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Bt crops: Predicting effects of escaped transgeneson the fitness of wild plants and their herbivores

Published online by Cambridge University Press:  15 January 2004

Deborah K. Letourneau
Affiliation:
Department of Environmental Studies, University of California, Santa Cruz, USA
Gaden S. Robinson
Affiliation:
Department of Entomology, The Natural History Museum, London, UK
Joy A. Hagen
Affiliation:
Department of Environmental Studies, University of California, Santa Cruz, USA

Abstract

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One prominent concern about genetically modified crops is the possibility of environmental impacts from the movement of fitness-enhancing traits to wild plant populations. Decisions to deregulate Bt crops in the USA have relied strongly on arguments that these crops will not interbreed with wild relatives in the permitted growing regions. Limited attention therefore has been directed to analyses of the consequences of gene flow. To provide a transparent evaluation process for risks associated with insecticidal transgene escape, we crafted a series of questions designed to guide this aspect of the risk assessment. We then explored the current knowledge base available for answering such risk-related questions for three Bt crops (cotton, rapeseed, and rice). First, we generated a list of wild relatives of these crops. A definitive list of potential transgene recipients is not yet possible for some crops. Sufficient data are not available for some crops to eliminate certain related plant species from consideration of fertile hybrid formation, thus making lists for these crops subject to speculation. Second, we queried the HOSTS database (UK) to obtain a worldwide listing of lepidopteran species that feed on these crops and their wild relatives, and to determine the host range of the larvae. To our knowledge, this list of 502 lepidopteran species is the first such list published for these crops and wild crop relatives. Third, we used a data set maintained by the Canadian Forest Service to assess Bt toxin susceptibility for these lepidopterans. Only 3% of those species have been tested for susceptibility; and the literature suggests that generalizations about susceptibility among taxa are difficult due to the variability within families. Fourth, we consulted the literature to interpret what is known about the ability of lepidopterans to regulate plant fitness or invasiveness. We could not eliminate the possibility of ecological release due to plant resistance against lepidopterans. In fact, there is strong experimental evidence that lepidopteran herbivores do limit the distribution and/or abundances of at least some wild plant species. Neither could we eliminate the possibility that non-target lepidopterans might have important functions in the ecosystem as pollinators or alternate hosts to natural enemies of pest species. This study suggests that crucial data are lacking for the development of a credible scientific basis to confirm or deny environmental risks associated with the escape of Bt transgene constructs to wild relatives. Given the absence of information on the identity, level of susceptibility, and ecological roles of lepidopterans exploiting specific wild relatives of Bt crops, we suggest that new efforts be directed to assessing possible consequences of lepidopteran mortality on resistant wild relatives.

Type
Research Article
Copyright
© ISBR, EDP Sciences, 2003

References

Acciarri, N, Vitelli, G, Arpaia, S, Mennella, G, Sunseri, F, Rotino, GL (2000) Transgenic resistance to the Colorado potato beetle in Bt expressing eggplant fields. Hortscience 35: 722
Agrawal, AA (1999) Induced responses to herbivory in wild radish: Effects on several herbivores and plant fitness. Ecology 80: 1713 CrossRef
Agrawal, AA, Strauss, SY, Stout, MJ (1999) Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53: 1093 CrossRef
