INSECT RESISTANCE MANAGEMENT INSECT RESISTANCE MANAGEMENT Biology, Economics, and Prediction Second Edition Edited by David W. Onstad Insect Resistance Management Science, DuPont Agricultural Biotechnology, Wilmington, DE, USA AMSTERDAM(cid:129)BOSTON(cid:129)HEIDELBERG(cid:129)LONDON NEWYORK(cid:129)OXFORD(cid:129)PARIS(cid:129)SANDIEGO SANFRANCISCO(cid:129)SINGAPORE(cid:129)SYDNEY(cid:129)TOKYO AcademicPressisanimprintofElsevier AcademicPressisanimprintofElsevier 32JamestownRoad,LondonNW17BY,UK 225WymanStreet,Waltham,MA02451,USA 525BStreet,Suite1800,SanDiego,CA92101-4495,USA Copyrightr2014,2008ElsevierLtd.Allrightsreserved Nopartofthispublicationmaybereproduced,storedinaretrievalsystemor transmittedinanyformorbyanymeanselectronic,mechanical,photocopying, recordingorotherwisewithoutthepriorwrittenpermissionofthepublisher PermissionsmaybesoughtdirectlyfromElsevier’sScience&TechnologyRights DepartmentinOxford,UK:phone(144)(0)1865843830;fax(144)(0)1865853333; email:[email protected],visittheScienceandTechnologyBooks websiteatwww.elsevierdirect.com/rightsforfurther information. 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BritishLibraryCataloguing-in-PublicationData AcataloguerecordforthisbookisavailablefromtheBritishLibrary LibraryofCongressCataloging-in-PublicationData AcatalogrecordforthisbookisavailablefromtheLibraryofCongress ISBN:978-0-12-396955-2 For informationonallAcademicPresspublications visitourwebsiteatelsevierdirect.com TypesetbyMPSLimited,Chennai,India www.adi-mps.com PrintedandboundinUnitedStatesofAmerica 14 15 16 17 10 9 8 7 6 5 4 3 2 1 DEDICATION To Dawn Dockter, my partner in life and science for 25 years, and Nora and Emma, who are amazing LIST OF CONTRIBUTORS AnalizaP.Alves InsectResistanceManagementScience,DuPontPioneer,Johnston,IA YvesCarrie`re DepartmentofEntomology,UniversityofArizona,Tucson,AZ JohnM.Clark DepartmentofVeterinaryandAnimalSciences,UniversityofMassachusetts, Amherst,MA J.LindseyFlexner InsectResistanceManagementScience,DuPontPioneer,Wilmington,DE PatrickGaffney DepartmentofStatistics,UniversityofWisconsin,Madison,WI AaronJ.Gassmann DepartmentofEntomology,IowaStateUniversity,Ames,IA JosephE.Huesing OfficeofAgriculturalResearchandPolicy,BureauforFoodSecurity,U.S.Agencyfor InternationalDevelopment,USDAARSOIRP,Washington,DC SarahA.Hughson DepartmentofEntomology,UniversityofIllinois,Urbana,IL TerranceM.Hurley DepartmentofAppliedEconomics,UniversityofMinnesota,St.Paul,MN LisaM.Knolhoff Genective,AgReliantGenetics,Champaign,IL SiHyeockLee DepartmentofAgriculturalBiotechnology,SeoulNationalUniversity,Seoul,South Korea EliLevine IllinoisNaturalHistorySurvey,PrairieResearchInstitute,UniversityofIllinois, Champaign,IL VenuMadhavMargam RegulatoryScience,DuPontKnowledgeCentre,Turkapally,ShameerpetMandal,Ranga ReddyDistrict,Hyderabad,AndhraPradesh,India PaulD.Mitchell DepartmentofAgriculturalandAppliedEconomics,UniversityofWisconsin, Madison,WI xiii xiv ListofContributors MarkE.Nelson InsectResistanceManagementScience,DuPontPioneer,Wilmington,DE BrettP.Olds DepartmentofAnimalBiology,UniversityofIllinois,Urbana,IL DavidW.Onstad InsectResistanceManagementScience,DuPontPioneer,Wilmington,DE BarryR.Pittendrigh DepartmentofEntomology,UniversityofIllinois,Urbana,IL AnthonyM.Shelton DepartmentofEntomology,CornellUniversity,Geneva,NY JosephL.Spencer IllinoisNaturalHistorySurvey,PrairieResearchInstitute,UniversityofIllinois, Champaign,IL BruceH.Stanley InsectResistanceManagementScience,DuPontPioneer,Wilmington,DE LauraD.Steele DepartmentofEntomology,UniversityofIllinois,Urbana,IL LijieSun SyntheticBiologyandBioenergy,J.CraigVenterInstitute,SanDiego,CA KentR.Walters,Jr. DepartmentofEntomology,UniversityofIllinois,Urbana,IL FOREWORD Resistance to pesticides has been with us for at least 100 years now, since the recognition of resistance to lime sulfur in the San Jose scale in the state of Washington in 19081. At least through the early 1950s, resistance was apparently seen by many entomologists as just a curiosity, and no real threat to the emerging field of integrated control (which later developed into integrated pest management, IPM). For example, when I arrived at Mississippi State University in 1981, I was housed in the Clay Lyle Entomology Building. Lyle was a very prominent applied entomologist, and reportedly once advised fellow entomologists that they should collect all of the houseflies they would ever need for museum specimens because DDT and other insecticides would drive them extinct. With no disrespect intended for Lyle and so many others of his time, I studied strains of houseflies in that building, by 1983, that were resistant to every major class of insecticides at the time. Houseflies were early responders to selection, starting in the 1940s, but by 1989 there were more than 500 species of insects, mites, or ticks that had evolved resistance to at least one pesticide somewhere in the world. At least 20 of these species evolve resistance so frequently that they remain a challenge to our attempts to manage them cost-effectively. These “resistance recidivists” include Anopheles mosquitoes, Helicoverpa armigera (a pest of many food crops in addition to being a major cotton bollworm), Plutella xylsotella (the diamondback moth, a major pest of cru- cifer crops), whiteflies such as Bemisia tabaci, the cockroach, Blattella ger- manica, Leptinotarsa decemlineata (the Colorado potato beetle), stored grain pests (contributing to some 40% of grain losses in storage in developing countries), and corn rootworms (Diabrotica spp). Some, such as mosqui- toes and Helicoverpa, contribute to great human illness and misery, includ- ing the transmission of malaria and other diseases (still killing more than a million people a