European Journal of Wildlife Research

, Volume 54, Issue 2, pp 171–178

Exposure to disease agents in the endangered Iberian lynx (Lynx pardinus)

  • Melody E. Roelke
  • Warren E. Johnson
  • Javier Millán
  • Francisco Palomares
  • Eloy Revilla
  • Alejandro Rodríguez
  • Javier Calzada
  • Pablo Ferreras
  • Luis León-Vizcaíno
  • Miguel Delibes
  • Stephen J. O’Brien
Original Paper

Abstract

The Iberian lynx (Lynx pardinus) is the most endangered felid species in the world. Lynx populations have decreased dramatically in size and distribution in the last four decades, thus becoming increasingly vulnerable to catastrophic events such as epizooties. From 1989 to 2000, serum samples were obtained from 48 free-ranging lynx captured in the Doñana National Park (DNP, n = 31) and mountains of Sierra Morena (SM, n = 17) in southern Spain. Samples were tested for antibodies against Toxoplasma gondii, feline herpesvirus 1 (FHV-1), feline calicivirus (FCV), feline/canine parvovirus (FPV/CPV), feline coronavirus, feline immunodeficiency virus (FIV), feline leukaemia virus and canine distemper virus (CDV) and for FeLV p27 antigen, to document baseline exposure levels. Antibodies against T. gondii were detected in 44% of lynx, with a significantly greater prevalence in DNP (61%) than in SM (12%). In DNP, prevalence was significantly higher in adult (81%) than in juvenile and sub-adult (41%) lynx, but no such difference was observed in SM. Low prevalences (≤11%) of minimally positive titres were found for FHV-1, FCV and FPV/CPV. This, combined with the lack of evidence for exposure to CDV, FIV and FeLV, suggests that these lynx populations are naïve and might be vulnerable to a disease outbreak in the future. Because of the reduced size of lynx populations, the documented low level of genetic variation (particularly in the DNP population) coupled with the recently documented state of immune depletion in a majority of necropsied lynx, it is important to better understand the threat and potential impact that disease agents might pose for the conservation of this endangered species. Future surveillance programs must include possible disease reservoir hosts such as domestic cats and dogs and other wild carnivores.

