Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Moving beyond honeybee-centric pesticide risk assessments to protect all pollinators

Currently honeybees are the sole model insect pollinator for regulatory pesticide risk assessments globally. Here we question whether this surrogacy approach provides adequate protection against potential non-target impacts of pesticide exposure for the wide diversity of insect pollinators on which agricultural production and wild plant ecosystems depend.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type



Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Predicted minimum detectable effect size relating to reduction in honeybee colony size in a range of field studies in which colonies were exposed to plants grown from neonicotinoid-treated seed.

Similar content being viewed by others


  1. Godfray, H. C. J. et al. Proc. R. Soc. B 281, 20140558 (2014).

    Article  Google Scholar 

  2. Godfray, H. C. J. et al. Proc. R. Soc. B 282, 20151821 (2015).

    Article  Google Scholar 

  3. Khoury, D. S., Myerscough, M. R. & Barron, A. B. PLoS ONE 6, e18491 (2011).

    Article  CAS  Google Scholar 

  4. Robinson, A. et al. PLoS ONE 12, e0176289 (2017).

    Article  Google Scholar 

  5. Bryden, J., Gill, R. J., Mitton, R. A. A., Raine, N. E. & Jansen, V. A. A. Ecol. Lett. 16, 1463–1469 (2013).

    Article  Google Scholar 

  6. Rundlöf, M. et al. Nature 521, 77–80 (2015).

    Article  Google Scholar 

  7. Woodcock, B. A. et al. J. Appl. Ecol. 53, 1358–1362 (2016).

    Article  Google Scholar 

  8. European Food Safety Authority EFSA J. 11, 3295 (2013).

  9. Solomon, K. R. & Stephenson, G. L. J. Toxicol. Environ. Health B 20, 316–382 (2017).

    Article  CAS  Google Scholar 

  10. European and Mediterranean Plant Protection Organization EPPO Bull. 40, 323–331 (2010).

  11. Becher, M. A. et al. J. Appl. Ecol. 51, 470–482 (2014).

    Article  Google Scholar 

  12. Khoury, D. S., Barron, A. B. & Myerscough, M. R. PLoS ONE 8, e59084 (2013).

    Article  CAS  Google Scholar 

  13. Gradish, A. E. et al. Environ. Entomol. 48, 12–21 (2019).

    Article  Google Scholar 

  14. Sgolastra, F. et al. Environ. Entomol. 48, 22–35 (2019).

    Article  Google Scholar 

  15. Vanbergen, A. J. et al. Front. Ecol. Environ. 11, 251–259 (2013).

    Article  Google Scholar 

  16. European Food Safety Authority EFSA J. 13, 4125 (2015).

  17. European Food Safety Authority EFSA J. 16, 5179 (2018).

  18. Woodcock, B. A. et al. Science 356, 1393–1395 (2017).

    Article  CAS  Google Scholar 

  19. Goulson, D. PeerJ 3, e854 (2015).

    Article  Google Scholar 

  20. Sterk, G., Peters, B., Gao, Z. & Zumkier, U. Ecotoxicology 25, 1666–1678 (2016).

    Article  CAS  Google Scholar 

  21. Baron, G. L., Jansen, V. A. A., Brown, M. J. F. & Raine, N. E. Nat. Ecol. Evol. 1, 1308–1316 (2017).

    Article  Google Scholar 

  22. Baron, G. L., Raine, N. E. & Brown, M. J. F. Proc. R. Soc. B 284, 20170123 (2017).

    Article  Google Scholar 

  23. Peters, B., Gao, Z. & Zumkier, U. Ecotoxicology 25, 1679–1690 (2016).

    Article  CAS  Google Scholar 

  24. Chan, D. S. W., Prosser, R. S., Rodríguez-Gil, J. L. & Raine, N. E. Sci. Rep. 9, 11870 (2019).

    Article  Google Scholar 

Download references


This work was supported by an Ontario Ministry of Environment and Climate Change (MOECC) Best in Science grant (BIS201617-06), a Natural Sciences and Engineering Research Council (NSERC) Discovery grant (2015-06783), and the Food from Thought: Agricultural Systems for a Healthy Planet Initiative, by the Canada First Research Excellent Fund (grant 000054). N.E.R. is supported as the Rebanks Family Chair in Pollinator Conservation by The W. Garfield Weston Foundation.

Author information

Authors and Affiliations



E.L.F. and N.E.R. conceived and designed the study, analysed the data and wrote the paper.

Corresponding authors

Correspondence to Elizabeth L. Franklin or Nigel E. Raine.

Ethics declarations

Competing interests

The authors declare no competing interests.

Supplementary information

Supplementary Information

Effect size formula. File includes derivation of the effect size formula used to calculate estimated percentage minimum detectable effect size, and a figure outlining the relationship between the number of replicate pairs (control versus insecticide treatment sites) and detectable percentage losses in honeybee colony size with different levels of replication within site (Supplementary Fig. 1).

Supplementary Data

Effect size calculations. Spreadsheet reporting the (a) effect size formula, (b) effect size calculations, (c) inter-site and inter-colony variance calculations for Bayer Science 2014d Report M-501261-01, and (d) the relationship between detectable effect size and the number of paired sites and number of honeybee colonies at each site (Supplementary Fig. 1). Effect size calculations (b) detail the number of paired (control versus insecticide treatment) sites (pairs), the number of honeybee colonies (replicates) per site and the calculated minimum detectable effect size for each study.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Franklin, E.L., Raine, N.E. Moving beyond honeybee-centric pesticide risk assessments to protect all pollinators. Nat Ecol Evol 3, 1373–1375 (2019).

Download citation

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing