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

Naranjo, S. E.

doi:10.1079/pavsnnr20094011

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

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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Canopy- and Ground-Dwelling Predatory Arthropods in Commercial Bt and non-Bt Cotton Fields: Patterns and Mechanisms
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Detectability of Coleopteran-specific Cry3Bb1 Protein in Soil and Its Effect on Nontarget Surface and Below-Ground Arthropods
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IMPROVING RISK ASSESSMENT FOR NONTARGET SAFETY OF TRANSGENIC CROPS
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Effects of Activated Bt Transgene Products (Cry1Ab, Cry3Bb) on Immature Stages of the Ladybird Adalia bipunctata in Laboratory Ecotoxicity Testing
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Impact of Cry3A-Intoxicated Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) and Pollen on Consumption, Development, and Fecundity of Coleomegilla maculata (Coleoptera: Coccinellidae)
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Field decomposition of transgenic Bt maize residue and the impact on non-target soil invertebrates
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Transgenic Bt maize and Rhopalosiphum padi (Hom., Aphididae) performance
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Impact of Bt cotton adoption on pesticide use by smallholders: A 2-year survey in Makhatini Flats (South Africa)
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Effects of Novel Pesticides on Bumble Bee (Hymenoptera: Apidae) Colony Health and Foraging Ability
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Field and Laboratory Evaluations of Transgenic Bacillus thuringiensis Corn on Secondary Lepidopteran Pests (Lepidoptera: Noctuidae)
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Tritrophic Choice Experiments with Bt Plants, the Diamondback Moth (Plutella xylostella) and the parasitoid Cotesia plutellae
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Biological Parameters of Convergent Lady Beetle (Coleoptera: Coccinellidae) Feeding on Aphids (Homoptera: Aphididae) on Transgenic Potato
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Effect ofBt-toxin (Cry1Ac) in Transgenic Cotton on the Adult Longevity of Four Heteropteran Predators
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Transmission ofBtToxin to the PredatorPropylaea japonica(Coleoptera: Coccinellidae) Through Its Aphid Prey Feeding on TransgenicBtCotton
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Can Bacillus thuringiensis (Bt) corn residues and Bt-corn plants affect life-history traits in the earthworm Aporrectodea caliginosa?
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Al-Deeb, M. A., Wilde, G. E., & Higgins, R. A. (2001) · Environmental Entomology · doi:10.1603/0046-225x-30.3.625 · Cited by 74 · see citing works
Effects of Bt corn pollen on honey bees: emphasis on protocol development
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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 72 · see citing works
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 72 · see citing works
Effects of Bt corn on Rhopalosiphum padi L. (Rhynchota Aphididae) and on its predator Chrysoperla carnea Stephen (Neuroptera Chrysopidae)
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Consumption of Bt Maize Pollen Expressing Cry1Ab or Cry3Bb1 Does Not Harm Adult Green Lacewings, Chrysoperla carnea (Neuroptera: Chrysopidae)
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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)
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Effect of Bt Corn Expressing the Cry3Bb1 Toxin for Corn Rootworm Control on Aboveground Nontarget Arthropods
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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 · see citing works
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 · see citing works
The effects of pollen consumption of transgenic Bt maize on the common swallowtail, Papilio machaon L. (Lepidoptera, Papilionidae)
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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 · see citing works
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 67 · see citing works
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 · see citing works
Bt Transgenic Crops: Risks and Benefits
Cannon, R. J. C. (2000) · Integrated Pest Management Reviews · doi:10.1023/a:1011347122894 · Cited by 65 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Effects of Cry1Ab Toxin onPropylea japonica(Thunberg) (Coleoptera: Coccinellidae) Through Its Prey,Nilaparvata lugensStål (Homoptera: Delphacidae), Feeding on TransgenicBtRice
