Simulated Effects of Transgenic Bt Crops on Specialist Parasitoids of Target Pests

Abstract Large-scale adoption of transgenic crops that produce Bacillus thuringiensis (Bt) toxins could greatly reduce populations of target pests and their specialist parasitoids. We used a spatially explicit model of host-parasitoid population dynamics to examine effects of Bt crops on parasitoid persistence. We modeled a 9,000-ha region with 900 fields of 10 ha, each planted with either a Bt crop or a non-Bt crop refuge. In the 13,524 simulations we conducted, the pest (i.e., host) was never lost from the region before the parasitoid. The parasitoid was lost from the region in 36% of the simulations. The host was lost after the parasitoid in 12% of all simulations. The probability of regional parasitoid loss increased as the percentage of Bt fields and rotation of field types (Bt and non-Bt) increased and as host reproductive rate and parasitoid attack rate decreased. Regional parasitoid loss also increased as the insecticide spray threshold for target pests in non-Bt fields decreased and as parasitoid susceptibility to insecticide increased. With field types fixed, regional parasitoid loss increased as parasitoid movement increased. However, with field types rotated, parasitoid movement did not influence regional parasitoid loss. Host movement did not influence regional parasitoid loss. Factors not modeled that would reduce risk of regional parasitoid loss include use of alternate hosts by the parasitoid, use of alternate host plants by the target pest, and evolution of resistance to the Bt crop by the pest. The results suggest that risk of regional parasitoid loss can be assessed from the parasitoid life history traits and reduced by increasing the percentage of refuge fields, fixing refuge locations, and increasing the insecticide spray threshold for target pests in refuges.

[1]  T. A. Brindley,et al.  SIGNIFICANT DEVELOPMENTS IN EUROPEAN CORN BORER RESEARCH1,2 , 1963 .

[2]  M. Hassell.  The dynamics of arthropod predator-prey systems. , 1979, Monographs in population biology.

[3]  Michael T. Johnson,et al.  Effects of natural enemies on the rate of herbivore adaptation to resistant host plants , 1991 .

[4]  Michael P. Hassell,et al.  Spatial structure and chaos in insect population dynamics , 1991, Nature.

[5]  M. T. Johnson,et al.  Interaction of genetically engineered host plant resistance and natural enemies of Heliothis viresce , 1992 .

[6]  B. Tabashnik,et al.  Host-Mediated Competition Between the Pathogen Bacillus thuringiensis and the Parasitoid Cotesia plutellae of the Diamondback Moth (Lepidoptera: Plutellidae) , 1997 .

[7]  D. Landis,et al.  Oviposition of European Corn Borer (Lepidoptera: Pyralidae) and Impact of Natural Enemy Populations in Transgenic Versus Isogenic Corn , 1997 .

[8]  M. T. Johnson,et al.  Effects of natural enemies on relative fitness of Heliothis virescens genotypes adapted and not adapted to resistant host plants , 1997 .

[9]  M. T. Johnson.  Interaction of Resistant Plants and Wasp Parasitoids of Tobacco Budworm (Lepidoptera: Noctuidae) , 1997 .

[10]  B. Tabashnik,et al.  Independent and Combined Effects of Bacillus thuringiensis and the Parasitoid Cotesia plutellae (Hymenoptera: Braconidae) on Susceptible and Resistant Diamondback Moth (Lepidoptera: Plutellidae) , 1997 .

[11]  G. Poppy,et al.  Parasitoid behaviour and Bt plants , 1999, Nature.

[12]  C. Pilcher.  Phenological, physiological, and ecological influences of transgenic Bt corn on European corn borer management , 1999 .

[13]  G. Poppy,et al.  Potential side effects of insect-resistant transgenic plants on arthropod natural enemies. , 1999, Trends in biotechnology.

[14]  F. Gould,et al.  THE INFLATED CALYX OF PHYSALIS ANGULATA: A REFUGE FROM PARASITISM FOR HELIOTHIS SUBFLEXA , 1999 .

[15]  A. Hilbeck,et al.  Tritrophic Interactions of Transgenic Bacillus thuringiensis Corn, Anaphothrips obscurus (Thysanoptera: Thripidae), and the Predator Orius majusculus (Heteroptera: Anthocoridae) , 2000 .

[16]  B. Tabashnik,et al.  Supporting a Cautious Approach to Agricultural Biotechnology , 2001 .

