Cited by 252Insect Resistance and GeneticsGenetically Modified Organisms ResearchInsect-Plant Interactions and Control

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Impacts of Bt crops on non-target invertebrates and insecticide use patterns.

Naranjo, S. E.·2009·CABI Reviews

DOI 10.1079/pavsnnr20094011

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Abstract

The ubiquitous nature of Bacillus thuringiensis ( Bt ), a Gram-positive bacterium capable of producing crystal proteins with insecticidal activity during sporulation, is now being mirrored in major crops plants that have been engineered through recombinant DNA to carry genes responsible for producing these crystal proteins and providing host plant resistance to major lepidopteran and coleopteran pests. In 2007, the 11th year of commercial production, Bt maize and Bt cotton were commercially produced on a total of ∼42 million hectares in 20 countries. Assessment of environmental safety has been and continues to be a key element of transgenic crop technology. This review focuses on two environmental elements, effects on non-target invertebrates and changes in insecticide use patterns since the adoption of Bt maize and cotton. Meta-analyses of the extant literature on invertebrate non-target effects reveals that the pattern and extent of impact varies in relation to taxonomy, ecological or anthropomorphic guild, route of exposure and the non- Bt control against which effects are gauged. Hazards identified in the laboratory may not always manifest in the field and the minor negative effects of Bt crops demonstrated in the field pale in comparison with alternative pest suppression measures based on insecticides. The efficacy of Bt maize and cotton against major pest species has been associated with an estimated 136.6 million kg global reduction in insecticide active ingredient used between 1996 and 2006 (29.9% reduction). Benefits vary by country and region and are heavily weighted towards cotton production, which has historically been one of the largest users of insecticides in the world.

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Schmidt, J. E. U., Braun, C. U., Whitehouse, L. P., & Hilbeck, A. (2008) · Archives of Environmental Contamination and Toxicology · doi:10.1007/s00244-008-9191-9 · Cited by 90
IMPROVING RISK ASSESSMENT FOR NONTARGET SAFETY OF TRANSGENIC CROPS
Marvier, M. (2002) · Ecological Applications · doi:10.1890/1051-0761(2002)012[1119:irafns]2.0.co;2 · Cited by 90
Effect ofBtCorn for Corn Rootworm Control on Nontarget Soil Microarthropods and Nematodes
Al-Deeb, M. A., Wilde, G. E., Blair, J. M., & TODD, T. C. (2003) · Environmental Entomology · doi:10.1603/0046-225x-32.4.859 · Cited by 86
Impact of Cry3A-Intoxicated Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) and Pollen on Consumption, Development, and Fecundity of Coleomegilla maculata (Coleoptera: Coccinellidae)
Riddick, E. W., & Barbosa, P. (1998) · Annals of the Entomological Society of America · doi:10.1093/aesa/91.3.303 · Cited by 86
Field decomposition of transgenic Bt maize residue and the impact on non-target soil invertebrates
Zwahlen, C., Hilbeck, A., & Nentwig, W. (2007) · Plant and Soil · doi:10.1007/s11104-007-9410-6 · Cited by 84
Transgenic Bt maize and Rhopalosiphum padi (Hom., Aphididae) performance
Lumbierres, B., Albajes, R., & Pons, X. (2004) · Ecological Entomology · doi:10.1111/j.0307-6946.2004.00597.x · Cited by 84
Effects of Novel Pesticides on Bumble Bee (Hymenoptera: Apidae) Colony Health and Foraging Ability
