Environmental Monitoring and Assessment

, Volume 186, Issue 2, pp 895–906 | Cite as

Exposure pathways of anticoagulant rodenticides to nontarget wildlife

  • John E. Elliott
  • Sofi Hindmarch
  • Courtney A. Albert
  • Jason Emery
  • Pierre Mineau
  • France Maisonneuve


Second-generation anticoagulant rodenticides are widely reported to contaminate and poison nontarget wildlife, primarily predatory birds and mammals. Exposure pathways, however, have not been well defined. Here, we examined potential movement of rodenticides from deployment of bait to exposure of small mammals and other biota. At two adjacent working farms, we placed baits containing either brodifacoum or bromadiolone. We monitored movement of those compounds to the surrounding environment by collecting small mammals, birds, and invertebrates. Similar collections were made at a third agricultural setting without active bait deployment, but located among intensive livestock production and regular rodenticide use by farmers. Livers and whole invertebrate samples were analyzed for rodenticides using a sensitive LC-MSMS method. Norway rats (Rattus norvegicus) from both baited and non-baited farms had residues of brodifacoum or bromadiolone, implicating rats as an important exposure pathway to wildlife. Among 35 analyzed nontarget small mammals, a single vole had high hepatic residues (18.6 μ/g), providing some indication of a small mammal pathway. One song sparrow (Melospiza melodia) sample from a baited farm contained 0.073 μg/g of brodifacoum in liver, while 0.39 μg/g of diphacinone was measured in a pool of carrion beetles (Dermestes spp.) from the non-baited farm area, implicating avian and invertebrate components in exposure pathways. Regurgitated pellets of barn owl (Tyto alba) selected randomly from baited farms contained no detectable rodenticide residues, while 90 % of owl pellets collected from a variety of farms, and selected for the presence of rat fur, contained detectable anticoagulant residues. We recorded behavior of a captive sample of a representative songbird, the house sparrow (Passer domesticus); they readily entered bait stations and fed on (unloaded) bait.


Anticoagulants Exposure pathways Nontargets Raptor Rat 



We thank the many cooperating farmers, particularly those at the intensive study sites in Delta, for making this work possible. Sandi Lee is thanked for her assistance with field studies. We thank the staff at the National Wildlife Research Center staff for specimen archiving and rodenticide residue analysis. Funding was primarily from the Pesticide Science Fund of Environment Canada.


