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      Combined pesticide exposure severely affects individual- and colony-level traits in bees

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          Abstract

          Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production 1- 3 . Bees contribute around 80% of insect pollination, so it is imperative we understand and mitigate the causes of current declines 4- 6 . Recent studies have implicated the role of pesticides as exposure to these chemicals has been associated with changes in bee behaviour 7- 11 and reductions in colony queen production 12 . However the key link between changes in individual behaviour and consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of numerous individual workers. So whilst field-level pesticide concentrations can have a subtle/sublethal effect at the individual level 8 , it is not known whether bee societies can buffer such effects or if it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means bees are exposed to numerous pesticides when foraging 13- 15 , yet the possible combinatorial effects of pesticide exposure have rarely been investigated 16, 17 . Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concentrations that could approximate field-level exposure impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success. We found worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with observed knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail.

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          Most cited references41

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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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            The conservation of bees: a global perspective

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              Pesticides and honey bee toxicity – USA

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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                15 October 2012
                21 October 2012
                1 November 2012
                01 May 2013
                : 491
                : 7422
                : 105-108
                Affiliations
                School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX
                Author notes
                Correspondence and requests for materials should be addresses to RJG ( richard.gill@ 123456rhul.ac.uk ) or NER ( nigel.raine@ 123456rhul.ac.uk ).

                Author Contributions RJG, ORR & NER carried-out the experiment, RJG & NER designed the experiment and wrote the paper, NER conceived the project.

                Article
                EMS49946
                10.1038/nature11585
                3495159
                23086150
                6d93310c-1d8a-4fe3-b362-6d6a9ac3a135

                Users may view, print, copy, download and text and data- mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms

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