Morandin, L. A., & Winston, M. L. (2003) · Environmental Entomology · doi:10.1603/0046-225x-32.3.555 · Cited by 84
Field and Laboratory Evaluations of Transgenic Bacillus thuringiensis Corn on Secondary Lepidopteran Pests (Lepidoptera: Noctuidae)
Pilcher, C. D., Rice, M. E., Obrycki, J. J., & Lewis, L. C. (1997) · Journal of Economic Entomology · doi:10.1093/jee/90.2.669 · Cited by 83
Impact of Bt cotton adoption on pesticide use by smallholders: A 2-year survey in Makhatini Flats (South Africa)
Hofs, J.-L., Fok, M. A. C., & Vaissayre, M. (2006) · Crop Protection · doi:10.1016/j.cropro.2006.01.006 · Cited by 83
Impact of transgenic cotton plants on a non‐target pest, Aphis gossypii Glover
Liu, X. D., Zhai, B. P., Zhang, X. X., & Zong, J. M. (2005) · Ecological Entomology · doi:10.1111/j.0307-6946.2005.00690.x · Cited by 82
Abundance of non-target pests in transgenic Bt-maize: A farm scale study
Pons, X., Lumbierres, B., López, C., & Albajes, R. (2005) · European Journal of Entomology · doi:10.14411/eje.2005.010 · Cited by 79
Tritrophic Choice Experiments with Bt Plants, the Diamondback Moth (Plutella xylostella) and the parasitoid Cotesia plutellae
Schuler, T. H., Potting, R. P. J., Denholm, I., Clark, S. J., Clark, A. J., Stewart, C. N., & Poppy, G. M. (2003) · Transgenic Research · doi:10.1023/a:1023342027192 · Cited by 79
Biological Parameters of Convergent Lady Beetle (Coleoptera: Coccinellidae) Feeding on Aphids (Homoptera: Aphididae) on Transgenic Potato
Doğan, E. B., Berry, R. E., Reed, G. L., & Rossignol, P. A. (1996) · Journal of Economic Entomology · doi:10.1093/jee/89.5.1105 · Cited by 79
Effect ofBt-toxin (Cry1Ac) in Transgenic Cotton on the Adult Longevity of Four Heteropteran Predators
Ponsard, S., Gutierrez, A. P., & Mills, N. J. (2002) · Environmental Entomology · doi:10.1603/0046-225x-31.6.1197 · Cited by 78
Impact of Transgenic Bacillus thuringiensis Corn and Crop Phenology on Five Nontarget Arthropods
Pilcher, C. D., Rice, M. E., & Obrycki, J. J. (2005) · Environmental Entomology · doi:10.1603/0046-225x(2005)034[1302:iotbtc]2.0.co;2 · Cited by 78
Transmission ofBtToxin to the PredatorPropylaea japonica(Coleoptera: Coccinellidae) Through Its Aphid Prey Feeding on TransgenicBtCotton
Zhang, G., Wan, F., Löveï, G. L., Liu, W., & Guo, J. (2006) · Environmental Entomology · doi:10.1603/0046-225x-35.1.143 · Cited by 77
Can Bacillus thuringiensis (Bt) corn residues and Bt-corn plants affect life-history traits in the earthworm Aporrectodea caliginosa?
Vercesi, M. L., Krogh, P. H., & Holmstrup, M. (2005) · Applied Soil Ecology · doi:10.1016/j.apsoil.2005.07.002 · Cited by 75
BT COTTON IN SOUTH AFRICA: ADOPTION AND THE IMPACT ON FARM INCOMES AMONGST SMALL-SCALE AND LARGE SCALE FARMERS
Gouse, M., Kirsten, J. F., & Jenkins, L. (2003) · Agrekon · doi:10.1080/03031853.2003.9523607 · Cited by 74
The Present and Future Role of Insect-Resistant Genetically Modified Maize in IPM
Hellmich, R. L., Albajes, R., Bergvinson, D., Prasifka, J. R., Wang, Z., & Weiss, M. J. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8373-0_5 · Cited by 73
Effects of Bt corn pollen on honey bees: emphasis on protocol development
Rose, R., Dively, G. P., & Pettis, J. S. (2007) · Apidologie · doi:10.1051/apido:2007022 · Cited by 73
Consumption of Bt Maize Pollen Expressing Cry1Ab or Cry3Bb1 Does Not Harm Adult Green Lacewings, Chrysoperla carnea (Neuroptera: Chrysopidae)
Li, Y., Meissle, M., & Romeis, J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002909 · Cited by 72
Effects of Bt corn on Rhopalosiphum padi L. (Rhynchota Aphididae) and on its predator Chrysoperla carnea Stephen (Neuroptera Chrysopidae)