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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 · see citing works
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 · see citing works
Effects of natural enemies on relative fitness of Heliothis virescens genotypes adapted and not adapted to resistant host plants
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Effects of Bt maize-fed prey on the generalist predator Poecilus cupreus L. (Coleoptera: Carabidae)
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The influence of pesticide applications on Helicoverpa armigera Hübner and sucking pests in transgenic Bt cotton and non-transgenic cotton in China
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Effects of Bt-corn decomposition on the composition of the soil meso- and macrofauna
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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
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Effects of Insecticide-Treated and Lepidopteran-Active Bt Transgenic Sweet Corn on the Abundance and Diversity of Arthropods
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Subacute Effects of Cry1AbBtCorn Litter on the EarthwormEisenia fetidaand the SpringtailFolsomia candida
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Bitrophic and tritrophic effects of Bt Cry3A transgenic potato on beneficial, non-target, beetles
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Bt-maize effects on biological parameters of the non-target aphid Sitobion avenae (Homoptera: Aphididae) and Cry1Ab toxin detection
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Impacts of Developing on Bt Maize-Intoxicated Hosts on Fitness Parameters of a Stem Borer Parasitoid
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Consumption of two Bt and six non-Bt corn varieties by the woodlouse Porcellio scaber
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Field Assessment of the Effects of Transgenic Rice Expressing a Fused Gene ofcry1Abandcry1AcfromBacillus thuringiensisBerliner on Nontarget Planthopper and Leafhopper Populations
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Bt maize pollen exposure and impact on the garden spider, Araneus diadematus
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Effect ofBacillus thuringiensisTransgenic Corn for Lepidopteran Control on Nontarget Arthropods
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Predaceous Arthropods and Lepidopteran Pests on Conventional, Bollgard, and Bollgard Ii Cotton Under Untreated and Disrupted Conditions
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Insect-Resistant Transgenic Crops and Biological Control
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Larval Feeding on Bt Hybrid and Non-Bt Corn Seedlings by Harmonia axyridis (Coleoptera: Coccinellidae) and Coleomegilla maculata (Coleoptera: Coccinellidae)
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Tritrophic Interactions Among Bt (Cry3Bb1) Corn, Aphid Prey, and the Predator Coleomegilla maculata (Coleoptera: Coccinellidae)
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Effects of Cry1Ab-Expressing Corn Anthers on Monarch Butterfly Larvae
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Utility of Ground Beetle Species in Field Tests of Potential Nontarget Effects of Bt Crops
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The Present and Future Role of Insect-Resistant Genetically Modified Potato Cultivars in IPM
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Assessing the Effects of Bt Maize on the Predatory Mite Neoseiulus cucumeris
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Impact of insecticidal proteins expressed in transgenic plants on bumblebee microcolonies
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Biodiversity and Community Structure of Epedaphic and Euedaphic Springtails (Collembola) in Transgenic Rootworm Bt Corn
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Arthropod Abundance and Diversity in Bt and Non-Bt Rice Fields
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Effects of the Cry1Ac toxin of Bacillus thuringiensis on Microplitis mediator, a parasitoid of the cotton bollworm, Helicoverpa armigera
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Comparing methods to evaluate the effects of Bt maize and insecticide on spider assemblages
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Target and non-target effects on the invertebrate community of Vip cotton, a new insecticidal transgenic
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Dusky Sap Beetles (Coleoptera: Nitidulidae) and Other Kernel Damaging Insects in Bt and Non-Bt Sweet Corn in Illinois
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Impacts of Bacillus thuringiensis toxins on parasitoids (Hymenoptera: Braconidae) of Spodoptera litura and Helicoverpa armigera (Lepidoptera: Noctuidae)
