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.
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We thank technicians at the University of Reading for assistance in apple collection and seed counting, and E. van Leeuwen and colleagues at Royal Holloway University of London for useful discussions. This study was supported by UK Insect Pollinators Initiative grants BB/I000178/1 awarded to N.E.R. and BB/1000348/1 awarded to S.G.P. (funded jointly by the Living with Environmental Change programme, Biotechnology and Biological Sciences Research Council (BBSRC), Wellcome Trust, Scottish Government, Department for Environment, Food and Rural Affairs (Defra) and Natural Environment Research Council (NERC)). N.E.R. is supported as the Rebanks Family Chair in Pollinator Conservation by The W. Garfield Weston Foundation.
The authors declare no competing financial interests.
Extended data figures and tables
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.
Extended Data Figure 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.
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Stanley, D., Garratt, M., Wickens, J. et al. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528, 548–550 (2015). https://doi.org/10.1038/nature16167
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