Lozzia, G. C., Furlanis, C., Manachini, B. R. I., & Rigamonti, I. E. (1998) · Cited by 71
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)
Riddick, E. W., Dively, G. P., & Barbosa, P. (1998) · Annals of the Entomological Society of America · doi:10.1093/aesa/91.5.647 · Cited by 71
No Effect ofBacillus thuringiensisCorn andBacillus thuringiensison the PredatorOrius insidiosus(Hemiptera: Anthocoridae)
Al-Deeb, M. A., Wilde, G. E., & Higgins, R. A. (2001) · Environmental Entomology · doi:10.1603/0046-225x-30.3.625 · Cited by 71
Effect of Bt Corn Expressing the Cry3Bb1 Toxin for Corn Rootworm Control on Aboveground Nontarget Arthropods
Al-Deeb, M. A., & Wilde, G. E. (2003) · Environmental Entomology · doi:10.1603/0046-225x-32.5.1164 · Cited by 71
Influence of transgenic Bacillus thuringiensis corn-fed prey on prey preference of immature Chrysoperla carnea (Neuroptera: Chrysopidae)
Meier, M., & Hilbeck, A. (2001) · Basic and Applied Ecology · doi:10.1078/1439-1791-00034 · Cited by 70
Effects of dietary transgenic Bt corn pollen on larvae ofApis melliferaandGalleria mellonella
Hanley, A. V., Huang, Z., & Pett, W. L. (2003) · Journal of Apicultural Research · doi:10.1080/00218839.2003.11101097 · Cited by 70
The effects of pollen consumption of transgenic Bt maize on the common swallowtail, Papilio machaon L. (Lepidoptera, Papilionidae)
Lang, A., & Vojtech, E. (2005) · Basic and Applied Ecology · doi:10.1016/j.baae.2005.10.003 · Cited by 68
Diversity and seasonal phenology of aboveground arthropods in conventional and transgenic maize crops in Central Spain
Farinós, G. P., de la Poza, M., Hernández‐Crespo, P., Ortego, F., & Castañera, P. (2008) · Biological Control · doi:10.1016/j.biocontrol.2007.11.007 · Cited by 68
Effects of Bt maize on Frankliniella tenuicornis and exposure of thrips predators to prey‐mediated Bt toxin
Obrist, L. B., Klein, H., Dutton, A. C., & Bigler, F. (2005) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2005.00298.x · Cited by 68
Have Bt Crops Led to Changes in Insecticide Use Patterns and Impacted IPM?
Fitt, G. P. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8373-0_11 · Cited by 67
Bt Transgenic Crops: Risks and Benefits
Cannon, R. J. C. (2000) · Integrated Pest Management Reviews · doi:10.1023/a:1011347122894 · Cited by 65
Select Nontarget Arthropod Abundance in Transgenic and Nontransgenic Field Crops in Ohio
Jasinski, J. R., Eisley, J. B., Young, C. E., Kovach, J., & Willson, H. R. (2003) · Environmental Entomology · doi:10.1603/0046-225x-32.2.407 · Cited by 65
Beyond Bt: Alternative Strategies for Insect-Resistant Genetically Modified Crops
Malone, L. A., Gatehouse, A. M. R., & Barratt, B. I. P. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8373-0_13 · Cited by 64
Evaluating the Induced-Odour Emission of a Bt Maize and its Attractiveness to Parasitic Wasps
Turlings, T. C. J., Jeanbourquin, P., Held, M., & Degen, T. (2005) · Transgenic Research · doi:10.1007/s11248-005-0008-6 · Cited by 64
Evaluation of effects of transgenic Bt maize on microarthropods in a European multi-site experiment
Cortet, J., Griffiths, B. S., Bohanec, M., Demšar, D., Andersen, M. N., Caul, S., Birch, A. N., Pernin, C., Tabone, É., de Vaufleury, A., et al. (2007) · Pedobiologia · doi:10.1016/j.pedobi.2007.04.001 · Cited by 64
Effects of Cry1Ab Toxin onPropylea japonica(Thunberg) (Coleoptera: Coccinellidae) Through Its Prey,Nilaparvata lugensStål (Homoptera: Delphacidae), Feeding on TransgenicBtRice
Bai, Y., Jiang, M., Cheng, J. A., & Wang, D. (2006) · Environmental Entomology · doi:10.1603/0046-225x-35.4.1130 · Cited by 64
