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.

Neonicotinoids and decline in bird biodiversity in the United States

Nature Sustainability volume 3, pages 1027–1035 (2020)Cite this article

Subjects

Abstract

Neonicotinoid insecticides are being widely used and have raised concerns about negative impacts on non-target organisms. However, there has been no large-scale, generalizable study on their impact on biodiversity of avian species in the United States. Here we show, using a rich dataset on breeding birds and pesticide use in the United States, that the increase in neonicotinoid use led to statistically significant reductions in bird biodiversity between 2008 and 2014 relative to a counterfactual without neonicotinoid use, particularly for grassland and insectivorous birds, with average annual rates of reduction of 4% and 3%, respectively. The corresponding rates are even higher (12% and 5%, respectively) when the dynamic effects of bird population declines on future population growth are considered. The effects of neonicotinoids on non-grassland and non-insectivorous birds are also statistically significant but smaller, with an average annual rate of reduction of 2% over this period.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

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

Fig. 1: Trends in total pesticide use in the United States.
Fig. 2: Dynamic effects on bird population due to to a 100 kg increase of neonicotinoid use in 2008.
Fig. 3: Predicted changes in bird populations due to an increase in neonicotinoid use and the observed bird populations in the United States from 2008 to 2014.
Fig. 4: Changes in bird populations due to neonicotinoid use from 2008 to 2014.

Data availability

All data compiled for this study are publicly available and are available at https://github.com/jewelli/Neonics-birds to replicate the findings in this manuscript. Source data are provided with this paper.

Code availability

The code to replicate all the regression analyses is available at https://github.com/jewelli/Neonics-birds.

References

  1. Brennan, L. A. & Kuvlesky, W. P. North American grassland birds: an unfolding conservation crisis? J. Wildl. Manage. 69, 1–13 (2005).

    Google Scholar 

  2. Rice, J. et al. (eds) Summary for Policymakers of the Regional Assessment Report on Biodiversity and Ecosystem Services for the Americas of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES Secretariat, 2018).

  3. Rosenberg, K. V. et al. Decline of the North American avifauna. Science 366, 120–124 (2019).

    CAS  Google Scholar 

  4. Sauer, J. R., Link, W. A., Fallon, J. E., Pardieck, K. L. & Ziolkowski, D. J. The North American breeding bird survey 1966–2011: summary analysis and species accounts. N. Am. Fauna 79, 1–32 (2013).

    Google Scholar 

  5. DiBartolomeis, M., Kegley, S., Mineau, P., Radford, R. & Klein, K. An assessment of acute insecticide toxicity loading (AITL) of chemical pesticides used on agricultural land in the United States. PLoS ONE 14, e0220029 (2019).

    CAS  Google Scholar 

  6. Riffell, S., Scognamillo, D. & Burger, L. W. Effects of the conservation reserve program on northern bobwhite and grassland birds. Environ. Monit. Assess. 146, 309–323 (2008).

    Google Scholar 

  7. Ay, J. S., Chakir, R., Doyen, L., Jiguet, F. & Leadley, P. Integrated models, scenarios and dynamics of climate, land use and common birds. Clim. Change 126, 13–30 (2014).

    CAS  Google Scholar 

  8. Forister, M. L. et al. Increasing neonicotinoid use and the declining butterfly fauna of lowland California. Biol. Lett. 12, 20160475 (2016).

    Google Scholar 

  9. Hurley, T. & Mitchell, P. Value of neonicotinoid seed treatments to US soybean farmers. Pest Manage. Sci. 73, 102–112 (2017).

    CAS  Google Scholar 

  10. 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).

    CAS  Google Scholar 

  11. Rundlöf, M. et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521, 77–80 (2015).

    Google Scholar 

  12. Woodcock, B. A. et al. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356, 1393–1395 (2017).

    CAS  Google Scholar 

  13. Tsvetkov, N. et al. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science 356, 1395–1397 (2017).

    CAS  Google Scholar 

  14. Gilburn, A. S. et al. Are neonicotinoid insecticides driving declines of widespread butterflies? PeerJ 3, e1402 (2015).

    Google Scholar 

  15. Morrissey, C. A. et al. Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review. Environ. Int. 74, 291–303 (2015).

    CAS  Google Scholar 

  16. Van Dijk, T. C., Van Staalduinen, M. A. & Van der Sluijs, J. P. Macro-invertebrate decline in surface water polluted with imidacloprid. PLoS ONE 8, e62374 (2013).

    Google Scholar 

  17. Mineau, P. & Palmer, C. The Impact of the Nation’s Most Widely Used Insecticides on Birds (American Bird Conservancy, 2013).

  18. Cimino, A. M., Boyles, A. L., Thayer, K. A. & Perry, M. J. Effects of neonicotinoid pesticide exposure on human health: a systematic review. Environ. Health Perspect. 125, 155–162 (2016).

