much injured by them as by many species of coleoptera (scarabs), and Tipulidae (long-legs) in their larva, or grub-state; and by unnoticed myriads of small and shell-less snails, called slugs, which silently and imperceptibly make amazing havoc in the field and garden.

It was not until almost a century later that Darwin (1881), in his book The Formation of Vegetable Mold Through the Action of Worms, firmly established the benefits of earthworms to soils. Other authors (Hensen 1877, 1882; Müller 1878, 1884; Wollny 1890) supported the positive role of earthworms in soil processes and plant growth, and Wollny (1890) was the first actually to quantify this relationship. Despite initial skepticism about the reports of Darwin and Hensen (Wollny 1882a), he became convinced that earthworms were important for plant production when his experiment showed increased yields of 12 species of plants, ranging from negligible amounts up to 733% (rape), by adding earthworms (Wollny 1890). However, he continued to warn about the generalization of these results to field situations. From the early 20th century to the present, the number of experiments increased, and the intervals between them decreased, so that there are presently more than 120 papers published on the effects of earthworms on plant production. The aim of most of these investigations was to answer the following questions: • • •

Do earthworms affect plant growth (positively or negatively), and if so, by how much? Which plants are affected most (positively or negatively)? Which earthworm species are most efficient at promoting plant growth?



How Earthworms Affect Plant Growth: Burrowing into the Mechanisms

15

However, despite the abundant literature on the responses of plants to earthworms and the identification of a number of soil, environmental, or earthworm factors associated with particular plant responses, rarely has the question of how these effects occur (i.e., what the mechanisms behind the observed effects are) been addressed properly (Blakemore and Temple-Smith 1995; Edwards and Bohlen 1996; Brussaard 1999). In most papers, mechanisms were alluded to only briefly, and in several instances, the possible reasons for the observed effects of earthworms were not even mentioned. Furthermore, the proposed mechanism often cannot be confirmed or validated. The reason for this apparent lack of focus on the mechanisms behind the effects of earthworms on plants may be partly because of the following: •

•

• •

The predominant paradigms driving agricultural development from Liebig (1840) up to the “green revolution” period (ending in the 1970s), with research focusing mainly on alleviating physical and chemical constraints to plant production through the use of artificial inorganic inputs and improved (often hybrid) crop varieties (Sánchez 1994) Production (yield-oriented) research that has concentrated mainly on aboveground plant responses and rarely has studied changes in root growth, morphology, distribution, and the belowground interactions (e.g., of earthworms with microorganisms) Inadequate experimental designs or insufficient criteria on parameters measured to assess the possible mechanisms involved The very complex nature of indirect and direct biological interactions that occur in soils, particularly between earthworms, soil properties and processes, and other organisms in soils

EARTHWORMS

AND

PLANT PRODUCTION

IN THE

TROPICS

Many aspects of the effects and management of earthworms in tropical agroecosystems were reviewed by Lavelle et al. (1999). In particular, Brown et al. (1999) summarized the results of 28 experiments in the greenhouse and at the field level that identified the various soil properties and processes affected by earthworm activities and their impacts on plant production. The experiments were done in 8 tropical countries and involved at least 34 earthworm species and 19 plant species and were tested in 23 soil types belonging to 8 soil groups. An analysis of 246 studies of the effects of earthworms on plant shoot production (Figure 2.1) and 88 studies of the effects of earthworms on grain yields demonstrated clearly that earthworms usually have positive effects on plant growth (75% of all studies resulted in plant growth increases) and biomass. A mean 57% increase was observed in plant shoot mass, and a 36% increase was found for grain yields. Important negative effects occurred only rarely, usually because of some dysfunction in the soil created or induced by earthworm activities. They also observed that root production, contrary to that of the aboveground parts, was usually affected less by earthworm activity, possibly because of difficulties in studying this parameter or because plants growing in more healthy soils (presumably the case in earthwormworked soils) tend to invest more energy in growing the aboveground plant parts, producing fewer roots per unit shoot biomass, resulting in higher shoot:root ratios. The factors that seemed to affect the ultimate responses of plants to earthworms were the following: • •

•

The part of the plant harvested, with greater effects of earthworms on biomass (positive) of shoots than grains and with the smallest effects on root growth. The species of plant involved, with greater effects of earthworms on the shoot growth of perennial plants (trees and bushes) and larger effects on yields of gramineous grain crops compared with legumes. The species of earthworms involved, with the pantropical endogeic species Pontoscolex corethrurus producing the greatest yield increases and the widespread Indian Dichogastrini



16


In 43% of cases, increase was >20%

100 to 200% (9%)

>300% (2%) –100 to – 60% 200 to 300% (0.4%) (5%) –60 to –20% (4%) –20 to 0% (20%)

60 to 100% (6%)

20 to 60% (21%) 0 to 20% (33%) In 75% of cases, earthworms affected plant biomass positively

Region of generally nonsignificant effects (with little short-term importance but with possible cumulative importance)

FIGURE 2.1 Effects of tropical earthworm species on plant shoot production. Each slice of the pie indicates a range of shoot biomass increase due to earthworms (e.g., 0 to 20%), and the percentage of cases where that range of increase was observed (values in parentheses). The chart was built using 246 data points (cases) taken from a total of 28 experiments involving at least 34 earthworm and 19 plant species tested in 23 soil types belonging to 8 great groups. (Modified from Brown et al., 1999.)

species Drawida willsii and West African species Millsonia anomala and various small eudrilids all having a good potential for introduction and management into soils. • The earthworm biomass introduced or present in the soil, with higher yields usually occurring in response to greater earthworm biomass in a curvilinear relationship (moderate yield increases of 20 to 40% occurred with earthworm biomass values above 17 g m−2 and over 40% of grain production increases occurred with earthworm biomasses above 32 g m−2). • Εarthworm survival. In both pot and field trials, the mortality of introduced earthworms was often high, particularly when the species was not adapted properly to the soil used or when few or no organic residues were applied (survival was greater when organic residues were present). • The presence of organic residues on the soil surface, with greater effects on plant yields when such residues were present. • The timescale of the measurements (i.e., the duration of the experiment), usually with positive cumulative increases in plant biomass because of earthworm activities with time, although occasionally (depending on the soil type or earthworm and plant species) the cumulative effects on plant biomass observed were negative. • Τhe spatial scale of the experiment (i.e., pot vs. field experiments), with effects on yield usually greater at the pot scale for any given plant and earthworm combination. • The natural richness of the soil used in the experiment, with greater benefits on productivity in poorer soils (low percentage carbon content, coarser textures) than in richer soils (more carbon, clayey texture) with earthworms producing higher yields in moderately acid soils (pH between 5.6 and 7.0) than in strongly acid soils (pH < 5.6) or alkaline soils (pH > 7.0). Different combinations of earthworm species, soil types and conditions, plant species, and various imposed human or environmental constraints may alter the potential effects of the earthworms on soil properties and plant growth. Thus, pinpointing the exact reasons for mechanisms




17

of a specific plant response to earthworms in an experiment is not easy; more often than not, several mechanisms rather than a single mechanism are probably operating simultaneously. The main aim of this chapter is to seek and identify possible mechanisms by which earthworms can promote or suppress plant growth. Furthermore, we dig further into some of these mechanisms and provide both conceptual diagrams of how they may be functioning and a few case studies dealing with each of the seven main mechanisms we propose. Finally, we end with some suggestions on how advancement will occur in this biologically complex area of research. Our basic premise is that through better understanding of the ways by which earthworms affect plant growth and production, plant and soil management techniques and practices can be adapted, improved, or implemented to prevent the occurrence of negative effects of earthworms on soils and plants and to maximize their positive effects on crops for the benefit of farmers, gardeners, ranchers, foresters, and other land users.

THE MECHANISMS BY WHICH EARTHWORMS AFFECT PLANT GROWTH: A CONCEPTUAL BACKGROUND TYPES

AND

MODES

OF INTERACTION

The effects of earthworms on soils can take three main forms: effects on biological, physical, or chemical soil properties and processes. Furthermore, because earthworms share the soil environment with roots, their effects on plant growth and root development can be either direct or indirect. Thus, the mechanisms of how earthworms influence plant productivity can be divided into three main types: physical, chemical, and biological. These can operate either directly or indirectly. Indirect effects mean that the plant is affected by earthworm activities through changes in the physical, chemical, or biological soil or rooting environment produced by earthworms; the direct mode of action means that the earthworms or their activities lead to direct changes in root growth and productivity.

SPATIAL

AND

TEMPORAL SCALES

OF

EARTHWORM ACTION

The soil volume affected by earthworm activities has been termed the drilosphere (Lavelle 1988); it constitutes one of the main soil functional domains (Beare et al. 1995; Lavelle 2002) that have significance in regulating major soil processes and functions, such as structure, organic matter (OM) decomposition, nutrient cycling, microbial and invertebrate populations, and plant growth. Because earthworm burrows and casts may outlive the earthworms themselves, and regulate the soil as an environment for other organisms (including plant roots) by controlling its physical structure, nutrient fluxes, and energetic status (resource availability), they have been termed ecosystem engineers (Jones et al. 1994; Lavelle et al. 1997). It is important to note that the drilosphere and the engineering effects of earthworms are very variable and depend on biological factors such as the type of vegetation and the characteristics and composition of the earthworm community at a particular location (species, abundance, biomass, age structure, ecological strategy) and abiotic regulating factors, including climate, soil type, and imposed anthropic (management) factors. Furthermore, the earthworm drilosphere is a dynamic zone of action that is constantly changing in both space and time as the earthworms ingest and reingest soil, burrow, and cast at different rates and in different locations in the soil. Therefore, the drilosphere can affect soil functions (including plant productivity) at different spatiotemporal scales, manifesting its effects at levels that range from the earthworm gut up to the soil profile (Lavelle 1997); these ideas are explored in Chapter 12. The effects of earthworms on plants in a given situation and the mechanisms involved are difficult to assess because, although earthworms and their structures (burrows, casts) are often easily identifiable or separable from the edaphosphere and their sphere of influence on the soil © 2004 by CRC Press LLC


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(drilosphere) can be measured and quantified physically, chemically, and biologically under controlled conditions, the drilosphere is connected with the rest of the soil system. This means that it can interact profoundly with other soil organisms and functional domains (e.g., rhizosphere, porosphere, aggregatusphere, detritusphere, mermycosphere, termitosphere) (Brown et al. 2000). This interconnectedness becomes even more evident as in attempts to separate the mechanisms responsible for plant responses to earthworms in any given situation, soil type, or area.

WHY FOCUS

ON

EFFECTS

OF

EARTHWORMS

ON

PLANT ROOTS?

Roots, as sensitive sensors of the soil environment and the producers of many signals that ultimately control plant shoot growth (Aiken and Smucker 1996), are the primary and immediate receivers of the contributions of earthworms to soil functions. By controlling nutrient and water supply to the shoots, it is the biomass, density, distribution, and activity (growth rate and longevity) of roots within the soil profile that will largely determine plant productivity (Brown and Scott 1984). Thus, it is the response of roots to earthworm activity that usually controls the overall plant response. A simple conceptual model connecting the physical, chemical, and biological effects of earthworms on soils with their potential effects on plant root or shoot growth and nutrition is provided in Figure 2.2. The interdependence of earthworm physical activities (production of casts and burrows) and earthworm physiological activities (excretions, secretions, and tissue death) in interactions with soil properties such as organic matter (soil OM, root and residue inputs), microbial populations, and plant production is evident. The effects of chemical substances on soil properties and processes are based on the selection by earthworms of particular soil particles and organic matter, the different nutrient compositions of their feces compared with uningested soil, cutaneous mucus secretion, and excretion of metabolic products. Biological effects on soils are caused primarily by interactions of earthworms with the rhizosphere and soil microorganisms, depending especially on feeding and digestive habits of the earthworms; the physical effects are associated mainly with the structural properties of the drilosphere. The following sections in this chapter explore the various ways in which earthworms can directly and indirectly affect plant growth, and we propose seven main mechanisms by which this is achieved. The focus is mainly on roots, although we recognize that indirect interactions with the aboveground plant parts and other organisms (both above- and belowground) may also be important (Wurst and Jones 2003). Given that the latter subject is a very recent field of study and that few results are available, we will limit the discussion primarily to belowground interactions and processes.

THE SEVEN MAIN MECHANISMS BY WHICH EARTHWORMS AFFECT PLANTS We define the seven main mechanisms by which earthworms affect plant growth as follows (see details in Table 2.1): 1. 2. 3. 4. 5. 6. 7.

Dispersal and changes in populations and activity of beneficial microorganisms Changes in populations and impacts of plant pests, parasites, and pathogens Production of plant growth-regulating (PGR) and plant growth-influencing (PGI) substances Root abrasion and ingestion of living plant parts by earthworms Interactions of earthworms with seeds Changes in soil structure caused by earthworms Changes in nutrient spatiotemporal availability caused by earthworms

Mechanisms 1 to 5 are mainly biological, operating indirectly (1 and 2) or directly (3 to 5); the last two (6 and 7) are indirect physical (6) or chemical (7) mechanisms. © 2004 by CRC Press LLC



19

PLANT

OTHER ORGANIC MATTER SOURCES

Nutrient absorption

ORGANIC MATTER

Rhizodeposition

Excretions, secretions, dead tissue

MICROBIAL POPULATIONS and ACTIVITY H2O and air circulation

EARTHWORMS CASTINGS

BURROWS Better root penetration SOIL FIGURE 2.2 Simplified conceptual model connecting the physical, chemical, and biological earthworm effects on soils with their potential effects on plant growth and nutrition. (Modified from Cuendet and Bieri, 1999; Syers and Springett, 1983.)

1. DISPERSAL AND CHANGES MICROORGANISMS

IN

POPULATIONS

AND

ACTIVITIES

OF

BENEFICIAL

Large populations of beneficial (plant growth promoting [PGP]) microorganisms such as saphrophytic and mycorrhizal fungi, actinomycetes (e.g., Frankia), bacteria, and microinvertebrates, such as protozoa and microbivore (fungivorous, bacteriophagous, predatory omnivorous and entomophathogenic) nematodes inhabit the soil. Nevertheless, because of their limited ability to disperse within the soil and the soil environmental and nutritional limitations to their activities, a large proportion of soil microorganisms are inactive at any given time, waiting for suitable conditions to promote higher levels of activity (Lavelle 1997). Invertebrate activities, such as earthworm burrowing and casting, promote soil mixing and bring microorganisms into contact with inaccessible soil resources, stimulating both their populations and their activity. The earthworm gut also provides an ideal environment for enhanced activity levels or multiplication of some microorganisms; others may be digested or their activity levels reduced by passage through the earthworm gut (Brown et al. 2000). The complex resulting effects of earthworms on microbial communities in soils (activity, populations, diversity) depend on the reactions of microorganisms to passage through the earthworm gut and the ability of microorganisms to utilize the drilosphere. Thus, earthworms may affect microbial populations (beneficial, facultatively pathogenic, and adverse species) directly, by feeding and digestive processes or indirectly by burrowing and casting activities, which change root growth and development and the soil environment, thereby making it more or less favorable to the development of microorganisms (Figure 2.3). Furthermore, as earthworms move through the soil matrix, they may disperse microorganisms, both superficially (on the earthworm body) or via ingestion-egestion (in casts). The ability of earthworms to disperse microorganisms or stimulate microbial activity and increase microbial populations depends greatly on the earthworm’s spatial range of activity, food requirements and sources, and behavior. Epigeic, litter feeding, and dwelling species of earthworms are much more © 2004 by CRC Press LLC


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TABLE 2.1 The Seven Main Mechanisms by Which Earthworms Affect Plant (Mostly Root) Growth either Directly or Indirectly through Physicochemical or Biological Changes to the Soil Environment Mechanism Category (Type) Mechanism Mode Indirect (mediated through changes in the rooting environment, or via interactions with organisms that affect root growth and production)

Direct (earthworm activities that influence root growth/production in a direct manner)

Biological

Physical

Chemical

1. Dispersal or changes in populations 6. Changes in soil 7. Changes in nutrient and activity of beneficial structure caused by spatiotemperal microorganisms (plant growth earthworms (pore and availability caused by promoting rhizobacteria, N2 fixing root aggregate size distribution earthworms (release or symbionts, saprophytic and mycorrhizal and associated processes, immobilization of fungi, microbial biocontrol agents, including aeration, water different plant nutrients, microbivorous and entomopathogenic retention, hydraulic leaching, denitrification, nematodes, protozoa) conductivity, infiltration, volatilization, OM 2. Effects of earthworms on populations erosion, runnoff, aggregate mineralization, protection and crust formation and and/or humification, of plant pests, parasites, and breakdown, chelation of metals, pH pathogens (increase or decrease in compaction/soil slumping changes) populations and incidence of plantand decompaction/soil parasitic nematodes, phytopathogenic fungi and bacteria, plant viruses?, shoot- loosening) and root-feeding insects) 3. Production of plant growth promoting/regulating substances (hormones, vitamins, humic matter, auxins, cytokinins, gibberellins, ethylene, microbially induced and/or excreted by earthworms. 4. Root abbrasion and ingestion of living plant parts by earthworms (feeding and/or ingestion by earthworms of living roots or plant shoots, and direct damage to growing roots) 5. Interactions between earthworms and seeds (ingestion, digestion, burial, dispersal, changes in germination rates and potential)

likely to affect microorganisms in the litter layer and the roots growing through the organic matter/humus (O/H) horizons and the soil surface-litter interface compared with the endogeic (soil-dwelling) geophagous (soil-feeding) earthworm species, which tend to have a greater effect on microorganisms living within the soil. Anecic, litter-burying species of earthworms, which create deep vertical burrows and surface middens (small mounds of leaves blocking the entrance of vertically oriented burrows connected to the soil surface) can have a major influence on microorganisms (fungi, bacteria, actinomycetes) and micro-, meso-, and macroinvertebrates (protozoa, nematodes, mites, springtails, enchytraeids, millipedes, isopods, other earthworms) in surface litter communities (Brown 1995; Anderson and Bohlen 1998; Maraun et al. 1999). However, their effects on the microbial communities living within the soil are probably less than those of endogeic species because of their decreased soil-burrowing activities as they tend to build more permanent burrow systems. Nevertheless, anecic earthworm species (and large endogeic species) often have burrows that reach depths of more than 2 m, which can represent important pathways of microbial dispersal and hot spots of microbial and root growth activity compared with that in the surrounding soil matrix (Bhatnagar 1975; Ehlers et al. 1983). © 2004 by CRC Press LLC



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Beneficial plant-growth promoting (PGP), facultative, or obligatory pathogenic rhizosphere microorganisms Earthworm feeding Time

Root growth and development

Soil/rooting environment

Earthworm burrowing and casting

FIGURE 2.3 Interactions among beneficial, facultative and obligatory plant-pathogenic rhizosphere microorganisms, earthworms, plant roots and the abiotic root environment, determining plant root growth and development (note: this is a modified version of the classic “plant disease triangle” taught in plant pathology).

It has often been suggested that earthworms tend to promote changes in the microbial community toward a bacterial-based trophic chain. Actually, phospholipid fatty acid (PLFA) methyl esters analyses of earthworm-worked soils indicated that Gram-negative bacteria seem to be favored compared with Gram-positive bacteria (Clapperton et al. 2001; Enami et al. 2001). Lumbricid earthworms also increase bacterial-to-fungal ratios (Clapperton et al. 2001), although when a plantpathogenic fungus was inoculated into the soils, earthworms decreased this ratio, implying that they may also increase the soil fungal biomass. Nevertheless, several species of fungi have been shown to be ingested preferentially by the earthworm Lumbricus terrestris (Moody et al. 1995; Cooke 1983; Moody et al. 1995; Bonkowski et al. 2000), and Edwards and Fletcher (1988) reported that fungi were a major food source for earthworms. This implies that earthworms (particularly the litter-burying or fragmenting anecic and epigeic species) may impose some selection pressures on fungal populations in both litter and soils. Bacterial-to-fungal ratios in soils are also often greater in earthworm-worked soils because bioturbation tends to affect fungal populations negatively more than those of bacteria (Hendrix et al. 1986). The rhizosphere, a less-than-0.5-mm soil layer surrounding plant roots, is rich in microorganisms, with species that are beneficial or adverse to root growth. Several earthworm species (especially some endogeics) seem to feed mainly in the rhizosphere (James and Seastedt 1986; Rovira et al. 1987; Robertson et al. 1994; Hirth et al. 1998). Activity of lumbricid earthworms has been reported in the rhizosphere of a temperate pasture (Carpenter 1985) and of wheat (Doube and Brown 1998), and feeding in the rhizosphere was inferred from radio- (14C) or stable isotope (15N, 13C) analyses of the tissues of earthworms (L. terrestris and P. corethrurus) living in soils under various plants (wheat, maize, Brachiaria decumbens, and sugarcane) (Spain et al. 1990; Spain and Le Feuvre 1997; Cortez and Bouché 1992; Brown 1999). There are also records of earthworms feeding on living and dead root tissues (see mechanism 4), but the role of root tissues and their derivatives (rhizodeposition) in earthworm diets remains little understood (Brown et al. 2000). Earthworm feeding or movement in or around the rhizosphere can have important consequences for associated microbial and faunal communities (activity, populations, diversity) and thus, indirectly, on plant productivity (Figure 2.3).



22


T3

T2

T1

700 mg (10 earthworms) 350 mg (5 earthworms) 0 mg (no earthworms) 31% MICORRIZAE

30% MICORRIZAE

6.6% MICORRIZAE

FIGURE 2.4 Stimulation of Eugenia stipitata (arazá) growth and root mycorrhizal colonization 120 days after inoculating tree nursery bags (filled with 2 parts soil and 1 part composted sawdust) with five (0.35 g total wet weight) or ten (0.7 g) individuals of the pantropical geophagous endogeic earthworm species P. corethrurus. (Ydrago 1994; Photograph P. Lavelle.)

Dispersal of mycorrhizal propagules (hyphae, infected root fragments, spores) has been reported by various authors (McIlveen and Cole 1976; Rabatin and Stinner 1988; Ponge 1991; Reddell and Spain 1991a; Gange 1993; Lee et al. 1996; Cavenden et al. 2003), and although some hyphae and spores may be digested, many are still infective after passage through the earthworm gut (Reddell and Spain 1991a; Gange 1993). Mycorrhizal dispersal and deposition of earthworm casts in the rhizosphere may benefit root colonization by fungi, aid plant establishment in early successional stages, and contribute to the heterogeneous nature of mycorrhizal distribution in soil communities (Gange 1993). For example, the pantropical geophagous endogeic earthworm species P. corethrurus increased colonization of roots by arbuscular mycorrhizae in various tropical tree seedlings (Ydrogo et al. 1994; Figure 2.4) and a pasture grass (Brown et al. 2000), also increasing plant biomass on several occasions. The actinomycete Frankia and ectomycorrhizae were also shown to be dispersed by P. corethrurus (Reddell and Spain 1991b; Reddell et al. unpublished), although the effects of this on plant productivity are little known. Nevertheless, soil bioturbation and feeding in the rhizosphere by earthworms may break up extramatrical hyphae and the hartig net, thereby reducing root colonization by these root symbionts, hence providing potential benefits to the plants (Pattinson et al. 1997; Brown et al. 2000; Tuffen et al. 2002). Plant growth-promoting rhizobacteria (PGPR) such as Enterobacter cloacae, Azotobacter, Azospirillum, Acinetobacter, Bacillus, and Pseudomonas spp. may also be dispersed and their populations or activity increased in the drilosphere (Bhat et al. 1960; Kozlovskaya and Zdhannikhova 1961; Kozlovskaya and Zaguralskaya 1966; Bhatnagar 1975; Loquet et al. 1977; Hand and Hayes 1983; Savalgi and Savalgi 1991; Pederson and Hendriksen 1993). The metabolites released by these microorganisms may be particularly important to the potential plant responses (mechanism 3). Dispersal of these and other microorganisms such as biocontrol bacteria (e.g., Pseudomonas corrugata) and fungi (e.g., Gliocladium virens, Trichoderma harzianum) that colonize the rhizosphere and prevent root diseases needs further investigation. The dispersal of various symbiotic N2-fixing rhizobacteria that nodulate legume roots (e.g., Rhizobium trifolii in clover; Doube et al. 1994a) also needs further research (Stephens et al. 1994e; Stephens and Davoren 1994; Singer et al. 1999). These microorganisms all have an inability to spread actively and rapidly through the




23

soil and colonize plant roots extensively, so earthworms may act as important dispersal vectors for them (Rouelle 1983; Stephens et al. 1993b; Doube et al. 1994b). Populations and activity of several groups of beneficial soil organisms important in plant litter decomposition and nutrient mineralization processes in soils (e.g., microfauna, mesofauna, and macroinvertebrates) may be affected by earthworms (Brown 1995). For instance, protozoa may be part of earthworm nutrition (Miles 1963; Flack and Hartenstein 1984; Bonkowski and Schaefer 1997), but many protozoan cysts can survive passage through the earthworm gut and can hatch, become more active, and reproduce rapidly in earthworm casts and earthworm-worked soils (Shaw and Pawluk 1986; Barois 1987; Winding et al. 1997; Binet et al. 1998). Earthworm casts may benefit bacteriophagic nematode populations preferentially over those of other nematode trophic groups (Roessner 1981, 1986; Senapati 1992), but the total numbers of freeliving nematodes in earthworm-worked soils may be reduced (e.g., Alphei et al. 1996; Dominguez et al. 2003) or increased (Winding et al. 1997), depending on the situation. Populations of other organisms, such as enchytraeids and various micro- and macroarthropods, may also be increased (e.g., in anecic earthworm middens) or decreased because of changes in microbial populations and food resources in earthworm-worked soils (Brown 1995). However, most of the consequences to plant growth of changes in the populations and activity of micro and macroinvertebrates in earthworm middens, castings, and earthworm-worked soils are unknown and deserve much more attention.