year) and, due to crop damage and desperate financial circumstances, suicides of farmers in India. The typical response of pesticide users to the evolution of resistance by pests is to use more pesticides or switch to more expensive pesticides, or sometimes to ones that are more environmentally risky. As the global 1 A.L.MelanderCaninsectsbecomeresistanttosprays?J.Econ.Entomol.71914167(cid:1)173 xv xvi Foreword agricultural community contemplates increasing crop production by some 70(cid:1)100% to meet the demands of a growing and more affluent human population, pesticide resistance continues to be a threat to both produc- tion and the hope of reducing the environmental impacts of agriculture. Ironically, the broader significance of resistance was perhaps first rec- ognized not by applied entomologists, but by evolutionary biologists, thanks to Theodosius Dobzhansky. In his 1937 classic, Genetics and the Origin of Species, arguably the most influential book of the modern Darwinian synthesis, Dobzhansky seized upon insecticide resistance to demonstrate that evolution was occurring in our lifetimes. The significance of the evolution of resistance for both the study of evolution and to IPM has been captured in this volume by David Onstad and the team of leading experts he has orchestrated. Onstad is well placed to discuss the diversity of evolutionary responses to control tactics in arthropods due to his own curiosity, the diversity of his own career inter- ests, and the network he has built across an even wider diversity of biolo- gists and social scientists. Onstad and colleagues describe and analyze the evolution of resistance to a wide range of pesticides (including the diversity of mechanisms and behavioral modification), conventionally bred and genetically modified crop varieties, crop rotation, and insect pathogens. In so doing, we are treated to a broad canvas of population dynamics, landscape processes, models, toxicology, and economics. We see the complexity and excite- ment of insect resistance management (IRM), some of the successes and the continuing challenges, including in regulation and compliance with IRM strategies. Resistance has been evolving to plant defenses for millennia, but has been less well documented than for pesticides. Given that resistance has been evolving to crop plants selected by humans over at least 40 years, we can suspect the same was happening to crop varieties even in the 1930s, but escaped attention. Anyone reading this book will now likely be on the lookout for a wider range of evolutionary responses, especially wherever the “greater the effectiveness and success of arthropod pest management.” In his final chapter, Onstad advises that we should “Always consider IRM within an IPM framework.” I would add that we must also “Always consider IPM within an IRM framework.” Not only is IRM part of IPM, IRM is most interesting and perhaps most powerful when the best resistance-management tactics are not obvious extensions of IPM. Foreword xvii Good IRM is often counterintuitive and runs contrary to some of the long-held tenants of IPM, such as applying tactics only when and where needed or on thresholds. The effectiveness and relative durability of high- expression,pyramided,transgeniccropssuggesttheneedforarethinkofthis dogma, especially where such varieties have so reduced pesticide use that theyhaveinturnopenedopportunitiesforenhancedIPMofotherpests. As suggested above, successful IPM is more important now than ever if we are to meet global demands for food and public health while reduc- ing the environmental impacts of agriculture and disease management. Pesticides should not be the basis of these IPM programs, but we need to maintain them and other tactics, such as resistant crop varieties, as effec- tive tools when required. Whether for crop varieties, crop rotation, or pesticides, this volume clearly illustrates that IPM programs can fail if we do not also implement countermeasures for evolution. This is a one-hundred-year-old story, with abundant lessons that we need to apply more vigorously if we are to meet the crop production and environmental challenges now before us. Rick Roush Melbourne School of Land and Environment, University of Melbourne, Parkville, Victoria, Australia PREFACE TO SECOND EDITION By the time we finished writing the chapters, it was obvious that a new edition of this book with additional knowledge and case studies was needed to keep pace with the science and the evolving arthropods. Although the book’s themes remain the same as before, the authors dem- onstrate that new challenges confront practitioners of insect resistance management. I thank the authors of the first edition who volunteered again to address the important concepts and examples. I am also pleased and thankful that the new authors agreed to join the group to make the sec- ond edition even better than the first. Rick Roush, Dean at the University of Melbourne, was kind enough to write a forward for this edition that places insect resistance management in a broader context. Dawn Dockter edited several chapters and helped produce the index (as she did for the first edition). Bruce Stanley and I thank Stephen Irving for use of his resistance-monitoring example in Chapter 15. I also thank the Academic Press and Elsevier staff who led me through the book- production process one more time. David Onstad Agricultural Biotechnology, DuPont Pioneer Department of Entomology and Wildlife Ecology, University of Delaware The cover photograph is used with permission from Joseph Spencer (copyright 2013). It is the shadow of an adult Diabrotica virgifera virgifera on a corn leaf. The front cover was designed with the help of Emma Onstad. xix