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      Neonicotinoids Interfere with Specific Components of Navigation in Honeybees

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          Abstract

          Three neonicotinoids, imidacloprid, clothianidin and thiacloprid, agonists of the nicotinic acetylcholine receptor in the central brain of insects, were applied at non-lethal doses in order to test their effects on honeybee navigation. A catch-and-release experimental design was applied in which feeder trained bees were caught when arriving at the feeder, treated with one of the neonicotinoids, and released 1.5 hours later at a remote site. The flight paths of individual bees were tracked with harmonic radar. The initial flight phase controlled by the recently acquired navigation memory (vector memory) was less compromised than the second phase that leads the animal back to the hive (homing flight). The rate of successful return was significantly lower in treated bees, the probability of a correct turn at a salient landscape structure was reduced, and less directed flights during homing flights were performed. Since the homing phase in catch-and-release experiments documents the ability of a foraging honeybee to activate a remote memory acquired during its exploratory orientation flights, we conclude that non-lethal doses of the three neonicotinoids tested either block the retrieval of exploratory navigation memory or alter this form of navigation memory. These findings are discussed in the context of the application of neonicotinoids in plant protection.

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          Most cited references28

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          A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees.

          Honey bees provide important pollination services to crops and wild plants. The agricultural use of systemic insecticides, such as neonicotinoids, may harm bees through their presence in pollen and nectar, which bees consume. Many studies have tested the effects on honey bees of imidacloprid, a neonicotinoid, but a clear picture of the risk it poses to bees has not previously emerged, because investigations are methodologically varied and inconsistent in outcome. In a meta-analysis of fourteen published studies of the effects of imidacloprid on honey bees under laboratory and semi-field conditions that comprised measurements on 7073 adult individuals and 36 colonies, fitted dose-response relationships estimate that trace dietary imidacloprid at field-realistic levels in nectar will have no lethal effects, but will reduce expected performance in honey bees by between 6 and 20%. Statistical power analysis showed that published field trials that have reported no effects on honey bees from neonicotinoids were incapable of detecting these predicted sublethal effects with conventionally accepted levels of certainty. These findings raise renewed concern about the impact on honey bees of dietary imidacloprid, but because questions remain over the environmental relevance of predominantly laboratory-based results, I identify targets for research and provide procedural recommendations for future studies.
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            Honey bees navigate according to a map-like spatial memory.

            By using harmonic radar, we report the complete flight paths of displaced bees. Test bees forage at a feeder or are recruited by a waggle dance indicating the feeder. The flights are recorded after the bees are captured when leaving the hive or the feeder and are released at an unexpected release site. A sequence of behavioral routines become apparent: (i) initial straight flights in which they fly the course that they were on when captured (foraging bees) or that they learned during dance communication (recruited bees); (ii) slow search flights with frequent changes of direction in which they attempt to "get their bearings"; and (iii) straight and rapid flights directed either to the hive or first to the feeding station and then to the hive. These straight homing flights start at locations all around the hive and at distances far out of the visual catchment area around the hive or the feeding station. Two essential criteria of a map-like spatial memory are met by these results: bees can set course at any arbitrary location in their familiar area, and they can choose between at least two goals. This finding suggests a rich, map-like organization of spatial memory in navigating honey bees.
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              The flight paths of honeybees recruited by the waggle dance.

              In the 'dance language' of honeybees, the dancer generates a specific, coded message that describes the direction and distance from the hive of a new food source, and this message is displaced in both space and time from the dancer's discovery of that source. Karl von Frisch concluded that bees 'recruited' by this dance used the information encoded in it to guide them directly to the remote food source, and this Nobel Prize-winning discovery revealed the most sophisticated example of non-primate communication that we know of. In spite of some initial scepticism, almost all biologists are now convinced that von Frisch was correct, but what has hitherto been lacking is a quantitative description of how effectively recruits translate the code in the dance into flight to their destinations. Using harmonic radar to record the actual flight paths of recruited bees, we now provide that description.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                19 March 2014
                : 9
                : 3
                : e91364
                Affiliations
                [1 ]Institut für Bienenkunde Oberursel, Polytechnische Gesellschaft Frankfurt am Main, Fachbereich Biowissenschaften, Goethe-Universität, Frankfurt am Main, Germany
                [2 ]Netzwerk Blühende Landschaften Fischermühle, Rosenfeld, Germany
                [3 ]Institut für Biologie, Freie Universität Berlin, Berlin, Germany
                Colorado State University, United States of America
                Author notes

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

                Conceived and designed the experiments: RM JF BG. Performed the experiments: TM A-KS UG RM JF. Analyzed the data: JF UG. Wrote the paper: JF RM BG.

                Article
                PONE-D-13-45395
                10.1371/journal.pone.0091364
                3960126
                24646521
                e48221a4-8579-40df-b244-80850d8b38b3
                Copyright @ 2014

                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
                : 11 November 2013
                : 8 February 2014
                Page count
                Pages: 10
                Funding
                The studies were financially supported by the following institutions: Deutsche Forschungsgemeinschaft (DFG grant ME 365/34-2 to RM), Hertie Gemeinnützige Stiftung (RM), Dr. Klaus Tschira Stiftung (RM, UG), and by the EU and the Land Hessen, Hessisches Ministerium für Umwelt, Ernährung, Landwirtschaft und Verbraucherschutz (BG). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Agriculture
                Agrochemicals
                Biochemistry
                Neurochemistry
                Neurotransmitters
                Acetylcholine
                Neurochemicals
                Proteins
                Transmembrane Receptors
                Acetylcholine Receptors
                Nicotinic Acetylcholine Receptors
                Ecology
                Chemical Ecology
                Neuroscience
                Behavioral Neuroscience
                Learning and Memory
                Neuroethology
                Toxicology
                Neurotoxicology
                Toxic Agents
                Zoology
                Animal Behavior
                Entomology
                Ecology and Environmental Sciences

                Uncategorized
                Uncategorized

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