2. CHANGES PATHOGENS

IN

POPULATIONS

AND IMPACTS OF

PLANT PESTS, PARASITES,

AND

As with beneficial microorganisms, earthworm feeding, burrowing, casting, and dispersing activities can alter the distribution of populations of plant pathogens such as viruses, bacteria, fungi, parasitic nematodes, or insect pests in soils. Furthermore, by making plants more or less susceptible to these pests, parasites, and pathogens, earthworms can affect root health (Brown 1995). These relationships are illustrated in a modified version of the classic “plant-disease triangle” (Figure 2.3) in which plant root growth and development are shown as a function of the interactions between a favorable environment for both roots and pathogens and the presence or activity of “virulent” of “infective” plant pathogens. The result of these interactions (i.e., plant health status) may therefore be influenced directly or indirectly by earthworm activities. Earthworms are known to transport and consume a wide variety of plant pathogenic fungi and bacteria and plant-parasitic nematodes (Brown 1995). If populations of these organisms are reduced either directly by transit through the earthworm gut or indirectly via changes in the soil environment, then the indirect consequences to plant growth may be important, particularly when disease or nematode pressure is reducing crop yields. The role of earthworms as vectors of plant diseases, parasites, and pests depends on the type of organism and species ingested, the amount of soil and inoculum ingested, the extent of beneficial or antagonistic intestinal secretions, the number of organisms digested in the earthworm gut, the amount of organisms deposited in casts, the infectivity of surviving organisms deposited in casts, the feeding and casting behavior of the earthworms (dependent on the earthworm species and ecological category), and the mobility and behavior of the earthworm. Potential Role of Earthworms in the Reduction of Plant Disease and Pest Problems Several reports of beneficial results to plants of earthworm-induced reductions of plant pathogens are known. For instance, work in the Soil Ecology Laboratory at The Ohio State University has shown that vermicomposts can suppress plant diseases such as Pythium and Rhizoctonia (Chaoui et al. 2002, 2003) in the greenhouse and Verticillium in the field. When cabbages were grown in the presence of the earthworm Pheretima hilgendorfi, Nakamura et al. (1995) observed lower incidence of club-root disease (Plasmodiophora brassicae) damage in the seedlings. They attributed this decrease to the © 2004 by CRC Press LLC


24


physical, chemical, and biological changes in the soil environment because of earthworm activity, reinforced by possible consumption of the pathogens by the earthworms (Nakamura 1996). In Australia, several complementary studies (Stephens et al. 1994a,b,c,e,f,g; Stephens and Davoren 1997) reported that the earthworms Aporrectodea rosea and Aporrectodea trapezoides could increase yields of wheat, ryegrass, and subterranean clover under greenhouse and field conditions by decreasing the incidence of Rhizoctonia solani (bare patch disease). Furthermore, wheat yields were also increased by these earthworms through a reduction in incidence of Gauemannomyces graminis var. tritici (takeall disease); A. trapezoides appeared to be more effective in disease suppression, probably because of higher feeding and casting levels compared with A. rosea. Although the exact mechanisms by which earthworms influence root diseases (including takeall) remain unknown, Clapperton et al. (2001) suggested that they are most probably mediated through changes in the soil microbial community, possibly via stimulation of biocontrol agents, antagonists, or microbial competition with the pathogens. Various other indirect mechanisms have also been proposed, such as acceleration of residue decomposition, burial of infected litter, increased soil porosity, and greater availability of plant nutrients in earthworm-worked soils. For instance, in various fruit-tree orchards, the burial of 12 fungal pathogens overwintering in the surface leaf litter (including Venturia inaequalis, the causal agent of apple scab) by the anecic earthworm species L. terrestris (Raw 1962) reduced their survival and ability to disperse, colonize, and infect the apple trees the following spring (Hirst and Stedman 1962; Niklas and Kennel 1981; Laing et al. 1986; Kennel 1990). Decreases in plant parasitic nematode populations by earthworm activity have also been documented for various (tropical and temperate) earthworm and nematode species combinations ( Dash et al. 1980; Roessner 1981, 1986; Senapati 1992; Boyer 1998). For instance, Boyer (1998) observed a reduction of Pratylenchus zeae populations in small pots (200 g soil) sown with rice and containing the earthworm species P. corethrurus. However, the effects of the earthworms on plant shoot and root growth was negative. Conversely, Boyer et al. (1999) observed significantly greater maize productivity and decreased Pratylenchus vulnus populations on maize roots when maize was undersown with the legume birdsfoot trefoil, and earthworms (Amynthas corticis) were introduced into the field. Yeates (1980, 1981) also reported greater plant productivity and lower populations of nematodes, including some plant parasitic species in pastures inoculated with lumbricid earthworms in New Zealand. Reduction of plant parasitic nematode populations in the field have also been observed after application of vermicomposts (Arancon et al. 2002, 2004a,b). Earthworm-induced decreases in nematode populations may be caused by direct ingestion and digestion of nematodes (Dash et al. 1980; Boyer 1998; Dominguez et al. 2003) or the release of fluids (enzymes, etc.), which affect the fertility, viability, and germination of cysts present in earthworm-worked soils and casts (Ellenby 1945; Roessner 1981; Boyer 1998), or they may be caused indirectly through modifications by earthworms of soil structure, water regimes, and nutrient cycling processes (Yeates 1981). Edwards and Fletcher (1988) and Manku (1980) have also suggested that earthworms may spread nematode-trapping fungi and nematode cyst pathogens of major importance in controlling nematode populations. Nematodes that pass unharmed through the earthworm gut or are able to take advantage of or adapt to earthworm-induced changes in soil properties and processes may be dispersed by earthworms. In the case of plant parasitic species, this could lead to potential problems, but for entomopathogenic nematodes commonly used in insect pest biocontrol, this may be beneficial (Shapiro et al. 1993). Several studies have demonstrated the potential effects of earthworms in reducing plant-pest incidence and damage. Boyer et al. (1999) reported fewer maize plants infested with the stalk borer Sesamia calamistis when the earthworm A. corticis was inoculated into field soils. The percentages of fertile maize plants infested by the borer were 75% without earthworms and 55% in soils with earthworms, although the total aboveground biomass of the two treatments did not differ significantly. In another study, L. terrestris was shown to reduce the numbers of leaf miners (Phyllonorycta blancardella) and leaf suckers (Psylla piri) overwintering in leaf litter of fruit-tree orchards by © 2004 by CRC Press LLC



25

promoting leaf burial and decomposition (Laing et al. 1986; Kennel 1990), thus reducing their potential to damage the orchard trees. However, leaf-litter burial also reduces populations of the natural biocontrol agents (brachonid wasps) of these insects (Laing et al. 1986). Potential Role of Earthworms in Increasing Plant Disease or Pest Problems Several species of plant pathogenic fungi have been found in earthworm casts (Hutchinson and Kamel 1956; Hoffmann and Purdy 1964; Thornton 1970; Melouk and Horner 1976; Toyota and Kimura 1994), and plant parasitic nematodes may survive passage through the earthworm gut (Ellenby 1945; Russom et al. 1993). However, there are relatively few data available on the potential negative effects that earthworm-induced microbial dispersal may have on incidence of plant diseases (of fungal or bacterial origin) or nematode damage. Increased dispersal of a plant pathogenic fungus, Syntrichium endobioticum, the causal agent of wart disease of potato, by L. terrestris and various other (probably lumbricid) earthworms was reported by Hampson and Coombs (1989), resulting in increased infection of several potato plants. Similarly, Melouk and Horner (1976) reported infection of mint seedlings by verticillium wilt (Verticillium dahliae) when the plants were grown with earthworm casts that contained viable spores of these pathogens. Dispersal of plant parasitic nematodes by earthworms was reported by Ellenby (1945) and Russom et al. (1993), but the potential of this for increased damage to plant roots was not evaluated. Casts of the Nigerian earthworm species Agrotoreutus nyongii had larger and more diverse populations of parasitic nematodes than did the surrounding soil (Russom et al. 1993). Casts of Aporrectodea longa contained nematode cysts with greater fertility, viability, and germination potential than those in surrounding soil (Ellenby 1945). Ilieva-Makulec and Makulec (2002) reported an increase in plant parasitic nematode populations in soil cores inoculated with Lumbricus rubellus after 60 and 90 days, but no negative effects on growth of grass roots were observed. The interactions between earthworms and plant insect pests still remain poorly explored. Kirk (1981) reported large numbers of the northern maize rootworm (Diabrotica: Coleoptera) eggs in earthworm burrows and suggested that this may contribute to the spottiness of rootworm distribution and damage often observed in maize fields. More recently, Wurst and Jones (2003) and Scheu et al. (1999) showed effects of lumbricid earthworms (Aporrectodea sp.) on increased numbers of leaf sap sucking aphids (Myzus persicae) and their offspring.

3. EARTHWORMS SUBSTANCES

AND

PLANT GROWTH-REGULATING

AND

GROWTH-INFLUENCING

The first suggestion that earthworms might produce plant growth regulators (PGRs) was by Gavrilov (1963). This was supported by the first report of the presence of PGR substances in the tissues of Aporrectodea caliginosa, L. rubellus, and Eisenia fetida by Nielson (1965), who extracted indole substances from earthworms and reported increases in the growth of peas because of them. He also extracted a substance that stimulated plant growth from A. longa, L. terrestris, and Dendrobaena rubidus, but his experiments did not exclude the possibility that the PGR substances he obtained came from microorganisms living in the earthworm guts and tissues. The presence of PGR substances in the tissues of A. caliginosa, L. rubellus, and E. fetida was confirmed by Nielson (1965), who isolated indole substances from whole earthworm tissues. This was confirmed for A. rosea and A. caliginosa by Nardi et al. (1988). More recently, El Harti et al. (2001a,b) isolated indole acetic acid (IAA)-like substances from gross extracts of tissues and feces of L. terrestris. These substances stimulated rhizogenesis and enhanced root growth of Phaseolus vulgaris (common beans) in a manner very similar to that of IAA. Graff and Makeschin (1980) tested the effects of substances produced by L. terrestris, A. caliginosa, and E. fetida on the dry matter production of ryegrass. They added liquid eluates from pots



26


containing earthworms to pots containing no earthworms and concluded that PGI substances were released into the soil by all three species, but the authors did not speculate further on the nature of these substances. Earthworms may liberate PGRs or PGIs themselves (Atlavinyte and Daciulyte 1969; El Harti et al. 2001a,b), or their production may be mediated by interactions with microorganisms in the drilosphere in a process that is not fully understood. It is clear that microorganisms are capable of producing PGR and PGI substances such as hormones, auxins, gibberellins, cytokinins, ethylene, and abscisic acid (Arshad and Frankenberger 1993; Frankenberger and Arshad 1995). Many microorganisms commonly found in the rhizosphere can produce PGR substances. Krishnamoorthy and Vajranabhaiah (1986) showed, in field experiments involving large earthworm populations, that seven species of earthworms could promote the production of cytokinins and auxins in soils. They also demonstrated significant positive correlations (r = 0.97) between earthworm populations and the levels of cytokinins and auxins present in ten different field soils and concluded that earthworm activity was linked strongly with PGR production. They reported that auxins and cytokinins produced through earthworm activity could persist in soils for up to 10 weeks although degraded in a few days if exposed to sunlight. For a more in-depth discussion of the role of earthworms in producing PGR substances through promoting populations and activity of microorganisms, see Chapter 18 this volume.

4. ROOT ABRASION

AND INGESTION OF

LIVING PLANT PARTS

BY

EARTHWORMS

Because earthworms burrow and cast near or within the rhizosphere, the soil disturbance and abrasion may affect plant roots negatively, particularly the small, fine roots or the root tips, which have not yet produced a protective cortex and are more susceptible to physical disturbance. This abrasion may also break up the mycorrhizal hyphal network (mechanism 1), decreasing root colonization and the many potential benefits of these fungi to plants. Several authors have reported damage by earthworms to rice crops in Southeast Asia (Stephenson 1930; Otanes and Sison 1947; Chen and Liu 1963; Inoue and Kondo 1962, cited in Lee 1985; Pradhan 1986; Barrion and Litsinger 1996), which may be caused by root abrasion if the earthworm population is large, although other factors such as excessive casting on the rice tillers, soil loosening, water drainage, and increased water turbidity have been proposed as the main factors responsible for the damage (Kale et al. 1989; Stevens and Warren 2000). Some authors have proposed that earthworms (mainly lumbricid species) can feed on living plant roots (Stephenson 1930; Carpenter 1985; Baylis et al. 1986; Sackville-Hamilton and Cherret 1991; Cortez and Bouché 1992; Gunn and Cherrett 1993; Hameed et al. 1993), although only in a few instances was this associated with decreased plant productivity. This phenomenon does not seem to be widespread because studies on the crop, gizzard, or gut contents of over 30 earthworm species revealed that roots form a very minor component of the ingested materials in most species (see Brown et al. 1999). The extent of root feeding by earthworms, the identification of the species involved, the conditions encouraging this to happen, and its possible damage to plant productivity still need further evaluation. Other negative effects, probably mostly caused by anecic earthworm species, involve the burial of living plant leaves (Darwin 1881; Zicsi 1954) or damage to germinating seedlings (Walton 1928; Olson 1929; Trifonov 1957; Patel and Patel 1959; Lee 1985; Shumway and Koide 1994). For instance, Darwin (1881) noted that the end of a Triticum repens leaf, still attached to the plant, had been pulled into the burrow of an anecic earthworm species and had dried and turned dark brown; although the rest of the leaf remained fresh and green. He attributed this to the fluids secreted by the earthworm mouth, which rapidly stained the plant tissues, causing cortical cell discoloration and disintegration. Edwards and Bohlen (1996) reported that L. terrestris destroyed a large part of a lettuce crop when soil containing large numbers of the earthworms was taken into a greenhouse. © 2004 by CRC Press LLC



27

Summarizing the available results on earthworms as pests of crops, Lee (1985) and Edwards and Bohlen (1996) stated that, although earthworms occasionally damage healthy plants, more commonly they attack very tender or moribund plants already damaged by some other mechanism, and that there is no reason to regard earthworms as serious pests of plants. However, there are clearly some instances when earthworms can damage plants either directly or indirectly (Edwards and Bohlen, 1996; Brown et al. 1999). Care should be taken to prevent these situations from occurring whenever possible.

5. INTERACTIONS

OF

EARTHWORMS

WITH

SEEDS

From the moment a seed germinates, it comes into contact with the soil, a physicochemical environment and a wide range of soil organisms, all of which may have variable degrees of influence on its growth and success as a plant. Moreover, even before a seed germinates, some of these factors may already be influencing its fate. For example, some earthworm species (e.g., L. terrestris) appear to show a preference for ingesting the seeds of certain plant species, depending on their size, shape, texture, and taste (Piearce et al. 1994; Shumway and Koide 1994). Observations made more than a century ago by Hensen (1877) and Darwin (1881) demonstrated the potential importance of surface-feeding anecic and endogeic earthworms in ingesting, transporting, and distributing seeds in the soil. Moreover, seed germination may be slower or more rapid in egested earthworm castings than in surrounding soils (McRill 1974; Atlavinyté and Zimkuviene 1985; Piearce et al. 1994). For example, Grant (1983) and Decaëns et al. (2001) observed lower germination rates and slower germination of the seeds of several weed species in earthworm casts. Furthermore, many seeds are damaged by passage through the earthworm gut, often affecting their germination success or vigor (Grant 1983). In view of the selective consumption and the digestive processes of earthworms, the preferential germination of different seed species in earthworm-linked structures, the dispersal of seeds through the soil, and the physical-chemical effects of earthworms on the soil environment, it has been suggested that earthworms may influence plant recruitment and the composition of plant communities considerably (Piearce et al. 1994; Willems and Huijsmans 1994). Some authors have suggested that earthworms seem to favor the proportion, and often biomass, of clover in pastures (Stebler et al. 1904; Bates 1933; Hopp and Slater 1948; Nielson 1953; Satchell 1955; Thompson et al. 1994; Nuutinen et al. 1998). Positive associations of earthworm casts with the frequency and distribution of the weeds Plantago spp., Trifolium, and Ranunculus were also observed in meadows in the U.K. (Bates 1933; Piearce et al. 1994). The effect of earthworms on the soil weed seed bank, particularly the influence of anecic species that preferentially ingest seeds, should not be underrated. Decäens et al. (2001) estimated that 1 to 13% of the total germinatable soil seed bank of a native savanna and two pastures were deposited in the surface casts of the anecic earthworm species Martiodrilus carimaguensis from the Colombian Eastern Plains. However, if there is preferential ingestion of weed seeds and differential growth of weed seedlings in earthworm casts or earthworm-worked soils (Piearce et al. 1994), this may eventually increase the level of weed infestations of crop fields or grasslands, potentially increasing competition of weeds with the crops or desired plants (Edwards and Bohlen 1996; Stinner et al. 1997).

6. CHANGES

IN

SOIL STRUCTURE CAUSED

BY

EARTHWORMS

The activities of earthworms in the physical “engineering” of soils can modify a wide range of chemical and biological properties and processes influenced by soil structure (see Chapters 10 and 11 this volume). Earthworm pedoturbation of soils can change soil structure by affecting aggregation (mostly by casting) and porosity to water and air (by burrowing and casting), thereby affecting soil physical functions important in root growth and penetration, such as aeration, gaseous exchange, water infiltration. and water-holding capacity (Figure 2.5). Earthworm burrowing creates mostly macropores (pores larger than 30 µm), and casting affects mainly the meso- and microporosity in



28


Earthworms Casting Micropores < 0.2 µm

Burrowing

Mesopores 0.2 to 30 µm

Water-holding capacity

Macropores >30 µm

Infiltrability, aeration

Soil structure (pore size distribution and aggregate stability)

Soil physical functions

Root penetration and growth FIGURE 2.5 Diagrammatic representation of ways by which earthworms can affect plant growth via physical changes in the soil environment by burrowing and casting. (Expanded from Syers and Springett, 1983.)

soils (pores smaller than 30 µm) and the stability of soil aggregates. However, earthworm species differ greatly in their ability to modify soil structure, depending on their ecological strategies and behavior. Plants also differ tremendously in their nutrient and water requirements and rooting strategies. The minimum pore size for effective penetration of the roots of most crop species is approximately 200 µm (Wiersum 1957), so many roots become concentrated in macropores, although some root hairs may penetrate mesopores 5 to 20 µm wide (Hofer 1996). Earthworm Casts Earthworms produce basically four types of casts (Lee 1985; Lavelle 1988; Edwards and Bohlen 1996): 1. Globular, consisting of coalescent round or flattened units, generally produced by the larger earthworm species (anecic and endogeic species). 2. Pastelike slurries, mainly produced by endogeic or anecic species and excreted as single masses of soil without a distinct shape, but that take on irregular shapes once dried. 3. Tall vertical heaps or columns of variable shapes, usually deposited on the soil surface where they are most visible by endogeic or anecic species. These are usually created by the sequential deposition of globular casts and, when in tower form, often have a hole in the middle (Darwin 1881; Edwards and Bohlen 1996). 4. Granular, typically in the form of pellets, produced mainly by smaller earthworm species (epigeic, small endogeic, and some anecic species) and distributed on or beneath the soil surface. Casts from different earthworm species can have very different effects on soil structure. The first three types of casts tend to be larger, heavier, and more compact and are usually produced by “compacting” earthworm species; the granular casts are normally smaller, lighter, and looser and break down more easily, and are mostly produced by “decompacting” earthworm species (Blanchart et al. 1997, 1999). Often, the casts of compacting species are consumed by decompacting species, a process that breaks up the larger aggregates into smaller ones, helping regulate overall soil aggregation (Blanchart et al. 1997; Decäens and Rossi 2001) and liberate nutrients that were protected in the casts for plant roots (see Figure 2.6).




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FIGURE 2.6 Pasture root growth into burrows and casting of earthworms from native savannas and pastures planted on highly weathered soils of the Colombian Eastern Plains. Note the two different types of structures: globular “compact” castings created by M. carimaguensis and their breakdown by smaller polyhumic endogeic “decompacting” earthworm species and mesofauna. (Photo P. Lavelle.)

The inner porosity of earthworm casts is also very variable depending on the earthworm species producing them, particularly the earthworm’s anterior and posterior internal morphology and musculature (Lapied and Rossi 2000). A predominance of mesopores (10 to 20 µm) was reported in the casts of M. anomala (Blanchart et al. 1999), whereas pores in the casts of the compacting species P. corethrurus were all smaller than 1 µm (Chauvel et al. 1997). Thus, casts are much more important for retaining plant-available water (fresh casts of many species have water contents above 70%) (Blanchart et al. 1999) and nutrients, whereas earthworm burrows are more important for water by-pass flow, infiltration rates, gaseous exchanges, and root penetration and elongation. Subsequently, several authors (Doube et al. 1997; Stockdill 1966; van Rhee 1969) reported increased water use efficiency by crops in soils inoculated with earthworms in both pot and field experiments. Earthworm casts, once they have undergone a stabilization process still not well understood (Edwards and Shipitalo 1998), become water-stable aggregates, although their stability is very dependent on the soil type, earthworm species, and earthworm feeding habits (Blanchart et al. 1999). Often, an important part (5% or more) of the surface (A) horizon of soils passes annually through earthworm intestines, particularly in tropical regions that are dominated by endogeic species (Lavelle 1988). Under some circumstances, most of the topsoil may be composed of earthworm castings of different ages, sometimes remaining long after the earthworms have disappeared (Buntley and Papendick 1960; Graff 1971b; Pop and Postolache 1987; Lavelle 1988). Thus, because interaggregate spaces are important in soil macroporosity, the physical arrangements of casts, particularly the larger casts containing mostly water-stable macroaggregates (>2 mm diameter), can also have an important effect © 2004 by CRC Press LLC


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on the total number of macropores in soils (see Chapter 10 this volume). Furthermore, casting on the soil surface may open new pores in the soil and can even break surface crusts, thereby helping germinating seedlings reach the soil surface (Kladivko et al. 1986). Compacted soils may also benefit from the activity of decompacting earthworm species (Blanchart et al. 1997, 1999), the incorporation of OM (aggregating agent) by anecic species, and the burrowing strength and stable aggregate formation by endogeic species (Zund et al. 1997; Larink and Schrader 2000). For example, the introduction of various endogeic and deeper-burrowing anecic species of lumbricid earthworms into New Zealand pastures aided the rates of decomposition of accumulated thatch and physical incorporation of lime, fertilizers, and pesticides into the soil, reducing physical, chemical, and biological limitations to root growth and pasture productivity (Stockdill 1982; Springett 1985). However, excessively loose soils or soils with greater proportions of sand that are prone to water stress, may actually benefit from the aggregating action of compacting earthworms. Not all the effects of earthworms on soil structure help plants to grow better. First, the deposition of fresh earthworm casts on the soil surface and the burial of protective surface litter by anecic earthworm species can expose soil particles to splash erosion ( Darwin 1881; Sharpley and Syers 1976; Sharpley et al. 1979; van Hoof 1983; Binet and Le Bayon 1999), promoting their downhill soil movement if the area is sloping. In particular situations and over long time periods, this could reduce the topsoil layer upslope considerably and increase its downslope, as well as change its texture (Nooren et al. 1995) and suitability for plants. In addition, when soils are prone to compaction and a single earthworm species of the compacting type dominates the community, reaching large populations, biomass, and activity levels, the ultimate effect of the earthworms on plant growth may be negative. Hence, Puttarudriah and Shivashankara-Sastry (1961), Blackemore (1994), Barros et al. (1996, 1998), Chauvel et al. (1999) and Ester and Rozen (2002) all observed increased soil compaction and “clodding” caused by earthworm (P. corethrurus and various other species) activities and related the lower soil porosity and water infiltration rates that occurred with decreased plant (radish, carrot, bean, pasture, sorghum, and potato) productivity. Excessive casting on the soil surface and base of plants by lumbricid earthworms in England caused difficulties in harvesting cereals and hay (Stephenson 1957; Edwards and Bohlen 1996), and large amounts of casts on the soil surface of grazed pastures led to “poaching” from cattle trampling, decreasing grass growth in the Netherlands (Hoogerkamp 1984) and New Zealand (Lee 1959). Earthworm Burrows Macropores usually represent only a very small part of the total soil porosity (particularly in clayey soils), yet they are very important in hydraulic conductivity and water infiltration rates when connected with the soil surface and in increasing aeration (Kretzschmar 1998, see Chapter 11, this volume). The positive effects of earthworms on water infiltration may help decrease runoff rates (Roth and Joschko 1991), thereby allowing more water to enter the soil and reducing overall erosion (Hopp 1946, 1973; Sharpley et al. 1979), as well as increasing the potential for water storage in the soil. Thus, the effect of earthworms on soil porosity and infiltration, as well as on organic matter breakdown, has been associated consistently with increased yields in New Zealand pastures (Stockdill 1959, 1982) and reclaimed Dutch polders (e.g., van de Westeringh 1972; Hoogerkamp 1984) and with greater hay and bean yields in large container experiments (Hopp and Slater 1948, 1949), although the interactions with incorporated or surface OM (another aggregating agent) are also likely to be implicated (Cogle et al. 1994) in some responses observed by these authors. Earthworm burrows can serve as preferential pathways for root elongation (Ehlers 1975; Edwards and Lofty 1980; Kirkham 1981; Ehlers et al. 1983; Wang et al. 1986; Kladivko and Timmenga 1990; Hirth et al. 1997; Jiménez 1999), especially in compacted zones found typically in deeper soil layers. In open, abandoned earthworm burrows, the greater aeration and the small © 2004 by CRC Press LLC



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amounts of nutrients associated with the earthworm burrow walls can benefit root growth (Graff 1971a), and cast-filled earthworm burrows usually have large quantities of plant-available nutrients stored in the casts (mechanism 7). The distribution of roots in soil is often related closely to the zones of earthworm activity (Edwards and Lofty 1978, 1980), and root densities can be increased significantly by earthworm activities. In newly reclaimed polders inoculated with earthworms and planted with fruit trees in the Netherlands, van Rhee (1977) reported significantly greater root densities in the earthworm-inoculated sites but no effects on fruit production. Conversely, in a pot experiment in Mexico that compared pots inoculated with earthworms those with no earthworms, Brown (1999) observed significantly greater root densities, as well as more root and shoot biomass, but no increase in productivity of beans in the presence of Polypheretima elongata. The earthworm burrows were commonly filled with roots, and the root distribution throughout these pots showed a much more even (homogeneous) distribution, a factor considered to confer greater plant resistance to environmental stresses (Smucker 1993). The proportion of roots found in deep earthworm burrows (e.g., in the B horizons) compared with those in the soil matrix can be very high (Kirkham 1981; Logsdon and Linden 1992), and these roots may be important in maintaining plant water dynamics. However, estimates of the proportion of roots in earthworm burrows may be exaggerated because roots in earthworm burrows are more easily observed, whereas the rest of the root system may be concealed in the soil matrix (Logsdon and Linden 1992; Kretzschmar 1998). A three-dimensional estimation of interactions between roots and earthworm burrows is still not available (Kretzschmar 1998), and considerable efforts need to be made to understand these interactions and the mechanisms that control them (Tisdall and McKenzie 1995). Thus, it is a combination of the composition (ecological category, species) of the earthworm community present at a given location, the placement of their casts (surface, belowground, deep in soil, near roots, etc.), the quantities of casts deposited and their age, and the amount, type, depth, and openness of the earthworm burrows produced, the interaction of microorganisms with earthworm structures, the physicochemical soil environment, and land management that determine the ultimate effects of earthworms on soil structure and the rooting environment.

