The DOI matches its Crossref record; 237 of the 239 references it cites were found in a registry or an index.
Impacts of Bt crops on non-target invertebrates and insecticide use patterns.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Citations
Cites
Wasserman, S. S., Hedges, L. V., & Olkin, I. (1988) · Journal of Educational Statistics · doi:10.2307/1164953 · Cited by 10,377
Transgenic pollen harms monarch larvae
Losey, J. E., Rayor, L. S., & Carter, M. E. (1999) · Nature · doi:10.1038/20338 · Cited by 1,171
Economic, Ecological, Food Safety, and Social Consequences of the Deployment of Bt Transgenic Plants
Shelton, A. M., Zhao, J.-Z., & Roush, R. T. (2002) · Annual Review of Entomology · doi:10.1146/annurev.ento.47.091201.145309 · Cited by 794
Yield effects of genetically modified crops in developing countries
Qaim, M., & Zilberman, D. (2003) · Science · doi:10.1126/science.1080609 · Cited by 757
Transgenic crops expressing Bacillus thuringiensis toxins and biological control
Romeis, J., Meissle, M., & Bigler, F. (2006) · Nature Biotechnology · doi:10.1038/nbt1180 · Cited by 719
The release of genetically modified crops into the environment
Conner, A. J., Glare, T. R., & Nap, J. (2003) · The Plant Journal · doi:10.1046/j.0960-7412.2002.001607.x · Cited by 606
The Ecological Risks and Benefits of Genetically Engineered Plants
Wolfenbarger, L. L., & Phifer, P. (2000) · Science · doi:10.1126/science.290.5499.2088 · Cited by 575
Bacillus thuringiensis : Biology, Ecology and Safety
Glare, T. R., & O’Callaghan, M. (2000) · Cited by 556
Omnivory in Terrestrial Arthropods: Mixing Plant and Prey Diets
Coll, M., & Guershon, M. (2002) · Annual Review of Entomology · doi:10.1146/annurev.ento.47.091201.145209 · Cited by 544
Carlini, C. R., & Grossi‐de‐Sá, M. F. (2002) · Toxicon · doi:10.1016/s0041-0101(02)00240-4 · Cited by 543
Cited by
Sorted by citations
Items 201–251 of 251
Diversity of arthropods communities in transgenic cotton varieties in Santa Fe province, Argentina
Sosa, M. A., & Almada, M. S. (2014) · Americanae (AECID Library) · Cited by 3
The Effects of Transgenic Crops on Non-target Organisms
Emani, C. (2014) · Sustainable development and biodiversity · doi:10.1007/978-3-319-09381-9_4 · Cited by 4
Integrated Pest Management, Bt Crops, and Insecticide Use: The U.S. Experience
Frisvold, G. B., & Reeves, J. M. (2014) · Springer eBooks · doi:10.1007/978-94-007-7802-3_2 · Cited by 3
Errors in Logic and Statistics Plague a Meta-Analysis (response to Andow and Lövei 2012): Table 1.