Keywords

Andalusia Conservation Disease risk Serosurvey Spain 

References

  1. Almería S, Calvete C, Pagés A, Gauss C, Dubey JP (2004) Factors affecting the seroprevalence of Toxoplasma gondii infection in wild rabbits (Oryctolagus cuniculus) from Spain. Vet Parasitol 123:265–270PubMedCrossRefGoogle Scholar
  2. Arjona A, Escolar E, Soto I, Barquero N, Martín D, Gómez-Lucía E (2000) Seroepidemiological survey of infection by feline leukemia virus and immunodeficiency virus in Madrid and correlation with some clinical aspects. J Clin Microbiol 38:3448–3449PubMedGoogle Scholar
  3. Artois M, Remond M (1994) Viral diseases as a threat to free-living wild cats (Felis silvestris) in continental Europe. Vet Rec 134:651–652PubMedGoogle Scholar
  4. Barker IK, Parrish CR (2001) Parvovirus infections. In: Williams ES, Barker IK (eds) Infectious diseases of wild mammals, 3rd edn. Iowa State University Press, Ames, IAGoogle Scholar
  5. Barker IK, Povey RC, Voigt DR (1985) Response of mink, skunk, red fox and raccoon to inoculation with mink virus enteritis, feline panleukopenia and canine parvovirus and prevalence of antibody to parvovirus in wild carnivores in Ontario. Can J Comp Med 47:188–197Google Scholar
  6. Barr MC, Calle PP, Roelke ME, Scott FW (1989) Feline immunodeficiency virus infection in nondomestic felids. J Zoo Wildl Med 20:265–272Google Scholar
  7. Biek R, Zarnke RL, Gillin C, Wild M, Squires JR, Poss M (2002) Serologic survey for viral and bacterial infections in western populations of Canada lynx (Lynx canadensis). J Wildl Dis 38:840–845PubMedGoogle Scholar
  8. Cotter SM (1980) Feline panleukopenia. In: Kirk RW (ed) Current veterinary therapy VII. Saunders, Philadelphia, PA, pp 1286–1288Google Scholar
  9. Courchamp F, Ponier D, Fromont E, Artois M (1995) Impact of two feline retroviruses on natural populations of domestic cat. Mammalia 59:589–598CrossRefGoogle Scholar
  10. Daniels MJ, Golder MC, Jarrett O, MacDonald DW (1999) Feline viruses in wildcats from Scotland. J Wildl Dis 35:121–124PubMedGoogle Scholar
  11. Decaro N, Martella V, Desario C, Bellacicco AL, Camero M, Manna L, d’Aloja D, Buonavoglia C (2006) First detection of canine parvovirus type 2c in pups with haemorrhagic enteritis in Spain. J Vet Med Ser B 53:468–472CrossRefGoogle Scholar
  12. de Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecol Lett 8:117–126CrossRefGoogle Scholar
  13. Delibes M (1980) Feeding ecology of the Spanish lynx in the Coto Doñana. Acta Theriol 25:309–324Google Scholar
  14. Dubey JP, Odening K (2001) Toxoplasmosis and related infections. In: Samuel WM, Pybus MJ, Kocan AA (eds) Parasitic diseases of wild mammals, 2nd edn. Mason, LondonGoogle Scholar
  15. Dubey JP, Quinn WJ, Weinandy D (1987) Fatal neonatal toxoplasmosis in a bobcat (Lynx rufus). J Wildl Dis 23:324–327PubMedGoogle Scholar
  16. Evermann JF, Roelke ME, Briggs MB (1986) Clinical and diagnostic features of feline coronavirus infections of cheetahs. Feline Pract 26:21–30Google Scholar
  17. Ferreras P, Aldama JJ, Beltrán JF, Delibes M (1994) Immobilization of the endangered Iberian lynx with xylazine- and ketamine-hydrochloride. J Wildl Dis 30(1):65–68PubMedGoogle Scholar
  18. Ferreras P, Delibes M, Palomares F, Fedriani JM, Calzada J, Revilla E (2004) Dispersal in the Iberian lynx: factors affecting the start, duration, distance and dispersal success. Behav Ecol 15:31–40CrossRefGoogle Scholar
  19. Fox JS (1983) Relationships of diseases and parasites to the distribution and abundance of bobcats in New York. Ph.D. dissertation, SUNY-ESF, SyracuseGoogle Scholar
  20. Gaskell R, Dawson S (1998) Feline respiratory disease. In: Greene CE (ed) Infectious diseases of dog and cat. Saunders, Pennsylvania, pp 11–24Google Scholar