Alstad, DN, Andow, DA (1995) Managing the evolution of resistance to transgenic plants. Science 268: 1894 CrossRef
Andow DA (2002) Resisting resitance to Bt crops. In Letourneau DK, Burrows BE, eds, Genetically Engineered Organisms: Assessing Environmental and Human Health Effects. CRC Press, Boca Raton, FL, pp 99–121
Archer, TL, Schuster, G, Patrick, C, Cronholm, G, Bynum, ED, Morrison, WP (2000) Whorl and stalk damage by European and Southwestern corn borers to four events of Bacillus thuringiensis transgenic maize. Crop Protection 19: 181 CrossRef
Ashfaq, M, Young, SY, McNew, RW (2000) Development of Spodoptera exigua and Helicoverpa zea (Lepidoptera: Noctuidae) on transgenic cotton containing CrylAc insecticidal protein. J. Entomol. Sci. 35: 360
Barbosa P (1993) Lepidopteran foraging on plants in agroecosystems: Constraints and consequences. In Stamp NE, Casey TM, eds, Ecological and Evolutionary Constraints on Foraging Caterpillars, pp 29
Barbosa P (1998) ed, Conservation Biological Control. Academic Press
Benbrook CM, Groth E, Halloran JM, Hansen MK, Marquardt S (1996) Pest Management at the Crossroads. Consumers Union, Yonkers, New York
Bergelson, J (1994) Changes in fecundity do not predict invasiveness: A model study of transgenic plants. Ecology 75: 249 CrossRef
Bergelson J, Purrington CB (2002) Factors affecting the spread of resistant Arabidopsis thaliana populations. In Letourneau DK, Burrows BE, eds, Genetically Engineered Organisms: Assessing Environmental and Human Health Effects. CRC Press, Boca Raton, FL, pp 33
Betz, FS, Hammond, BG, Fuchs, RL (2000) Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. Regul. Toxicol. Pharmacol. 32: 156173 CrossRef
Bourget, D, Bethenod, MT, Trouve, C, Frederique, V (2000) Host-plant diversity of the European corn borer Ostrinia nubilalis: What value for sustainable transgenic insecticidal Bt maize? Proc. R. Soc. Lond. B Biol. Sci. 267: 1177 CrossRef
Callaway RM, DeLuca TH, Belliveau WM (1999) Biological-control herbivores may increase competitive ability of the noxious weed Centaurea maculosa. Ecology 80: 1196–1201 CrossRef
Caswell H (2001) Matrix Population Models. Sinauer, Sunderland, Massachusetts
Chèvre, AM, Eber, F, Baranger, A, Hureau, G, Barret, P, Picault, H, Renard, M (1998) Characterization of backcross generations obtained under field conditions from oilseed rape wild radish F-1 interspecific hybrids – An assessment of transgene dispersal. Theor. Appl. Genet. 97: 9098
Colwell, RK, Norse, EA, Pimentel, D, Sharples, FE, Simberloff, D (1985) Genetic engineering in agriculture. Science 229: 111 CrossRef
Crawley, M, Harvey, PH, Purvis, A (1996) Comparative ecology of the native and alien floras of the British Isles. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351: 1251 CrossRef
Daehler, CC, Strong, DR (1996) Status, prediction and prevention of introduced cordgrass Spartina spp. Invasions in Pacific Estuaries, USA. Biol. Conserv. 78: 5158 CrossRef
Darmency, H (1994) The impact of hybrids between genetically modified crop plants and their related species – Introgression and weediness. Mol. Ecol. 3: 3740 CrossRef
Doak, DF (1991) The consequences of herbivory for dwarf fireweed: Different time scales, different morphological scales. Ecology 72: 1397 CrossRef
Doak, DF (1992) Lifetime impacts of herbivory for a perennial plant. Ecology 73: 20862099 CrossRef
Dyer, LA, Letourneau, DK (1999) Trophic cascades in a complex terrestrial community. Proc. Natl. Acad. Sci. USA 96: 50725076 CrossRef
Ellstrand, NC, Prentice, HC, Hancock, JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annu. Rev. Ecol. Syst. 30: 539563 CrossRef
Felton GW, Dahlman DL (1984) Allelochemical Induced Stress – Effects of L-canavanine on the pathogenicity of Bacillus thuringiensis in Manduca sexta. J. Invertebr. Pathol. 44: 187–191
Fitton, MG, Shaw, MR, Gauld, ID (1988) Pimpline ichneumon-flies, Hymenoptera, Ichneumonidae (Pimplinae). Handbook for the Identification of British Insects 7: 1
Fretwell, SD (1977) The regulation of plant communities by food chains exploiting them. Perspect. Biol. Med. 20: 169 CrossRef