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Effect of corn hybrids expressing the coleopteran-specific Cry3Bb1 protein for corn rootworm control on aboveground insect predators
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Recombinant and classically selected factors of potato plant resistance to the Colorado potato beetle, Leptinotarsa decemlineata, variously affect the potato aphid parasitoid Aphidius nigripes
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Interactions of Bt-cotton and the omnivorous big-eyed bug Geocoris punctipes (Say), a key predator in cotton fields
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Early instar response to plant-delivered Bt-toxin in a herbivore (Spodoptera litura) and a predator (Propylaea japonica)
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Abundance and diversity of ground‐dwelling arthropods of pest management importance in commercial Bt and non‐Bt cotton fields
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Longevity of phytophagous heteropteran predators feeding on transgenic Btt‐potato plants
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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 · see citing works
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 · see citing works
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 · see citing works
Assessing the Risk to Nontarget Organisms from Bt Corn Resistant to Corn Rootworms (Coleoptera: Chrysomelidae): Tier-I Testing with Orius insidiosus (Heteroptera: Anthocoridae)
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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 38 · see citing works
Physiologically based demographics of Bt cotton–pest interactions
Gutierrez, A. P., Adamczyk, J. J., Ponsard, S., & Ellis, C. K. (2005) · Ecological Modelling · doi:10.1016/j.ecolmodel.2005.06.002 · Cited by 37 · see citing works
Short-term assessment of Bt maize on non-target arthropods in Brazil
Fernandes, O. A., Faria, M., Martinelli, S., Schmidt, F., Carvalho, V. F., & Moro, G. (2007) · Scientia Agricola · doi:10.1590/s0103-90162007000300006 · Cited by 37 · see citing works
Effects of Bt transgenic cotton lines on the cotton bollworm parasitoid Microplitis mediator in the laboratory
Liu, X., Zhang, Q., Zhao, Y., Li, J., Xu, B., & Xiaomu, M. (2005) · Biological Control · doi:10.1016/j.biocontrol.2005.08.006 · Cited by 37 · see citing works
A 3-year field-scale monitoring of foliage-dwelling spiders (Araneae) in transgenic Bt maize fields and adjacent field margins
Ludy, C., & Lang, A. (2006) · Biological Control · doi:10.1016/j.biocontrol.2006.05.010 · Cited by 37 · see citing works
Ecological impact of Bt-transgenic plants [Bacillus thuringiensis]. 1: Assessing possible effects of CryIIIB toxin on honey bee (Apis mellifera L.) colonies
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Prey-mediated effects of transgenic canola on a beneficial, non-target, carabid beetle
Ferry, N., Mulligan, E. A., Stewart, C. N., Tabashnik, B. E., Port, G. R., & Gatehouse, A. M. R. (2006) · Transgenic Research · doi:10.1007/s11248-006-0021-4 · Cited by 35 · see citing works
Long-Term Assessment of the Effects of TransgenicBtCotton on the Function of the Natural Enemy Community
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The economics of biotechnology under ecosystem disruption
Pemsl, D. E., Gutierrez, A. P., & Waibel, H. (2007) · Ecological Economics · doi:10.1016/j.ecolecon.2007.08.022 · Cited by 34 · see citing works
Effects on Fitness and Behavior of Monarch Butterfly Larvae Exposed to a Combination ofCry1Ab-Expressing Corn Anthers and Pollen
Anderson, P. L., Hellmich, R. L., Prasifka, J. R., & Lewis, L. C. (2005) · Environmental Entomology · doi:10.1603/0046-225x-34.4.944 · Cited by 33 · see citing works
Spring aphid-parasitoid (Hom., Aphididae, Hym., Braconidae) associations and interactions in a Mediterranean arable crop ecosystem, including Bt maize
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Transgenic Resistance to the Colorado Potato Beetle in Bt-expressing Eggplant Fields
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Effects of Bt on Non-Target Organisms
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Effects of Bacillus thuringiensisδδ‐endotoxins on food utilization, growth, and survival of selected phytophagous insects
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Economic and Social Considerations in the Adoption of Bt Crops
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Hierarchical classification of environmental factors and agricultural practices affecting soil fauna under cropping systems using Bt maize
Debeljak, M., Cortet, J., Demšar, D., Krogh, P. H., & Džeroski, S. (2007) · Pedobiologia · doi:10.1016/j.pedobi.2007.04.009 · Cited by 30 · see citing works
