Skip to main content
Log in

High Exposure Rates of Anticoagulant Rodenticides in Predatory Bird Species in Intensively Managed Landscapes in Denmark

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

The extensive use of anticoagulant rodenticides (ARs) for rodent control has led to widespread secondary exposure in nontarget predatory wildlife species. We investigated exposure rates and concentrations of five ARs in liver samples from five raptors and six owls from Denmark. A total of 430 birds were analysed. ARs were detected in 84–100 % of individual birds within each species. Multiple AR exposure was detected in 73 % of all birds. Average number of substances detected in individual birds was 2.2 with no differences between owls and raptors. Difenacoum, bromadiolone, and brodifacoum were the most prevalent substances and occurred in the highest concentrations. Second-generation ARs made up 96 % of the summed AR burden. Among the six core species (sample size >30), summed AR concentrations were lower in rough-legged buzzard (Buteo lagopus) and long-eared owl (Asio otus) than in barn owl (Tyto alba), buzzard (B. buteo), kestrel (Falco tinnunculus), and tawny owl (Strix aluco). There was a strong tendency for seasonal variations in the summed AR concentration with levels being lowest during autumn, which is probably related to an influx of less-exposed migrating birds from northern Scandinavia during autumn. High hepatic AR residue concentrations (>100 ng/g wet weight), which have been associated with symptoms of rodenticide poisoning and increased mortality, were recorded high frequencies (12.9–37.4 %) in five of the six core species. The results suggest that the present use of ARs in Denmark, at least locally, may have adverse effects on reproduction and, ultimately, population status in some raptors and owls.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • Albert CA, Wilson LK, Mineau P, Trudeau S, Elliott JE (2010) Anticoagulant rodenticides in three owl species from Western Canada, 1988–2003. Arch Environ Contam Toxicol 58:451–459

    Article  CAS  Google Scholar 

  • Anonymous (2007) Vildt undersøgt ved Danmarks Fødevareforskning i 2005. National Food Institute, Danish Technical University, Aarhus

    Google Scholar 

  • Baker K (1993) Identification guide to European non-passerines. BTO Guide 24. British Trust for Ornithology, Thetford, UK

  • Berny PJ, Buronfosse T, Buronfosse F, Lamarque F, Lorgue G (1997) Field evidence of secondary poisoning of foxes (Vulpes vulpes) and buzzards (Buteo buteo) by bromadiolone: a 4-year survey. Chemosphere 35:1817–1829

    Article  CAS  Google Scholar 

  • Bønløkke J, Madsen JJ, Thorup K, Pedersen KT, Bjerrum M, Rahbek C (2006) Dansk Trækfugleatlas. Rhodos, Humlebæk

    Google Scholar 

  • Cramp S, Simmons KEL (1980) Handbook of the birds of Europe the Middle East and North Africa: the Birds of Western Palearctic, vol II. Oxford University Press, Oxford, UK

    Google Scholar 

  • Dawson A, Garthwaite DG (2004) Pesticide usage survey report 185: rodenticide usage by local authorities in Great Britain 2001. DEFRA, London

    Google Scholar 

  • Dawson A, Bankes J, Garthwaite DG (2003) Pesticide usage survey report 175: rodenticide use on farms in Great Britain growing arable crops 2000. DEFRA, London

    Google Scholar 

  • de Snoo GR, Scheidegger NM, de Jong FMV (1999) Vertebrate wildlife incidents with pesticides: a European survey. Pestic Sci 55:47–54

    Article  Google Scholar 

  • Dowding CV, Shore RF, Worgan A, Baker PJ, Harris S (2010) Accumulation of anticoagulant rodenticides in a non-target insectivore, the European hedgehog (Erinaceus europaeus). Environ Pollut 158:161–166

    Article  CAS  Google Scholar 

  • Eason CT, Murphy EC, Wright GRG, Spurr EB (2002) Assessment of risk of brodifacoum to non-target birds and mammals in New Zealand. Ecotoxicology 11:35–48

    Article  Google Scholar 

  • Elmeros M, Christensen TK, Lassen P (2011) Concentrations of anticoagulant rodenticides in stoats Mustela erminea and weasels Mustela nivalis from Denmark. Sci Total Environ 409:2373–2378

    Article  CAS  Google Scholar 

  • Erickson W, Urban D (2004) Potential risks of nine rodenticides to birds and non-target mammals: A comparative approach. United States Environmental Protection Agency report. USEPA Office of Pesticide Programs, Washington, DC

    Google Scholar 

  • Fisher P, O’Conor C, Wright G, Eason CT (2003) Persistence of four anticoagulant rodenticides in the livers of laboratory rats. Department of Conservation, DOC Science Internal Series 139, Wellington

  • Forsman D (1998) The raptors of Europe and the Middle East: a handbook of field identification. Academic Press, Waltham, MA

