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 production. Bees contribute approximately 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations . Recent studies have implicated the role of pesticides in these declines, as exposure to these chemicals has been associated with changes in bee behaviour and reductions in colony queen production. 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 level, 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 foraging, yet the possible combinatorial effects of pesticide exposure have rarely been investigated. 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.

Fig. 1

Worker production and mortality. A) Mean (±s.e.m.) number of workers per colony that eclosed by the end of the experiment. B) Mean percentage of workers per colony found dead inside the next-box by the end of the experiment. C) Colony growth shown by daily counts of the cumulative number of workers eclosed minus the cumulative number of workers found dead (mean (±s.e.m.) per colony). Control=filled circle (n=10), I=open triangle (n=10), LC=filled square (n=10), M=open diamond (n=10). M treatment includes the two collapsed colonies. Asterisks indicate a significant treatment difference from Control (p-value: 0.1^■, 0.05, * 0.01, ** 0.001, ***).

Fig. 2

Foraging performance. A) Mean (±s.e.m.) number of foragers per colony (column), and foraging bouts per worker per colony (filled circles: n=259 foragers). B) Mean pollen score per worker per colony for all observed foraging bouts (n=228 foragers). C) Mean pollen score per successful foraging bout for each worker per colony (column), and mean duration of successful foraging bouts per worker per colony (filled circles) (n=147 foragers). Significant differences from Control treatment for column data shown at base of columns, and for filled circle data shown above columns (panels A and C). n colonies shown in top left corner of columns.

Fig. 3

Overall worker losses (n=40 colonies). Mean (±s.e.m.) overall percentage of workers lost per colony, including workers lost outside (below dashed line) and worker mortality (dead workers found in nest-box; above dashed line), during the 4-week experiment.