Shelton, A. M., Naranjo, S. E., Romeis, J., & Hellmich, R. L. (2012) · Environmental Entomology · doi:10.1603/en11238a · Cited by 3
Self-citationGautam, B. K. (2014) · Sociobiology · doi:10.13102/sociobiology.v59i4.505 · Cited by 3
Yang, F., Liu, B. Y., Zhu, Y., Desneux, N., Liu, L., Li, C., Wyckhuys, K. A. G., & Lu, Y. (2021) · Pest Management Science · doi:10.1002/ps.6627 · Cited by 2
An Assessment of Environmental Risk of Bt-Maize on Rove Beetle Communities
Twardowski, J. P., Gruss, I., Bereś, P. K., HUREJ, M., & Klukowski, Z. (2022) · Ecological Chemistry and Engineering S · doi:10.2478/eces-2022-0019 · Cited by 2
Influence of Bt Maize on Diversity and Composition of Non-target Arthropod Species
de Sousa, M. F., Fernandes, M. G., & Guimarães, A. J. D. S. (2019) · Journal of Agricultural Science · doi:10.5539/jas.v11n2p201 · Cited by 2
Knox, O. G. G., Hall, C., McVittie, A., Walker, R. L., & Knight, B. (2013) · Food and Nutrition Sciences · doi:10.4236/fns.2013.46a004 · Cited by 2
ARTHROPODS BIODIvERSITY INDEx IN BOllgARD ® COTTON (Cry1Ac) IN BRAzIl
Thomazoni, D., Soria, M. F., Degrande, P. E., Faccenda, O., & Silvie, P. J. (2013) · Agritrop (Cirad) · Cited by 2
Santana‐Espinoza, S., Ávila-Rodríguez, V., Gaytán, G. C., de la Cruz-Lázaro, E., la Peña, C. G.-D., Romero-Méndez, U., & Márquez-Hernández, C. (2015) · Southwestern Entomologist · doi:10.3958/059.040.0113 · Cited by 2
Sharma, H. C., & Dhillon, M. K. (2018) · The Indian Journal of Agricultural Sciences · doi:10.56093/ijas.v88i6.80542 · Cited by 2
Lee, M. S., Ardanuy, A., Juárez‐Escario, A., & Albajes, R. (2021) · Ecological Indicators · doi:10.1016/j.ecolind.2021.107380 · Cited by 2
Midgut — Transgenic Crops Expressing Bacillus thuringiensis Cry Proteins
Rie, J. V., & Jansens, S. (2007) · Wiley eBooks · doi:10.1002/9783527619580.ch27 · Cited by 2
Arthropods dataset from different genetically modified maize events and associated controls
Pálinkás, Z., Zalai, M., Szénási, Á., Dorner, Z., Kiss, J. G., North, S. M., Woodward, G., & Balog, A. (2018) · Scientific Data · doi:10.1038/sdata.2018.19 · Cited by 2
Archibald, W. R., Stowe, H. E., Collins, R., Daniel, S. R., Wright, R., & Peterson, J. A. (2025) · Entomologia Experimentalis et Applicata · doi:10.1111/eea.70004 · Cited by 1
Cruz, J. C., Mampuys, R., Reyes, G., & Dryhurst, S. (2026) · NATO science for peace and security series. A, Chemistry and biology · doi:10.1007/978-3-032-05246-9_7 · Cited by 1
Pal, R., & Prasad, C. S. (2015) · Indian Farming · Cited by 1
Gadaleta, P. G. (2020) · Topics in biodiversity and conservation · doi:10.1007/978-3-030-53183-6_15 · Cited by 2
Errors in Logic and Statistics Plague a Meta-Analysis (Response to Andow and Lövei 2012)
Shelton, A. M., Naranjo, S. E., Romeis, J., & Hellmich, R. L. (2012) · Environmental Entomology · doi:10.1603/022.041.0502 · Cited by 1
Self-citationLandscape Considerations in Pest Management: Case Study of the Arizona Cotton IPM System
Naranjo, S. E., & Ellsworth, P. C. (2024) · CABI eBooks · doi:10.1079/97818006227777.0003 · Cited by 6
Self-citationAreal, F., Dunwell, J. M., Jones, P., Park, J. R., MCFARLANE, I. D., Srinivasan, C. S., & Tranter, R. (2015) · Cited by 1
Grabowski, M., Lipska, A., Żmijewska, E., Kozák, M., & Dąbrowski, Z. T. (2014) · Egyptian Journal of Biological Pest Control · Cited by 1
GM Crop Risk Debate, Science and Socioeconomics
Ammann, K. (2013) · Springer eBooks · doi:10.1007/978-1-4614-5797-8_130 · Cited by 1
Midgut‐Transgenic Crops ExpressingBacillus thuringiensisCry Proteins
Rie, J. V., & Jansens, S. (2019) · Wiley eBooks · doi:10.1002/9783527699261.ch31 · Cited by 1
