Integration of Insect Resistant Genetically Modified Crops Insect Resistant Programs (Progress in Biological Control) Integration of Insect Resistant Genetically Modified Crops within IPM Programs Progress.
Integration of Insect-Resistant Genetically Modified Crops within IPM Programs Progress in Biological Control Volume Published: Volume H.M.T Hokkanen and A.E Hajek (eds.): Environmental Impacts of Microbial Insecticides – Need and Methods for Risk Assessment 2004 ISBN 978-1-4020-0813-9 Volume J Eilenberg and H.M.T Hokkanen (eds.): An Ecological and Societal Approach to Biological Control 2007 ISBN 978-1-4020-4320-8 Volume J Brodeur and G Boivin (eds.): Trophic and Guild Interactions in Biological Control 2006 ISBN 978-1-4020-4766-4 Volume J Gould, K Hoelmer and J Goolsby (eds.): Classical Biological Control of Bemisia tabaci in the United States 2008 ISBN 978-1-4020-6739-6 Volume J Romeis, A M Shelton, and G G Kennedy (eds.): Integration of Insect-Resistant Genetically Modified Crops within IPM Programs 2008 ISBN 978-1-4020-8372-3 Forthcoming: Use of Microbes for Control and Eradication of Invasive Arthropods Edited by A.E Hajek, M O’Callaghan and T Glare Ecological & Evolutionary Relationships among Entomphagous Arthropods and Non-prey Foods By J Lundgren Biocontrol-based Integrated Management of Oilseed Rape Pests Edited by I.H Williams and H.M.T Hokkanen Biological Control of Plant-Parasitic Nematodes: Building Coherence between Microbial Ecology and Molecular Mechanisms Edited by Y Spiegel and K Davies Egg Parasitoids in Agroecosystems with emphasis on Trichogramma Edited by F Consali, J Parra, R Zucchi Jưrg Romeis • Anthony M Shelton George G Kennedy Editors Integration of Insect-Resistant Genetically Modified Crops within IPM Programs Editors Jörg Romeis Agroscope Reckenholz-Tänikon Research Station ART Reckenholzstrasse 191 8046 Zurich Switzerland joerg.romeis@art.admin.ch Anthony M Shelton Department of Entomology Cornell University/NYSAES Geneva, NY 14456 USA ams5@cornell.edu George G Kennedy Department of Entomology North Carolina State University Raleigh, NC 27695-7630 USA George_Kennedy@ncsu.edu ISBN 978-1-4020-8459-1 (PB) ISBN 978-1-4020-8372-3 (HB) e-ISBN 978-1-4020-8373-0 (e-book) Library of Congress Control Number: 2008923181 © 2008 Springer Science + Business Media B.V No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work Cover Illustration: Upper left: Scouting a maize crop Lower left: Cotton crop Upper right: European corn borer, Ostrinia nubilalis (Lepidoptera: Crambidae), damage and fungal infection in non-Bt (left) maize and Bt maize Lower right: A green lacewing, Chrysoperla rufilabris (Neuroptera: Chrysopidae), larva preying on whitefly nymphs The picture in the upper right was kindly provided by Gary Munkvold (Iowa State University, IA, USA) All others are from the USDA-ARS Image Gallery Printed on acid-free paper springer.com Endorsements The products of biotechnology will be essential for moving agriculture forward to help meet the food and fiber needs of the growing world population Biotech crops (GM crops) offer tremendous advances in our ability to manage agricultural pests safely and effectively, and have been rapidly adopted by farmers worldwide Until recently, plant breeders have been unable to develop crops that are highly resistant to many of our most serious insect pests, but this changed when plants expressing proteins from the bacterium Bacillus thuringiensis (Bt) were developed Bt crops fit in well with the concept and practice of Integrated Pest Management (IPM), and are becoming the cornerstone for IPM in the world’s most important crops This comprehensive book provides valuable information and analysis by many of the world’s leading experts involved with integrating transgenic insect-resistant crops into IPM Norman E Borlaug - Nobel Peace Prize Laureate, 1970 Using transgenic plants for pest management requires the best of science to retain both the public’s trust and the durability of the technology This comprehensive book contains the best scientific knowledge to date about transgenic insecticidal plants and the importance of their use within an IPM context Transgenes, especially those from Bacillus thuringiensis, are increasingly used to protect the world’s most important crops (cotton, maize, potato and rice) from insect damage However the durability of their effectiveness is under pressure from insect evolution, and should thus be protected by appropriate IPM practices This book has collected the wisdom and experience of many of the leading experts on this extremely important aspect of food and fiber security and will serve as an important guide to the future of IPM in transgenic crop management for students, regulators, and a wide array of scientists in developed and developing countries Thomas Lumpkin, former Director General, AVRDC - The World Vegetable Center and new Director General of CIMMYT v Foreword The Green Revolution of the 1960s, 1970s and 1980s demonstrated the potential of science and technology to contribute to agricultural development, food security and economic growth in poor and predominantly agrarian countries as well as rich industrial countries The benefits reached many of the world’s poorest people and the proportion of the population that is undernourished in developing countries declined from 40% in 1960 to 17% in 2000 While this was a great accomplishment, further research and development clearly needs to be done to better feed those that remain undernourished And, since agro-ecosystems are not static but rather are continually evolving, considerable research and development is needed to maintain the productivity gains already achieved and to so through farming practices that are more sustainable and leave a much smaller environmental footprint than current practices Research to reduce crop losses caused by insect pests and pathogens has made and will continue to make important contributions toward the necessary increases in yield, productivity and sustainability This book reviews the potential for integrating, and thereby strengthening, two insect pest control technologies that have each already made significant contributions to reducing both crop losses and insecticide use in many countries Integrated pest management (IPM) was developed as an insect control strategy in part due to the failure of insecticides to keep insect pests under control For some crops, such as cotton and rice, inordinant insecticide applications had resulted in development of insects resistant to insecticides, emergence of new pests that were worse than those being targeted, increasing crop losses and negative environmental impacts IPM has gone a long way in solving these problems by utilizing a collection of pest monitoring and control strategies designed to maintain pest populations below levels causing economic loss This almost always includes genetic host plant resistance combined with biological control, cultural methods, behavioral methods and farmer knowledge Effective IPM strategies have now been developed for many crops, including those that feed the developing world, and further