Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees

Sally M. Williamson, Christopher Moffat, Martha A. E. Gomersall, Nastja Saranzewa, Christopher N. Connolly, Geraldine A. Wright

    Research output: Contribution to journalArticle

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    Abstract

    Cholinergic signaling is fundamental to neuromuscular function in most organisms. Sub-lethal doses of neurotoxic pesticides that target cholinergic signaling can alter the behavior of insects in subtle ways; their influence on non-target organisms may not be readily apparent in simple mortality studies. Beneficial arthropods such as honeybees perform sophisticated behavioral sequences during foraging that, if influenced by pesticides, could impair foraging success and reduce colony health. Here, we investigate the behavioral effects on honeybees of exposure to a selection of pesticides that target cholinergic signaling by inhibiting acetylcholinesterase (AChE). To examine how continued exposure to AChE inhibitors affected motor function, we fed adult foraging worker honeybees sub-lethal concentrations of these compounds in sucrose solution for 24h. Using an assay for locomotion in bees, we scored walking, stopped, grooming, and upside down behavior continuously for 15min. At a 10nM concentration, all the AChE inhibitors caused similar effects on behavior, notably increased grooming activity and changes in the frequency of bouts of behavior such as head grooming. Coumaphos caused dose-dependent effects on locomotion as well as grooming behavior, and a 1µM concentration of coumaphos induced symptoms of malaise such as abdomen grooming and defecation. Biochemical assays confirmed that the four compounds we assayed (coumaphos, aldicarb, chlorpyrifos, and donepezil) or their metabolites acted as AChE inhibitors in bees. Furthermore, we show that transcript expression levels of two honeybee AChE inhibitors were selectively upregulated in the brain and in gut tissues in response to AChE inhibitor exposure. The results of our study imply that the effects of pesticides that rely on this mode of action have subtle yet profound effects on physiological effects on behavior that could lead to reduced survival.
    Original languageEnglish
    Article number13
    JournalFrontiers in Physiology
    Volume4
    DOIs
    Publication statusPublished - 5 Feb 2013

    Fingerprint

    Grooming
    Cholinesterase Inhibitors
    Coumaphos
    Pesticides
    Cholinergic Agents
    Bees
    Locomotion
    Aldicarb
    Chlorpyrifos
    Defecation
    Arthropods
    Acetylcholinesterase
    Abdomen
    Walking
    Insects
    Sucrose
    Head
    Mortality
    Health
    Brain

    Cite this

    Williamson, Sally M. ; Moffat, Christopher ; Gomersall, Martha A. E. ; Saranzewa, Nastja ; Connolly, Christopher N. ; Wright, Geraldine A. / Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees. In: Frontiers in Physiology. 2013 ; Vol. 4.
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    abstract = "Cholinergic signaling is fundamental to neuromuscular function in most organisms. Sub-lethal doses of neurotoxic pesticides that target cholinergic signaling can alter the behavior of insects in subtle ways; their influence on non-target organisms may not be readily apparent in simple mortality studies. Beneficial arthropods such as honeybees perform sophisticated behavioral sequences during foraging that, if influenced by pesticides, could impair foraging success and reduce colony health. Here, we investigate the behavioral effects on honeybees of exposure to a selection of pesticides that target cholinergic signaling by inhibiting acetylcholinesterase (AChE). To examine how continued exposure to AChE inhibitors affected motor function, we fed adult foraging worker honeybees sub-lethal concentrations of these compounds in sucrose solution for 24h. Using an assay for locomotion in bees, we scored walking, stopped, grooming, and upside down behavior continuously for 15min. At a 10nM concentration, all the AChE inhibitors caused similar effects on behavior, notably increased grooming activity and changes in the frequency of bouts of behavior such as head grooming. Coumaphos caused dose-dependent effects on locomotion as well as grooming behavior, and a 1µM concentration of coumaphos induced symptoms of malaise such as abdomen grooming and defecation. Biochemical assays confirmed that the four compounds we assayed (coumaphos, aldicarb, chlorpyrifos, and donepezil) or their metabolites acted as AChE inhibitors in bees. Furthermore, we show that transcript expression levels of two honeybee AChE inhibitors were selectively upregulated in the brain and in gut tissues in response to AChE inhibitor exposure. The results of our study imply that the effects of pesticides that rely on this mode of action have subtle yet profound effects on physiological effects on behavior that could lead to reduced survival.",
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    Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees. / Williamson, Sally M.; Moffat, Christopher; Gomersall, Martha A. E.; Saranzewa, Nastja; Connolly, Christopher N.; Wright, Geraldine A.

    In: Frontiers in Physiology, Vol. 4, 13, 05.02.2013.

    Research output: Contribution to journalArticle

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