Laserna, M. P. (2012) · Repositorio Digital Institucional de la Universidad de Buenos Aires (Universidad de Buenos Aires)
Genetically Modified Organisms for Pest Management: Environmental Impact
Dhillon, M. K., & Sharma, H. C. (2012) · Open Access Repository of ICRISAT (International Crops Research Institute for the Semi-Arid Tropics)
Time for a New Look at the Relationship Between Bt Plants and Insect Natural Enemies
Chen, M., & Shelton, A. M. (2011) · Springer eBooks · doi:10.1007/978-3-642-17815-3_16
Current outline of regulation of Bt‐maize and transgenic insects in Mexico
Rodríguez-Pérez, M. A., & Real-Najarro, O. (2010) · Entomological Research · doi:10.1111/j.1748-5967.2009.00257.x
Reply to Science-based risk assessment requires careful evaluation of all studies
Romeis, J., McLean, M. A., & Shelton, A. M. (2013) · Nature Biotechnology · doi:10.1038/nbt.2762
HUREJ, M., Miętkiewski, R., & Twardowski, J. P. (2014) · Zemdirbyste-Agriculture · doi:10.13080/z-a.2014.101.036
6. EFFECT OF ERP SOFTWARE ON PERFORMANCE OF INDUSTRIES IN SME SECTOR
Aneja, N., Economy, F. I., Sharma, V. K., Kumar, N., Kannan, M., Byahatti, P., Faisal, U., & Khan, A. A. (2015) · International journal of research in commerce, economics and management
Biotechnological interventions for crop improvement in the context of food security
Yuan, D. (2012) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas)
Bacillus thuringiensis: Transgenic Crops
Peterson, J. A., Obrycki, J. J., & Harwood, J. D. (2013) · doi:10.1081/e-eem-120046904
What is environmentally acceptable plant protection
Shelton, A. M. (2015)
Bt corn and Bt cotton: Valuable tools for IPM
Hamel, W., Werts, P., & Green, T. (2017) · Crops & Soils · doi:10.2134/cs2017.50.0606
Marques, L. H. D. S. F. (2018) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.59.2018.tde-19022018-001516
Álvarez‐Alfageme, F., Devos, Y., Guajardo, I. M., Li, Y., Romeis, J., & Meissle, M. (2019) · Environmental Evidence · doi:10.1186/s13750-019-0169-z
Aguirre, L. A., Juárez, A. H., Cerna, E., Flores, M., Frías, G. A., & Fuentes, Y. M. O. (2021) · Journal of Entomological Science · doi:10.18474/jes20-84
Midgut–Transgenic Crops ExpressingBacillus thuringiensisCry Proteins
Rie, J. V., & Jansens, S. (2011) · Wiley eBooks · doi:10.1002/9783527644179.ch30
(2012) · Environmental Entomology · doi:10.1603/022.041.0501
RetractedPlant Breeding for Tolerance to Biotic Stressors Including Nematodes, Diseases, and Insect Pests
Bozbuğa, R., Kara, P. A., Yıldız, H. N., Güler, P. G., Erol, Ü. H., Özgören, B., Kahya, D., & Arpacı, B. B. (2025) · IntechOpen eBooks · doi:10.5772/intechopen.1011650
Meissle, M., Naranjo, S. E., & Romeis, J. (2022) · Figshare · doi:10.6084/m9.figshare.20004740
Self-citationMeissle, M., Naranjo, S. E., & Romeis, J. (2022) · Figshare · doi:10.6084/m9.figshare.20004737
Self-citationMeissle, M., Naranjo, S. E., & Romeis, J. (2022) · Figshare · doi:10.6084/m9.figshare.20004743
Self-citationMeissle, M., Naranjo, S. E., & Romeis, J. (2022) · Figshare · doi:10.6084/m9.figshare.20004734
Self-citationMeissle, M., Naranjo, S. E., & Romeis, J. (2022) · Figshare · doi:10.6084/m9.figshare.20004752
Self-citationJang, Y.-J., Oh, S., Kim, D., Kim, Y.-K., Lee, S.-K., Chang, A., Sun, H.-J., Lee, H.-Y., & Suh, S. J. (2026) · GM crops & food · doi:10.1080/21645698.2026.2704431
Farhan, Y., Ruttink, T., Abdelgaffar, H., Tandy, P., Lamour, K., Smith, J. L., & Jurat‐Fuentes, J. L. (2026) · Journal of Economic Entomology · doi:10.1093/jee/toag248
Metadata
- 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)
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review