Letter | Published:

Declines in insectivorous birds are associated with high neonicotinoid concentrations

Nature volume 511, pages 341343 (17 July 2014) | Download Citation


Recent studies have shown that neonicotinoid insecticides have adverse effects on non-target invertebrate species1,2,3,4,5,6. Invertebrates constitute a substantial part of the diet of many bird species during the breeding season and are indispensable for raising offspring7. We investigated the hypothesis that the most widely used neonicotinoid insecticide, imidacloprid, has a negative impact on insectivorous bird populations. Here we show that, in the Netherlands, local population trends were significantly more negative in areas with higher surface-water concentrations of imidacloprid. At imidacloprid concentrations of more than 20 nanograms per litre, bird populations tended to decline by 3.5 per cent on average annually. Additional analyses revealed that this spatial pattern of decline appeared only after the introduction of imidacloprid to the Netherlands, in the mid-1990s. We further show that the recent negative relationship remains after correcting for spatial differences in land-use changes that are known to affect bird populations in farmland. Our results suggest that the impact of neonicotinoids on the natural environment is even more substantial than has recently been reported and is reminiscent of the effects of persistent insecticides in the past. Future legislation should take into account the potential cascading effects of neonicotinoids on ecosystems.

  • Subscribe to Nature for full access:



Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

Change history

  • Corrected online 13 October 2014

    ED Figs 2, 5 and 6 were corrected on 13 Oct 2014


  1. 1.

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

  2. 2.

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

  3. 3.

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

  4. 4.

    , & Macro-invertebrate decline in surface water polluted with imidacloprid. PLoS ONE 8, e62374 (2013)

  5. 5.

    & The neonicotinoid insecticide imidacloprid repels pollinating flies and beetles at field-realistic concentrations. PLoS ONE 8, e54819 (2013)

  6. 6.

    , , & The neonicotinoid imidacloprid shows high chronic toxicity to mayfly nymphs. Environ. Toxicol. Chem. 32, 1096–1100 (2013)

  7. 7.

    & The Birds of the Western Palearctic (Oxford Univ. Press, 1994)

  8. 8.

    An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 50, 977–987 (2013)

  9. 9.

    et al. Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol. Sci. 22, 573–580 (2001)

  10. 10.

    & Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu. Rev. Pharmacol. Toxicol. 45, 247–268 (2005)

  11. 11.

    Fine Chemicals: The Industry and the Business (Wiley, 2011)

  12. 12.

    Statistics Netherlands. StatLine Databank (2013)

  13. 13.

    Institute of Environmental Sciences, Leiden University and Rijkswaterstaat-Water Services. Dutch Pesticides Atlas (2009)

  14. 14.

    Population Limitation in Birds (Elsevier, 1998)

  15. 15.

    et al. Evidence for the indirect effects of pesticides on farmland birds. Ibis 146, 131–143 (2004)

  16. 16.

    , & Red flag for green spray: adverse trophic effects of Bti on breeding birds. J. Appl. Ecol. 47, 884–889 (2010)

  17. 17.

    , , , & Life-history and ecological correlates of population change in Dutch breeding birds. Biol. Conserv. 143, 173–181 (2010)

  18. 18.

    , , , & Scale-dependent homogenization: changes in breeding bird diversity in the Netherlands over a 25-year period. Biol. Conserv. 134, 505–516 (2007)

  19. 19.

    The recent declines of farmland bird populations in Britain: an appraisal of causal factors and conservation actions. Ibis 146, 579–600 (2004)

  20. 20.

    & Local extinctions and changes in species richness of lowland farmland birds in England and Wales in relation to recent changes in agricultural land-use. Agric. Ecosyst. Environ. 78, 1–17 (2000)

  21. 21.

    in Ecology and Conservation of Lowland Farmland Birds (eds , , & ) 5–16 (British Ornithologists’ Union, 2000)

  22. 22.

    et al. Developing indicators for European birds. Phil. Trans. R. Soc. Lond. B 360, 269–288 (2005)

  23. 23.

    et al. Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl. Ecol. 11, 97–105 (2010)

  24. 24.

    & Pesticide acute toxicity is a better correlate of US grassland bird declines than agricultural intensification. PLoS ONE 8, e57457 (2013)

  25. 25.

    , & Bird Census Techniques (Academic, 1992)

  26. 26.

    Handleiding Broedvogel Monitoring Project (Sovon Vogelonderzoek Nederland, 2004)

  27. 27.

    et al. Differences in the climatic debts of birds and butterflies at a continental scale. Nature Clim. Chang. 2, 121–124 (2012)

  28. 28.

    , , & Large-scale changes in community composition: determining land use and climate change signals. PLoS ONE 7, e35272 (2012)

Download references


We thank A. J. van Dijk, H. Sierdsema and D. Zoetebier for processing the bird data sets and J. P. van der Sluijs for sharing the database with imidacloprid concentration measurements. The Breeding Bird Monitoring Program is organised in close collaboration with Statistics Netherlands and provinces and is funded by the Dutch Ministry of EZ. We thank Sovon volunteers for their efforts in the field. The study was supported by NWO grants 840.11.001 and 841.11.007 and was the result of a collaboration within the Center for Avian Population Studies.

Author information


  1. Radboud University, Institute of Water and Wetland Research, Departments of Experimental Plant Ecology & Animal Ecology and Ecophysiology, PO Box 9100 (Mail Box 31), 6500 GL Nijmegen, The Netherlands

    • Caspar A. Hallmann
    • , Hans de Kroon
    •  & Eelke Jongejans
  2. Sovon, Dutch Centre for Field Ornithology, PO Box 6521, 6503 GA Nijmegen, The Netherlands

    • Caspar A. Hallmann
    • , Ruud P. B. Foppen
    •  & Chris A. M. van Turnhout
  3. Birdlife Netherlands, PO Box 925, 3700 AX Zeist, The Netherlands

    • Ruud P. B. Foppen


  1. Search for Caspar A. Hallmann in:

  2. Search for Ruud P. B. Foppen in:

  3. Search for Chris A. M. van Turnhout in:

  4. Search for Hans de Kroon in:

  5. Search for Eelke Jongejans in:


C.A.H. performed the statistical analysis. C.A.H., R.P.B.F., C.A.M.v.T., H.d.K. and E.J. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Caspar A. Hallmann.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Data, Supplementary Methods and Supplementary References.

About this article

Publication history






Rights and permissions

To obtain permission to re-use content from this article visit RightsLink.


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.