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Chronic exposure to imidacloprid increases neuronal vulnerability to mitochondrial dysfunction in the bumblebee (Bombus terrestris)

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moffat2015fasebj2112.pdf (965.6Kb)
Date
05/2015
Author
Moffat, C.
Goncalves Pacheco, J.
Sharpe, S.
Samson, A.J.
Bollan, K.A.
Huang, J.
Buckland, Stephen Terrence
Connolly, C.N.
Keywords
Nicotinic acetylcholine receptors
Neuronal culture
QH301 Biology
QA Mathematics
NDAS
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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 (Bombusterrestris 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.
Citation
Moffat , C , Goncalves Pacheco , J , Sharpe , S , Samson , A J , Bollan , K A , Huang , J , Buckland , S T & Connolly , C N 2015 , ' Chronic exposure to imidacloprid increases neuronal vulnerability to mitochondrial dysfunction in the bumblebee ( Bombus terrestris ) ' , FASEB Journal , vol. 29 , no. 5 , pp. 2112-2119 . https://doi.org/10.1096/fj.14-267179
Publication
FASEB Journal
Status
Peer reviewed
DOI
https://doi.org/10.1096/fj.14-267179
ISSN
0892-6638
Type
Journal article
Rights
© The author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution 4.0 International (CC BY 4.0) (http://creativecommons.org/licenses/by/4.0/) which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Description
This work was funded jointly by the Biotechnology and Biological Sciences Research Council, the Department for Environment, Food and Rural Affairs, the Natural Environment Research Council, the Scottish Government, and The Wellcome Trust, under the Insect Pollinators Initiative (United Kingdom) Grant BB/ 1000313/1 (to C.N.C.).
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  • University of St Andrews Research
URI
http://hdl.handle.net/10023/6986

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