Bt Rice in Asia: Potential Benefits, Impact, and Sustainability
Cohen, M. B., Chen, M., Bentur, J. S., Heong, K. L., & Yè, G. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8373-0_8 · Cited by 63
Effects of transgenic cry1Ab rice pollen on fitness of Propylea japonica (Thunberg)
Bai, Y., Jiang, M., & Cheng, J. A. (2005) · Journal of Pest Science · doi:10.1007/s10340-004-0078-x · Cited by 63
Effects of natural enemies on relative fitness of Heliothis virescens genotypes adapted and not adapted to resistant host plants
Johnson, M. T., Gould, F. L., & Kennedy, G. G. (1997) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.1997.00133.x · Cited by 63
Effects of Bt maize-fed prey on the generalist predator Poecilus cupreus L. (Coleoptera: Carabidae)
Meissle, M., Vojtech, E., & Poppy, G. M. (2005) · Transgenic Research · doi:10.1007/s11248-004-6458-4 · Cited by 63
The influence of pesticide applications on Helicoverpa armigera Hübner and sucking pests in transgenic Bt cotton and non-transgenic cotton in China
Men, X., Ge, F., Edwards, C. A., & Yardım, E. N. (2004) · Crop Protection · doi:10.1016/j.cropro.2004.08.006 · Cited by 62
Effects of a Bacillus thuringiensis toxin, two Bacillus thuringiensis biopesticide formulations, and a soybean trypsin inhibitor on honey bee (Apis mellifera L.) survival and food consumption
Malone, L. A., Burgess, E. P. J., & Stefanovic, D. (1999) · Apidologie · doi:10.1051/apido:19990601 · Cited by 61
Development of hypopharyngeal glands in adult honey bees fed with a Bt toxin, a biotin-binding protein and a protease inhibitor
Malone, L. A., Todd, J. H., Burgess, E. P. J., & Christeller, J. T. (2004) · Apidologie · doi:10.1051/apido:2004063 · Cited by 61
Effects of Insecticide-Treated and Lepidopteran-Active Bt Transgenic Sweet Corn on the Abundance and Diversity of Arthropods
Rose, R., & Dively, G. P. (2007) · Environmental Entomology · doi:10.1603/0046-225x(2007)36[1254:eoialb]2.0.co;2 · Cited by 61
Effects of Bt-corn decomposition on the composition of the soil meso- and macrofauna
Hönemann, L., Zurbrügg, C., & Nentwig, W. (2008) · Applied Soil Ecology · doi:10.1016/j.apsoil.2008.04.006 · Cited by 60
A methodology to assess the profitability of Bt-cotton: case study results from the state of Karnataka, India
Pemsl, D. E., Waibel, H., & Orphal, J. (2004) · Crop Protection · doi:10.1016/j.cropro.2004.05.011 · Cited by 60
Subacute Effects of Cry1AbBtCorn Litter on the EarthwormEisenia fetidaand the SpringtailFolsomia candida
Clark, B. W., & Coats, J. R. (2006) · Environmental Entomology · doi:10.1603/0046-225x-35.4.1121 · Cited by 60
Bitrophic and tritrophic effects of Bt Cry3A transgenic potato on beneficial, non-target, beetles
Ferry, N., Mulligan, E. A., Majerus, M. E. N., & Gatehouse, A. M. R. (2007) · Transgenic Research · doi:10.1007/s11248-007-9088-9 · Cited by 59
Bt-maize effects on biological parameters of the non-target aphid Sitobion avenae (Homoptera: Aphididae) and Cry1Ab toxin detection
Ramírez‐Romero, R., Desneux, N., Chaufaux, J., & Kaiser, L. (2008) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2008.01.010 · Cited by 59
Consequences for Protaphorura armata (Collembola: Onychiuridae) following exposure to genetically modified Bacillus thuringiensis (Bt) maize and non-Bt maize
Heckmann, L., Griffiths, B. S., Caul, S., Thompson, J., Pusztai‐Carey, M., Moar, W. J., Andersen, M. N., & Krogh, P. H. (2005) · Environmental Pollution · doi:10.1016/j.envpol.2005.10.008 · Cited by 59
Impacts of Developing on Bt Maize-Intoxicated Hosts on Fitness Parameters of a Stem Borer Parasitoid
