Investigating infectious disease threats to the recovery of the European polecat in Britain

Abstract

The European polecat (Mustela putorius) almost became extinct in Britain in the early twentieth century, but populations are now recovering. As seen in other endangered carnivore populations, disease is one potential threat to recovery. This study assessed exposure of wild polecats (n = 149) to three, multi-host pathogens which could limit reproduction and/or cause morbidity and mortality. Serum, lung and brain samples were collected from polecats which died from 2011 to 2016 across Britain. Exposure to Toxoplasma gondii and 12 Leptospira serovars was assessed serologically by antibody detection using the latex agglutination test and microscopic agglutination test, respectively, and the presence of canine distemper virus (CDV) RNA in lung and brain tissue samples was assessed using PCR. Generalised linear models were used to test for relationships between exposure to each pathogen and season, sex, age, and location. All organ samples tested PCR negative for CDV (95% CI 0.00–0.05%). There was evidence of frequent exposure to T. gondii with a recorded seroprevalence of 71.8% (95% CI 64.2–79.4%) and moderate exposure to Leptospira serovars, 14.5% (95% CI 8.6–20.4%). Season, sex, age, and location were not significantly associated with exposure to T. gondii or Leptospira serovars. Evidence of exposure to T. gondii and Leptospira serovars in European polecats could potentially affect mortality, longevity or fecundity. Further studies are warranted to assess the impact of these pathogens on polecat populations in Britain.

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

Fig. 1

References

  1. Alexander KA, McNutt JW, Briggs MB, Standers PE, Funston P, Hemson G, Keet D, van Vuuren M (2010) Multi-host pathogens and carnivore management in southern Africa. Comp Immunol Microbiol Infect Dis 33(3):249–265

    CAS  PubMed  Article  Google Scholar 

  2. Barros M, Cabezón O, Dubey J, Almería S, Puig Ribas M, Escobar LE, Ramos B, Medina Vogel G (2018) Toxoplasma gondii infection in wild mustelids and cats across an urban-rural gradient. PLoS ONE 13(6):e0199085

    PubMed  PubMed Central  Article  Google Scholar 

  3. Birks J (2015) Polecats the British natural history collection, vol 5. Whittet Books Ltd, Essex, pp 82–97

    Google Scholar 

  4. Birks JDS (1998) Secondary rodenticide poisoning risk arising from winter farmyard use by the European polecat Mustela putorius. Biol Cons 85:233–240

    Article  Google Scholar 

  5. Birks JDS (2008) The Polecat Survey of Britain 2004–2006. A report on the Polecat's distribution, status and conservation. The Vincent Wildlife Trust, Ledbury

    Google Scholar 

  6. Burns R, Williams ES, O'Toole D, Dubey JP (2003) Toxoplasma gondii infections in captive black-footed ferrets (Mustela nigripes) 1992–1998: clinical signs, serology, pathology, and prevention. J Wildl Dis 39(4):787–797

    PubMed  Article  Google Scholar 

  7. Burrells A, Bartley PM, Zimmer IA, Roy S, Kitchener AC, Meredith A, Wright SE, Innes EA, Katzer F (2013) Evidence of the three main clonal Toxoplasma gondii Lineages from wild mammalian carnivores in the UK. Parasitology 140(14):1768–1776

    CAS  PubMed  Article  Google Scholar 

  8. Costa M, Fernandes C, Birks JDS, Kitchener AC, Santos-Reis M, Bruford M (2013) The genetic legacy of the 19th-century decline of the British polecat: evidence for extensive introgression from feral ferrets. Mol Ecol 22(20):5130–5147

    CAS  PubMed  Article  Google Scholar 

  9. Croose E (2016) The distribution and status of the polecat (Mustela putorius) in Britain 2014–2015. The Vincent Wildlife Trust Ledbury

  10. Delahay R, Frölich K (2000) Absence of antibodies against canine distemper virus in free-ranging populations of the Eurasian badger in great Britain. J Wildl Dis 36(3):576–579

    CAS  PubMed  Article  Google Scholar 

  11. Ellis WA (2015) Animal leptospirosis. In: Adler B (ed) Leptospira and leptospirosis. Current topics in microbiology and immunology, Springer, Berlin, Heidelberg, pp 99–137

