Poisoning of reintroduced red kites (Milvus Milvus) in England

Abstract

Programmes to reintroduce predatory birds are resource intensive and expensive, yet there are few long-term studies on the health of these reintroduced birds following release. A total of 326 red kites (Milvus milvus) were released at four sites in England between 1989 and 2006 as part of efforts to reintroduce this species to England and Scotland, resulting in the establishment of several rapidly expanding populations in the wild. Detailed post-mortem examinations were carried out on 162 individuals found dead between 1989 and 2007, involving both released and wild-fledged birds. Toxicological analysis of one or more compounds was performed on 110 of the 162 birds. Poisoning was diagnosed in 32 of these 110 kites, 19 from second-generation anticoagulant rodenticides, 9 from other pesticides and 6 from lead. Criteria for diagnosing anticoagulant rodenticide poisoning included visible haemorrhage on gross post-mortem examination and levels of anticoagulant rodenticide exceeding 100 ng/g, but levels were elevated above 100 ng/g in a further eight red kites without visible haemorrhages, suggesting poisoning may have occurred in more birds. The anticoagulant rodenticides difenacoum and bromadiolone were the most common vertebrate control agents involved during this period. Poisoning of red kites may be slowing their rate of population recovery and range expansion in England. Simple modifications of human activity, such as best practice in rodent control campaigns, tackling the illegal use of pesticides and the use of non-toxic alternatives to lead ammunition, can reduce our impact on red kites and probably other populations of predatory and scavenging species.

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References

  1. Bainbridge I, Evans R, Brad R, et al (2003) Reintroduction of white-tailed eagles (Haliaeetus albicilla) to Scotland. In: Birds of prey in a changing environment. Scottish Natural Heritage, Edinburgh, pp 393–406

  2. Balmer D, Gillings S, Caffrey B et al (2013) Bird atlas 2007–11: the breeding and wintering birds of Britain and Ireland. BTO Books, Thetford

    Google Scholar 

  3. Barnett EA, Fletcher M, Hunter K, et al (2007) Pesticide poisoning of animals in 2006—investigations of suspected incidents in the United Kingdom. DEFRA

  4. Barton N, Houston D (1994) Morphological adaptation of the digestive tract in relation to feeding ecology of raptors. J Zool:133–150

  5. Brown P, Turnbull G, Charman S et al (2005) Analytical methods used in the United Kingdom Wildlife Incident Investigation Scheme for the detection of animal poisoning by pesticides. J Assoc Anal Chem Int 88:204–220

    CAS  Google Scholar 

  6. Carter I (2007) The red kite, 2nd edn. Arlequin Press, Shrewsbury

    Google Scholar 

  7. Cromie R, Newth J, Reeves J (2015) The sociological and political aspects of reducing lead poisoning from ammunition in the UK: why the transition to non-toxic ammunition is so difficult. In: Delahay R, Spray C (eds) Proceedings of the Oxford Lead Symposium, Edward Grey institute, University of Oxford, UK, 10 December 2014. pp 104–120

  8. Dawson A, Garthwaite D (2002) Pesticide usage survey report 185—rodenticide usage by local authorities in Great Britain 2001. Central Science Laboratory York

  9. Erickson W, Urban D (2004) In: United States Environmental Protection Agency (ed) Potential risks of nine rodenticides to birds and nontarget mammals: a comparative approach. Office of Pesticides Programs Environmental Fate and Effects Division, Washington, D.C.

    Google Scholar 

  10. IUCN (1987) Position statement on translocaton of living organisms. IUCN Species Survival Commission, Gland

    Google Scholar 

  11. Kelly TR, Rideout BA, Grantham J et al (2015) Two decades of cumulative impacts to survivorship of endangered California condors in California. Biol Conserv 191:391–399

    Article  Google Scholar 

  12. Lasseur R, Grandemange A, Longin-Sauvageon C et al (2007) Comparison of the inhibition effect of different anticoagulants on vitamin K epoxide reductase activity from warfarin-susceptible and resistant rat. Pestic Biochem Physiol 88:203–208

    CAS  Article  Google Scholar 

  13. Leighton K, Chilvers D, Charles A, Kelly A (2008) Post-release survival of hand-reared tawny owls (Strix aluco) based on radio-tracking and leg-band return data. Anim Welf 17:207–214

    CAS  Google Scholar 

  14. Love JA (1988) The reintroduction of the white-tailed sea eagle to Scotland: 1975–1987. Nature Conservancy Council, Peterborough

    Google Scholar 

  15. Newton I, Shore RF, Wyllie I et al (1999) Empirical evidence of side-effects of rodenticides on some predatory birds and mammals. In: Cowan D, Feare C (eds) Advances in vertebrate pest management. Filander Verlag, Fürth, pp 347–367

    Google Scholar 

  16. Ntampakis D, Carter I (2005) Red kites and rodenticides—a feeding experiment. Br Birds 98:411–416

    Google Scholar 

  17. Pain DJ, Carter I, Sainsbury AW et al (2007) Lead contamination and associated disease in captive and reintroduced red kites Milvus milvus in England. Sci Total Environ 376:116–127

