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

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Abstract
Chronic exposure of bumblebees to two pesticides (a neonicotinoid and a pyrethroid) independently and in combination, at concentrations approximating field-level exposure, impairs natural foraging behaviour and increases worker mortality, with knock-on effects for brood development and colony success. Exposure to neonicotinoid pesticides is known to influence bee behaviour, and could be a key factor in current bee declines. It has not been possible to establish a mechanistic link between individual and colony effects, but this study demonstrates a direct link between detrimental behavioural effects and field-level pesticide exposure — to neonicotinoid and pyrethroid — in individual worker bumblebees, and consequent impacts on colony development and survival. The pesticides reduce the effectiveness of foraging behaviour, with knock-on effects on brood care and colony productivity. 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.