, Volume 22, Issue 6, pp 974–984 | Cite as

Monitoring agricultural rodenticide use and secondary exposure of raptors in Scotland

  • J. HughesEmail author
  • E. Sharp
  • M. J. Taylor
  • L. Melton
  • G. Hartley


Despite the documented risk of secondary poisoning to non-target species by anticoagulant rodenticides there is no statutory post-approval monitoring of their use in the UK. This paper presents results from two Scottish monitoring schemes for the period 2000–2010; recording rodenticide use on arable farms and the presence of residues in raptor carcasses. More than three quarters of arable farms used anticoagulant rodenticides; predominately the second generation compounds difenacoum and bromadiolone. There was widespread exposure to anticoagulant rodenticides in liver tissues of the raptor species tested and the residues encountered generally reflected agricultural use patterns. As found in other studies, Red Kites (Milvus milvus) appeared to be particularly vulnerable to rodenticide exposure, 70 % of those sampled (n = 114) contained residues and 10 % died as a result of rodenticide ingestion. More unexpectedly, sparrowhawks (Accipiter nisus), which prey almost exclusively on birds, had similar exposure rates to species which prey on rodents. Although, with the exception of kites, confirmed mortality from rodenticides was low, the widespread exposure recorded is concerning. Particularly when coupled with a lack of data about the sub-lethal effects of these compounds. This raises questions regarding whether statutory monitoring of use is needed; both to address whether there are deficiencies in compliance with approval conditions or whether the recommended risk management procedures are themselves adequate to protect non-target wildlife.


Anticoagulant rodenticides Secondary exposure Raptors 



The authors would like to thank those who have assisted in the coordination and collection of rodenticide use data (Chris Bierley, Chris Griffiths, John Kerr, Gillian Reay, Louis Thomas, Andrew Walker and Jeremy Snowden) and those who conducted residue analyses (Anna Giela and Jennifer Watson). The authors would also like to thank the paper’s anonymous reviewers whose comments greatly improved the manuscript.

Conflict of interest

The post-registration surveillance of wildlife poisoning is funded by the pesticide industry under the Food and and Environmental Protection Act 1985 (FEPA) and the Control of Pesticides Regulations (COPR). The monitoring of rodenticide use is funded by the Scottish Government. The authors declare that they have no conflict of interest.

Ethical standards

All experiments comply with the current laws of the country in which they were performed.


