Exposure to Acetylcholinesterase Inhibitors Alters the Physiology and Motor Function of Honeybees

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 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.

Effects of Sublethal Concentrations of Chlorpyrifos on Olfactory Learning and Memory Performances in Two Bee Species, Apis mellifera and Apis cerana

“…Acetylcholine (ACh) is a potent neurotransmitter during this process (Goldberg et al, 1999). Chlorpyrifos, an important organophosphate, exert its mode of action by inhibiting AChE activity (Williamson et al, 2013). This enzyme cannot hydrolyze ACh and terminate excitatory neurotransmission in the central nervous systems of forager bees exposed to sublethal chlorpyrifos concentrations (Palmer et al, 2013).…”

“…Therefore, the acquisition and retention capacities of chlorpyrifos-treated forager bees were impaired. Chlorpyrifos oxon is a chlorpyrifos metabolite more potent than the parent compound in terms of inhibiting AChE activities (Williamson et al, 2013). Acquisition tests were performed 2 and 24 h after the honey bees were exposed to chlorpyrifos in the test.…”

Toksisitas beberapa jenis fungisida komersial pada serangga penyerbuk, Trigona (Tetragonula) laeviceps Smith

“…Pelepasan ACh secara kontinu mengurangi cadangan neurotransmiter dan akumulasi ACh pada ruang antar sinaps mengganggu transmisi sinyal pada neuromuscular junction sehingga dapat menyebabkan gangguan motorik. Pada lebah Apis mellifera Linnaeus ditemukan bahwa inhibisi AChE menyebabkan gangguan perilaku righting reflex dan gangguan kerja perut yang berakibat pada pengeluaran feses berlebihan (Williamson et al 2013). Gangguan pada perilaku righting reflex sangat berbahaya pada lebah pekerja karena mengurangi kemampuan terbang dan mencari makanan.…”

“…Ketidakberadaan enzim ini akan menyebabkan penumpukan ACh pada ruang sinapstik sehingga selalu mengatifkan reseptor ACh dimana dapat menyebabkan paralisis lalu kematian pada level individu (Krieger 2001). Selain itu, seperti yang telah dijelaskan sebelumnya, inhibisi AChE dapat menyebabkan gangguan perilaku righting reflex dan gangguan kerja perut yang dapat berakibat kematian baik pada tingkatan individu hingga tingkatan koloni (Alaux et al 2010;Williamson et al 2013).…”

Spontaneous honeybee behaviour is altered by persistent organic pollutants

“…Understandably the vast majority of studies examining the sublethal effects of environmental chemicals on honeybee behaviour have focussed on currently used pesticides (Desneux et al 2007). Sublethal doses of pesticides including neonicotinoid, pyrethroid, phenylpyrazole and organophosphate insecticides have been shown to alter honeybee motor activity (Charreton et al 2015; Williamson et al 2013b, 2014), learning and memory, (Decourtye et al 2004; Han et al 2010b; Lambin et al 2001; Williamson et al 2013b), and appetite and foraging behaviour (Colin et al 2004; Dively et al 2015; Han et al 2012, 2010a; Vandame et al 1995). However, currently used agrochemicals are not the only environmental chemicals in honeybee habitats.…”