improvements are continually being made The second pest control technology reviewed utilizes crop genetic engineering Genes from the bacterium, Bacillus thuringiensis (Bt), strains of which have long vii viii Foreword been used as microbial insecticides, are added to the genome of crop plants There the Bt genes express proteins that are toxic to target agronomic pests but not to other organisms The technology has spread rapidly and in 2007 maize and cotton crops having this new form of host plant resistance were planted on 42 million hectares in 22 countries Control of target insects has been excellent, insecticide use has been reduced significantly and strategies designed to delay or prevent the development of insects resistant to the Bt proteins have so far worked successfully Field trials of numerous other crops containing Bt genes have demonstrated similar efficacy Clearly this is a powerful new pest control technology that needs to be used wisely and for the benefit of a much greater number of the world’s farmers, including those who cannot afford premium priced seed Several chapters in this book present evidence indicating that it should be possible to integrate crop plants having host plant resistance from Bt genes into existing and emerging IPM strategies Unlike insecticides, Bt proteins are toxic only to the specific targeted pests and only to those insects that feed on Bt plant tissues They are not toxic to all the other beneficial insects and organisms that are essential for biocontrol and ecosystem balance within an effective IPM system To achieve integration and broader adoption of these two pest control strategies, further research is needed to: (1) develop an even better understanding of the impact of Bt crops on the general ecology of pests populations and their natural enemies, particularly under field conditions, (2) develop Bt based host plant resistance in a broader range of locally adapted crop varieties, including those that are essential for food security and economic growth in developing countries, and (3) develop strategies for incorporating Bt varieties into IPM systems in a ways that are most compatible with all other components of the IPM systems, are durable and empower farmers to become even more competent in the management of both pests and natural resources This book is an excellent first step in bringing together in one volume the relevant information necessary to achieve this integration of technologies Now it is up to the IPM specialists and the crop genetic engineers to work together more effectively than they have to date to provide farmers throughout the world with the best pest control methods science has to offer Gary Toenniessen Managing Director Rockefeller Foundation Preface Insect pests remain one of the main constraints to food and fiber production worldwide despite farmers deploying a range of techniques to protect their crops Modern pest control is guided by the principles of integrated pest management (IPM), defined as “a decision support system for the selection and use of pest control tactics, singly or harmoniously coordinated into a management strategy, based on cost/benefit analyses that take into account the interests of and impacts on producers, society, and the environment” (Kogan, 19981) Pest resistant germplasm should be an important part of the foundation for IPM, but traditional breeding has not been able to achieve insect-resistant germplasm to many of our most serious pests In the past decades, molecular tools of biotechnology have become available that allow the transfer of genes that provide strong plant resistance to certain groups of pests Products of such genetic engineering procedures have been termed “genetically modified (GM)” by the public, although we take issue with this term since all of our agriculturally important plant species have been “modified” by farmers and breeders in some way over the last 10,000 years of agriculture However, the editors and authors use the term GM because of its common use, as well as the terms “genetically engineered”, “transgenic crops”, or “biotech crops” Since 1996, when the first insect-resistant GM maize variety was commercialized in the USA, the area planted to insect-resistant maize and cotton varieties has grown to 42.1 million hectares in 22 countries in 2007 This represents the fastest adoption rate of any agricultural technology in human history While GM varieties have proven to be a powerful tool for pest management and their use has been accompanied by dramatic economic and environmental benefits, parts of the world (including most of Europe) are still engaged in discussions about potential negative impacts of these crops on the environment Fear about potential negative effects of GM crops has lead to the implementation of very stringent regulatory systems in several countries and regulations that are far more restrictive for GM crops than for Kogan, M., 1998 Integrated pest management: Historical perspectives and contemporary developments Annual Review of Entomology 43: 243–270 ix x Preface other agricultural technologies This has precluded many farmers and consumers from sharing benefits these crops can provide In this book we focus on insect-resistant GM plants and their place in agricultural IPM systems These plants are designed to protect the crop from specific major insect pests in a very effective manner As such the deployment of GM varieties will affect the way farmers manage their crop and, in particular, the way they apply other pest control measures The intent of this book is to provide an overview of the development, adoption, and impact of insect-resistant GM plants and the role they play or could potentially play in IPM in different crop systems worldwide We hope that the book will contribute to a more rational debate about the role GM crops can play in plant protection for food and fiber production Jörg Romeis Anthony M Shelton George G Kennedy 426 A.M Shelton et al discourses on biotechnology, farmers are adopting GM plants if they see an advantage in using them This is now happening in Vietnam and Brazil And if GM seed are too expensive or bureaucratically restricted, farmers make, trade, and save their own stealth seeds (Herring, 2007a) The Indian example is interesting because it illustrates the long-standing power of Indian farmers No regime in Delhi, or in many other countries, can ignore the farmers as a voting block, nor can regulations from Delhi that are opposed by rural people be enforced in the villages The Bt cotton episode in Gujarat illustrates this phenomenon: the genetic engineering approval committee (GEAC) ordered the destruction of the stealth-seed cotton crop, but had no power to enforce its edict on either the state government or the farmers Social and cultural contexts are critical in explaining differential spread of biotechnology, both above ground-through official channels- and underground through farmers’ stealthful agency Unfortunately, for the adoption of GM plants an alternative outcome is also possible Paarlberg (2007) makes the argument that in all countries in Africa (except