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      Do Biopesticides Affect the Demographic Traits of a Parasitoid Wasp and Its Biocontrol Services through Sublethal Effects?

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          Abstract

          Pesticide risk assessments are usually based on short-term acute toxicity tests, while longer-term population dynamic related traits, critical to the success of biological control and Integrated Pest Management (IPM) programs, are often overlooked. This is increasingly important with respect to new biopesticides that frequently cause no short-term acute effects, but that can induce multiple physiological and behavioral sublethal effects, leading to a decrease in population growth and ecosystem services. In this study we assessed the lethal and sublethal effects of six biopesticides [abamectin, azadirachtin, Bacillus thuringiensis, borax plus citrus oil (Prev-Am®), emamectin benzoate, and spinosad], used in tomato crops to control the invasive pest Tuta absoluta (Lepidoptera: Gelechiidae), on adults and pupae of the parasitoid Bracon nigricans (Hymenoptera: Braconidae). Data on female survival and production of female offspring were used to calculate population growth indexes as a measure of population recovery after pesticide exposure. Spinosad caused 100% and 80% mortality in exposed adults (even 10 d after the treatment) and pupae, respectively. Although most of the biopesticides had low levels of acute toxicity, multiple sublethal effects were observed. The biocontrol activity of both females that survived 1-h and 10-d old residues, and females that emerged from topically treated pupae was significantly affected by the application of the neurotoxic insecticides emamectin benzoate and abamectin. Furthermore, very low B. nigricans demographic growth indices were estimated for these two insecticides, indicating potential local extinction of the wasp populations. Among the tested products, Bt proved to be the safest for B. nigricans adults and pupae. Our findings emphasize that acute toxicity assessment alone cannot fully predict the actual impact of pesticides on non-target parasitoids. Thus, sublethal effects related to the species specific life-history variables must be carefully considered in order to assess pesticide risks and to incorporate new pesticides, including biopesticides, into IPM programmes.

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          Evolution of developmental strategies in parasitic hymenoptera.

          Parasitoid wasps have evolved a wide spectrum of developmental interactions with hosts. In this review we synthesize and interpret results from the phylogenetic, ecological, physiological, and molecular literature to identify factors that have influenced the evolution of parasitoid developmental strategies. We first discuss the origins and radiation of the parasitoid lifestyle in the Hymenoptera. We then summarize how parasitoid developmental strategies are affected by ecological interactions and assess the inventory of physiological and molecular traits parasitoids use to successfully exploit hosts. Last, we discuss how certain parasitoid virulence genes have evolved and how these changes potentially affect parasitoid-host interactions. The combination of phylogenetic data with comparative and functional genomics offers new avenues for understanding the evolution of biological diversity in this group of insects.
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            Sex determination in the hymenoptera.

            The dominant and ancestral mode of sex determination in the Hymenoptera is arrhenotokous parthenogenesis, in which diploid females develop from fertilized eggs and haploid males develop from unfertilized eggs. We discuss recent progress in the understanding of the genetic and cytoplasmic mechanisms that make arrhenotoky possible. The best-understood mode of sex determination in the Hymenoptera is complementary sex determination (CSD), in which diploid males are produced under conditions of inbreeding. The gene mediating CSD has recently been cloned in the honey bee and has been named the complementary sex determiner. However, CSD is only known from 4 of 21 hymenopteran superfamilies, with some taxa showing clear evidence of the absence of CSD. Sex determination in the model hymenopteran Nasonia vitripennis does not involve CSD, but it is consistent with a form of genomic imprinting in which activation of the female developmental pathway requires paternally derived genes. Some other hymenopterans are not arrhenotokous but instead exhibit thelytoky or paternal genome elimination.
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              Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus.

              The generalist predator Orius laevigatus (Fieber) (Hemiptera: Anthocoridae) is a key natural enemy of various arthropods in agricultural and natural ecosystems. Releases of this predator are frequently carried out, and it is included in the Integrated Pest Management (IPM) programs of several crops. The accurate assessment of the compatibility of various pesticides with predator activity is key for the success of this strategy. We assessed acute and sublethal toxicity of 14 pesticides on O. laevigatus adults under laboratory conditions. Pesticides commonly used in either conventional or organic farming were selected for the study, including six biopesticides, three synthetic insecticides, two sulfur compounds and three adjuvants. To assess the pesticides' residual persistence, the predator was exposed for 3d to pesticide residues on tomato sprouts that had been treated 1 h, 7 d or 14 d prior to the assay. The percentage of mortality and the sublethal effects on predator reproductive capacity were summarized in a reduction coefficient (E(x)) and the pesticides were classified according to the IOBC (International Organization for Biological Control) toxicity categories. The results showed that the pesticides greatly differed in their toxicity, both in terms of lethal and sub lethal effects, as well as in their persistence. In particular, abamectin was the most noxious and persistent, and was classified as harmful up to 14 d after the treatment, causing almost 100% mortality. Spinosad, emamectin, metaflumizone were moderately harmful until 7 d after the treatment, while the other pesticides were slightly harmful or harmless. The results, based on the combination of assessment of acute mortality, predator reproductive capacity pesticides residual and pesticides residual persistence, stress the need of using complementary bioassays (e.g. assessment of lethal and sublethal effects) to carefully select the pesticides to be used in IPM programs and appropriately time the pesticides application (as function of natural enemies present in crops) and potential releases of natural enemies like O. laevigatus. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                30 September 2013
                : 8
                : 9
                : e76548
                Affiliations
                [1 ]Department of Agri-food and Environmental Systems Management, University of Catania, Catania, Italy
                [2 ]French National Institute for Agricultural Research (INRA), Sophia-Antipolis, France
                [3 ]Departments of Entomology-Puyallup Research and Extension Center, Washington State University, Puyallup, Washington, United States of America
                Texas Tech University, United States of America
                Author notes

                Competing Interests: Dr. Nicolas Desneux is currently an Academic editor of PLOS ONE, but this does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: AB LZ JS ND. Performed the experiments: AB. Analyzed the data: AB JS LZ. Contributed reagents/materials/analysis tools: AB LZ ND. Wrote the paper: AB.

                Article
                PONE-D-13-15429
                10.1371/journal.pone.0076548
                3787011
                24098793
                6034efd3-f1c2-48de-9c97-3912e18a1781
                Copyright @ 2013

                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
                : 17 April 2013
                : 26 August 2013
                Page count
                Pages: 11
                Funding
                This research was partially funded by the Italian Ministry of Education, University and Research (PRIN project 2010CXXHJE_004) and the French Ministry of Agriculture (CASDAR project 10063). Antonio Biondi received a PhD grant from the University of Catania. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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