Skip to main content

Thank you for visiting nature.com. 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.

Combined pesticide exposure severely affects individual- and colony-level traits in bees

Abstract

Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production1,2,3. Bees contribute approximately 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations 4,5,6. Recent studies have implicated the role of pesticides in these declines, as exposure to these chemicals has been associated with changes in bee behaviour7,8,9,10,11 and reductions in colony queen production12. However, the key link between changes in individual behaviour and the consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of many individual workers. Thus, although field-level pesticide concentrations can have subtle or sublethal effects at the individual level8, it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means that bees are exposed to numerous pesticides when foraging13,14,15, yet the possible combinatorial effects of pesticide exposure have rarely been investigated16,17. Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concentrations that could approximate field-level exposure impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success. We found that worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with observed knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Worker production and mortality.
Figure 2: Foraging performance.
Figure 3: Overall worker losses.

References

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

    Article  ADS  CAS  Google Scholar 

  2. Klein, A. M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 274, 303–313 (2007)

    Article  Google Scholar 

  3. Kremen, C. et al. Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol. Lett. 10, 299–314 (2007)

    Article  Google Scholar 

  4. Potts, S. G. et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353 (2010)

    Article  Google Scholar 

  5. Oldroyd, B. P. What's killing American honey bees? PLoS Biol. 5, e168 (2007)

    Article  Google Scholar 

  6. Brown, M. J. F. & Paxton, R. J. The conservation of bees: a global perspective. Apidologie 40, 410–416 (2009)

    Article  Google Scholar 

  7. Thompson, H. M. Behavioural effects of pesticides in bees - their potential for use in risk assessment. Ecotoxicology 12, 317–330 (2003)

    Article  CAS  Google Scholar 

  8. Desneux, N., Decourtye, A. & Delpuech, J. M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 52, 81–106 (2007)

    Article  CAS  Google Scholar 

  9. Cresswell, J. E. A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (Imidacloprid) on honey bees. Ecotoxicology 20, 149–157 (2011)

    Article  CAS  Google Scholar 

  10. Schneider, C. W., Tautz, J., Grünewald, B. & Fuchs, S. RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS ONE 7, e30023 (2012)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  12. Whitehorn, P. R., O'Connor, S., Wackers, F. L. & Goulson, D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352 (2012)

    Article  ADS  CAS  Google Scholar 

  13. Johnson, R. M., Ellis, M. D., Mullin, C. A. & Frazier, M. Pesticides and honey bee toxicity — USA. Apidologie 41, 312–331 (2010)

    Article  CAS  Google Scholar 

  14. Mullin, C. A. et al. High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS ONE 5, e9754 (2010)

    Article  ADS  Google Scholar 

  15. Krupke, C. H., Hunt, G. J., Eitzer, B. D., Andino, G. & Given, K. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7, e29268 (2012)

    Article  ADS  CAS  Google Scholar 

  16. Johnson, R. M., Pollock, H. S. & Berenbaum, M. R. Synergistic interactions between in-hive miticides in Apis mellifera. J. Econ. Entomol. 102, 474–479 (2009)

    Article  CAS  Google Scholar 

  17. Pilling, E. D. & Jepson, P. C. Synergism between EBI fungicides and a pyrethroid insecticide in the honeybee (Apis mellifera). Pestic. Sci. 39, 293–297 (1993)

    Article  CAS  Google Scholar 

  18. Elbert, A., Haas, M., Springer, B., Thielert, W. & Nauen, R. Applied aspects of neonicotinoid uses in crop protection. Pest Manag. Sci. 64, 1099–1105 (2008)

    Article  CAS  Google Scholar 

  19. Rortais, A., Arnold, G., Halm, M. P. & Touffet-Briens, F. Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36, 71–83 (2005)

    Article  CAS  Google Scholar 

  20. Chauzat, M. P. et al. A survey of pesticide residues in pollen loads collected by honey bees in France. J. Econ. Entomol. 99, 253–262 (2006)

    Article  CAS  Google Scholar 

  21. Blacquière, T., Smagghe, G., van Gestel, C. A. M. & Mommaerts, V. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21, 973–992 (2012)

    Article  Google Scholar 

  22. Molet, M., Chittka, L., Stelzer, R. J., Streit, S. & Raine, N. E. Colony nutritional status modulates worker responses to foraging recruitment pheromone in the bumblebee Bombus terrestris. Behav. Ecol. Sociobiol. 62, 1919–1926 (2008)

    Article  Google Scholar 

  23. Schmid-Hempel, R. & Schmid-Hempel, P. Colony performance and immunocompetence of a social insect, Bombus terrestris, in poor and variable environments. Funct. Ecol. 12, 22–30 (1998)

