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 24 h. Using an assay for locomotion in bees, we scored walking, stopped, grooming, and upside down behavior continuously for 15 min. At a 10 nM 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 1 μM 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.
Keywords: honeybee, honey bee, acetylcholinesterase inhibitor, acetylcholine, pesticide, motor function, coumaphos, aldicarb
Citation: Williamson SM, Moffat C, Gomersall MAE, Saranzewa N, Connolly CN and Wright GA (2013) Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees. Front. Physio. 4:13. doi: 10.3389/fphys.2013.00013
Received: 18 September 2012; Accepted: 14 January 2013;
Published online: 05 February 2013.
Edited by:Monique Gauthier, University Paul Sabatier Toulouse 3, France
Reviewed by:Laura Ann Miller, University of North Carolina at Chapel Hill, USA
Copyright: © 2013 Williamson, Moffat, Gomersall, Saranzewa, Connolly and Wright. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.
*Correspondence: Geraldine A. Wright, Institute of Neuroscience, Newcastle University, Henry Wellcome Building, Newcastle upon Tyne NE1 7RU, UK. e-mail: firstname.lastname@example.org