title: Chronic exposure to neonicotinoids increases neuronal vulnerability to mitochondrial dysfunction in the bumblebee (Bombus terrestris).
abstract: The global decline in the abundance and diversity of insect pollinators could result from habitat loss, disease, and pesticide exposure. The contribution of the neonicotinoid insecticides (e.g., clothianidin and imidacloprid) to this decline is controversial, and key to understanding their risk is whether the astonishingly low levels found in the nectar and pollen of plants is sufficient to deliver neuroactive levels to their site of action: the bee brain. Here we show that bumblebees (Bombus terrestris audax) fed field levels [10 nM, 2.1 ppb (w/w)] of neonicotinoid accumulate between 4 and 10 nM in their brains within 3 days. Acute (minutes) exposure of cultured neurons to 10 nM clothianidin, but not imidacloprid, causes a nicotinic acetylcholine receptor-dependent rapid mitochondrial depolarization. However, a chronic (2 days) exposure to 1 nM imidacloprid leads to a receptor-dependent increased sensitivity to a normally innocuous level of acetylcholine, which now also causes rapid mitochondrial depolarization in neurons. Finally, colonies exposed to this level of imidacloprid show deficits in colony growth and nest condition compared with untreated colonies. These findings provide a mechanistic explanation for the poor navigation and foraging observed in neonicotinoid treated bumblebee colonies.
authors: *Medical Research Institute, University of Dundee, Dundee, United Kingdom; and Centre for Research into Ecological and Environmental Modelling, University of St. Andrews, St. Andrews, United Kingdom.
authors: Christopher
authors: C
authors: Moffat
authors: *Medical Research Institute, University of Dundee, Dundee, United Kingdom; and Centre for Research into Ecological and Environmental Modelling, University of St. Andrews, St. Andrews, United Kingdom.
authors: Joao Goncalves
authors: JG
authors: Pacheco
authors: *Medical Research Institute, University of Dundee, Dundee, United Kingdom; and Centre for Research into Ecological and Environmental Modelling, University of St. Andrews, St. Andrews, United Kingdom.
authors: Sheila
authors: S
authors: Sharp
authors: *Medical Research Institute, University of Dundee, Dundee, United Kingdom; and Centre for Research into Ecological and Environmental Modelling, University of St. Andrews, St. Andrews, United Kingdom.
authors: Andrew J
authors: AJ
authors: Samson
authors: *Medical Research Institute, University of Dundee, Dundee, United Kingdom; and Centre for Research into Ecological and Environmental Modelling, University of St. Andrews, St. Andrews, United Kingdom.
authors: Karen A
authors: KA
authors: Bollan
authors: *Medical Research Institute, University of Dundee, Dundee, United Kingdom; and Centre for Research into Ecological and Environmental Modelling, University of St. Andrews, St. Andrews, United Kingdom.
authors: Jeffrey
authors: J
authors: Huang
authors: *Medical Research Institute, University of Dundee, Dundee, United Kingdom; and Centre for Research into Ecological and Environmental Modelling, University of St. Andrews, St. Andrews, United Kingdom.
authors: Stephen T
authors: ST
authors: Buckland
authors: *Medical Research Institute, University of Dundee, Dundee, United Kingdom; and Centre for Research into Ecological and Environmental Modelling, University of St. Andrews, St. Andrews, United Kingdom c.n.connolly@dundee.ac.uk.
authors: Christopher N
authors: CN
authors: Connolly
mesh_terms: D000110:Acetylcholinesterase / Q000378:metabolism; D000818:Animals; D017209:Apoptosis / Q000187:drug effects; D001516:Bees; D001921:Brain / Q000187:drug effects / Q000473:pathology*; D049109:Cell Proliferation / Q000187:drug effects; D002478:Cells, Cultured; D002853:Chromatography, Liquid; D006146:Guanidines / Q000633:toxicity*; D007093:Imidazoles / Q000633:toxicity*; D007306:Insecticides / Q000633:toxicity*; D007553:Isotope Labeling; D053078:Membrane Potential, Mitochondrial / Q000187:drug effects; D008928:Mitochondria / Q000187:drug effects / Q000473:pathology*; D000073943:Neonicotinoids; D009474:Neurons / Q000187:drug effects / Q000473:pathology*; D009574:Nitro Compounds / Q000633:toxicity*; D019032:Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization; D013844:Thiazoles / Q000633:toxicity*
chemical_list: D006146:Guanidines; D007093:Imidazoles; D007306:Insecticides; D000073943:Neonicotinoids; D009574:Nitro Compounds; D013844:Thiazoles; C480342:clothianidin; C082359:imidacloprid; D000110:Acetylcholinesterase
keywords: neuronal culture; nicotinic acetylcholine receptors
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