  1. 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 58:451–459CrossRefGoogle Scholar
  2. Anonymous (2007) Difenacoum pesticide fact sheet. Environmental Protection Agency, Seattle, p 34Google Scholar
  3. Berny P, Gaillet JR (2008) Acute poisoning of red kites (Milvus milvus) in France: data from SAGIR network. J Wildl Dis 44:417–426Google Scholar
  4. 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 35:1817–1829CrossRefGoogle Scholar
  5. Booth LH, Eason CT, Spurr EB (2001) Literature review of the acute toxicity and persistence of brodifacoum to invertebrates. Sci Conserv 177:1–9Google Scholar
  6. Brakes CR, Smith RH (2005) Exposure of non-target small mammals to rodenticides: short-term effects, recovery and implications for secondary poisoning. J Appl Ecol 42:118–128CrossRefGoogle Scholar
  7. Buckle AP, Prescott CV, Ward KJ (1994) Resistance to the first and second generation anticoagulant rodenticides—a new perspective. In: Proceedings of the sixteenth vertebrate pest conference, University of California, Davis, pp 138–144Google Scholar
  8. Carter I, Burn A (2000) Problems with rodenticides: the threat to red kites and other wildlife. Br Wildl 11:192–197Google Scholar
  9. Cox P, Smith RH (1992) Rodenticide ecotoxicology: pre-lethal effects of anticoagulants on rat behaviour. In: Proceedings of the fifteenth vertebrate pest conference, University of Nebraska, Lincoln, pp 65–170Google Scholar
  10. Dowding CV, Shore RF, Worgan R, Baker PJ, Harris S (2010) Accumulation of anticoagulant rodenticides in a non-target insectivore, the European hedgehog (Erinaceus europaeus). Environ Pollut 158:161–166CrossRefGoogle Scholar
  11. Dunlevy PA, Campbell EW, Lindsey GW (2000) Broadcast application of a placebo rodenticide bait in a native Hawaiian forest. Int J Biodeter Biodegrad 45:199–208CrossRefGoogle Scholar
  12. DuVall MD, Murphy MJ, Ray AC, Reagor JC (1989) Case studies on second-generation anticoagulant rodenticide toxicities in non target species. J Vet Diagn Invest 1:66–68CrossRefGoogle Scholar
  13. Eason CT, Murphy E (2001) Recognising and reducing secondary and tertiary risks associated with brodifacoum. In: Johnston JJ (ed) Pesticides and wildlife. American chemical society symposium series 771, pp 157–163Google Scholar
  14. Empson RA, Miskelly CM (1999) The risks, costs and benefits of using brodifacoum to eradicate rats from kapiti Island, New Zealand. N Z J Ecol 23:241–254Google Scholar
  15. Erickson W, Urban D (2004) Potential risks of nine rodenticides to birds and non-target mammals: a comparative approach. Environmental protection agency office of prevention, pesticides and toxic substances, Washington, DCGoogle Scholar
  16. Fisher PM (2009) Residual concentrations and persistence of the anticoagulant rodenticides brodifacoum and diphacinone in fauna dissertation. Lincoln University, New ZealandGoogle Scholar
  17. Hughes J (2012) Pesticide usage in Scotland: rodenticides on arable farms 2000 to 2010. Scottish Government Agriculture Food and Rural Communities Directorate, EdinburghGoogle Scholar
  18. Hunter K, Sharp EA (1988) Modification to procedures for the determination of chlorophacinone and for multi-residue analysis of rodenticides in animal tissues. J Chromatogr 437:301–305CrossRefGoogle Scholar
  19. Joermann G (1998) A review of secondary-poisoning studies with rodenticides. Bull OEPP 28:157–176CrossRefGoogle Scholar
  20. Johnston JJ, Pitt WC, Sugihara RT, Eisemann JD, Primus TM, Holmes MJ, Crocker J, Hart A (2005) Probabilistic risk assessment for snails, slugs and endangered honeycreepers in diphacinone rodenticide baited areas on Hawaii, USA. Environ Toxicol Chem 24:1557–1567CrossRefGoogle Scholar
  21. Leemus JA, Bravo C, Garcia-Montijano M, Palacín C, Ponce C, Magańa M, Alonso JC (2011) Side effects of rodent control on non-target species: rodenticides increase parasite and pathogen burden in great bustards. Sci Total Environ 409:4729–4734CrossRefGoogle Scholar
  22. Meehan AP (1984) Rats and mice: their biology and control. Rentokil Limited, East GrinsteadGoogle Scholar
  23. Morgan DR, Wright GR, Ogilvie SC, Pierce R, Thompson P (1996) Assessment of the environmental impact of brodifacoum during rodent eradication operations in New Zealand. In: Proceedings of the seventeenth vertebrate pest conference, Rhonert Park, California, pp 213–218Google Scholar
  24. Myllymäki A, Pihlava J, Tuuri H (1999) Predicting the exposure and risk to predators and scavengers associated with using single-dose second-generation anticoagulants against field rodents. In: Cowan DP, Freare CJ (eds) Advances in vertebrate pest management. Filander Verlag, Furth, pp 387–404Google Scholar
  25. Naim M, Hafidzi MN, Azhar K, Jalila A (2010) Growth performance of nestling barn owls, Tyto Alba javanica in rat baiting area in Malaysia. ARPN J Agric Biol Sci 5:1–13CrossRefGoogle Scholar
  26. Newton I, Wyllie I, Freestone P (1990) Rodenticides in British barn owls. Environ Pollut 68:01–17CrossRefGoogle Scholar