  1. Albert, C. A., Mineau, P., Wilson, L. K., Trudeau, S., & Elliott, J. E. (2010). Rodenticide residues and autopsy data for three owl species from British Columbia, Canada. Archives Environmental Contamination and Toxicology, 58, 451–459.CrossRefGoogle Scholar
  2. Brakes, C. R., & Smith, C. H. (2005). Exposure of non-target small mammals to rodenticides: short-term effects, recovery and implications for secondary poisoning. Journal of Applied Ecology, 42, 118–128.CrossRefGoogle Scholar
  3. Buckle, A. P., Prescott, C. V., & Ward, K. J. (1994). Resistance to the first and second generation anticoagulant rodenticides—a new perspective. In W. S. Halverson & R. E. Marsh (Eds.), Proceedings of the Sixteenth Vertebrate Pest Conference (pp. 138–144). Lincoln: University of Nebraska–Lincoln.Google Scholar
  4. Christensen, T. K., Lassen, P., & Elmeros, M. (2012). High exposure rates of anticoagulant rodenticides in predatory bird species in intensively managed landscapes in Denmark. Archives of Environmental Contamination and Toxicology, 63, 437–444.CrossRefGoogle Scholar
  5. Clare, J., Brantingham, P., & Brantingham, P. (2010). Problem-oriented policing approaches to outdoor cannabis growing (Public Safety Canada. Report No. 005 ISBN No.: 978-1-100-19935-1). ON: Ottawa.Google Scholar
  6. Cox, P. R., & Smith, R. H. (1990). Rodenticide ecotoxicology: assessing non-target population effects. Functional Ecology, 4, 315–320.CrossRefGoogle Scholar
  7. Cox, P. R., & Smith, R. H. (1992). Rodenticide ecotoxicology: pre-lethal effects of anticoagulants on rat behaviour. In J. E. Borrecco & R. E. Marsh (Eds.), Proceedings of the fifteenth vertebrate pest conference (pp. 165–170). Davis: University of California.Google Scholar
  8. Eason, C. T., Murphy, E., Wright, G. R., & Spurr, E. B. (2002). Assessment of risks of brodifacoum to non-target birds and mammals in New Zealand. Ecotoxicology, 11, 35–48.CrossRefGoogle Scholar
  9. Gabriel, M. W., Woods, L. W., Poppenga, R., Sweitzer, R. A., Thompson, C., Matthews, S. M., Higley, J. M., et al. (2012). Anticoagulant rodenticides on our public and community lands: spatial distribution of exposure and poisoning of a rare forest carnivore. PLoS One, 7, e40163.CrossRefGoogle Scholar
  10. Hegdal, P. L., & Colvin, B. A. (1988). Potential hazard to eastern screech-owls and other raptors of brodifacoum bait used for vole control in orchards. Environmental Toxicology and Chemistry, 7, 245–260.CrossRefGoogle Scholar
  11. Himsworth, C. G., Feng, A. Y., Parsons, K., Kerr, T., & Patrick, D. M. (2013). Using experiential knowledge to understand urban rat ecology: a survey of Canadian pest control professionals. Urban Ecosystems, 16, 341–350.CrossRefGoogle Scholar
  12. Hindmarch, S., Krebs, E. A., Elliott, J. E., & Green, D. J. (2012). Do landscape features predict the presence of barn owls in a rapidly changing agricultural landscape? Landscape and Urban Planning, 107, 255–262.CrossRefGoogle Scholar
  13. Hoare, J. M., & Kelly, K. M. (2006). The impact of brodifacoum on non-target wildlife: gaps in knowledge. New Zealand Journal of Ecology, 30, 157–167.Google Scholar
  14. Howald, G. R. (1997). The risk of non-target species poisoning from brodifacoum used to eradicate rats from Langara Island, British Columbia, Canada (PhD dissertation), The University of British Columbia. BC: Vancouver.Google Scholar
  15. Howald, G. R., Mineau, P., Elliott, J. E., & Cheng, K. M. (1999). Brodifacoum poisoning of avian scavengers during rat control on a seabird colony. Ecotoxicology, 8, 431–447.CrossRefGoogle Scholar
  16. Lambert, O., Pouliquen, H., Larhantec, M., Thorin, C., & L'Hostis, M. (2007). Exposure of raptors and waterbirds to anticoagulant rodenticides (difenacoum, bromadiolone, coumatetralyl, coumafen, brodifacoum): epidemiological survey in Loire Atlantique (France). Bulletin of Environmental Contamination and Toxicology, 79, 91–94.CrossRefGoogle Scholar
  17. Lima, L. L., & Salmon, T. P. (2010). Assessing some potential environmental impacts from agricultural anticoagulant uses. In R. M. Timm & K. A. Fagerstone (Eds.), Proceedings of the 24th Vertebrate Pest Conference (pp. 199–203). Davis: University of California Davis.Google Scholar
  18. Mendenhall, V. M., & Pank, L. F. (1980). Secondary poisoning of owls by anticoagulant rodenticides. Wildlife Society Bulletin, 8, 311–315.Google Scholar
  19. Merson, M. H., Byers, R. E., & Kaukeinen, D. E. (1984). Residues of the rodenticide brodifacoum in voles and raptors after orchard treatment. Journal of Wildlife Management, 48, 212–216.CrossRefGoogle Scholar
  20. Murray, M. (2011). Anticoagulant rodenticide exposure and toxicosis in four species of birds of prey presented to a wildlife clinic in Massachusetts, 2006–2010. Journal of Zoo and Wildlife Medicine, 42, 88–97.CrossRefGoogle Scholar
  21. Newton, I., Wyllie, I., & Freestone, P. (1990). Rodenticides in British barn owls. Environmental Pollution, 68, 101–117.CrossRefGoogle Scholar
  22. Newton, I., Wyllie, I., Gray, A., & Eadsforth, C. V. (1994). The toxicity of the rodenticide flocoumafen to barn owls and its elimination via pellets. Pesticide Science, 41, 187–193.CrossRefGoogle Scholar
  23. Newton, I., Afsarm A., Dale, L,, Finnie, J., Shore, R. F., Wright, J., Wyatt, C., Wyllie, I. (2000). Wildlife and Pollution. 1998/99 Annual Report, JNCC Report, No.305.Google Scholar
