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Nematodes as Biocontrol Agents This page intentionally left blank Nematodes as Biocontrol Agents Edited by Parwinder S. Grewal Department of Entomology Ohio State University, Wooster, Ohio USA Ralf-Udo Ehlers Department of Biotechnology and Biological Control Institute for Phytopathology Christian-Albrechts-University Kiel, Raisdorf Germany David I. Shapiro-Ilan United States Department of Agriculture Agriculture Research Service Southeastern Fruit and Tree Nut Research Laboratory, Byron, Georgia USA CABI Publishing CABI Publishing is a division of CAB International CABI Publishing CABI Publishing CAB International 875 Massachusetts Avenue Wallingford 7th Floor Oxfordshire OX10 8DE Cambridge, MA 02139 UK USA Tel: þ44 (0)1491 832111 Tel: þ1 617 395 4056 Fax: þ44 (0)1491 833508 Fax: þ1 617 354 6875 E-mail: [email protected] E-mail: [email protected] Web site: www.cabi-publishing.org ßCAB International 2005. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mech- anically, by photocopying, recording or otherwise, without the prior permission of the copyright owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data Nematodes as biocontrol agents / edited by Parwinder S. Grewal, Ralf- Udo Ehlers, David I. Shapiro-Ilan. p. cm. Includes bibliographical references and index. ISBN 0-85199-017-7 (alk. paper) 1. Nematoda as biological pest control agents. I. Grewal, Parwinder S. II. Ehlers, Ralf-Udo. III. Shaprio-Ilan, David I. SB976.N46N46 2005 632’.96–dc22 2004030022 ISBN 0 85199 0177 Typeset by SPI Publisher Services, Pondicherry, India Printed and bound in the UK by Biddles Ltd., King’s Lynn This volume is dedicated to Dr Harry K. Kaya in recognition of his numerous contributions to insect pathology. His early contributions to the ecology of entomopathogenic nematodes provided a solid foundation for the development of application strategies for use of nematodes in insect biocontrol. Dr Kaya has co-edited four books on entomopathogenic nematodes and insect pathology/biological control and co-authored a book on insect pathology. He has published more than 230 research papers on the ecology and application of insect nematodes and other pathogens and is one of the co-founding editors of the journal Biological Control. His outstanding leadership and scholarly accomplishments, spanning nearly three decades, have played a key role in expanding research and applica- tion in insect nematology to laboratories and industries around the world. This page intentionally left blank Contents Contributors xi Preface xv Glossary of Terms xvii PART I. NEMATODE MORPHOLOGY AND TAXONOMY 1 1. Morphology and Systematics of Nematodes Used in Biocontrol 3 S.P. Stock and D.J. Hunt PART II. ENTOMOPATHOGENIC NEMATODES 45 2. Biology and Behaviour 47 C.T. Griffin, N.E. Boemare and E.E. Lewis 3. Mass Production 65 R.-U. Ehlers and D.I. Shapiro-Ilan 4. Formulation and Quality 79 P.S. Grewal and A. Peters 5. Application Technology 91 D.J. Wright, A. Peters, S. Schroer and J.P. Fife 6. Forum on Safety and Regulation 107 R.-U. Ehlers 7. Lawn, Turfgrass and Pasture Applications 115 P.S. Grewal, A.M. Koppenho¨ fer and H.Y. Choo 8. Glasshouse Applications 147 M. Tomalak, S. Piggott and G.B. Jagdale 9. Nursery and Tree Applications 167 R.W.H.M. Van Tol and M.J. Raupp vii viii Contents 10. Mushroom Applications 191 S. Jess, H. Schweizer and M. Kilpatrick 11. Orchard Applications 215 D.I. Shapiro-Ilan, L.W. Duncan, L.A. Lacey and R. Han 12. Soft Fruit Applications 231 R.S. Cowles, S. Polavarapu, R.N. Williams, A. Thies and R.-U. Ehlers 13. Vegetable and Tuber Crop Applications 255 G. Be´lair, D.J. Wright and G. Curto 14. Cereal, Fibre, Oilseed and Medicinal Crop Applications 265 H.E. Cabanillas, R.J. Wright and R.V. Vyas 15. Forestry Applications 281 P. Torr, M.J. Wilson and S. Heritage 16. Applications for the Control of Pests of Humans and Animals 295 I. Glazer, M. Samish and F.G. del Pino 17. Applications for Social Insect Control 317 D.H. Gouge 18. A Systems Approach to Conservation of Nematodes 331 M.E. Barbercheck and C.W. Hoy 19. Interactions with Plant-parasitic Nematodes 349 E.E. Lewis and P.S. Grewal 20. Compatibility and Interactions with Agrochemicals and Other Biocontrol Agents 363 A.M. Koppenho¨ fer and P.S. Grewal PART III. ENTOMOPHILIC NEMATODES 383 21. Application of Beddingia siricidicola for Sirex Woodwasp Control 385 R.A. Bedding and E.T. Iede 22. The Entomophilic Thripinema 401 J. Funderburk and K.S. Latsha 23. Mermithid Nematodes 411 E.G. Platzer, B.A. Mullens and M.M. Shamseldean PART IV. SLUG-PARASITIC NEMATODES 419 24. Biology, Production and Formulation of Slug-parasitic Nematodes 421 M.J. Wilson and P.S. Grewal 25. Application of Slug-parasitic Nematodes 431 A. Ester and M.J. Wilson PART V. PREDATORY NEMATODES 445 26. Potential of Predatory Nematodes to Control Plant-parasitic Nematodes 447 A.L. Bilgrami and C. Brey Contents ix PART VI. FUNGAL-FEEDING NEMATODES 465 27. Potential of Fungal-feeding Nematodes for the Control of Soil-borne Plant Pathogens 467 N. Ishibashi PART VII. CONCLUSIONS AND FUTURE DIRECTIONS 477 28. Critical Issues and Research Needs for Expanding the Use of Nematodes in Biocontrol 479 P.S. Grewal, R.