[17]  J. Losey,et al.  Transgenic Insecticidal Corn: Beyond Insecticidal Toxicity to Ecological Complexity , 2001 .

[18]  B. Siegfried,et al.  Development of European corn borer larvae on Event 176 Bt corn: influence on survival and fitness , 2001 .

[19]  Adrian Ely,et al.  Assessing risks and benefits: Bt maize in Kenya , 2001 .

[20]  J. Losey,et al.  Evaluation of Noncorn Host Plants as a Refuge in a Resistance Management Program for European Corn Borer (Lepidoptera: Crambidae) on Bt-Corn , 2001 .

[21]  D. Bourguet,et al.  Ostrinia nubilalis parasitism and the field abundance of non-target insects in transgenic Bacillus thuringiensis corn (Zea mays). , 2002, Environmental biosafety research.

[22]  Marcel Dicke,et al.  Insect-resistant transgenic plants in a multi-trophic context. , 2002, The Plant journal : for cell and molecular biology.

[23]  F. Bigler,et al.  Uptake of Bt‐toxin by herbivores feeding on transgenic maize and consequences for the predator Chrysoperla carnea , 2002 .

[24]  J. Bernal,et al.  Impacts of Developing on Bt Maize-Intoxicated Hosts on Fitness Parameters of a Stem Borer Parasitoid , 2002 .

[25]  F. Ramsey,et al.  The statistical sleuth : a course in methods of data analysis , 2002 .

[26]  Timothy J. Dennehy,et al.  Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  F. Ge,et al.  Diversity of Arthropod Communities in Transgenic Bt Cotton and Nontransgenic Cotton Agroecosystems , 2003 .

[28]  Richard T. Roush,et al.  Insect Resistance to Transgenic Bt Crops: Lessons from the Laboratory and Field , 2003, Journal of economic entomology.

[29]  B. Manachini.  Effects of transgenic corn on Lydella thompsoni Herting (Diptera:Tachinidae) parasitoid of Ostrinia nubilalis Hb. (Lepidoptera Crambidae) , 2003 .

[30]  A. Felsot,et al.  Effect ofBacillus thuringiensisCorn on Natural Enemies of the European Corn Borer , 2003 .

[31]  Gerald E. Wilde,et al.  Effect of Bt Corn Expressing the Cry3Bb1 Toxin for Corn Rootworm Control on Aboveground Nontarget Arthropods , 2003 .

[32]  M. Baur,et al.  Effect of Bt-cotton expressing Cry1A(c) on the survival and fecundity of two hymenopteran parasitoids (Braconidae, Encyrtidae) in the laboratory , 2003 .

[33]  Jan-Peter Nap,et al.  The release of genetically modified crops into the environment. Part II. Overview of ecological risk assessment. , 2003, The Plant journal : for cell and molecular biology.

[34]  Guofa Zhou,et al.  Species richness and parasitism in an assemblage of parasitoids attacking maize stem borers in coastal Kenya , 2003 .

[35]  J. Kovach,et al.  Select Nontarget Arthropod Abundance in Transgenic and Nontransgenic Field Crops in Ohio , 2003 .

[36]  B. Tabashnik,et al.  Resistance Management for Sustainable Use of Bacillus thuringiensis Crops in Integrated Pest Management , 2004 .

[37]  Timothy J. Dennehy,et al.  Arthropod Abundance and Diversity in Bt and Non-Bt Cotton Fields , 2004 .

[38]  Ian Denholm,et al.  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). , 2004, Journal of insect physiology.

[39]  M. Sisterson,et al.  Coevolution across landscapes: a spatially explicit model of parasitoid-host coevolution , 2004, Evolutionary Ecology.

[40]  Yu-yuan Guo,et al.  Evaluation of maize as a refuge for management of resistance to Bt cotton by Helicoverpa armigera (Hübner) in the Yellow River cotton-farming region of China , 2004 .

[41]  G. Prütz,et al.  Effect of Bt corn leaf suspension on food consumption by Chilo partellus and life history parameters of its parasitoid Cotesia flavipes under laboratory conditions , 2004 .

[42]  S. Heuberger,et al.  Long-term evaluation of compliance with refuge requirements for Bt cotton. , 2005, Pest management science.

[43]  S. Lawrence.  Agbio keeps on growing , 2005, Nature Biotechnology.