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Seed coating with a neonicotinoid insecticide negatively affects wild bees

Naturevolume 521, pages77–80 (2015)Cite this article

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Abstract

Understanding the effects of neonicotinoid insecticides on bees is vital because of reported declines in bee diversity and distribution1,2,3 and the crucial role bees have as pollinators in ecosystems and agriculture4. Neonicotinoids are suspected to pose an unacceptable risk to bees, partly because of their systemic uptake in plants5, and the European Union has therefore introduced a moratorium on three neonicotinoids as seed coatings in flowering crops that attract bees6. The moratorium has been criticized for being based on weak evidence7, particularly because effects have mostly been measured on bees that have been artificially fed neonicotinoids8,9,10,11. Thus, the key question is how neonicotinoids influence bees, and wild bees in particular, in real-world agricultural landscapes11,12,13. Here we show that a commonly used insecticide seed coating in a flowering crop can have serious consequences for wild bees. In a study with replicated and matched landscapes, we found that seed coating with Elado, an insecticide containing a combination of the neonicotinoid clothianidin and the non-systemic pyrethroid β-cyfluthrin, applied to oilseed rape seeds, reduced wild bee density, solitary bee nesting, and bumblebee colony growth and reproduction under field conditions. Hence, such insecticidal use can pose a substantial risk to wild bees in agricultural landscapes, and the contribution of pesticides to the global decline of wild bees1,2,3 may have been underestimated. The lack of a significant response in honeybee colonies suggests that reported pesticide effects on honeybees cannot always be extrapolated to wild bees.

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Figure 1: Paired design with replicated landscapes.
Figure 2: Bee density and reproduction.
Figure 3: Bumblebee colony development.

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Acknowledgements

We thank the farmers for collaboration, the project group for feedback, A. Gunnarson for farmer contacts and seeds, M. Ahlström Olsson and Lindesro AB for bumblebee colonies, A. Andersson and C. Du Rietz for examining bumblebee colonies, B. Andréasson, T. Carling and A. Andersson for producing and assessing honeybee colonies, J. Kreuger for discussions on pesticide quantification, and M. Stjernman for extracting land use information. Funding was provided by the Swedish Civil Contingencies Agency to R.B., I.F., T.R.P. and H.G.S., by the Carl Tryggers Foundation for Scientific Research, the Royal Physiographic Society, and the Swedish Research Council (330-2014-6439) to M.R, and by Formas to H.G.S. and R.B.

Author information

Authors and Affiliations

  1. Department of Biology, Lund University, Lund, 223 62, Sweden

    Maj Rundlöf, Georg K. S. Andersson, Veronica Hederström, Johanna Yourstone & Henrik G. Smith

  2. Lund University, Centre for Environmental and Climate Research, Lund, 223 62, Sweden

    Georg K. S. Andersson, Lina Herbertsson, Björn K. Klatt & Henrik G. Smith

  3. Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, 750 07, Sweden

    Riccardo Bommarco & Ingemar Fries

  4. Department of Aquatic Sciences and Assessment, Swedish University of Agricultural Sciences, Uppsala, 750 07, Sweden

    Ove Jonsson

  5. Swedish University of Agricultural Sciences, Centre for Chemical Pesticides, Uppsala, 750 07, Sweden

    Ove Jonsson

  6. Swedish Board of Agriculture, Jönköping, 551 82, Sweden

    Thorsten R. Pedersen

Authors
  1. Maj Rundlöf
  2. Georg K. S. Andersson
  3. Riccardo Bommarco
  4. Ingemar Fries
  5. Veronica Hederström
  6. Lina Herbertsson
  7. Ove Jonsson
  8. Björn K. Klatt
  9. Thorsten R. Pedersen
  10. Johanna Yourstone
  11. Henrik G. Smith

Contributions

R.B., I.F., T.R.P. and H.G.S. conceived the project. M.R. designed the study, coordinated the work, analysed the data, and prepared the manuscript. G.K.S.A., V.H., L.H., B.K.K. and J.Y. collected the data. O.J. quantified the pesticide residues. All authors contributed to the interpretation of results and writing of the manuscript.