7. CHANGES IN NUTRIENT SPATIOTEMPORAL AVAILABILITY CAUSED BY EARTHWORMS The availability of many essential plant nutrients has been shown to increase in structures produced by various earthworm species, especially in their casts (e.g., Mulongoy and Bedoret 1989; Barois et al. 1999) and burrow walls. This greater nutrient availability is mainly a result of the selective feeding of earthworms on regions of the soil rich in organic matter, clay, and nutrients (Barois et al. 1999; Cortez and Hameed 2001), gut-associated processes, and cast-associated processes (Figure 2.7), together with some earthworm burrow-associated processes (especially with anecic earthworm species; Devliegher and Verstraete 1997; Brussaard 1999). Such processes include the grinding action of the gizzard, the priming of microbial activity in the gut, and the greater populations and activity of microorganisms in the earthworm casts and burrows (Figure 2.7), that induce chemical changes in earthworm-worked soil (e.g., Lee 1985; Edwards and Bohlen 1996). These nutrient enrichment processes (Devliegher and Verstraete 1995; Brussaard 1999) differ greatly according to the earthworm species involved, their ecological categories, and the feeding habits, particularly the amounts of plant litter they ingest. The type and placement of the earthworm casts are also important, affecting the spatiotemporal availability of the nutrients they contain (Figure 2.7). Surface earthworm casts dry out much more quickly, harden, and, if compact, are likely to limit root penetration, thereby reducing the ability of plant roots to obtain the nutrients stored inside the casts (nutrient protection) until they are broken down (Figure 2.6 and Figure 2.7). Belowground earthworm casts remain fresh and moist for much longer periods of time and, if they are of the decompact types (with more meso- and macropores and macroaggregates), allow roots to penetrate more easily (Figure 2.6) and profit from the greater nutrient contents available to plants. © 2004 by CRC Press LLC


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Mineral soil + OM (food) inputs

Physical breakdown

comminution

(Bio)chemical breakdown

Mucus, enzyme production, pH changes

Fresh casts Compact

Decompact

Aging casts Nutrient “protection”

Breakdown

GAPs (grinding in gizzard, microbial activity)

CAPs (microbial activity and soil chemical changes)

Nutrient release

Plant nutrient spatiotemporal availability

Root growth and development FIGURE 2.7 Diagrammatic representation of ways by which earthworms can positively affect plant growth via chemical changes in the soil environment induced by gut-associated processes (GAPs) and cast-associated processes (CAPs).

Most of the reported increases in uptake of nutrients (especially N and P) by plants in response to earthworms has been related to increased P and N mineralization rates and their availability in castings, earthworm burrow linings, and earthworm-worked soils (e.g., Graff 1967; 1970; Aldag and Graff 1975; Lee 1985; Lavelle et al. 1992; López-Hernández et al. 1993; Brossard et al. 1995; Chapuis-Lardy et al. 1998; Barois et al. 1999; Rangel et al. 1999). This is particularly important because N and P are commonly the most limiting nutrients in soils for optimum plant productivity. Because cast production rates can reach large quantities, ranging from a few tonnes per hectare in temperate arable land up to more than 1000 t ha−1 in tropical savannas with a predominance of geophagous endogeic earthworm species (Lavelle 1988), the amount of nutrients cycled and made available to plants by earthworm activity can be enormous, ranging from a few up to several hundred kilograms of mineral N per hectare and tens of kilograms per hectare of plant-available P (Lee 1985, Hauser 1993). Because of the enhanced rates of nutrient release and availability in the drilosphere, plants grown in the presence of earthworms often have more nutrients, particularly N and P (e.g., Atlavinyte and Vanagas 1982; McColl 1982; Graff and Makeschin 1983; Spain et al. 1992; Blakemore 1994; Baker et al. 1997; Stephens et al. 1994a; Tomati et al. 1996, etc.). Greater availability and rates of




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uptake of nutrients by plants in response to earthworm activity have often led to greater transfer of C and N from soils to shoots and more shoot biomass relative to that of roots (Wolters and Stickan 1991; Klebsch et al. 1995). The actual benefits derived by the plants from earthworms depend on the ability of the plant to extract these nutrients from the drilosphere and the soil solution. If nutrients are released and made available to plants during drier or colder periods when plants are dormant or not growing as actively or when the field is bare, then they may be lost (e.g., by leaching) and will provide very few benefits to the plants. Thus, the synchrony of nutrient availability (especially N) with the needs of the plants is critical, and earthworms may play an important role in this process (Fragoso et al. 1997). The increased amounts of plant-available nutrients in earthworm casts and burrows can promote root growth considerably (Darwin 1881; Ehlers 1975; Spiers et al. 1986; see Figure 2.6), and their importance to plant nutrition increases proportionally to the differences in nutrient status between the earthworm casts the surrounding soils, the quantities of casts produced and their synchronization and synlocalization with root growth needs. Thus, in deeper and possibly poorer soil zones, earthworm casts and burrows may serve as hot spots of nutrient availability to plant roots (Mouat and Keogh 1987) and promote fine root growth. Conversely, when the plants are growing in nutrientrich soils, the relative nutrient bioavailability stimulation in response to earthworm activities may be less than in poor soils, and expected plant growth increases may also be less (e.g., Atlavinyte and Vanagas 1973; Brown et al. 1999; Buse 1990; Doube et al. 1997) because the plants can obtain most of their required nutrients without the earthworms. Many experiments have demonstrated the importance of plant-available nutrients and PGR substances in earthworm casts to plant responses (e.g., Dash and Das 1989; Kang and Ojo 1996; Kang et al. 1994; Nijhawan and Kanwar 1952; Reddy et al. 1994; Tomati et al. 1987; Norgrove and Hauser 1999; Kollmannsperger 1980). The plant response is usually proportional and related positively to the quantity of earthworm casts applied or to the ratio of casts to soil or other substrates used. However, experiments of this nature have the disadvantage of unrealistic experimental conditions compared with the field and the vastly different chemical, physical, and biological properties of the casts, depending on their source and age. The effects of earthworms on nutrient mineralization are especially evident in sites newly invaded by earthworms. For example, lumbricid or pheretimoid earthworm invasions into the forests of North America have sometimes resulted in dramatic changes in the chemical status of soil, transforming humus types from mor to mull (Langmaid 1964; Nielson and Hole 1964; see Chapter 5 this volume). Corresponding C and N losses and increased nutrient turnover rates resulting from earthworm invasion of new sites may be on the order tens to hundreds of kilograms per hectare (O’Brien and Stout 1978; Alban and Berry 1994; Scheu and Parkinson 1994a; Burtelow et al. 1998). Some plants may benefit from the increased amounts of available nutrients (Scheu and Parkinson 1994b), but in general little is known of the effect of such large nutrient fluxes on overall plant growth and their potential effects on plant communities (e.g., species composition and biodiversity). Eutrophic and opportunistic plants may profit preferentially from earthworm presence during the nutrient release phase (which may last several years) until a new “equilibrium” is reached, when the lower total nutrient stocks and more rapid rates of turnover may exert relatively larger and different selection pressures on the plant communities present. Litter burial, ingestion, and digestion by earthworms, particularly anecic and epigeic earthworm species, accelerates rates of decomposition, whereas endogeic earthworm species tend to promote mineralization of the particular light and coarse organic matter fractions in soils (McCartney et al. 1997; Lavelle et al. 1998; Parmelee et al. 1998). Thus, the incorporation of organic matter by an anecic earthworm species such as M. carimaguensis in the savannas of Colombia has been associated with reduced Al saturation (through binding with organic matter) and reduced Al limitation to grass growth (Decaëns et al. 1999). In New Zealand pastures, earthworms have been shown to accelerate the incorporation of lime, fertilizers, and insecticides such as DDT (for grass grub control) (Stockdill 1966, 1982; MacKay et al. 1982; Springett 1985), thereby promoting grass productivity. © 2004 by CRC Press LLC


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The soil-mixing activities of earthworms have been shown to promote the recovery of N and P from organic residues, inorganic fertilizers, and rock phosphate in various pot and field trials using the plant species B. decumbens, Panicum maximum, ryegrass, and maize (MacKay et al. 1982; Mansell et al. 1981; Spain et al. 1992; Hameed et al. 1993, 1994a,b; Hu and Wu 1994; GilotVillenave et al. 1996; G.G. Brown et al. 2000; Cortez et al. 2000). However, earthworm activities can also sometimes lead to decreases in the availability of nutrients to plant roots. Fresh earthworm casts rich in nutrients (especially N and P) that are deposited on the soil surface may be eroded easily and are also hot spots of denitrification and NH3 volatilization (Elliott et al. 1990; Lensi et al. 1992; Karsten and Drake 1997). Furthermore, earthworm burrows, especially those of anecic species, connected to the soil surface may promote water bypass or mass flow, causing increased leaching of soluble nutrients (Anderson et al. 1983; Hoogerkamp 1984; Knight et al. 1989; Haimi and Boucelham 1991; Edwards and Shipitalo 1998). Nutrients from Earthworms (Death, Excretion) Some authors have proposed that most N excretions and mucus secretions from earthworms may be utilized rapidly by plants (e.g., Bouché and Ferrière 1986; Bouché et al. 1987; Hameed et al. 1994a,b; Whalen et al. 1999, 2000). However, this contribution is probably not very large unless the earthworm biomass is high and most of their activities are concentrated in the root zone. Further field research on this topic, particularly using homogeneously labeled (15N, 32P) earthworms, is needed. The release of nutrients from dead earthworm tissues has often been believed to play important role in plant productivity (Russell 1910; Satchell 1958; Barley 1961; Callaham and Hendrix 1998; Whalen et al. 1999). However, although visual observations show that earthworm bodies decompose very rapidly in soil, only a few reports have been published on the quantities of nutrients made available from dead earthworm biomass (e.g., Satchell 1967; Christensen 1988; Martin 1990; Whalen et al. 1999; Hodge et al. 2000). Furthermore, earthworm biomass is probably an important and significant source of plant nutrients only in field and pot experiments, in which the inoculation rates of earthworm biomass into soils is very high and when earthworm mortality or turnover rates are high. For instance, the small soil volumes often used in pot experiments may be insufficient to maintain earthworm populations inoculated into them to levels above the carrying capacity of the soil. Under such conditions, many earthworms may die, liberating nutrients that, although in small amounts relative to typical soil nutrient supplies, are enough to influence plant growth because of the low soil:earthworm biomass ratio. This has occurred in many experiments, even in those that based the rates of addition of earthworms to field populations but not to field biomass, thus adding greater biomass than would normally occur in the field (e.g., Satchell 1958; Doube et al. 1994c; Baker et al. 1996, 1997; Callaham and Hendrix 1998; Whalen et al. 1999). When larger soil volumes were used, or more realistic earthworm populations and biomass were added, nutrients from dead earthworms played a much smaller role in plant nutrition. This is probably the case even in field situations with large earthworm biomass turnovers of up to 600 kg ha−1 year−1 (fresh mass), which nevertheless can supply only a few kilograms per hectare per year of mineral N from decomposing earthworm tissues (Brown et al., unpublished data).

CRAWLING FORWARD: THE CHALLENGE OF IDENTIFYING AND QUANTIFYING THE POTENTIAL OF EARTHWORMS TO INCREASE PLANT GROWTH It is clear that a wide range of direct and indirect mechanisms of earthworm activities on plant growth can be identified. However, to benefit from the potential of plant growth stimulation by earthworms, promotion and decrease mechanisms in plant growth and their modes of action must be understood within a given practical soil-plant-earthworm species and population context. There




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are many possible combinations of soil types and associated plant and earthworm species. Because several PGI mechanisms may be operating simultaneously, identifying the most important modes of action on the plant in a given situation is a difficult task. However, there are guiding principles that can be followed to help predict potential benefits of earthworm activities to plant growth and identify some of the mechanisms involved.

“ALL-MINUS-ONE” TESTS

AND

FIELD TRIALS

First, existing limitations to plant growth in a given site, situation, soil type, and abiotic and biotic environmental conditions should be assessed and classified hiearchically. Then, the potential of earthworms to ameliorate any of the limiting factors must be evaluated. Such potentials can be assessed using pot and laboratory methodologies, not necessarily including plants. To be able to deal adequately with the multiple limiting factors, commonly present under field conditions, and identify the interactions between the limiting factors and effects of earthworms on the soil and plants, a series of “all-minus-one” trials could be designed in a greenhouse. In such experiments, all the environmental, nutrient, and physical requirements would be provided to the plant except one. Each requirement can then be altered to test how earthworms affect it and to determine any associated plant responses. Such experiments could begin with proper identification of all the soil-associated chemical limitations to plant growth, which can be assessed by soil analyses, plant analyses, and limitingnutrient pot experiments. Fertilization with all but one nutrient and inclusion or exclusion of earthworms could permit the assessment of the role of earthworms in facilitating nutrient availability and uptake by the plants. Soil sterilization and inoculation with a range of different microorganisms is also possible to help assess the role of their interactions with earthworms on plant productivity, but this could be time consuming and laborious. In shorter-term experiments, the physical effects of earthworms on soil studies are probably less important than the chemical and biological effects, although as the length of the experimental periods increase, physical effects (especially limitations when only one earthworm species is included) may become more important. To separate the chemical, physical, and biological mechanisms, simultaneous experiments using different methodologies and experimental designs, such as pots with and without earthworms and pots with soil previously processed by earthworms and various other treatment combinations (e.g., ± residues, ± fertilizers, ± sterilized or unsterilized), or with one or more earthworm species in combination could be developed. The approaches described are far from ideal because some interactions may occur when only a single factor is manipulated, and such experiments do not take into account the complementary or adverse roles of other organisms present in soils. Furthermore, such an experimental design will require a very large number of replicates and treatments, making it very complex and somewhat impractical. Therefore, experiments should be mainly in the field, while recognizing both their drawbacks and benefits (Brown et al. 1999). In field experiments, a great many more variables, many of them uncontrollable, can occur, although the results obtained should be much more realistic and useful to practicing farmers, foresters, or other environmental managers. In such instances, proper assessment of the soil physical limitations to plant growth is essential because, under such conditions, physical effects of earthworms on soils may be of much greater importance (Alegre et al. 1996; Barros 1999). Obviously, the characterization of changes in earthworm communities by periodic population sampling, the quantification of earthworm casting and burrowing activities (e.g., by physical description of soil cores or x-ray commuted tomography), and their chemical and biological analyses are important to assess the extent of earthworm changes to soil structure, biology, and fertility. In such studies, controls (without introduced or native earthworms) must be used and maintained, and if earthworms are to be introduced to them, realistic biomass, populations, and species assemblages should be used.



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THE EARTHWORM THRESHOLD CONCEPT Probably the most important effects of earthworms on crop yields will occur when earthworms are able to significantly modify factors that also happen to be those most limiting to plant growth. Almost all the soil physical, biological, and chemical needs of plants can become limiting when they fall below a certain lower threshold or become excessively above it. The range between these two thresholds is the zone ideal for plant growth. Hence, possible effects of earthworms on plants can be regulated by their ability to increase some of these factors that are limiting plant growth above the lower thresholds and decrease factors adverse to growth below the upper thresholds. The combination of effects of the drilosphere and the threshold level at which each of the biological, chemical, or physical factors are limiting plant growth will ultimately determine the effects of earthworm activities on the plants. For example, if a population of a parasitic nematode or an infestation by a particular fungal or bacterial pathogen has reached disease proportions and become a primary limiting factor in plant production, and if earthworms are able to reduce the population, it seems likely that this would be a dominant mechanism influencing plant growth, although other factors, such as the influence of earthworms on soil structure and fertility and biological interactions with soil microorganisms and invertebrates, will also be important and operate simultaneously. Similarly, if availability of N or P are limiting factors, earthworm-induced increases in the availability of the nutrients or changes in the mycorrhizal colonization of roots may become important controlling mechanisms. Finally, if soils are compacted or prone to compaction and associated hydrological limitations are complicating plant growth, earthworm bioturbation and associated soil structural changes may be the most important mechanisms that enhance plant productivity.

FUTURE NEEDS

IN

EARTHWORM RESEARCH

An ultimate goal in the process of assessing the potential effects of earthworms on plant productivity would be the development of effective simulation models in which the soil environmental constraints are matched with the earthworm and plant species (or communities) present at a site to predict any potential direct and indirect influences of earthworm activities on soil physical, chemical, and biological limitations and plant productivity. Unfortunately, there are still many gaps in knowledge of these processes that need to be filled to be able to develop such models and predict accurately whether a particular earthworm species, population, or community will enhance or suppress plant productivity. Thus, future research should strive to use more holistic approaches using detailed experiments that address potential mechanisms individually as well as in combination, but do not attempt to “kill all birds with one stone.” On the positive side, the study of increased production of PGR substances; promotion of beneficial rhizobacteria; reductions in plant pests, pathogens, or parasites; the interactions of earthworms with plant seeds; and the potential attraction of earthworms to roots and of roots to earthworm structures such as casts deserve more attention. On the negative side, the assessment of plant growth suppression by direct and indirect effects of earthworms also requires more research to verify any potential incompatibilities between existing earthworm communities and established plant species and populations, soils, cropping systems, and crops. There may be situations for which it is better to plant gramineous plant species rather than legumes or vegetables (Puttarudriah and Sastry, 1961) or to manage the soil in a way to decrease potentially negative effects of earthworm activity on plant production. Finally, many earthworm species with potential benefits for plant growth have never been studied experimentally and deserve more attention. Further studies should focus especially on the potential benefits of earthworms to plant productivity in crop fields, pastures, and managed forests, where site-specific management practices and technological innovations (e.g., precision agriculture) could be used to manage the earthworm community for the benefit of plant growth.




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ACKNOWLEDGMENTS We would like to thank the Instituto de Ecología, A.C., IRD and CNPg-Prefix for their support during the writing of this chapter. We also thank the many colleagues who provided insightful ideas and comments for its development.

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Part II Earthworm Taxonomy, Diversity, and Biogeography


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Processes and Their 3 Planetary Interactions with Earthworm Distributions and Ecology Samuel W. James Department of Life Sciences, Maharishi University of Management, Fairfield, Iowa, U.S.A.

CONTENTS Plate Tectonics and Earthworm Phylogeny .....................................................................................54 Applications of Earthworm Biogeography to the Earth’s History .................................................56 How the Earth’s History Affects Earthworm Distributions ............................................................58 References ........................................................................................................................................61

Studies of the history of earth are traditionally the domain of geologists and those in various paleodisciplines (paleontology, paleoecology, paleoclimatology, paleobotany, etc.). However, the history of biology has many examples of research into the connections between present-day biogeography and ecology on the one hand and earth history on the other. Such research may be considered in three broad categories. First, there is application of data derived from life forms of the present to questions of earth history. For example, the use of phylogenetic trees in combination with distributional data can provide valuable insights into the history of land-area relationships, as in the field of vicariance biogeography, which studies processes that split distributions (vicariating events) in relation to phylogeny (Wiley 1988). It may be claimed that earthworms were of some importance in the early development of plate tectonic theory and, therefore, of vicariance biogeography, because the former discipline has been very important to the ascendance of the latter. Plate tectonics theory attempts to account for the movement of parts of the Earth’s crust and provides a means of recovering the ancient positions of those crustal pieces. The Oligochaete systematist Michaelsen (1933) named an earthworm genus after Wegener in honor of Wegener’s work toward understanding the distributions of earthworms. It is possible that the two men (who were office neighbors at the University of Hamburg) discussed earthworm distributions, providing Wegener with more evidence for his theory, which was radical at the time. Many other groups of organisms have been used in arguments supporting or refuting various hypotheses about the history of events (Rosen 1985; Humphries and Parenti 1999; Liebherr 1988). One can also find a significant thread of research to trace the contributions of living organisms to global processes. In its boldest version, this area is termed the Gaia hypothesis (Lovelock 1988), but numerous more mundane examples can be found in the literature on biogeochemical cycles, trace gas fluxes, and many other topics relevant to global climate models. For example, earthworms may influence landforms. Charles Darwin (1881) described a process by which earthworms could increase rates of soil erosion and thereby the rates of change of land 53 © 2004 by CRC Press LLC


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topography. This subject has not been thoroughly researched, and there is some evidence that suggests that earthworms may actually reduce rates of soil erosion (Hopp 1946; Sharpley and Syers 1977) in agricultural land. Nooren et al. (1995) suggested that earthworms could increase rates of clay loss from an African soil, thereby creating nutrient-poor sandy topsoils. Lavelle and Martin (1992) hypothesized that, by protecting soil organic matter from oxidation, earthworms could have an important influence on atmospheric carbon dioxide levels. Because rates of carbon loss from soils make an important contribution to the elevation of atmospheric carbon dioxide levels, any organism that is capable of contributing to reversing or moderating that trend should be investigated closely (see Chapter 10 this volume). A third way in which earth history can play a significant role in field biology is in the understanding of ecological interactions and of organism taxon distributions. For example, the presence of a particular taxon and its unique ecological contributions to the biological community of one site, but its absence from another, could be interpreted as caused by differences in history. Perhaps the taxon could have existed in the latter site but did not get there. Thus, it may not be some ecological or evolutionary necessity that determines certain characteristics of the system but instead a historical accident. This is an important distinction because some simplistic interpretations of community dynamics assume a long history of community optimization. It seems probable that nature has not tried all possible combinations but has instead relied on the interactions and evolution of what is present combined intermittently with unpredictable arrivals of new organisms to the site. An analogy can be seen in communities of earthworms in which most or all the species are introduced or exotic to a location. The organismal content of such communities is clearly accidental, and any further interpretation of that content assumes that other potential invaders (i.e., those species not currently present) have had an opportunity to invade, but only those ecologically compatible with the community qualities have succeeded. Of these three connections of earth history to modern biology, in terms of earthworms, I focus on two: the first and the last. These may be stated briefly as using modern organisms to learn more about the history of the Earth and viewing modern organismal distributions and ecology as the outcomes of an interaction between evolutionary and large-scale abiotic processes. My purpose in this chapter is to outline some of the ways that research into earthworm systematics and biogeography can contribute significantly to the broader subject of earth history and vice versa. As I develop these discussions, I suggest that researchers into earthworm systematics and biogeography can profit from close attention to some of the recent developments in organizing their ideas and analyzing their data.

PLATE TECTONICS AND EARTHWORM PHYLOGENY The first subject is mutual enrichment between geology and systematics, from either geological data informing on probable phylogeny or vice versa. An example of the first case is provided by ongoing debates about the higher-level classification of the Clitellata. The earliest application of earthworm systematics to earth history was in the connection with Wegener’s theory that continents move, which has since been transformed into plate tectonics theory. The vicariance events (splitting of land masses) are quite ancient, and the resulting taxonomic divisions within earthworms are generally at the family level, although some are within genera. Various family-level classifications have been superimposed on paleoreconstructions of the past 250 million years of crustal movements (Jamieson 1981; Bouché 1983; Omodeo 2000), but all those classification systems were contradicted by the results of Jamieson et al. (2002), who were the first to apply deoxyribonucleic acid data to studies of earthworm phylogeny (Figure 3.1). For instance, the Octochaetidae were shown to be polyphyletic, the various concepts of the Acanthodrilidae were paraphyletic, and the Crassiclitellata (earthworms as commonly understood minus the Moniligastridae) were clearly monophyletic.



