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      Risk Assessment of Genetically Engineered Maize Resistant to Diabrotica spp.: Influence on Above-Ground Arthropods in the Czech Republic

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          Abstract

          Transgenic maize MON88017, expressing the Cry3Bb1 toxin from Bacillus thuringiensis ( Bt maize), confers resistance to corn rootworms ( Diabrotica spp.) and provides tolerance to the herbicide glyphosate. However, prior to commercialization, substantial assessment of potential effects on non-target organisms within agroecosystems is required. The MON88017 event was therefore evaluated under field conditions in Southern Bohemia in 2009–2011, to detect possible impacts on the above-ground arthropod species. The study compared MON88017, its near-isogenic non- Bt hybrid DK315 (treated or not treated with the soil insecticide Dursban 10G) and two non- Bt reference hybrids (KIPOUS and PR38N86). Each hybrid was grown on five 0.5 ha plots distributed in a 14-ha field with a Latin square design. Semiquantitative ELISA was used to verify Cry3Bb1 toxin levels in the Bt maize. The species spectrum of non-target invertebrates changed during seasons and was affected by weather conditions. The thrips Frankliniella occidentalis was the most abundant species in all three successive years. The next most common species were aphids Rhopalosiphum padi and Metopolophium dirhodum. Frequently observed predators included Orius spp. and several species within the Coccinellidae. Throughout the three-year study, analysis of variance indicated some significant differences (P<0.05). Multivariate analysis showed that the abundance and diversity of plant dwelling insects was similar in maize with the same genetic background, for both Bt (MON88017) and non- Bt (DK315) untreated or insecticide treated. KIPOUS and PR38N86 showed some differences in species abundance relative to the Bt maize and its near-isogenic hybrid. However, the effect of management regime on arthropod community was insignificant and accounted only for a negligible portion of the variability.

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          Most cited references19

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          Adaptation and invasiveness of western corn rootworm: intensifying research on a worsening pest.

          The western corn rootworm, Diabrotica virgifera virgifera LeConte, is an established insect pest of maize (Zea mays L.) in North America. The rotation of maize with another crop, principally soybeans, Glycine max (L.), was the primary management strategy utilized by North American producers and remained highly effective until the mid-1990s. In 1995, widespread and severe root injury occurred in east-central Illinois and northern Indiana maize fields that had been annually rotated with soybeans on a regular basis for several decades. The failure of this cultural tactic from a pest management perspective was attributed to a behavioral adaptation by a variant western corn rootworm that had lost fidelity to maize for egg laying. In 1992, an infestation of western corn rootworm was found within a small maize field near the Belgrade Airport. By 2007, the presence of this insect pest had been confirmed in 20 European countries. More recent molecular studies have confirmed that at least three separate invasions (until 2004) of western corn rootworms have occurred in Europe, increasing the risk that rotation-resistant western corn rootworms will be introduced into a new continent. Although biological control and use of conventional resistant maize hybrids have not achieved widespread success in the management of western corn rootworms in North America, these tactics are being evaluated in Europe.
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            Predaceous Coccinellidae in biological control.

            Coccinellids have been widely used in biological control for over a century, and the methods for using these predators have remained virtually unchanged. The causes for the relatively low rates of establishment of coccinellids in importation biological control have not been examined for most species. Augmentative releases of several coccinellid species are well documented and effective; however, ineffective species continue to be used because of ease of collection. For most agricultural systems, conservation techniques for coccinellids are lacking, even though they are abundant in these habitats. Evaluation techniques are available, but quantitative assessments of the efficacy of coccinellids have not been done for most species in most agricultural crops. Greater emphasis is needed on evaluation, predator specificity, understanding colonization of new environments, and assessment of community-level interactions to maximize the use of coccinellids in biological control.
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              Bt Crop Effects on Functional Guilds of Non-Target Arthropods: A Meta-Analysis

              Background 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. Methodology/Principal Findings 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. Conclusions/Significance 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; insecticde 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.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                17 June 2015
                2015
                : 10
                : 6
                : e0130656
                Affiliations
                [1 ]Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic
                [2 ]Institute of Entomology, Biology Centre CAS, České Budějovice, Czech Republic
                [3 ]Department of Entomology, University of Minnesota, St. Paul, Minnesota, United States of America
                French National Institute for Agricultural Research (INRA), FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: OSH FS. Performed the experiments: OSH ZS HMH. Analyzed the data: ZS OSH. Wrote the paper: ZS FS WDH OSH HMH.

                Article
                PONE-D-14-31470
                10.1371/journal.pone.0130656
                4470634
                26083254
                13c80842-4f70-4fb8-ba36-550d51cdcace
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 14 July 2014
                : 25 May 2015
                Page count
                Figures: 2, Tables: 4, Pages: 16
                Funding
                Funding: Funding was provided by National Agency for Agricultural Research ( http://www.nazv.cz/cz/), grant QH91093. The field rent and the land management were contracted to the Agricultural Company Dubné a.s. and paid from the QH91093 grant. The maize seeds were provided free by the Monsanto ČR s.r.o. Research was promoted with institutional support RVO:60077344 from Institute of Entomology, Biology Centre of the Czech Academy of Sciences ( http://www.entu.cas.cz/en/). The PhD student Z. Svobodová was partially supported by grant GAJU 038/2014/P from the University of South Bohemia ( http://www.jcu.cz/research/gaju). None of the funders had any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Research Article
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