Effects of transgenic Cry1A+CpTI cotton and Cry1Ac toxin on the parasitoid, Campoketis chlorideae (Hymenoptera: Ichneumonidae)
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Season-Long Abundance of Generalist Predators in Transgenic versus Nontransgenic Potato Fields2
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The Impacts of the Pollen of Insect-resistant Transgenic Cotton on Honeybees
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Response of Danaus plexippus to pollen of two new Bt corn events via laboratory bioassay
Mattila, H. R., Sears, M. K., & Duan, J. J. (2005) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2005.00304.x · Cited by 28 · see citing works
Field Evaluation of the Impact of Corn Rootworm (Coleoptera: Chrysomelidae)–ProtectedBtCorn on Foliage-Dwelling Arthropods
Bhatti, M. A., Duan, J., Head, G. P., Jiang, C., McKee, M. J., Nickson, T. E., Pilcher, C. L., & Pilcher, C. D. (2005) · Environmental Entomology · doi:10.1093/ee/34.5.1336 · Cited by 28 · see citing works
Bales and Balance: A Review of the Methods Used to Assess the Economic Impact of Bt Cotton on Farmers in Developing Economies
Smale, M., Zambrano, P., & Cartel, M. A. (2006) · CGSPace A Repository of Agricultural Research Outputs (Consultative Group for International Agricultural Research) · Cited by 28 · see citing works
Evaluation of Effects of Coleopteran-Specific Cry3Bb1 Protein on Earthworms Exposed to Soil Containing Corn Roots or Biomass
Ahmad, A., Wilde, G. E., & Zhu, K. Y. (2006) · Environmental Entomology · doi:10.1603/0046-225x-35.4.976 · Cited by 27 · see citing works

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Large-Scale Deployment of Seed Treatments Has Driven Rapid Increase in Use of Neonicotinoid Insecticides and Preemptive Pest Management in U.S. Field Crops
Douglas, M. R., & Tooker, J. F. (2015) · Environmental Science & Technology · doi:10.1021/es506141g · Cited by 531 · see citing works
Evolutionary ecology of insect adaptation to Bt crops
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Insect-Resistant Genetically Modified Rice in China: From Research to Commercialization
Chen, M., Shelton, A. M., & Yè, G. (2010) · Annual Review of Entomology · doi:10.1146/annurev-ento-120709-144810 · Cited by 290 · see citing works
Genetically engineered crops help support conservation biological control
Romeis, J., Naranjo, S. E., Meissle, M., & Shelton, A. M. (2019) · Biological Control · doi:10.1016/j.biocontrol.2018.10.001 · Cited by 231 · see citing works
“Results mirror those found in prior meta-analyses with fewer studies (Naranjo, 2009) in showing that a variety of Bt plants and Cry proteins have no negative effects on a broad range of natural enemy species when the non-target species were exposed in an ecologically realistic manner (Fig.”
BackgroundResultInfluentialSelf-citation
Recommendations for the design of laboratory studies on non-target arthropods for risk assessment of genetically engineered plants
Romeis, J., Hellmich, R. L., Candolfi, M. P., Carstens, K., de Schrijver, A., Gatehouse, A. M. R., Herman, R. A., Huesing, J. E., McLean, M. A., Raybould, A. F., et al. (2010) · Transgenic Research · doi:10.1007/s11248-010-9446-x · Cited by 232 · see citing works
The food and environmental safety of Bt crops
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Conservation biological control using selective insecticides – A valuable tool for IPM
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Impact of genetically engineered maize on agronomic, environmental and toxicological traits: a meta-analysis of 21 years of field data
Pellegrino, E., Bedini, S., Nuti, M., & Ercoli, L. (2018) · Scientific Reports · doi:10.1038/s41598-018-21284-2 · Cited by 177 · see citing works
RNAi-Based Insecticidal Crops: Potential Effects on Nontarget Species
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Bacterial Entomopathogens
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No effects of Bacillus thuringiensis maize on nontarget organisms in the field in southern Europe: a meta-analysis of 26 arthropod taxa
Comas, C., Lumbierres, B., Pons, X., & Albajes, R. (2014) · Transgenic Research · doi:10.1007/s11248-013-9737-0 · Cited by 129 · see citing works
Extrapolating non-target risk of Bt crops from laboratory to field
Duan, J. J., Lundgren, J. G., Naranjo, S., & Marvier, M. (2010) · Biology Letters · doi:10.1098/rsbl.2009.0612 · Cited by 127 · see citing works
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Deriving criteria to select arthropod species for laboratory tests to assess the ecological risks from cultivating arthropod-resistant genetically engineered crops
Romeis, J., Raybould, A. F., Bigler, F., Candolfi, M. P., Hellmich, R. L., Huesing, J. E., & Shelton, A. M. (2012) · Chemosphere · doi:10.1016/j.chemosphere.2012.09.035 · Cited by 119 · see citing works
Microbial biopesticides: opportunities and challenges.