Geervliet, JBF, Posthumus, MA, Vet, LEM, Dicke, M (1997) Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. J. Chem. Ecol. 23: 29352954 CrossRef
Hails, RS (2000) Genetically modified plants – The debate continues. Trends. Ecol. Evol. 15: 1418 CrossRef
Hauser, TP, Shaw, RG, Ostergard, H (1998) Fitness of F-1 hybrids between weedy Brassica rapa and oilseed rape (B. napus). Heredity 81: 429435 CrossRef
Hedin, PA, Lindig, OH, Sikorowski, PP, Wyatt, M (1978) Suppressants of gut bacteria in the boll weevil from the cotton plant. J. Econ. Entomol. 71: 394396 CrossRef
Hellmich, RL, Siegfried, BD, Sears, MK, Stanley-Horn, DE, Daniels, MJ, Mattila, HR, Spencer, T, Bidne, KG, Lewis, LC (2001) Monarch larvae sensitivity to Bacillus thuringiensis-purified proteins and pollen. Proc. Natl. Acad. Sci. USA 98: 1192511930 CrossRef
Hilbeck A (2002) Transgenic host plant resistance and non-target effects. In Letourneau DK, Burrows BE, eds, Genetically engineered organisms: assessing environmental and human health effects. CRC Press, Boca Raton, Florida, pp 33
Hoffman, CA (1990) Ecological risks of genetic engineering of crop plants: scientific and social analyses are critical to realize benefits of the new techniques. Bioscience 40: 434 CrossRef
Hull LA, Beers EH (1985) Ecological selectivity: modifying chemical control practices to preserve natural enemies. In Hoy MA, Herzog DC, eds, Biological Control in Agricultural IPM Systems. Academic Press, Inc., New York
James, RR, Miller, JC, Lighthart, B (1993) Bacillus thuringiensis var. kurstaki affects a beneficial insect, the cinnabar moth (Lepidoptera: Arctiidae). J. Econ. Entomol. 86: 334 CrossRef
Jenczewski, E, Ronfort, J, Chèvre, AM (2003) Crop-to-wild gene flow, introgression and possible fitness effects of transgenes. Environ. Biosafety Res. 2: 924 CrossRef
Jesse, LCH, Obrycki, JJ (2000) Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly. Oecologia 125: 241248 CrossRef
Johnson, KS, Scriber, JM, Nitao, JK, Smitley, DR (1995) Toxicity of Bacillus thuringiensis var. kurstaki to three nontarget lepidoptera in field studies. Environ. Entomol. 24: 288297 CrossRef
Jorgensen, RB, Andersen, B (1994) Spontaneous hybridization between oilseed rape (Brassica napus) and weedy Brassica campestris (Brassicaceae) – a rise of growing genetically- modified oilseed rape. Am. J. Bot. 81: 16201626 CrossRef
Jorgensen RB, Andersen B, Landbo L, Mikkelsen TR, Dias JS, Crute I, Monteiro AA (1996) Spontaneous hybridization between oilseed rape (Brassica napus) and weedy relatives. Acta Hort. 407: 193
Juenger T, Bergelson J (1998) Pairwise versus diffuse natural selection and the multiple herbivores of scarlet gilia, Ipomopsis aggregata. Evolution 52: 1583–1592 CrossRef
Kareiva, P, Morris, W, Jacobi, CM (1994) Studying and managing the risk of cross-fertilization between transgenic crops and wild relatives. Mol. Ecol. 3: 1521 CrossRef
Kareiva, P, Parker, IM, Pascual, M (1996) Can we use experiments and models in predicting the invasiveness of genetically engineered organisms. Ecology 77: 16701675 CrossRef
Klinger T (2002) Variability and uncertainty in crop-to-wild hybridization. In Letourneau DK, Burrows BE, eds, Genetically engineered organisms: assessing environmental and human health effects. CRC Press, Boca Raton, Florida, pp 1
Klinger T, Ellstrand NC (1994) Engineered genes in wild populations – Fitness of weed-crop hybrids of Raphanus sativus. Ecol. Appl. 4: 117–120 CrossRef
Koptur, S (1990) Early season defoliation can affect Carex laxiflora Cyperaceae seed set in same year or reproductive allocation in subsequent years. Bull. Ecol. Soc. Am. 71: 217
Krishik, VA, Barbosa, P, Reichelderfer, CF (1988) Three trophic level interactions: allelochemicals, Manduca sexta, and Bacillus thuringiensis var. kurstaki Berliner. Environ. Entomol. 17: 476482 CrossRef
Kriticos, D, Brown, J, Radford, I, Nicholas, M (1999) Plant population ecology and biological control: Acacia nilotica as a case study. Biol. Control. 16: 230239 CrossRef
