Skip to main content
SpringerLink
Log in

The leafcutter bee, Megachile rotundata, is more sensitive to N-cyanoamidine neonicotinoid and butenolide insecticides than other managed bees

  • Brief Communication
  • Published:

From Nature Ecology & Evolution

View current issue Submit your manuscript

Abstract

Recent research has shown that several managed bee species have specific P450 enzymes that are preadapted to confer intrinsic tolerance to some insecticides including certain neonicotinoids. However, the universality of this finding across managed bee pollinators is unclear. Here we show that the alfalfa leafcutter bee, Megachile rotundata, lacks such P450 enzymes and is >2,500-fold more sensitive to the neonicotinoid thiacloprid and 170-fold more sensitive to the butenolide insecticide flupyradifurone than other managed bee pollinators. These findings have important implications for the safe use of insecticides in crops where M. rotundata is used for pollination, and ensuring that regulatory pesticide risk assessment frameworks are protective of this species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1: Distribution and phylogeny of the CYP9 family of P450 genes in bee pollinators.
Fig. 2: Biological and biochemical characterization of the response of M. rotundata to select insecticides.

Similar content being viewed by others

Data availability

The accession numbers of the M. rotundata P450 genes analysed in this study are shown in Supplementary Table 1. All other data generated or analysed during the study are included in this published article and its Supplementary Information files.

References

  1. Johnson, R. M. Annu. Rev. Entomol. 60, 415–434 (2015).

    Article  CAS  Google Scholar 

  2. Beadle, K. et al. PLoS Genet. 15, e1007903 (2019).

    Article  CAS  Google Scholar 

  3. Manjon, C. et al. Curr. Biol. 28, 1137–1143.e5 (2018).

    Article  CAS  Google Scholar 

  4. Mao, W., Schuler, M. A. & Berenbaum, M. R. Proc. Natl Acad. Sci. USA 108, 12657–12662 (2011).

    Article  CAS  Google Scholar 

  5. Pitts-Singer, T. L. & Cane, J. H. Annu. Rev. Entomol. 56, 221–237 (2011).

    Article  CAS  Google Scholar 

  6. Scott-Dupree, C. D., Conroy, L. & Harris, C. R. J. Econ. Entomol. 102, 177–182 (2009).

    Article  CAS  Google Scholar 

  7. Gradish, A. E., Scott-Dupree, C. D. & Cutler, G. C. J. Pest Sci. 85, 133–140 (2012).

    Article  Google Scholar 

  8. Kapheim, K. M. et al. Science 348, 1139–1143 (2015).

    Article  CAS  Google Scholar 

  9. Nauen, R. et al. Pest Manage. Sci. 71, 850–862 (2015).

    Article  CAS  Google Scholar 

  10. Claudianos, C. et al. Insect Mol. Biol. 15, 615–636 (2006).

    Article  CAS  Google Scholar 

  11. Edgar, R. C. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article  CAS  Google Scholar 

  12. Nei, M. & Kumar, S. Molecular Evolution and Phylogenetics (Oxford Univ. Press, 2000).

  13. Guindon, S. et al. Syst. Biol. 59, 307–321 (2010).

    Article  CAS  Google Scholar 

  14. Ronquist, F. et al. Syst. Biol. 61, 539–542 (2012).

    Article  Google Scholar 

  15. OECD Guidelines for the Testing of Chemicals. Test 214. Honeybees, Acute Contact Toxicity Test (Organisation for Economic Co-operation and Development, 1998); https://www.oecd-ilibrary.org/environment/test-no-214-honeybees-acute-contact-toxicity-test_9789264070189-en

  16. Roessink, I., van der Steen, J. J. M. & Hanewald, N. Solitary Bee, Acute Contact Toxicity Test (ICPPR Workgroup non-Apis bees, 2016).

  17. European Food Safety Authority EFSA J. 13, 4020 (2015).

  18. Arena, M. & Sgolastra, F. Ecotoxicology 23, 324–334 (2014).

    Article  CAS  Google Scholar 

  19. Nauen, R., Ebbinghaus-Kintscher, U. & Schmuck, R. Pest Manage. Sci. 57, 577–586 (2001).

    Article  CAS  Google Scholar 

  20. Wheelock, G. D. & Scott, J. G. Entomol. Exp. Appl. 61, 295–299 (1991).

    Article  Google Scholar 

  21. Zhu, F. et al. Proc. Natl Acad. Sci. USA 107, 8557–8562 (2010).

    Article  CAS  Google Scholar 

  22. Guidance for Assessing Pesticide Risks to Bees (United States Environmental Protection Agency, Health Canada Pest Management Regulatory Agency & California Department of Pesticide Regulation, 2014); https://www.epa.gov/sites/production/files/2014-06/documents/pollinator_risk_assessment_guidance_06_19_14.pdf

Download references

Acknowledgements

This study received funding from the Biotechnology and Biological Sciences Research Council and Bayer AG through an Industrial CASE studentship award (no. BB/P504774/1). The technical assistance of J. Hens is gratefully acknowledged.

Author information

Authors and Affiliations

  1. College of Life and Environmental Sciences, Biosciences, University of Exeter, Penryn, UK

    Angela Hayward, Katherine Beadle, Kumar Saurabh Singh & Chris Bass

  2. Bayer AG, Crop Science Division, R&D, Monheim, Germany

    Nina Exeler, Marion Zaworra, Maria-Teresa Almanza, Alexander Nikolakis, Christina Garside, Johannes Glaubitz & Ralf Nauen

Authors
  1. Angela Hayward
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katherine Beadle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kumar Saurabh Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nina Exeler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marion Zaworra
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria-Teresa Almanza
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alexander Nikolakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Christina Garside
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Johannes Glaubitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Chris Bass
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ralf Nauen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C.B. and R.N. conceived and directed the study, A.H., K.B., K.S.S. and J.G. performed the experiments and analysis. N.E., M.Z., M.-T.A., A.N. and C.G. analysed and interpreted the data. A.H., C.B. and R.N. wrote the paper with contributions from all authors.

Corresponding authors

Correspondence to Chris Bass or Ralf Nauen.

Ethics declarations

Competing interests

This study received funding from Bayer AG, a manufacturer of neonicotinoid and butenolide insecticides. N.E., M.Z., M.-T.A., A.N., C.G., J.G. and R.N. are employees of Bayer AG.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Tables 1 and 3.

Reporting Summary

Supplementary Table

Supplementary Table 2 Comparison of the CYPomes of 4 managed bee species.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hayward, A., Beadle, K., Singh, K.S. et al. The leafcutter bee, Megachile rotundata, is more sensitive to N-cyanoamidine neonicotinoid and butenolide insecticides than other managed bees. Nat Ecol Evol 3, 1521–1524 (2019). https://doi.org/10.1038/s41559-019-1011-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-1011-2

  • Springer Nature Limited

This article is cited by

Search

Navigation