Declines in insectivorous birds are associated with high neonicotinoid concentrations

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Abstract

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.

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Figure 1: Effect of imidacloprid on bird trends in the Netherlands.
Figure 2: Comparison of the effect of agricultural land-use changes and the effect of imidacloprid on bird population trends.

Change history

  • 13 October 2014

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

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Acknowledgements

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.

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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.

Corresponding author

Correspondence to Caspar A. Hallmann.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Distribution of the 555 imidacloprid measurement averages over the period 2003–2009, as used in the main analysis.

The data are taken from refs 4 and 13.

Extended Data Figure 2 Distribution of the 354 bird monitoring plots in the Netherlands.

The figure depicts the spatial distribution of bird monitoring plots from which local species-specific trends were calculated.

Extended Data Figure 3 Spatial and serial (yearly) autocorrelation of imidacloprid measurements.

a, Semivariance (dots) and Matern variogram model (fitted line) used in the interpolation of the concentrations (nugget = 0.1901, sill = 1.6989, range = 13.2 km). b, Serial correlation (between years) of imidacloprid concentrations. Each value gives the number of pairs of measurements at each year lag that were used to calculate the coefficients. Serial correlations remain invariant with respect to temporal lag, indicating high temporal consistency in local imidacloprid concentrations.

Extended Data Figure 4 Population trends as a function of imidacloprid concentration per individual bird species.

The red lines depict the weighted mean trend, also given as slope coefficients (β) and with corresponding P values.

Extended Data Figure 5 Robustness check for the effect of the cut-off value for the distance between bird monitoring plots and water measurement locations (varied between 1 and 25 km).

The larger the cut-off distance, the more species–plot annual rates of increase are retained in the analysis subset of the total database of 3,947 records (a) but at the cost of increased noise in the response and a decrease in the effect of imidacloprid on the bird trends (b). However, in all cases, the effect of imidacloprid was significant and negative (P < 0.0001).

Extended Data Figure 6 Bird species trends before and after imidacloprid introduction.

Comparison of the relationship of bird species trends in the periods 1984–1995 (a) and 2003–2010 (b) with the imidacloprid concentrations in 2003–2009, based on all plots monitored in both time periods. Each point in the scatter plot represents the average intrinsic rate of increase of a species over all plots in the same concentration class. Binning into classes was performed to reduce scatter noise and aid in visual interpretation. The actual analyses and the depicted significant regression line were based on raw data. The bird trends were significantly affected by the imidacloprid concentration in 2003–2010 (t = −2.16, d.f. = 365, P = 0.031) but were not significantly affected in the period before imidacloprid administration (t = −1.43, d.f. = 365, P = 0.15).

Extended Data Table 1 Species information
Extended Data Table 2 Multiple mixed effects regression of population trends (pooled over 15 species, n = 1,926)

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Hallmann, C., Foppen, R., van Turnhout, C. et al. Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511, 341–343 (2014). https://doi.org/10.1038/nature13531

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