*

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Glossoscolecidae

Eudrilidae

Microchaetidae

Lumbricidae

Hormogastridae

other Lumbricoidae

Ocnerodrilidae

Acanthodrilidae

Megascolecidae

Planetary Processes and Their Interactions with Earthworm Distributions and Ecology

other Clitellata

FIGURE 3.1 Simplified phylogenetic tree of major groups of earthworms. The node with the asterisk is the polytomy discussed in detail in the text. (After Jamieson et al. 2002.)

To provide an example with biogeographic relevance, the Glossoscolecidae (South America) are clearly a sister group of the Eudrilidae (Africa) rather than allied to the Microchaetidae (Africa), as presented by Bouché (1983) and Omodeo (1998). The Lumbricina of Omodeo and similar concepts of other groups emerged relatively intact but with significant modifications, particularly the possible inclusion of the Eudrilidae. This remains unclear because a probable trichotomy of Megascolecoidea (M), Lumbricoidea (L), and Glossoscolecidae plus Eudrilidae (G) was unresolved by Jamieson et al. (2002) and could be resolved in three different ways: (M, (L, G)); ((M, L),G); or ((M, G), L). Like Omodeo (2000), one could resort to paleogeography to support a phylogenetic theory, choosing the last of the three because this leaves the Gondwanan taxa sharing a more recent common ancestor than with the primarily Laurasian Lumbricoidea. However, this was not the conclusion reached by Omodeo (1998), who placed the Glossoscolecidae with the Lumbricoidea, nor is it consistent with the work of Bouché (1983), who placed the Glossoscolecidae with the Microchaetidae, Kynotidae, and Almidae as the Glossoscolecoidea, leaving the Eudrilidae with the Megascolecoidea. What is needed is to expand the taxon sampling (see Zwickl and Hillis 2002) of Jamieson et al. (2002) to include more Lumbricoidea, Glossoscolecidae, Ocnerdrilidae, and Eudrilidae to resolve the polytomy and to address more definitively Omodeo’s (1998) polyphyletic model of earthworm evolution. This should also include some species of Alluroididae, because that family is proposed as the source of two independent ancestors of major trunks of the Crassiclitellata tree (Omodeo 1998). Another problem is that some versions of the distribution of Lumbricoidea have members (the Microchaetidae) located in sub-Saharan Africa. Can this indicate that earthworms have a significant pre-Pangaea history, such that their biogeography can be understood only with reference to two cycles of continental fragmentation? Clearly, this issue cannot be settled until the proposed phylogeny can be stabilized, but some pre-Pangaea reconstructions link continental geologic units that are now far apart, such as northeastern North America and South Africa. Although geological models of earth evolution can provide some corroboration of phylogenetic hypotheses, the main burden of gathering evidence lies with biologists. I now consider the contributions of biological data to understanding geological events.



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APPLICATIONS OF EARTHWORM BIOGEOGRAPHY TO THE EARTH’S HISTORY There are good reasons to apply earthworm systematics and biogeography to the study of the geological history of the Earth, with particular reference to movements of the Earth’s crust. Such an idea began from two pieces of biogeographical data. First, earthworms (except anthropochorous peregrines) are absent from midoceanic volcanic islands (Gates 1969; Nakamura 1990; Talavera 1990) and uplifted carbonate platforms, indicating that earthworms may experience great difficulty crossing saltwater (Stephenson 1930). Second, there are endemic earthworm species on some oceanic islands. The possibility of over-water dispersal has been debated extensively in the past, particularly in relation to the endemic species of the subantarctic islands (Michaelsen 1911; Stephenson 1930; Lee 1959). There is an opportunity to test the hypothesis of no over-water dispersal of earthworms in a general way and to use it, if supported, to argue that earthworms are biogeographical model organisms. By the term model organism in this context, I mean an organism with dispersal that has been so poor that its distribution can be viewed as determined entirely by past land connections and vicariance events that introduced saltwater barriers between land areas. If earthworm transoceanic dispersal has been negligible in history, then earthworm phylogenies can be used to unlock many earth historical riddles, such as the geological evolution of complex areas like the Caribbean Basin (Maury et al. 1990; Pindell and Barrett 1990) and the archipelagoes of Southeast Asia (Hall 1996, 1998). This application of phylogeny to earth history follows from the simplest form of allopatric speciation. The biota of the separated areas will have evolutionary histories that mirror the fragmentation history of the land. However, postfragmentation dispersal muddles the land area cladogram that can be derived from the hypothesized phylogenetic tree of the organisms. Therefore, a low- or no-dispersal taxon is preferable to one able to cross the barrier (Noonan 1988; Sober 1988). In spite of this rather obvious conclusion, most of the work to date in the field of historical biogeography has focused on relatively vagile organisms, such as reptiles, birds, and insects. Biogeography can be considered under many formats, and it is useful to define which kinds of biogeography are concerned. Ball (1975) described three phases of the science of biogeography. The first is the empirical or descriptive phase, in which basic data are collected. At this point, it is known where the various taxa are located, and there may be some synthesis, such as the definition of the classical biogeographic provinces (e.g., Nearctic, Ethiopian). Then, an attempt is made to explain the distributions, and a narrative phase is the result. A plausible story is constructed, one that seems to fit the evidence fairly well. Work to date on the subject of oceanic island earthworm distributions has achieved this much, leaving room for an analytical approach. As mentioned earlier, it appears that earthworms have rarely or never crossed saltwater (other than the saltwater-tolerant species inhabiting seashores). This could lead to the statement of an hypothesis that earthworms cannot survive, or do not have natural means of, transport across bodies of saltwater. This is testable, although it would be difficult to release test earthworms or cocoons by all possible means of conveyance (rafting vegetation, logs, on debris in violent cyclonic storms, and so on) and even harder to track their fates. It may be easier to test the predictions of the hypothesis. The hypothesis that earthworms cannot survive natural means of transport across bodies of saltwater predicts that land areas arising from midoceanic uplift of submerged rock or from volcanic eruption should not have earthworms. Obviously, this hypothesis arose from the observation that such islands either lack earthworms or harbor only earthworms that have been distributed widely by human activity. It can be tested by examining islands conforming to the modes of origin just mentioned and that have earthworm fauna about which little or nothing is known. The Lesser Antilles fit this description. These islands constitute a fairly strong test because they are close to one another and to potential sources of colonization, unlike the Hawaiian archipelago and the © 2004 by CRC Press LLC



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islands of the Mid-Atlantic Ridge. There is ample evidence that other fauna have colonized the Lesser Antilles from South America and from the Greater Antilles and other islands to the north (Savage 1982; Roughgarden 1990; Humphries and Parenti 1999), so it would not be particularly surprising to find another group of organisms doing the same. Another region with many islands, a mix of geological histories, and partly known or unknown earthworm faunas is Southeast Asia. There, the possibility of dispersal of earthworms from the Australian region or East Asia into the extensive archipelagoes is found. The general pattern of distribution of earthworms in the Lesser Antilles has been presented elsewhere (Fragoso et al. 1995). No earthworms other than peregrine species were found in the southern Lesser Antilles or the small volcanic islands north of Guadeloupe. Many new species endemic to their islands were found on Guadeloupe, Dominica, Martinique, and St. Lucia (James, unpublished data). Based on the number of genera and morphologically homogeneous groups of species within genera, at least nine successful dispersal events would be required to establish the current earthworm fauna of those four islands. If so, this is a very dense cluster of dispersal events in the middle of the archipelago, farthest from sources of colonization. However, earthworms have failed to colonize the Lesser Antilles by over-water dispersal from nearby land masses populated with indigenous earthworms. There is no evidence that the South American earthworm fauna has spread northward into the Lesser Antilles, or that the elements of the earthworm fauna of the Greater Antilles, particularly Puerto Rico and the Virgin Islands, have dispersed to the east and south. The Guadeloupe–St. Lucia axis poses a challenge to the conclusions that otherwise could be reached easily from the data from other islands. Without recourse to an analytical approach, the challenge cannot be met because hypotheses of dispersal are logically unfalsifiable. Any distribution could arise by postfragmentation dispersal if sufficient complexity of dispersal history is allowed. In this case, progress will come only from testing the hypothesis that the distributions are the result of vicariance because it is logically conceivable that such a hypothesis could be rejected. If, for the time being, it can be accepted that over-water dispersal can be ignored as a factor in earthworm distribution to islands, or between any two land areas separated by saltwater, then earthworms provide nearly ideal indicators of past land-area connections. Their evolutionary history should mirror these past connections because a severing of the land connection isolates populations of species. From the perspective of vicariance biogeography, these isolating or vicariating events are the primary factors of interest in the history of the flora and fauna of land areas. Dispersal is seen as a source of noise in the data, analogous to homoplasious character evolution (Sober 1988). Vicariance biogeography represents a system of formulating hypotheses that predict organismal distribution patterns based on underlying historical models (Wiley 1988). The underlying historical models have to do with creation of barriers to genetic exchange. Any species, earthworms included, could be affected by the fragmentation of a range because of climatic, geologic, or other processes. Thus, it should be possible to make a very good map relating the branch points on an earthworm cladogram and the separations of the land masses on which earthworm taxa occur. In the jargon of vicariance biogeography, one replaces the terminal taxa on the phylogenetic tree with the names of collection locations to make an area cladogram. A geological model provides a predicted area cladogram, which can then be compared with a biologically derived one. The success of this approach depends heavily on a very good phylogenetic analysis, on having the data set that is as free as possible from dispersal-induced noise, and on a proper choice of area units. Hausdorf (2002) argued for the use of biotic elements, rather than the more traditional areas of endemism, as the units of biogeographical analysis. An area of endemism is a region characterized by a number of taxa unique to the area. Hausdorf defined a biotic element as “a group of taxa whose ranges are significantly more similar to each other than to those of taxa of other such groups.” The difficulty in defining areas of endemism arises from dispersal: “The delimitation of areas of endemism is not problematic when species originate by vicariance and there is no dispersal” (Hausdorf 2002). The biotic element concept is a general rule, encompassing a range of natural possibilities, including sharply delimited areas of endemism inhabited by nearly dispersal-free taxa. © 2004 by CRC Press LLC


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Again, it is seen that earthworms potentially simplify the job of biogeographical analysis if their biotic elements have very little overlap. It should be clear that any analytical biogeography of this sort absolutely requires a prior phylogenetic analysis (Wiley 1988). Ball (1975) remarked pointedly that earthworms had nothing to offer to biogeographical analyses because the treatment of the data available then was too superficial. With two exceptions (Jamieson 1988; Jamieson et al. 2002), all the higher-level taxonomic research on earthworms is based on classical methodology (e.g., Sims 1980; Omodeo 1998, 2000). This is not to say that the classical method was bad, but that “new” methods, particularly cladistic analysis (Hennig 1966; Sudhaus and Rehfeld 1992), have emerged since the older generation of earthworm taxonomists was trained. Unfortunately, very few of those specialists have taken advantage of the revolution in systematics that has occurred. Techniques of analyzing data for phylogenetic reconstruction are evolving and diversifying rapidly. Although maximum parsimony remains very important, other tools are coming into more general use. Maximum likelihood and Bayesian methods have been extended from molecular to morphological data sets and to combined morphological and molecular data (Lewis 2001). These tools allow certain flexibilities in data treatment and coping with homoplasy (independent evolution of characteristics by lineages with common ancestor that did not have the characteristics in question) that will be useful in redressing the phylogenetic deficiencies mentioned here. Both Bayesian and maximum likelihood methods use underlying mathematical models of evolution and compare the results of the model with the actual data obtained (molecular sequences or morphological data) on the way to deriving an estimate of phylogenetic relationships. Jamieson et al. (2002) provided an example of the application of several methods of analysis to a phylogenetic problem, but it is just the beginning of what needs to be done. The field of earthworm systematics is long overdue for a reinvigoration and an influx of ideas and techniques that are new to many of us. Good classical systematics will never lose its fundamental value and is the foundation for the standards of publication that are often ignored by modern authors. However, a century of work by a small but dedicated group has failed to resolve such fundamentals as the definitions of families (e.g., Sims 1980). To date, only Jamieson (1988) and Jamieson et al. (2002) have offered a rigorous analysis of this problem. The higher-level taxonomics of earthworms seems to be a very good area in which to apply molecular data. Biogeographical contributions from earthworm phylogeny need not be confined to questions involving taxa separated by oceanic barriers. In general, earthworms are slow to disperse, mating is highly localized, and populations may be easily isolated. If the earthworm fauna of New Zealand is an example, it can be seen that, in mountainous regions, there can be a tremendous overall species diversity, although the number of species present at any one site may be small (Lee 1959). Thus, the possibility exists to investigate the phylogeny of the earthworms of a single land area in relation to many potential fragmentations and reannealings of ranges because of geological, hydrological, or climatological processes. Although the noise in the data may be greater than in the case of transoceanic questions, it should still be as good as or better than the data derived from other taxa widely cited in the biogeographical literature.

HOW THE EARTH’S HISTORY AFFECTS EARTHWORM DISTRIBUTIONS The question of how to learn about the history of the Earth from earthworm phylogeny and biogeography is worth asking only because there is good reason to believe that the history of life is linked in many ways to the history of the Earth. On the other hand, have earthworms been affected by historical processes and on what scales of time and space? Certainly, much of the distributions of higher earthworm taxa can be illuminated by a study of the history of the Earth’s crust. What appears in the present as anomalous, disjunct distributions can be understood as the




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results of the fragmentation of a continuous distribution. At other time scales, the impacts of other events of earth history on earthworm distributions can be examined. Glaciation is one example of such an event. The second subject I use as an illustration of biogeographical research looks at the distributions of Nearctic earthworms in relation to the maximal extent of the Wisconsin (Würm) glaciation and how the process of postglacial recovery affects the composition of earthworm fauna at different points from south to north. This may also provide some basis for figuring out the larger modern ecological consequences of the processes affecting earthworm distributions. Work to date on the subject of glaciation and earthworm distributions has resulted in limited distributional data (Gates 1977; Reynolds 1994, 1995) and a plausible explanation for the distribution patterns (Gates 1977; Reynolds 1994), still leaving a need for an analytical approach. Analytical biogeography requires that hypotheses be formulated and their predictions tested. For example, it could be stated as a hypothesis that earthworms cannot survive beneath glaciers. This is testable, although it would be difficult to release test earthworms at the underside of a glacier and even harder to go back and look for them. It may be preferable to examine the predictions of the hypothesis: There should be no native earthworms in areas recently uncovered by receding glaciers, regardless of preglacial history of earthworm presence on that site. However, even if the observed distributions are in accord with the above historical model (the glaciers made it impossible for earthworms to be there), this does not prove a causal link. In the present case, there are conflicting data and alternative explanations to consider. For instance, Schwert (1979) found a fossil earthworm cocoon in postglacial sediments of southern Ontario, Canada. This is well north of the extent of maximum glaciation, and the discovery is old enough to indicate that colonization must have been more rapid than conventional estimates allow (about 6 to 10 m per year from points of introduction). It also worth noting that periglacial conditions (permafrost, for example) also affected earthworm distributions, such that simply marking the locations of terminal moraines is not sufficient to tell the whole picture (Schwert 1977, 1990). Finally, semiaquatic species have such as Eisenoides lönnbergi natural distributions in glaciated areas in the eastern United States (Schwert and James, unpublished data). It inhabits wetlands and so may have different propagule dispersal mechanisms than terrestrial worms. Returning to the alternative hypotheses, it is conceivable that modern-day earthworm species in North America were not capable of surviving the climate any farther north than they presently occur. Second, it is conceivable that North American earthworms were present farther north before the colonization of North America by settlers from Europe, but that European earthworms (or some combination of European earthworm invasion and habitat destruction) eliminated the native species by competition. An additional hypothesis needs to be made that climate affects the outcome of the process of competition, rendering it possible for native species to persist in the southerly areas. To meet these complaints against what seems a simple and obvious narrative explanation, I conducted experiments and made several altitudinal transects to test the hypothesis of climate limitation. Transects are comparative, not experimental, and so do not constitute a strong class of evidence. To address the climate question, I transplanted Eisenoides carolinensis and several Diplocardia species from Pennsylvania and southern Iowa, respectively, to forest and grassland sites in northern Minnesota in 1990. All the species survived the two winters of the experimental period and were still present on the site in 1994. Juveniles were found in both Minnesota sites, indicating that reproduction had taken place. Similarly, on altitudinal transects in the Appalachian Mountains of Virginia, West Virginia, and North Carolina, native earthworms were found in the highest elevations attainable, in vegetation zones characteristic of low elevation areas much farther north and presently not occupied by native species in those northern locations. Thus, climate limitation (and vegetation type) has been eliminated for the species in question and is unlikely to be a significant determinant of the northern boundary of native North American earthworm distributions. The evidence favors abiotic historical factors to explain modern North American earthworm distributions: Glaciation removed earthworms from areas once covered by ice or underlain by © 2004 by CRC Press LLC


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permafrost in periglacial areas, and the earthworms have been very slow to diffuse northward again. I hesitate to use the word “disperse” because there appear to be few events in the normal course of the earthworm life cycle that promote dispersal, other than coming out to crawl over the soil surface after heavy rains. Using estimates of rates of spread obtained from the Netherlands (Marinissen and van den Bosch 1992), 10,000 years is enough time for some peregrine earthworms to advance 60 to 100 km. Thus, range expansions of 100 to 200 km would be expected because of the maximal extent of the icecap in the Northern Hemisphere. Bouché (1983) reported on the earthworm recolonization of glaciated France along the Rhône River, with some ecological interpretations of species interactions. Range expansion rates may differ among earthworm species for various reasons, including modes of reproduction and ecological niche. For example, epigeic species may have a higher natural rate of diffusion than do oligohumic endogeic species. If this is true, this would result in something analogous to a chromatographic fractionation of the earthworm fauna. Should such a pattern emerge, earthworm ecological functions would be represented differently in the natural vegetation of locations along north-south transects crossing the limits of native earthworms. This should have some observable impact on ecosystem processes. The extreme case would be in the northern regions, where no earthworms are present and forest litter layers are quite deep. The contribution that I have tried to make to the question of how glaciation (or any other historical factor important to a species distribution) affects earthworm distributions has been to remove the question from the narrative domain and to formulate and test hypotheses. Those hypotheses tested were either the predictions of the central hypothesis (in the present case, that glaciation made impossible the occupation of ice-covered lands) or the alternatives to the central hypothesis. Although negative data are never as satisfying as positive data and can be overturned by a single positive datum, broad-scale events are often amenable to investigation only by a process of elimination of alternatives. Much earthworm biogeography (e.g., Reynolds 1995) (see Chapter 4 this volume) has been directed to the distributions of peregrine species. Completely different historical agents, such as patterns of human migration and horticultural and agricultural trade routes, would seem to be involved. Totally different ecological concerns emerge: Are absences of earthworm species because of historical factors alone or because of incompatibilities between sites and species? Are the present distributions of the peregrine earthworm species determined by their transport history or by ecological factors? To what extent is habitat disturbance involved in successful establishment of peregrines? Does it make sense to talk of species associations when the species found together may have nothing more in common than a collection of travelers in a train station? Are there forms of data, such as molecular data, that will allow the origins of populations of peregrine species to be traced to their areas of origin? The task of bringing rigorous scientific methodology to this topic will require much insight and may yield further insights into the connections between ecology and human history. Earthworm systematics has been making primary contributions to the work of people whose interests lie in ecology, agriculture, and other fields in need of a coherent classification of earthworm species. This is caused in part by the service functions of the field and a shortage of earthworm taxonomic specialists. However, using the new types of data and analytical methods discussed here, it should soon be possible to move toward providing the robust phylogenies required for good biogeography. The potential for contributions to the understanding of the Earth’s history and its interactions with the history of the biota is great. There may be few other terrestrial taxa so widely distributed, so ancient, and so amenable to collection and study as earthworms. When the high degree of endemicity of earthworm species also is considered, it is surprising that scientists working on biogeographical questions have not already taken more advantage of the marvelous research opportunities provided in earthworm systematics and biogeography.




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REFERENCES Ball, I. 1975. Nature and formulation of biogeographic hypotheses, Syst. Zool., 24:407–430. Bouché, M.B. 1983. The establishment of earthworm communities, in J.E. Satchell, Ed., Earthworm Ecology, Chapman & Hall, London, U.K. Darwin, C. 1881. The Formation of Vegetable Mould Through the Action of Worms with Observations on Their Habits, Murray, London. Fragoso, C., S.W. James, and S. Borges. 1995. Native earthworms of the north neotropical region: current status and controversies, in P. Hendrix, Ed., Earthworm Ecology and Biogeography in North America, CRC Press, Boca Raton, FL, pp. 67–116. Gates, G.E. 1969. On the earthworms of Ascension and Juan Fernandez Islands, Breviora, 323:1–4. Gates, G.E. 1977. More on the earthworm genus diplocardia, Megadriogica, 3:1–48. Hall, R. 1996. Reconstructing Cenozoic Southeast Asia, in R. Hall and D.J. Blundell, Eds., Tectonic Evolution of Southeast Asia, Geological Society of London Special Publication, London, pp. 106, 153–184. Hall, R. 1998. The plate tectonics of Cenozoic Southeast Asia and the distribution of land and sea, in R. Hall and J.D. Holloway, Eds., Biogeography and Geological Evolution of Southeast Asia, Backhuys Publishers, Leiden, the Netherlands, pp. 99–131. Hausdorf, B. 2002. Units in biogeography, Syst. Biol., 51:648–652. Hennig, W. 1966. Phylogenetic Systematics, University of Illinois Press, Urbana, IL. Hopp, H. 1946. Earthworms fight erosion, too, Soil Cons., 11:252–255. Humphries, C.J. and L.R. Parenti. 1999. Cladistic Biogeography, Oxford University Press, Oxford, U.K. James, S.W. 1996. Nine new species of dichogaster (Oligochaeta: Megascolecidae) from Guadeloupe (French West Indies), Zool. Scripta, 25(l):21–34. Jamieson, B.G.M. 1981. Historical biogeography of Australian Oligochaeta, in A. Keast, Ed., Ecological Biogeography of Australia, W. Junk, The Hague, the Netherlands, pp. 887–921. Jamieson, B.G.M. 1988. On the phylogeny and higher classification of the Oligochaeta, Cladistics, 4:367–401. Jamieson, B.G.M., S. Tillier, A. Tillier, J.-L. Justine, E. Ling, S. James, K. McDonald, and A.F. Hugall. 2002. Phylogeny of the Megascolecidae and Crassiclitellata (Annelida, Oligochaeta): combined vs. partitioned analysis using nuclear (28S) and mitochondrial (12S, 16S) rDNA, Zoosystema, 24(4):707–734. Lavelle, P. and A. Martin. 1992. Small-scale and large-scale effects of endogeic earthworms on soil organic matter dynamics in the humid tropics, Soil Biol. Biochem., 24:1491–1498. Lee, K.B. 1959. The Earthworm Fauna of New Zealand, New Zealand Department of Scientific and Industrial Research Bulletin 130, Wellington, New Zealand. Lewis, P.O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data, Syst. Biol., 50(6):913–925. Liebherr, J.K. 1988. General patterns in West Indian insects, and graphical biogeographic analysis of some circum-Caribbean Platynus beetles (Carabidae), Syst. Zool., 37:385–409. Lovelock, J. 1988. The Ages of Gaia: A Biography of Our Living Earth, Norton and Company, New York. Marinissen, J.C.Y. and F. van den Bosch. 1992. Colonization of new habitats by earthworms, Oecologia, 91:371–376. Maury, R.C., G.K. Westbrook, P.E. Baker, Ph. Bouysse, and D. Westercamp. 1990. Geology of the Lesser Antilles, in G. Dengo and J.E. Case, Eds., The Caribbean Region, Vol. H, The Geology of North America, Geological Society of America, Boulder, CO, pp. 141–165. Michaelsen, W. 1911. Zur Kenntnis der Eodrilaceen und ihrer Verbreitungsverhältnisse Zool, Jahrb. Abt. f. Syst., 30:527–572. Michaelsen, W. 1933. Die Oligochaetenfauna Surinames mit Erörterung der verwandtschaftlichen Beziehungen der Octochatinen, Tijdschr. Ned. Dierk. Vereen., 3:112–131 Nakamura, M. 1990. How to identify Hawaiian earthworms, Chuo Univ. Res. Notes, 11:101–110. Noonan, G.R. 1988. Biogeography of North American and Mexican insects, and a critique of vicariance biogeography, Syst. Zool., 37:366–384. Nooren, C.A.M., N. van Breemen, J.J. Stoorvogel, and A.G. Jongmans. 1995. The role of earthworms in the formation of sandy surface soils in a tropical forest in Ivory Coast, Geoderma, 65:135–148. Omodeo, P. 1998. History of Clitellata, Ital. J. Zool., 65:51–73. Omodeo, P. 2000. Evolution and biogeography of megadriles (Annelida, Clitellata), Ital. J. Zool., 67:179–201.