    Google Scholar 

  • Fournier-Chambrillon C, Berny PJ, Coiffier O, Barbedienne P, Dassé B, Delas G et al (2004) Evidence of secondary poisoning of free-ranging riparian mustelids by anticoagulant rodenticides in France: Implications for conservation of European mink (Mustela lutreola). J Wildl Dis 40:688–695

    CAS  Google Scholar 

  • Garthwaite DG, De’Ath A, Thomas MR (2000) Pesticide usage survey report 154: rodenticide usage on farms in Great Britain growing grassland and fodder crops 1997. DEFRA, London

    Google Scholar 

  • Giraudoux P, Tremolières C, Barbier B, Defaut R, Rieffel D, Bernard N et al (2006) Persistence of bromadiolone anticoagulant rodenticides in Arvicola terrestris populations after field control. Environ Res 102:291–298

    Article  CAS  Google Scholar 

  • Grolleau G, Lorgue G, Nahas K (1989) Toxicité secondaire, en laboratoire, d’un rodenticide anticoagulant (bromadiolone) pour des prédateurs de rongeurs champêtres: Buse variable (Buteo buteo) et hermine (Mustela erminea). EPPO Bull 19:633–648

    Article  Google Scholar 

  • Guan F, Ishii A, Seno H, Watanabe K, Kumazawa T, Suzuki O (1999) A method for simultaneous determination of five anticoagulant rodenticides in whole blood by high-performance liquid chromatography. J Pharm Biomed Anal 21:179–185

    Article  CAS  Google Scholar 

  • Heldbjerg H, Lerche-Jørgensen M, Eskildsen A (2011) Overvågning af de almindelige fuglearter i Danmark 1975–2010. Årsrapport for Punkttællingsprojektet. (Annual report on the Danish Point Count Census 1975–2010). Dansk Ornitologisk Forening, Copenhagen

  • Hoare JM, Hare KM (2006) The impact of brodifacoum on non-target wildlife: gaps in knowledge. N Z J Ecol 30:157–167

    Google Scholar 

  • Jones A (1996) HPLC determination of anticoagulant rodenticide residues in animal livers. Bull Environ Contam Toxicol 56:8–15

    Article  CAS  Google Scholar 

  • Laakso S, Suomalainen K, Koivisto S (2010) Literature review on residues of anticoagulant rodenticides in non-target animals. Nordic Council of Ministers TemaNord, Copenhagen, p 541

    Google Scholar 

  • Lemarchand C, Rosoux R, Berny P (2010) Organochlorine pesticides, PCBs, heavy metals and anticoagulant rodenticides in tissues of Eurasian otters (Lutra lutra) from upper Loire River catchment (France). Chemosphere 80:1120–1124

    Article  CAS  Google Scholar 

  • Lemus JA, Bravo C, García-Montijano M, Palacín C, Ponce C, Magaña M et al (2011) Side effects of rodent control on non-target species: rodenticides increase parasite and pathogen burden in great bustards. Sci Total Environ 409:4729–4734

    Article  CAS  Google Scholar 

  • Lodal J (2010) Resistens hos brune rotter: monitering af resistens hos den brune rotte i Danmark 2008. Danish Pest Infestation Laboratory and Danish Environmental Protection Agency, Copenhagen

    Google Scholar 

  • Lodal J, Hansen OC (2002) Human and environmental exposure scenarios for rodenticides: focus on the Nordic countries. Nordic Council of Ministers TemaNord, Copenhagen, p 575

    Google Scholar 

  • Meiser H (2005) Detection of anticoagulant residues by a new HPLC method in specimens of poisoned animals and a poison control case study. J Anal Toxicol 29:556–563

    CAS  Google Scholar 

  • Mendenhall VM, Pank LF (1980) Secondary poisoning of owls by anticoagulant rodenticides. Wildl Soc Bull 8:311–315

    Google Scholar 

  • Merson MH, Byers RE (1984) Residues of the rodenticide brodifacoum in voles and raptors after orchard treatment. J Wildl Manag 48:212–216

    Article  CAS  Google Scholar 

  • Miljøstyrelsen (2005) Rotter. Lovgivning, bekæmpelse og forebyggelse. Vejledning fra Miljøstyrelsen 1/2005 Danish Environmental Protection Agency. Copenhagen

  • Miljøstyrelsen (2011) Annual statistics on pesticide use 1999–2009. Danish Environmental Protection Agency. Available at: http://www.mst.dk. Accessed 7 Jan 2011

  • Moser VC (2011) Age-related differences in acetylcholinesterase inhibition produced by organophosphorus and N-methyl carbamate pesticides. In: Stoytcheva M (ed) Pesticides in the modern world: pest control and pesticides exposure and toxicity assessment. InTech, Rijeka, pp 495–506

    Google Scholar 

  • Murphy EC, Clapperton BK, Bradfield PMF, Speed HJ (1998) Brodifacoum residues in target and non-target animals following large-scale poison operations in New Zealand podocarp-hardwood forests. N Z J Zool 25:307–314