    Google Scholar 

  12. Frank RK (2001) An outbreak of toxoplasmosis in farmed mink (Mustela vison S.). J Vet Diagn Invest 13(3):245–249

    CAS  PubMed  Article  Google Scholar 

  13. Harrington LA, Gelling M, Simpson V, Harrington A, Macdonald DW (2012) Notes on the health status of free-living, non-native American mink, Neovison vison, in southern England. Eur J Wildl Res 58(5):875–880

    Article  Google Scholar 

  14. Hollings T, Jones M, Mooney N, McCallum H (2013) Wildlife disease ecology in changing landscapes: mesopredator release and toxoplasmosis. Int J Parasitol Paras Wildl 2:110–118

    Article  Google Scholar 

  15. Horton NJ, Kleinman K (2015) Using R and RStudio for data management, statistical analysis, and graphics, 2nd edn. Chapman and Hall/CRC, Boca Raton

    Google Scholar 

  16. Hughes JM, Thomasson D, Craig PS, Georgin S, Pickles A, Hide G (2008) Neospora caninum: Detection in wild rabbits and investigation of co-infection with Toxoplasma gondii by PCR analysis. Exp Parasitol 120(3):255–260

    CAS  PubMed  Article  Google Scholar 

  17. Johnson N, Mansfield KL, Marston DA, Wilson C, Goddard T, Selden D, Hemson G, Edea L, van Kesteren F, Shiferaw F, Stewart AE, Sillero−Zubiri C, Fooks AR (2010) A new outbreak of rabies in rare Ethiopian wolves (Canis simensis). Arch Virol 155(7):1175–1177

    CAS  PubMed  Article  Google Scholar 

  18. Kiupel M, Perpiñán D (2014) Viral diseases of ferret biology and diseases of the ferret, 3rd edn. Wiley, Ames, pp 439–517

    Google Scholar 

  19. Langley PJW, Yalden DW (1977) The decline of the rarer carnivores in Great Britain during the nineteenth century. Mammal Rev 7:95–116

    Article  Google Scholar 

  20. Mathews F, Kubasiewicz M, Gurnell J, Harrower C, McDonald R, Shore R (2018) A review of the population and conservation status of British Mammals: technical summary. Natural, England, Peterborough

    Google Scholar 

  21. Matson GM, Van Daele L, Goodwin E, Aumiller L, Reynolds H, Hristienko H (1993) A laboratory manual for cementum age determination of Alaska Brown Bear PM1 teeth. Matson's Lab, Milltown, Montana

    Google Scholar 

  22. Moinet M, Fournier-Chambrillon C, André-Fontaine G, Aulagnier S, Mesplède A, Blanchard B, Descarsin V, Dumas P, Dumas Y, Coïc C, Couzi L, Fournier P (2010) Leptospirosis in free-ranging endangered European Mink (Mustela lutreola) and other small carnivores (mustelidae, viverridae) from SouthWestern France. J Wildl Dis 46(4):1141–1151

    PubMed  Article  Google Scholar 

  23. Sainsbury KA, Shore RF, Schofield H, Croose E, Pereira MG, Sleep D, Kitchener AC, Hantke G, McDonald RA (2018) Long-term increase in secondary exposure to anticoagulant rodenticides in European polecats Mustela putorius in Great Britain. Environ Pollut 236:689–698

    CAS  PubMed  Article  Google Scholar 

  24. Sainsbury KA, Shore RF, Schofield H, Croose E, Campbell RD, McDonald RA (2019) Recent history, current status, conservation and management of native mammalian carnivore species in Great Britain. Mammal Rev 49(2):171–188

    Article  Google Scholar 

  25. Sainsbury KA, Shore RF, Schofield H, Croose E, Hantke G, Kitchener AC, McDonald RA (2020) Diets of European polecat Mustela putorius in Great Britain during fifty years of population recovery. Mammal Res 65(2):181–190

    Article  Google Scholar 

  26. Sato JJ, Hosoda T, Wolsan M, Tsuchiya K, Yamamoto M, Suzuki H (2003) Phylogenetic relationships and divergence times among mustelids (Mammalia: Carnivora) based on nucleotide sequences of the nuclear interphotoreceptor retinoid binding protein and mitochondrial cytochrome b genes. Zool Sci 20(2):243–264

