Abstract
The area devoted to growing transgenic plants expressing insecticidal Cry proteins derived from Bacillus thuringiensis (Bt) is increasing worldwide. A major concern with the adoption of Bt crops is their potential impact on nontarget organisms including biological control organisms. Regulatory frameworks should advocate a step-wise (tiered) approach to assess possible nontarget effects of Bt crops. Laboratory and glasshouse studies have revealed effects on natural enemies only when Bt-susceptible, sublethally damaged herbivores were used as prey or host, with no indication of direct toxic effects. Field studies have confirmed that the abundance and activity of parasitoids and predators are similar in Bt and non-Bt crops. In contrast, applications of conventional insecticides have usually resulted in negative impacts on biological control organisms. Because Bt-transgenic varieties can lead to substantial reductions in insecticide use in some crops, they can contribute to integrated pest management systems with a strong biological control component.
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References
Glare, T.R. & O'Callaghan, M. Bacillus thuringiensis: Biology, Ecology and Safety (John Wiley & Sons Ltd, Chichester, UK, 2000).
Shelton, A.M., Zhao, J.Z. & Roush, R.T. Economic, ecological, food safety, and social consequences of the deployment of Bt transgenic plants. Annu. Rev. Entomol. 47, 845–881 (2002).
James, C. Preview: Global Status of Commercialized Biotech/GM Crops: 2004. ISAA Brief No. 32 (International Service for the Acquisition of Agri-Biotech Applications, Ithaca, NY, USA, 2004).
Bates, S.L., Zhao, J.-Z., Roush, R.T. & Shelton, A.M. Insect resistance management in GM crops: past, present and future. Nat. Biotechnol. 23, 57–62 (2005).
Fitt, G.P. et al. Global Status and Impacts of Biotech Cotton. Report of the Second Expert Panel on Biotechnology of Cotton (International Cotton Advisory Committee, Washington DC, USA 2004).
Food and Agriculture Organization of the United Nations. The State of Food and Agriculture (FAO, Rome, 2004).
Dale, P.J., Clarke, B. & Fontes, E.M.G. Potential for the environmental impact of transgenic crops. Nat. Biotechnol. 20, 567–574 (2002).
Nap, J.P., Metz, P.L.J., Escaler, M. & Conner, A.J. The release of genetically modified crops into the environment—Part I. Overview of current status and regulations. Plant J. 33, 1–18 (2003).
Conner, A.J., Glare, T.R. & Nap, J.P. The release of genetically modified crops into the environment—Part II. Overview of ecological risk assessment. Plant J. 33, 19–46 (2003).
European Food Safety Authority Guidance document of the Scientific Panel on Genetically Modified Organisms for the risk assessment of genetically modified plants and derived food and feed. The EFSA Journal 99, 1–94 (2004).
Kok, E.J. & Kuiper, H.A. Comparative safety assessment for biotech crops. Trends Biotechnol. 21, 439–444 (2003).
European Community Directive 2001/18/EC of the European Parliament and of the Council, 12 March 2001, on the deliberate release into the environment of genetically modified organisms and repealing Council Directive 90/220/EEC. Official J. Eur. Communities L 106, 1–39 (2001).
Bradford, K.J., Van Deynze, A., Gutterson, N., Parrott, W. & Strauss, S.H. Regulating transgenic crops sensibly: lessons from plant breeding, biotechnology and genomics. Nat. Biotechnol. 23, 439–444 (2005).
EPA. Guidelines for Ecological Risk Assessment. EPA 630/R-95–002F (Environmental Protection Agency, Washington, DC, USA, 1998).
Hill, R.A. & Sendashonga, C. General principles for risk assessment of living modified organisms: lessons from chemical risk assessment. Environ. Biosafety Res. 2, 81–88 (2003).
Dutton, A., Romeis, J. & Bigler, F. Assessing the risks of insect resistant transgenic plants on entomophagous arthropods: Bt-maize expressing Cry1Ab as a case study. BioControl 48, 611–636 (2003).
Mendelsohn, M., Kough, J., Vaituzis, Z. & Matthews, K. Are Bt crops safe? Nat. Biotechnol. 21, 1003–1009 (2003).