Bernal, J. S., Griset, J. G., & Gillogly, P. O. (2002) · Journal of Entomological Science · doi:10.18474/0749-8004-37.1.27 · Cited by 59
Consumption of two Bt and six non-Bt corn varieties by the woodlouse Porcellio scaber
Wandeler, H., Bahylova, J., & Nentwig, W. (2002) · Basic and Applied Ecology · doi:10.1078/1439-1791-00124 · Cited by 57
Field Assessment of the Effects of Transgenic Rice Expressing a Fused Gene ofcry1Abandcry1AcfromBacillus thuringiensisBerliner on Nontarget Planthopper and Leafhopper Populations
Chen, M., Ye, G. Y., Liu, Z., Yao, H., Chen, X. X., Shen, Z. C., Hu, C., & Datta, S. K. (2006) · Environmental Entomology · doi:10.1603/0046-225x-35.1.127 · Cited by 57
Impact assessment of Bt-maize on a moth parasitoid, Cotesia marginiventris (Hymenoptera: Braconidae), via host exposure to purified Cry1Ab protein or Bt-plants
Ramírez‐Romero, R., Bernal, J. S., Chaufaux, J., & Kaiser, L. (2006) · Crop Protection · doi:10.1016/j.cropro.2006.09.001 · Cited by 55
Bt maize pollen exposure and impact on the garden spider, Araneus diadematus
Ludy, C., & Lang, A. (2006) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2006.00375.x · Cited by 55
Effect of Bacillus thuringiensis Transgenic Corn for Lepidopteran Control on Nontarget Arthropods
Daly, T., & Buntin, G. D. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1292 · Cited by 55
Predaceous Arthropods and Lepidopteran Pests on Conventional, Bollgard, and Bollgard Ii Cotton Under Untreated and Disrupted Conditions
Hagerty, A. M., Kilpatrick, A. L., Turnipseed, S. G., Sullivan, M. J., & Bridges, W. C. (2005) · Environmental Entomology · doi:10.1603/0046-225x-34.1.105 · Cited by 54
Impacts of transgenic cry1Ab rice on non-target planthoppers and their main predator Cyrtorhinus lividipennis (Hemiptera: Miridae)—A case study of the compatibility of Bt rice with biological control
Chen, M., Liu, Z.-C., Yè, G., Shen, Z., Hu, C., Peng, Y., Altosaar, I., & Shelton, A. M. (2007) · Biological Control · doi:10.1016/j.biocontrol.2007.05.005 · Cited by 53
Effects of ingestion of a Bacillus thuringiensis toxin and a trypsin inhibitor on honey bee flight activity and longevity
Malone, L. A., Burgess, E. P. J., Gatehouse, H. S., Voisey, C. R., Tregidga, E. L., & Philip, B. A. (2001) · Apidologie · doi:10.1051/apido:2001111 · Cited by 52
Spatial and temporal dynamics of oviposition behavior of bollworm and three of its predators in Bt and non‐Bt cotton fields
Torres, J. B., & Ruberson, J. R. (2006) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2006.00422.x · Cited by 51
Unexpected Effects of Different Potato Resistance Factors to the Colorado Potato Beetle (Coleoptera: Chrysomelidae) on the Potato Aphid (Homoptera: Aphididae)
Ashouri, A., Michaud, D., & Cloutier, C. (2001) · Environmental Entomology · doi:10.1603/0046-225x-30.3.524 · Cited by 51
Insect-Resistant Transgenic Crops and Biological Control
Romeis, J., Driesche, R. G. V., Barratt, B. I. P., & Bigler, F. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8373-0_4 · Cited by 50
Larval Feeding on Bt Hybrid and Non-Bt Corn Seedlings by Harmonia axyridis (Coleoptera: Coccinellidae) and Coleomegilla maculata (Coleoptera: Coccinellidae)
Moser, S. E., Harwood, J. D., & Obrycki, J. J. (2008) · Environmental Entomology · doi:10.1603/0046-225x(2008)37[525:lfobha]2.0.co;2 · Cited by 50
Effects of Cry1Ab-Expressing Corn Anthers on Monarch Butterfly Larvae
Anderson, P. L., Hellmich, R. L., Sears, M. K., Sumerford, D. V., & Lewis, L. C. (2004) · Environmental Entomology · doi:10.1603/0046-225x-33.4.1109 · Cited by 48