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Recombinant protease inhibitors for herbivore pest control: a multitrophic perspective
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Application of pyramided traits against Lepidoptera in insect resistance management forBtcrops
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Meta-analysis reveals that seed-applied neonicotinoids and pyrethroids have similar negative effects on abundance of arthropod natural enemies
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Risk Assessment and Ecological Effects of Transgenic Bacillus thuringiensis Crops on Non‐Target Organisms F
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Laboratory toxicity studies demonstrate no adverse effects of Cry1Ab and Cry3Bb1 to larvae of Adalia bipunctata (Coleoptera: Coccinellidae): the importance of study design
Álvarez‐Alfageme, F., Bigler, F., & Romeis, J. (2010) · Transgenic Research · doi:10.1007/s11248-010-9430-5 · Cited by 104 · see citing works
The web‐building spider Theridion impressum (Araneae: Theridiidae) is not adversely affected by Bt maize resistant to corn rootworms
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Philosophy and the Precautionary Principle: Science, Evidence, and Environmental Policy
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Biological control of cotton pests in China
Luo, S., Naranjo, S. E., & Wu, K. (2013) · Biological Control · doi:10.1016/j.biocontrol.2013.06.004 · Cited by 83 · see citing works
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Is the German suspension of MON810 maize cultivation scientifically justified?
Ricroch, A., Bergé, J. B., & Kuntz, M. (2010) · Transgenic Research · doi:10.1007/s11248-009-9297-5 · Cited by 80 · see citing works
Natural Enemies Delay Insect Resistance to Bt Crops
Liu, X., Chen, M., Collins, H. L., Onstad, D. W., Roush, R. T., Zhang, Q., Earle, E. D., & Shelton, A. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090366 · Cited by 79 · see citing works
The impact of secondary pests on Bacillus thuringiensis (Bt) crops
Catarino, R., Ceddia, G., Areal, F., & Park, J. R. (2015) · Plant Biotechnology Journal · doi:10.1111/pbi.12363 · Cited by 76 · see citing works
When bad science makes good headlines: Bt maize and regulatory bans
Romeis, J., McLean, M. A., & Shelton, A. M. (2013) · Nature Biotechnology · doi:10.1038/nbt.2578 · Cited by 74 · see citing works
Setting the record straight: a rebuttal to an erroneous analysis on transgenic insecticidal crops and natural enemies
Shelton, A. M., Naranjo, S. E., Romeis, J., Hellmich, R. L., Wolt, J. D., Federici, B. A., Albajes, R., Bigler, F., Burgess, E. P. J., Dively, G. P., et al. (2009) · Transgenic Research · doi:10.1007/s11248-009-9260-5 · Cited by 73 · see citing works
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A synthesis of laboratory and field studies on the effects of transgenic Bacillus thuringiensis (Bt) maize on non‐target Lepidoptera
Lang, A., & Otto, M. (2010) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2010.00981.x · Cited by 73 · see citing works
Non-target organism effects tests on Vip3A and their application to the ecological risk assessment for cultivation of MIR162 maize
Raybould, A. F., & Vlachos, D. (2010) · Transgenic Research · doi:10.1007/s11248-010-9442-1 · Cited by 72 · see citing works
Characterizing indirect prey-quality mediated effects of a Bt crop on predatory larvae of the green lacewing, Chrysoperla carnea
Lawo, N. C., Wäckers, F. L., & Romeis, J. (2010) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2010.06.012 · Cited by 66 · see citing works
Textile Finishing Industry as an Important Source of Organic Pollutants