  21. Gil-Sánchez JM, Ballesteros-Duperon E, Bueno-Segura JF (2006) Feeding ecology of the Iberian lynx Lynx pardinus in eastern Sierra Morena (Southern Spain). Acta Theriol 51:85–90Google Scholar
  22. Gortazar C (1999) Ecología y patología del zorro (Vulpes vulpes L.) en el Valle medio del Ebro. Consejo de Protección de la Naturaleza de Aragón, Zaragoza, SpainGoogle Scholar
  23. Guzmán JN, García FJ, Garrote G, Pérez de Ayala R, Iglesias C (2004) El lince ibérico (Lynx pardinus) en España y Portugal. Censo-diagnóstico de sus poblaciones. Dirección General para la Biodiversidad, Ministerio de Medio Ambiente, Madrid, SpainGoogle Scholar
  24. Ikeda Y, Mochizuki M, Naito R, Nakamura K, Miyazawa T, Mikami T, Takahashi E (2000) Predominance of canine parvovirus (CPV) in unvaccinated cat populations and emergence of new antigenic types of CPVs in cats. Virology 278:13–19PubMedCrossRefGoogle Scholar
  25. Johnson WE, Godoy JA, Palomares F, Delibes M, Fernandes M, Revilla E, O’Brien SJ (2004) Phylogenetic and phylogeographic analysis of Iberian lynx populations. J Heredity 95:19–28CrossRefGoogle Scholar
  26. Kikuchi Y, Chomel BB, Kasten RW, Martenson JS, Swift PK, O’Brien SJ (2004) Seroprevalence of Toxoplasma gondii in American free-ranging or captive pumas (Felis concolor) and bobcats (Lynx rufus). Vet Parasitol 120:1–9CrossRefGoogle Scholar
  27. Labelle P, Dubey JP, Mikaelian I, Blanchette N, Lafond R, St-Onge S, Martineau D (2001) Seroprevalence of antibodies to Toxoplasma gondii in lynx (Lynx canadensis) and bobcats (Lynx rufus) from Quebec, Canada. J Parasitol 87:1194–1196PubMedGoogle Scholar
  28. Lappin MR, Powell CC (1991) Comparison of latex agglutination, indirect hemagglutination, and ELISA techniques for the detection of Toxoplasma gondii-specific antibodies in the serum of cats. J Vet Intern Med 5:299–301PubMedCrossRefGoogle Scholar
  29. Leutenegger CM, Hofmann-Lehmann R, Riols C, Liberek M, Worel G, Lups P, Fehr D, Hartmann M, Weilenmann P, Lutz H (1999) Viral infections in free-living populations of the European wildcat. J Wildl Dis 35:678–686PubMedGoogle Scholar
  30. Luaces I, Aguirre E, Garcia-Montijano M, Velarde J, Tesouro MA, Sanchez C, Galka M, Fernandez P, Sainz A (2005) First report of an intraerythrocytic small piroplasm in wild Iberian lynx (Lynx pardinus). J Wildl Dis 41:810–815PubMedGoogle Scholar
  31. Maggs DJ, Lappin MR, Reif JS, Collins JK, Carman J, Dawson DA, Bruns C (1999) Evaluation of serologic and viral detection methods for diagnosing feline herpesvirus-1 infection in cats with acute respiratory tract or chronic ocular disease. J Am Vet Med Assoc 214:502–507PubMedGoogle Scholar
  32. Martín-Atance P, León-Vizcaíno L, Palomares F, Revilla E, González-Candela M, Calzada J, Cubero-Pablo MJ, Delibes M (2006) Antibodies to Mycobacterium bovis in wild carnivores from Doñana National Park (Spain). J Wildl Dis 42:704–708PubMedGoogle Scholar
  33. Mazumder P, Chuang HY, Wentz MW, Wiedbrauk DL (1988) Latex agglutination test for detection of antibodies to Toxoplasma gondii. J Clin Microbiol 26:2444–2446PubMedGoogle Scholar
  34. Mia AS, Kahn DE, Tierney MM, Post JE (1981) A microenzyme linked immunosorbent assay test for detection of FeLV in cats. Comp Immunol Microbiol Infect Dis 4:111–117PubMedCrossRefGoogle Scholar
  35. Millán J, Naranjo V, Rodríguez A, Pérez de la Lastra JM, Mangold AJ, de la Fuente J (2007) Prevalence of infection and 18S rRNA gene sequences of Cytauxzoon species in Iberian lynx (Lynx pardinus) in Spain. Parasitology 134:995–1001PubMedCrossRefGoogle Scholar
  36. Munson L, Wack R, Duncan M, Montali RJ, Boon D, Stalis I, Crawshaw GJ, Cameron KN, Mortenson J, Citino S, Zuba J, Junge RE (2004) Chronic eosinophilic dermatitis associated with persistent feline herpes virus infection in cheetahs (Acinonyx jubatus). Vet Pathol 41:170–176PubMedCrossRefGoogle Scholar
