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Thursday, 10 July 2014

Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature (2014) 09 July


Declines in insectivorous birds are associated with high neonicotinoid concentrations

Caspar A. Hallmann, Ruud P. B. Foppen, Chris A. M. van Turnhout, Hans de Kroon & Eelke Jongejans

Author Affiliations
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
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
Birdlife Netherlands, PO Box 925, 3700 AX Zeist, The Netherlands
  • Ruud P. B. Foppen
Received: 04 March 2014; Accepted: 27 May 2014; Published online: 09 July 2014 (2014) 
When neonicotinoids are applied as a seed dressing to crops, the bulk of the active ingredients (80–98%) enter the soil and soil water. There, they can persist for long periods, accumulate, be taken up by the roots of vegetation at the margins of fields and follow-on crops, or leach into aquatic systems. Neonicotinoids are highly toxic to insects, which are exposed to the chemicals in plants, soil and water. Hallmann et al have observed rapid declines in bird populations in regions with high environmental neonicotinoid concentrations, and suggest that they are the result of insect poisoning depleting the birds' food supply.

Recent studies have shown that neonicotinoid insecticides have adverse effects on non-target invertebrate species 1, 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.

Abstract References
1. Gill, R. J., Ramos-Rodriguez, O. & Raine, N. E. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108 (2012)
2. Henry, M. et al. A common pesticide decreases foraging success and survival in honey bees. Science 336, 348–350 (2012)
3. 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)
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, 1096–1100 (2013)
7. Cramp, S. & Perrins, C. M. The Birds of the Western Palearctic (Oxford Univ. Press, 1994)
Figure 1

Effect of imidacloprid on bird trends in the Netherlands.

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.


We derived population trends for 15 insectivorous farmland passerine species using long-term breeding bird data from the Dutch Common Breeding Bird Monitoring Scheme, a standardized monitoring scheme maintained and coordinated by Sovon, Dutch Centre for Field Ornithology, in collaboration with Statistics Netherlands. The scheme has been running in the Netherlands since 1984. Data originating from these monitoring plots are generally considered to be adequately representative and reliable for population trend estimation. The monitoring plots are well scattered throughout the Netherlands and range in size between 10 ha and 1,000 ha. 

Bird Species Studied

Author Conclusions

So far, the suggested potential risks of neonicotinoids for birds have focused on the acute toxic effects caused by direct consumption. Our results suggest another possibility: that is, that the depletion of insect food resources has caused the observed relationships. Two lines of evidence seem to support this. First, 9 out of 15 species tested in the present study are exclusively insectivorous. All 15 species feed their young (almost) exclusively with invertebrates, and food demand is the highest in this period. Adult skylarks, tree sparrows, common starlings, yellowhammers, meadow pipits and mistle thrushes are also granivorous to some extent and may thus directly consume coated seed. However, meadow pipits and mistle thrushes forage on seeds only outside the breeding season, and for all 15 species the bulk of the diet during the breeding season consists of invertebrates. Second, recent in situ research involving the same areas as the present study revealed strong declines in insect macrofauna, including species that have a larval stage in water, where imidacloprid concentrations were elevated. These insects (particularly Diptera, Ephemeroptera, Odonata, Coleoptera and Hemiptera) are an important food source in the breeding season for the bird species that we investigated. However, as our results are correlative, we cannot exclude other trophic or direct ways in which imidacloprid may have an effect on the bird population trends. Food resource depletion may not be the only or even the most important cause of decline. Other possible causes of decline include trophic accumulation of this neonicotinoid through consumption of contaminated invertebrates and, for the six partly granivorous species involved, sublethal or lethal effects through the ingestion of coated seeds. The relative effect sizes of these pathways urgently need to be investigated.

Farmland birds have experienced tremendous population declines in Europe in the past three decades, with agricultural intensification as the primary causal factor. Among aspects of intensification, pesticides are known to be a major threat to farmland birds. Neonicotinoids have recently replaced older intensively used insecticides such as carbamates, pyrethroids and organophosphates. After neonicotinoids were introduced to the Netherlands in the mid-1990s, their application was intensified, and the concentrations found in the environment frequently exceeded environmental standards, despite these concentrations being shown to have severe detrimental effects on several insect communities. Our results on the declines in bird populations suggest that neonicotinoids pose an even greater risk than has been anticipated. Cascading trophic effects deserve more attention in research on the ecosystem effects of this class of insecticides and must be taken into account in future legislation.

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