    CAS  PubMed  Article  Google Scholar 

  27. SAVSNET (2018) SAVSNET in realtime. https://www.liverpool.ac.uk/savsnet/real-time-data/. Accessed 23 May 2018

  28. Schuller S, Francey T, Hartmann K, Hugonnard M, Kohn B, Nally JE, Sykes J (2015) European consensus statement on leptospirosis in dogs and cats. J Small Anim Pract 56(3):159–179

    CAS  PubMed  Article  Google Scholar 

  29. Sepúlveda MA, Muñoz-Zanzi C, Rosenfeld C, Jara R, Pelican KM, Hill D (2011) Toxoplasma gondii in feral American minks at the Maullín river, Chile. Vet Parasitol 175(1–2):60–65

    PubMed  Article  Google Scholar 

  30. Sobrino R, Cabezón O, Millán J, Pabón M, Arnal MC, Luco DF, Gortázar C, Dubey JP, Almeria S (2007) Seroprevalence of Toxoplasma gondii antibodies in wild carnivores from Spain. Vet Parasitol 148(3–4):187–192

    CAS  PubMed  Article  Google Scholar 

  31. Soulsbury CD, Iossa G, Baker PJ, Cole NC, Funk SM, Harris S (2007) The impact of sarcoptic mange Sarcoptes scabiei on the British fox Vulpes vulpes population. Mammal Rev 37(4):278–296

    Google Scholar 

  32. Swennes AG, Fox JG (2014) Bacterial and mycoplasmal diseases biology and diseases of the ferret, 3rd edn. Wiley, Ames, pp 519–552

    Google Scholar 

  33. Thorne ET, Williams ES (1988) Disease and endangered species: the black-footed ferret as a recent example. Conserv Biol 2(1):66–74

    PubMed Central  Article  Google Scholar 

  34. Thornton RN, Cook TG (1986) A congenital Toxoplasma-like disease in ferrets (Mustela putorius furo). NZeal Veterin J 34(3):31–33

    CAS  Google Scholar 

  35. Twigg GI (2008) A review of the occurrence in British mammals of the major organisms of zoonotic importance. Mammal Rev 10(4):139–149

    Article  Google Scholar 

  36. Webster JP (2001) Rats, cats, people and parasites: the impact of latent toxoplasmosis on behaviour. Microbes Infect 3(12):1037–1045

    CAS  PubMed  Article  Google Scholar 

  37. Webster JP, Ellis WA, Macdonald DW (1995) Prevalence of Leptospira spp. in wild brown rats (Rattus norvegicus) on UK farms. Epidemiol Infect 114(1):195–201

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Acknowledgements

The Vincent Wildlife Trust supported the study by providing the polecat specimens used in this research. The National Museums Scotland supported the study by collecting the blood and tissue samples, and ACK is grateful to the Negaunee Foundation for their continuing generous support of a preparatory at the National Museums Scotland. Veterinary Diagnostic Services at the University of Glasgow and the Leptospirosis laboratory at Agri-Food and Biosciences Institute Stormont Belfast carried out the serological assays reported in this study and the Animal and Plant Health Agency carried out the CDV PCR testing. The authors thank Colm Gilmore for his advice on the Leptospira serovar assay and Professor Brian Willet for advice on CDV serological assays. Matson’s Laboratory LLC USA supported the study by ageing the specimens. KAS was supported by the University of Exeter, Vincent Wildlife Trust and Centre for Ecology & Hydrology.

Funding

The diagnostic testing was supported by Dr. Johnny Birks, The Blodwen Lloyd Binns Bequest Fund of the Glasgow Natural History Society and The Zebra Foundation of the British Veterinary Zoological Society. The teeth ageing analysis was funded by a Peoples’ Trust for Endangered Species grant. The funders’ sole role for the project was to support it financially.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Kari-Anne Heald.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations

Handling editor: Emmanuel Serrano.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 21 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Heald, KA., Millins, C., Kitchener, A.C. et al. Investigating infectious disease threats to the recovery of the European polecat in Britain. Mamm Biol 100, 439–444 (2020). https://doi.org/10.1007/s42991-020-00046-6

Download citation

Keywords

  • Canine distemper virus
  • Leptospira
  • Mustela putorius
  • Toxoplasma gondii