for South Africa) no GM crops can be planted because of post-colonial European influence over governmental policies in Africa He argues that this influence extends to international commodity markets, financial and technical assistance policies, European dominance with the special agencies of the United Nations, and advocacy campaigns by European-based NGOs Thus, he concludes that Europe, “where farmers can be highly productive and consumers well-fed, has exported its rejection of GMOs to Africa” where the opposite occurs Unlike in India, African states are not faced with highly mobilized and assertive farmers, nor does an established democratic machinery allow African farmers to present their interests and punish at the polls those who work against their interests However, the situation in Africa may change with recent pressure in several countries by farmers who wish to produce Bt cotton (e.g., Burkina Faso, Kenya, Uganda) and Bt maize (Kenya, Uganda) and other crops Farmers’ visits to South Africa and India to see insect-resistant GM crops have spurred their interests (Shelton, unpublished), and studies have shown the benefits of GM plant technology for Africa (Thomson, 2008) However, for legal production, biosafety laws must be passed But if their biosafety regulations are too restrictive or not balanced (i.e not compare risks and benefits of GM technology to other technologies), then GM crops, including insect-resistant varieties, may not be available to farmers…at least legally 14.4 Conclusions Controversies in biology are not new Controversy about evolution continues to exist in many countries, although most biologists accept evolution as a unifying principle of biology Likewise, controversies in agriculture continue to garner public attention In the early 1900s consumption of raw milk accounted for high infant mortality rates in the USA Pasteurization of milk, a major food safety innovation that resulted from basic scientific studies, virtually eliminated this problem but was 14 Thoughts for the Future 427 highly controversial for many of the same reasons some critics use against biotechnology (Shelton et al., 2002b) In genetic engineering, one type of biotechnology, controversy followed the first recombinant DNA experiments (1972) by Boyer and Cohen when they manufactured insulin (Kelves, 2001) Controversy about the use of Bt plants for insect management has focused largely on their potential to affect non-target organisms such as the monarch butterfly (Shelton and Sears, 2001) and natural enemies (Romeis et al., chapter 4), or cause insect pests to develop resistance to the plants (Ferré et al., chapter 3) But as documented in the chapters of this book, an abundance of studies have indicated that, compared to other insectmanagement technologies, use of Bt plants has provided definite benefits not only to farmers but also to the environment and overall global economy (Qaim et al., chapter 12; Fitt, chapter 11) The increasing demands that are being placed on the global food, energy and fresh water supplies by population growth and economic development will necessitate increased efficiency in agricultural production This is especially evident in developing countries where 83% of the world’s population presently resides, where population growth rates are highest and where agricultural problems are most severe Crops with improved input and output traits derived by genetic engineering will certainly be able play a vital role in meeting this need For example, insectresistance GM plants provide the ability to significantly reduce the energy and labor required to manage insect pests, as well as the ecological impact of insect management when used within the context of IPM programs It is also important to remember that the present genetically engineered insect-resistant crops of cotton and maize are primarily used for fabric and processed food ingredients, respectively However, insect-resistant plants can and should play an increased role in providing food crops, such as potatoes, rice, fruits and vegetable, to meet the growing needs of consumers Worldwide, there is increased demand for foods with fewer residues of potentially harmful pesticides and, in fact, this is one of the drivers of the increased marketing of organic foods We suggest that the organic community reevaluate their opposition to using genetically engineered insect-resistant crops if, in fact, a major goal of their approach to agriculture is to reduce the risk of agriculture to human health and the environment As the scientific evidence on Bt plants has accumulated since 1996, it is clear that they have provided substantial benefits to human health and the environment It appears fortunate that the first insect-resistant GM plants produced Bt proteins, since they have a long history of safe use Indeed, Bt plants can be considered another delivery method of such proteins that were so strongly advocated by Carson (1962) in Silent Spring As new insecticide molecules are being developed for expression in plants (Malone et al., chapter 13) or plant genes are altered to affect biochemical pathways to elicit insect resistance, they must also be evaluated to ensure their safety But risk assessments need to be done in context and be conducted in a scientifically rigorous manner with testable hypotheses and formal decision guidelines (Raybould, 2007; Johnson et al., 2007; Romeis et al., 2008) When done properly, there should be a high degree of transparency of the risk assessment process and transportability of results from risk assessment studies 428 A.M Shelton et al across crops and countries This will ensure that countries with limited resources will have access to vital information with which to make regulatory decisions Countries that delay in developing workable, biosafety regulations, for whatever reason, will be challenged by farmers if they see benefits to the technology In today’s world, information and products move more freely across political boundaries than ever before References Bates, S.L., Zhao, J.-Z., Roush, R.T., and Shelton, A.M., 2005 Insect resistance management in GM crops: Past, present and future Nature Biotechnology 23: 57–62 Brookes, G., and Barfoot, P., 2006a Global impact of biotech crops: Socio-economic and environmental effects in the first ten years of commercial use AgBioForum 9: 139–151 Brookes, G., and Barfoot, P., 2006b GM Crops: The First Ten Years – Global Socio-Economic and Environmental Impacts ISAAA Brief No 36, International Service for the Acquisition of Agri-Biotech Applications, Ithaca, NY, USA Carson, R., 1962 Silent Spring Houghton Mifflin, Boston, MA, USA CBD Secretariat, 2000 Secretariat of the Convention on Biological Diversity Cartagena Protocol on Biosafety to the Convention on Biological Diversity: Text and Annexes Secretariat of the Convention on Biological Diversity, Montreal, Canada Chen, M., Zhao, J.