Andow, D.A. & Hilbeck, A. Science-based risk assessment for non-target effects of transgenic crops. Bioscience 54, 637–649 (2004).
Birch, A.N.E. & Wheatley, R.E. GM pest-resistant crops: assessing environmental impacts on non-target organisms. Issues Environ. Sci. Technol. 21, 31–57 (2005).
Ponsard, S., Gutierrez, A.P. & Mills, N.J. Effect of Bt-toxin (Cry1Ac) in transgenic cotton on the adult longevity of four heteropteran predators. Environ. Entomol. 31, 1197–1205 (2002).
Riddick, E.W. & Barbosa, P. Impact of Cry3A-intoxicated Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) and pollen on consumption, development, and fecundity of Coleomegilla maculata (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 91, 303–307 (1998).
Meissle, M., Vojtech, E. & Poppy, G.M. Effects of Bt maize-fed prey on the generalist predator Poecilus cupreus L. (Coleoptera: Carabidae). Transgenic Res. 14, 123–132 (2005).
Obrist, L.B., Dutton, A., Romeis, J. & Bigler, F. Biological activity of Cry1Ab toxin expressed by Bt maize following ingestion by herbivorous arthropods and exposure of the predator Chrysoperla carnea. BioControl (in the press).
Romeis, J., Dutton, A. & Bigler, F. Bacillus thuringiensis toxin (Cry1Ab) has no direct effect on larvae of the green lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). J. Insect Physiol. 50, 175–183 (2004).
Rodrigo-Simón, A. et al. Lack of detrimental effects of Bacillus thuringiensis Cry toxins on the insect predator Chrysoperla carnea: a toxicological, histopathological, and biochemical approach. Appl. Environ. Microbiol. (in the press).
Hilbeck, A., Moar, W.J., Pusztai-Carey, M., Filippini, A. & Bigler, F. Toxicity of Bacillus thuringiensis Cry1Ab toxin to the predator Chrysoperla carnea (Neuroptera: Chrysopidae). Environ. Entomol. 27, 1255–1263 (1998).
De Maagd, R.A., Bravo, A. & Crickmore, N. How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet. 17, 193–199 (2001).
Hilbeck, A., Baumgartner, M., Fried, P.M. & Bigler, F. Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla carnea (Neuroptera: Chrysopidae). Environ. Entomol. 27, 480–487 (1998).
Dutton, A., Klein, H., Romeis, J. & Bigler, F. Uptake of Bt-toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea. Ecol. Entomol. 27, 441–447 (2002).
Lozzia, G.C., Furlanis, C., Manachini, B. & Rigamonti, I. Effects of Bt corn on Rhopalosiphum padi L. (Rhynchota Aphididae) and on its predator Chrysoperla carnea Stephen (Neuroptera, Chrysopidae). Boll. Zool. Agr. Bachic. Ser. II 30, 153–164 (1998).
Zwahlen, C., Nentwig, W., Bigler, F. & Hilbeck, A. Tritrophic interactions of transgenic Bacillus thuringiensis corn, Anaphothrips obscurus (Thysanoptera: Thripidae), and the predator Orius majusculus (Heteroptera: Anthocoridae). Environ. Entomol. 29, 846–850 (2000).
Raps, A. et al. Immunological analysis of phloem sap of Bacillus thuringiensis corn and of the non-target herbivore Rhopalosiphum padi (Homoptera: Aphididae) for the presence of Cry1Ab. Mol. Ecol. 10, 525–533 (2001).
Head, G., Brown, C.R., Groth, M.E. & Duan, J.J. Cry1Ab protein levels in phytophagous insects feeding on transgenic corn: implications for secondary exposure risk assessment. Entomol. Exp. Appl. 99, 37–45 (2001).
Obrist, L.B., Dutton, A., Albajes, R. & Bigler, F. Exposure of arthropod predators to Cry1Ab toxin in Bt maize fields. Ecol. Entomol. (in the press).
Schuler, T.H. et al. Laboratory studies of the effects of reduced prey choice caused by Bt plants on a predatory insect. Bull. Entomol. Res. 95, 243–247 (2005).
