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      Is Osmia bicornis an adequate regulatory surrogate? Comparing its acute contact sensitivity to Apis mellifera

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          Abstract

          Bees provide essential ecosystem services and help maintain floral biodiversity. However, there is an ongoing decline of wild and domesticated bee species. Since agricultural pesticide use is a key driver of this process, there is a need for a protective risk assessment. To achieve a more protective registration process, two bee species, Osmia bicornis/ Osmia cornuta and Bombus terrestris, were proposed by the European Food Safety Authority as additional test surrogates to the honey bee Apis mellifera. We investigated the acute toxicity (median lethal dose, LD50) of multiple commercial insecticide formulations towards the red mason bee ( O. bicornis) and compared these values to honey bee regulatory endpoints. In two thirds of all cases, O. bicornis was less sensitive than the honey bee. By applying an assessment factor of 10 on the honey bee endpoint, a protective level was achieved for 87% (13 out 15) of all evaluated products. Our results show that O. bicornis is rarely an adequate additional surrogate species for lower tier risk assessment since it is less sensitive than the honey bee for the majority of investigated products. Given the currently limited database on bee species sensitivity, the honey bee seems sufficiently protective in acute scenarios as long as a reasonable assessment factor is applied. However, additional surrogate species can still be relevant for ecologically meaningful higher tier studies.

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          Most cited references23

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          High Levels of Miticides and Agrochemicals in North American Apiaries: Implications for Honey Bee Health

          Background Recent declines in honey bees for crop pollination threaten fruit, nut, vegetable and seed production in the United States. A broad survey of pesticide residues was conducted on samples from migratory and other beekeepers across 23 states, one Canadian province and several agricultural cropping systems during the 2007–08 growing seasons. Methodology/Principal Findings We have used LC/MS-MS and GC/MS to analyze bees and hive matrices for pesticide residues utilizing a modified QuEChERS method. We have found 121 different pesticides and metabolites within 887 wax, pollen, bee and associated hive samples. Almost 60% of the 259 wax and 350 pollen samples contained at least one systemic pesticide, and over 47% had both in-hive acaricides fluvalinate and coumaphos, and chlorothalonil, a widely-used fungicide. In bee pollen were found chlorothalonil at levels up to 99 ppm and the insecticides aldicarb, carbaryl, chlorpyrifos and imidacloprid, fungicides boscalid, captan and myclobutanil, and herbicide pendimethalin at 1 ppm levels. Almost all comb and foundation wax samples (98%) were contaminated with up to 204 and 94 ppm, respectively, of fluvalinate and coumaphos, and lower amounts of amitraz degradates and chlorothalonil, with an average of 6 pesticide detections per sample and a high of 39. There were fewer pesticides found in adults and brood except for those linked with bee kills by permethrin (20 ppm) and fipronil (3.1 ppm). Conclusions/Significance The 98 pesticides and metabolites detected in mixtures up to 214 ppm in bee pollen alone represents a remarkably high level for toxicants in the brood and adult food of this primary pollinator. This represents over half of the maximum individual pesticide incidences ever reported for apiaries. While exposure to many of these neurotoxicants elicits acute and sublethal reductions in honey bee fitness, the effects of these materials in combinations and their direct association with CCD or declining bee health remains to be determined.
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            Non-bee insects are important contributors to global crop pollination

            Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25-50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.
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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
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                2019
                8 August 2019
                : 14
                : 8
                : e0201081
                Affiliations
                [001] University of Koblenz-Landau, Institute for Environmental Sciences, Landau, Germany
                University of Illinois at Urbana-Champaign, UNITED STATES
                Author notes

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

                [¤]

                Current address: Federal Institute of Hydrology, Koblenz, Germany

                Author information
                http://orcid.org/0000-0003-4697-5949
                Article
                PONE-D-18-19836
                10.1371/journal.pone.0201081
                6687126
                31393875
                bd6c10ba-8ad7-45ca-b3c5-19a658934cb0
                © 2019 Uhl et al

                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
                : 4 July 2018
                : 23 July 2019
                Page count
                Figures: 1, Tables: 2, Pages: 12
                Funding
                The author(s) received no specific funding for this work.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Bees
                Honey Bees
                Biology and Life Sciences
                Agriculture
                Agrochemicals
                Insecticides
                Biology and Life Sciences
                Agriculture
                Agrochemicals
                Pesticides
                Biology and Life Sciences
                Agriculture
                Pest Control
                Pesticides
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Bees
                Medicine and Health Sciences
                Pharmacology
                Drug Research and Development
                Toxicity Testing
                Biology and Life Sciences
                Toxicology
                Toxicity
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Toxicology
                Toxicity
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Ethers
                Organophosphates
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Ethers
                Organophosphates
                Biology and Life Sciences
                Agriculture
                Agroecology
                Colony Collapse
                Biology and Life Sciences
                Ecology
                Agroecology
                Colony Collapse
                Ecology and Environmental Sciences
                Ecology
                Agroecology
                Colony Collapse
                Custom metadata
                All files are available as: Uhl, Philipp; Awanbor, Osarobo; Schulz, Robert S.; Brühl, Carsten A. (2018): Raw data - Ecotoxicologal tests with Osmia bicornis and 16 insecticides. figshare. Fileset. under: https://doi.org/10.6084/m9.figshare.6143945.v9.

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