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      Estimating the effects of Cry1F Bt-maize pollen on non-target Lepidoptera using a mathematical model of exposure

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          Abstract

          1. In farmland biodiversity, a potential risk to the larvae of non-target Lepidoptera from genetically modified (GM) Bt-maize expressing insecticidal Cry1 proteins is the ingestion of harmful amounts of pollen deposited on their host plants. A previous mathematical model of exposure quantified this risk for Cry1Ab protein. We extend this model to quantify the risk for sensitive species exposed to pollen containing Cry1F protein from maize event 1507 and to provide recommendations for management to mitigate this risk.

          2. A 14-parameter mathematical model integrating small- and large-scale exposure was used to estimate the larval mortality of hypothetical species with a range of sensitivities, and under a range of simulated mitigation measures consisting of non- Bt maize strips of different widths placed around the field edge.

          3. The greatest source of variability in estimated mortality was species sensitivity. Before allowance for effects of large-scale exposure, with moderate within-crop host-plant density and with no mitigation, estimated mortality locally was <10% for species of average sensitivity. For the worst-case extreme sensitivity considered, estimated mortality locally was 99·6% with no mitigation, although this estimate was reduced to below 40% with mitigation of 24-m-wide strips of non- Bt maize. For highly sensitive species, a 12-m-wide strip reduced estimated local mortality under 1·5%, when within-crop host-plant density was zero. Allowance for large-scale exposure effects would reduce these estimates of local mortality by a highly variable amount, but typically of the order of 50-fold.

          4. Mitigation efficacy depended critically on assumed within-crop host-plant density; if this could be assumed negligible, then the estimated effect of mitigation would reduce local mortality below 1% even for very highly sensitive species.

          5. Synthesis and applications. Mitigation measures of risks of Bt-maize to sensitive larvae of non-target lepidopteran species can be effective, but depend on host-plant densities which are in turn affected by weed-management regimes. We discuss the relevance for management of maize events where cry1F is combined (stacked) with a herbicide-tolerance trait. This exemplifies how interactions between biota may occur when different traits are stacked irrespective of interactions between the proteins themselves and highlights the importance of accounting for crop management in the assessment of the ecological impact of GM plants.

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          A meta-analysis of effects of Bt cotton and maize on nontarget invertebrates.

          Although scores of experiments have examined the ecological consequences of transgenic Bacillus thuringiensis (Bt) crops, debates continue regarding the nontarget impacts of this technology. Quantitative reviews of existing studies are crucial for better gauging risks and improving future risk assessments. To encourage evidence-based risk analyses, we constructed a searchable database for nontarget effects of Bt crops. A meta-analysis of 42 field experiments indicates that nontarget invertebrates are generally more abundant in Bt cotton and Bt maize fields than in nontransgenic fields managed with insecticides. However, in comparison with insecticide-free control fields, certain nontarget taxa are less abundant in Bt fields.
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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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              Corn pollen deposition on milkweeds in and near cornfields.

              The density of corn pollen on leaves of milkweed plants inside and outside of cornfields was measured in several studies from different localities. The purpose was to obtain a representative picture of naturally occurring pollen densities to provide a perspective for laboratory and field studies of monarch larvae feeding on milkweed leaves with Bt corn pollen. Pollen density was highest (average 170.6 grains per cm(2)) inside the cornfield and was progressively lower from the field edge outward, falling to 14.2 grains per cm(2) at 2 m. Inside the cornfield, and for each distance from the field edge, a frequency distribution is presented showing the proportion of leaf samples with different pollen densities. Inside cornfields, 95% of leaf samples had pollen densities below 600 grains per cm(2) and the highest pollen density observed was 1400 grains per cm(2), which occurred in a study with a rainless anthesis period. All other studies had rainfall events during the anthesis period. A single rain event can remove 54-86% of the pollen on leaves. Leaves on the upper portion of milkweed plants, where young monarch larvae tend to feed, had only 30-50% of the pollen density levels of middle leaves.
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                Author and article information

                Journal
                J Appl Ecol
                J Appl Ecol
                jpe
                The Journal of Applied Ecology
                Blackwell Publishing Ltd (Oxford, UK )
                0021-8901
                1365-2664
                February 2012
                : 49
                : 1
                : 29-37
                Affiliations
                [1 ]simpleOaklands Barn, Lug’s Lane, Broome Norfolk NR35 2HT, UK
                [2 ]simpleEuropean Food Safety Authority, GMO Unit Largo Natale Palli 5/A, IT-43121 Parma, Italy
                [3 ]simpleItalian National Agency for New Technologies, Energy and Environment, Research Centre Trisaia IT-75026 Rotondella, Italy
                [4 ]simpleFederal Office of Consumer Protection and Food Safety Mauerstrasse 39-42, DE-10117 Berlin, Germany
                [5 ]simpleCEH-Wallingford, Maclean Building, Crowmarsh Gifford Wallingford, Oxon OX10 8BB, UK
                [6 ]simpleAarhus University, NERI, Department of Environmental Chemistry and Microbiology Frederiksborgvej 399, DK-4000 Roskilde, Denmark
                [7 ]simpleSzent István University, Plant Protection Institute Pater K. 1, HU-2100 Gödöllo˝, Hungary
                [8 ]simpleINRA, Unité Eco-Innov, BP1 Campus de Grignon FR-78850 Thiveral-Grignon, France
                [9 ]simpleBüro für Landschaftsökologie und Umweltstudien Muehlenweg 60, D-29358 Eicklingen, Germany
                [10 ]simpleUniversità di Pisa, Facoltà di Agraria, Dipartimento di Biologia delle Piante Agrarie Via del Borghetto 80, IT-56124 Pisa, Italy
                [11 ]simpleSweet Environmental Consultants 6 The Green, Willingham, Cambridge CB24 5JA, UK
                [12 ]simpleJohann Heinrich von Thünen-Institute, Institute for Biodiversity Bundesallee 50, DE-38116 Braunschweig, Germany
                Author notes
                Correspondence author. E-mail: joe.perry@ 123456rothamsted.ac.uk

                Re-use of this article is permitted in accordance with the Terms and Conditions set out at http://wileyonlinelibrary.com/onlineopen#OnlineOpen_Terms

                Article
                10.1111/j.1365-2664.2011.02083.x
                3321227
                22496596
                09ad3b8d-2514-42ef-af84-54d776183832
                © 2011 The Authors. Journal of Applied Ecology © 2011 British Ecological Society

                Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

                History
                : 31 May 2011
                : 07 October 2011
                Categories
                Risk Assessment

                Ecology
                mitigation measures,exposure,crop management,non-target lepidoptera,ecological impact,bt,genetically modified maize,mathematical model,cry1f

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