  24. Newton, I., Shore, R. F., Wyllie, I., Birks, J. D. S., & Dale, L. (1999). Empirical evidence of side-effects of rodenticides on some predatory birds and mammals. In H. J. Pelz, D. P. Cowan, & C. J. Feare (Eds.), Advances in Vertebrate Pest Management (pp. 347–367). Furth: Filander.Google Scholar
  25. Nimish, B. V., Hulse, C. S., Meteyer, C. U., & Rice, C. P. (2013). Evidence of songbird intoxication from Rozol® application at a black-tailed prairie dog colony. Journal of Fish and Wildlife Management, 4, 97–103.CrossRefGoogle Scholar
  26. Parmar, G., Bratt, H., Moore, R., & Batten, P. L. (1987). Evidence for a common binding-site in vivo for the retention of anticoagulants in rat liver. Human Toxicology, 6, 431–432.Google Scholar
  27. Pimentel, D., Zuniga, R., & Morrison, D. (2005). Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics, 52, 273–288.CrossRefGoogle Scholar
  28. PMRA. 2006. Re-evaluation Decision Document. Brodifacoum, Bromadiolone, Chlorophacinone, Diphacinone and Warfarin. RRD2006-11. Pest Management Regulatory Agency, Health Canada, Ottawa, Ontario, Canada.Google Scholar
  29. PMRA. 2010. Proposed Risk Mitigation Measures for Eight Rodenticides. REV2010-17. Pest Management Regulatory Agency, Health Canada, Ottawa, Ontario, Canada.Google Scholar
  30. Quy, R. J., Cowan, D. P., Prescott, C. V., Gill, J. E., Kerins, G. M., Dunsford, G., Jones, A., & Macnicoll, A. D. (1995). Control of a population of Norway rats resistant to anticoagulant rodenticides. Pesticide Science, 45, 247–256.CrossRefGoogle Scholar
  31. Rattner, B. A., Horak, K. E., Warner, S. E., Day, D. D., Meteyer, C. U., Volker, S. F., Eisemann, J. D., & Johnston, J. J. (2011). Acute toxicity, histopathology, and coagulopathy in American kestrels (Falco sparverius) following administration of the rodenticide diphacinone. Environmental Toxicology and Chemistry, 30, 1213–1222.CrossRefGoogle Scholar
  32. Rattner, B. A., Horak, K. E., Lazarus, R. S., Eisenreich, K. M., Meteyer, C. U., Volker, S. F., Campton, C. M., Eisemann, J. D., & Johnston, J. J. (2012). Assessment of toxicity and potential risk of the anticoagulant rodenticide diphacinone using Eastern screech-owls (Megascops asio). Ecotoxicology, 21, 1–15.CrossRefGoogle Scholar
  33. Riley, S. P. D., Bromley, C., Poppenga, R. H., Uzai, F. A., Whited, L., & Sauvajot, R. M. (2007). Anticoagulant exposure and notoedric mange in bobcats and mountain lions in urban southern California. Journal of Wildlife Management, 7, 1874–1884.CrossRefGoogle Scholar
  34. Shore, R. F., Birks, J. D. S., Freestone, P., & Kitchener, A. C. (1996). Second-generation rodenticides and polecats (Mustela putorius) in Britain. Environmental Pollution, 91, 279–282.CrossRefGoogle Scholar
  35. Stone, W. B., Okoniewski, J. C., & Stedelin, J. R. (1999). Poisoning of wildlife with anticoagulant rodenticides in New York. Journal of Wildlife Disease, 35, 187–193.CrossRefGoogle Scholar
  36. Stone, W. B., Okoniewski, J. C., & Stedelin, J. R. (2003). Anticoagulant Rodenticides and Raptors: Recent Findings from New York, 1998–2001. Bulletin of Environmental Contamination and Toxicology, 70, 34–40.CrossRefGoogle Scholar
  37. Thijssen, H. H. W. (1995). Warfarin-based rodenticides: mode of action and mechanism of resistance. Pesticide Science, 43, 73–78.CrossRefGoogle Scholar
  38. Thomas, P. H., Mineau, P., Shore, R. F., Champoux, L., Martin, P. A., Wilson, L. K., Fitzgerald, G., & Elliott, J. E. (2011). Second generation anticoagulant rodenticides in predatory birds: probabilistic characterization of toxic liver concentrations and implications for predatory bird populations in Canada. Environment International, 37, 914–920.CrossRefGoogle Scholar
  39. Tobin, M. E., Sugihara, R. T., Koehler, A. E., & Ueunten, G. R. (1996). Seasonal activity and movements of Rattus rattus (Rodentia, Muridae) in a Hawaiian macadamia orchard. Mammalia, 60, 3–13.CrossRefGoogle Scholar
  40. US EPA. (2004). Potential Risks of Nine Rodenticides to Birds and Nontarget Mammals: A Comparative Approach. Environmental Protection Agency, Office of Pesticides Programs, Environmental Fate and Effects Division, Washington, DC, USAGoogle Scholar
  41. US EPA. (2011). Risks of Non-Compliant Rodenticides to Non-target Wildlife. Background Paper for Science Advisory Panel on Notice of Intent to Cancel Non-RMD compliant Rodenticide Products. Environmental Protection Agencey, Office of Chemical Safety and Pollution Prevention. Washington, DC, USAGoogle Scholar
  42. Walker, L. A., Turk, A., Long, S. M., Wienburg, C. L., Best, J., & Shore, R. F. (2008). Second generation anticoagulant rodenticides in tawny owls (Strix aluco) from Great Britain. Science of the Total Environment, 392, 93–98.CrossRefGoogle Scholar
  43. Watt, B. E., Proudfoot, A. T., Bradberry, S. M., & Vale, J. A. (2005). Anticoagulant rodenticides. Toxicological Reviews, 24, 259–269.CrossRefGoogle Scholar

Copyright information

© Her Majesty the Queen in Right of Canada as represented by: Environment of Canada 2013

Authors and Affiliations

  • John E. Elliott
    • 1
  • Sofi Hindmarch
    • 2
  • Courtney A. Albert
    • 3
  • Jason Emery
    • 4
  • Pierre Mineau
    • 5
  • France Maisonneuve
    • 5
  1. 1.Science and Technology Branch, Environment CanadaPacific and Yukon RegionDeltaCanada
  2. 2.RichmondCanada
  3. 3.Canadian Wildlife Service, Environment CanadaPacific and Yukon RegionDeltaCanada
  4. 4.SOLITUDO Environmental Services Inc.DeltaCanada
  5. 5.Science and Technology Branch, Environment CanadaNational Wildlife Research CenterOttawaCanada

Personalised recommendations