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United States Department of Agriculture

Agricultural Research Service

Risk Assessment in Transgenic Crops
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Non-target Effects of Transgenic Bt cottons with Emphasis on Natural Enemy Abundance
Steve Naranjo

A six-year field study assessed the long term impact of Bt cotton producing the Cry1Ac d-endotoxin on 22 taxa of foliar-dwelling arthropod natural enemies in Arizona. No chronic, long-term effects of Bt cotton were observed over multiple generations of non-target taxa. Zero-2 taxa declined significantly in unsprayed Bt compared with non-Bt cotton each year. In contrast, positive control studies showed that insecticide applications for caterpillars and other pests in both non-Bt and Bt cotton had much greater negative effects on 10 taxa. Multivariate principal response curves supported the findings of univariate analyses for the entire natural enemy community, showing no effect of Bt cotton but large and long-lasting negative effects from the use of insecticides. Multi-year analyses provided greater statistical power and indicated significant reductions that averaged 19% in five arthropod predator taxa in unsprayed Bt compared with non-Bt cotton. Most of these reductions were likely associated with reductions in lepidopteran prey. However, results of a companion study examining natural enemy function suggest that these minor reductions in Bt cotton have little ecological meaning. Multi-year analyses showed an average significant reduction of 48% in 13 taxa for plots receiving insecticide applications. On average, a three year study with four replicates per year was sufficient to discern changes of ≈20% with 80% power in unsprayed cotton. This long-term study indicates that the effects of Bt cotton on a representative non-target community are minor, especially in comparison with the alternative use of broad-spectrum insecticides. Guidelines for improving non-target field studies are discussed.  (PDF)

Non-target Effects of Transgenic Bt cottons with Emphasis on Natural Enemy Function
Steve Naranjo

Field studies to assess effects of transgenic crops on non-target organisms primarily have focused on non-target abundance and diversity, while few have examined effects on non-target community function. A five-year field study in Arizona assessed whether transgenic cotton producing the Cry1Ac toxin of Bacillus thuringiensis had an effect on the natural enemy community’s impact on three key pests. Predator:prey ratios for Bemisia tabaci (Gennadius) and Lygus hesperus Knight were similar in unsprayed Bt and non-Bt cotton. Insecticide applications in positive control plots inconsistently altered ratios for B. tabaci. Predation indices based on the known feeding activity of selected predators showed that potential predator impact was unaltered by Bt cotton, but was consistently depressed with insecticide applications. Sentinel eggs and pupae of Pectinophora gossypiella (Saunders) experienced the same rates of predation in both unsprayed Bt and non-Bt cotton. Cohort-based life tables for B. tabaci showed that rates of sucking predation, parasitism and dislodgement (chewing predation in part) were unchanged by Bt cotton. Underlying experimental designs were sufficient to consistently detect changes of <20% in predator:prey ratios and predation indices, and changes of <10% in rates of P. gossypiella and B. tabaci mortality with >80% power (a = 0.05). These long-term studies demonstrated essentially no effects of Bt cotton on natural enemy function in Arizona cotton and further showed that minor reductions in density of several predator taxa in Bt cotton observed in a companion study may have little ecological meaning relative to natural enemy impact on key pests in the system. (PDF)

Non-target Effects of Transgenic Crops on Ecological Functional Guilds

Steve Naranjo, LaRessa Wolfenbarger (UNeb), Jon Lundgren (ARS South Dakota, Royce Bitzer (Iowa State Univ), Lidia Watrud (EPA)


Uncertainty persists over the environmental effects of genetically-engineered crops that produce the insecticidal Cry proteins of Bacillus thuringiensis (Bt). We performed meta-analyses on a modified public database to synthesize current knowledge about the effects of Bt cotton, maize and potato on the abundance and interactions of arthropod non-target functional guilds. We compared the abundance of predators, parasitoids, omnivores, detritivores and herbivores under scenarios in which neither, only the non-Bt crops, or both Bt and non-Bt crops received insecticide treatments. Predators were less abundant in Bt cotton compared to unsprayed non-Bt controls. As expected, fewer specialist parasitoids of the target pest occurred in Bt maize fields compared to unsprayed non-Bt controls, but no significant reduction was detected for other parasitoids. Numbers of predators and herbivores were higher in Bt crops compared to sprayed non-Bt controls, and type of insecticide influenced the magnitude of the difference. Omnivores and detritivores were more abundant in insecticide-treated controls and for the latter guild this was associated with reductions of their predators in sprayed non-Bt maize. No differences in abundance were found when both Bt and non-Bt crops were sprayed. Predator-to-prey ratios were unchanged by either Bt crops or the use of insecticides; ratios were higher in Bt maize relative to the sprayed non-Bt control. Overall, we find no uniform effects of Bt cotton, maize and potato on the functional guilds of non-target arthropods. Use of and type of insecticides influenced the magnitude and direction of effects; insecticide effects were much larger than those of Bt crops. These meta-analyses underscore the importance of using controls not only to isolate the effects of a Bt crop per se but also to reflect the replacement of existing agricultural practices. Results will provide researchers with information to design more robust experiments and will inform the decisions of diverse stakeholders regarding the safety of transgenic insecticidal crops. (PDF)


Non-target Effects of Transgenic Crops and Insecticide Use Patterns

Steve Naranjo


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 to 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. (PDF)


Predicting Field Non-target Effects of Transgenic Crops from Tier I Studies

Jian Duan (ARS Deleware), Jon Lundgren (ARS South Dakota), Steve Naranjo, Michelle Marvier (Santa Clara Univ)


The tiered approach to assessing ecological risk of insect-resistant transgenic crops assumes that lower tier laboratory studies, which expose surrogate non-target organisms to high doses of insecticidal proteins, can detect harmful effects that might be manifested in the field. To test this assumption, we performed meta-analyses comparing results for non-target invertebrates exposed to Bacillus thuringiensis (Bt) Cry proteins in laboratory studies with results derived from independent field studies examining effects on the abundance of non-target invertebrates. For Lepidopteran-active Cry proteins, laboratory studies correctly predicted the reduced field abundance of non-target Lepidoptera. However, laboratory studies incorporating tri-trophic interactions of Bt plants, herbivores and parasitoids were better correlated with the decreased field abundance of parasitoids than were direct exposure assays. For predators, laboratory tri-trophic studies predicted reduced abundances that were not realized in field studies and thus overestimated ecological risk. Exposure to Coleopteran-active Cry proteins did not significantly reduce the laboratory survival or field abundance of any functional group examined. Our findings support the assumption that laboratory studies of transgenic insecticidal crops show effects that are either consistent with, or more conservative than, those found in field studies, with the important caveat that laboratory studies should explore all ecologically relevant routes of exposure. (PDF)


Last Modified: 5/14/2012