Bernal, C.C., Aguda, R.M. & Cohen, M.B. Effect of rice lines transformed with Bacillus thuringiensis toxin genes on the brown planthopper and its predator Cyrtorhinus lividipennis. Entomol. Exp. Appl. 102, 21–28 (2002).
Coll, M. & Guershon, M. Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu. Rev. Entomol. 47, 267–297 (2002).
Duan, J.J. et al. Evaluation of dietary effects of transgenic corn pollen expressing Cry3Bb1 protein on a non-target ladybird beetle, Coleomegilla maculata. Entomol. Exp. Appl. 104, 271–280 (2002).
Lundgren, J.G. & Wiedenmann, R.N. Nutritional suitability of corn pollen for the predator Coleomegilla maculata (Coleoptera: Coccinellidae). J. Insect Physiol. 50, 567–575 (2004).
Lundgren, J.G. & Wiedenmann, R.N. Coleopteran-specific Cry3Bb toxin from transgenic corn pollen does not affect the fitness of a non-target species, Coleomegilla maculata DeGeer (Coleoptera: Coccinellidae). Environ. Entomol. 31, 1213–1218 (2002).
Bai, Y.Y., Jiang, M.X. & Cheng, J.A. Effects of transgenic cry1Ab rice pollen on fitness of Propylea japonica (Thunberg). J. Pest Sci. 78, 123–128.
Godfray, H.C.J. Parasitoids (Princeton University Press, Princeton, USA, 1994).
Schuler, T.H. et al. Tritrophic choice experiments with Bt plants, the diamondback moth (Plutella xylostella) and the parasitoid Cotesia plutellae. Transgenic Res. 12, 351–361 (2003).
Schuler, T.H., Denholm, I., Clark, S.J., Stewart, C.N. & Poppy, G.M. Effects of Bt plants on the development and survival of the parasitoid Cotesia plutellae (Hymenoptera: Braconidae) in susceptible and Bt-resistant larvae of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). J. Insect Physiol. 50, 435–443 (2004).
Meissle, M., Vojtech, E. & Poppy, G.M. Implications for the parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae) when developing in Bt maize-fed Spodoptera littoralis larvae (Lepidoptera: Noctuidae). IOBC WPRS Bull. 27 (3), 117–123 (2004).
Vojtech, E., Meissle, M. & Poppy, G.M. Effects of Bt maize on the herbivore Spodoptera littoralis (Lepidoptera: Noctuidae) and the parasitoid Cotesia marginiventris (Hymenoptera: Braconidae). Transgenic Res. 14, 133–144 (2005).
Ashouri, A., Michaud, D. & Cloutier, C. Unexpected effects of different potato resistance factors to the Colorado potato beetle (Coleoptera: Chrysomelidae) on the potato aphid (Homoptera: Aphididae). Environ. Entomol. 30, 524–532 (2001).
Ashouri, A., Michaud, D. & Cloutier, C. Recombinant and classically selected factors of potato plant resistance to the Colorado potato beetle, Leptinotarsa decemlineata, variously affect the potato aphid parasitoid Aphidius nigripes. BioControl 46, 401–418 (2001).
Conner, A.J., Jacobs, J.M.E. & Genet, R.A. Transgenic potatoes versus “traditional” potatoes: what's the difference? in Commercialisation of Transgenic Crops: Risk, Benefit and Trade Considerations. (eds. McLean, G.D., Waterhouse, P.M., Evans, G. & Gibbs, M.J.) 23–36 (Australian Government Publishing Service, Canberra, Australia, 1997).
Jepson, P.C. Insects, spiders and mites. in Handbook of Ecotoxicology (ed. Calow, P.) 299–325 (Blackwell Science, Oxford, UK, 1994).
Candolfi, M. et al. Principles for regulatory testing and interpretation of semi-field studies with non-target arthropods. J. Pest Sci. 73, 141–147 (2000).
Johnson, M.T. & Gould, F. Interaction of genetically engineered host plant-resistance and natural enemies of Heliothis virescens (Lepidoptera, Noctuidae) in tobacco. Environ. Entomol. 21, 586–597 (1992).
Johnson, M.T. Interaction of resistant plants and wasp parasitoids of tobacco budworm (Lepidoptera: Noctuidae). Environ. Entomol. 26, 207–214 (1997).