Lefol, E, Seguinswarts, G, Downey, RK (1997) Sexual hybridisation in crosses of cultivated Brassica species with the crucifers Erucastrum gallicum and Raphanus raphanistrum – Potential for gene introgression. Euphytica 95: 127139 CrossRef
Letourneau DK, Hagen JA, Robinson GS (2002) Bt crops: Evaluating benefits under cultivation and risks from escaped transgenes in the wild. In Letourneau DK, Burrows BE, eds, Genetically Engineered Organisms: Assessing Environmental and Human Health Effects. CRC Press, Boca Raton, Florida, pp 33
Losey JE, Obrycki JJ, Hufbauer RA (2002) Impacts of genetically engineered crops on non-target herbivores: Bt corn and monarch butterflies as a case study. In Letourneau DK, Burrows BE, eds, Genetically Engineered Organisms: Assessing Environmental and Human Health Effects. CRC Press, Boca Raton, Florida, pp 143
Losey, JE, Rayor, LS, Carter, ME (1999) Transgenic pollen harms monarch butterflies. Nature 399: 214 CrossRef
Louda SM (1999) Insect limitation of weedy plants and its implications. In Traynor PL, Westwood JH, eds, Conference Proceedings: Workshop on Ecological Effects of Pest Resistance Genes in Managed Ecosystems. Information Systems for Biotechnology, Bethesda, Maryland
Macintosh, SC, Stone, TB, Sims, SR, Hunst, PL, Greenplate, JT, Marrone, PG, Perlak, J, Fischhoff, DA, Fuchs, RL (1990) Specificity and efficacy of purified Bacillus thuringiensis proteins against agronomically important insects. J. Invertebr. Pathol. 56: 258 CrossRef
Maron, JL (1998) Insect Herbivory above- and below-ground – Individual and joint effects on plant fitness. Ecology 79: 12811293 CrossRef
Marquis, RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226: 537 CrossRef
Marquis, RJ (1992) A bite is a bite is a bite? Constraints on response to folivory in Piper arietinum (Piperaceae). Ecology 73: 143152 CrossRef
Marvier M, Kareiva P (1999) Extrapolating from field experiments that remove herbivores to population-level effects of herbivore-resistant transgenes. In Traynor PL, Westwood JH, eds, Conference Proceedings: Workshop on Ecological Effects of Pest Resistance Genes in Managed Ecosystems. Information Systems for Biotechnology, Blacksburg, Virginia, http://www.nbiap.vt.edu
Mauricio, R, Bowers, MD, Bazzaz, FA (1993) Pattern of leaf damage affects fitness of the annual plant Raphanus sativus (Brassicaceae). Ecology 74: 20662071 CrossRef
McCall, PJ, Turlings, TCJ, Loughrin, J, Proveaux, AT, Tumlinson, JH (1994) Herbivore-induced volatile emissions from cotton (Gossypium hirsutum L.) seedlings. J. Chem. Ecol. 20: 30393050 CrossRef
McNaughton, SJ (1986) On plants and herbivores. Am. Nat. 128: 765 CrossRef
Messeguer, J, Fogher, C, Guiderdoni, E, Marfa, V, Catala, MM, Baldi, G, Mele, E (2001) Field assessments of gene flow from transgenic to cultivated rice (Oryza sativa L.) using a herbicide resistance gene as tracer marker. Theor. Appl. Genet. 103: 11511159 CrossRef
Meyer GA (2000) Interactive effects of soil fertility and herbivory on Brassica nigra. Oikos 88: 433–441 CrossRef
Mikkelsen TR, Jensen J, Jorgensen RB (1996) Inheritance of oilseed rape (Brassica napus) RAPD markers in a backcross progeny with Brassica campestris. Theor. Appl. Genet. 92: 492–497 CrossRef
Mullin CA, Croft BA (1985) An update on development of selective pesticides favoring arthropod natural enemies. In Hoy MA, Herzog DC, eds, Biological Control in Agriculture IPM Systems. Academic Press, Inc., New York
Naber, AC, Aarssen, LW (1998) Effects of shoot apex removal and fruit herbivory on branching, biomass and reproduction in Verbascum thapsus (Scrophulariaceae). Am. Midl. Nat. 140: 4254 CrossRef
National Research Council (2000) Genetically Modified Pest-Protected Plants: Science and Regulation. National Academy Press, Washington DC
National Research Council (2002) Environmental Effects of Transgenic Plants: The scope and adequacy of regulation. National Academy Press, Washington DC