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Pindell, J.L. and S.F. Barrett. 1990. Geological evolution of the Caribbean region; a plate-tectonic perspective, in G. Dengo and J.E. Case, Eds., The Caribbean Region, Vol. H, The Geology of North America, Geological Society of America, Boulder, CO, pp. 405–432. Reynolds, J.W. 1994. The distribution of the earthworms (Oligochaeta) of Indiana: a case for the postQuaternary introduction theory for megadrile migration in North America, Megadrilogica, 5:13–32. Reynolds, J.W. 1995. Status of exotic earthworm systematics and biogeography in North America, in P. Hendrix, Ed., Earthworm Ecology and Biogeography in North America, CRC Press, Boca Raton, FL, pp. 1–27. Rosen, D.E. 1985. Geological hierarchies and biogeographical congruence in the Caribbean, Ann. Mo. Bot. Gard., 72:636–659. Roughgarden, J. 1990. Origin of the eastern Caribbean: data from reptiles and amphibians, in D. LaRue and G. Draper, Eds., Trans. 12th Caribbean Conf. St. Croix, USVI Miami Geological Society, Miami, FL, pp. 10–26. Savage, J.M. 1982. The enigma of the Central American herpetofauna: dispersals or vicariance? Ann. Missouri Bot. Gard., 69:464–547. Schwert, D.P. 1977. The first North American record of Aporrectodea icterica (Savigny 1826) (Oligochata: Lumbricidae), with observations on the colonization of exotic earthworm species in Canada, Can. J. Zool., 55(1):245–248. Schwert, D.P. 1979. Description and significance of a fossil earthworm cocoon (Oligochata: Lumbricidae) from postglacial sediments in southern Ontario, Can. J. Zool., 57(7):1402–1405. Schwert, D.P. 1990. Lumbricidae, in D. L. Dindal, Ed., Soil Biology Guide, John Wiley & Sons, New York, pp. 341–356. Sharpley, A.N. and J.K. Syers. 1977. Seasonal variation in casting activity and in the amounts and release to solution of phosphorus forms in earthworm casts, Soil Biol. Biochem., 9:227–231. Sims, R.W. 1980. A classification and the distribution of earthworms, suborder Lumbricina (Haplotaxida Oligochaeta), Bull. Br. Mus. (Nat. Hist.) Zool. Ser., 39(2):103–124. Sober, E. 1988. The conceptual relationship of cladistic phylogenetics and vicariance biogeography, Syst. Zool., 37:245–270. Stephenson, J. 1930. The Oligochaeta, Clarendon Press, Oxford, U.K. Sudhaus, W. and K. Rehfeld. 1992. Einführung in die Phylogenetik und Systematik, Gustav Fischer, New York. Talavera, J.A. 1990. Claves de identificacion de las lombrices de tierra (Annelida Oligochaeta) de Canarias, Vieraea, 18:113–119. Wiley, E.O. 1981. Phylogenetics, Wiley Interscience, New York. Wiley, E.O. 1988. Parsimony analysis and vicariance biogeography, Syst. Zool., 37:271–290. Zwickl, D.J. and D.M. Hillis. 2002. Increased taxon sampling greatly reduces phylogenetic error, Syst. Biol., 51(4):588–598.


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Status of Earthworm 4 The Biogeography, Diversity, and Taxonomy in North America Revisited with Glimpses into the Future John W. Reynolds Oligochaetology Laboratory, Kitchener, Ontario, Canada

CONTENTS Introduction ......................................................................................................................................63 Earthworm Biogeography, Diversity, and Taxonomy .....................................................................65 Biogeography ............................................................................................................................65 North America .................................................................................................................65 Other Countries ...............................................................................................................67 Diversity ....................................................................................................................................67 Taxonomy..................................................................................................................................67 Presentations at the International Earthworm Ecology Symposia..................................................68 Future Trends and Research Imperatives in Earthworm Taxonomy...............................................69 Training of Earthworm Taxonomists........................................................................................69 Earthworm Parthenogenesis and Effects on Taxonomy...........................................................69 Earthworm Surveys...................................................................................................................69 Earthworm Life Histories .........................................................................................................70 Modern Earthworm Techniques................................................................................................70 Use of Earthworms for Waste Management ............................................................................70 Earthworms for Environmental Monitoring .............................................................................70 Plain Language and Less Esotery ............................................................................................70 References ........................................................................................................................................71

INTRODUCTION A discussion of the distribution of earthworms in North America Reynolds (1994a) included the three steps of biogeographical theory. The first step is descriptive or faunistics, the gathering of facts and identification and enumeration of animals in an area, including research and literature surveys. This step, although seldom fully achieved, seeks to present a clear distributional picture of all the animals in all areas. The second step is the classification of data, grouping of the distributional data according to as many different points of view as a particular investigation may



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find necessary, including comparison of the distributional ranges of phylogenetically related groups. This step also includes analyzing the fauna of a geographically, ecologically, or historically uniform area. The third and final step, causal analysis, tries to explain the reasons for the present distribution as identified. It is from this step that the principles of biogeography emerge. At present, in North America, with megadrile earthworms the situation is probably somewhere between the first two stages (Reynolds, 1975a, 1976b, 1994a). Studies of the status quo of animal distributions and of the grouping of these distributions according to different principles are investigations of momentary phenomena. Faunistic and regional zoogeography is basically static zoogeography because present distributions are the result of processes that have moved the animals in space, resulting in change of the distributional picture with the passage of time. Thus, causal zoogeography can be identical to dynamic zoogeography because causations of distributions are dynamic processes. As long as the inquiry probes the reasons for the arrival and colonization of a species in a certain area, the investigation is within the field of dynamic zoogeography. For example, the lack of an animal species in a certain area may be caused by ecological (it cannot exist there) or zoogeographical (it has not arrived there) reasons. The answers pertaining to dynamic zoogeography are often ecological, but the ecological cause is followed by movement of individuals or populations and of the subject organism. When the ecological cause is followed by a positive or negative response of the organism or population, and when a spatial shift is not involved, the whole phenomenon falls within the sphere of ecology. This, however, is usually assigned to the taxonomist because evolutionary changes are most easily discerned by noting morphological changes. Lindroth (1962) expressed the relationship of these two disciplines as follows: Zoogeography always depends on taxonomy to know what to study, but taxonomy also depends on zoogeography because geographic speciation is the accepted norm of the formation of its basic working unit. Every animal species originated from a few ancestors in a limited area; if a particular species is now widespread, it must of necessity have reached parts of its present range at an earlier period. The first aspect of dynamic zoogeography pertains to dispersal. If the details of dispersal processes are known, much about the presence or absence of animals can be explained. Dispersal may result as a by-product of other important phenomena, belonging to the biological habits of the animal, or it can result from distinct, adaptive characteristics of the species that directly assist dissemination into wider areas. Although every animal species has a capability to migrate, dispersing individuals must find suitable areas in which to settle and reproduce through many generations. When the process of settling or colonization is studied, the ecological factors that make the existence of a species possible in a given area must be scrutinized, as well as the adaptations and limitations of a species, such as structural, physiological, behavioral, or population dynamic properties that enable it to initiate a new population and survive (successfully) in the newly colonized area. Factors of dispersal as well as factors of existence in an area can influence the size, extent, and dynamism of the distributional range of the animal. James (1995) (see Chapter 3 this volume) uses a coincidently similar approach when he elaborates on the concepts of Ball (1975). Ball described three phases of biogeographic methodology: (1) empirical or descriptive, (2) narrative, and (3) analytical. James concentrates his discussion on two main points: (1) deoxyribonucleic acid (DNA) sequence information and (2) biogeographical research related to glaciation. I have very limited personal experience with DNA research, but for more than 2 decades (Reynolds 1973a) I have advocated this approach but have never had the opportunity for follow-up. It now appears that James, his colleagues, and their students have the means to do so, and earthworm ecology and biology should benefit greatly from the results of their work. I have devoted considerable time and activity to the second topic over the years. My earthworm research has concentrated on presenting wide-ranging formal surveys in North America and



The Status of Earthworm Biogeography, Diversity, and Taxonomy in North America

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elsewhere (Table 4.1). James and others are going back to some of these areas and, with knowledge of the species that should be present, are conducting more detailed studies (e.g., using transects to assess distributions).

EARTHWORM BIOGEOGRAPHY, DIVERSITY, AND TAXONOMY In this section, I discuss some of the advances and innovations in oligochaetology during the past 2 years, particularly in those areas in which I have participated either as a journal referee or an editor, and for which I know, sometimes more than a year or two in advance, what will be appear in the literature regarding earthworm biogeography, diversity, and taxonomy. I summarize some of my relevant impressions on these developments.

BIOGEOGRAPHY North America Canada Considerable advances have been made in the distributional reports of earthworm taxa for many regions of North America. The first complete picture of the megadrile earthworm distributional patterns in the Province of Quebec was presented in the early 1990s (Reynolds and Reynolds 1992). Several earlier reports (Reynolds 1975a,b,c,d; 1976a,c,d) presented segments of the Quebec earthworm distribution patterns, but it was not until later (Reynolds and Reynolds 1992) that distribution over the whole province was considered. In this report, 19 species were recorded for the province, and Sparganophilus eiseni was reported for the first time from two widely separated collections more than 700 km east of any previously known records. Scheu and McLean (1993) presented the first report of the earthworm distributions in wideranging areas of southern Alberta. In their article, they reported eight species, with Lumbricus rubellus reported for the first time from the province. They also included considerable discussion on the ecological aspects of the species in the area. One of the more interesting and surprising reports was by two Russian scientists working in Siberia and the Yukon (Berman and Marusik 1994). Until their paper appeared, there were no published reports on earthworms from these Canadian territories. They found Bimastos parvus, Dendrobaena octaedra, and Dendrodrilus rubidus in these far north areas. They presented their views in great depth on earthworm migrations, isolated populations, and earthworm introductions in the far north to explain why the Siberian megadrile earthworm fauna is lacking in the Yukon. Subsequent papers (Reynolds and Moore 1996; Reynolds 2003b,c) have added to the earthworm species list of the Northwest Territories and the new territory of Nunavut in northern Canada. United States There has been considerable expansion in the knowledge of earthworm distributions in the United States. There were 37 species recorded (Reynolds 1994b) in the state of Indiana, 10 of which were reported for the first time. In North Carolina, Reynolds (1994f) reported 42 species, of which 10 were reported for the first time from the state. In Virginia (Reynolds 1994h), another Atlantic coastal state, 37 species were reported, with 6 species recorded for the first time for the state. Later in that year, the earthworm distributions in two more southern states, Florida (Reynolds 1994e) and Mississippi (Reynolds 1994g), were published. In the state of Florida, there were 51 species, and 3 subspecies were reported from 8 families. Of these species, 7 were reported for the first time from Florida. In the case of Mississippi, 27 species were recorded, and 10 of these were reported for the first time for the state. The earthworm distributional patterns of several other states and provinces are currently in preparation (Reynolds and Wetzel 2004b). The scientific and common names plus the distributional ranges for all the groups in the Clitellata and Aphanoneura have been described (Coates et al. 1995). © 2004 by CRC Press LLC


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TABLE 4.1 Regional Earthworm Surveys in North America Number of Species

Number of Units (%) Surveyed

Alabama Alberta

28 12

75 35

Arkansas Bermuda Colorado Connecticut Delaware Florida Georgia Illinois Indiana Louisiana Manitoba Maryland Massachusetts Michigan Minnesota Mississippi Missouri Montana New Brunswick

21 9+ 14 21 14 54 42 32 37 17 12 26 21 20 15 27 21 8 15

29 100 51 100 100 85 75 45 100 100 n/a 100 100 64 59 77 27 14 100

New York Newfoundland and Labrador North Carolina North Dakota Northwest Territories Nova Scotia Nunavut Ohio Ontario Oregon Prince Edward Island Quebec (south shore) Quebec (north shore) Rhode Island Saskatchewan South Carolina South Dakota Tennessee Virginia Washington

20 11 42 5 2 15 2 22 19 25 12 15 19 14 6 26 3 41 37 22

47 n/a 79 15 n/a 100 n/a 63 96 70 100 100 86 100 n/a 100 3 100 77 40

Wyoming Yukon

12 3

71 100

Region

n/a, not applicable


Ref. Reynolds 1994c Scheu and McLean 1993; Reynolds and Clapperton 1996 Causey 1952, 1953 Reynolds and Fragoso 2004 Reynolds and Reeves 2004 Reynolds 1973b Reynolds 1973c Reynolds 1994e Reynolds in prep. Harman 1960 Reynolds 1994b Harman 1952; Gates 1965, 1967 Reynolds 2000a Reynolds 1974a Reynolds 1977b Snider 1991 Reynolds et al. 2002 Reynolds 1994g Olson 1936 Reynolds 1972 Reynolds 1976d, 2001b; Reynolds and Christie 1977; McAlpine et al. 2001 Olson 1940; Eaton 1942 Reynolds 2000b Reynolds 1994f Reynolds 1978a Reynolds and Moore 1996; Reynolds 2003b Reynolds 1976b Reynolds 2003b,c Olson 1928, 1932 Reynolds 1977a MacNab and McKey-Fender 1947; Fender 1985 Reynolds 1975d Reynolds 1975c,d,e, 1976a Reynolds and Reynolds 1992 Reynolds 1973d, 2002 Reynolds and Khan 1999 Reynolds 2001b; Reynolds and Reeves 2004 Gates 1979 Reynolds et al. 1974; Reynolds 1977c,d, 1978b Reynolds 1994h Altman 1936; Fender 1985; MacNab and McKey-Fender 1947 Reynolds 2004 Berman and Marusik 1994



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The first attempt to present a regional review of the earthworm distributions in continental North America was in the 1970s (Reynolds 1975a, 1976b). During the past 20 years, there have been many advances and additional available data for many regions (states and provinces) in North America. The first summary of regional earthworm surveys in North America was made (Reynolds et al. 1974). Since that time, there have been wide-ranging earthworm collections in North America, resulting in many publications on the distribution of various species of earthworms in North America and Mexico (Fragoso et al. 1994). An updated version of that table appeared in 1994 and 1995 (Reynolds 1994c, 1995), and the most recent revision is given in Table 4.1. Other Countries There has been considerable expansion of knowledge of megadrile earthworm distributions on other continents as well. For instance, de Mischis (1992, 1993) expanded the distributional records for Argentina. The first survey of the earthworms of Swaziland appeared (Reynolds 1993). This survey reported seven species from that small African country. Earthworm surveys undertaken during 1992 and 1993 contributed to the first survey of the earthworms of Bangladesh (Reynolds 1994d), where 14 species were reported, and there were speculations on the possible presence of an additional 28 species. The first survey and report of earthworms from Belize indicated three species: Dichogaster bolaui, Pontoscolex corethrurus, and a new species, Eodrilus jenniferae (Reynolds and Righi 1994). Additional earthworm samples were obtained subsequently (Reynolds and Guerra 1994). Two additional examples of original surveys were in San Andres and Contadora Island (Reynolds and Reynolds 2002a,b) and Gough Island, South Atlantic Ocean (Reynolds et al. 2002).

DIVERSITY There have been considerable data published on earthworm diversity in the Americas. The current status of various aspects of earthworm research on this continent has been summarized (Fragoso et al. 1994; Fender 1995; Hendrix 1995; James 1995; Reynolds 1995). Bøgh (1992) published an interesting and innovative article, “Identification of Earthworms (Lumbricidae): Choice of Method and Distinction Criteria.” In this article, he discussed the use of electrophoretic techniques in the identification of earthworm species. One of the immediate benefits of this approach is the potentially more accurate determination of juveniles and fragments of the caliginosa complex that the late Dr. Gordon Gates and I have long advocated. The morphological criteria developed by Gates (1972a) that were used in many of my surveys throughout North America were supported by Bøgh (1992). I (1994a) prepared a summary in Earthworms of the World. This included discussions of global distributions, barriers to migration, habitat requirements, and functions of earthworms in the soil.

TAXONOMY For a field of science as limited as oligochaetology, it is fortunate there are books that combine all the description citations and type depositions of earthworms: the Nomenclatura Oligochaetologica and its three supplements (Reynolds and Cook 1976, 1981, 1989, 1993). The third supplement (Supplementum Tertium), which recorded new taxa found up to December 31, 1992, suggested that 739 earthworm genera, 40 subgenera, and 7254 species have been described. A fourth supplement (Reynolds and Wetzel 2004a) described more than 1048 new species. Some of the most exciting discoveries regard the presence of nearctic species in the far reaches of North America, areas where they were not previously recorded. These include Fender’s (1985) and McNab and McKey-Fender’s (1947) work on Bimastos and Arctiostrotus in the northwestern United States and southwestern British Columbia (Canada) as well as James’s (1995) discoveries of Argilophilus and Diplocardia in the southwestern United States.



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The status of exotic earthworm systematics and biogeography in North America was reviewed (Reynolds 1995). This review dealt mainly with the Lumbricidae and excluded the nearctic genera Bimastos and Eisenoides. The section on historical perspectives traced the associations and classiù ´ (1991) and discussed the lumping of fications of authors from Linnaeus (1758) through Mrsic certain species inter- and intragenerically. These frequent realignments by taxonomists have created many nomenclatural and taxonomic problems for ecological researchers for many years. The review also included discussions on earthworm contributions and activity in North America, which is often lacking in some European publications. Some portions of the biogeographical section are summarized here and in Table 4.1. James (1995) addressed the issue of systematics, biogeography, and ecology of nearctic earthworms from the eastern, central, southern, and southwestern United States. He dealt with five families, two of which are monospecific: Lutodrilidae (Lutodrilus multivesiculatus) and Komarekionidae (Komarekiona eatoni). The family Sparganophilidae is monogeneric with 12 species. The Lumbricidae were included mainly in the two nearctic genera Bimastos and Eisenoides, with nine and two species, respectively. James’s version of the Megascolecidae (Acanthodrilidae sensu Gates and Reynolds) was restricted to the genus Diplocardia and its 42 species. James’s ecological section included discussions of earthworm population studies and emphasized the lack of earthworm community studies and economic applications. Fender (1985, 1995) provided an ecological overview of native earthworms of the Pacific Northwest. He dealt with a group of earthworms (Megascolecidae, Argilophilini) unfamiliar to many earthworm scientists. Fender stated that the Pacific Northwest possesses a “rich, varied, and interesting, but highly underreported” earthworm fauna. There are a vast number of taxa to be described and data that have been collected and are waiting analysis. Fender discussed the historical biogeography, ecology, and variation of this group of little-known oligochaetes. Fragoso et al. (1994) reviewed the native earthworms of the north neotropical region and their current status and controversies. Their lists of earthworm species and the authors cited may not be familiar to many North American earthworm scientists, although the early works cited in their historical perspective included researchers such as Beddard, Benham, Cognetti, Eisen, Gates, and Michaelsen, who are well-known earthworm taxonomists. They also reviewed species of earthworms from Mexico (Fragoso et al. 1994). The authors explained in great detail the biogeography, ecology, and taxonomy of the earthworms from their region. In their list of the earthworm fauna of the north neotropical region, Fragoso et al. (1995) indicated the absence of any reports on earthworms from Belize (formerly British Honduras). I had the opportunity to work in this small Central American country and collect earthworms. The results of these collections were published in a paper by Gilberto, and two well-known species (Dichogaster bolaui and Pontoscolex corethrurus) are reported together with a new species, Eodrilus jenniferae. In addition to the description of a new species and the first record of earthworms from Belize, this article includes a discussion on the retention of eodrilus and diplotrema as separate and distinct genera based on four criteria. We also continued with suggestions for distinguishing four closely related genera: eodrilus, notiodrilus, acanthodrilus, and microscolex. Our solution for distinguishing these genera will undoubtedly spark discussion in the future, and as a result of these debates, earthworm taxonomists should come closer to agreement.

PRESENTATIONS AT THE INTERNATIONAL EARTHWORM ECOLOGY SYMPOSIA There have been seven International Earthworm Ecology Symposia, at Grange-over-Sonids, England (1981); Bologna, Italy (1985); Hamburg, Germany (1987); Avignon, France (1990); Columbus, OH, United States (1994); Vigo, Spain (1998); and Cardiff, Wales (2002). Each was




69

attended by 200 to 300 earthworm scientists, including many international systematists. All the symposia included sections on taxonomy, distributions, and biogeography of earthworms.

FUTURE TRENDS AND RESEARCH IMPERATIVES IN EARTHWORM TAXONOMY One of the major problems for earthworm taxonomy in North America and elsewhere has been the paucity of earthworm systematists and their geographical isolation. Gordon Gates, one of the most productive taxonomists, died in 1987. Although he began publishing on earthworm systematics in 1926, it was not until the latter part of his career that he devoted much time to describing the Lumbricidae and other earthworms of North America. Before 1950, taxonomists included Frank Smith (publication period 1985 to 1937) and Henry Olson (publication period 1928 to 1940), who made significant contributions to earthworm taxonomy and distributions, respectively. In the past few decades, Dorothy McKey-Fender and William Fender have concentrated on the taxonomy and distribution of the native and exotic earthworm fauna of the west coast of North America, and Sam James has investigated the endemic species of the southeastern and plains areas of the United States. Since 1972, I have collected earthworms widely throughout North America, and the results of these collections have been published primarily as distribution data, with relatively minimal contributions to systematics sensu stricto. The Nomenclatura Oligochaetologica series put together in a single source the essential basic reference data for anyone involved in the taxonomy and nomenclature of earthworms or who need a ready, up-to-date reference list of species authorities have described. The fourth supplement (Reynolds and Wetzel 2004a) should be available at the end of 2004. I suggest the following priorities for future earthworm research.

TRAINING

OF

EARTHWORM TAXONOMISTS

For more than 2 decades, it has been obvious that the scarcity of competent earthworm systematists and taxonomists was detrimental to progress in research by ecologists and others (Reynolds 1973a; Reynolds et al. 1974a,b). Institutions that normally employ taxonomists and encourage their development (e.g., museums, departments of agriculture, and universities) have not done so in North America. There is a need for a concerted effort to support this type of research before there are few or no earthworm taxonomists remaining. However, the large number of scientists actively working in various aspects of earthworm biogeography and taxonomy elsewhere in the world is most gratifying and bodes well for the future of the science.

EARTHWORM PARTHENOGENESIS

AND

EFFECTS

ON

TAXONOMY

A major exotic group of earthworms in North America (Megascolecidae and pheretimoid groups) has long been plagued with taxonomic problems, which have resulted from the incidence of widespread parthenogenesis among its species (Gates 1972). Parthenogenesis also occurs within the Lumbricidae. One study showed that localized populations of Octolasion tyrtaeum (Jaenike et al. 1980, 1982; Jaenike and Selander 1985) have exhibited parthenogenesis. Previously, taxonomic problems with some morphotypes of what is now recognized as Dendrodrilus rubidus may be attributed to parthenogenesis. The issue of parthenogenesis in earthworms has only recently received more attention and may have major impacts on earthworm taxonomy.

EARTHWORM SURVEYS It is obvious from the data in Table 4.1 that, in spite of what has already been achieved, there are major areas of North America in which there have been no earthworm surveys. In certain areas



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where native species still exist, there is still very considerable potential for discovery of new species. Any new species reported in the lumbricidae will most probably come from the two native genera bimastos and isenoides or even from a new genus. Additional new species might also be expected to occur in other nearctic genera, such as arctiostrotus, diplocardia, and komarekiona.

EARTHWORM LIFE HISTORIES It is amazing that, of the nearly 8000 oligochaete species described (Reynolds and Cook 1993), ecological and life history studies have been made on relatively few species, probably fewer than 20. Lee (1992) suggested that only about six lumbricid and six tropical species have been studied in sufficient detail to provide adequate life history information. However, Barois et al. (1999) provided basic ecological and life history data on 58 tropical earthworm species, but not all described in detail. Some of the information gathered on the ecology of common lumbricidae was obtained from a time when species lumping occurred; that is, descriptions were attributed to Allolobophora caliginosa, which now includes several species, so further studies may be needed for clarification.

MODERN EARTHWORM TECHNIQUES One technique that has been considered for years, but only recently had any evidence to support its potential in taxonomy, is electrophoresis. Using this technique, Bøgh (1992) illustrated that certain earthworm species were different (i.e., Aporrectodea tuberculata and Aporrectodea turgida were distinct species), and he demonstrated how to identify species from fragments. There is also considerable scope for use of DNA analyses in taxonomy (see Chapter 3, this volume).

USE

OF

EARTHWORMS

FOR

WASTE MANAGEMENT

The acceptance of organic waste recycling and vermicomposting using earthworms has gained increasing acceptance over the past 2 decades and is increasing rapidly in both industrialized and nonindustrialized countries (see Chapter 18, this volume). In North America, the research is restricted to only a few species (Eisenia foetida, Eudrilus eugeniae, Perionyx excavatus), but with almost 4000 megadrile species available, the search should be for additional species that may be harnessed to assist the decomposition and transformation of waste products into useful materials (see Chapters 18, 19, and 20 this volume).

EARTHWORMS

FOR

ENVIRONMENTAL MONITORING

The ability of many species of earthworms to accumulate heavy metals and various pesticides into their tissues offers opportunities to trace the movement of these materials in the soil. One aquatic microdrile species, Tubifex tubifex, has been used for decades as a biological indicator in polluted waters. Eisenia andrei is used in a standardized terrestrial assay using artificial soil to assess the toxicity of pesticides and other chemicals (Edwards and Bohlen 1992). Research is needed on the toxicities uptake mechanisms, distribution, and concentration of chemicals in various types of earthworm tissues. In particular, interpretation of the findings on chemicals and earthworms as they relate to our daily lives is needed.

