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      Sub-Lethal Effects of Pesticide Residues in Brood Comb on Worker Honey Bee ( Apis mellifera) Development and Longevity

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      PLoS ONE
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          Abstract

          Background

          Numerous surveys reveal high levels of pesticide residue contamination in honey bee comb. We conducted studies to examine possible direct and indirect effects of pesticide exposure from contaminated brood comb on developing worker bees and adult worker lifespan.

          Methodology/Principal Findings

          Worker bees were reared in brood comb containing high levels of known pesticide residues (treatment) or in relatively uncontaminated brood comb (control). Delayed development was observed in bees reared in treatment combs containing high levels of pesticides particularly in the early stages (day 4 and 8) of worker bee development. Adult longevity was reduced by 4 days in bees exposed to pesticide residues in contaminated brood comb during development. Pesticide residue migration from comb containing high pesticide residues caused contamination of control comb after multiple brood cycles and provided insight on how quickly residues move through wax. Higher brood mortality and delayed adult emergence occurred after multiple brood cycles in contaminated control combs. In contrast, survivability increased in bees reared in treatment comb after multiple brood cycles when pesticide residues had been reduced in treatment combs due to residue migration into uncontaminated control combs, supporting comb replacement efforts. Chemical analysis after the experiment confirmed the migration of pesticide residues from treatment combs into previously uncontaminated control comb.

          Conclusions/Significance

          This study is the first to demonstrate sub-lethal effects on worker honey bees from pesticide residue exposure from contaminated brood comb. Sub-lethal effects, including delayed larval development and adult emergence or shortened adult longevity, can have indirect effects on the colony such as premature shifts in hive roles and foraging activity. In addition, longer development time for bees may provide a reproductive advantage for parasitic Varroa destructor mites. The impact of delayed development in bees on Varroa mite fecundity should be examined further.

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          Most cited references9

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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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            A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee

            The honeybee genome has substantially fewer protein coding genes (≈ 11 000 genes) than Drosophila melanogaster (≈ 13 500) and Anopheles gambiae (≈ 14 000). Some of the most marked differences occur in three superfamilies encoding xenobiotic detoxifying enzymes. Specifically there are only about half as many glutathione-S-transferases (GSTs), cytochrome P450 monooxygenases (P450s) and carboxyl/cholinesterases (CCEs) in the honeybee. This includes 10-fold or greater shortfalls in the numbers of Delta and Epsilon GSTs and CYP4 P450s, members of which clades have been recurrently associated with insecticide resistance in other species. These shortfalls may contribute to the sensitivity of the honeybee to insecticides. On the other hand there are some recent radiations in CYP6, CYP9 and certain CCE clades in A. mellifera that could be associated with the evolution of the hormonal and chemosensory processes underpinning its highly organized eusociality.
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              Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): a factor in colony loss during overwintering?

              The ectoparasitic mite Varroa destructor (Anderson & Trueman) is the most destructive pest of the honey bee, Apis mellifera L., in Europe and the United States. In temperate zones, the main losses of colonies from the mites occur during colony overwintering. To obtain a deeper knowledge of this phenomenon, we studied the mites' impact on the vitellogenin titer, the total protein stores in the hemolymph, the hemocyte characteristics, and the ecdysteroid titer of adult honey bees. These physiological characteristics are indicators of long-time survival and endocrine function, and we show that they change if bees have been infested by mites during the pupal stage. Compared with noninfested workers, adult bees infested as pupae do not fully develop physiological features typical of long-lived wintering bees. Management procedures designed to kill V. destructor in late autumn may thus fail to prevent losses of colonies because many of the adult bees are no longer able to survive until spring. Beekeepers in temperate climates should therefore combine late autumn management strategies with treatment protocols that keep the mite population at low levels before and during the period when the winter bees emerge.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                23 February 2011
                : 6
                : 2
                : e14720
                Affiliations
                [1]Department of Entomology, Washington State University, Pullman, Washington, United States of America
                INRA - Paris 6 - AgroParisTech, France
                Author notes

                Conceived and designed the experiments: JYW CMA WSS. Performed the experiments: JYW. Analyzed the data: JYW. Contributed reagents/materials/analysis tools: WSS. Wrote the paper: JYW CMA WSS.

                Article
                10-PONE-RA-18658R2
                10.1371/journal.pone.0014720
                3044129
                21373182
                f6bea189-bda1-4511-9896-967ee9f66d30
                Wu 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 May 2010
                : 20 January 2011
                Page count
                Pages: 11
                Categories
                Research Article
                Evolutionary Biology
                Chemistry/Applied Chemistry
                Genetics and Genomics/Population Genetics

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