Utility of Ground Beetle Species in Field Tests of Potential Nontarget Effects of Bt Crops
Lopez, M. D., Prasifka, J. R., Bruck, D. J., & Lewis, L. C. (2005) · Environmental Entomology · doi:10.1603/0046-225x(2005)034[1317:uogbsi]2.0.co;2 · Cited by 48
Tritrophic Interactions Among Bt (Cry3Bb1) Corn, Aphid Prey, and the Predator Coleomegilla maculata (Coleoptera: Coccinellidae)
Lundgren, J. G., & Wiedenmann, R. N. (2005) · Environmental Entomology · doi:10.1603/0046-225x-34.6.1621 · Cited by 48
The Present and Future Role of Insect-Resistant Genetically Modified Potato Cultivars in IPM
Grafius, E. J., & Douches, D. S. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8373-0_7 · Cited by 48
Assessing the Effects of Bt Maize on the Predatory Mite Neoseiulus cucumeris
Obrist, L. B., Klein, H., Dutton, A. C., & Bigler, F. (2006) · Experimental and Applied Acarology · doi:10.1007/s10493-006-0008-0 · Cited by 46
Effects of the Cry1Ac toxin of Bacillus thuringiensis on Microplitis mediator, a parasitoid of the cotton bollworm, Helicoverpa armigera
Liu, X., Zhang, Q., Zhao, Y., Cai, Q., Xu, H., & Li, J. (2005) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2005.00248.x · Cited by 45
Comparing methods to evaluate the effects of Bt maize and insecticide on spider assemblages
Meissle, M., & Lang, A. (2005) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2004.12.007 · Cited by 45
Impact of insecticidal proteins expressed in transgenic plants on bumblebee microcolonies
Babendreier, D., Reichhart, B., Romeis, J., & Bigler, F. (2008) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2007.00652.x · Cited by 45
Altered host plant preference of Tetranychus urticae and prey preference of its predator Phytoseiulus persimilis (Acari: Tetranychidae, Phytoseiidae) on transgenic Cry3Bb-eggplants
Rovenská, G. Z., Zemek, R., Schmidt, J. E. U., & Hilbeck, A. (2005) · Biological Control · doi:10.1016/j.biocontrol.2005.03.017 · Cited by 45
Biodiversity and Community Structure of Epedaphic and Euedaphic Springtails (Collembola) in Transgenic Rootworm Bt Corn
Bitzer, R. J., Rice, M. E., Pilcher, C. D., Pilcher, C., & Lam, W.-K. F. (2005) · Environmental Entomology · doi:10.1603/0046-225x(2005)034[1346:bacsoe]2.0.co;2 · Cited by 45
Arthropod Abundance and Diversity in Bt and Non-Bt Rice Fields
Li, F., Yè, G., Wu, Q. H., Peng, Y., & Chen, X. (2007) · Environmental Entomology · doi:10.1603/0046-225x(2007)36[646:aaadib]2.0.co;2 · Cited by 45
Development of European corn borer larvae on Event 176 Bt corn: influence on survival and fitness
Siegfried, B. D., Zoerb, A. C., & Spencer, T. (2001) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.2001.00843.x · Cited by 44
Target and non-target effects on the invertebrate community of Vip cotton, a new insecticidal transgenic
Whitehouse, M., Wilson, L., & Constable, G. A. (2007) · Australian Journal of Agricultural Research · doi:10.1071/ar06100 · Cited by 44
Dusky Sap Beetles (Coleoptera: Nitidulidae) and Other Kernel Damaging Insects in Bt and Non-Bt Sweet Corn in Illinois
Dowd, P. F. (2000) · Journal of Economic Entomology · doi:10.1603/0022-0493-93.6.1714 · Cited by 42
Impacts of Bacillus thuringiensis toxins on parasitoids (Hymenoptera: Braconidae) of Spodoptera litura and Helicoverpa armigera (Lepidoptera: Noctuidae)
Walker, G. P., Cameron, P. J., MacDonald, F., Madhusudhan, V. V., & Wallace, A. R. (2006) · Biological Control · doi:10.1016/j.biocontrol.2006.09.008 · Cited by 42
Effect of corn hybrids expressing the coleopteran-specific Cry3Bb1 protein for corn rootworm control on aboveground insect predators
