Long-Term Assessment of the Effects of Transgenic Bt Cotton on the Abundance of Nontarget Arthropod Natural Enemies

Abstract A 6-yr field study assessed the long-term impact of Bt cotton producing the Cry1Ac δ-endotoxin on 22 taxa of foliar-dwelling arthropod natural enemies in Arizona. No chronic, long-term effects of Bt cotton were observed over multiple generations of nontarget taxa. Zero-2 taxa declined significantly in unsprayed Bt compared with non-Bt cotton each year. In contrast, positive control studies showed that insecticide applications for caterpillars and other pests in both non-Bt and Bt cotton had much greater negative effects on 10 taxa. Multivariate principal response curves supported the findings of univariate analyses for the entire natural enemy community, showing no effect of Bt cotton but large and long-lasting negative effects from the use of insecticides. Multi-year analyses provided greater statistical power and indicated significant reductions that averaged 19% in five arthropod predator taxa in unsprayed Bt compared with non-Bt cotton. Most of these reductions were likely associated with reductions in lepidopteran prey. However, results of a companion study examining natural enemy function suggest that these minor reductions in Bt cotton have little ecological meaning. Multi-year analyses showed an average significant reduction of 48% in 13 taxa for plots receiving insecticide applications. On average, a 3-yr study with four replicates per year was sufficient to discern changes of ≈20%, with 80% power in unsprayed cotton. This long-term study indicates that the effects of Bt cotton on a representative nontarget community are minor, especially in comparison with the alternative use of broad-spectrum insecticides. Guidelines for improving nontarget field studies are discussed.

[1]  D. R. Ring,et al.  Transgenic crops expressing Bt proteins: current status, challenges and outlook. , 2004 .

[2]  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.

[3]  J. Hagler,et al.  Determining the frequency of heteropteran predation on sweetpotato whitefly and pink bollworm using multiple ELISAs , 1994 .

[4]  C. Ellers-kirk,et al.  Large-Scale Management of Insect Resistance to Transgenic Cotton in Arizona: Can Transgenic Insecticidal Crops be Sustained? , 2001, Journal of economic entomology.

[5]  Steven E. Naranjo,et al.  Mortality dynamics and population regulation in Bemisia tabaci , 2005 .

[6]  R. Venette,et al.  In-field monitoring of beneficial insect populations in transgenic corn expressing a Bacillus thuringiensis toxin , 2001 .

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

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

[9]  Ter Braak,et al.  Canoco reference manual and CanoDraw for Windows user''s guide: software for canonical community ord , 2002 .

[10]  Steven E. Naranjo,et al.  Improved Conservation of Natural Enemies with Selective Management Systems for Bemisia tabaci (Homoptera: Aleyrodidae) in Cotton* , 2003 .

[11]  B. Ekbom,et al.  A Comparison of Vacuum and Whole-Plant Methods for Sampling Predaceous Arthropods on Cotton , 1977 .

[12]  J. Obrycki,et al.  Field deposition of Bt transgenic corn pollen: lethal effects on the monarch butterfly , 2000, Oecologia.

[13]  Paul C. Jepson,et al.  A metapopulation approach to modelling the long-term impact of pesticides on invertebrates. , 1993 .

[14]  L. Ehler,et al.  Secondary Outbreak Induction of Beet Armyworm by Experimental Insecticide Applications in Cotton in California , 1973 .

[15]  A. J. Underwood,et al.  Environmental decision-making and the precautionary principle: what does this principle mean in environmental sampling practice? , 1997 .

[16]  Steven E. Naranjo,et al.  Spatial Distribution of Preimaginal Bemisia tabaci (Homoptera: Aleyrodidae) in Cotton and Development of Fixed-Precision Sequential Sampling Plans , 1994 .

[17]  P. Jepson,et al.  Analysis of the spatial component of pesticide side effects on non-target invertebrate populations and its relevance to hazard analysis. , 1990 .

[18]  R. Berry,et al.  Longevity of phytophagous heteropteran predators feeding on transgenic Btt‐potato plants , 2000 .