Wold, S.J., Burkness, E.C., Hutchison, W.D. & Venette, R.C. In-field monitoring of beneficial insect populations in transgenic corn expressing a Bacillus thuringiensis toxin. J. Entomol. Sci. 36, 177–187 (2001).
Riddick, E.W., Dively, G. & Barbosa, P. Effect of a seed-mix deployment of Cry3A-transgenic and nontransgenic potato on the abundance of Lebia grandis (Coleoptera: Carabidae) and Coleomegilla maculata (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 91, 647–653 (1998).
Pilcher, C.D., Rice, M.E. & Obrycki, J.J. Impact of transgenic Bacillus thuringiensis corn and crop phenology on five non-target arthropods. Environ. Entomol. 34, 1302–1316 (2005).
Naranjo, S.E. Long-term assessment of the effects of transgenic Bt cotton on the abundance of non-target arthropod natural enemies. Environ. Entomol. 34, 1193–1210 (2005).
Daly, T. & Buntin, G.D. Effects of Bacillus thuringiensis transgenic corn for lepidopteran control on non-target arthropods. Environ. Entomol. 34, 1292–1301 (2005).
Whitehouse, M.E., Wilson, L.J. & Fitt, G.P. A comparison of arthropod communities in transgenic Bt and conventional cotton in Australia. Environ. Entomol. 34, 1224–1241 (2005).
Torres, J.B. & Ruberson, J.R. Canopy- and ground-dwelling predatory arthropods in commercial Bt and non-Bt cotton fields: Patterns and mechanisms. Environ. Entomol. 34, 1242–1256 (2005).
Head, G. et al. A multi-year, large-scale comparison of arthropod populations on commercially managed Bt and non-Bt cotton fields. Environ. Entomol. 34, 1257–1266 (2005).
Bourguet, D. et al. Ostrinia nubilalis parasitism and the field abundance of non-target insects in transgenic Bacillus thuringiensis corn (Zea mays). Environ. Biosafety Res. 1, 49–60 (2002).
Siegfried, B.D., Zoerb, A.C. & Spencer, T. Development of European corn borer larvae on Event 176 Bt corn: influence on survival and fitness. Entomol. Exp. Appl. 100, 15–20 (2001).
Manachini, B. Effects of transgenic corn on Lydella thompsoni Hertig (Diptera: Tachinidae) parasitoid of Ostrinia nubilalis Hb. (Lepidoptera: Crambidae). Boll. Zool. Agr. Bachic. Ser. II 35, 111–125 (2003).
Naranjo, S.E. Long-term assessment of the effects of transgenic Bt cotton on the function of the natural enemy community. Environ. Entomol. 34, 1211–1223 (2005).
Musser, F.R. & Shelton, A.M. Bt sweet corn and selective insecticides: Impacts on pests and predators. J. Econ. Entomol. 96, 71–80 (2003).
Sisterson, M.S. et al. Arthropod abundance and diversity in Bt and non-Bt cotton fields. Environ. Entomol. 33, 921–929 (2004).
Reed, G.L., Jensen, A.S., Riebe, J., Head, G. & Duan, J.J. Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: comparative efficacy and non-target impacts. Entomol. Exp. Appl. 100, 89–100 (2001).
Wu, K.M. & Guo, Y.Y. Influences of Bacillus thuringiensis Berliner cotton planting on population dynamics of the cotton aphid, Aphis gossypii Glover, in northern China. Environ. Entomol. 32, 312–318 (2003).
Bhatti, M.A. et al. Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on foliage-dwelling arthropods. Environ. Entomol. 34, 1336–1345 (2005).
Green, J.K., Turnipseed, S.G., Sullivan, M.J. & May, O.L. Treatment thresholds for stink bugs (Hemiptera: Pentatomidae) in cotton. J. Econ. Entomol. 94, 403–409 (2001).
Wu, K., Li, W., Feng, H. & Guo, Y. Seasonal abundance of the mirids, Lygus lucorum and Adelphocoris spp. (Hemiptera: Miridae) on Bt cotton in northern China. Crop Prot. 21, 997–1002 (2002).
O'Callaghan, M., Glare, T.R., Burgess, E.P.J. & Malone, L.A. Effects of plants genetically modified for insect resistance on nontarget organisms. Annu. Rev. Entomol. 50, 271–292 (2005).
