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

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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.

At a glance


  1. Worker production and mortality.
    Figure 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 nest 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). Data shown on the x axis indicate the number of days since the start of the experiment (day 1 = 24h after the start of experimentation). M treatment includes the two collapsed colonies. *P0.05, **P0.01, ***P0.001 (comparison with control).

  2. Foraging performance.
    Figure 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 (pollen) foraging bout for each worker per colony (column), and mean duration of successful foraging bouts per worker per colony (filled-circles) (n = 147 foragers). n colonies shown in top left corner of columns. Significant differences from control treatment for column data are shown at the bases of columns, and for filled-circle data are shown above columns (a and c). #P0.1, *P0.05, **P0.01, ***P0.001 (comparison with control).

  3. Overall worker losses.
    Figure 3: Overall worker losses.

    Mean (±s.e.m.) overall percentage of workers lost per colony, including workers lost outside (below the dashed line) and worker mortality (dead workers found in nest box; above the dashed line), during the 4-week experiment. n = 40 colonies. #P0.1, **P0.01, ***P0.001 (comparison with control).


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  1. School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

    • Richard J. Gill,
    • Oscar Ramos-Rodriguez &
    • Nigel E. Raine


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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The authors declare no competing financial interests.

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  1. Supplementary Information (1.4M)

    This file contains Supplementary Methods, Supplementary Analyses and Results, Supplementary References, Supplementary Figures 1-8, Supplementary Tables 1-2 and Supplementary Box 1.

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