Declines in insectivorous birds are associated with high neonicotinoid concentrations

Journal name:
Nature
Volume:
511,
Pages:
341–343
Date published:
DOI:
doi:10.1038/nature13531
Received
Accepted
Published online
Corrected online

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.

At a glance

Figures

  1. Effect of imidacloprid on bird trends in the Netherlands.
    Figure 1: Effect of imidacloprid on bird trends in the Netherlands.

    a, Interpolated (universal kriging) mean logarithmic concentrations of imidacloprid in the Netherlands (2003–2009). b, Relationship between the average annual intrinsic rate of population increase over 15 passerine bird species and imidacloprid concentrations in Dutch surface water. Each point represents the average intrinsic rate of increase of a species over all plots in the same concentration class, whereas the size of the point is scaled proportionally to the number of species–plot combinations on which the calculated mean is based. Binning into classes was performed to reduce scatter noise and aid in visual interpretation. Actual analysis, and the depicted regression line, was performed on raw data (n = 1,459). The regression line is given by 0.1110 − 0.0374 (s.e.m. = 0.0066) × log[imidacloprid] (P < 0.0001). Dashed lines delineate the 95% confidence interval.

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

    a, The marginal variance ratio (F) of each effect was estimated from a mixed effects model with all species data pooled. b, The standardized effect size (t value) for each covariate from the mixed effects model. The vertical dotted lines represent significance thresholds at α = 0.05 (two-sided test). The imidacloprid concentrations and the proportional changes in bulb production areas were the only variables that had significant effects (LMER: d.f. = 1,349, t = −3.825, P = 0.0001 for imidacloprid; and t = 1.989, P = 0.0468 for bulbs).

  3. Distribution of the 555 imidacloprid measurement averages over the period 2003-2009, as used in the main analysis.
    Extended Data Fig. 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.

  4. Distribution of the 354 bird monitoring plots in the Netherlands.
    Extended Data Fig. 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.

  5. Spatial and serial (yearly) autocorrelation of imidacloprid measurements.
    Extended Data Fig. 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.

  6. Population trends as a function of imidacloprid concentration per individual bird species.
    Extended Data Fig. 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.

  7. 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).
    Extended Data Fig. 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).

  8. Bird species trends before and after imidacloprid introduction.
    Extended Data Fig. 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).

Tables

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

Change history

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

References

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  4. 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)
  5. Easton, A. H. & Goulson, D. The neonicotinoid insecticide imidacloprid repels pollinating flies and beetles at field-realistic concentrations. PLoS ONE 8, e54819 (2013)
  6. Roessink, I., Merga, L. B., Zweers, H. J. & van den Brink, P. J. The neonicotinoid imidacloprid shows high chronic toxicity to mayfly nymphs. Environ. Toxicol. Chem. 32, 10961100 (2013)
  7. Cramp, S. & Perrins, C. M. The Birds of the Western Palearctic (Oxford Univ. Press, 1994)
  8. Goulson, D. An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 50, 977987 (2013)
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  11. Pollak, P. Fine Chemicals: The Industry and the Business (Wiley, 2011)
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  18. Van Turnhout, C. A. M., Foppen, R. P. B., Leuven, R. S. E. W., Siepel, H. & Esselink, H. Scale-dependent homogenization: changes in breeding bird diversity in the Netherlands over a 25-year period. Biol. Conserv. 134, 505516 (2007)
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Author information

Affiliations

  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

Contributions

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 financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: Distribution of the 555 imidacloprid measurement averages over the period 2003–2009, as used in the main analysis. (471 KB)

    The data are taken from refs 4 and 13.

  2. Extended Data Figure 2: Distribution of the 354 bird monitoring plots in the Netherlands. (229 KB)

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

  3. Extended Data Figure 3: Spatial and serial (yearly) autocorrelation of imidacloprid measurements. (89 KB)

    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.

  4. Extended Data Figure 4: Population trends as a function of imidacloprid concentration per individual bird species. (444 KB)

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

  5. 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). (103 KB)

    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).

  6. Extended Data Figure 6: Bird species trends before and after imidacloprid introduction. (111 KB)

    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 Tables

  1. Extended Data Table 1: Species information (381 KB)
  2. Extended Data Table 2: Multiple mixed effects regression of population trends (pooled over 15 species, n = 1,926) (353 KB)

Supplementary information

PDF files

  1. Supplementary Information (158 KB)

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

Comments

  1. Report this comment #63833

    Francisco Sanchez-Bayo said:

    I?m surprised that this article does not mention even once the pioneering work on the same issue by Henk. A. Tennekes.

    In 2010, Dr Tennekes alerted the world about the indirect impacts of neonicotinoid insecticides on birds by publishing his book ?Systemic Neonicotinoids: A Disaster in the Making? (ETS Nederland BV, 2010). Although not a peer-reviewed work, the book made the claim, for the first time, that the recent decline of many species of birds in the Netherlands and other European countries is correlated with the increasing use of imidacloprid and other neonicotinoids during the last two decades. Insectivorous birds and waders were identified in that book as the species most at risk. In fact, 8 among the 14 species of birds studied by Hallmann et al. were explicitly named in that book. Even more interesting is that the declining populations of 5 bird species mentioned by Dr Tennekes were found, by Hallmann et al., to have a positive and significant correlation with neonicotinoid residues in waters. So, why the authors of that paper omitted to cite this source is incomprehensible to me and anyone who has been following developments on this controversial topic.

    Science builds upon the foundations laid by previous researchers or people with vision who are able to point out the way forward. This is the main reason for including citations in the scientific literature, other than paying tribute to the authors. However, I wonder if the researchers from Radboud University could have ever thought about the impact that neonicotinoid insecticides may have had on bird populations. My doubts arise from the following:
    i) The only other report dealing with the effects of neonicotonoids on birds was released late last year (Mineau, P. & Palmer, C. The Impact of the Nation?s Most Widely Used Insecticides on Birds. American Bird Conservancy, 2013). Although that report focuses on the acute and chronic toxicity of such insecticides to birds, it also deals with the issue of indirect effects by depletion of the invertebrate food source, acknowledging Dr Tennekes as the promoter of this idea and citing his book as a reference.
    ii) Neonicotinoid insecticides are not particularly toxic to vertebrates and, to my knowledge, no peer-reviewed papers have yet been published proving the contrary. There are a few studies about the sublethal effects of these compounds on birds, but they do not attract much attention from terrestrial ecotoxicologists for that very reason, let alone interest from ecologists and ornithologists.

    It is very likely, therefore, that Hallmann et al. were prompted to thoroughly investigate this issue based on the insights of that book or the numerous public dissertations of Dr Tennekes on this matter. As far as I am aware, scientific citations do not need to be restricted to peer-reviewed papers or to work carried out only by experts on a particular field (note that Dr Tennekes is neither a professional nor an amateur ornithologist). Anyone who has the vision to suggest a new direction in research should be acknowledged and given the due credit.

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