Lövei, G.L. & Arpaia, S. The impact of transgenic plants on natural enemies: a critical review of laboratory studies. Entomol. Exp. Appl. 114, 1–14 (2005).
Candolfi, M.P., Brown, K., Grimm, C., Reber, B. & Schmidli, H. A faunistic approach to assess potential side-effects of genetically modified Bt-corn on non-target arthropods under field conditions. Biocontr. Sci. Technol. 14, 129–170 (2004).
de la Poza, M. et al. Impact of farm-scale Bt maize on abundance of predatory arthropods in Spain. Crop Prot. 24, 677–684 (2005).
Boethel, D.J. & Eikenbarry, R.D. Interactions of Plant Resistance and Parasitoids and Predators of Insects (Ellis Horwood Limited, Chichester, UK, 1986).
Croft, B.A. Arthropod Biological Control Agents and Pesticides (John Wiley & Sons, New York, 1990).
Fitt, G.P., Mares, C.L. & Llewellyn, D.J. Field-evaluation and potential ecological impact of transgenic cottons (Gossypium hirsutum) in Australia. Biocontr. Sci. Technol. 4, 535–548 (1994).
Sisterson, M.S. & Tabashnik, B.E. Simulated effects of transgenic Bt crops on specialist parasitoids of target pests. Environ. Entomol. 34, 733–742 (2005).
Secretariat, C.B.D. 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, 2000).
Candolfi, M.P. et al. Guidance document on regulatory testing and risk assessment procedures for plant protection products with non-target arthropods (Society of Environmental Toxicology and Chemistry Office, Pensacola, USA, 2001).
Lynch, L.D. et al. Insect biological control and non-target effects: a European perspective. In Evaluating Indirect Ecological Effects of Biological Control (eds. Wajnberg, E., Scott, J.K. & Quimby, P.C.) 99–125 (CABI Publishing, Wallingford, UK, 2001).
Dogan, E.B., Berry, R.E., Reed, G.L. & Rossignol, P.A. Biological parameters of convergent lady beetle (Coleoptera: Coccinellidae) feeding on aphids (Homoptera: Aphididae) on transgenic potato. J. Econ. Entomol. 89, 1105–1108 (1996).
Kalushkov, P. & Nedvêd, O. Genetically modified potatoes expressing Cry 3A protein do not affect aphidophagous coccinellids. J. Appl. Entomol. 129, 401–406 (2005).
Kalushkov, P. & Hodek, I. The effects of six species of aphids on some life history parameters of the ladybird Propylea quatuordecimpunctata (Coleoptera: Coccinellidae). Eur. J. Entomol. 102, 449–452 (2005).
Prütz, G. & Dettner, K. Effect of Bt corn leaf suspension on food consumption by Chilo partellus and life history parameters of its parasitoid Cotesia flavipes under laboratory conditions. Entomol. Exp. Appl. 111, 179–187 (2004).
Bernal, J.S., Griset, J.G. & Gillogly, P.O. Impacts of developing on Bt maize-intoxicated hosts on fitness parameters of a stem borer parasitoid. J. Entomol. Sci. 37, 27–40 (2002).
Baur, M.E. & Boethel, D.J. Effect of Bt-cotton expressing Cry1A(c) on the survival and fecundity of two hymenopteran parasitoids (Braconidae, Encyrtidae) in the laboratory. Biol. Contr. 26, 325–332 (2003).
Liu, X.X., Sun, C.G. & Zhang, Q.W. Effects of transgenic Cry1A+CpTI cotton and Cry1Ac toxin on the parasitoid, Campoletis chlorideae (Hymenoptera: Ichneumonidae). Insect Sci. 12, 101–107 (2005).
Schuler, T.H. et al. Population scale laboratory studies of the effect of transgenic plants on non-target insects. Mol. Ecol. 10, 1845–1853 (2001).
Obrist, L., Klein, H., Dutton, A. & Bigler, F. Effects of Bt maize on Frankliniella tenuicornis and exposure of thrips predators to prey-mediated Bt toxin. Entomol. Exp. Appl. 115, 409–416 (2005).
