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Sulfoxaflor exposure reduces bumblebee reproductive success


Intensive agriculture currently relies on pesticides to maximize crop yield1,2. Neonicotinoids are the most widely used insecticides globally3, but increasing evidence of negative impacts on important pollinators4,5,6,7,8,9 and other non-target organisms10 has led to legislative reassessment and created demand for the development of alternative products. Sulfoximine-based insecticides are the most likely successor11, and are either licensed for use or under consideration for licensing in several worldwide markets3, including within the European Union12, where certain neonicotinoids (imidacloprid, clothianidin and thiamethoxam) are now banned from agricultural use outside of permanent greenhouse structures. There is an urgent need to pre-emptively evaluate the potential sub-lethal effects of sulfoximine-based pesticides on pollinators11, because such effects are rarely detected by standard ecotoxicological assessments, but can have major impacts at larger ecological scales13,14,15. Here we show that chronic exposure to the sulfoximine-based insecticide sulfoxaflor, at dosages consistent with potential post-spray field exposure, has severe sub-lethal effects on bumblebee (Bombus terrestris) colonies. Field-based colonies that were exposed to sulfoxaflor during the early growth phase produced significantly fewer workers than unexposed controls, and ultimately produced fewer reproductive offspring. Differences between the life-history trajectories of treated and control colonies first became apparent when individuals exposed as larvae began to emerge, suggesting that direct or indirect effects on a small cohort may have cumulative long-term consequences for colony fitness. Our results caution against the use of sulfoximines as a direct replacement for neonicotinoids. To avoid continuing cycles of novel pesticide release and removal, with concomitant impacts on the environment, a broad evidence base needs to be assessed prior to the development of policy and regulation.

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Fig. 1: The impact of sulfoxaflor exposure on life-history trajectories of bumblebee colonies.
Fig. 2: Male offspring production.

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We thank E. Bailes, J. Bagi, J. Blackwell, A. Folly, C. Martin, A. Samuelson, K. Liu, M. Burke, S. Cobacho Jimenez and E. Wrake for technical assistance in the field and laboratory; Natural England and the Crown Estate for permission to collect bumblebees from Windsor Great Park. H.S. was supported by a Royal Holloway University of London Reid PhD Scholarship and by contributions from High Wickham Beekeeper’s Association. This project has received funding from the European Horizon 2020 research and innovation programme under grant agreement no.773921. E.L. was supported by European Research Council Starting Grant BeeDanceGap (638873).

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Nature thanks R. Paxton, N. E. Raine and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Authors and Affiliations



H.S. conceived the experiment and all authors contributed to the design of the study. H.S. ran the experiments, H.S. and E.L. performed the statistical analysis and all authors contributed to the writing of the manuscript.

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Correspondence to Harry Siviter.

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Extended data figures and tables

Extended Data Fig. 1 Concentrations of sulfoxaflor in forager-collected resources from a USA EPA cotton study.

Mean µg of active ingredient (a.i.) per kg (mean ± s.e.m.) found in the nectar (a, c, e) and pollen (b, d, f) of honeybees foraging on cotton crops sprayed with sulfoxaflor. Note the differences in y-axis scale between graphs, owing to considerably higher concentrations in pollen. Red lines indicate spray application. Dosage: twice over ten days at 0.045 pounds a.i. per acre (a, b); once over ten days at 0.045 pounds a.i. per acre (c, d); twice over ten days at 0.089 pounds a.i. per acre (e, f). The black dotted horizontal line indicates the equivalent amount of sulfoxaflor (5 ppb) that was fed to sulfoxaflor-treated colonies in sucrose in our experiment. Data are means from two hives; number of individual bees sampled is not published27.

Extended Data Fig. 2 Timing of colony life-history events.

ac, The probability of reproductive onset (a), queen survival (b) and colony survival (c) for control (n = 26) and sulfoxaflor-treated (n = 25) colonies (± confidence intervals).

Extended Data Fig. 3 Pollen foraging.

The proportion (mean ± s.e.m.) of foragers returning to the nest with large pollen loads, for control (n = 25) and pesticide-treated (n = 22) colonies (note that not all of the colonies in the experiment had pollen foragers).

Extended Data Fig. 4 Distribution of colonies across the Royal Holloway Campus.

Blue dots indicate control colonies; red dots indicate treated colonies. Grid reference: TQ000706; Imagery © Google, Map Data © 2018 Google.

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Siviter, H., Brown, M.J.F. & Leadbeater, E. Sulfoxaflor exposure reduces bumblebee reproductive success. Nature 561, 109–112 (2018).

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