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.
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Items 201–237 of 237
Ahmad, A., Wilde, G. E., & Zhu, K. Y. (2006) · Environmental Entomology · doi:10.1603/0046-225x-35.4.976 · Cited by 26
Zhang, G., Wan, F., Murphy, S. T., Guo, J., & Liu, W. (2008) · Environmental Entomology · doi:10.1603/0046-225x(2008)37[1035:rbotni]2.0.co;2 · Cited by 26
Evaluation of Bt oilseed rape on the non‐target herbivore Athalia rosae
Howald, R., Zwahlen, C., & Nentwig, W. (2003) · Entomologia Experimentalis et Applicata · doi:10.1046/j.1570-7458.2003.00012.x · Cited by 25
Effects of transgenic Bt corn pollen on a non-target lycaenid butterfly, Pseudozizeeria maha
Shirai, Y., & Takahashi, M. (2005) · Applied Entomology and Zoology · doi:10.1303/aez.2005.151 · Cited by 25
Geng, J.-H., Shen, Z., Song, K., & Zheng, L. (2006) · Environmental Entomology · doi:10.1603/0046-225x(2006)35[1661:eoporc]2.0.co;2 · Cited by 25
González-Zamora, J. E., Camúñez, S., & Avilla, C. (2007) · Environmental Entomology · doi:10.1603/0046-225x(2007)36[1246:eobtct]2.0.co;2 · Cited by 24
Chen, M., Zhao, Y., Shelton, A. M., Cao, J. W., & Earle, E. D. (2007) · Transgenic Research · doi:10.1007/s11248-007-9127-6 · Cited by 23
Hoheisel, G., & Fleischer, S. J. (2007) · Journal of Insect Science · doi:10.1673/031.007.6101 · Cited by 22
TRANSGENIC CROPS EXPRESSING Bt PROTEINS: CURRENT STATUS, CHALLENGES AND OUTLOOK
(2004) · CRC Press eBooks · doi:10.1201/9781482294378-4 · Cited by 21
Tschenn, J., Losey, J. E., Jesse, L. C. H., Obrycki, J. J., & Hufbauer, R. A. (2001) · Environmental Entomology · doi:10.1603/0046-225x-30.3.495 · Cited by 21
Zhang, S. ‐., Li, D. ‐., Cui, J., & Xie, B. ‐. (2006) · Journal of Applied Entomology · doi:10.1111/j.1439-0418.2006.01049.x · Cited by 20
Impact of Bt corn on the diplopod Allajulus latestriatus
Weber, M., & Nentwig, W. (2006) · Pedobiologia · doi:10.1016/j.pedobi.2006.06.004 · Cited by 19
Studying the effect of exposure of the snail Helix aspersa to the purified Bt toxin, Cry1Ab
Kramarz, P. E., de Vaufleury, A., & Carey, M. P. (2007) · Applied Soil Ecology · doi:10.1016/j.apsoil.2007.06.006 · Cited by 19
Laboratory studies of the effects of reduced prey choice caused by Bt plants on a predatory insect
Schuler, T. H., Clark, A. J., Clark, S. J., Poppy, G. M., Stewart, C. N., & Denholm, I. (2005) · Bulletin of Entomological Research · doi:10.1079/ber2004356 · Cited by 19
Laboratory studies on the effects of transgenic corn on the spider mite Tetranychus urticae Koch.