Ashfaq, M., Young, S.Y. & McNew, R.W. Development of Spodoptera exigua and Helicoverpa zea (Lepidoptera: Noctuidae) on transgenic cotton containing Cry1Ac insecticidal protein. J. Entomol. Sci. 35, 360–372 (2000).
Pilcher, C.D., Rice, M.E., Obrycki, J.J. & Lewis, L.C. Field and laboratory evaluations of transgenic Bacillus thuringiensis corn on secondary lepidopteran pests (Lepidoptera: Noctuidae). J. Econ. Entomol. 90, 669–678 (1997).
Al-Deeb, M.A., Wilde, G.E. & Higgins, R.A. No effect of Bacillus thuringiensis corn and Bacillus thuringiensis on the predator Orius insidiosus (Hemiptera: Anthocoridae). Environ. Entomol. 30, 625–629 (2001).
Pons, X., Lumbierres, B., Lopez, C. & Albajes, R. No effects of Bt maize on the development of Orius majusculus. IOBC WPRS Bull. 27 (3), 131–136 (2004).
Armer, C.A., Berry, R.E. & Kogan, M. Longevity of phytophagous heteropteran predators feeding on transgenic Btt-potato plants. Entomol. Exp. Appl. 95, 329–333 (2000).
Dowd, P.F. Indirect reduction of ear molds and associated mycotoxins in Bacillus thuringiensis corn under controlled and open field conditions: utility and limitations. J. Econ. Entomol. 93, 1669–1679 (2000).
Dowd, P.F. Dusky sap beetles (Coleoptera: Nitidulidae) and other kernel damaging insects in Bt and non-Bt sweet corn in Illinois. J. Econ. Entomol. 93, 1714–1720 (2000).
Hassell, R.L. & Shepard, B.M. Insect populations on Bacillus thuringiensis transgenic sweet corn. J. Entomol. Sci. 37, 285–292 (2002).
Jasinski, J.R., Eisley, J.B., Young, C.E., Kovach, J. & Willson, H. Select nontarget arthropod abundance in transgenic and nontransgenic field crops in Ohio. Environ. Entomol. 32, 407–413 (2003).
Lopez, M.D., Prasifka, J.R., Bruck, D.J. & Lewis, L.C. Utility of ground beetle species in field tests of potential non-target effects of Bt crops. Environ. Entomol. 34, 1317–1324 (2005).
Lozzia, G.C. Biodiversity and structure of ground beetle assemblages (Coleoptera Carabidae) in Bt corn and its effects on non target insects. Boll. Zool. Agr. Bachic. Ser. II 31, 37–58 (1999).
Meissle, M. & Lang, A. Comparing methods to evaluate the effects of Bt maize and insecticide on spider assemblages. Agric. Ecosyst. Environ. 107, 359–370 (2005).
Orr, D.B. & Landis, D.A. Oviposition of European corn borer (Lepidoptera: Pyralidae) and impact of natural enemy populations in transgenic versus isogenic corn. J. Econ. Entomol. 90, 905–909 (1997).
Pons, X. & Stary, P. Spring aphid-parasitoid (Hom., Aphididae, Hym., Braconidae) associations and interactions in a Mediterranean arable crop ecosystem, including Bt maize. J. Pest Sci. 76, 133–138 (2003).
Tóth, F. et al. (2004) Spider web survey or whole plant visual sampling? Impact assessment of Bt corn on non-target predatory insects with two concurrent methods. Environ. Biosafety Res. 3, 225–231 (2004).
Volkmar, C. & Freier, B. Spinnenzönosen in Bt-Mais und nicht gentechnisch veränderten Maisfeldern. Z. Pflanzenkrankh. Pflanzenschutz 110, 572–582 (2003).
Ahmad, A., Wilde, G.E. & Zhu, K.Y. Detectability of coleopteran-specific Cry3Bb1 protein in soil and its effect on nontarget surface and below-ground arthropods. Environ. Entomol. 34, 385–394 (2005).
Al-Deeb, M.A. & Wilde, G.E. Effect of Bt corn expressing the Cry3Bb1 toxin for corn rootworm control on aboveground non-target arthropods. Environ. Entomol. 32, 1164–1170 (2003).