-Z., Colins, H.L., Earle, E.D., Cao, J., and Shelton, A.M., 2008 A critical assessment of the effects of Bt transgenic plants on parasitoids PLoS ONE 3(5): e2284 doi:10.1371/journal.pone.0002284 Easterbrook, G., 1997 Forgotten benefactor of humanity The Atlantic Monthly 279: 75–82 Goklany, I., 2002 From precautionary principle to risk-risk analysis Nature Biotechnology 20: 1075 Herring, R.J., 2007a Stealth seeds: Bioproperty, biosafety and biopolitics Journal of Development Studies 43: 130–157 Herring, R.J., 2007b Suicide seeds? Biotechnology meets the development state http://casi.ssc upenn.edu/india/index.html (accessed 11 January 2008) Hesser, L., 2006 The man who fed the world: Nobel Peace Prize Laureate Norman Borlaug and his battle to end world hunger Durban House Publishing, Dallas, TX, USA James, C., 2007 Global Status of Commercialized Biotech/GM Crops: 2007 ISAAA Brief No 37, International Service for the Acquisition of Agri-Biotech Applications, Ithaca, NY, USA Johnson, K.L., Raybould, A.F., Hudson, M.D., and Poppy, G.M., 2007 How does scientific risk assessment of GM crops fit within the wider risk analysis? Trends in Plant Sciences 12: 1–5 Kelves, D.J., 2001 The battle over biotechnology In: Days of Destiny, Crossroads in American History, D Rubel, ed., DK Publishing, New York, USA, pp 453–463 Kovach, J., Petzoldt, C., Degni, J., and Tette, J., 1992 A method to measure the environmental impact of pesticides New York’s Food and Life Sciences Bulletin NYS Agricultural Experiment Station, Cornell University, Geneva, NY, USA http://www.nysipm.cornell.edu/ publications/eiq/ (accessed January 2008) Marvier, M., McCreedy, C., Regetz, J., and Kareiva, P., 2007 A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates Science 316: 1475–1477 O’Callaghan, M., Glare, T.R., Burgess, E.P.J., and Malone, L.A., 2005 Effects of plants genetically modified for insect resistance on nontarget organisms Annual Review of Entomology 50: 271–292 Paarlberg, R., 2007 Keeping genetically engineered crops out of Africa (Abstract) Workshop on contentious knowledge and the diffusion of social protest http://www.socialsciences.cornell edu/0609/Diffusion.html#Agenda/ (accessed January 2008) 14 Thoughts for the Future 429 Painter, R.H., 1951 Insect Resistance in Crop Plants University of Kansas Press, Lawrence, KS, USA Raybould, A., 2007 Ecological versus ecotoxicological methods for assessing the environmental risks of transgenic crops Plant Science 173: 589–602 Romeis, J., Meissle M., and Bigler, F., 2006 Transgenic crops expressing Bacillus thuringiensis toxins and biological control Nature Biotechnology 24: 63–71 Romeis, J., Bartsch, D., Bigler, F., Candolfi, M.P., Gielkens, M.M.C., Hartley, S.E., Hellmich, R.L., Huesing, J.E., Jepson, P.C., Layton, R., Quemada, H., Raybould, A., Rose, R.I., Schiemann, J., Sears, M.K., Shelton, A.M., Sweet, J., Vaituzis, Z., and Wolt, J.D., 2008 Assessment of risk of insect-resistant transgenic crops to nontarget arthropods Nature Biotechnology 26: 203–208 Sanvido, O., Romeis, J., and Bigler, F., 2007 Ecological impacts of genetically modified crops: Ten years of field research and commercial cultivation Advances in Biochemical Engineering and Biotechnology 107: 235–278 Shelton, A.M., and Sears, M.K., 2001 The monarch butterfly controversy: Scientific interpretations of a phenomenon The Plant Journal 27: 483–488 Shelton, A.M., Zhao, J.-Z., and Roush, R.T., 2002a Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants Annual Review of Entomology 47: 845–881 Shelton, A.M., McCandless, L., Lewenstein, B., Hawkes, J., Lyson, T., Bauman, T., and Aldwinckle, H 2002b Agricultural biotechnology: Informing the dialogue, 2002 Available online at http://www.nysaes.cornell.edu/comm/gmo/ (accessed January 2008) Stern, V.M., Smith, R.F., van den Bosch, R., and Hagen, K., 1959 The integrated control concept Hilgardia 29: 81–101 Tabashnik, B.E., Carrière, Y., Dennehy, T.J., Morin, S., Sisterson, M.S., Roush, R.T., Shelton, A.M., and Zhao, J.Z., 2003 Insect resistance to transgenic Bt crops: Lessons from the laboratory and field Journal of Economic Entomology 96: 1031–1038 Thomson, J.A., 2008 The role of biotechnology for agricultural sustainability in Africa Philosophical Transactions of the Royal Society B 363: 905–913 Van Emden, H.F., and Peakall, D.B., eds., 1996 Beyond Silent Spring: Integrated Pest Management and Chemical Safety Chapman & Hall, London, UK Index A Acrosternum hilare 165, 284 Adoption dynamics 338 Adzuki bean weevil See Callosobruchus chinensis African stem borer See Busseola fusca African sugarcane borer See Eldana saccharina Agricultural Biotechnology Stewardship Technical Committee (ABSTC) 67, 71, 136, 292 Agricultural sustainability 293, 294 Agriotes ipsilon (Black cutworm) 3, 127, 133, 196, 277, 393 Agrobiodiversity 350, 351, 353 See also Biodiversity Agroecosystem 2, 3, 17, 18, 273, 422 Alabama argillacea (Cotton leafworm) 164, 305 Alpha-amylase inhibitor 94, 107, 357, 360, 389–391, 400, 402 Aminopeptidase-N 53 Amrasca terraereginae 167 Anthonomus grandis (Boll weevil) 166, 170, 178, 284, 310, 393, 394 Antibiosis 12, 89, 121, 304 Antixenosis 12, 89, 90, 121 Apanteles chilonis 228 Aphids 16, 17, 92, 93, 100, 103, 106, 133, 138, 140, 167, 169, 178, 195, 198–200, 202, 205, 208, 210, 211, 213, 251–255, 260, 261, 263, 289, 309, 310, 317, 318, 338, 359, 362, 366, 370, 371, 374, 375, 377, 383, 389, 401 See also Aphis gossypii, Macrosiphum euphorbiae, Myzus persicae, Sitobium avenae Aphelinus abdominalis 362, 366, 367, 371, 374, 383 Aphidius ervi 362, 367, 371, 374, 375, 383 Aphidius nigripes 371, 374 Aphis gossypii (Cotton aphid) 16, 165, 167, 169, 170, 317, 370, 378, 379, 388, 389 Apis mellifera (Honey bee) 128, 177, 395 Aprotinin 367 Arabidopsis 107, 371, 372, 401 Archytus marmoratus 91 Area-wide Effects 186 Management 175, 278 Populations 15, 18, 279, 281, 282 Argentina 11, 17, 120, 126, 127, 133, 159–161, 164–166, 172, 178, 182, 305, 307, 315, 320, 330–335, 344, 349, 351 Asian corn borer See Ostrinia furnacalis Australia 17, 30, 32, 44, 47, 48, 52, 61, 65, 68, 99, 159–161, 163–184, 227, 235, 259, 281, 287, 292, 305–309, 313, 317, 318, 230, 322, 329, 330, 349, 363, 369, 370, 390–393 Austroasca viridigrisea 167 B Bacillus cereus 205, 206, 394 Bacillus thuringiensis (Bt) Bt aizawai 42 Bt israelensis 42 Bt kurstaki 42, 44, 49, 204 Bt thuringiensis 1, 2, 6, 27, 41, 42, 44, 47, 49, 87, 88, 119, 124, 141, 159, 160, 184, 185, 195, 196, 204–206, 223, 255, 258, 273, 275, 329, 331, 357, 391, 393, 394, 419, 420 Insecticide 42, 62, 73, 260 See also Bt crops, Cry toxins Beauveria bassiana 140 Bemisia tabaci 100, 165, 167, 169 Bean chitinase 205 Binary toxin 11, 15, 43 431 432 Biodiversity Arthropod abundance 96, 98, 108, 128, 146, 290 Species richness 96, 98, 228, 266, 293 Biological control 16, 17, 31, 87–108, 122, 123, 141, 169, 170, 176, 177, 185, 186, 200, 227–229, 260, 360, 380 Classical 103 Conservation 105, 169 See also Non-target effects Biosafety Regulations 347–349, 426, 428 See also Cartegena Protocol on Biosafety, Non-target effects, Risk assessment Biotin-binding proteins (BBP) 395, 396 Avidin 94, 395, 397 Streptavidin 395 Black cutworm See Agriotes ipsilon Black market seeds 311, 313, 315, 352 Bollgard® 32, 61, 64, 64, 310, 358, 398 Bollgard II® 32, 44, 63–65, 99, 133, 163, 172, 178, 184, 287, 306–310 Bollgard III® 184 Bollworms 14, 17, 18, 43, 