PLAIN LANGUAGE

AND

LESS ESOTERY

I have long advocated the necessity for scientific information to be more accessible to the general nonscientific community. Entomologists and ornithologists have advanced more rapidly because of the joint contributions of “amateurs” and general collectors. In the early part of this century, earthworm biology had one such person, the Hilderic Friend, who was turned aside and dismissed




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by the many earthworm specialists of the day. He was a good naturalist, but many of his contributions were ridiculed and discounted. If he had been encouraged, his work might have had a greater impact on oligochaetology as we know it today.

REFERENCES Altman, L.C. 1936. Oligochaeta of Washington, Univ. Wash. Publ. Biol., 4(1), 1–137. Ball, I.R. 1975. Nature and formulation of biogeographical hypotheses, Syst. Zool., 24(4), 407–430. Barois, I., Lavelle, D., Brossard, M., Tondoh, J., Martinez, M.A., Rossi, J.P., Senapati, B.K., Angeles, A., Fragoso, C., Jimenez, J.J., Decaens, T., Lattand, C., Kanyono, J., Blanchart, E., Chapuis, L., Brown, G., and Moreno, A. 1999. Ecology of earthworm species with large environmental tolerances and/or extended distributions, in Earthworms Management in Tropical Agroecosystems, Lavelle, P., Brussaard L., and Hendrix, P. Eds., CABI Publishing, Wallingford, U.K., pp. 57–86. Berman, D.I. and Marusik, Y.M. 1994. On Bimastos parvus (Oligochaeta: Lumbricidae) from Yukon Territory (Canada) with notes on distribution of the earthworms in northwest North America and northeast Siberia, Megadrilogica, 5(10), 113–116. Bøgh, P.S. 1992. Identification of earthworms (Lumbricidae): choice of method and distinction criteria, Megadrilogica, 4(10), 163–174. Causey, D. 1952. The earthworms of Arkansas, Proc. Ark. Acad. Sci., 5, 31–42. Causey, D. 1953. Additional records of Arkansas earthworms, Proc. Ark. Acad. Sci., 6, 47–48 de Mischis, C.C. 1992. The first record of the species Amynthas diffringens (Baird, 1869) (Oligochaeta: Megascolecidae) in the province of Cordoba (Argentina), Megadrilogica, 4(8), 143–144. de Mischis, C.C. 1993. A contribution to the knowledge of megascolecid fauna (Annelida, Oligochaeta) from the province of Cordoba, Argentina, Megadrilogica, 5(2), 9–12. Eaton, T.H. 1942. Earthworms of the northeastern United States: a key, with distribution records, J. Wash. Acad. Sci., 32(8), 242–249. Edwards, C.A., Ed. 1997. Proceedings of Fifth International Symposium on Earthworm Ecology, Soil Biol. Biochem., 29(3/4), 217–766. Edwards, C.A. and Bohlen, P.J. 1992. The effects of toxic chemicals on earthworms, Rev. Environ. Contam. Toxicol., 125, 23–99. Fender, W.B. 1985. Earthworms of the western United States. Part. I. Lumbricidae, Megadrilogica, 4(5), 93–129. Fender, W.B. 1995. Native earthworms of the Pacific Northwest: an ecological overview, in Ecology and Biogeography of Earthworms in North America, Hendrix, P.F., Ed., Lewis Publishers, Boca Raton, FL, pp. 53–66. Fragoso, C. and Fernández, P.R. 1994. Earthworms from southwestern Mexico. New Acanthodriline genera and species (Megascolecidae, Oligochaeta), Megadrilogica, 6(1), 1–12. Fragoso, C., James, S.W., and Borges, S. 1995. Native earthworms of the north neotropical region: current status and controversies, in Ecology and Biogeography of Earthworms in North America, Hendrix, P.F., Ed., Lewis Publishers, Boca Raton, FL, pp. 67–114. Gates, G.E. 1965. Louisiana earthworms. I. A preliminary survey, La. Acad. Sci., 28(1), 12–20. Gates, G.E. 1967. On the earthworm fauna of the Great American desert and adjacent areas, Gt. Basin Nat., 27(3), 142–176. Gates, G.E. 1972. Burmese earthworms. An introduction to the systematics and biology of megadrile oligochaetes with special reference to southeast Asia, Trans. Am. Philos. Soc., 62(7), 1–326. Gates, G.E. 1979. South Dakota does have earthworms! Megadrilogica, 3(9), 165–166. Harman, W.J. 1952. A taxonomic survey of the earthworms of Lincoln Parish, Louisiana, Proc. La. Acad. Sci., 15, 19–23. Harman, W.J. 1960. Studies on the Taxonomy and Musculature of the Earthworms of Central Illinois, Ph.D. dissertation, University of Illinois, Champaign, IL. Hendrix, P.F. 1995. Ecology and Biogeography of Earthworms in North America, Lewis Publishers, Boca Raton, FL. Jaenike, J. and Selander, R.K. 1985. On the co-existence of ecologically similar clones of parthenogenetic earthworms, Oikos, 44(3), 512–514. © 2004 by CRC Press LLC


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Jaenike, J., Ausubel, S., and Grimaldi, D.A. 1982. On the evolution of clonal diversity in parthenogenetic earthworms, Pedobiologia, 23(3–4), 304–310. Jaenike, J., Parker, E.D., and Selander, R.K. 1980. Clonal niche structure in the parthenogenetic earthworm Octolasion tyrtaeum, Am. Nat., 116, 196–205. James, S.W. 1995. Systematics, biogeography and ecology of earthworms from eastern, central, southern and southwestern USA, in Ecology and Biogeography of Earthworms in North America, Hendrix, P.F., Ed., Lewis Publishers, Boca Raton, FL, pp. 29–51. Kretzschmar, A., Ed. 1992. Proceedings of Fourth International Symposium on Earthworm Ecology, Soil Biol. Biochem., 24(12), 1193–1771. Lee, K.E. 1992. Some trends and opportunities in earthworm research or: Darwin’s children — the future of our discipline, Soil Biol. Biochem., 24(12), 1765–1771. Lindroth, C.H. 1962. Foreword, in Taxonomy and Geography, Nichols, D., Ed., Systemics Assoc. Publ., London, U.K., pp. 3–5. Linnaeus, C. 1758. Systema Naturae. Regnum Animale, 10th ed. MacNab, J.A. and McKey-Fender, D. 1947. An introduction to Oregon earthworms with additions to the Washington list, Northwest Sci., 21(2), 69–75. McAlpine, D.F., Reynolds, J.W., Fletcher, T.J., Trecartin, J.L., and Sabine, D.L. 2001. Megadrilogica, 8(10), 53–56. ÿ ´ N. 1991. Monograph on Earthworms (Lumbricidae) of the Balkans, Slovenska Akademija Znanosti Mrsic, Umetnosti, Ljubljana, Slovenia. Olson, H.W. 1928. The Earthworms of Ohio, with a study of their distribution in relation to hydrogen-ion concentration, moisture and organic content of the soil, Bull. Ohio Biol. Surv., 4(2), Bull. 17, 47–90. Olson, H.W. 1932. Two new species of earthworms for Ohio, Ohio J. Sci., 32, 192–193. Olson, H.W. 1936. Earthworms of Missouri, Ohio J. Sci., 36(2), 102–193. Olson, H.W. 1940. Earthworms of New York State, Am. Mus. Nov., 1090, 9. Reynolds, J.W. 1972. A contribution to the earthworm fauna of Montana, Proc. Mont. Acad. Sci., 32, 6–13. Reynolds, J.W. 1973a. Earthworm (Annelida, Oligochaeta) ecology and systematics, in Proc., Dindal, D.L., Ed., Proc. 1st Soil Microcommunities Conf., U.S. Atomic Energy Commission, National Tech. Inform. Serv., Springfield, pp. 95–120. Reynolds, J.W. 1973b. The earthworms of Connecticut (Oligochaeta: Lumbricidae, Megascolecidae and Sparganophilidae), Megadrilogica, 1(7), 1–6. Reynolds, J.W. 1973c. The earthworms of Delaware (Oligochaeta: Acanthodrilidae and Lumbricidae), Megadrilogica, 1(5), 1–4. Reynolds, J.W. 1973d. The earthworms of Rhode Island (Oligochaeta: Lumbricidae), Megadrilogica, 1(6), 1–4. Reynolds, J.W. 1974a. The earthworms of Maryland (Oligochaeta: Acanthodrilidae, Lumbricidae, Megascolecidae and Sparganophilidae), Megadrilogica, 1(11), 1–12. Reynolds, J.W. 1974b. Are oligochaetes really hermaphroditic amphimictic organisms? Biologist, 56(2), 90–99. Reynolds, J.W. 1975a. Die biogeographie van Noorde-Amerikaanse (Oligochaeta) noorde van Meksike — I, Indikator, 7(4), 11–20. Reynolds, J.W. 1975b. The earthworms of Prince Edward Island (Oligochaeta: Lumbricidae), Megadrilogica, 2(7), 4–10. Reynolds, J.W. 1975c. Les Lombricidés (Oligochaeta) de la Gaspésie, Québec, Megadrilogica, 2(4), 4–9. Reynolds, J.W. 1975d. Les Lombricidés (Oligochaeta) des Îles-de-la-Madeleine, Megadrilogica, 2(3), 1–8. Reynolds, J.W. 1975e. Les Lombricidés (Oligochaeta) de Î’Ile d’Orléans, Québec, Megadrilogica, 2(5), 8–11. Reynolds, J.W. 1976a. Die biogeographie van Noorde-Amerikaanse (Oligochaeta) noorde van Meksike — II, Indikator, 8(1), 6–20. Reynolds, J.W. 1976b. A preliminary checklist and distribution of the earthworms of New Brunswick, New Brunswick Nat., 7(2), 16–17. Reynolds, J.W. 1977a. The Earthworms (Lumbricidae and Sparganophilidae) of Ontario, Life Sci. Misc. Publ., Roy. Ont. Mus., 141 pp. Reynolds, J.W. 1977b. The earthworms of Massachusetts (Oligochaeta: Lumbricidae, Megascolecidae and Sparganophilidae), Megadrilogica, 3(2), 49–54 Reynolds, J.W. 1977c. The earthworms of Tennessee (Oligochaeta). II. Sparganophilidae, with the description of a new species, Megadrilogica, 3(3), 61–64.




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Reynolds, J.W. 1977d. The earthworms of Tennessee (Oligochaeta). III. Komarekionidae, with notes on distribution and biology, Megadrilogica, 3(4), 65–69. Reynolds, J.W. 1978a. A contribution to our knowledge of the earthworm fauna of North Dakota, Megadrilogica, 3(8), 148–149. Reynolds, J.W. 1978b. The earthworms of Tennessee (Oligochaeta). IV. Megascolecidae, with notes on distribution, biology and a key to the species in the state, Megadrilogica, 3(7), 117–129. Reynolds, J.W. 1993. On some earthworms from Swaziland (Oligochaeta: Glossoscolecidae, Megascolecidae, Microchaetidae and Octochaetidae), Megadrilogica, 5(1), 1–8. Reynolds, J.W. 1994a. The distribution of earthworms (Annelida, Oligochaeta) in North America, in Advances in Ecology and Environmental Science, Mishra, P.C., Behera, N., Senapati, B.K., and Guru, B.C., Eds., Ashish Publication, New Delhi, India, pp. 133–153. Reynolds, J.W. 1994b. The distribution of the earthworms (Oligochaeta) of Indiana: a case for the post quaternary introduction theory for megadrile migration in North America, Megadrilogica, 5(3), 13–32. Reynolds, J.W. 1994c. Earthworms of Alabama (Oligochaeta: Acanthodrilidae, Eudrilidae, Lumbricidae, Megascolecidae, Ocnerodrilidae and Sparganophilidae), Megadrilogica, 6(4), 35–46. Reynolds, J.W. 1994d. The earthworms of Bangladesh (Oligochaeta: Megascolecidae, Moniligasteridae and Octochaetidae), Megadrilogica, 5(4), 33–44. Reynolds, J.W. 1994e. Earthworms of Florida (Oligochaeta: Acanthodrilidae, Eudrilidae, Glossoscolecidae, Lumbricidae, Megascolecidae, Ocnerodrilidae, Octochaetidae and Sparganophilidae), Megadrilogica, 5(12), 125–141. Reynolds, J.W. 1994f. Earthworms of North Carolina (Oligochaeta: Acanthodrilidae, Komarekionidae, Lumbricidae, Megascolecidae, Ocnerodrilidae and Sparganophilidae), Megadrilogica, 5(6), 53–72. Reynolds, J.W. 1994g. Earthworms of Mississippi (Oligochaeta: Acanthodrilidae, Lumbricidae, Megascolecidae, Ocnerodrilidae and Sparganophilidae), Megadrilogica, 6(3), 17–29. Reynolds, J.W. 1994h. Earthworms of Virginia (Oligochaeta: Acanthodrilidae, Komarekionidae, Lumbricidae, Megascolecidae and Sparganophilidae), Megadrilogica, 5(8), 77–94. Reynolds, J.W. 1995. The status of exotic earthworm systematics and biogeography in North America, in Ecology and Biogeography of Earthworms in North America, Hendrix, P.F., Ed., Lewis Publishers, Boca Raton, FL, pp. 1–28. Reynolds, J.W. 2000a. A contribution to our knowledge of the earthworm fauna of Manitoba, Canada (Oligochaeta, Lumbricidae), Megadrilogica, 8(3), 9–12. Reynolds, J.W. 2000b. A contribution to our knowledge of the earthworm fauna of Newfoundland and Labrador, Canada (Oligochaeta, Lumbricidae), Megadrilogica, 8(2), 5–8. Reynolds, J.W. 2001a. The earthworms of New Brunswick (Oligochaeta: Lumbricidae), Megadrilogica, 8(8), 37–47. Reynolds, J.W. 2001b. The earthworms of South Carolina (Oligochaeta: Acanthodrilidae, Lumbricidae, Megascolecidae, Ocnerodrilidae and Sparganophilidae), Megadrilogica, 8(7), 25–36. Reynolds, J.W. 2002. Additional earthworm (Oligochaeta: Lumbricidae and Megascolecidae) records from Rhode Island, USA, Megadrilogica, 9(4), 21–27. Reynolds, J.W. 2003a. The earthworms (Oligochaeta: Lumbricidae) of Wyoming, USA, Megadrilogica, 9(6), 33–39. Reynolds, J.W. 2003b. First earthworm record from Nunavut, Canada and the second from the Northwest Territories, Megadrilogica, 9(6), 40. Reynolds, J.W. 2003c. A second earthworm species (Lumbricidae) from Nunavut, Canada, Megadrilogica, 9(8), 52. Reynolds, J.W. and Christie, D.S. 1977. Additional records of New Brunswick earthworms, New Brunswick Nat., 8(3), 25. Reynolds, J.W. and Clapperton, M.J. 1996. New earthworm records for Alberta (Oligochaeta: Lumbricidae) including the description of a new Canadian species, Megadrilogica, 6(8), 73–82. Reynolds, J.W. and Cook, D.G. 1976. Nomenclatura Oligochaetologica, a Catalogue of Names, Descriptions and Type Specimens of the Oligochaeta, University of New Brunswick, Fredericton, Canada. Reynolds, J.W. and Cook, D.G. 1981. Nomenclatura Oligochaetologica Supplementum Primum, Catalogue of Names, Descriptions and Type Specimens of the Oligochaeta, University of New Brunswick, Fredericton, Canada.



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Reynolds, J.W. and Cook, D.G. 1989. Nomenclatura Oligochaetologica Supplementum, A Catalogue of Names, Descriptions and Type Specimens of the Oligochaeta, New Brunswick Museum Monograph Series (Natural History), No. 8, Fredericton, New Brunswick, Canada, 37 pp. Reynolds, J.W. and Cook, D.G. 1993. Nomenclatura Oligochaetologica Supplementum Tertium, A Catalogue of Names, Descriptions and Type Specimens of the Oligochaeta, New Brunswick Museum Monograph Series (Natural History), No. 9, New Brunswick, Canada, 93 pp. Reynolds, J.W. and Fragoso, C. 2004. The earthworms (Oligochaeta) of Bermuda, Megadrilogica, 10, in press. Reynolds, J.W. and Guerra, C.A. 1994 Two species of earthworms newly reported from Belize, C.A. (Oligochaeta: Glossoscolecidae and Megascolecidae), Megadrilogica, 5(10), 122–124. Reynolds, J.W. and Khan, M.N. 1999. A contribution to our knowledge of the earthworm fauna of Saskatchewan, Canada, Megadrilogica, 7(12), 81–82. Reynolds, J.W. and Moore, S.M. 1996. Note on the first earthworm record from the Northwest Territories, Canada, Megadrilogica, 6(10), 96. Reynolds, J.W. and Reeves, W.K. 2004. Additional earthworm records (Oligochaeta: Acanthodrilidae, Lumbricidae, Megascolecidae, Ocnerodrilidae and Sparganophilidae) from South Carolina, USA, Megadrilogica, 9(12), 100–111. Reynolds, J.W. and Reynolds, K.W. 1992. Les vers de terre (Oligochaeta: Lumbricidae et Sparganophilidae) sur la rive nord du Saint-Laurent (Québec), Megadrilogica, 4(9), 145–161. Reynolds, J.W. and Reynolds, D.W. 2002a. Primeros datos de lombrices de tierra (Oligochaeta) de la Isla de San Andrés, Colombia, Megadrilogica, 8(6), 21–24. Reynolds, J.W. and Reynolds, D.W. 2002b. Primeros datos de lombrices de tierra (Oligochaeta) de la Isla de Contadora, Panamá, Megadrilogica, 9(1), 1–4. Reynolds, J.W. and Righi, G. 1994. On some earthworms from the Belize, C.A. with the description of a new species (Oligochaeta: Acanthodrilidae, Glossoscolecidae and Octochaetidae), Megadrilogica, 5(9), 97–106. Reynolds, J.W. and Wetzel, M.J. 2004a. Nomenclatura Oligochaetologica Supplementum Quartum, a Catalogue of Names, Descriptions and Type Specimens of the Oligochaeta, Illinois Natural History Survey Special Publication, in press. Reynolds, J.W. and Wetzel, M.J. 2004b. Terrestrial Oligochaeta (Annelida: Clitellata) in North America north of Mexico, Megadrilogica, 9(11), 71–99. Reynolds, J.W., Clebsch, E.E.C., and Reynolds, W.M. 1974. The Earthworms of Tennessee (Oligochaeta). I. Lumbricidae, Bull. Tall Timbers Res. Stn., 17, 1–133. Reynolds, J.W., Jones, A.G., Gaston, K.J., and Chown, S.L. 2002. The earthworms (Oligochaeta: Lumbricidae) of Gough Island, South Atlantic Ocean, Megadrilogica, 9(2), 5–15. Reynolds, J.W., Linden, D.R., and Hale, C.M. 2002. The earthworms of Minnesota (Oligochaeta: Acanthodrilidae, Lumbricidae and Megascolecidae), Megadrilogica, 8(12), 85–99. Scheu, S. and McLean, M.A. 1993. The earthworm (Lumbricidae) distribution in Alberta (Canada), Megadrilogica, 4(11), 175–180. Snider, R.M. 1991. Checklist and distribution of Michigan earthworms, Mich. Academician, 24, 105–114.



of Exotic Earthworms 5 Invasion into North America and Other Regions Samuel W. James Department of Life Sciences, Maharishi University of Management, Fairfield, Iowa, U.S.A.

Paul F. Hendrix Institute of Ecology and Department of Crop and Soil Sciences, University of Georgia, Athens, Georgia, U.S.A.

CONTENTS Introduction ......................................................................................................................................75 Criteria of Exotic Earthworm ..........................................................................................................77 Characteristics of Earthworms That Make Them Invasive .............................................................78 Mechanisms of Earthworm Invasion and the Dynamics of Invading Populations.........................79 How Do Invasive Earthworms Interact with Native Earthworms?.................................................80 How Do Invasive Earthworms Interact with Other Organisms?.....................................................81 Effects of Exotic Earthworms Invasions on Ecosystem Processes.................................................82 What Can be Done about Exotic Earthworm Invasions? ...............................................................83 Acknowledgments ............................................................................................................................86 References ........................................................................................................................................86

INTRODUCTION Invasions of earthworms and their redistribution around the globe involve only a small proportion of the overall diversity of earthworms, but the phenomenon is very widespread. It is safe to say that few places occupied by humans are free of introduced exotic earthworms. Those few areas would be environments that are inhospitable to earthworms because of either climate or soil characteristics; otherwise, it is almost certain that there will be foreign earthworms in most soils affected by human activity. In this chapter, we discuss the timing and extent of earthworm movements, how and when they came to the attention of scientists, and how to be sure an earthworm is exotic in a particular location. Then, we explore several ecological aspects of exotic earthworm species and their invasions into new habitats and regions. The ecological aspect includes the general biological features contributing to the ability of an earthworm species to be invasive or simply to be transported inadvertently by humans; the dynamics of invasions; the biotic interactions of exotic earthworms with other groups of organisms, including native earthworms; and the potential for ecosystem-level effects of these invasions.



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It is certain that humans have been aware of earthworms for a very long time, yet only in the past several millennia have people had the motivation or wherewithal to alter global distributions of earthworms in any ecologically significant way. This required the birth of agriculture and thus an incentive to transport live plant materials, perhaps with or in soil, from one place to another. It may be speculated that the Polynesian peoples, or other seafaring groups with some reliance on agriculture, were among the first to cause the long-distance transport of earthworms, although there is no reason to suspect them of doing so intentionally. As transportation technology advanced and trade routes, road networks, and convenient means of moving heavy loads over long distances became readily available in Europe and Asia, earthworms were likely to move as well. To be sure or suspect that a species of earthworm or any other organism is outside its natural habitat range, there has to be a concept of natural range and some knowledge of the diversity and phylogenetic relationships of the organisms concerned. Otherwise, there is no basis for inferring that an occurrence at a particular site is unnatural; after all, until the late 19th century A.D., any such situation could be explained as the will of the Creator. Even well into the post-Darwin age, describers of new earthworm species found outside what is now believed to be the natural ranges of the species often used the foreign place names as specific epithets. There are numerous cases of earthworm species that were either first discovered out of their indigenous ranges or were given synonyms based on specimens collected outside their natural range (Reynolds and Cook 1976). For example, Amynthas gracilis Kinberg 1867 is an East Asian species that is found commonly well out of its normal range and in Hawaii was given the junior synonym A. hawayanus Rosa 1891. On the other hand, certain more familiar species of European Lumbricidae (virtually all earthworm taxonomists were European until the 20th century) kept turning up in odd places, such as Australia (Blakemore 1999) and New Zealand (Lee 1959), such that by 1900, it was generally believed that certain earthworm species had been widely distributed by human activity (e.g., Michaelsen 1900); these are collectively referred to as peregrine species. Once some basic outlines of earthworm taxa, including families and their generic distributions, were worked out (1895 to 1930), the extent of artificial earthworm distributions could be much better appreciated. Because certain earthworm species turn up in unexpected places, early observations often considered that native indigenous earthworms of many areas were declining in numbers and species, and that exotic earthworms were increasing in abundance. Eisen (1900) observed the phenomenon in California, and in the central United States, Smith (1928) noted a transition from an abundance of the native Diplocardia communis Garmann in 1888 to domination by Lumbricus terrestris L. over the period 1900 to 1925. Significantly, this occurred in urban lawns and gardens, so the Diplocardia had survived a habitat conversion. Much later, Ljungstrom (1972) noted replacement of the South African native earthworm fauna by exotic species. The mechanisms of replacement of native earthworm species by exotic species are complex, and there has been little experimentation to identify the key processes involved. These mechanisms could include the intolerance of the native earthworm to altered habitats, a loss of key biotic relationships present in intact ecosystems, competition pressures from exotic species, and an inability to reestablish populations after partial recovery of ecosystems (Stebbings 1962; Kalisz and Wood 1995). Earthworms are still traveling, although recent increased stringency of border controls may have reduced international traffic to some extent. Gates (1982) received thousands of specimens that had been intercepted at the U.S. borders over several decades in the 1900s. The result of the many years of earthworm transport is global homogenization of earthworm communities, in agricultural and urban lands, modified by climate conditions. The U.K. is now populated by the same species of Lumbricidae that were present in the rest of glaciated Europe. The same set of species, for the most part, occupy soils in the temperate zone of North America and the cooler regions of Australia, New Zealand, North Africa, South America, and South Africa and are part of a mixed earthworm fauna in temperate East Asia. Aporrectodea spp. have been seen in irrigated highway rest areas in the Humboldt Sink region of Nevada, a cold desert with salt alkaline soils, where they © 2004 by CRC Press LLC


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must have arrived with nursery stock or other plant materials used in landscaping. Species of Lumbricidae are present in Costa Rican montane forests at an elevation of 2000 m near Heredia and in similar habitats in Venezuela. Significantly, the peregrine Lumbricidae are now the only earthworms currently present in large areas of glaciated North America and Eurasia, where they are modifying soils and litter decomposition dynamics, but this subject is discussed below. A later wave of immigrant earthworms from temperate Asia (probably Japan) is now progressing through North American soils. The most important of these is Amynthas hilgendorfi Michaelsen 1892, which may be a range of parthenogenetic morphs. In tropical climates, a different set of exotic species is now distributed globally, dominated by the ubiquitous Pontoscolex corethrurus Müller 1856, a member of the South American family Glossoscolecidae. This species is believed to have originated in northeast South America, where the rest of its congenitors are found (Righi 1984). This earthworm is now abundant in all tropical areas where rainfall is adequate to support earthworm activity for at least a few months each year. It lives in lowland evergreen tropical forests up to cloud forests along elevational transects in high rainfall areas and can maintain populations in seasonally tropical dry forests, including some with xerophytic vegetation. It also prospers under agricultural conditions, including pastures, tree plantations, row crops, and paddies (along the margins, not in flooded soils). Reforestation programs using root-ball planting stock provide another means of dispersal of these species, and in many places in Southeast Asia and Fiji, only the disturbance of logging and the probable movement of P. corethrurus on heavy equipment was required for virtual elimination of the native species and introduction and establishment of this exotic species. Some other widespread tropical peregrine earthworm species are Dichogaster bolaui, Dichogaster affinis, Eudrilus eugeniae, Drawida barwelli, Pithemera bicincta, Perionyx excavatus, Amynthas corticis, and Polypheretima elongata (Fragoso et al. 1999). Of these, the most important is probably the last because it is capable of surviving in a broad range of environmental conditions and has been blamed for degradation of soil structure in some agricultural settings (Shah and Patel 1978). Some of the species in this list are used in vermicomposting and so are maintained in cultures even where they cannot survive ambient winter temperatures.

