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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Book Reviews: Statistical Methods for Meta-Analysis Larry V. Hedges and Ingram Olkin New York: Academic Press, 1985. xxii + 369 pp
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
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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
Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides
Carlini, C. R., & Grossi‐de‐Sá, M. F. (2002) · Toxicon · doi:10.1016/s0041-0101(02)00240-4 · Cited by 543

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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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