Ahmad, A., Wilde, G. E., Whitworth, R. J., & Zolnerowich, G. (2006) · Journal of Economic Entomology · doi:10.1093/jee/99.4.1085 · Cited by 42
Recombinant and classically selected factors of potato plant resistance to the Colorado potato beetle, Leptinotarsa decemlineata, variously affect the potato aphid parasitoid Aphidius nigripes
Ashouri, A., Michaud, D., & Cloutier, C. (2001) · BioControl · doi:10.1023/a:1014123712776 · Cited by 41
Interactions of Bt-cotton and the omnivorous big-eyed bug Geocoris punctipes (Say), a key predator in cotton fields
Torres, J. B., & Ruberson, J. R. (2006) · Biological Control · doi:10.1016/j.biocontrol.2006.03.006 · Cited by 41
Early instar response to plant-delivered Bt-toxin in a herbivore (Spodoptera litura) and a predator (Propylaea japonica)
Zhang, G., Wan, F., Liu, W., & Guo, J. (2005) · Crop Protection · doi:10.1016/j.cropro.2005.08.008 · Cited by 41
Abundance and diversity of ground‐dwelling arthropods of pest management importance in commercial Bt and non‐Bt cotton fields
Torres, J. B., & Ruberson, J. R. (2006) · Annals of Applied Biology · doi:10.1111/j.1744-7348.2006.00087.x · Cited by 41
Longevity of phytophagous heteropteran predators feeding on transgenic Btt‐potato plants
Armer, C. A., Berry, R. E., & Kogan, M. (2000) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.2000.00672.x · Cited by 40
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
Duan, J. J., Head, G., Jensen, A. S., & Reed, G. L. (2004) · Environmental Entomology · doi:10.1603/0046-225x-33.2.275 · Cited by 40
Effects of Bacillus thuringiensisδ‐endotoxin‐fed Helicoverpa armigera on the survival and development of the parasitoid Campoletis chlorideae
Sharma, H. C., Dhillon, M. K., & Arora, R. (2007) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2007.00637.x · Cited by 39
Assessing Nontarget Impacts ofBtCorn Resistant to Corn Rootworms: Tier-1 Testing with Larvae ofPoecilus chalcites(Coleoptera: Carabidae)
Duan, J. J., Paradise, M. S., Lundgren, J. G., Bookout, J. T., Jiang, C., & Wiedenmann, R. N. (2006) · Environmental Entomology · doi:10.1603/0046-225x-35.1.135 · Cited by 39
Arthropods on Maize Ears for Detecting Impacts ofBtMaize on Nontarget Organisms
Eckert, J., Schuphan, I., Hothorn, L. A., & Gathmann, A. (2006) · Environmental Entomology · doi:10.1603/0046-225x-35.2.554 · Cited by 39
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Authors: Naranjo, S. E.
Corresponding author: Naranjo, S. E.
ORCID: Naranjo, S. E.
Venue: CABI Reviews
Publisher: CABI Publishing
Published: 2009-06-10
Pages: 1-11
ISSN: 1749-8848 (ISSN-L)
DOI: 10.1079/pavsnnr20094011
OpenAlex: W2171756104
Cited by: 252
References: 239
Citations by year: 2026: 3 · 2025: 6 · 2024: 3 · 2023: 2 · 2022: 9 · 2021: 10 · 2020: 11 · 2019: 7 · 2018: 17 · 2017: 14 · 2016: 15 · 2015: 17 · 2014: 33 · 2013: 25 · 2012: 30
FWCI: 10.56
Type: journal article
Language: en
Open access: closed
Locations: CABI Reviews (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
Life Sciences › Agricultural and Biological Sciences › Plant Science › Genetically Modified Organisms Research
Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
Keywords: Bt crops, Bacillus thuringiensis, non-target invertebrates, insecticide reduction, Bt maize, Bt cotton, genetically modified crops, environmental safety, insecticidal proteins, pest suppression, non-target effects

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Impacts of Bt crops on non-target invertebrates and insecticide use patterns.

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