61, 64, 105, 159, 162–164, 167–169, 172, 173, 175, 178, 184, 277, 278, 305, 310, 320, 370, 425 See also Diparopsis castanea, Heliothis spp., Helioverpa spp., Pectinophora spp Borlaug, Norman 420, 421 Brassica oleracea 90, 256, 258 See also Bt-crops (Broccoli, Cabbage, Cauliflower) and Cabbage Brazil 120, 126, 159–161, 164–166, 172, 182–184, 186, 252, 393, 426 Breeding capacity 352 Brevibacillus laterosporus 393 Bruchus pisorum (Pea weevil) 389–391 Bt crops Adoption 30, 31, 67, 240, 287, 329, 342, 352 Brassica 256–258, 265 Broccoli 65, 107, 256–258, 261, 265, 423 Cabbage 46, 164, 256–260, 265, 277, 285, 372 Cauliflower 256–260, 265, 363 Corn See Maize Cotton 1, 6, 9, 11, 13–18, 32, 34, 41, 43, 44, 47, 48, 51, 61–64, 68, 71, 72, 98– 101, 103, 106, 137, 142, 159–165, 167–196, 230, 232, 234, 235, 240, 241, 258, 264, 267, 275–281, 283, 284, 286, 287, 290, 292, 303–315, 317–323, 329–338, 340–343, 348–353, 359, 370, 388, 419, 420, 422, 423, 425, 426 Eggplant 264, 322, 33, 340, 343, 344, 353 Index Maize 1, 6, 8, 9, 11, 13–18, 34, 36, 43, 48, 49, 61, 62, 67, 71, 72, 92, 94, 97–100, 119, 124–126, 128–137, 139–142, 144–146, 171, 172, 177, 183, 184, 230, 232, 235, 238, 241, 255, 258, 265, 275, 277–285, 290, 292, 303, 315, 316, 320, 322, 329, 330, 332–334, 340, 344, 345, 350, 351, 353, 419–422, 424, 426 Potato 8, 100, 196, 210, 212, 213, 266, 329 Rice 9, 16, 44, 94, 96, 97, 99, 100, 223–242, 267, 330, 333, 353, 387 Bt maize Economic tool (BET) 137 Bt resistance 28, 51, 73, 206, 207, 258, 288, 304, 333, 334 See also Insect Resistance Management (IRM) and Resistance Bt spray 46, 50, 130, 171, 172, 204, 228, 229, 260, 288 See also Bacillus thuringiensis insecticide Bt toxin 6, 10, 15, 16, 18, 58, 94, 95, 101, 103, 130, 137, 139, 141, 160, 163, 168, 171, 173, 176, 178, 181, 186, 206, 210, 232, 235, 237–241, 305, 317, 331, 358, 359, 399, 400, 423, 429 See also Cry toxins Budworm See Heliothis virescens Burkina Faso 160, 426 Busseola fusca (African stem borer) 127, 143–145, 333 Bucculatrix spp 164, 305 C Cabbage 46, 164, 256–260, 265, 277, 285, 372 Caddisflies See Trichoptera Cadherin gene 53, 54, 57, 58 Cadherin-like protein 53, 56 Callosobruchus spp C analis (Graham bean weevil) 390, 391 C chinensis (Adzuki bean weevil) 389–391 C maculatus (Cowpea weevil) 389, 391 Canada 17, 29, 30, 32, 119, 120, 126, 133, 134, 142, 198, 235, 329, 330, 349 Carpophilus lugubris (Dusky sap beetle) 103, 256 Carson, Rachel 420, 421, 427 Cartagena Protocol on Biosafety (CPB) 27, 34, 35, 425 Cauliflower 256–260, 265, 363 Chilo spp C infuscatellus (Millet borer) 141 C orichalcociliellus (Coastal stem borer) 143 Index C partellus (Spotted stem borer) 123, 127, 143, 144, 333 C suppressalis (Striped stem borer) 44, 223, 224, 228, 232, 235–237, 239, 240, 333, 363, 399 China 11, 17, 19, 30, 34, 43, 48, 61, 62, 65, 68, 99, 106, 119, 120, 123, 127, 128, 130, 133, 140–142, 144, 146, 159–161, 164–170, 172, 173, 178–184, 186, 225, 226, 228, 229, 232, 234, 235, 240, 249, 250, 252, 254, 267, 305–308, 311–314, 317, 318, 329, 330, 333–337, 340–343, 349, 351, 353, 358, 360, 363, 369, 370, 378, 387, 388, 392, 399 Chitinases 132, 205, 357, 389, 390, 397, 398, 402 Chrysoperla carnea (Green lacewing) 93, 95, 99, 129, 169, 260, 381, 393 Chrysoperla sinica 228 Cnaphalocrocis medinalis 224, 363, 378, 399 Coleomegilla maculata 92, 100, 256 Collaboration on Insect Management for Brassicas in Asia and Africa (CIMBAA) 257, 259–261 Collembola 229, 366 Colorado potato beetle See Leptinotarsa decemlineata Colombia 159–161, 164–166, 171, 182 Conogethes punctiferalis (Yellow peach borer) 141 Consumer Acceptance 211, 214, 241, 329, 330, 345, 352, 353 Attitudes 212, 347, 353 Corn earworm See Helicoverpa zea Corn silk fly See Euxesta stigmatias Coastal stem borer See Chilo orichalcociliellus Cotesia spp C flavipes 123, 143, 384 C congregata 91 C sesamiae 143 Cotton Bt cotton 1, 6, 9, 11, 13–18, 32, 34, 41, 43, 44, 47, 48, 51, 61–64, 68, 71, 72, 98–101, 103, 106, 137, 142, 159–165, 167–196, 230, 232, 234, 235, 240, 241, 258, 264, 267, 275–281, 283, 284, 286, 287, 290, 292, 303–315, 317–323, 329–338, 340–343, 348–353, 359, 370, 388, 419, 420, 422, 423, 425, 426 CpTI cotton 43, 65, 161, 360, 369, 370, 398–400 GNA cotton 378, 388 Vip cotton 103, 392, 393 433 Cotton aphid See Aphis gossypii Cotton leafworm See Alabama argillacea Cotton tipworm See Crocidosema plebejana Cowpea trypsin inhibitor (CpTI) 43, 65, 161, 205, 226, 231, 232, 234, 241, 358, 360, 362–364, 369, 370, 378, 399, 400 Cowpea weevil See Callosobruchus maculatus Creontiades dilutus (Green mirid) 17, 165, 167 Crocidolomia binotalis 260 Crocidosema plebejana (Cotton tipworm) 164, 305 Cryptolestes ferrugineus 397 Cry protein See Cry toxins Cry toxins 2, 6, 9, 13, 37, 41, 42, 44–46, 49, 50, 52–57, 59–62, 69, 70, 87, 92, 94, 96, 98, 100, 105–108, 119, 124, 127, 129, 132, 133, 144, 159, 163, 171–173, 176, 184, 204, 205, 207, 225, 228–230, 240, 255, 258, 260, 261, 288, 289, 331, 357–360, 377, 387, 389, 391–393, 396, 400–403, 420, 421, 424 Cry1Aa 44, 55, 56, 58, 161, 225, 226 Cry1Ab 15, 43–45, 47–50, 52, 55, 56, 58, 61, 64, 65, 92–95, 97, 98, 125, 127, 129, 133, 136, 137, 139, 141, 142, 144, 161, 225, 226, 228–230, 239–241, 255, 256, 284, 285, 287, 288, 315, 316, 358, 392, 393 Cry1Ac 14, 43, 44, 47, 48, 52, 55–58, 61, 65, 68, 72, 98, 104, 125, 144, 161, 164, 168, 173, 174, 177, 184, 204, 208, 225, 226, 230, 232, 239, 240, 258, 262, 287, 288, 305, 306, 313, 315, 319, 358, 369, 370, 388, 391, 392, 399, 400 Cry1A.105 133, 358 Cry1Ba 55, 144 Cry1Ca 55, 56, 144 Cry1E 144 Cry1F 15, 33, 43, 44, 55, 56, 61, 64, 125, 127, 130, 137, 161, 184, 284, 285, 287, 358 Cry1Ia1 204, 206, 212 Cry1J 55, 56, 64 Cry2Aa 47, 52, 55–57, 144 Cry2Ab2 133, 161, 173, 174, 358 Cry3 11, 94, 124, 276, 282, 358 Cry3Bb1 63, 92, 125, 315, 358 Cry5B 55, 58 Cry9C 8, 9, 43, 69, 125 Cry34Ab1 125, 282, 358 Cry35Ab1 282, 358 Modified Cry3A 125, 127, 392 Mode of action 42, 52, 94, 133 434 Ctenognathus novaezelandiae 362, 368, 396 Cultural control 17, 121, 122, 138, 170, 200 Cyrtorhinus lividipennis 100, 228, 229 D Damage control framework 331 Danaus plexippus (Monarch butterfly) 18, 92, 129, 285, 427 Decision Making 28, 124, 137, 168, 223, 232, 233, 347 Rules 2, 13 Defensins 357, 389–391, 402 Delta-endotoxins 42, 87, 94, 184, 185, 276 See also Cry toxins Diadegma insulare 260, 423 Diaeretiella rapae 371, 375 Diabrotica spp (Rootworm) D virgifera virgifera (Western corn rootworm) 15, 63, 95, 121, 138, 282, 390 D barberi (Northern corn rootworm) 122, 135, 137, 282 D undecimpunctata howardi (Southern corn rootworm) 135, 394 Diamondback moth See Plutella xylostella Diatraea spp D grandiosella (Southwestern corn borer) 127, 133, 135, 277 D saccharalis (Sugarcane borer) 49, 127, 277, 283, 378, 384 Diparopsis castanea (Red bollworm) 164, 165, 305 Dipel® 44, 45, 47–49, 55 Distributional impact 336 Dow AgroSciences 33, 124, 125, 184, 358, 392, 394 Dusky sap beetle See Carpophilus lugubris E Economic impact 182, 316, 335, 345 Economic injury level (EIL) 12, 14, 87, 88, 121, 123, 138, 168, 186, 199, 207, 360 Economic threshold (ET) 14, 62, 121, 123, 138, 168, 186, 199, 207, 360 Eggplant fruit and shoot borer See