    Article  Google Scholar 

  24. Pelletier, L. & McNeil, J. N. The effect of food supplementation on reproductive success in bumblebee field colonies. Oikos 103, 688–694 (2003)

    Article  Google Scholar 

  25. Thompson, H. & Wilkins, S. Assessment of the synergy and repellency of pyrethroid/fungicide mixtures. Bull. Insectol. 56, 131–134 (2003)

    Google Scholar 

  26. Bortolotti, L. et al. Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull. Insectol. 56, 63–67 (2003)

    Google Scholar 

  27. Decourtye, A., Devillers, J., Cluzeau, S., Charreton, M. & Pham-Delègue, M. H. Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol. Environ. Saf. 57, 410–419 (2004)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  29. Yang, E. C., Chuang, Y. C., Chen, Y. L. & Chang, L. H. Abnormal foraging behavior induced by sublethal dosage of Imidacloprid in the Honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 101, 1743–1748 (2008)

    Article  CAS  Google Scholar 

  30. Halm, M. P., Rortais, A., Arnold, G., Taséi, J. N. & Rault, S. New risk assessment approach for systemic insecticides: the case of honey bees and imidacloprid (Gaucho). Environ. Sci. Technol. 40, 2448–2454 (2006)

    Article  ADS  CAS  Google Scholar 

  31. Thompson, H. M. Assessing the exposure and toxicity of pesticides to bumblebees (Bombus sp.). Apidologie 32, 305–321 (2001)

    Article  CAS  Google Scholar 

  32. Brittain, C. & Potts, S. G. The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic Appl. Ecol. 12, 321–331 (2011)

    Article  Google Scholar 

  33. Garthwaite, D., Thomas, M. R., Parrish, G., Smith, L. & Barker, I. Pesticide Usage Survey Report 224. Arable Crops in Great Britain 2008 (Including Aerial Applications 07–08) (Food and Environmental Research Agency, 2008)

    Google Scholar 

  34. Garthwaite, D. et al. Pesticide Usage Survey Report 235. Arable Crops in UK 2010 (Including Aerial Applications 2010) (Food and Environmental Research Agency, 2010)

  35. Bonmatin, J. M. et al. A LC/APCI-MS/MS method for analysis of imidacloprid in soils, in plants, and in pollens. Anal. Chem. 75, 2027–2033 (2003)

    Article  CAS  Google Scholar 

  36. Bonmatin, J. M. et al. Quantification of imidacloprid uptake in maize crops. J. Agric. Food Chem. 53, 5336–5341 (2005)

    Article  CAS  Google Scholar 

  37. Chauzat, M. P. et al. Influence of pesticide residues on honey bee (Hymenoptera: Apidae) colony health in France. Environ. Entomol. 38, 514–523 (2009)

    Article  CAS  Google Scholar 

  38. Krischik, V. A., Landmark, A. L. & Heimpel, G. E. Soil-applied imidacloprid is translocated to nectar and kills nectar-feeding Anagyrus pseudococci (Girault) (Hymenoptera: Encyrtidae). Environ. Entomol. 36, 1238–1245 (2007)

    Article  CAS  Google Scholar 

  39. Raine, N. E. & Chittka, L. The correlation of learning speed and natural foraging success in bumble-bees. Proc. R. Soc. B 275, 803–808 (2008)

    Article  Google Scholar 

  40. Goulson, D. Bumblebees: Behaviour, Ecology and Conservation. (Oxford Univ. Press, 2010)

    Book  Google Scholar 

Download references

Acknowledgements

We thank M.J.F. Brown, M. Clook, J. Culverhouse, A. Dixon, M. Fürst, D. Garthwaite, A. Horsell, V. Jansen and I. Pedroso-Rovira for comments and technical assistance, and Syngenta Bioline Bees for supplying colonies. The study was supported by the Insect Pollinator Initiative (funded under the auspices of the Living with Environmental Change programme, Biotechnology and Biological Sciences Research Council (BBSRC), Wellcome Trust, Scottish Government, Department for Environment, Food and Rural Affairs (DEFRA) and Natural Environment Research Council (NERC): grant BB/I000178/1).

Author information

Authors and Affiliations

Authors

Contributions

R.J.G., O.R.-R. and N.E.R. carried out the experiment; R.J.G. and N.E.R. designed the experiment and wrote the paper; N.E.R. conceived the project.

Corresponding authors

Correspondence to Richard J. Gill or Nigel E. Raine.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Analyses and Results, Supplementary References, Supplementary Figures 1-8, Supplementary Tables 1-2 and Supplementary Box 1. (PDF 1495 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gill, R., Ramos-Rodriguez, O. & Raine, N. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108 (2012). https://doi.org/10.1038/nature11585

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature11585

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

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