  37. Murray DL, Kapke CA, Evermann JF, Fuller TK (1999) Infectious disease and the conswervation of free-ranging large carnivores. Anim Conserv 2:241–254CrossRefGoogle Scholar
  38. Nieto JM, Quiroga M, López M, Antonio RF (1992) Distemper in mink in the NW of Spain. Nor J Agric Sci 9:398–404Google Scholar
  39. Nowell K, Jackson P (1996) Wild cats: status survey and conservation action plan. IUCN Publications. Burlington, Cambridge, UKGoogle Scholar
  40. O’Brien SJ, Roelke ME, Marker L, Newman A, Winkler CA, Meltzer D, Colby L, Evermann JF, Bush M, Wildt DE (1985) Genetic basis for species vulnerability in the cheetah. Science 227:428–434CrossRefGoogle Scholar
  41. OIE (2004) Manual of diagnostic tests and vaccines for terrestrial animals, 5th edn. World Organization for Animal Health. http://www.oie.int/eng/normes/mmanual/A_summry.htm
  42. Omata Y, Oikawa H, Kanda M, Midazuki K, Dilorenzo C, Claveria FG, Takahashi M, Igarashi I, Saito A, Suzuki N (1994) Transfer of antibodies to kittens from mother cats chronically infected with Toxoplasma gondii. Vet Parasitol 52:211–218PubMedCrossRefGoogle Scholar
  43. Peña L, García P, Jiménez MA, Benito A, Alenza MDP, Sánchez B (2006) Histopathological and immunohistochemical findings in lymphoid tissues of the endangered Iberian lynx (Lynx pardinus). Comp Immunol Microbiol 29:114–126CrossRefGoogle Scholar
  44. Pérez JM, Palma RL (2001) A new species of Felicola (Phthiraptera: Trichodectidae) from the endangered Iberian lynx: another reason to ensure its survival. Biodivers Conserv 10:929–937CrossRefGoogle Scholar
  45. Pérez J, Calzada J, León-Vizcaíno L, Cubero MJ, Velarde J, Mozos E (2001) Tuberculosis in an Iberian lynx (Lynx pardina). Vet Rec 148:414–415PubMedGoogle Scholar
  46. Powell CC, Brewer M, Lappin MR (2001) Detection of Toxoplasma gondii in the milk of experimentally infected lactating cats. Vet Parasitol 102:29–33PubMedCrossRefGoogle Scholar
  47. Riley SP, Foley J, Chomel B (2004) Exposure to feline and canine pathogens in bobcats and gray foxes in urban and rural zones of a national park in California. J Wildl Dis 40:11–22PubMedGoogle Scholar
  48. Rodríguez A, Carbonell E (1998) Gastrointestinal parasites of the Iberian lynx and other wild carnivores from central Spain. Acta Parasitol 43:128–136Google Scholar
  49. Rodríguez A, Delibes M (2002) Internal structure and contraction patterns in the geographic range of the Iberian lynx. Ecography 25:314–328CrossRefGoogle Scholar
  50. Roelke ME, Forrester DJ, Jacobson ER, Kollias GV (1991) Rationale for surveillance and prevention of infectious and parasitic disease transmission among free-ranging and captive Florida panthers (Felis concolor coryi). Proceedings of the Annual Conference of the American Association of Zoo Veterinarians, Philadelphia, PAGoogle Scholar
  51. Roelke ME, Forrester DJ, Jacobson ER, Kollias GV, Barr MC, Evermann JF, Pirtle EG (1993) Seroprevalence of infectious disease agents in free-ranging Florida panthers (Felis concolor coryi). J Wildl Dis 29:36–49PubMedGoogle Scholar
  52. Roelke-Parker ME, Munson L, Packer C, Kock R, Cleaveland S, Carpenter M, O’Brien SJ, Pospischil A, Hofmann-Lehmann R, Lutz H, Mwamengele GLM, Mgasa MN, Machange GA, Summers BA, Appel MJG (1996) A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379:441–445PubMedCrossRefGoogle Scholar
  53. Ryser-Degiorgis MP, Hofmann-Lehmann R, Leutenegger CM, af Segerstad CH, Morner T, Mattsson R, Lutz H (2005) Epizootiologic investigations of selected infectious disease agents in free-ranging Eurasian lynx from Sweden. J Wildl Dis 41:58–66PubMedGoogle Scholar
  54. Ryser-Degiorgis MP, Jakubek EB, af Segerstad CH, Brojer C, Morner T, Jansson DS, Lunden A, Uggla A (2006) Serological survey of Toxoplasma gondii infection in free-ranging Eurasian lynx (Lynx lynx) from Sweden. J Wildl Dis 42:182–187PubMedGoogle Scholar
