Letter | Published:

Seed coating with a neonicotinoid insecticide negatively affects wild bees

Nature volume 521, pages 7780 (07 May 2015) | Download Citation

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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References

  1. 1.

    et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354 (2006)

  2. 2.

    , & Quantitative historical change in bumblebee (Bombus spp.) assemblages of red clover fields. PLoS ONE 6, e25172 (2011)

  3. 3.

    et al. Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc. Natl Acad. Sci. USA 110, 4656–4660 (2013)

  4. 4.

    et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611 (2013)

  5. 5.

    , , , & Applied aspects of neonicotinoid uses in crop protection. Pest Manag. Sci. 64, 1099–1105 (2008)

  6. 6.

    Commission Implementing Regulation (EU) No 485/2013 of 24 May 2013 amending Implementing Regulation (EU) No 540/2011, as regards the conditions of approval of the active substances clothianidin, thiamethoxam and imidacloprid, and prohibiting the use and sale of seeds treated with plant protection products containing those active substances. OJ L 139, 12–26 (2013)

  7. 7.

    Bees, lies and evidence-based policy. Nature 494, 283 (2013)

  8. 8.

    , & Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108 (2012)

  9. 9.

    et al. A common pesticide decreases foraging success and survival in honey bees. Science 336, 348–350 (2012)

  10. 10.

    , , & Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352 (2012)

  11. 11.

    et al. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. Biol. Sci. 281, (2014)

  12. 12.

    Towards an integrated environmental risk assessment of multiple stressors on bees: review of research projects in Europe, knowledge gaps and recommendations. EFSA J. 12, 3594 (2014)

  13. 13.

    et al. Effects of neonicotinoids and fipronil on non-target invertebrates. Environ. Sci. Pollut. Res. Int. 22, 68–102 (2015)

  14. 14.

    , , & Overview of the status and global strategy for neonicotinoids. J. Agric. Food Chem. 59, 2897–2908 (2011)

  15. 15.

    , & Impact of currently used or potentially useful insecticides for canola agroecosystems on Bombus impatiens (Hymenoptera: Apidae), Megachile rotundata (Hymentoptera: Megachilidae), and Osmia lignaria (Hymenoptera: Megachilidae). J. Econ. Entomol. 102, 177–182 (2009)

  16. 16.

    & A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23, 324–334 (2014)

  17. 17.

    , , & Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris). Pest Manag. Sci. 70, 332–337 (2014)

  18. 18.

    , & Movement, persistence and uptake by plants of 14C-labelled cyfluthrin. Pak. J. Biol. Sci. 3, 104–109 (2000)

  19. 19.

    , , & Late-season mass-flowering red clover increases bumble bee queen and male densities. Biol. Conserv. 172, 138–145 (2014)

  20. 20.

    , & Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23, 317–323 (2014)

  21. 21.

    & Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Funct. Ecol. 28, 1459–1471 (2014)

  22. 22.

    et al. Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19, 207–215 (2010)

  23. 23.

    , , , & A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. PeerJ 2, e652 (2014)

  24. 24.

    , , & Mass-flowering crops enhance wild bee abundance. Oecologia 172, 477–484 (2013)

  25. 25.

    , , & Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21, 973–992 (2012)

  26. 26.

    , , , & Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7, e29268 (2012)

  27. 27.

    Environmental risk assessment scheme for plant protection products. Chapter 2: guidance on identifying aspects of environmental concern. OEPP/EPPO Bulletin 33, 113–114 (2003)

  28. 28.

    Scientific opinion on the development of specific protection goal options for environmental risk assessment of pesticides, in particular in relation to the revision of the guidance documents on aquatic and terrestrial ecotoxicology (SANCO/3268/2001 and SANCO/10329/2002). EFSA J. 8, 1821 (2010)

  29. 29.

    & Promises and problems for the new paradigm for risk assessment and an alternative approach involving predictive systems models. Environ. Toxicol. Chem. 31, 2663–2671 (2012)

  30. 30.

    & Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science 341, 759–765 (2013)

  31. 31.

    & Honeybee foraging in differentially structured landscapes. Proc. Biol. Soc. 270, 569–575 (2003)

  32. 32.

    , , & Bee foraging ranges and their relationship to body size. Oecologia 153, 589–596 (2007)

  33. 33.

    Entwicklungsstadien Mono- Und Dikotyler Pflanzen. BBCH Monografie. 2nd edn (Biologische Bundesanstalt für Land und Forstwirtschaft, 2001)

  34. 34.

    , & Insecticide use on Scottish oilseed rape crops: historical use patterns and pest control options in the absence of neonicotinoid seed treatments. In Proc. Crop Protection in Northern Britain 21–26 (2014)

  35. 35.

    & Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. J. Econ. Entomol. 100, 765–772 (2007)

  36. 36.

    et al. Pesticide Usage Survey Report 250. Arable Crops in the United Kingdom 2012 (Department for Environment, Food and Rural Affairs, 2013)

  37. 37.

    Färre frön med hybrider. Svensk Frötidning 2, 9–10 (2013)

  38. 38.

    , , & Insekter. En Fälthandbok (Interpublishing, 2004)

  39. 39.

    Humlor. Alla Sveriges Arter - Så Känner Du Igen Dem i Naturen Och i Trädgården (Östlings bokförslag, 2007)

  40. 40.

    & Humlor i Sverige - 40 Arter Att Älska Och Förundras Över (Bonnier Fakta, 2012)

  41. 41.

    The biology of the solitary bee Osmia rufa (L.) (Megachilidae). T. Roy. Ent. Soc. London 124, 213–229 (1972)

  42. 42.

    Field experiments with the pollinator species, Osmia lignaria propinqua Cresson (Hymenoptera, Megachilidae) in apple orchards: III, 1977 studies. J. Kans. Entomol. Soc. 57, 517–521 (1984)

  43. 43.

    & Developing and establishing bee species as crop pollinators: the example of Osmia spp. (Hymenoptera: Megachilidae) and fruit trees. Bull. Entomol. Res. 92, 3–16 (2002)

  44. 44.

    & Do resources or natural enemies drive bee population dynamics in fragmented habitats? Ecology 89, 1375–1387 (2008)

  45. 45.

    Artportalen Swedish Species Observation System, Swedish Species Information Centre, SLU. (access, 9 February 2014)

  46. 46.

    et al. The Trojan hives: pollinator pathogens, imported and distributed in bumblebee colonies. J. Appl. Ecol. 50, 1207–1215 (2013)

  47. 47.

    , , , & A test of the method of estimation of brood areas and number of worker bees in free-flying colonies. Apidologie (Celle) 18, 137–146 (1987)

  48. 48.

    , & Standard methods for estimating strength parameters of Apis mellifera colonies. J. Apicult. Res. 52, 1 (2013)

  49. 49.

    & Course in Determination of Colony Strength (Swiss Bee Research Centre, 2001)

  50. 50.

    , , , & Validation of a bioanalytical method using capillary microsampling of 8 µl plasma samples: application to a toxicokinetic study in mice. Bioanalysis 4, 1989–1998 (2012)

  51. 51.

    et al. Capillary microsampling of 25 µl blood for the determination of toxicokinetic parameters in regulatory studies in animals. Bioanalysis 4, 661–674 (2012)

  52. 52.

    in Microsampling in Pharmaceutical Bioanalysis (eds Zane, P. & Emmons, G. T.) 68–82 (Future Science Ltd, 2013)

  53. 53.

    , , , & SAS for Mixed Models 2nd edn (SAS Institute Inc., 2006)

  54. 54.

    , & Effects of clothianidin on Bombus impatiens (Hymenoptera: Apidae) colony health and foraging ability. J. Econ. Entomol. 97, 369–373 (2004)

  55. 55.

    , & Assessing insecticide hazard to bumble bees foraging on flowering weeds in treated lawns. PLoS ONE 8, e66375 (2013)

  56. 56.

    , , & Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory. J. Appl. Ecol. 51, 450–459 (2014)

  57. 57.

    EFSA guidance document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J. 11, 3295 (2013)

  58. 58.

    A Large-Scale Field Experiment to Quantify the Impacts of Neonicotinoids (NNIs) on Honeybees (The Centre for Ecology and Hydrology, 2014)

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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

Affiliations

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

    • Maj Rundlöf
    • , Georg K. S. Andersson
    • , Veronica Hederström
    • , Johanna Yourstone
    •  & Henrik G. Smith
  2. Lund University, Centre for Environmental and Climate Research, 223 62 Lund, Sweden

    • Georg K. S. Andersson
    • , Lina Herbertsson
    • , Björn K. Klatt
    •  & Henrik G. Smith
  3. Swedish University of Agricultural Sciences, Department of Ecology, 750 07 Uppsala, Sweden

    • Riccardo Bommarco
    •  & Ingemar Fries
  4. Swedish University of Agricultural Sciences, Department of Aquatic Sciences and Assessment, 750 07 Uppsala, Sweden

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

    • Ove Jonsson
  6. Swedish Board of Agriculture, 551 82 Jönköping, Sweden

    • Thorsten R. Pedersen

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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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Maj Rundlöf.

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https://doi.org/10.1038/nature14420

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