Leucinodes orbanalis Egypt 160, 207, 212 Eldana saccharina (African sugarcane borer) 143 Empoasca fabae (Potato leafhopper) 196, 200, 211 Encarsia formosa 90 Endangered species 10, 18, 285 Enhancins 357, 394 Index Enzyme-linked immunosorbent assays (ELISA) 229 Ephestia cautella 44 Euchistus servus 284 Eulophus pennicornis 96, 364, 365, 382, 385, 386 European Food Safety Authority (EFSA) 31, 68 Ethical concerns 7, 345 Environment effects 6–8, 31, 90, 108, 315 Benefits 2, 11, 13, 20, 28, 105, 169, 182, 263, 304, 348, 419 Concerns 8, 9, 89, 129, 141, 177, 263, 290, 319 See also Gene flow, Non-target effects Environmental Impact Quotient (EIQ) 31, 178, 306, 310, 311, 422 Eoreuma loftini 378, 380, 384 Epicuticular waxes 90, 107, 108 Eriborus terebrans 123 Europe, European Union (EU) 8, 28, 29, 31, 44, 49, 68, 122, 128–130, 137, 139, 196, 200, 211–214, 227, 250, 264, 283, 315, 344, 349, 371, 426 European corn borer See Ostrinia nubilalis Euxesta stigmatias (Corn silk fly) 103, 256 Exotic stem borer See Chilo partellus F Fall armyworm See Spodoptera frugiperda Feltia jaculifera (Dingy cutworm) 279, 280 F2 screen 51, 70, 240 Fitness cost 57, 63, 65, 237, 286, 288, 424 Food safety 180, 241, 264, 317, 341, 344, 347, 353, 426 Food Quality Protection Act (FQPA) 32 Frankliniella spp F occidentalis (Western flower thrips) 167, 372, 399, 401 F schultzei 167 F tenuicornis 93, 112 Fruit 11, 16, 44, 160, 170, 178, 250–252, 255, 261, 262, 265, 266, 333 See also Papaya Fusion gene 43, 44, 61, 65 Fusion proteins 357, 360, 398–400, 402 G Galanthus nivalus agglutinin (GNA) 96, 106, 225, 244, 363, 377, 378, 380–389, 398, 399, 408, 414–416 Gene Flow 128, 129, 146, 177, 178, 209, 421 See also Outcrossing Index Gene Transfer 7, 9, 277 Genetic effects 291 Genetic engineering 5–7, 19, 87, 88, 107, 195, 196, 203, 208–210, 225, 263, 347, 351, 424, 426, 427 Germplasm effect 337 Glycoalkaloids 195, 201, 202, 208, 209 Golden rice 241, 242 Gonsalves, Dennis 265 Graham bean weevil See Callosobruchus analis Green lacewing See Chrysoperla carnea Green peach aphid See Myzus persicae Green revolution 227, 236, 350, 420 Gross margins 11, 139, 140, 334–338, 352 H Harmonia axyridis 100, 256, 373 Health Benefits 11, 128, 196, 311, 314, 329, 341, 344, 345, 352, 353 Concerns 19, 202, 211, 420 Effects 98, 300, 341–343, 345 Helicoverpa spp H armigera 14, 43, 46, 47, 52, 53, 57, 58, 61, 62, 95, 106, 127, 139–142, 163, 164, 168, 170, 172, 178, 180, 235, 260, 277, 305, 311, 313, 314, 317, 320, 322, 363, 367, 370, 391, 398, 399, 425 H gelotopoeon 164, 305 H punctigera 164, 320, 363, 391 H zea 14, 21, 43, 48, 52, 61, 62, 69, 73, 75, 78, 91, 99, 121, 127, 130, 136, 137, 163, 164, 173, 255, 256, 277, 279, 280, 281, 305, 316, 320, 398 Heliothis spp H virescens 18, 43, 45–47, 51–53, 56–58, 61, 62, 73, 96, 164, 277, 279, 284, 305, 310, 320, 370, 391, 397, 398 Hellula undalis 260 Herbicide tolerance 15, 32, 43, 63, 72, 73, 87, 120, 124, 134, 184, 275, 279, 305, 306, 315, 421 Herculex® 61, 125, 358, 398 High dose / refuge strategy 19, 41, 60–64, 68, 73, 130, 139, 146, 206, 207, 236, 240, 263, 305, 424 Hippodamia convergens 90 Homeosoma electellum (Sunflower moth) 44 Honeydew 92, 93, 380, 388 Host plant resistance (HPR) 1, 2, 4, 5, 12, 13, 15, 19, 87, 88, 90, 121, 122, 132, 134, 138, 144, 146, 162, 170, 183, 185, 201, 202, 204, 207–209, 251, 304, 318, 421 435 Hypogaster annulipes 91 Hyposoter exiguae 91 I India 11, 17, 19, 32, 34, 36, 47, 62, 68, 120, 159–161, 164–167, 169, 170, 172, 173, 177–185, 225, 234, 235, 249, 250, 257, 259–261, 263, 305–307, 312, 313, 317, 318, 322, 329–333, 335–338, 340, 343, 344, 346–349, 351–353, 369, 378, 392, 425, 426 Indonesia 160, 183, 227, 254, 305 Ingard® 61, 65, 172, 178, 306, 308–310 Innovation rent 339, 340, 350 Insecticidal proteins 41–44, 46, 47, 50, 59–61, 63–66, 68, 72–73, 88, 91–94, 102, 106, 125, 132, 195, 205, 208, 256, 273, 275, 276, 282, 288, 293, 304, 322, 357, 360, 361, 380, 387, 391, 393–395, 400, 401, 403, 419, 420 See also Cry toxins, Protease inhibitors, Lectins, Alphaamylase inhibitor, Biotin-binding proteins Insecticide Active ingredient (a.i.) 98, 126, 306, 309, 315, 332, 422 Poisoning 311, 341–343, 353 Reduction 99, 170, 273, 311, 313, 314, 316, 331–33, 337, 338 Resistance 2, 208–210, 249, 332, 420, 423 Savings 311, 312, 316, 330, 335 Seed treatments 138, 260, 266 Use 1, 11, 15, 16 Insect Resistance Management (IRM) 10, 20, 29, 30, 32, 33, 41–73, 130–133, 144, 163, 171–174, 206–209, 235–239, 258, 263, 286–288, 322, 423, 424 Compliance 59, 63, 66–68, 70–73, 136, 142, 172, 183, 206 High dose/refuge strategy 10, 19, 41, 60–64, 68, 73, 130, 139, 146, 206, 207, 235, 236, 240, 263, 305, 322, 424 See also Resistance, Refuge and F2 screen Temporal rotation 65, 66 Insect Resistant Maize for Africa Project (IRMA) 144, 145 Insect viruses 394, 395 Integrated Pest Management (IPM) 1–21, 27–37, 67, 87–89, 90, 102, 104, 108, 119–147, 159–186, 195, 199, 208, 209, 249, 251, 254, 255, 260, 261, 263, 265–267, 273, 274, 276, 283, 284, 309–323, 357, 360–362, 377, 380, 392–395, 401–403, 419–423, 427 436 Intellectual Property Rights (IPR) 11, 13, 180, 259, 329, 331, 335, 337, 340, 350–353 International Maize and Wheat Improvement Center (CIMMYT) 144 Iran 225–227, 330, 387 Isolation distance 9, 129, 146 J Japanese beetle 256 Jassids 165, 261, 319, 370 K Kenya 119, 120, 123, 127, 133, 142–146, 426 Kenyan Agricultural Research Institute (KARI) 144 Key pest 1, 4–6, 14, 16, 17, 20, 97, 101, 102, 104, 106, 174, 186, 256, 266, 274, 276, 284, 304, 311, 314, 318, 320, 321, 421 L Labeling 29, 67, 129, 180 Labor 4, 8, 13, 34, 70, 104, 240, 335, 336, 427 Lacanobia oleracea (Tomato moth) 96, 205, 362–364, 385, 398 Ladybird beetles 31, 289, 381, 382, 400 See also Coleomegilla maculata, Harmonia axyridis, Hippodamia convergens, Propylea japonica Landscape-level (See also Area-wide) Effects 17–19, 105, 275, 277, 278, 288–291 Management 322 Laodelphax striatellus (Small brown planthopper) 224, 378 Larger grain borer See Prostephanus truncates Leaffolder 223–225, 227, 231, 233, 240 See also Cnaphalocrocis medinalis, Marasmia spp Leafhoppers 92, 103, 133, 138, 165, 167, 196, 202, 208, 224, 225, 228, 229, 231, 232, 251, 261, 263 See also Amrasca terraereginae, Austroasca viridigrisea, Empoasca fabae, Nephotettix spp Lectins Amaranthus caudatus lectin (ACA) 379, 388 Galanthus nivalis agglutinin (GNA) 96, 106, 225, 244, 363, 377, 378, 380–389, 398, 399, 408, 414–416 Garlic lectin 225, 377–379 Mode of action 377 Index Leptinotarsa decemlineata (Colorado potato beetle) 3, 8, 44, 46, 73, 97, 195–200, 204–211, 214, 283, 316, 363, 371–373, 376, 393, 394, 402 Leptocorisa spp (Rice bug) 224 Leucinodes orbonalis (Eggplant fruit and shoot borer) 44, 261–263, 333 Life system 3, 286 Lipid acyl hydrolases 389, 390 Lissorhoptrus oryzophilus (Rice water weevil) 224 Lydella thompsoni 97, 122, 138 Lygus spp 165, 167, 170, 175, 185, 392 L hesperus 100 L lineolaris (Tarnished plant bug) 281, 284 M Macrocentrus spp M cingulum 97, 122 M grandii 103, 105 Macrosiphum euphorbiae (Potato aphid) 199, 263, 366, 372, 374, 375, 383 Maharashtra Hybrid Seeds Company Limited (Mahyco) 190, 192, 262, 263, 337, 338, 351, 