[19]  G. Lozzia Biodiversity and structure of ground beetle assemblages (Coleoptera Carabidae) in Bt corn and its effects on non target insects. , 1999 .

[20]  Steven E. Naranjo,et al.  Long-Term Assessment of the Effects of Transgenic Bt Cotton on the Function of the Natural Enemy Community , 2005 .

[21]  Travis R. Glare,et al.  Bacillus Thuringiensis: Biology, Ecology and Safety , 2000 .

[22]  H. M. Flint,et al.  Seasonal infestation by pink bollworm, Pectinophora gossypiella (Saunders) of transgenic cotton, containing the Bollgard gene, planted in commercial fields in central Arizona , 1996 .

[23]  M. Rice,et al.  Preimaginal Development, Survival, and Field Abundance of Insect Predators on Transgenic Bacillus thuringiensis Corn , 1997 .

[24]  J. Hagler,et al.  Use of a gut content ELISA to detect whitefly predator feeding activity after field exposure to different insecticide treatments , 2005 .

[25]  R. Littell SAS System for Mixed Models , 1996 .

[26]  B. Croft,et al.  Test systems to determine the ecological risks posed by toxin release from Bacillus thuringiensis genes in crop plants , 1994 .

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

[28]  A. Shelton,et al.  Bt Sweet Corn and Selective Insecticides: Impacts on Pests and Predators , 2003, Journal of economic entomology.

[29]  Peter C. Ellsworth,et al.  Cost-Effective Lygus Managment in Arizona Cotton , 2001 .

[30]  Steven E. Naranjo,et al.  Conservation of natural enemies in cotton: role of insect growth regulators in management of Bemisia tabaci , 2004, Biological Control.

[31]  Deng Shu Effect of transgenic Bt cotton on population dynamics of the non target pests and natural enemies of pests , 2003 .

[32]  J. Carroll,et al.  Bollgard Cotton: An Assessment of Global Economic, Environmental, and Social Benefits , 2001 .

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

[34]  C.J.F. ter Braak,et al.  CANOCO Reference Manual and User's Guide to Canoco for Windows: Software for Canonical Community Ordination (Version 4) , 1998 .

[35]  M. A. Al-Deeb,et al.  No Effect of Bacillus thuringiensis Corn and Bacillus thuringiensis on the Predator Orius insidiosus (Hemiptera: Anthocoridae) , 2001 .

[36]  Steven E. Naranjo,et al.  Spatial Distribution of Adult Bemisia tabaci (Homoptera: Aleyrodidae) in Cotton and Development and Validation of Fixed-Precision Sampling Plans for Estimating Population Density , 1995 .

[37]  John R. Ruberson,et al.  Canopy- and Ground-Dwelling Predatory Arthropods in Commercial Bt and non-Bt Cotton Fields: Patterns and Mechanisms , 2005 .

[38]  A. Hilbeck,et al.  Effects of transgenic Bacillus thuringiensis corn-fed prey on mortality and development time of immature Chrysoperla cornea (Neuroptera: Chrysopidae) , 1998 .

[39]  H. Seney Integrated pest management for cotton in the western region of the United States. , 1984 .

[40]  M. O’Callaghan,et al.  Effects of plants genetically modified for insect resistance on nontarget organisms. , 2005, Annual review of entomology.

[41]  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.

[42]  Steven E. Naranjo,et al.  Integrated management approaches for pink bollworm in the southwestern United States , 1998 .

[43]  S. Turnipseed,et al.  A Multiyear, Large-Scale Comparison of Arthropod Populations on Commercially ManagedBtand Non-BtCotton Fields , 2005 .

[44]  R. Cannon,et al.  Bt Transgenic Crops: Risks and Benefits , 2000 .

[45]  Leslie C. Lewis,et al.  Assessing the Effects of Pest Management on Nontarget Arthropods: The Influence of Plot Size and Isolation , 2005 .

[46]  Michelle Marvier,et al.  IMPROVING RISK ASSESSMENT FOR NONTARGET SAFETY OF TRANSGENIC CROPS , 2002 .

