title: Neonicotinoids target distinct nicotinic acetylcholine receptors and neurons, leading to differential risks to bumblebees.
abstract: There is growing concern over the risk to bee populations from neonicotinoid insecticides and the long-term consequences of reduced numbers of insect pollinators to essential ecosystem services and food security. Our knowledge of the risk of neonicotinoids to bees is based on studies of imidacloprid and thiamethoxam and these findings are extrapolated to clothianidin based on its higher potency at nicotinic acetylcholine receptors. This study addresses the specificity and consequences of all three neonicotinoids to determine their relative risk to bumblebees at field-relevant levels (2.5 ppb). We find compound-specific effects at all levels (individual cells, bees and whole colonies in semi-field conditions). Imidacloprid and clothianidin display distinct, overlapping, abilities to stimulate Kenyon cells, indicating the potential to differentially influence bumblebee behavior. Bee immobility was induced only by imidacloprid, and an increased vulnerability to clothianidin toxicity only occurred following chronic exposure to clothianidin or thiamethoxam. At the whole colony level, only thiamethoxam altered the sex ratio (more males present) and only clothianidin increased queen production. Finally, both imidacloprid and thiamethoxam caused deficits in colony strength, while no detrimental effects of clothianidin were observed. Given these findings, neonicotinoid risk needs to be considered independently for each compound and target species.
authors.affiliation: Centre for Environmental Change and Human Resilience, University of Dundee, Dundee, DD1 9SY.
authors.forename: Christopher
authors.initials: C
authors.lastname: Moffat
authors.affiliation: Centre for Research into Ecological and Environmental Modelling, University of St.Andrews, KY16 9LZ.
authors.forename: Stephen T
authors.initials: ST
authors.lastname: Buckland
authors.affiliation: Centre for Environmental Change and Human Resilience, University of Dundee, Dundee, DD1 9SY.
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: Samson
authors.affiliation: Centre for Environmental Change and Human Resilience, University of Dundee, Dundee, DD1 9SY.
authors.forename: Robin
authors.initials: R
authors.lastname: McArthur
authors.affiliation: Centre for Environmental Change and Human Resilience, University of Dundee, Dundee, DD1 9SY.
authors.forename: Victor
authors.initials: V
authors.lastname: Chamosa Pino
authors.affiliation: Centre for Environmental Change and Human Resilience, University of Dundee, Dundee, DD1 9SY.
authors.forename: Karen A
authors.initials: KA
authors.lastname: Bollan
authors.affiliation: Biomarker and Drug Analysis Core Facility, School of Medicine, University of Dundee, Dundee, DD1 9SY.
authors.forename: Jeffrey T-J
authors.initials: JT
authors.lastname: Huang
authors.affiliation: Centre for Environmental Change and Human Resilience, University of Dundee, Dundee, DD1 9SY.
authors.forename: Christopher N
authors.initials: CN
authors.lastname: Connolly
mesh_terms: D000818:Animals; D001516:Bees / Q000187:drug effects* / Q000502:physiology; D001522:Behavior, Animal / Q000187:drug effects; D001921:Brain / Q000378:metabolism; D002478:Cells, Cultured; D002851:Chromatography, High Pressure Liquid; D006146:Guanidines / Q000032:analysis / Q000633:toxicity; D007306:Insecticides / Q000032:analysis / Q000633:toxicity*; D000073943:Neonicotinoids / Q000032:analysis / Q000633:toxicity*; D009474:Neurons / Q000166:cytology / Q000187:drug effects* / Q000378:metabolism; D009574:Nitro Compounds / Q000032:analysis / Q000633:toxicity; D010078:Oxazines / Q000032:analysis / Q000633:toxicity; D011978:Receptors, Nicotinic / Q000378:metabolism*; D012306:Risk; D012744:Sex Ratio; D053719:Tandem Mass Spectrometry; D000077922:Thiamethoxam; D013844:Thiazoles / Q000032:analysis / Q000633:toxicity
chemical_list: D006146:Guanidines; D007306:Insecticides; D000073943:Neonicotinoids; D009574:Nitro Compounds; D010078:Oxazines; D011978:Receptors, Nicotinic; D013844:Thiazoles; C480342:clothianidin; C082359:imidacloprid; D000077922:Thiamethoxam