352, 354 Maize 1, 4, 6, 8, 9, 11, 13–18, 20, 30, 33, 34, 36, 41, 43, 48–50, 61–63, 66, 67, 69–72, 92–100, 103, 105, 119–146, 171, 172, 177, 183, 184, 195, 210, 212, 225, 230, 232, 235, 238, 240, 241, 250, 255, 256, 258, 265, 266, 275, 277–285, 287, 290, 292, 303, 304, 315, 316, 320, 322, 329, 330, 332–335, 340, 344, 345, 349–351, 353, 387, 396, 397, 399, 419–427 Maize weevil See Sitophilus zeamais Manduca sexta (Tobacco hornworm) 6, 53, 91, 397, 398 Marasmia spp 224 Mealy bugs 167 Media 211, 234, 312, 347, 425 Mediterranean corn borer See Sesamia nonagrioides Mexican bean weevil See Zabrotes subfasciatus Mexico 9, 11, 120, 129, 159, 161, 163–166, 171, 175, 176, 179, 182, 200, 278, 283, 305, 308, 329, 330, 332, 334, 345, 351 Milkweed 129, 285 Millet borer See Chilo infuscatellus Mirids 103, 167, 170, 175, 309, 310, 317, 318, 359, 370, 392 See also Index Creontiades dilutus, Cyrtorhinus lividipennis, Lygus spp Monarch butterfly See Danaus plexippus Monitoring Ecological 28, 29, 145 Population 4, 70, 134, 168, 173, 200, 279, 281, 284 Resistance 29, 30, 32, 58, 63, 67, 68, 70, 71, 139, 144, 174, 239, 240, 261, 263, 286, 424 Monsanto 71, 92, 125, 144, 184, 185, 196, 210, 252, 262, 335, 351, 352, 358, 390, 392 Mycotoxins 28, 128, 140, 341, 344, 345, 353 Mythimna separata (Oriental armyworm) 127, 141 Myzus persicae (Green peach aphid) 3, 196, 199, 200, 205, 263, 372, 375, 378, 379, 382 N National Corn Growers Association (USA) 71 Natural enemies 122, 140, 169, 261 Conservation 1, 20, 87, 88, 104, 108 See also Biological control Nectar 92, 104, 170, 360, 380, 403 Neonicotinoid 197, 198, 201 Neozygites fresenii 170 Nephotettix cinticeps 229 Nephotettix virescens (Green leafhopper) 224, 229, 378 NewLeaf® 8, 196, 210, 211 New Zealand 89, 180 Nezara viridula 165, 167, 284 Nilaparvata lugens (Rice brown planthopper) 3, 91, 102, 224, 228, 229, 363, 378, 379, 387, 398, 399 Non-Governmental Organizations (NGOs) 67, 183, 264, 312, 425, 426 Non-target effects 7, 10, 13, 16, 18, 27, 28, 31, 35, 88, 92, 94, 96, 106, 108, 128, 129, 144, 145, 146, 176, 177, 186, 228, 258, 266, 273, 276, 290, 291, 292, 304, 318, 321, 341, 394, 401, 424, 427 Direct effects 91, 94, 229, 289–291, 293 Exposure 10, 91, 285 Hazard 10, 91, 285 Indirect effects 91, 167, 229, 289, 291, 293, 360 Prey/host-quality mediated effects 95, 96, 260, 360 See also Biosafety regulations, Risk assessment 437 North American Free Trade Agreement (NAFTA) 29 Northern corn rootworm See Diabrotica barberi Nunhems seeds 259 O Organic 9, 124, 129, 146, 255, 288, 344, 423, 427 Oriental armyworm See Mythimna separata Orius spp O insidiosus 100, 256 O tristicolor 99 Orseolia oryzae (Asian rice gall midge) 224 Oryza sativa (Rice) 195, 224, 225, 230, 231, 235, 236 O nivara 230 O rufipogon 230–232 Ostrinia spp O furnacalis (Asian corn borer) 123, 127, 130, 140–142, 164, 378 O nubilalis (European corn borer) 15, 18, 43, 46, 48, 49, 52, 61, 62, 69, 72, 97–100, 103, 105, 119, 120–123, 127, 128, 130, 132–140, 164, 200, 204, 255, 256, 277, 279–282, 284, 315, 316, 320, 333, 393 Outcrossing 9, 130, 223, 230–232, 238 See also Gene flow P Pakistan 123, 160, 183, 225, 226, 240, 241, 369, 388 Papaya 35, 249, 252–255, 265, 266, 397 Parasitoids 16, 19, 31, 88, 90–92, 95–97, 101–103, 105–108, 122, 123, 128, 138, 141, 143, 169, 170, 176, 223, 227, 228, 258, 260, 288–290, 318, 321, 362, 364, 365, 367, 369, 371, 373, 374, 375, 377, 380, 381, 386, 392, 393, 396, 397, 400, 401, 403, 422, 423 Pea weevil See Bruchus pisorum Pectinophora spp P gossypiella (Pink bollworm) 18, 43, 46, 48, 51–53, 56, 58, 61–63, 67, 100, 105, 163, 164, 168, 171–173, 175, 240, 277, 278, 282, 283, 305, 310, 320, 370, 399 P scutigera (Pink spotted bollworm) 164, 305 Penknife model 54 Pepper 207, 254 Pest Adaptation 1, 10, 19, 20, 273, 286–288 Shift 16, 422 438 Pest outbreaks Pest resurgence 101, 102 Secondary pests 1, 2, 9, 16, 20, 101–106, 136, 137, 140, 142, 147, 163, 171, 186, 256, 266, 273, 276, 283, 284, 293, 311–313, 317–319, 334, 359, 392, 420 Phaseolus vulgaris (Bean) 107, 389, 391 Philippines 32, 34, 45, 55, 126, 127, 133, 227–229, 233, 236, 240, 252, 254, 261, 263, 330, 333, 345 Photorhabdus insect related proteins 394 Photorhabdus luminescens 394 Phthorimaea operculella (Potato tuber moth) 107, 195, 196, 198–200, 204, 206–210, 212–214 Pieris spp P brassicae 260 P rapae 260, 285, 303 Pink bollworm See Pectinophora gossypiella Pink spotted bollworm See Pectinophora scutigera Pink stem borer See Sesamia calamistis Pioneer Hi-Bred International 33, 125 Pisum sativum (Pea) 90 Plant-Incorporated Protectants (PIP) 67, 73 See also Insecticidal proteins Planthoppers 91, 100, 102, 224, 225, 227, 229, 387 See also Laodelphax striatellus, Nilaparvata lugens, Sogatella furcifera Plodia interpunctella (Indian meal moth) 44, 45, 55, 73 Plum 35 Plutella xylostella (Diamondback moth) 44–46, 52, 55, 56, 64, 73, 130, 208, 257–261, 285, 363, 367, 373, 394, 423 Podisus maculiventris 362, 364, 371, 376, 385 Poisoning 311, 341–343, 353 Pollen 18, 92, 94, 102, 104, 128, 129, 177, 228, 231, 266, 275–277, 285, 363, 367, 373, 423 Pollinators 16, 31 Potato Breeding 195–197, 201, 208, 209, 214 Bt potato 8, 94, 100, 196, 198, 210–213, 266, 329, 330 Future of GM potato 212–214 GNA potato 96, 378 History of GM potato 209–212 Potato aphid See Macrosiphum euphorbiae Potato leafhopper See Empoasca fabae Potato leafroll virus (PLRV) 195, 199, 213 Index Potato tuber moth See Phthorimaea operculella Potato virus Y (PVY) 195, 199, 200, 210 Poverty 336 Predators 3, 16, 31, 87, 88, 90–102, 106–108, 122, 123, 128, 129, 170, 176, 223, 227–229, 232, 256, 260, 279, 282, 284, 288–290, 316, 318, 321, 362, 364, 369, 371, 373, 375, 377, 380, 381, 385, 389, 390, 392, 393, 396, 397, 400, 403, 422, 423 Proceras venosatus (Sugarcane striped borer) 141 Promoters Constitutive 61, 66, 106, 387 Inducible 66, 107, 133, 204, 258 Phloem-specific 106, 387 Propylea japonica 228 Prostephanus truncates (Larger grain borer) 143 Protease Inhibitors (PI) 41, 93, 96, 102, 103, 132, 185, 225, 357, 359, 360–364 Bowman-Birk inhibitor (SbBBI) 362, 366 Cysteine Proteinase Inhibitors 204, 205 Cowpea trypsin inhibitor (CpTI) 43, 65, 161, 205, 225, 226, 231, 232, 234, 241, 358, 360, 362–364, 369, 370, 383, 388, 399, 400 Maize proteinase inhibitor (MPI) 66 Oryzacystatin (OC1) 205, 263, 371–375 Soybean Kunitz trypsin inhibitor 305 Pseudoperichaeta nigrolineata 97 Puerto Rico 33, 130 Push-pull strategy 143 Pyramid See Traits R Red bollworm See Diaparopsis castanea Refuge Compliance 59, 63, 66-68, 70-73, 136, 142, 172, 183, 206 Placement 21, 62, 73 See also Insect Resistance Management Size 21, 63, 64, 67, 71, 237 Regulation Regulatory framework 8, 27, 28, 424 Regulatory risk assessment 27, 28, 36, 94 Regulatory systems 8, 27, 28, 30, 33, 34, 36, 37, 259, 348 Resistance Allele frequency 52 Binding site competition 55 Cross resistance 19, 47, 48, 55–57, 64, 65, 198, 206, 259, 287 Index Evolution 41, 67, 68, 73, 147, 258, 260, 261, 263, 286, 287, 320, 358, 424 Field 33, 45, 46, 68, 171, 261, 359, 424 Laboratory 44–49, 54, 55, 57, 68, 73 Mechanism 10, 13, 57, 58, 141, 171, 208 Monitoring 29, 30, 32, 58, 63, 67, 68, 70, 71, 139, 144, 