Maréchal, A. M. L., Krianec, B., Vajnhandl, S., & Volmajer, J. (2012) · InTech eBooks · doi:10.5772/32272 · Cited by 65 · see citing works
Influence of transgenic hybrid rice expressing a fused gene derived from cry1Ab and cry1Ac on primary insect pests and rice yield
Wang, Y., Zhang, G., Du, J., Liu, B., & Wang, M. (2009) · Crop Protection · doi:10.1016/j.cropro.2009.10.004 · Cited by 64 · see citing works
Assessing environmental impacts of genetically modified plants on non-target organisms: the relevance of in planta studies
Arpaia, S., Birch, A. N. E., Kiss, J., van Loon, J. J. A., Messéan, A., Nuti, M., Perry, J. N., Sweet, J. B., & Tebbe, C. C. (2017) · Science of The Total Environment · doi:10.1016/j.scitotenv.2017.01.039 · Cited by 62 · see citing works
A Review on Impacts of Genetically Modified Food on Human Health
Verma, C. (2011) · The Open Nutraceuticals Journal · doi:10.2174/1876396001104010003 · Cited by 63 · see citing works
The potential impact of plant biotechnology on the Millennium Development Goals
Yuan, D., Bassié, L., Sabalza, M., Miralpeix, B., Dashevskaya, S., Farré, G., Rivera, S. M., Banakar, R., Bai, C., Sanahuja, G., et al. (2011) · Plant Cell Reports · doi:10.1007/s00299-010-0987-5 · Cited by 57 · see citing works
Recent Advances in Entomological Research
Liu, T., & Kang, L. (2011) · Springer eBooks · doi:10.1007/978-3-642-17815-3 · Cited by 79 · see citing works
Bt Crops Producing Cry1Ac, Cry2Ab and Cry1F Do Not Harm the Green Lacewing, Chrysoperla rufilabris
Tian, J., Wang, X., Long, L.-P., Romeis, J., Naranjo, S. E., Hellmich, R. L., Wang, P., Earle, E. D., & Shelton, A. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060125 · Cited by 52 · see citing works
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Multi-State Trials of Bt Sweet Corn Varieties for Control of the Corn Earworm (Lepidoptera: Noctuidae)
Shelton, A. M., Olmstead, D. L., Burkness, E. C., Hutchison, W. D., Dively, G. P., Welty, C., & Sparks, A. N. (2013) · Journal of Economic Entomology · doi:10.1603/ec13146 · Cited by 52 · see citing works
Biotechnological advances in Bacillus thuringiensis and its toxins: Recent updates
Azizoğlu, U., Jouzani, G. S., Sansinenea, E., & Sanchis, V. (2023) · Reviews in Environmental Science and Bio/Technology · doi:10.1007/s11157-023-09652-5 · Cited by 51 · see citing works
Tier‐1 assays for assessing the toxicity of insecticidal proteins produced by genetically engineered plants to non‐target arthropods
Li, Y., Romeis, J., Wu, K., & Peng, Y. (2013) · Insect Science · doi:10.1111/1744-7917.12044 · Cited by 51 · see citing works
Effect of Bt Maize and Soil Insecticides on Yield, Injury, and Rootworm Survival: Implications for Resistance Management
Petzold-Maxwell, J. L., Meinke, L. J., Gray, M. E., Estes, R. E., & Gassmann, A. J. (2013) · Journal of Economic Entomology · doi:10.1603/ec13216 · Cited by 51 · see citing works
Laboratory and Field Assessments of Prey-Mediated Effects of Transgenic Bt Rice on Ummeliata insecticeps (Araneida: Linyphiidae)
Tian, J. C., Liu, Z. C., Chen, M., Chen, Y., Chen, X. X., Peng, Y., Hu, C., & Ye, G. Y. (2010) · Environmental Entomology · doi:10.1603/en10003 · Cited by 51 · see citing works
Effects of field history on resistance to Bt maize by western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae)
Shrestha, R. B., Dunbar, M. W., French, B. W., & Gassmann, A. J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0200156 · Cited by 50 · see citing works
Behavioral effects of insect-resistant genetically modified crops on phytophagous and beneficial arthropods: a review
Han, P., Velasco-Hernández, M. C., Ramírez‐Romero, R., & Desneux, N. (2016) · Journal of Pest Science · doi:10.1007/s10340-016-0791-2 · Cited by 50 · see citing works