[47]  Richard L. Hellmich,et al.  Impact of Bt corn pollen on monarch butterfly populations: A risk assessment , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[48]  G. D. Buntin,et al.  Effect of Bacillus thuringiensis Transgenic Corn for Lepidopteran Control on Nontarget Arthropods , 2005 .

[49]  A. Jensen,et al.  Transgenic Bt potato and conventional insecticides for Colorado potato beetle management: comparative efficacy and non‐target impacts , 2001 .

[50]  L L Wolfenbarger,et al.  The Ecological Risks of Engineered Crops , 1996 .

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

[52]  H. R. Prendeville,et al.  Ecological Effects of Transgenic Crops and the Escape of Transgenes into Wild Populations , 2004 .

[53]  S. Arpaia,et al.  The impact of transgenic plants on natural enemies: a critical review of laboratory studies , 2005 .

[54]  Paul J. Van den Brink,et al.  Multivariate analysis of stress in experimental ecosystems by Principal Response Curves and similarity analysis , 1998, Aquatic Ecology.

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

[56]  H. Schmidli,et al.  A faunistic approach to assess potential side-effects of genetically modified Bt-Corn on non-target arthropods under field conditions , 2004 .

[57]  J. Lundgren,et al.  Coleopteran-specific Cry3Bb Toxin from Transgenic Corn Pollen Does Not Affect the Fitness of a Nontarget Species, Coleomegilla maculata DeGeer (Coleoptera: Coccinellidae) , 2002 .

[58]  P. Barbosa,et al.  Impact of Cry3A-Intoxicated Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) and Pollen on Consumption, Development, and Fecundity of Coleomegilla maculata (Coleoptera: Coccinellidae) , 1998 .

[59]  A. Shelton,et al.  Economic, ecological, food safety, and social consequences of the deployment of bt transgenic plants. , 2002, Annual review of entomology.

[60]  Kent M. Daane,et al.  Commercialization of Predators: Recent Lessons from Green Lacewings (Neuroptera: Chrysopidae: Chrosoperla) , 2000 .

[61]  J. Losey,et al.  Transgenic pollen harms monarch larvae , 1999, Nature.

[62]  B. Federici,et al.  Effects of Bt on Non-Target Organisms , 2003 .

[63]  Paul J. Van den Brink,et al.  Principal response curves: Analysis of time‐dependent multivariate responses of biological community to stress , 1999 .

[64]  F. Bigler,et al.  Bacillus thuringiensis toxin (Cry1Ab) has no direct effect on larvae of the green lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). , 2004, Journal of insect physiology.

[65]  Julian Di Stefano,et al.  How much power is enough? Against the development of an arbitrary convention for statistical power calculations , 2003 .

[66]  D. Andow,et al.  Science-Based Risk Assessment for Nontarget Effects of Transgenic Crops , 2004 .

[67]  S. Turnipseed,et al.  Predaceous Arthropods and Lepidopteran Pests on Conventional, Bollgard, and Bollgard II Cotton Under Untreated and Disrupted Conditions , 2005 .

[68]  A. Hilbeck,et al.  Prey‐mediated effects of Cry1Ab toxin and protoxin and Cry2A protoxin on the predator Chrysoperla carnea , 1999 .

[69]  S. Turnipseed,et al.  A Multiyear, Large-Scale Comparison of Arthropod Populations on Commercially Managed Bt and Non-Bt Cotton Fields , 2005 .

[70]  H. M. Flint,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 , 1995 .

[71]  R. Downey Environmental Effects of Transgenic Plants , 2003 .

[72]  P. Barbosa,et al.  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) , 1998 .

[73]  M. Whitehouse,et al.  A Comparison of Arthropod Communities in Transgenic Bt and Conventional Cotton in Australia , 2005 .

[74]  Nicholas J. Mills,et al.  Effect of Bt-toxin (Cry1Ac) in Transgenic Cotton on the Adult Longevity of Four Heteropteran Predators , 2002 .