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Combined pesticide exposure severely affects individual- and colony-level traits in bees


Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production1,2,3. Bees contribute approximately 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations 4,5,6. Recent studies have implicated the role of pesticides in these declines, as exposure to these chemicals has been associated with changes in bee behaviour7,8,9,10,11 and reductions in colony queen production12. However, the key link between changes in individual behaviour and the consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of many individual workers. Thus, although field-level pesticide concentrations can have subtle or sublethal effects at the individual level8, it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means that bees are exposed to numerous pesticides when foraging13,14,15, yet the possible combinatorial effects of pesticide exposure have rarely been investigated16,17. Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concentrations that could approximate field-level exposure impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success. We found that worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with observed knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail.

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Figure 1: Worker production and mortality.
Figure 2: Foraging performance.
Figure 3: Overall worker losses.


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We thank M.J.F. Brown, M. Clook, J. Culverhouse, A. Dixon, M. Fürst, D. Garthwaite, A. Horsell, V. Jansen and I. Pedroso-Rovira for comments and technical assistance, and Syngenta Bioline Bees for supplying colonies. The study was supported by the Insect Pollinator Initiative (funded under the auspices of the Living with Environmental Change programme, Biotechnology and Biological Sciences Research Council (BBSRC), Wellcome Trust, Scottish Government, Department for Environment, Food and Rural Affairs (DEFRA) and Natural Environment Research Council (NERC): grant BB/I000178/1).

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R.J.G., O.R.-R. and N.E.R. carried out the experiment; R.J.G. and N.E.R. designed the experiment and wrote the paper; N.E.R. conceived the project.

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Correspondence to Richard J. Gill or Nigel E. Raine.

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The authors declare no competing financial interests.

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This file contains Supplementary Methods, Supplementary Analyses and Results, Supplementary References, Supplementary Figures 1-8, Supplementary Tables 1-2 and Supplementary Box 1. (PDF 1495 kb)

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Gill, R., Ramos-Rodriguez, O. & Raine, N. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108 (2012).

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