Navon A (1993) Control of lepidopteran pests with Bacillus thruingiensis. In Entwistle PF, Cory S, Bailey MJ, Higgs S, eds, Bacillus thuringiensis, an environmental biopesticide: theory and practice. Wiley, Chichester England, New York, pp 311
Neeser C (1999) Report of the Brassica crops working group. In Traynor PL, Westwood JH, eds, Conference Proceedings: Workshop on Ecological Effects of Pest Resistance Genes in Managed Ecosystems. Information Systems for Biotechnology, Bethesda, Maryland
Obrycki, JJ, Losey, JE, Taylor, OR, Jesse, LCH (2001) Transgenic insecticidal corn: Beyond insecticidal toxicity to ecological complexity. Bioscience 51: 353361 CrossRef
Parker, IM (2000) Invasion dynamics of Cytisus scoparius: A matrix model approach. Ecol. Appl. 10: 726743 CrossRef
Paulison, MA (1987) Exploitation by, and the effects of, caterpillar grazers on the annual, Rudbeckia hirta (Compositae). Am. Midl. Nat. 117: 439 CrossRef
Peacock, JW, Schweitzer, DF, Carter, JL, Dubois, NR (1998) Laboratory assessment of the effects of Bacillus thuringiensis on native Lepidoptera. Environ. Entomol. 27: 450457 CrossRef
Peferoen M (1997) Progress and prospects for field use of Bt genes in crops. Trends Biotechnol. 15: 173–177
Peterson, G, Cunningham, S, Deutsch, L, Erickson, J, Quinlan, A, Raez-Luna, E, Tinch, R, Troell, M, Woodbury, P, Zens, S (2000) The risks and benefits of genetically modified crops: A multidisciplinary perspective. Conserv. Ecol. 4: 3849
Phipps, RH, Park, JR (2002) Environmental benefits of genetically modified crops: Global and European perspectives on their ability to reduce pesticide use. J. Anim. Feed. Sci. 11: 118 CrossRef
Pilson, D (1996) Two herbivores and constraints on selection for resistance in Brassica rapa. Evolution 50: 1492 CrossRef
Pilson D (2000) Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus. Oecologia 122: 72–82 CrossRef
Pilson, D, Decker, KL (2002) Compensation for herbivory in wild sunflower: Response to simulated damage by the head- clipping weevil. Ecology 83: 30973107 CrossRef
Price PW (1992) Plant resources as the mechanistic basis for insect herbivore population dynamics. In Hunter MD, Ohgushi T, Price PW, eds, Effects of Resource Distribution on Animal-Plant Interactions. Academic Press, San Diego, California, pp 139
Reichelderfer CF (1991) Interactions among allelochemicals, some Lepidoptera, Bacillus thuringiensis Berliner. In Barbosa B, Kirschik VA, Jones CG, eds, Microbial Mediation of Plant-Herbivore Interactions. Wiley Press, New York
Robinson GS (1998) Bugs, hollow curves and species-diversity indexes. STATS – American Statistical Association 21
Robinson, GS (1999) HOSTS – A database of the hostplants of the world's Lepidoptera. Nota Lepidopterologica 22: 35
Robinson GS, Ackery PR, Kitching IJ, Beccaloni GW, Hernandez LM (2001) Hostplants of the moth and butterfly caterpillars of the oriental region. Southdene Sdn Bhd, Kuala Lumpur
Robinson, GS, Ackery, PR, Kitching, IJ, Beccaloni, GW, Hernandez, LM (2002a) Hostplants of the moth and butterfly caterpillars of America north of Mexico. Mem. Am. Entomol. Inst. 69: 1824
Robinson GS, Ackery PR, Kitching IJ, Beccaloni GW, Hernandez LM (2002b) HOSTS – A database of hostplants of the world's Lepidoptera, http://www/nhm.ac.uk/entomology/hostplants/index.html
Royal Society of Canada (2001) An Expert Panel Report on the Future of Food Biotechnology. The Royal Society of Canada, Ottawa, Canada
Saxena, D, Flores, S, Stotzky, G (1999) Insecticidal toxin in root exudates from Bt corn. Nature 402: 480 CrossRef
Schuster MR, Calderon M (1986) Interactions of host plant resistant genotypes and beneficial insects in cotton ecosys- tems. In Boethel DJ, Eikenbary RD, eds, Interaction of Host Plant Resistance and Parasitoids and Predators of Insects. Halstead Press, New York, pp 84–97
Sears, MK, Hellmich, RL, Stanley-Horn, DE, Oberhauser, KS, Pleasants, JM, Mattila, HR, Siegfried, BD, Dively, GP (2001) Impact of Bt corn pollen on monarch butterfly populations: A risk assessment. Proc. Natl. Acad. Sci. USA 98: 1193711942 CrossRef