-U. Ehlers and D.I. Shapiro-Ilan Index 491 This page intentionally left blank Contributors Mary Barbercheck, Department of Entomology, Pennsylvania State University, University Park, PA 16802, USA (email: [email protected]) Robin A. Bedding, Division of Entomology, CSIRO, GPO Box 1700, Canberra, ACT 2601, Australia (email: [email protected]) Guy Be´lair, Horticultural Research and Development Centre, Agriculture and Agri-Food Canada, St-Jean-sur-Richelieu, Quebec, Canada J3B 3E6 (email: [email protected]) Anwar L. Bilgrami, Department of Entomology, Rutgers University, NJ 08901, USA (email: [email protected]) Noel E. Boemare, Laboratoire EMIP, UMR, INRA, Universite Montpellier II, Montpellier, Cedex 5, France (email: [email protected]) Christopher Brey, Department of Entomology, Rutgers University, NJ 08901, USA (email: [email protected]) H. Enrique Cabanillas, USDA, ARS, Kika de la Garza SARC, Beneficial Insects Research Unit, 2413 E. Hwy 83, Weslaco, TX 78596, USA (email: [email protected]. gov) Ho Y. Choo, Department of Applied Biology and Environmental Science, Gyeongsang National University, Jinju, Gyeongnam 660–701, Republic of Korea (email: hychoo@ nongae.gsnu.ac.kr) Richard Cowles, Connecticut Agricultural Experiment Station, Valley Laboratory, Wind- sor, CT 06095, USA (email: [email protected]) Giovanna Curto, Servizio Fitosanitario Regione emilia-Romagna, Bologna, Italy (email: [email protected]) Fernando Garcia del Pino, Department of Animal Biology, Faculty of Science, Universitat Auto`noma de Barcelona, 08193, Bellaterra, Barcelona, Spain (email: Fernando. [email protected]) Larry W. Duncan, University of Florida, CREC, Lake Alfred, FL 33850, USA (email: [email protected]) Ralf-Udo Ehlers, Department for Biotechnology and Biological Control, Institute for Phytopathology, Christian-Albrechts-University Kiel, 24223, Raisdorf, Germany (email: [email protected]) Albert Ester, Applied Plant Research Ltd, Business Unit Arable Farming and Field Production of Vegetables, PO Box 430, 8200 AK Lelystad, The Netherlands (email: [email protected]) xi xii Contributors Jane Patterson Fife, Aerosol and Process Technologies, Battelle Memorial Institute, 505 King Avenue, Columbus, OH 43201, USA (email: [email protected]) Joe E. Funderburk, North Florida Research and Education Center, University of Florida, Quincy, 155 Research Road, FL 32351, USA (email: [email protected]) Itamar Glazer, Department of Nematology, ARO, Volcani Center, Bet-Dagan, 50250, Israel (email: [email protected]) Dawn H. Gouge, Department of Entomology, University of Arizona, Maricopa, AZ 85239, USA (email: [email protected]) Parwinder S. Grewal, Department of Entomology, Ohio State University, Wooster, OH 44691, USA (email: [email protected]) Christine T. Griffin, Department of Biology and Institute of Bioengineering and Agroecol- ogy, National University of Ireland, Maynooth, Ireland (email: [email protected]) Richou Han, Guangdong Entomological Institute, Guangzhou 510260, China (email: [email protected]) Stuart Heritage, Entomology Branch, Forest Research, Northern Research Station, Roslin, Midlothian EH25 9SY, UK (email; [email protected]) Casey W. Hoy, Department of Entomology, Ohio State University, Wooster, OH 44691, USA (email: [email protected]) David J. Hunt, CABI Bioscience (UK Centre), Egham, Surrey TW20 9TY, UK (email: [email protected]) Edson T. Iede, EMBRAPA Florestas, Brazil (email: [email protected]) Nobuyoshi Ishibashi, Saga University, 1090-3, Kinryu-Chifu, Saga, 849-0905, Japan (email: [email protected]) Ganpati Jagdale, Department of Entomology, Ohio State University, Wooster, OH 44691, USA (email: [email protected]) Stephen Jess, Applied Plant Science Division, Department of Agriculture and Rural De- velopment for Northern Ireland, Newforge Lane, Belfast BT9 5PX, UK (email: stephen. [email protected]) Mairead Kilpatrick, Applied Plant Science Division, Department of Agriculture and Rural Development for Northern Ireland, NIHPBS Loughgall, County Armagh, BT61 8JB, UK (email: [email protected]) Albrecht M. Koppenho¨fer, Department of Entomology, Rutgers University, New Bruns- wick, NJ 08901, USA (email: koppenho¨[email protected]) Lawrence A. Lacey, USDA-ARS, Yakima Agricultural Research Laboratory, Wapato, WA 98951, USA (email: [email protected]) Kelly Sims Latsha, North Florida Research and Education Center, University of Florida, Quincy, FL 32351, USA (email: [email protected]) Edwin E. Lewis, Department of Nematology and Department of Entomology, 1 Shields Avenue, University of California Davis, Davis, CA 95616, USA (email: eelewis@ucdavis. edu) Bradley A. Mullens, Department of Entomology, University of California, Riverside, CA 92521, USA (email: [email protected]) Arne Peters, e-nema GmbH, Klausdorfer Str.