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      Assessment of risk to hoary squash bees ( Peponapis pruinosa) and other ground-nesting bees from systemic insecticides in agricultural soil

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          Abstract

          Using the hoary squash bee ( Peponapis pruinosa) as a model, we provide the first probabilistic risk assessment of exposure to systemic insecticides in soil for ground-nesting bees. To assess risk in acute and chronic exposure scenarios in Cucurbita and field crops, concentrations of clothianidin, thiamethoxam and imidacloprid (neonicotinoids) and chlorantraniliprole (anthranilic diamide) in cropped soil were plotted to produce an environmental exposure distribution for each insecticide. The probability of exceedance of several exposure endpoints (LC 50s) was compared to an acceptable risk threshold (5%). In Cucurbita crops, under acute exposure, risk to hoary squash bees was below 5% for honey bee LC 50s for all residues evaluated but exceeded 5% for clothianidin and imidacloprid using a solitary bee LC 50. For Cucurbita crops in the chronic exposure scenario, exposure risks for clothianidin and imidacloprid exceeded 5% for all endpoints, and exposure risk for chlorantraniliprole was below 5% for all endpoints. In field crops, risk to ground-nesting bees was high from clothianidin in all exposure scenarios and high for thiamethoxam and imidacloprid under chronic exposure scenarios. Risk assessments for ground-nesting bees should include exposure impacts from pesticides in soil and could use the hoary squash bee as an ecotoxicology model.

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          Foraging ranges of solitary bees

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            Pesticide Residues and Bees – A Risk Assessment

            Bees are essential pollinators of many plants in natural ecosystems and agricultural crops alike. In recent years the decline and disappearance of bee species in the wild and the collapse of honey bee colonies have concerned ecologists and apiculturalists, who search for causes and solutions to this problem. Whilst biological factors such as viral diseases, mite and parasite infections are undoubtedly involved, it is also evident that pesticides applied to agricultural crops have a negative impact on bees. Most risk assessments have focused on direct acute exposure of bees to agrochemicals from spray drift. However, the large number of pesticide residues found in pollen and honey demand a thorough evaluation of all residual compounds so as to identify those of highest risk to bees. Using data from recent residue surveys and toxicity of pesticides to honey and bumble bees, a comprehensive evaluation of risks under current exposure conditions is presented here. Standard risk assessments are complemented with new approaches that take into account time-cumulative effects over time, especially with dietary exposures. Whilst overall risks appear to be low, our analysis indicates that residues of pyrethroid and neonicotinoid insecticides pose the highest risk by contact exposure of bees with contaminated pollen. However, the synergism of ergosterol inhibiting fungicides with those two classes of insecticides results in much higher risks in spite of the low prevalence of their combined residues. Risks by ingestion of contaminated pollen and honey are of some concern for systemic insecticides, particularly imidacloprid and thiamethoxam, chlorpyrifos and the mixtures of cyhalothrin and ergosterol inhibiting fungicides. More attention should be paid to specific residue mixtures that may result in synergistic toxicity to bees.
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              Environmental fate and exposure; neonicotinoids and fipronil

              Systemic insecticides are applied to plants using a wide variety of methods, ranging from foliar sprays to seed treatments and soil drenches. Neonicotinoids and fipronil are among the most widely used pesticides in the world. Their popularity is largely due to their high toxicity to invertebrates, the ease and flexibility with which they can be applied, their long persistence, and their systemic nature, which ensures that they spread to all parts of the target crop. However, these properties also increase the probability of environmental contamination and exposure of nontarget organisms. Environmental contamination occurs via a number of routes including dust generated during drilling of dressed seeds, contamination and accumulation in arable soils and soil water, runoff into waterways, and uptake of pesticides by nontarget plants via their roots or dust deposition on leaves. Persistence in soils, waterways, and nontarget plants is variable but can be prolonged; for example, the half-lives of neonicotinoids in soils can exceed 1,000 days, so they can accumulate when used repeatedly. Similarly, they can persist in woody plants for periods exceeding 1 year. Breakdown results in toxic metabolites, though concentrations of these in the environment are rarely measured. Overall, there is strong evidence that soils, waterways, and plants in agricultural environments and neighboring areas are contaminated with variable levels of neonicotinoids or fipronil mixtures and their metabolites (soil, parts per billion (ppb)-parts per million (ppm) range; water, parts per trillion (ppt)-ppb range; and plants, ppb-ppm range). This provides multiple routes for chronic (and acute in some cases) exposure of nontarget animals. For example, pollinators are exposed through direct contact with dust during drilling; consumption of pollen, nectar, or guttation drops from seed-treated crops, water, and consumption of contaminated pollen and nectar from wild flowers and trees growing near-treated crops. Studies of food stores in honeybee colonies from across the globe demonstrate that colonies are routinely and chronically exposed to neonicotinoids, fipronil, and their metabolites (generally in the 1–100 ppb range), mixed with other pesticides some of which are known to act synergistically with neonicotinoids. Other nontarget organisms, particularly those inhabiting soils, aquatic habitats, or herbivorous insects feeding on noncrop plants in farmland, will also inevitably receive exposure, although data are generally lacking for these groups. We summarize the current state of knowledge regarding the environmental fate of these compounds by outlining what is known about the chemical properties of these compounds, and placing these properties in the context of modern agricultural practices.
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                Author and article information

                Contributors
                dchan05@uoguelph.ca
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                14 August 2019
                14 August 2019
                2019
                : 9
                : 11870
                Affiliations
                [1 ]ISNI 0000 0004 1936 8198, GRID grid.34429.38, School of Environmental Sciences, , University of Guelph, ; Guelph, Ontario N1G 2W1 Canada
                [2 ]ISNI 0000 0001 2182 2255, GRID grid.28046.38, Department of Biology, , University of Ottawa, ; Ottawa, Ontario K1N 6N5 Canada
                Author information
                http://orcid.org/0000-0003-1910-0768
                http://orcid.org/0000-0001-9325-9131
                http://orcid.org/0000-0001-6343-2829
                Article
                47805
                10.1038/s41598-019-47805-1
                6694176
                31413274
                ef5f27b6-ed35-4683-9335-4aa263972894
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 18 March 2019
                : 22 July 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100000094, Ontario Ministry of Agriculture, Food and Rural Affairs (Ministère de l'Agriculture, de l'Alimentation et des Affaires rurales);
                Award ID: UofG2015-2466
                Award ID: UofG2015-2466
                Award Recipient :
                Funded by: Fresh Vegetable Growers of Ontario: http://www.freshvegetablesontario.com/
                Funded by: FundRef https://doi.org/10.13039/501100002790, Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada (NSERC Canadian Network for Research and Innovation in Machining Technology);
                Award ID: 2018- 04641
                Award ID: 2015-06783
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100010785, Canada First Research Excellence Fund (Fonds d'excellence en recherche Apogée Canada);
                Award ID: 000054
                Award Recipient :
                Funded by: Ontario Ministry of the Environment, Conservation, and Parks: https://www.ontario.ca/page/ministry-environment-conservation-parks, grant provided under former name: Ontario Ministry of Environment and Climate Change (MOECC) Best in Science grant #BIS201617-06
                Categories
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                Custom metadata
                © The Author(s) 2019

                Uncategorized
                environmental impact,agroecology
                Uncategorized
                environmental impact, agroecology

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