Bhatti, M.A. et al. Field evaluation of the impact of corn rootworm (Coleoptera: Chrysomelidae)-protected Bt corn on ground-dwelling invertebrates. Environ. Entomol. 34, 1325–1335 (2005).
Dively, G.P. Impact of transgenic VIP3A x Cry1Ab lepidopteran-resistant field corn on the non-target arthropod community. Environ. Entomol. 34, 1267–1291 (2005).
Wilson, F.D. et al. Resistance of cotton lines containing a Bacillus thuringiensis toxin to pink bollworm (Lepidoptera, Gelechiidae) and other insects. J. Econ. Entomol. 85, 1516–1521 (1992).
Bambawale, O.M. et al. Performance of Bt cotton (MECH-162) under Integrated Pest Management in farmers' participatory field trial in Nanded district, Central India. Curr. Sci. 86, 1628–1633 (2004).
Flint, H.M. et al. The effects of transgenic cotton, Gossypium hirsutum L. containing Bacillus thuringiensis toxin genes for the control of the pink bollworm, Pectinophora gossypiella (Saunders) and other arthropods. Southw. Entomol. 20, 281–292 (1995).
Hagerty, A.M., Kilpatrick, A.L., Turnipseed, S.G., Sullivan, M.J. & Bridges, W.C. Predaceous arthropods and lepidopteran pests on conventional, Bollgard, and Bollgard II cotton under untreated and disrupted conditions. Environ. Entomol. 34, 105–114 (2005).
Hardee, D.D. & Bryan, W.W. Influence of Bacillus thuringiensis-transgenic and nectariless cotton on insect populations with emphasis on the tarnished plant bug (Heteroptera: Miridae). J. Econ. Entomol. 90, 663–668 (1997).
Mellet, M.A., Schoeman, A.S., Broodryk, S.W. & Hofs, J.L. Bollworm (Helicoverpa armigera (Hubner), Lepidoptera: Noctuidae) occurrences in Bt- and non-Bt-cotton fields, Marble Hall, Mpumalanga, South Africa. Afr. Entomol. 12, 107–115 (2004).
Men, X.Y., Ge, F., Edwards, C.A. & Yardim, E.N. Influence of pesticide applications on pest and predatory arthropods associated with transgenic Bt cotton and nontransgenic cotton plants. Phytoparasitica 32, 246–254 (2004).
Duan, J.J., Head, G., Jensen, A. & Reed, G. Effects of transgenic Bacillus thuringiensis potato and conventional insecticides for Colorado potato beetle (Coleoptera: Chrysomelidae) management on the abundance of ground-dwelling arthropods in Oregon potato ecosystems. Environ. Entomol. 33, 275–281 (2004).
Riddick, E.W., Dively, G. & Barbosa, P. Season-long abundance of generalist predators in transgenic versus nontransgenic potato fields. J. Entomol. Sci. 35, 349–359 (2000).
Hoffmann, M.P. et al. Field-evaluation of transgenic tobacco containing genes encoding Bacillus thuringiensis delta-endotoxin or cowpea trypsin-inhibitor-efficacy against Helicoverpa zea (Lepidoptera, Noctuidae). J. Econ. Entomol. 85, 2516–2522 (1992).
Warren, G.W., Carozzi, N.B., Desai, N. & Koziel, M.G. Field evaluation of transgenic tobacco containing a Bacillus thuringiensis insecticidal protein gene. J. Econ. Entomol. 85, 1651–1659 (1992).
Acciarri, N. et al. Transgenic resistance to the Colorado potato beetle in Bt-expressing eggplant fields. HortScience 35, 722–725 (2000).
Acknowledgements
We are very grateful to Anthony M. Shelton, Paul Jepson, Alan Raybould, Detlef Bartsch and Felix L. Wäckers for their thoughtful reviews and helpful comments. We also thank our colleagues at FAL Reckenholz for fruitful discussions. This project was partially funded by the National Center of Competence in Research (NCCR) Plant Survival, research program of the Swiss National Science Foundation.
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Romeis, J., Meissle, M. & Bigler, F. Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24, 63–71 (2006). https://doi.org/10.1038/nbt1180
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DOI: https://doi.org/10.1038/nbt1180
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