Shea, K, Kelly, D (1998) Estimating biocontrol agent impact with matrix models: Carduus nutans in New Zealand. Ecol. Appl. 8: 824832 CrossRef
Smith, RA, Couche, GA (1991) The phylloplane as a source of Bacillus thuringiensis variants. Appl. Environ. Microbiol. 57: 311
Snow AA, Andersen B, Jorgensen RB (1999) Costs of transgenic herbicide resistance introgressed from Brassica napus into weedy B. rapa. Mol. Ecol. 8: 605–615
Snow, AA, Palma, PM (1997) Commercialization of transgenic plants: Potential ecological risks. Bioscience 47: 206206 CrossRef
Snow, AA, Pilson, D, Rieseberg, LH, Paulsen, MJ, Pleskac, N, Reagon, MR, Wolf, DE, Selbo, SM (2003) A Bt transgene reduces herbivory and enhances fecundity in wild sunflowers. Ecol. Appl. 13: 279286 CrossRef
Song, ZP, Lu, BR, Zhu, YG, Chen, JK (2003) Gene flow from cultivated rice to the wild species Oryza rufipogon under experimental field conditions. New Phytol. 157: 657665 CrossRef
Srinivasan, G, Babu, PC (2001) Effects of Bacillus thuringiensis Berliner on predatory green lacewing, Chrysoperla carnea Stephens (Chrysopidae: Neroptera). Pestic Res. J. 13: 266269
Stewart, CN, All, JN, Raymer, PL, Ramachandran, S (1997) Increased fitness of transgenic insecticidal rapeseed under insect selection pressure. Mol. Ecol. 6: 773779 CrossRef
Story, JM, Good, WR, White, LJ, Smith, L (2000) Effects of the interaction of the biocontrol agent Agapeta zoegana L. (Lepidoptera: Cochylidae) and grass competition on spotted knapweed. Biol. Control 17: 182190 CrossRef
Strauss, SY, Siemens, DH, Decher, MB, Mitchell-Olds T (1999) Ecological costs of plant resistance to herbivores in the currency of pollination. Evolution 53: 11051113 CrossRef
Strong DR (1984) Density-vague ecology and liberal population regulation in insects. In Price PW, Slobodchikoff CN, Gaud WS, eds, Wiley, New York, pp 313
Strong, DR (1992) Are trophic cascades all wet – Differentiation and donor-control in speciose ecosystems. Ecology 73: 747754 CrossRef
Tiedje, JM, Colwell, RK, Grossman, YL, Hodson, RE, Lenski, RE, Mack, RN, Regal, PJ (1989) The planned introduction of genetically engineered organisms: ecological considerations and recommendations. Ecology 70: 298 CrossRef
Tscharntke, T (1999) Insects on common reed (Phragmites australis): community structure and the impact of herbivory on shoot growth. Aquat. Bot. 64: 399410 CrossRef
Turkington, R, Klein, E, Chanway, CP (1993) Interactive effects of nutrients and disturbance – an experimental test of plant strategy theory. Ecology 74: 863878 CrossRef
Turlings, TCJ, Bernasconi, M, Bertossa, R, Bigler, F, Caloz, G, Dorn, S (1998) The induction of volatile emissions in maize by three herbivore species with different feeding habits – Possible consequences for their natural enemies. Biol. Control 11: 122129 CrossRef
U N (1935) Genome-analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jap. J. Bot. 7: 389452
van Frankenhuyzen K, Nystrom C (1999) The Bacillus thuringiensis toxin specificity database. http://www.glfc.cfs.nrcan.gc.ca/bacillus;
van Frankenhuyzen, K, Gringorten, JL, Milne, RE, Gauthier, D, Pusztai, M, Brousseau, R, Masson, L (1991) Specificity of activated Cry1a proteins from Bacillus thuringiensis subsp. kurstaki Hd-1 for defoliating forest Lepidoptera. Appl. Environ. Microbiol. 57: 16501655
Volenberg, DS, Hopen, HJ, Campobasso, G (1999) Biological control of yellow toadflax (Linaria vulgaris) by Eteobalea serratella in peppermint (Mentha piperita). Weed Sci. 47: 226232
Wagner, DL, Peacock, JW, Carter, JL, Talley, SE (1996) Field assessment of Bacillus thuringiensis on nontarget lepidoptera. Environ. Entomol. 25: 14441454 CrossRef
Wolfenbarger, LL, Phifer, PR (2000) The ecological risks and benefits of genetically engineered plants. Science 290: 2088 CrossRef
Zangerl, AR, McKenna, D, Wraight, CL, Carroll, M, Ficarello, P, Warner, R, Berenbaum, MR (2001) Effects of exposure to event 176 Bacillus thuringiensis corn pollen on monarch and black swallowtail caterpillars under field conditions. Proc. Natl. Acad. Sci. USA 98: 1190811912 CrossRef