CRITERIA OF EXOTIC EARTHWORM We have mentioned briefly some criteria for determining whether an earthworm is an exotic species. Essentially, it requires broad knowledge of the global or regional distribution of the larger taxon to which the species belongs. Thus, if outside South America and some neighboring areas (Central America and a few Caribbean islands), a glossoscolecid such as P. corethrurus is clearly an exotic species because that family is otherwise confined to South America and its environs (Righi 1972; Fragoso et al. 1995). Similarly, a species of the exclusively African family Eudrilidae would be exotic on any other continent, and even within Africa it is exotic north of the Sahara and south of the Kalahari deserts. The problem is harder when the larger taxon has a wider global distribution, such as the Lumbricidae, with species native to Europe and North America and a known direct land connection prior to the opening of the Atlantic Ocean. In this case, the debate has raged longer (Omodeo 1963) but was settled ultimately by the observation that the two genera occurring in North America are completely absent from Europe, and there are no endemic North American species of any, otherwise European, genera (Gates 1982). Furthermore, the same members of European lumbricid genera that are found in North America are also found in temperate zones of other continents. Looking in more detail at earthworm distributions in Europe, it is clear that the peregrine species are the only earthworms in the northern regions of the continent, whereas in southern Europe, a very diverse earthworm fauna exists. Thus, the peregrine species are only a small subset of the total, a pattern that is repeated in all higher earthworm taxa containing peregrine species.



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Some of the earthworm distributions in East Asia are more difficult to assess because numerous Amynthas and Metaphire species have been transported, perhaps for hundreds of years, and concomitant habitat alterations have all but eliminated any chance of locating the ancestral homes of these peregrine species. Some species are often found mainly in anthropogenic habitats, and others are found only in undisturbed or relatively undisturbed soil systems. Without any other data, it can be determined that certain earthworm species are at least potentially peregrines, but it may not be possible now to determine their original ranges (see Chapter 3, this volume).

CHARACTERISTICS OF EARTHWORMS THAT MAKE THEM INVASIVE Four primary features of earthworms are suggested as important for their ability to travel and establish populations in new areas: a tolerance of environmental variability; suitable ecological niches; high reproductive potential; and an appropriate reproductive system, which may be biparental or uniparental (Barois et al. 1999; Fragoso et al. 1999). To be transported successfully to other regions, an earthworm species or its cocoons must be able to survive some degree of disturbance, perhaps including fluctuations in temperature and moisture levels, and be able to survive in a new habitat with different soil conditions, novel sets of soil organisms, and potentially unaccustomed seasonal patterns of temperature and moisture. The simplest case is the transport of a body of soil containing the earthworms or cocoons; the larger the body of soil is, the greater its degree of insulation from environmental changes during the movement. It would be expected that large amounts of soil would be least challenging to an earthworm species that lives in it but also less likely to occur than the movement of smaller quantities of soil. Therefore, the most successful earthworm travelers will be those with the maximum degree of tolerance for adverse soil conditions. Among the known tolerance mechanisms of earthworms is their ability to enter dormancy in response to higher temperatures, low soil moisture, or both (Lee 1985). Many peregrine species of Lumbricidae, such as the Aporrectodea species, which are common throughout the world, have this ability. Similarly, the ubiquitous tropical peregrine species P. corethrurus can become dormant in drought conditions. On the other hand, Diplocardia species in the central United States can enter dormancy during drought periods, but none of these species is known to be peregrine, although several do well in moderately disturbed anthropogenic habitats such as lawns and gardens. The only obvious difference suggesting why the Diplocardia species may not have traveled with human aid is the physical robustness of construction among the Lumbricidae, which appears to be greater than that of Diplocardia spp. Yet, robustness is hard to quantify and perhaps even harder to put to a meaningful test. On the other hand, some Diplocardia species commonly collected for fishing bait can survive soil temperatures of 35 °C in small containers, which is invariably fatal to most peregrine Lumbricidae. Bouché (1977) outlined several major aspects of earthworm behavior and morphology correlated with ecology and defined the ecological categories now in wide use, that is, epigeic, endogeic, and anecic species. Epigeic species are those inhabiting superficial organic matter accumulations and the soil-litter interface and are typically small bodied, dark colored, and capable of rapid movements. Many of the common vermicomposting species fall into this category. Their natural food sources are short lived and widely scattered, so they produce large numbers of offspring or may even be parthenogenetic and rely on dispersal to locate new resource patches. Endogeic earthworm species live and feed in the mineral soil layer, are usually lightly pigmented or unpigmented, range in size from small to very large, do not move quickly, and have lower reproductive rates. Further division of endogeic species has been made (i.e., polyhumic, mesohumic, and oligohumic) based on the relative age, concentration, and location of organic matter they utilize as food. The polyhumic species somewhat resemble epigeic species in coloration but are capable




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of living in mineral soil. Oligohumic species are those that feed mostly on greatly modified organic matter in the soil and are virtually always unpigmented. Most anecic species maintain deep burrows from which they emerge to feed on surface organic matter. They usually are large bodied, have dark anterior pigmentation, and have lower reproductive rates. From this quick overview of earthworm ecological categories, it might be guessed that the epigeic species are those most likely to be invasive, but this is not entirely true because some of their habitat requirements can be restrictive. Many invasive species are endogeic, and these are primarily of the poly- or mesohumic types. Some anecic species, such as L. terrestris, are also invasive. The reproductive potential of a species also plays some role in its potential to be invasive, although it probably is less important than its ecological relations, which are intimately related to the life history strategy of the particular species (r vs. K selection, for example). A more obviously important factor in the ability of earthworms to colonize new habitats successfully is the nature of the reproductive system. Although most species of earthworms are obligately outcrossing hermaphrodites, some use other options. Some species may self-fertilize, and others are parthenogenetic. In either of these cases, reproduction is or can be uniparental as opposed to biparental. A single uniparentally reproducing earthworm can found a new population, and it is clear that this has been important in establishing earthworms in new areas. For instance, the invasive Octolasion species are parthenogenetic, as are many of the invasive Amynthas and Microscolex species and probably P. corethrurus. Uniparental reproduction, although not necessary or sufficient to achieve successful invasiveness, is certainly a useful property for this purpose.

MECHANISMS OF EARTHWORM INVASION AND THE DYNAMICS OF INVADING POPULATIONS We mentioned some of the mechanisms of earthworm invasions, especially those directly involving human activity and the transportation of earthworms to new locations. In this section, we review the available knowledge of earthworm invasion dynamics in earthworm-free habitats (typically, higher latitudes subject to recent glaciation). There are still some unresolved questions about situations in which an indigenous earthworm fauna is still present on a site where exotic species have been introduced. Invasions of agroecosystems by exotic earthworms are virtually the general rule, particularly in North America, because native species capable of tolerating a less-buffered soil environment and the frequent soil disturbances are uncommon. It is fair to say that the diversity of agriculturetolerant earthworms is to the total diversity of earthworms as the diversity of cultivated plants is to the total diversity of plants. If it is not quite true yet, it seems likely that soon there will be two or three major earthworm groups operating in temperate, subtropical, and tropical climate zones. For this reason, and because the vast majority of earthworm research on agroecosystems has dealt with exotic species, readers are referred to reviews of earthworm ecology in agroecosystems (Edwards and Bohlen 1996; Baker 1998; Hendrix 1998; Lavelle et al. 1999). Here, we confine discussion to earthworms in nonagricultural land. In the temperate deciduous and mixed forests of North America, several research groups have recorded profound changes in the structure of soils and the forest floor following the introduction of exotic species of earthworms. The first publication on this subject was by Nielsen and Hole (1964), who noted the conversion of podzols to a mixed mineral-humus soil in New Brunswick, Canada. These authors saw nearly total destruction of forest floor litter, leaving only the most recent leaf fall on the ground, in several locations in Michigan and Iowa. Similar situations have been reported or are under investigation in Minnesota (Alban and Berry 1994; Hale et al. 2000); New Jersey (Kourtev et al. 1999); Rhode Island, Pennsylvania, and New York (Steinberg et al. 1996; Burtelow et al. 1998); Alberta, Canada (Scheu and Parkinson 1994;



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McLean and Parkinson 1997, 2000a,b); and in North American natural grasslands (Callaham and Blair 1999; Callaham et al. 2001). In Minnesota, the invasion by exotic earthworms consisted of several species arriving in successive invasion fronts. First came the epigeic litter-dwelling species, followed by polyhumic endogeic species and then slower-moving anecic and endogeic species. This phenomenon of successive waves of invasion by earthworms depends on the presence of diverse ecological types of earthworm, so it is not necessarily going to apply to all places. However, it demonstrates that an earthworm invasion is not a simple monolithic process, and that it may require several years to determine the outcome of an invasion of a single site. The species content of invasive waves are in accordance with what we might predict given the life histories, ecology, and reproductive potentials of the various ecological categories of earthworms. On the other hand, sometimes the results of the initial invasive wave, such as that of epigeic species (Dendrobaena octaedra), have proven different in places like Minnesota (Gundale 2002; Hale et al. 2000) and Alberta (Scheu and Parkinson 1994; McLean and Parkinson 1997). In the former area, little impact of the invasion on soil horizons was noted, whereas in the latter, there were significant effects on the soil strata. In Minnesota, the main effects of invasive earthworms on soil organic horizons occurred after the arrival of Lumbricus rubellus in the second wave of invasion. In some New England forests, the arrival of A. hilgendorfi is now causing total destruction of the organic horizon in spite of centuries of opportunity for European earthworms to do the same. When earthworms arrive in a forest with soils with thick organic horizons but previously devoid of earthworms, there is a large and readily available supply of food. Years later, the amount of organic matter per square meter has probably diminished significantly or, if not, it has been transformed profoundly and mixed with the mineral soil. In either case, negative consequences would be expected for the early invading species that took advantage of the mass of surface organic matter, with more favorable conditions occurring for endogeic species. Anecic species might be less affected, except as small juveniles, because the larger earthworms can pull surface organic material into their burrows. Nevertheless, populations may be limited by food availability at some point because the entire litter fall is usually consumed annually. Such long-term changes in the total food supply available should mean that populations of some earthworm species would go through peaks and declines during the course of the invasion and then reach something approximating a steady state or equilibrium, because the earthworms have to live off current food income rather than the organic capital accrued prior to their arrival.

HOW DO INVASIVE EARTHWORMS INTERACT WITH NATIVE EARTHWORMS? When exotic earthworm species arrive at a site already occupied by a native earthworm fauna, there could be several other things occurring. We have noted the replacement of native earthworm species by exotic species in Illinois, California, and South Africa, but this was mainly in urban and agricultural areas, so it is a different situation from similar replacements in undisturbed habitats or in less-disturbed systems such as second-growth forests, where earthworm invasions are unlikely (Kalisz and Dotson 1989). In some disturbed habitats, native and exotic species coexist (Fragoso et al. 1995, 1999; Callaham and Blair 1999; Bhadauria et al. 2000); in others, the exotic species dominate. Stebbings (1962) suggested that exotic earthworm species may be out-competing the native species on some forested sites in the central United States, but Kalisz and Wood (1995) suggested that replacements might not occur in at least some minimal area of undisturbed habitats. Lavelle and Pashanasi (personal communication) reported that P. corethrurus did not invade adjacent primary Peruvian forests from agricultural land, where it was well established. The primary forest had an endemic earthworm fauna that was absent from the land that was converted to agriculture. Dalby et al.




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(1998) reported resistance to invasion by exotic earthworm species in Australian forests inhabited by native species. On the other hand, we have observed that the species Diplocardia riparia which inhabits the riparian zone was absent from a Skunk River, Iowa, riverbank habitat near public access points, and that the Asian species Amynthas hupeiensis (used as fish bait) was abundant. However, after prolonged inundation during the summer floods of 1993, populations of A. hupeiensis were apparently wiped out, and populations of D. riparia recovered. In this example, the native species was better adapted to the natural disturbance regime of the riparian zone, but under current conditions of flood control by reservoirs upstream (decreased disturbance frequency or intensity), the exotic species can dominate. A combination of factors is probably involved in the outcome of earthworm invasions when a native earthworm fauna is already present (Hendrix and Bohlen 2002). Habitat destruction or disturbance is almost always cited as a precursor to earthworm invasions, but it is difficult to say whether it is a necessary prerequisite. Appropriate experiments have not been done to determine the outcome of earthworm introductions to areas of primary vegetation with an intact native earthworm community. Parallel experimental introductions could be made to primary vegetation soils where earthworms have been removed and in sites with populations of native earthworms intact. A related question is whether the rate of earthworm expansion into a new area is slower (but greater than zero) when native species are present than when they are absent. The reduction or elimination of native earthworm species is another factor or prerequisite to invasion, but it is difficult to say if it is a necessary factor for successful earthworm invasions; most examples suggest that it certainly helps (Kalisz and Wood 1995). The only factor clearly necessary for successful establishment is the arrival of the exotic species, without which there can be no invasion.

HOW DO INVASIVE EARTHWORMS INTERACT WITH OTHER ORGANISMS? Hawaii, which had no earthworms prior to human colonization, is now occupied by a variety of exotic earthworm species (Nakamura 1990). In a massive invasional meltdown (Simberloff and von Holle 1999), the invasive nitrogen-fixing tree Myrica faya is increasing the amounts of nitrogen cycling in the ecosystems and increasing earthworm populations by a factor between 2 and 10, depending on site (Aplet 1990). In addition, feral hogs, when foraging for earthworms, are ripping up the forest floor, creating more open sites for germination of the seeds of an exotic flora. The best that can be said of the Hawaiian situation is that it creates an opportunity for humans to hunt feral pigs. There are several recorded examples of invasive earthworms altering the composition of soil microbial and faunal communities. For example, McLean and Parkinson (2000a) reported that populations of D. octaedra in pine-forest floors in Alberta significantly altered microfaunal abundance and diversity in the organic horizon and in the mineral soil, increasing the number of the faster-growing microinvertebrate taxa. Similarly, soil microarthropod communities were changed by the presence of P. elongate in pastures in Martinique (Loranger et al. 1998) and by that of D. octeadra in pine forests in Alberta (McLean and Parkinson 2000b). In both instances, there were positive and negative correlations between earthworm populations and measures of microarthropod diversity and abundance; these effects were attributed to changes in physical structure of the soil and organic layers. In Minnesota, perturbation by introduced earthworms was responsible for the reduction of populations of the endangered fern Botrychium mormo (Gundale 2002), and interactions between effects of earthworms and deer browsing dramatically reduced the forest-floor vegetation (Hale et al. 2000). We have observed a large gallery-forming beetle larva in the thick, forest organic horizons



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with no earthworms at the University of Michigan Biological Station. Adjacent earthworm-populated areas seem to have no place for this beetle to live. If earthworm introductions were the only thing that changed, there would be little cause for concern, but many interactions and ecosystem processes can be altered profoundly, sometimes with clear negative effects (Hendrix and Bohlen 2002).

EFFECTS OF EXOTIC EARTHWORMS INVASIONS ON ECOSYSTEM PROCESSES In addition to issues concerning the population and community dynamics of exotic species of earthworms, there are questions about the impacts of earthworm invasions on ecosystem processes. Of particular importance are soil processes mediated by biological activities (e.g., litter decomposition, nutrient mineralization), which may be susceptible to the intensified earthworm activities characteristic of earthworm invasions. Although exotic earthworm invasions have been reported for over a century, quantitative studies of their effects on soils have been much more recent. In North America, invasions by European lumbricids and Asian megascolecids have been reported north of Pleistocene glacial margins in Canada and the United States, that is, in areas previously devoid of earthworms. One early study by Buntley and Papendick (1960) described a large area in eastern South Dakota (approximately 3400 km2) where the soil profile, of a chernozem on Pleistocene deposits, had been disrupted by earthworms. Soil horizon boundaries were obliterated, and the physical structure of the soil consisted of casts and filled earthworm burrows to a depth of 90 cm. Organic carbon and nitrogen, CaCO3, and clay distributions were also changed because of vertical translocation of these substances. The earthworm species involved was not indicated, but the area was probably previously devoid of native earthworms. However, Gates (1967) reported that the species in question was L. terrestris, which could have been introduced less than 100 years earlier with the first European settlements in the area. He cited several examples of early settlers transporting fruit trees and other horticultural materials during the westward migrations of the 19th century. In Idaho, there was even an attempt to establish exotic earthworms into soils for use as fishing bait because no indigenous species of earthworms were found in the region. The time required for the extensive alteration of soils observed in South Dakota was probably less than 100 years. More recent studies in New Brunswick and Minnesota demonstrated that only a few years are needed for transformations of mor horizons into mull horizons in forests that are invaded by several lumbricid species (Langmaid 1964; Alban and Berry 1994). Current research in Minnesota (Hale et al. 2000) and Alberta (Migge et al. 2003) suggest that these lumbricid invasions tend to proceed across the landscape in sequential waves, as noted in the section on mechanisms of invasion. In the Minnesota instance, it began with D. octaedra, which consumed the F and H layers; followed by L. rubellus and Aporrectodea spp., which mixed the organic and mineral horizons; and finally by L. terrestris, which drew recent litter into its burrows and produced middens and casts on the soil surface. The final result of this multistage invasion was a compacted, bare mineral soil surface covered only by recent litterfall. Impacts of the loss of the O-horizon on plant and animal populations in the forest floor have been reported (e.g., Maerz et al. 2001; Gunndale 2002). Intensive experimental studies of D. octaedra and Octolasion lacteum invasions in aspen and pine forests in the Rocky Mountains of Alberta showed significant changes in structures of microbial communities, decreases in microbial biomass, and increases in nutrient leaching rates in the Ohorizon in addition to physical disruptions of the soil profile. Declines in the total organic matter content were also noted in response to the highest earthworm population densities (Scheu and Parkinson 1994; McLean and Parkinson 1997, 2000a,b). Similarly, studies of undisturbed hardwood-forest patches in New York that were invaded by a variety of lumbricids revealed the




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elimination of the forest floor litter, reductions in carbon storage in soil, changed carbon:nitrogen ratios, and reductions in fine-root biomass in the upper mineral soil (Bohlen et al. 2003a; Fisk et al. 2003). The impacts of earthworm invasions on soil carbon dynamics in previously cultivated forest patches were less, emphasizing the importance of the site history as a determinant of earthworm effects of invasions on soil processes (Bohlen et al. 2003b). Interestingly, soil phosphorus fractions were affected differentially by different earthworm species. The anecic species L. terrestris increased the total phosphorus in surface soils by transporting parent material from deeper soil layers, and the epi-endogeic species L. rubellus increased the extent of exchangeable phosphorus and phosphorus leaching by consuming organically enriched surface materials and producing phosphorus-enriched castings (Suárez et al. 2003). Such results demonstrate the difficulty in making generalizations about effects of earthworm invasions. Further research is needed under a wider range of climatic, edaphic, and land-use conditions and a larger number of invasive earthworm species. Models of earthworm effects on soil process dynamics (e.g., Chertov and Komarov 1997) may be useful in the search for broad-scale patterns of earthworm invasions. Exotic earthworm invasions also have been reported in areas inhabited by native earthworms, but their impacts on ecosystem processes appear to depend on the previous disturbance history of the site, earthworm invasion pressure, and the degree to which the native earthworm assemblage is intact (Figure 5.1). In highly disturbed soils, native earthworm populations are often reduced, and invasions by the typical anthropochore species usually have significant effects on soil processes. Observations have been made worldwide in agricultural and pastoral ecosystems, where introduced European lumbricids have modified soil structure, rates of organic matter decomposition, nutrient dynamics, and in some cases plant productivity, for example, in reclaimed polders in the Netherlands (Hoogerkamp et al. 1983); grasslands in New Zealand and California (Stockdill 1982; Winsome 2003); and cropping systems in Australia and the United States (Parmelee et al. 1990; Baker 1998). Similar impacts of invasive earthworms have also been reported in at least moderately disturbed natural areas where native earthworm species are still present but probably not at natural abundances, for example, in California chaparral (Graham and Wood 1991) and tropical forests (Fragoso et al. 1995; Liu and Zou 2002). Where native and exotic earthworm species coexist, the magnitude of their effects on soil processes may be determined by the relative abundance of the various species of earthworms, ecological strategies, and environmental fitness of the dominant species. James (1991) suggested that native earthworms were usually better adapted to local soil and climatic conditions and hence could maintain longer periods of activity and have greater effects on nutrient dynamics in tallgrass prairie soils than could invading European lumbricids. Lachnicht et al. (2002) reported that native Estherilla spp. and the exotic P. corethrurus coexisted by partitioning the soil volume physically in microcosms containing forest floor and mineral soil from tabonuco forests in Puerto Rico. Interactions between the two species reduced the impact of P. corethrurus on carbon and nitrogen mineralization rates. The dynamics and impacts of earthworm invasions in undisturbed ecosystems in which soil, vegetation, and indigenous earthworm assemblages are intact have not been well studied. In such instances, there may even be some degree of biotic resistance to earthworm invasions; hence, the impacts on ecosystem processes in these situations may be different from those in areas that were previously devoid of earthworms. This possibility needs further research.

WHAT CAN BE DONE ABOUT EXOTIC EARTHWORM INVASIONS? Many exotic earthworm species are now naturalized in areas beyond their place of origin, notable examples being European lumbricids in temperate regions worldwide and P. corethrurus throughout the tropics (Reynolds 1994; Fragoso et al. 1999). Although humans and their disturbed habitats are



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INITIAL STATE

Disturbance

A

Severe

INTERMEDIATE STATE

Exotic Invasion

Native Earthworms Eliminated

Successful

CURRENT STATE Exotic Earthworms Exclusively

Successful "Pristine" System (Native Earthworms B Exclusively)

Moderate

Native Earthworms Diminished

1 2

Successful?

Native and Exotic Earthworms Coexisting

Successful?