    Google Scholar 

  19. Hallmann, C. A., Foppen, R. P. B., Van Turnhout, C. A. M., De Kroon, H. & Jongejans, E. Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511, 341–343 (2014).

    CAS  Google Scholar 

  20. EFED Section 3 Registration for a Clothianidin and Beta-Cyfluthrin Combination Product for Use on Sugar Beets as a Seed Treatment (USEPA, 2007); https://go.nature.com/32DaXPU

  21. Eng, M. L., Stutchbury, B. J. M. & Morrissey, C. A. Imidacloprid and chlorpyrifos insecticides impair migratory ability in a seed-eating songbird. Sci. Rep. 7, 15176 (2017).

    Google Scholar 

  22. Eng, M. L., Stutchbury, B. J. M. & Morrissey, C. A. A neonicotinoid insecticide reduces fueling and delays migration in songbirds. Science 365, 1177–1180 (2019).

    CAS  Google Scholar 

  23. Pandey, S. P. & Mohanty, B. The neonicotinoid pesticide imidacloprid and the dithiocarbamate fungicide mancozeb disrupt the pituitary–thyroid axis of a wildlife bird. Chemosphere 122, 227–234 (2015).

    CAS  Google Scholar 

  24. Hill, A. B. The environment and disease: association or causation? Proc. R. Soc. Med. 58, 295–300 (1965).

    CAS  Google Scholar 

  25. Meehan, T. D., Hurlbert, A. H. & Gratton, C. Bird communities in future bioenergy landscapes of the upper Midwest. Proc. Natl Acad. Sci. USA 107, 18533–18538 (2010).

    CAS  Google Scholar 

  26. Evans, S. G. & Potts, M. D. Effect of agricultural commodity prices on species abundance of US grassland birds. Environ. Resour. Econ. 62, 549–565 (2015).

    Google Scholar 

  27. Illán, J. G. et al. Precipitation and winter temperature predict long-term range-scale abundance changes in western North American birds. Glob. Change Biol. 20, 3351–3364 (2014).

    Google Scholar 

  28. Davey, C. M., Chamberlain, D. E., Newson, S. E., Noble, D. G. & Johnston, A. Rise of the generalists: evidence for climate driven homogenization in avian communities. Glob. Ecol. Biogeogr. 21, 568–578 (2012).

    Google Scholar 

  29. National Water-Quality Assessment Project—Pesticide National Synthesis Project (USGS, 2018); https://water.usgs.gov/nawqa/pnsp/usage/maps/county-level/

  30. Conley, T. G. GMM estimation with cross-sectional dependence. J. Econ. 92, 1–45 (1999).

    Google Scholar 

  31. Baker, N. T. & Wesley, W. S. Estimated Annual Agricultural Pesticide Use for Counties of the Conterminous United States, 2008–12 (US Department of the Interior, USGS, 2014).

  32. Zeileis, A., Kleiber, C. & Jackman, S. Regression models for count data in R. J. Stat. Softw. 27, 1–25 (2008).

    Google Scholar 

  33. Arellano, M. & Bond, S. Some tests of specification for panel data: Monte Carlo evidence and an application to employment equations. Rev. Econ. Stud. 58, 277–297 (1991).

    Google Scholar 

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

    CAS  Google Scholar 

  35. Heller, M. Bill aims to ban pesticides harmful to bees. E&E News (21 February 2019); https://www.eenews.net/eenewspm/2019/02/21/stories/1060121799

  36. Zeng, G., Chen, M. & Zeng, Z. Risks of neonicotinoid pesticides. Science 340, 1403 (2013).

    CAS  Google Scholar 

  37. Grassland Birds (USDA-NRCS, Wildlife Habitat Council, 1999); ftp://ftp-fc.sc.egov.usda.gov/WHMI/WEB/pdf/GRASS1.pdf

  38. Hladik, M. L. & Kolpin, D. W. First national-scale reconnaissance of neonicotinoid insecticides in streams across the USA. Environ. Chem. 13, 12–20 (2016).

    CAS  Google Scholar 

  39. Loss, S. R., Will, T. & Marra, P. P. Direct mortality of birds from anthropogenic causes. Annu. Rev. Ecol. Evol. Syst. 46, 99–120 (2015).

    Google Scholar 

  40. Böcker, T. G. & Finger, R. A meta-analysis on the elasticity of demand for pesticides. J. Agric. Econ. 68, 518–533 (2017).

    Google Scholar 

  41. Fernandez-Cornejo, J. & Jans, S. Pest Management in US Agriculture Report No. 717 (USDA ERS, 1999).

  42. Commodity Costs and Returns (USDA ERS, 2018); https://www.ers.usda.gov/data-products/commodity-costs-and-returns/

  43. Li, Y., Miao, R. & Khanna, M. Effects of ethanol plant proximity and crop prices on land-use change in the United States. Am. J. Agric. Econ. 101, 467–491 (2019).