174, 239, 240, 261, 263, 286, 424 See also Insect Resistance Management (IRM) Rice (See also Oryza sativa) 195, 224, 243 Bt rice 9, 16, 44, 94, 96, 97, 99, 100, 223–242, 267, 330, 333, 353, 387 GNA rice 225, 378, 387 RNA interference (RNAi) 53, 95, 185, 322 Risk Assessment 8, 10, 27–29, 31, 34, 36, 37, 67, 68, 88, 94, 108, 144, 285, 291, 341, 400, 401, 427 See also Biosafety regulations, Environmental effects, Non-target effects, Tiered-testing Rootworm 11, 15, 43, 63, 70, 92, 121, 122, 127, 135, 138, 256, 278, 282, 315, 333, 358, 390, 393, 394 See also Diabrotica S Saprophagous Diptera 128 Scirpophaga incertulas (Yellow rice stemborer) 44, 223, 224, 235–237, 239, 240, 333, 363, 399 Scorpion toxins 398 Secondary metabolites (as insecticidal proteins) 202, 344, 401 Secondary pests 1, 2, 4, 16, 20, 101–106, 136, 137, 140, 142, 147, 163, 171, 186, 256, 266, 273, 276, 283, 284, 293, 311–313, 317–319, 334, 359, 392, 420 Seed Black Market 311, 313, 335, 352 Companies 72, 139, 181, 183, 212, 313, 335, 340, 350, 352 Farm-saved 335, 340 Markets 329, 331, 350–353 Mixture 59, 66, 206, 236–238 Sesamia spp S calamistis (Pink stem borer) 143, 232 S nonagrioides (Mediterranean corn borer) 52, 130, 138, 139, 143 Silent Spring 420, 427 See also Carson, Rachel Sitobium avenae (Wheat aphid) 389 Sitophilus zeamais (Maize weevil) 143, 397 Small farms 142, 144, 181, 183, 223, 235, 334, 336, 337, 341, 345 439 Snowdrop lectin 205, 225, 363, 377, 378, 381, 388, 398, 399 See also Galanthus nivalis agglutinin Socio-economic issues 7, 8, 19, 212, 239, 252 Sogatella furcifera (Whitebacked planthopper) 3, 224, 229, 378 Soil microorganisms 129, 223, 230, 232 South Africa 11, 34, 126, 133, 144, 145, 159–161, 165–167, 171, 173, 179–182, 207, 212, 213, 305, 307, 308, 314, 316–318, 329, 330, 333–336, 343, 345, 351, 353, 369, 426 Southern corn rootworm See Diabrotica undecimpunctata howardi Southwestern corn borer See Diatraea grandiosella Spain 11, 49, 52, 119, 10, 126, 127, 133, 137–139, 225, 226, 290, 316, 330, 332–335, 340 Spider mites 17, 93, 95, 102, 103, 140, 166, 167, 170, 178, 397 Spider toxins 398 Spodoptera spp (Armyworm) 44, 61, 100, 163, 164, 184, 277 S exigua (Beet armyworm) 64, 127, 140–142, 393, 394 S litura 53, 167, 260, 368, 396, 397 S frugiperda (Fall armyworm) 33, 43, 64, 99, 121, 127, 130, 133, 137, 255, 256, 277, 283, 316, 393 Spotted stem borer See Chilo partellus Squash 249, 252–254, 266 Stack See traits StarLink® 8, 9, 125 Stem and stalk borer 15, 44, 120, 123, 127, 130, 134, 135, 138, 139, 143, 145, 166, 223–225, 227, 231–235, 237, 239, 240, 316, 387 See also Busseola fusca, Chilo spp., Diatraea spp., Eldana saccharin, Ostrinia spp., Scirpophaga incertulas, Sesamia spp., Eoreuma loftini Stern, Vern 14, 120, 121, 420, 421 Stewardship 67, 70, 71, 136, 144, 186, 264, 265, 274, 292 Stinkbugs 17, 91, 103, 165, 167, 178, 359 See also Acrosternum hilare, Euchistus servus, Nezara viridula, Podisus maculiventris Streptomyces avidiniii 395 Striacosta albicosta (Western bean cutworm) 127, 137, 277, 284 Striped stem borer See Chilo suppressalis Sturmiopsis parasitica 143 440 Sugarcane striped borer See Proceras venosatus Surplus Consumer 339 Distribution 340 Economic 330, 339, 340, 353 Producer 339, 340 Sweet corn 50, 69, 99, 100, 103, 108, 125, 135, 138, 249, 255, 256, 265, 266, 316, 318, 319, 321 Syngenta 125, 184, 212, 358, 392 T Tarnished plant bug See Lygus lineolaris Technology fee 15, 132, 182, 184, 259, 334, 335, 339, 352 Temporal rotation 65, 66 Tetranychus urticae (Two-spotted spider mite) 95, 167 Thailand 45, 241, 252 Thecolax elegans 397 Thrips 93, 142, 166, 167, 171, 251, 261, 309, 310, 359, 370, 371, 392, 401 See also Frankliniella spp., Thrips tabaci Thrips tabaci 167 Tiered-testing (Tiered approach) 10, 28, 291 Tissue-specific expression 66 Tolerance 12–15, 32, 63, 72, 73, 87, 89, 90, 95, 119–122, 124, 134, 161, 163, 184, 185, 210, 275, 279, 291, 305, 306, 319, 421 Tomato 91, 173, 207, 210, 254, 358, 378, 386 Tomato moth See Lacanobia oleracea Toxin complex genes (tc genes) 394 Traits Stacked 15, 72, 124, 132, 134, 163, 208, 306, 358, 359, 360, 362, 392, 398, 399 Pyramided 133, 204, 213, 225, 240, 241, 287, 398 Transformation events Bt11 61, 92, 125, 126, 139, 141, 25, 256 DAS-21023–5 64 DAS-24236–5 64 DAS-59122–7 125, 126, 282 Event127 144 Event176 129, 139 Event396 144 MIR604 125, 126, 282 MON531 61, 64, 161 MON810 61, 92, 125, 126, 139, 141, 144 MON863 125, 126, 139 Index MON15985 64, 161 MON88017 125, 126 TC1507 33, 61, 125, 126 Trap crop 143, 255 Tribolium castaneum 397 Trichogramma spp T brassicae 138, 260, 381 T dendrolimi 141, 142 Trichomes 12, 90, 107, 108, 195, 201–203, 208, 209 Trichoptera 129 Tri-trophic interactions 13, 90, 362, 369, 380, 396, 397, 403 U Umbrella model 54 USA 4, 6, 8, 10, 11, 14, 15, 17, 18, 29, 30, 32, 33, 41, 44, 46–49, 99, 105, 119–123, 125–128, 130, 133–136, 140, 142, 159–161, 163–176, 178–182, 184, 186, 195–201, 204, 206, 210, 211, 213, 214, 235, 249, 252, 254–256, 259, 266, 275, 283, 285, 287, 292, 305, 306, 310, 315–317, 320, 322, 329, 330, 333–335, 337, 340, 344, 345, 347, 351, 353, 360, 369, 392, 423, 425, 426 US Department of Agriculture (USDA) 31, 70, 124, 126, 133–135, 163, 180, 275, 330, 337, 351, 392 US Environmental Protection Agency (US EPA) 8, 29, 31, 32, 62, 64, 66–69, 71, 73, 128, 172, 180, 287, 400, 423 US Food and Drug Administration (FDA) 180 US Scientific Advisory Panel (SAP) 68–70, 287 V Vegetable 11, 16, 35, 44, 50, 94, 99, 142, 167, 235, 249–267, 279, 280, 322, 344, 346, 347, 349, 421, 422, 427 See also cabbage, cauliflower, eggplant, pepper, potato, squash, sweet corn, tomato Vegetative insecticidal proteins (Vip) Vip1 206 Vip2 206 Vip3A 43, 94, 96, 98, 122, 184, 206, 256, 322, 391–393 Vietnam 231, 241, 426 VipCot® 64, 184 Virus diseases 196, 199, 200, 213 Virus resistance 210, 213, 252, 316 Index W Welfare Effects 340, 353 Gains 329, 340, 353 Western bean cutworm See Striacosta albicosta Western corn rootworm See Diabrotica virgifera virgifera Wheat aphid See Sitobium avenae Whiteflies 16, 17, 90, 165, 167, 169, 251 See also Bemisia tabaci WideStrike® 63, 64, 133, 163, 184, 358 Wound-induced expression 66 X Xenorhabdus nematophilus 394 Xestia c-nigrum (Spotted cutworm) 279, 280 441 Y Yellow peach borer See Conogethes punctiferalis Yellow stem borer See Scirpophaga incertulas Yield Effects 181, 182, 331–333, 337, 352 Increase 223, 225, 241, 306, 316, 336 Loss 15, 135, 140, 143, 199, 223, 224, 233, 252, 293, 315, 370 YieldGard® 61, 125, 358 Z Zabrotes subfasciatus (Mexican bean weevil) 390 Zizania latifolia 235 ... Integration of Bt Crops within IPM Programs Sharlene R Matten, Graham P Head, and Hector D Quemada 27 Insecticidal Genetically Modified Crops and Insect Resistance Management (IRM) ... (eds.), Integration of Insect- Resistant Genetically Modified Crops within IPM Programs © Springer Science + Business Media B.V 2008 27 28 S.R Matten et al barriers for insect- resistant GM crops. .. Parra, R Zucchi Jưrg Romeis • Anthony M Shelton George G Kennedy Editors Integration of Insect- Resistant Genetically Modified Crops within IPM Programs Editors Jörg Romeis Agroscope Reckenholz-Tänikon