Lozzia, G. C., Rigamonti, I. E., Manachini, B. R. I., & Rocchetti, R. (2000) · Cited by 18
Yao, H., Yè, G., Jiang, C., Fan, L., Datta, K., Hu, C., & Datta, S. K. (2006) · Applied Entomology and Zoology · doi:10.1303/aez.2006.339 · Cited by 18
Li, W., Wu, K., Wang, X.-Q., Wang, G., & Guo, Y. (2005) · Environmental Entomology · doi:10.1603/0046-225x-34.4.922 · Cited by 18
Zhu, S., Su, J.-W., Liu, X., Du, L., Yardım, E. N., & Ge, F. (2006) · Zoological studies · Cited by 17
Naranjo, S. E., & Luttrell, R. G. (2008) · Cambridge University Press eBooks · doi:10.1017/cbo9780511626463.026 · Cited by 16
Self-citationGuo, J., Wan, F., Liang, D., Löveï, G. L., & Han, Z. (2008) · Environmental Entomology · doi:10.1603/0046-225x(2008)37[263:tibbct]2.0.co;2 · Cited by 16
Cloutier, C., Boudreault, S., & Michaud, D. (2008) · Cahiers Agricultures · doi:10.1684/agr.2008.0213 · Cited by 16
Harwood, J. D., & Obrycki, J. J. (2005) · Biocontrol Science and Technology · doi:10.1080/09583150500257216 · Cited by 15
Carter, M. E., Villani, M. G., Allee, L. L., & Losey, J. E. (2004) · Journal of Applied Entomology · doi:10.1046/j.1439-0418.2003.00788.x · Cited by 15
Arpaia, S., Leo, G. M. D., Fiore, M. C., Schmidt, J. E. U., & Scardi, M. (2007) · Environmental Entomology · doi:10.1603/0046-225x(2007)36[213:coasai]2.0.co;2 · Cited by 15
Genetically modified potatoes expressing Cry 3A protein do not affect aphidophagous coccinellids
Kalushkov, P., & Nedvěd, O. (2005) · Journal of Applied Entomology · doi:10.1111/j.1439-0418.2005.00987.x · Cited by 14
Árpás, K., Tóth, F., & Kiss, J. G. (2005) · Acta Phytopathologica et Entomologica Hungarica · doi:10.1556/aphyt.40.2005.3-4.16 · Cited by 14
Shieh, J. N., Berry, R. E., Reed, G. L., & Rossignol, P. A. (1994) · Journal of Economic Entomology · doi:10.1093/jee/87.3.618 · Cited by 14
Szekeres, D., Kádár, F., & Kiss, J. G. (2006) · Entomologica Fennica · doi:10.33338/ef.84344 · Cited by 14
Cry3A-Intoxicated Leptinotarsa decemlineata (Say) are Palatable Prey for Lebia grandis Hentz
Riddick, E. W., & Barbosa, P. (2000) · Journal of Entomological Science · doi:10.18474/0749-8004-35.3.342 · Cited by 13
Tounou, A., Gounou, S., Borgemeister, C., Goumedzoe, Y. M. D., & Schulthess, F. (2005) · Biocontrol Science and Technology · doi:10.1080/09583150400015995 · Cited by 12
Kim, Y. H., Kang, J. S., Kim, J. I., Kwon, M. J., Lee, S., Cho, H. S., & Lee, S. H. (2008) · Journal of Economic Entomology · doi:10.1603/0022-0493(2008)101[1134:eobtcc]2.0.co;2 · Cited by 12
Effect of Transgenic Bt Rice on the Survival of Three Nontarget Stored Product Insect Pests
Riudavets, J., Gabarra, R., Pons, M. J., & Messeguer, J. (2006) · Environmental Entomology · doi:10.1603/0046-225x(2006)35[1432:eotbro]2.0.co;2 · Cited by 11
Shirai, Y. (2006) · Applied Entomology and Zoology · doi:10.1303/aez.2006.607 · Cited by 8
Xiaomu, M., LIU, X., Zhang, Q., LI, J., & REN, A. (2006) · Insect Science · doi:10.1111/j.1744-7917.2006.00095.x · Cited by 7
Zhang, S. ‐., Xie, B. ‐., Cui, J., & Li, D. ‐. (2006) · Journal of Applied Entomology · doi:10.1111/j.1439-0418.2006.01052.x · Cited by 7
Tóth, F., Árpás, K., Szekeres, D., Kádár, F., Szentkirályi, F., Szénási, Á., & Kiss, J. G. (2004) · Environmental Biosafety Research · doi:10.1051/ebr:2005006 · Cited by 6
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Douglas, M. R., & Tooker, J. F. (2015) · Environmental Science & Technology · doi:10.1021/es506141g · Cited by 544
Evolutionary ecology of insect adaptation to Bt crops
Carrière, Y., Crowder, D. W., & Tabashnik, B. E. (2010) · Evolutionary Applications · doi:10.1111/j.1752-4571.2010.00129.x · Cited by 318
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
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
“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-citationRomeis, 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
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
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