    Article  Google Scholar 

  • Newton I, Shore RF, Wyllie I, Briks JDS, Dale L (1999) Empirical evidence of side-effects of rodenticides on some predatory birds and mammals. In: Cowan DP, Frear CJ (eds) Advances in vertebrate pest management. Filander-Verlag, Fürth, pp 347–367

    Google Scholar 

  • Normander B, Jensen TS, Henrichs T, Sanderson H, Pedersen AB (2009) Natur og Miljø 2009—Del A: Danmarks miljø under globale udfordringer. NERI research report no. 750, Aarhus University, Aarhus

  • Palazoglu MG, Tor ER, Holstege DM, Galey FD (1998) Multiresidue analysis of nine anticoagulant rodenticides in serum. J Agric Food Chem 46:4260–4266

    Article  CAS  Google Scholar 

  • Salmon TP, Marsh RE (1979) Age as a factor in rodent susceptibility to rodenticides: a review. In: Beck JR (ed) Vertebrate pest control and management materials. American Society for Testing and Materials, Philadelphia, PA, pp 84–99

    Chapter  Google Scholar 

  • Shore RF, Asfar A, Horne JA, Wright J (2000) Rodenticide and lead concentrations in red kite Milvus milvus. Centre for Ecology and Hydrology, Lancaster, UK

    Google Scholar 

  • Shore RF, Malcolm HM, Horne JA, Turner S, Wienburg CL (2001) Rodenticide residues in the kestrel Falco tinnunculus. Centre for Ecology and Hydrology, Lancaster, UK

    Google Scholar 

  • Stone WB, Okoniewski JC, Stedelin JR (1999) Poisoning of wildlife with anticoagulant rodenticides in New York. J Wildl Dis 35:187–193

    CAS  Google Scholar 

  • Stone WB, Okoniewski JC, Stedelin JR (2003) Anticoagulant rodenticides and raptors: recent findings from New York, 1998–2001. Bull Environ Contam Toxicol 70:34–40

    Article  CAS  Google Scholar 

  • Thomas PJ, Mineau P, Shore RF, Champoux L, Martin PA, Wilson LK et al (2011) Second generation anticoagulant rodenticides in predatory birds: Probabilistic characterization of toxic liver concentrations and implications for predatory bird populations in Canada. Environ Int 37:914–920

    Article  CAS  Google Scholar 

  • Thorup K, Sunde P, Jacobsen LB, Rahbek C (2010) Breeding season food limitation drives population decline of the Little Owl Athene noctua in Denmark. Ibis 152:802–814

    Article  Google Scholar 

  • Vandenbrough V, Bouquet-Melou A, De Backer P, Croubels S (2008) Pharmacokinetics of eight anticoagulant rodenticides in mice after single oral administration. J Vet Pharmacol Ther 31:437–445

    Article  Google Scholar 

  • Walker LA, Turk A, Long SM, Wienburg CL, Best J, Shore RF (2008a) Second generation anticoagulant rodenticides in tawny owls (Strix aluco) from Great Britain. Sci Total Environ 392:93–98

    Article  CAS  Google Scholar 

  • Walker LA, Shore RF, Turk A, Pereira MG, Best J (2008b) The predatory bird monitoring scheme: identifying chemical risk to top predators in Britain. Ambio 37:466–471

    Article  Google Scholar 

  • Walker LA, Llewellyn NR, Pereira MG, Potter ED, Sainsbury AW, Shore RF (2010a) Anticoagulant rodenticides in predatory birds 2009: a Predatory Bird Monitoring Scheme (PBMS) report. Centre for Ecology and Hydrology, Lancaster, UK

    Google Scholar 

  • Walker LA, Llewellyn NR, Pereira MG, Potter ED, Sainsbury AW, Shore RF (2010b) Anticoagulant rodenticides in predatory birds 2007–2008: a Predatory Bird Monitoring Scheme (PBMS) report. Centre for Ecology and Hydrology, Lancaster, UK

  • World Health Organization (1995) Environmental health criteria 175: anticoagulant rodenticides. WHO, Geneva

    Google Scholar 

Download references

Acknowledgments

We thank the private taxidermists, the Danish National Veterinary Institute, Copenhagen Airport, natural history museums, and the Danish Society for Animal Welfare for collecting carcasses and tissue samples for the study. Karin R. Petersen and Jeanette Rasmussen are acknowledged for the chemical analyses. Anonymous reviewers are acknowledged for their valuable comments to an earlier draft of the manuscript. The study was financed by the Danish National Forest and Nature Agency.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Morten Elmeros.

Additional information

T.K. Christensen and M. Elmeros contributed equally to this paper

Rights and permissions

Reprints and permissions

About this article

Cite this article

Christensen, T.K., Lassen, P. & Elmeros, M. High Exposure Rates of Anticoagulant Rodenticides in Predatory Bird Species in Intensively Managed Landscapes in Denmark. Arch Environ Contam Toxicol 63, 437–444 (2012). https://doi.org/10.1007/s00244-012-9771-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-012-9771-6

Keywords