    CAS  Article  PubMed  Google Scholar 

  18. Pesticides Safety Directorate (2008) Strychnine withdrawal. Pesticide Safety Directorate

  19. Development Core Team R (2017) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna

    Google Scholar 

  20. Rattner BA, Horak KE, Warner SE et al (2011) Acute toxicity, histopathology, and coagulopathy in American kestrels (Falco sparverius) following administration of the rodenticide diphacinone. Environ Toxicol Chem 30:1213–1222

    CAS  Article  PubMed  Google Scholar 

  21. Rideout BA, Stalis I, Papendick R et al (2012) Patterns of mortality in free-ranging California condors (Gymnogyps californianus). J Wildl Dis 48:95–112

    Article  PubMed  Google Scholar 

  22. Shore RF, Birks J, Afsar A et al (2003a) Spatial and temporal analysis of second-generation anticoagulant rodenticide residues in polecats (Mustela putorius) from throughout their range in Britain, 1992-1999. Environ Pollut 122:183–193

    CAS  Article  PubMed  Google Scholar 

  23. Shore RF, Fletcher M, Walker LA (2003b) Agricultural pesticides and mammals in Britain. In: Tattersall F, Manley W (eds) Conservation and conflict: mammals and farming in Britain. Linnean Society Occasional Publication. pp 37–50

  24. Shore RF, Malcolm H, Mclennan D et al (2006) Did foot-and-mouth disease control operations affect rodenticide exposure in raptors? J Wildl Manag 70:588–593

    Article  Google Scholar 

  25. Thomas H, Simpson D, Prescott L (1988) The toxic effects of alpha-chloralose. Hum Toxicol 7:285–287

    CAS  Article  PubMed  Google Scholar 

  26. Thomas P, Mineau P, Shore RF et al (2011) Second generation anticoagulant rodenticides in predatory birds: probabilistic characterisation of toxic liver concentrations and implications for predatory bird populations in Canada. Environ Int 37:914–920

    CAS  Article  PubMed  Google Scholar 

  27. Thomas V (2014) Availability and use of lead-free shotgun and rifle cartridges in the UK, with reference to regulations in other jurisdictions. Proceedings of the Oxford Lead Symposium:85–97

  28. Walker LA, Lister L, Long S et al (2007) Wildlife and pollution: 2005/06 annual report. JNCC, Peterborough

    Google Scholar 

  29. Walker LA, Llewellyn NR, Pereira MG, et al (2010) Anticoagulant rodenticides in predatory birds 2007 & 2008: a Predatory Bird Monitoring Scheme (PBMS) report

  30. Walker LA, Shore RF, Turk A et al (2008a) Predators in Britain The predatory bird monitoring scheme: identifying chemical risks to top predators in Britain. Ambio 37:466–471

    Article  PubMed  Google Scholar 

  31. Walker LA, Turk A, Long SM et al (2008b) Second generation anticoagulant rodenticides in tawny owls (Strix aluco) from Great Britain. Sci Total Environ 392:93–98

    CAS  Article  PubMed  Google Scholar 

  32. Zar J (1974) Circular distributions: hypothesis testing. In: Biostatistical analysis. Prentice-Hall International Ltd, London, pp 440–469

    Google Scholar 

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Acknowledgements

The authors thank the following for their contributions to this study: James Kirkwood for initiating the study of disease in reintroduced red kites, Keith Bowey, Derek Holman, the late Peter Newbery, Helen Olive, Doug Simpson, Nigel Snell and Peter Stevens for collecting and submitting red kite carcasses, Jonathan Cracknell, Andrew Cunningham, Yedra Feltrer, Edmund Flach, Tracy Howard, Iain McGill, Romain Pizzi and Ann Pocknell for carrying out post-mortem examinations, Belinda Clark for pathological support, Shinto Kunjamma John and Shaheed Karl Macgregor for microbiological support, Ilona Furrokh, Gillian Ahearne, Christine Dean, Judith Howlett, Tony Fitzgerald, Joanne Korn, Janet Markham and Matthew Rendle for the care of hospitalised red kites, the analytical chemistry team in the Wildlife Incident Unit at Fera (lead by Ainsley Jones, Andrew Charlton and Sheonaidh Charman), Becki Lawson for scientific input into this paper and all the members of the public that have reported red kite carcasses.

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Correspondence to Jenny E. Jaffe.

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Molenaar, F.M., Jaffe, J.E., Carter, I. et al. Poisoning of reintroduced red kites (Milvus Milvus) in England. Eur J Wildl Res 63, 94 (2017). https://doi.org/10.1007/s10344-017-1152-z

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Keywords

  • Birds of prey
  • Scavenger
  • Reintroduction
  • Pathology
  • Toxicology
  • Anticoagulant rodenticide
  • Pesticide
  • Lead