Corresponding author

Correspondence toMaj Rundlöf.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1O. bicornis emergence andB. terrestris colonies.

a, Mean (± 95% confidence limits) proportion emergence ofO. bicornis from cocoons in relation to treatment (control or insecticide seed coating), with higher emergence for males than females (generalized linear mixed model, binomial error distribution, logit link;F1, 14 = 14.97,P = 0.0017), no difference between treatments (F1, 7 = 0.71,P = 0.43) and no interaction (F1, 14 = 0.01,P = 0.94).n = 8 fields per treatment, with 12 female and 15 male cocoons at each field. Photos (with permission; Morgan Boch): left, emergedO. bicornis cocoon; right,O. bicornis female at a trap nests filled with cardboard nest tubes.b, Mean (± 95% confidence limits) weight ofB. terrestris colonies at placement at the fields in relation to treatment (linear mixed model,F1, 7 = 0.99,P = 0.35).n = 8 fields per treatment, with six colonies at each field. Photos (M.R.): left,B. terrestris worker foraging in the oilseed rape; right, house containing threeB. terrestris colonies. Means and confidence limits in panelsa andb are based on back-transformed, model-estimated least square means.c,B. terrestris silk cocoon width distribution of all cocoons in four colonies (two from two different control fields and two from two different fields with insecticide seed treatment) initially examined to separate between queen and worker/male cocoons. Dashed vertical line indicates selected cut-off width at 12 mm (the lowest value between the two peaks), with queens larger (or equal) and workers/males smaller. Photo (M.R.):B. terrestris colony under examination.

Extended Data Figure 2 Power curves for honeybee colony strength.

a,b, Relationship between power and effect size estimated for the honeybee model (Extended Data Table 6), with effect size expressed as the difference in honeybee colony strength (number of bees per colony) (a) and the percentage change in colony strength (b) between colonies at control fields and at fields with insecticide seed coating after placement at the oilseed rape fields. Grey reference lines indicate a power of 0.8 and the corresponding effect size.

Extended Data Table 1 2013 field size and 2011 and 2013 land use in the landscapes surrounding (radius = 2 km) the oilseed rape
Extended Data Table 2 Phenology (date, BBCH33 and flower cover) in the oilseed rape fields and delivery, placement and survey* of bees
Extended Data Table 3 Use of plant protection products in the oilseed rape fields during the 2013 growing season
Extended Data Table 4 Wild bee density in oilseed rape fields and borders in relation to insecticide seed treatment and covariates
Extended Data Table 5 Statistical tests and mean values for bee-related variables in relation to the insecticide seed treatment in the oilseed rape fields
Extended Data Table 6 Bumblebee colony growth (net weight gain) and honeybee colony strength (adult bees per hive) in relation to insecticide seed treatment
Extended Data Table 7 Number of individuals of wild bee species or groups at control (n = 8) and insecticide-treated (n = 8) oilseed rape fields
Extended Data Table 8 Residues of neonicotinoids (n) and a pyrethroid (p) in bee-collected pollen and nectar from control fields and fields sown with insecticide treated seeds

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Rundlöf, M., Andersson, G., Bommarco, R.et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees.Nature521, 77–80 (2015). https://doi.org/10.1038/nature14420

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Editorial Summary

Bees' responses to neonicotinoids examined

Reports that neonicotinoid insecticides have adverse effects on bee populations remain controversial. Some studies have been criticized as using unrealistically high insecticide dosages or conditions far removed from those in the field, and it has been suggested that bees might be able to detect the insecticides and avoid treated crops. Two papers in this issue ofNature present results that fill some of the gaps in our knowledge. In laboratory experiments Sébastien Kessleret al. use field-level doses of three commonly used neonicotinoids — clothianidin, imidacloprid and thiamethoxam — to show that both honeybees and bumblebees are able to detect their presence. However, the bees do not avoid neonicotinoid-treated food and may even prefer it. Maj Rundlöfet al. sowed oilseed rape with and without a clothianidin seed coating in matched and replicated agricultural landscapes. They found the seed coating to be associated with reduced density of wild bees, as well as reduced nesting of solitary bees and reduced colony growth of bumblebees, but they did not detect an effect on honeybees.

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