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      Acute exposure to a sublethal dose of imidacloprid and coumaphos enhances olfactory learning and memory in the honeybee Apis mellifera

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          Abstract

          The decline of honeybees and other pollinating insects is a current cause for concern. A major factor implicated in their decline is exposure to agricultural chemicals, in particular the neonicotinoid insecticides such as imidacloprid. Honeybees are also subjected to additional chemical exposure when beekeepers treat hives with acaricides to combat the mite Varroa destructor. Here, we assess the effects of acute sublethal doses of the neonicotinoid imidacloprid, and the organophosphate acaricide coumaphos, on honey bee learning and memory. Imidacloprid had little effect on performance in a six-trial olfactory conditioning assay, while coumaphos caused a modest impairment. We report a surprising lack of additive adverse effects when both compounds were administered simultaneously, which instead produced a modest improvement in learning and memory.

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          Most cited references39

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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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            Classical conditioning of proboscis extension in honeybees (Apis mellifera).

            Extension of the proboscis was conditioned in restrained honeybees with odor as the conditioned stimulus (CS) and sucrose solution--delivered to the antenna (to elicit extension of the proboscis) and then to the proboscis itself--as the unconditioned stimulus (US). In a first series of experiments, acquisition was found to be very rapid, both in massed and in spaced trials; its associative basis was established by differential conditioning and by an explicitly unpaired control procedure (which produced marked resistance to acquisition in subsequent paired training); and both extinction and spontaneous recovery in massed trials were demonstrated. In a series of experiments on the nature of the US, eliminating the proboscis component was found to lower the asymptotic level of performance, whereas eliminating the antennal component was without effect; reducing the concentration of sucrose from 20% to 7% slowed acquisition but did not lower the asymptotic level of performance; and second-order conditioning was demonstrated. In a series of experiments on the role of the US, an omission contingency designed to eliminate adventitious response-reinforcer contiguity was found to have no adverse effect on acquisition. In a series of experiments designed to analyze the resistance to acquisition found after explicitly unpaired training in the first experiments, no significant effect was found of prior exposure either to the CS alone or to the US alone, although the unpaired procedure again produced substantial resistance that was shown to be due to inhibition rather than to inattention; extinction after paired training was found to be facilitated by unpaired presentations of the US. The relation between these results for honeybees and those of analogous experiments with vertebrates is considered.
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              Sub-Lethal Effects of Pesticide Residues in Brood Comb on Worker Honey Bee (Apis mellifera) Development and Longevity

              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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                Author and article information

                Contributors
                sally.williamson@ncl.ac.uk
                Journal
                Invert Neurosci
                Invert. Neurosci
                Invertebrate Neuroscience
                Springer-Verlag (Berlin/Heidelberg )
                1354-2516
                1439-1104
                17 November 2012
                17 November 2012
                June 2013
                : 13
                : 1
                : 63-70
                Affiliations
                [ ]Faculty of Medical Sciences, Centre for Behaviour and Evolution, Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, NE1 7RU UK
                [ ]School of Biology, Newcastle University, Newcastle upon Tyne, NE1 7RU UK
                Article
                144
                10.1007/s10158-012-0144-7
                3672510
                23160709
                d7688500-f8f1-42bd-97f7-b64d96940ce9
                © The Author(s) 2012
                History
                : 8 October 2012
                : 5 November 2012
                Categories
                Original Paper
                Custom metadata
                © Springer-Verlag Berlin Heidelberg 2013

                Neurosciences
                apis mellifera,olfactory learning,imidacloprid,coumaphos,pesticide
                Neurosciences
                apis mellifera, olfactory learning, imidacloprid, coumaphos, pesticide

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