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

Abstract

Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production1-3. Bees contribute around 80% of insect pollination, so it is imperative we understand and mitigate the causes of current declines4-6. Recent studies have implicated the role of pesticides as exposure to these chemicals has been associated with changes in bee behaviour7-11 and reductions in colony queen production12. However the key link between changes in individual behaviour and consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of numerous individual workers. So whilst field-level pesticide concentrations can have a subtle/sublethal effect at the individual level8, it is not known whether bee societies can buffer such effects or if it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means bees are exposed to numerous pesticides when foraging13-15, 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 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.