Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees

Journal name:
Nature
Volume:
528,
Pages:
548–550
Date published:
DOI:
doi:10.1038/nature16167
Received
Accepted
Published online

Recent concern over global pollinator declines has led to considerable research on the effects of pesticides on bees1, 2, 3, 4, 5. Although pesticides are typically not encountered at lethal levels in the field, there is growing evidence indicating that exposure to field-realistic levels can have sublethal effects on bees, affecting their foraging behaviour1, 6, 7, homing ability8, 9 and reproductive success2, 5. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants10, 11, 12, but until now research on pesticide effects has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence to our knowledge that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Bumblebee colonies exposed to a neonicotinoid pesticide provided lower visitation rates to apple trees and collected pollen less often. Most importantly, these pesticide-exposed colonies produced apples containing fewer seeds, demonstrating a reduced delivery of pollination services. Our results also indicate that reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour, but most likely due to effects at the colony level. These findings show that pesticide exposure can impair the ability of bees to provide pollination services, with important implications for both the sustained delivery of stable crop yields and the functioning of natural ecosystems.

At a glance

Figures

  1. Effects of pesticide treatment on colony-level behaviour.
    Figure 1: Effects of pesticide treatment on colony-level behaviour.

    a, b, Visitation rates provided by colonies to Scrumptious apple flowers (number of visits per flower per minute) (a) and number of foraging trips from which bees returned carrying pollen (b), from colonies exposed to different pesticide treatments. Eight colonies were observed per treatment group, and means ± s.e.m. are shown, *P < 0.05. NS, not significant. Results from statistical models are given in Extended Data Table 1.

  2. Effects of pesticide treatment on fruit and seed set.
    Figure 2: Effects of pesticide treatment on fruit and seed set.

    a, b, The change in proportion of fruit set for trees (48 trees in total, 16 per treatment) pollinated by colonies exposed to different pesticide treatments measured early (May) and late (September), which represents fruit abortion level (a), and number of seeds produced per apple (134 apples in total; 53 in control, 46 in 2.4 ppb and 35 in 10 ppb pesticide treatments) pollinated by colonies exposed to different pesticide treatments (b). Eight colonies were observed per treatment group, and means ± s.e.m. are shown, *P < 0.05, † indicates a difference of P = 0.06 between control and 10 ppb. NS, not significant. Results from statistical models are given in Extended Data Table 1.

  3. Effects of pesticide treatment on individual bee behaviour.
    Figure 3: Effects of pesticide treatment on individual bee behaviour.

    a, b, Time spent foraging per foraging trip (seconds; n = 68 bees) (a) and number of switches between Scrumptious and Everest apple varieties (n = 93 bees) (b) for individual bees exposed to different pesticide treatments. Means ± s.e.m. are shown, *P < 0.05, † indicates a difference of P = 0.06 between control and 2.4 ppb. NS, not significant. Results from statistical models are given in Extended Data Table 2.

  4. An example of the experimental setup at the Sonning Farm field site.
    Extended Data Fig. 1: An example of the experimental setup at the Sonning Farm field site.

    Experimental pollinator exclusion cages containing a bumblebee colony (located in the corner of the cage) and potted experimental apple trees are shown. Photos: D.A.S.

  5. An experimental bumblebee (Bombus terrestris) worker visiting an apple flower (left), and an example of an apple produced from a marked (yellow cable tie) apple flower (right; Scrumptious variety).
    Extended Data Fig. 2: An experimental bumblebee (Bombus terrestris) worker visiting an apple flower (left), and an example of an apple produced from a marked (yellow cable tie) apple flower (right; Scrumptious variety).

    Photos: D.A.S. and C. L. Truslove.

Tables

  1. Results from the colony-level experiment
    Extended Data Table 1: Results from the colony-level experiment
  2. Results from the individual-level experiment
    Extended Data Table 2: Results from the individual-level experiment

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Author information

Affiliations

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

    • Dara A. Stanley &
    • Nigel E. Raine
  2. Centre for Agri-Environmental Research, School of Agriculture, Policy and Development, University of Reading, Reading RG6 6AR, UK

    • Michael P. D. Garratt,
    • Jennifer B. Wickens,
    • Victoria J. Wickens &
    • Simon G. Potts
  3. School of Environmental Sciences, University of Guelph, Guelph, Ontario N1G 2W1, Canada

    • Nigel E. Raine

Contributions

D.A.S. and N.E.R. conceived the project, D.A.S., N.E.R. and M.P.D.G. designed the research, D.A.S., J.B.W and V.J.W. carried out the research, D.A.S., N.E.R., M.P.D.G. and S.G.P. contributed equipment for the research, D.A.S. analysed the data, all authors were involved in writing the manuscript.

Competing financial interests

The authors declare no competing financial interests.

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Comments

  1. Report this comment #67309

    Chris Exley said:

    I am concerned that there is now a burgeoning tendency to adopt a 'one toxin fits all' approach to our understanding of how environmental toxins are influencing pollination.

    No evidence is presented herein that bees accumulated any pesticide only that exposure to the pesticide in an artificial sugar solution over several days influenced their subsequent 'pollinator' behaviour or services delivered.

    We have shown that the pupae of naturally-foraging bumble bees contain very high amounts of the neurotoxin, aluminium ( http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0127665). We have speculated that aluminium could be a contributor to the decline in pollinator activities through its known neurotoxicity and synergisms with other environmental pollutants such as pesticides.

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