  55. Schmidt-Posthaus H, Breitenmoser-Wursten C, Posthaus H, Bacciarini L, Breitenmoser U (2002) Causes of mortality in reintroduced Eurasian lynx in Switzerland. J Wildl Dis 38:84–92PubMedGoogle Scholar
  56. Scott FW (1977) Evaluation of a feline viral rhinotracheitis-feline calicivirus disease vaccine. Am J Vet Res 38:229–234PubMedGoogle Scholar
  57. Scott ME (1988) The impact of infection and disease on animal populations: implications for conservation biology. Conserv Biol 2:40–65CrossRefGoogle Scholar
  58. Scott FW (1990) Feline parvovirus infection. In: Tijssen P (ed) Handbook of parvoviruses, vol. 2. CRC, Boca Raton, FL, pp 103–111Google Scholar
  59. Scott FW, Csiza CK, Gillespie JH (1970) Maternally derived immunity to feline panleukopenia. J Am Vet Med Assoc 156:439–453PubMedGoogle Scholar
  60. Sillero-Zubiri C, King AA, Macdonald DW (1996) Rabies and mortality in Ethiopian wolves (Canis simensis). J Wildl Dis 32:80–86PubMedGoogle Scholar
  61. Smith KF, Sax DF, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conserv Biol 20:1349–1357PubMedCrossRefGoogle Scholar
  62. Sleeman JM, Keane JM, Johnson JS, Brown RJ, Woude SV (2001) Feline Leukemia Virus in a captive bobcat. J Wildl Dis 37:194–200PubMedGoogle Scholar
  63. Stiles J (2000) Feline herpesvirus. Vet Clin North Am Small Anim Pract 30:1001–1014PubMedGoogle Scholar
  64. Thorne ET, Williams ES (1988) Disease and endangered species: the black-footed ferret as a recent example. Conserv Biol 2:66–74CrossRefGoogle Scholar
  65. Troyer JL, Pecon-Slattery J, Roelke ME, Johnson W, VandeWoude S, Vazquez-Salat N, Brown M, Frank L, Woodroffe R, Winterbach C, Winterbach H, Hemson G, Bush M, Alexander KA, Revilla E, O’Brien SJ (2005) Seroprevalence and genomic divergence of circulating strains of feline immunodeficiency virus among Felidae and Hyaenidae species. J Virol 79:8282–8294PubMedCrossRefGoogle Scholar
  66. Truyen U, Evermann JF, Vieler E, Parrish CR (1996) Evolution of canine parvovirus involved loss and gain of Feline host range. Virology 215:186–189PubMedCrossRefGoogle Scholar
  67. Vicente J, Palomares F, de Ibáñez RR, Ortiz J (2003) Epidemiology of Ancylostoma spp. in the endangered Iberian lynx (Lynx pardinus) in the Doñana National Park, south-west Spain. J Helminthol 78:179–183CrossRefGoogle Scholar
  68. Villafuerte R, Calvete C, Gortazar C, Moreno S (1994) First epizootic of rabbit hemorrhagic disease in free living populations of Oryctolagus cuniculus at Doñana National Park, Spain. J Wildl Dis 30:176–179PubMedGoogle Scholar
  69. Wassmer DA, Guenther DD, Layne JN (1988) Ecology of the bobcat in South-Central Florida. Bull Fla State Mus, Biol Sci 3:159–228Google Scholar
  70. Williams ES, Barker IK (2001) Infectious diseases of wild mammals. Iowa State University Press, IowaGoogle Scholar
  71. Zarnke RL, Dubey JP, Ver Hoef JM, Mcnay ME, Kwok OCH (2001) Serologic survey for Toxoplasma gondii in lynx from interior Alaska. J Wildl Dis 37:36–38PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Melody E. Roelke
    • 1
  • Warren E. Johnson
    • 2
  • Javier Millán
    • 3
  • Francisco Palomares
    • 3
  • Eloy Revilla
    • 3
  • Alejandro Rodríguez
    • 3
  • Javier Calzada
    • 4
  • Pablo Ferreras
    • 5
  • Luis León-Vizcaíno
    • 6
  • Miguel Delibes
    • 3
  • Stephen J. O’Brien
    • 2
  1. 1.Laboratory of Genomic Diversity, SAIC-FrederickNCI-FrederickFrederickUSA
  2. 2.Laboratory of Genomic Diversity, National Cancer InstituteNCI-FrederickFrederickUSA
  3. 3.Department of Conservation BiologyEstación Biológica de Doñana (CSIC)SevillaSpain
  4. 4.Departamento de Biología Ambiental y Salud Pública, Facultad de Ciencias ExperimentalesUniversidad de HuelvaHuelvaSpain
  5. 5.IREC (CSIC-UCLM-JCCM)Ciudad RealSpain
  6. 6.Infectious Diseases Area, Faculty of Veterinary MedicineUniversity of MurciaMurciaSpain

Personalised recommendations