Use of a Pollen-Based Diet to Expose the Ladybird Beetle Propylea japonica to Insecticidal Proteins
Zhang, X., Li, Y., Romeis, J., Yin, X., Wu, K., & Peng, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085395 · Cited by 49 · see citing works
Bt-maize event MON 88017 expressing Cry3Bb1 does not cause harm to non-target organisms
Devos, Y., de Schrijver, A., CLERCQ, P. D., Kiss, J. G., & Romeis, J. (2012) · Transgenic Research · doi:10.1007/s11248-012-9617-z · Cited by 46 · see citing works
Bt eggplant (Solanum melongena L.) in Bangladesh: Fruit production and control of eggplant fruit and shoot borer (Leucinodes orbonalis Guenee), effects on non-target arthropods and economic returns
Prodhan, M. Z. H., Hasan, M. T., Chowdhury, M. M. I., Alam, M. S., Rahman, M. L., Azad, A. K., Hossain, M. J., Naranjo, S. E., & Shelton, A. M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0205713 · Cited by 46 · see citing works
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Bt crops and food security in developing countries: realised benefits, sustainable use and lowering barriers to adoption
Raybould, A. F., & Quemada, H. D. (2010) · Food Security · doi:10.1007/s12571-010-0066-3 · Cited by 44 · see citing works
Health effect of agricultural pesticide use in China: implications for the development of GM crops
Zhang, C., Hu, R., Huang, J., Huang, X., Shi, G., Li, Y., Yin, Y., & Chen, Z. (2016) · Scientific Reports · doi:10.1038/srep34918 · Cited by 44 · see citing works
Use of an artificial diet system to study the toxicity of gut-active insecticidal compounds on larvae of the green lacewing Chrysoperla sinica
Li, Y., Hu, L., Romeis, J., Wang, Y., Han, L., Chen, X., & Peng, Y. (2013) · Biological Control · doi:10.1016/j.biocontrol.2013.10.017 · Cited by 43 · see citing works
Interactions of transgenic Bacillus thuringiensis insecticidal crops with spiders (Araneae)
Peterson, J. A., Lundgren, J. G., & Harwood, J. D. (2011) · Journal of Arachnology · doi:10.1636/m10-98.1 · Cited by 43 · see citing works
Bt crops benefit natural enemies to control non-target pests
Tian, J.-C., Yao, J., Long, L.-P., Romeis, J., & Shelton, A. M. (2015) · Scientific Reports · doi:10.1038/srep16636 · Cited by 41 · see citing works
Interactions between Bt crops and aquatic ecosystems: A review
Venter, H. J., & Bøhn, T. (2016) · Environmental Toxicology and Chemistry · doi:10.1002/etc.3583 · Cited by 41 · see citing works
Transportable data from non-target arthropod field studies for the environmental risk assessment of genetically modified maize expressing an insecticidal double-stranded RNA
Ahmad, A., Negri, I., de Oliveira, W. S., Brown, C., Asiimwe, P., Sammons, B., Horak, M. J., Jiang, C., & Carson, D. B. (2015) · Transgenic Research · doi:10.1007/s11248-015-9907-3 · Cited by 41 · see citing works
Bt rice producing Cry1C protein does not have direct detrimental effects on the green lacewing Chrysoperla sinica (Tjeder)
Li, Y., Chen, X., Hu, L., Romeis, J., & Peng, Y. (2014) · Environmental Toxicology and Chemistry · doi:10.1002/etc.2567 · Cited by 40 · see citing works
Impact of Lepidoptera (Crambidae, Noctuidae, and Pyralidae) Pests on Corn Containing Pyramided Bt Traits and a Blended Refuge in the Southern United States
Reay‐Jones, F. P. F., Bessin, R. T., Brewer, M. J., Buntin, D. G., Catchot, A. L., Cook, D. R., Flanders, K. L., Kerns, D. L., Porter, R. P., Reisig, D. D., et al. (2016) · Journal of Economic Entomology · doi:10.1093/jee/tow109 · Cited by 40 · see citing works
Short-term effects of different genetically modified maize varieties on arthropod food web properties: an experimental field assessment
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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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