  27. Newton I, Shore RF, Wyllie I, Birks JDS, Dale L (1999) Empirical evidence of side-effects of rodenticides on some predatory birds and mammals. In: Cowan DP, Feare CJ et al (eds) Advances in vertebrate pest management. Filander Verlag, Fürth, pp 347–367Google Scholar
  28. Ntampakis D, Carter I (2005) Red Kite and rodenticides—a feeding experiment. Br Birds 98:411–416Google Scholar
  29. Parmar G, Bratt H, Moore R, Batten PL (1987) Evidence for a common binding site in vivo for the retention of anticoagulants in rat liver. Hum Toxicol 6:431–432Google Scholar
  30. Rammel CG, Hoogenboom JJL, Cotter M, Williams JM, Bell J (1984) Brodifacoum residues in target and non-target animals following rabbit poisoning trials. N Z J Exp Agric 12:107–111Google Scholar
  31. Rattner BA, Horak KE, Warner SE, Day DD, Meteyer CU, Volker SF, Eisemann JD, Johnston JJ (2011) Acute toxicity, histopathology, and coagulopathy in American kestrels (Falco sparverius) following administration of the rodenticide diphacinone. Environ Toxicol Chem 30:1213–1222CrossRefGoogle Scholar
  32. Record CR, Marsh RE (1988) Rodenticide residues in animal carcasses and their relevance to secondary hazards. In: Proceedings of the thirteenth vertebrate pest conference, University of Nebraska, Lincoln, pp 163–168Google Scholar
  33. Redfern R, Gill JE, Hadler MR (1976) Laboratory evaluation of WBA 8119 as a rodenticide for use against warfarin resistant and non-resistant rats and mice. J Hyg 77:419–426CrossRefGoogle Scholar
  34. Riley SPD, Bromley C, Poppenga RH, Uzal FA, Whited L, Sauvajot RM (2007) Anticoagulant exposure and notoedric mange in bobcats and mountain lions in urban southern California. J Wildlife Manage 71:1874–1884CrossRefGoogle Scholar
  35. Sánchez-Barbudo IS, Camarero PR, Mateo R (2012) Primary and secondary poisoning by anticoagulant rodenticides of non-target animals in Spain. Sci Total Environ 420:280–288CrossRefGoogle Scholar
  36. Sharp EA, Melton LM, Taylor MJ, Watson JE (2012) Pesticide poisoning of animals in 2011: A report of investigations in Scotland. Scottish Government Agriculture Food and Rural Communities Directorate, EdinburghGoogle Scholar
  37. Shore RF, Birks JDS, Afsar A, Wienburg CL, Kitchener AC (2003) Spatial and temporal analysis of second-generation anticoagulant rodenticide residues in polecats (Mustela putorius) from throughout their range in Britain, 1992–1999. Environ Pollut 122:183–193CrossRefGoogle Scholar
  38. Shore RF, Malcolm HM, McLennan D, Turk A, Walker LA, Wienburg CL, Burn AJ (2006) Did foot-and-mouth disease-control operations affect rodenticide exposure in raptors? J Wildl Manag 70:588–593CrossRefGoogle Scholar
  39. Shore RF, Walker LA, Thomas GO, Barber JL, Martin FR, Jones KC, Beresford NA, Rowland P, Pickup RW (2007) Review of the predatory bird monitoring scheme (PBMS) 2006. JNCC Report, No. 400Google Scholar
  40. Spurr EB, Drew KW (1999) Invertebrates feeding on baits used for vertebrate pest control in New Zealand. N Z J Ecol 23:167–173Google Scholar
  41. Stone WB, Okonlewski JC, Stedelin JR (1999) Poisoning of wildlife with anticoagulant rodenticides in New York, 1998–2001. Bull Environ Contam Toxicol 70:34–40CrossRefGoogle Scholar
  42. Thomas PJ, Mineau P, Shore RF, Champoux L, Martin PA, Wilson LK, Fitzgerald G, Elliot JE (2011) Second generation anticoagulant rodenticides in predatory birds: probabilistic characterisation of toxic liver concentrations and implications for predatory bird populations in Canada. Environ Int 37:914–920CrossRefGoogle Scholar
  43. Tosh DG, Shore RF, Jess S, Withers A, Bearhop S, Montgomery WI, McDonald RA (2011) User behaviour, best practice and the risks of non-target exposure associated with anticoagulant rodenticide use. J Environ Manag 92:1503–1508CrossRefGoogle Scholar
  44. Tosh DG, McDonald RA, Bearhop S, Llewellyn NR, Montgomery WI, Shore RF (2012) Rodenticide exposure in wood mouse and house mouse populations on farms and potential secondary risk to predators. Ecotoxicology 21:1325–1332CrossRefGoogle Scholar
  45. Vandenbroucke V, Bousquet-Melou A, De Backer P, Croubels S (2008) Pharmacokinetics of eight anticoagulant rodenticides in mice after single oral administration. J Vet Pharmacol Ther 31:437–445CrossRefGoogle Scholar
  46. Walker LA, Shore RF, Turk A, Pereira MG, Best J (2008) The predatory bird monitoring scheme: identifying chemical risks to top predators in Britain. Ambio 37:466–471CrossRefGoogle Scholar
  47. Walker LA, Llewellyln NR, Pereira MG, Potter ED, Molenaar FM, Sainsbury AW, Shore RF (2010) Anticoagulant rodenticides in predatory birds 2007 & 2008: a predatory bird monitoring scheme (PBMS) report. Centre for Ecology and Hydrology, LancasterGoogle Scholar
  48. Wyllie I (1995) Potential secondary poisoning of barn owls by rodenticides. Pestic Outlook 6:19–25Google Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2013

Authors and Affiliations

  • J. Hughes
    • 1
    Email author
  • E. Sharp
    • 1
  • M. J. Taylor
    • 1
  • L. Melton
    • 1
  • G. Hartley
    • 1
  1. 1.Science and Advice for Scottish Agriculture (SASA), Scottish GovernmentEdinburghUK

Personalised recommendations