C

Minimal

Native Earthworms Exclusively

1 2

Unsuccessful

Native Earthworms Exclusively

FIGURE 5.1 Hypothesized pathways of exotic earthworm invasions in ecosystems inhabited by native earthworms. Pathway A is the extreme case leading to exclusively exotic assemblages, as often observed with anthropochorous earthworms in agricultural soils; the same outcome may occur under less-severe disturbance but perhaps with more aggressive exotic invaders via pathway B-1. Pathways B-2 and C-1 lead to the sometimes observed co-occurrence of native and exotic species through varying levels of habitat disturbance and invasion intensity; pathway C-1 suggests direct competitive displacement of native species by exotic species. Whether co-occurrence is a stable condition or whether native species or exotic species maintain dominance is an interesting long-term question, and hence the question marks are shown for successful invasion on these pathways. Pathway C-2 suggests that native earthworm assemblages under minimally disturbed, native conditions are resistant to invasion by exotic species. The alternative is best represented by pathway C-1, by which forest fragmentation, for example, may foster exotic invasions without direct habitat disturbance. (Modified from Hendrix et al. 2004.)

the cause, these peregrine earthworm distributions must still be considered expansions of range for these species, albeit at very rapid rates in ecological and geological time. The important issues now are how, at local-to-regional scales, the spread of invasive species into areas where they are not wanted (e.g., remote or sensitive ecosystems) can be impeded and how, at national-to-continental scales, introduction of new invasive earthworm species can be prevented. The management of earthworm populations, whether invasive or not, has received considerable attention in the context of agriculture and organic waste management, and there are numerous cases of successful outcomes of such management, for example, enhanced plant productivity or accelerated decomposition of organic wastes (Lee 1995; Edwards 1998; Lavelle et al. 1999). Indeed, there probably would be no incentive to prevent or regulate earthworm introductions for such purposes. The management of earthworm populations in the context of mitigation of invasions has only recently emerged as a topic in need of development after it was brought to light by some of the reports noted here of adverse effects in forested ecosystems. There are at least two approaches to the management of invasive exotic earthworms. The first is essentially to provide no management at all, allowing invasions to run their course and assuming that, over time, invaded ecosystems will reach a new “equilibrium” under the influence of the newly reassembled biotic community. This approach accepts any changes in soil characteristics, biogeochemical cycling rates, and above- and belowground biotic communities that are likely to occur. In fact, this approach is in effect by default, in many areas where earthworm invasions are in progress and where the changes are witnessed as they occur, as in some of the experimental studies described here. Additional chronosequence studies, which compare sites at various stages of earthworm invasion from the beginning to equilibrium, might reveal a long-term progression in such changes and whether the ultimate outcomes are acceptable in particular regions. For example, © 2004 by CRC Press LLC



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forests in central to northern European countries may represent the very long-term postglacial end points of lumbricid invasions; similar situations might occur in tropical ecosystems (e.g., Fragoso et al. 1999). Such studies should help create predictive models of earthworm invasion dynamics, which would be useful in developing improved management strategies. A second approach to managing earthworm invasions is human intervention. It is a well-known tenet in invasion biology that it is much easier to prevent an invasion than to stop one in progress. Therefore, the first step is the one most often used by governments, that is, interception and quarantine at the borders. As reviewed by Hendrix and Bohlen (2002), some countries have specific regulations concerning the importation of earthworms; others do not. Canada, for example, allows earthworm imports only from the Netherlands (L. terrestris) and the United States (i.e., only species that are known already to occur in Canada). This represents a “clean-list” or “guilty-until-proveninnocent” approach to invasive species control (Reichard and Hamilton 1997; Mack et al. 2000). The converse or “innocent-until-proven-guilty” appears to be the default approach followed by many nations, including the United States, where current regulations regarding earthworm imports are based on the Federal Plant Pest Act, under which the U.S. Department of Agriculture Animal and Plant Health Inspection Service (APHIS) controls imports of soils that might carry pathogens. In the absence of any pathogens, there are no specific considerations of earthworms as invasive organisms, although this situation may be changing as APHIS develops new guidelines (Hendrix and Bohlen 2002). There is a rich literature base on the invasion biology of plants and insects of economic importance (Simberloff 1989; Mack et al. 2000), but invasions by soil invertebrates have not been well studied (Ehrenfeld and Scott 2001). There are some precedents in the Formosan termite, fire ant, and Japanese beetle invasions in the United States and terrestrial flatworm invasions in Europe and Australia; we may at least learn what not to do from these case studies. However, invasions by more cryptic and less-mobile earthworms appear to be qualitatively and quantitatively different from those by most other invertebrates and may be more similar to plant invasions than to those of other animals (di Castri 1991). Invasions by terrestrial planarians that attack earthworms (Boag and Yeates 2001) may be the best model for understanding and controlling earthworm invasions because of similarities between these groups with respect to ecology, life history, and modes of transport. Control or mitigation of earthworm invasions after they occur has received very little attention, probably because it is a daunting proposition. As anyone knows who has sampled earthworm populations in the field, removing them from soil is often very destructive to soils and almost never 100% effective, even in small plots. Removal of invasive earthworms over large areas is probably not feasible. Therefore, the best approach may be containment of exotic earthworm populations to areas where they already exist or, at least, a reduction of rates of dispersal from such areas into surrounding ecosystems in which the earthworms may have adverse effects. Physical barriers, such as buffer zones of unsuitable habitat around agricultural sites, might impede earthworm migration. Also, simple practices, such as not dumping fishing bait on stream banks or cleaning horse hooves or off-road equipment tires before transporting them into remote areas, might reduce the likelihood of earthworm invasions. In addition to experimental studies on the effectiveness of preventive measures, public awareness campaigns, e.g., those by conservation and outreach groups such as Minnesota Worm Watch (http://www.nrri.umn.edu/worms) could help reduce the flow of propagules of earthworms as well as those of other exotic species. Ultimately, regulations at state, provincial, or regional levels may be needed to prevent the transport of exotic earthworms into remote or particularly sensitive areas. Finally, as discussed by Hendrix and Bohlen (2002), more basic knowledge is needed in terms of the natural history and ecology of invasive earthworms, both in their native habitats and in ecosystems in which they have invaded and had significant impacts. Which factors control earthworm populations under natural local conditions? Which characteristics of the organisms and of the habitats have contributed to successful invasions and to earthworm invasion failures? How © 2004 by CRC Press LLC


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important is biotic resistance, which may occur in ecosystems inhabited by native earthworms or other native competitors and predators? Are native species competitive with aggressive exotic species under native conditions? Is habitat disturbance a prerequisite to invasion? Case studies and experimental manipulations are needed to answer these and other pertinent questions. In addition, there is still a need for basic survey and taxonomic work to assess the diversity and distribution of earthworm species both in their native habitats and in new areas where they may become invasive.

ACKNOWLEDGMENTS This work was supported by grant DEB 0236276 from the National Science Foundation to the University of Georgia. We are grateful to colleagues at the Seventh International Symposium on Earthworm Ecology, Cardiff University, Wales, U.K., in 2002 for useful discussions of the topics covered in this chapter.

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Edwards, C.A. and P.J. Bohlen. 1996. Biology and Ecology of Earthworms, 3rd ed., Chapman & Hall, London. Eisen, G. 1900. Researches in American Oligochaeta, with especial reference to those of the Pacific Coast and adjacent islands, Proc. Calif. Acad. Sci., II:85–276. Fisk, M.C., T.J. Fahey, P.M. Groffman, and P.J. Bohlen. 2004. Earthworm invasion, fine root distributions and soil respiration in north temperate forest, Ecosystems, in press. Fragoso, C., I. Barois, and S. James. 1995. Native earthworms of the north neotropical region, in Hendrix, P., Ed., Earthworm Ecology and Biogeography in North America, Lewis Publishers, Boca Raton, FL, pp. 67–115. Fragoso, C., J. Kanyonyo, A. Moreno, B.K. Senapati, E. Blanchart, and C. Rodriguez. 1999. A survey of tropical earthworms: taxonomy, biogeography and environmental plasticity, in Lavelle, P., L. Brussard, and P. Hendrix, Eds., Earthworm Management in Tropical Agroecosystems, CABI Publishing, New York, pp. 1–26. Gates, G.E. 1982. Farewell to North American megadriles, Megadrilogica, 4:12–77. Graham, R.C. and H.B. Wood. 1991. Morphologic development and clay redistribution in lysimeter soils under chaparral and pine, Soil Sci. Soc. Am. J., 55:1638–1646. Gundale, M.J. 2002. Influence of exotic earthworms on the soil organic horizon and the rare fern Botrychium mormo, Conserv. Biol., 16:1555–1561. Hale, C.M., L.E. Frelich, and P.B. Reich. 2000. Impacts of invading European earthworms on understory plant communities in previously worm-free hardwood forest of Minnesota, Abstr. Ecol. Soc. Am., 85:112. Hendrix, P.F. 1998. Earthworms in agroecosystems: a summary of current research, in Edwards, C., Ed., Earthworm Ecology, St. Lucie Press, Boca Raton, FL, pp. 259–272. Hendrix, P.F. and P.J. Bohlen. 2002. Exotic earthworm invasions in North America: ecological and policy implications, Bioscience, 52:801–811. Hoogerkamp, M., H. Rogaar, and H.J.P. Eijsackers. 1983. Effect of earthworms on grassland on recently reclaimed polder soils in the Netherlands, in Satchell, J.E., Ed., Earthworm Ecology from Darwin to Vermiculture, Chapman & Hall, London, U.K., pp. 85–106. James, S.W. 1991. Soil, nitrogen, phosphorus, and organic matter processing by earthworms in tallgrass prairie, Ecology, 72:2101–2109. Kalisz, P.J. and D.B. Dotson. 1989. Land-use history and the occurrence of exotic earthworms in the mountains of eastern Kentucky, Am. Midl. Nat., 122:288–297. Kalisz, P.J. and H.B. Wood. 1995. Native and exotic earthworms in wildland ecosystems, in Hendrix, P., Ed., Earthworm Ecology and Biogeography in North America, Lewis Publishers, Boca Raton, FL, 117–126. Kourtev, P.S., W.Z. Huang, and J.G. Ehrenfeld. 1999. Differences in earthworm densities and nitrogen dynamics in soils under exotic and native plant species, Biol. Invasions, 1:237–245. Lachnicht, S.L, P.F. Hendrix, and X. Zou. 2002. Interactive effects of native and exotic earthworms on resource use and nutrient mineralization in a tropical wet forest soil of Puerto Rico, Biol. Fertil. Soils, 36:43–52. Lavelle, P., L. Brussard, and P. Hendrix, Eds. 1999. Earthworm Management in Tropical Agroecosystems, CABI Publishing, New York. Lee, K.E. 1959. The Earthworm Fauna of New Zealand, New Zealand Department of Scientific and Industrial Research Bulletin 130, Wellington, New Zealand. Liu, Z.G. and X.M. Zou. 2002. Exotic earthworms accelerate plant litter decomposition in a Puerto Rican pasture and a wet forest, Ecol. Appl., 12:1406–1417. Ljungstrom, P.O. 1972. Introduced earthworms of South Africa. On their taxonomy, distribution, history of introduction and on the extermination of endemic earthworms, Zool. Jb. Syst., 99:1–81. Loranger, G., J.F. Ponge, E. Blanchart, and P. Lavelle. 1998. Impact of earthworms on the diversity of microarthropods in a Vertisol (Martinique), Biol. Fertil. Soil, 27:21–26. Mack, R.N., D. Simberloff, W.M. Lonsdale, H. Evans, M. Clout, and F.A. Bazzaz. 2000. Biotic invasions: causes, epidemiology, global consequences, and control, Ecol. Appl., 10:689–710. Maerz, J.C., B. Blossey, and V. Nuzzo. 2001. The impact of garlic mustard invasions on woodland salamander populations in New York, in Abstr. Ecol. Soc. America, Madison, WI. McLean, M.A. and D. Parkinson. 1997. Soil impacts of the epigeic earthworm Dendrobaena octaedra on organic matter and microbial activity in lodgepole pine forest, Can. J. Forest Res., 27:1907–1913. McLean, M.A. and D. Parkinson. 2000a. Field evidence of the effects of the epigeic earthworm Dendrobaena octaedra on the microfungal community in pine forest floor, Soil Biol. Biochem., 32:351–360.



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McLean, M.A. and D. Parkinson. 2000b. Introduction of the epigeic earthworm Dendrobaena octaedra changes the oribatid community and microathropod abundances in a pine forest, Soil Biol. Biochem., 32:1671–1681. Michaelsen, W. 1900. Oligochaaeta, in Das Tierreich, Lief. 10, Friedlander, Berlin. Migge, S., D. Parkinson, and S. Scheu. 2004. Earthworm invasion of Canadian aspen forest soils: Impact on soil microarthropod communities, in Abstr. Ninth Biennial Mtg. Soil Ecol. Soc., Palm Springs, CA, in press. Nakamura, M. 1990. How to identify Hawaiian earthworms, Chuo Univ. Res. Notes, 11:101–110. Nielsen, G.A. and F.D. Hole. 1964. Earthworms and the development of coprogenous A1 horizons in forest soils of Wisconsin, Soil Sci. Soc. Am. Proc., 28:426–430. Omodeo, P. 1963. Distribution of the terricolous oligochaetes on the two shores of the Atlantic, in Love, D. and A. Love, Eds., North Atlantic Biota and Their History, Pergamon Press, New York, pp. 127–151. Parmelee, R.W., M.H. Beare, W. Cheng, P.F. Hendrix, S.J. Rider, D.A. Crossley, Jr., and D.C. Coleman. 1990. Earthworms and enchytraeids in conventional and no-tillage agroecosystems: a biocide approach to assess their role in organic matter breakdown, Biol. Fertil. Soil, 10:1–10. Reichard, S.H. and C.W. Hamilton. 1997. Predicting invasion of woody plants introduced into North America, Conserv. Biol., 11:193–203. Reynolds, J.W. 1994. Earthworms of the world, Global Biodiversity, 4:11–16. Reynolds, J.W. and D.G. Cook 1976. Nomenclatura Oligochaetologica: A Catalogue of Names, Descriptions and Type Specimens of the Oligochaeta, New Brunswick Museum Monographic Series No. 9, Fredericton, New Brunswick, Canada. Righi, G. 1972. Bionomic considerations on the Glossoscolecidae, Pedobiologia, 12:254–260. Righi, G. 1984. Pontoscolex (Oligochaeta, Glossoscolecidae) a new evaluation, Stud. Neotrop. Fauna, 19(3): 159–177. Scheu, S. and D. Parkinson. 1994. Effects of invasion of an aspen forest (Canada) by Dendrobaena octaedra (Lumbricidae) on plant growth, Ecology, 75:2348–2361. Shah, A.H. and C.B. Patel. 1978. Annelids as pests of paddy crop, in Edwards, C.A. and G.K. Veeresh, Eds., Soil Biology and Ecology in India, University of Agricultural Sciences, Bangalore, p. 83. Simberloff, D. and B. von Holle. 1999. Positive interactions of nonindigenous species: invasional meltdown? Biol. Invasions, 1:21–32. Smith, F. 1928. An account of changes in the earthworm fauna of Illinois and a description of one new species, Bull. Ill. Nat. Hist. Surv., 17:347–362. Stebbings, J.H. 1962. Endemic-exotic earthworm competition in the American Midwest, Nature, 196:905–906. Steinberg, D.A., R.V. Pouyat, R.W. Parmelee, and P. M. Groffman. 1996. Earthworm abundance and nitrogen mineralization rates along an urban-rural gradient, Soil Biol. Biochem., 29:427–430. Stockdill, S.M.J. 1982. Effects of introduced earthworms on the productivity of New Zealand pastures, Pedobiologia, 24:29–35. Suárez, E.R, D.M. Pelletier, T.J. Fahey, P.M. Groffman, P.J. Bohlen, and M.C. Fisk. 2004. Effects of exotic earthworms on soil phosphorus cycling in two broadleaf temperate forests, Ecosystems, in press. Winsome, T. 2003. Native and Exotic Earthworms in a California Oak Savanna Ecosystem, Ph.D. dissertation, University of Georgia, Athens.


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Part III Earthworm Biology, Ecology, Behavior, and Physiology



Affecting the 6 Factors Abundance of Earthworms in Soils James P. Curry Department of Environmental Resource Management, University College, Belfield, Dublin, Ireland

CONTENTS Introduction ......................................................................................................................................91 Climate .............................................................................................................................................92 Soil Properties ..................................................................................................................................93 Food..................................................................................................................................................94 Competition......................................................................................................................................98 Predation...........................................................................................................................................99 Parasitism and Disease...................................................................................................................100 Land Management..........................................................................................................................100 Mining and Industrial Wastes .................................................................................................101 Deforestation ...........................................................................................................................102 Afforestation ...........................................................................................................................102 Grassland Management...........................................................................................................103 Arable Cropping .....................................................................................................................103 Manures and Fertilizers ..........................................................................................................105 Pesticides and Pollutants ........................................................................................................106 Soil Water Management..........................................................................................................106 Conclusions ....................................................................................................................................107 References ......................................................................................................................................108

INTRODUCTION Earthworm populations show a considerable amount of variability in time and space, with mean population densities and biomass ranging from fewer than 10 individuals and 1 g m–2, respectively, to more than 1000 individuals and 200 g m–2, respectively, under favorable conditions. However, within particular climatic zones, earthworm assemblages, with fairly characteristic species richness, composition, abundance, and biomass, can often be recognized in broadly different habitat types, such as coniferous forests, deciduous woodland, grassland, and arable land. There is a considerable volume of literature describing the earthworm communities of such habitats, and much of this was summarized by Lee (1985) and updated by Edwards and Bohlen (1996). There is also a considerable amount of information describing the influence of various environmental and management factors on earthworm populations, but in comparison with insects, for which the population ecology of



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many species has been subjected to quantitative analysis, earthworm population ecology is still largely at a descriptive stage. Population modeling has been used for particular purposes such as risk assessment (Baveco and De Roos 1996), but development of realistic models of field populations has been hindered by a lack of information on key life history parameters and the factors that influence them. In this chapter, the main factors that influence earthworm abundance are reviewed. These factors fall into two broad categories: external factors, which determine the habitat (climate, soil, vegetation, and litter supply and management), and biotic interactions within the communities to which earthworms belong (competition, predation, parasitism, disease, and food relationships).

CLIMATE Climate affects earthworms directly by influencing their biology and life processes and indirectly through its effects on their habitat and food supply. Temperature is a factor of primary importance because it determines individual earthworm metabolic rates, and on a global scale, it can have a major role in determining patterns of earthworm distribution and activity. The range of temperatures within which most earthworms can function is narrow, with upper lethal temperatures rather low (25 to 35°C) and optimum temperatures typically in the range 10 to 20°C for cool temperate species and 20 to 30°C for tropical and subtropical species (Lee 1985; Edwards and Bohlen 1996). Few species can tolerate temperatures below 0°C, although many species have behavioral or physiological adaptations that enable them to survive unfavorable periods in areas with strongly seasonal climates. Temperature may be a factor of primary importance in determining the composition and structures of earthworm communities (Lavelle 1983; Lavelle et al. 1989, 1999). Faster organic matter decomposition rates at higher temperatures result in decreased litter availability, and litter-feeding epigeic and anecic earthworm populations tend to be depleted in tropical soils compared with those in temperate soils (Lavelle et al. 1999). With increasing temperatures, endogeic species, which can utilize resources of increasingly lower quality through more efficient digestive processes involving mutualistic interactions with ingested soil microflora, are favored. Thus, in Mediterranean and humid tropical areas, oligohumic earthworm species that are able to feed on soils poor in organic matter are found deep in the soil profile. These are typically K-strategists, i.e., with large body size, slow growth, and low fecundity and mortality rates. However, very large endogeic species such as Octochaetus multiporus in New Zealand and Megascolides australis in Australia appear to be more common in temperate than in tropical soils (Lee personal communication). Thus, although large body size is an adaptation that facilitates earthworm feeding in nutrient-poor soils, in warmer soils body size may be constrained by increased energy demands for respiration, resulting in a severely limited energy supply for tissue production from a low-energy diet. High temperatures are often associated with moisture shortages, and seasonal earthworm mortality in temperate soils has usually been attributed to moisture stress rather than to temperature extremes (e.g., Gerard 1967; Phillipson et al. 1976). Indeed, the overwhelming importance of soil moisture in determining earthworm distributions and activity has frequently been demonstrated. Rainfall can explain more of the variance in earthworm numbers than any other variable in a range of agricultural soils, with annual rainfall varying from 230 to 1150 mm in southern Australia (Baker 1998). Optimum soil moisture content varies for different earthworm species and ecological groups, and within species, there appears to be a considerable capacity to adapt to local conditions (Lee 1985). In general, earthworms are most active at moisture tensions approaching field capacity (~10 kPa), and activity declines rapidly as the moisture tension exceeds 100 kPa and ceases for most species at moisture tensions below the permanent wilting point (1500 kPa) (Lavelle 1974; Nordström and Rundgren 1974; Nordström 1975; Baker et al. 1993).



Factors Affecting the Abundance of Earthworms in Soils

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Although adapted populations in areas with strongly seasonal climates have the capacity to survive periods of drought, they nevertheless suffer heavy mortality, particularly among juveniles unable to escape desiccation by moving deeper into the soil and becoming inactive (e.g., Gerard 1967). The severity and duration of summer droughts impose severe constraints on the duration of earthworm activity and undoubtedly influence both the overall earthworm population density and the biomass, which can be attained when growth and development are restricted to relatively short periods in autumn and spring.

SOIL PROPERTIES Many studies have attempted to relate earthworm distributions to a range of soil physical and chemical parameters, often with inconclusive results. Other than soil moisture, the soil properties that appear to be most important include texture, depth, pH, and organic matter content. Medium-textured soils appear to be more favorable to earthworms than sandy soils or soils with high clay content (Guild 1948). Nordström and Rundgren (1974) reported a positive relationship between clay content and the abundance of Aporrectodea caliginosa, Aporrectodea longa, Aporrectodea rosea, and Lumbricus terrestris in 15 forest, pasture, and heath soils in Sweden, with clay contents ranging from 5 to 25%. A stepwise multiple regression indicated a positive relationship between clay content and the numbers and biomass of introduced Aporrectodea spp. in 113 pasture soils in South Australia (Baker et al. 1992). Decreasing population densities of A. caliginosa were linked with increasing proportions of sand and gravel in Egyptian soils (Khalaf El-Duweini and Ghabbour 1965), and low earthworm densities (max 73 m−2) occurred in sandy and silty coastal grassland sites in County Wexford, Ireland, compared with those in similarly managed loam soils (max 516 m−2) (Cotton and Curry 1980b). Although texture could have a direct effect on earthworm activity in the case of abrasive gravelly soils, more often the influence of texture may be indirect through its effect on moisture relationships. Heavy, poorly drained clay soils may become anaerobic in areas of high rainfall, and light sandy soils are prone to drought. The depth of soil is a significant factor governing earthworm distributions in temperate (Phillipson et al. 1976) and tropical (Fragoso and Lavelle 1992; Lavelle et al. 1999) forest soils. Lack of a sufficient depth of aerobic soil could be a factor limiting the establishment of deep-burrowing earthworm species in soils reclaimed after mining (Curry and Cotton 1983). Earthworms are generally absent from very acid soils (pH less than 3.5) and are scarce in soils with pH less than 4.5. Although there are considerable differences among species in their pH preference, the majority of temperate climate species are found in the pH range 5.0 to 7.4 (Satchell 1967; Bouché 1972). Other edaphic factors that have been linked with earthworm distributions include calcium, magnesium, and nitrogen content (Fragoso and Lavelle 1992), and populations can be affected adversely by high salt concentrations, which can occur, for example, in irrigated soils (Khalaf El-Duweini and Ghabbour 1965). The nature and quality of the soil organic matter are determined largely by the litter input from the vegetation. Litter from grass, herbaceous plants, and deciduous trees growing on base-rich, fertile soils is generally of high quality, with ratios of carbon to nitrogen close to or less than 20:1; the vegetation on impoverished acidic soils produces tough, unpalatable litter low in nutrients (carbon-to-nitrogen ratio more than 60:1) and unfavorable for earthworms. The organic matter that provides the food base for the earthworm community is vitally important in determining their distribution and abundance, and the soil organic matter content can sometimes be a good predictor of earthworm abundance (Edwards and Bohlen 1996). For example, Hendrix et al. (1992) reported a highly significant correlation between earthworm populations and soil organic carbon content over a range of sites in the state of Georgia, which included a wide variety of soil and vegetation types and management histories.



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FOOD There is little doubt that earthworm populations are often food limited; this is evident from the fact that populations often increase following organic amendment. The response to organic amendments can be particularly marked in disturbed habitats of low organic matter content (Edwards 1983; Lofs-Holmin 1983; Lowe and Butt 2002), but significant population increases can also occur in favorable habitats, such as permanent pasture, following the application of high-quality organic materials like animal manures (Curry 1976; Cotton and Curry 1980a,b; Edwards and Lofty 1982b). In the absence of other constraints, it is likely that the earthworm-carrying capacity of most habitats could be increased considerably by increasing the food supply. Hartenstein and Bisesi (1989) estimated from laboratory studies conducted by Hartenstein and Amico (1983) that a biomass of L. terrestris up to 0.5 kg m–2 could be sustained under conditions of unlimited food supply in soil irrigated with livestock wastes. However, it is unlikely that such a high earthworm biomass could be sustained under field conditions (Schmidt et al. 2003). The main source of the organic matter on which earthworms feed is litter from aboveground plant parts in most ecosystems, although dead roots and rhizodeposition can also be important food sources. Some species, including Allolobophora chlorotica, are found in close association with roots, and some species are known to ingest living roots (Baylis et al. 1986). Earthworm populations in woodlands can be limited by the amount and continuity of the litter supply; this was apparent, for example, in afforested coal mine dumps in Germany, where the epigeic species (Dendrobaena spp., Lumbricus rubellus) flourished when a well-developed litter layer was present but declined in importance when the litter layer was depleted by the action of anecic species such as L. terrestris (Dunger 1989). Zicsi (1983) concluded that the continuity of food supply was of cardinal importance in determining the suitability of deciduous woodlands in central Europe for the survival of largebodied, anecic earthworms. However, it appears to be the quality rather than the actual quantity of litter that most often limits earthworm populations (Satchell 1967; Swift et al. 1979; Boström and Lofs-Holmin 1986). Much of the litter input into soil is poor in nutrients, with nitrogen in particular often in short supply. Satchell (1963) calculated that the nitrogen requirement of the L. terrestris population in an English deciduous woodland (about 100 kg ha−1 year–1) was at least equivalent to, and was possibly in excess of, the nitrogen supply from litter. Nitrogen is often considered the critical factor limiting earthworm populations in many ecosystems, both temperate (Satchell 1967) and tropical (Lee 1983). Nitrogen content can be a useful indicator of food quality when comparing widely different types of litter but may be less useful as a predictor of earthworm performance on more palatable residues from agricultural crops and deciduous trees (Table 6.1). Boström and Lofs-Holmin (1986) and Boström (1987, 1988), for example, found no consistent relationships between nitrogen content and the growth rates of A. caliginosa cultured in soil amended with plant materials, with nitrogen contents ranging from 0.37 to 4%, although adult growth rates and cocoon production rates were significantly lower on unfertilized barley straw (0.35% nitrogen) than on meadow fescue (2.57% nitrogen) and lucerne (2.3% nitrogen) residues. Particle size has an important influence on the quality of plant materials as food for endogeic species, such as A. caliginosa (Boström and Lofs-Holmin 1986), but not for large anecic species such as L. terrestris. Boyle (1990) reared juvenile L. terrestris and A. caliginosa in mixed cultures (1 L. terrestris plus 1 A. caliginosa per 1-L container) in a peat/mineral soil medium with chopped (8-mm pieces) or milled (

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