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      Pesticide residues in honeybee-collected pollen: does the EU regulation protect honeybees from pesticides?

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          Abstract

          Researchers globally identify pesticides as one of the main reasons for pollinator decline. In the European Union (EU), extensive legislation is implemented to protect pollinators from harmful pesticide exposure. The aim of our study was to discover whether the pesticide residue levels in honeybee matrices, such as nectar and pollen, exceeded the chronic or acute toxicity levels when beehives were located next to fields treated with specific insecticides. The insecticides were used according to the EU legislation and its national implementation. The experiments were conducted in turnip rape, oilseed rape, and caraway fields in southern Finland during the years 2019 and 2020. The pesticides used in the experiments contained the active substances lambda-cyhalothrin (2019), esfenvalerate (2020), and tau-fluvalinate (2020). However, the honeybee-collected pollen and nectar were analyzed for residues of more than 100 active substances. The results showed that the pesticide residue levels clearly remained under the oral acute toxicity for honeybees, although we found high levels of thiacloprid residues in the pollen collected in 2019. The pesticide residues in nectar were below LOQ values, which was most likely due to the rainy weather conditions together with the chosen sampling method. No statistically significant differences were observed between the insecticide-treated and untreated fields. In light of our research, the EU legislation protected honeybees from oral acute toxicity during the years 2019 and 2020. However, potential sublethal effects of thiacloprid and other pesticide compounds found in the collected pollen cannot be ruled out. In the future, constant monitoring of pesticide exposure of honeybees and wild pollinators should be established to ensure that pesticide legislation, and its implementation across the EU successfully protects pollinators and their services in agricultural environments.

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          Most cited references27

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          Global pollinator declines: trends, impacts and drivers.

          Pollinators are a key component of global biodiversity, providing vital ecosystem services to crops and wild plants. There is clear evidence of recent declines in both wild and domesticated pollinators, and parallel declines in the plants that rely upon them. Here we describe the nature and extent of reported declines, and review the potential drivers of pollinator loss, including habitat loss and fragmentation, agrochemicals, pathogens, alien species, climate change and the interactions between them. Pollinator declines can result in loss of pollination services which have important negative ecological and economic impacts that could significantly affect the maintenance of wild plant diversity, wider ecosystem stability, crop production, food security and human welfare. Copyright (c) 2010 Elsevier Ltd. All rights reserved.
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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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              Foraging ranges of solitary bees

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                Author and article information

                Contributors
                lotta.kaila@helsinki.fi , ext.lotta.kaila@luke.fi
                jarmo.ketola@luke.fi
                marjaana.toivonen@syke.fi
                olli.loukola@oulu.fi
                kati.hakala@ruokavirasto.fi
                sakari.raiskio@luke.fi
                timo.hurme@luke.fi
                marja.jalli@luke.fi
                Journal
                Environ Sci Pollut Res Int
                Environ Sci Pollut Res Int
                Environmental Science and Pollution Research International
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0944-1344
                1614-7499
                23 October 2021
                23 October 2021
                2022
                : 29
                : 12
                : 18225-18244
                Affiliations
                [1 ]GRID grid.7737.4, ISNI 0000 0004 0410 2071, Department of Agricultural Sciences, , University of Helsinki, ; P.O. Box 27, 00014 Helsinki, Finland
                [2 ]GRID grid.22642.30, ISNI 0000 0004 4668 6757, Natural Resources Institute Finland (Luke), ; Latokartanonkaari 9, 00790 Helsinki, Finland
                [3 ]GRID grid.22642.30, ISNI 0000 0004 4668 6757, Natural Resources Institute Finland (Luke), ; Tietotie 4, 31600 Jokioinen, Finland
                [4 ]GRID grid.410381.f, ISNI 0000 0001 1019 1419, Finnish Environment Institute (SYKE), ; Biodiversity Centre, Latokartanonkaari 11, 00790 Helsinki, Finland
                [5 ]GRID grid.10858.34, ISNI 0000 0001 0941 4873, Ecology and Genetics Research Unit, , University of Oulu, University of Oulu, ; PO Box 3000, 90014 Oulu, Finland
                [6 ]GRID grid.509946.7, ISNI 0000 0004 9290 2959, Finnish Food Authority, ; Mustialankatu 3, 00790 Helsinki, Finland
                Author notes

                Responsible Editor: Philippe Garrigues

                Author information
                http://orcid.org/0000-0002-3844-0971
                Article
                16947
                10.1007/s11356-021-16947-z
                8873129
                34689272
                82540039-da16-4668-a4f2-271a6c853fb6
                © The Author(s) 2021

                Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 7 July 2021
                : 4 October 2021
                Funding
                Funded by: University of Helsinki including Helsinki University Central Hospital
                Categories
                Research Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2022

                General environmental science
                sustainable agriculture,pollinators,field-realistic residues,eu legislation,implementation,risk assessment

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