    Google Scholar 

  44. Wang, T. et al. Determinants of motives for land use decisions at the margins of the Corn Belt. Ecol. Econ. 134, 227–237 (2017).

    Google Scholar 

  45. Chamberlain, D. E., Fuller, R. J., Bunce, R. G. H., Duckworth, J. C. & Shrubb, M. Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. J. Appl. Ecol. 37, 771–788 (2000).

    Google Scholar 

  46. Atkinson, P. W., Buckingham, D. & Morris, A. J. What factors determine where invertebrate-feeding birds forage in dry agricultural grasslands? Ibis 146, 99–107 (2004).

    Google Scholar 

  47. Kovács-Hostyánszki, A., Batáry, P., Peach, W. J. & Báldi, A. Effects of fertilizer application on summer usage of cereal fields by farmland birds in central Hungary. Bird Study 58, 330–337 (2011).

    Google Scholar 

  48. Stock, J. H. & Yogo, M. in Identification and Inference for Econometric Models: Essays in Honor of Thomas J. Rothenberg (eds Stock, J. H. & Andrews, D. W. K.) 80–108 (Cambridge Univ. Press, 2005).

  49. Windmeijer, F. Moment conditions for fixed effects count data models with endogenous regressors. Econ. Lett. 68, 21–24 (2000).

    Google Scholar 

  50. Allison, P. D. & Waterman, R. P. Fixed-effects negative binomial regression models. Sociol. Methodol. 32, 247–265 (2002).

    Google Scholar 

  51. Guimarães, P. The fixed effects negative binomial model revisited. Econ. Lett. 99, 63–66 (2008).

    Google Scholar 

  52. North American Breeding Bird Survey Dataset 1966–2018 (USGS Patuxent Wildlife Research Center, 2018); https://doi.org/10.5066/P9HE8XYJ

  53. Peterjohn, B. G. & Sauer, J. R. North American breeding bird survey annual summary 1990–1991. Bird Popul. 1, 52–67 (1993).

    Google Scholar 

  54. Smith, A. C., Anne, M., Hudson, R., Downes, C. M. & Francis, C. M. Change points in the population trends of aerial–insectivorous birds in North America: synchronized in time across species and regions. PLoS ONE 10, e013076 (2015).

    Google Scholar 

  55. Jost, L. Entropy and diversity. Oikos 113, 363–375 (2006).

    Google Scholar 

  56. Fishel, F. Pesticide Toxicity Profile: Neonicotinoid Pesticides (Univ. of Florida, IFAS, 2016); https://edis.ifas.ufl.edu/pi117

  57. Cropland Data Layer (USDA-NASS, 2020); http://nassgeodata.gmu.edu/CropScape/

  58. Parameter-Elevation Regression on Independent Slopes Model (PRISM) Climate Group (Oregon State Univ., 2018); http://prism.oregonstate.edu

  59. Population and Housing Unit Estimates Datasets (US Census Bureau, 2018); https://www.census.gov/programs-surveys/popest/data.html

  60. Fertilizer Use and Price (USDA ERS, 2018); https://www.ers.usda.gov/data-products/fertilizer-use-and-price/

Download references

Acknowledgements

We thank NIFA, USDA for hatch funding for this research. We also thank J. Tooker for helpful insights on the ways in which neonicotinoid use impact various organisms.

Author information

Authors and Affiliations

  1. Department of Agricultural and Consumer Economics, University of Illinois at Urbana-Champaign, Urbana, IL, USA

    Yijia Li & Madhu Khanna

  2. Department of Agricultural Economics and Rural Sociology, Auburn University, Auburn, AL, USA

    Ruiqing Miao

Authors
  1. Yijia Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruiqing Miao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Madhu Khanna
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the design of the empirical methods and the writing of the manuscript. Y.L. collected the data and conducted the regression analysis.

Corresponding author

Correspondence to Madhu Khanna.

Ethics declarations

Competing interests

The authors declare no competing interests.

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 Fig. 1 and Tables 1–22.

Supplementary Data 1

BBS survey route map.

Source data

Source Data Fig. 1

Aggregate pesticide use trend.

Source Data Fig. 2

Bird population change trend.

Source Data Fig. 3

Bird population change trend.

Source Data Fig. 4

Bird population change maps.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Miao, R. & Khanna, M. Neonicotinoids and decline in bird biodiversity in the United States. Nat Sustain 3, 1027–1035 (2020). https://doi.org/10.1038/s41893-020-0582-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41893-020-0582-x

This article is cited by

Search

Advanced 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