The impact of a pathogenic bacterium on a social carnivore population

Journal of Animal Ecology

Volumn 81, Issue 1, 2012, Pages 36-46

  Höner, Oliver P ^a   Wachter, Bettina ^a   Goller, Katja V ^a   Hofer, Heribert ^a   Runyoro, Victor ^b   Thierer, Dagmar ^a   Fyumagwa, Robert D ^c   Müller, Thomas ^d   East, Marion L ^a  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^b Ngorongoro Conservation Area Authority   (Tanzania)

^c TANZANIA WILDLIFE RESEARCH INSTITUTE   (Tanzania)

^d FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

Basic reproductive rate (R 0); Crocuta crocuta; Disease ecology; Ngorongoro Crater; Population dynamics; Population regulation; Spotted hyena; Streptococcus

Indexed keywords

AGE CLASS; BACTERIUM; BOTTOM-UP CONTROL; BREEDING POPULATION; CARNIVORE; DENSITY DEPENDENCE; DISEASE PREVALENCE; DISEASE TRANSMISSION; ECOLOGICAL IMPACT; HOST-PATHOGEN INTERACTION; JUVENILE; MAMMAL; MORTALITY; PATHOGEN; POPULATION DYNAMICS; POPULATION GROWTH; POPULATION OUTBREAK; POPULATION REGULATION; REPRODUCTIVE PRODUCTIVITY; SURVIVAL; TOP-DOWN CONTROL;

ANIMAL; ANIMAL DISEASE; ARTICLE; CARNIVORA; DEMOGRAPHY; DISEASE TRANSMISSION; EPIDEMIC; FEMALE; MALE; MICROBIOLOGY; NUTRITIONAL STATUS; PHYSIOLOGY; POPULATION DENSITY; POPULATION DYNAMICS; SOCIAL DOMINANCE; STREPTOCOCCUS EQUI; STREPTOCOCCUS INFECTION; TANZANIA;

ANIMALS; DEMOGRAPHY; DISEASE OUTBREAKS; FEMALE; HYAENIDAE; MALE; NUTRITIONAL STATUS; POPULATION DENSITY; POPULATION DYNAMICS; SOCIAL DOMINANCE; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS EQUI; TANZANIA;

ARUSHA [TANZANIA]; NGORONGORO CRATER; TANZANIA;

BACTERIA (MICROORGANISMS); CROCUTA CROCUTA; MAMMALIA; STREPTOCOCCUS; STREPTOCOCCUS EQUI;

EID: 83155181698     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2011.01873.x     Document Type: Article

References (53)

1. Akineden, Ö., Hassan, A.A., Alber, J., El-Sayed, A., Estoepangestie, A.T.S., Lämmler, C., Weiss, R. & Siebert, U. (2005) Phenotypic and genotypic properties of Streptococcus equi subsp. zooepidemicus isolated from harbour seals (Phoca vitulina) from the German North Sea during the phocine distemper outbreak in 2002. Veterinary Microbiology, 110, 147-152.
2. Anderson, R.M. & May, R.M. (1985) Vaccination and herd immunity to infectious diseases. Nature, 318, 323-329.
3. Anderson, R.M. & May, R.M. (1991) Infectious Diseases of Humans: Dynamics and Control. Oxford University Press, Oxford.
4. Archie, E.A., Morrison, T.A., Foley, C.A.H., Moss, C.J. & Alberts, S.C. (2006) Dominance rank relationships among wild female African elephants, Loxodonta africana. Animal Behaviour, 71, 117-127.
5. Barret, T., Visser, I.K.G., Mamaev, L., Goatley, L., Van Bressem, M.F. & Osterhaus, A.D.M.E. (1993) Dolphin and porpoise morbilliviruses are genetically distinct from Phocine distemper virus. Virology, 193, 1010-1012.
6. Begon, M., Townsend, C.R. & Harper, J.L. (2006) Ecology: From Individuals to Ecosystems. Blackwell Publishing, Oxford.
7. Beldomenico, P.M., Telfer, S., Gebert, S., Lukomski, L., Bennett, M. & Begon, M. (2008) Poor condition and infection: a vicious circle in natural populations. Proceedings of the Royal Society of London B, 275, 1753-1759.
8. Burthe, S., Telfer, S., Begon, M., Bennett, M., Smith, A. & Lambin, X. (2008) Cowpox virus infection in natural field vole Microtus agrestis populations: significant negative impacts on survival. Journal of Animal Ecology, 77, 110-119.
9. Chanter, N., Talbot, N.C., Newton, J.R., Hewson, D. & Verheyen, K. (2000) Streptococcus equi with truncated M-proteins isolated from outwardly healthy horses. Microbiology, 146, 1361-1369.
10. Chesson, J. (1983) The estimation and analysis of preference and its relationship to foraging models. Ecology, 64, 1297-1304.
11. Coleman, P.G. & Dye, C. (1996) Immunization coverage required to prevent outbreaks of dog rabies. Vaccine, 14, 185-186.
12. Coulson, T., Benton, T.G., Lundberg, P., Dall, S.R.X., Kendall, B.E. & Gaillard, J.-M. (2006) Estimating individual contributions to population growth: evolutionary fitness in ecological time. Proceedings of the Royal Society of London B, 273, 547-555.
13. Dennis, B. & Taper, M.L. (1994) Density dependence in time-series observations of natural populations: estimation and testing. Ecological Monographs, 64, 205-224.
14. Dietz, R., Ansen, C.T., Have, P. & Heide-Jørgensen, M.-P. (1989) Clue to seal epizootic? Nature, 338, 627.
15. East, M.L., Moestl, K., Benetka, V., Pitra, C., Höner, O.P., Wachter, B. & Hofer, H. (2004) Coronavirus infection of spotted hyenas in the Serengeti ecosystem. Veterinary Microbiology, 102, 1-9.
16. Forchhammer, M.C. & Asferg, T. (2000) Invading parasites cause a structural shift in red fox dynamics. Proceedings of the Royal Society of London B, 267, 779-786.
17. Goller, K.V., Fyumagwa, R.D., Nikolin, V., East, M.L., Kilewo, M., Speck, S., Müller, T., Matzke, M. & Wibbelt, G. (2010) Fatal canine distemper infection in a pack of African wild dogs in the Serengeti ecosystem, Tanzania. Veterinary Microbiology, 146, 245-252.
18. Goymann, W., East, M.L., Wachter, B., Höner, O.P., Möstl, E. & Hofer, H. (2003) Social status does not predict corticosteroid levels in post-dispersal male spotted hyenas. Hormones and Behavior, 43, 474-479.
19. Guiserix, M., Bahi-Jaber, N., Fouchet, D., Sauvage, F. & Pontier, D. (2007) The canine distemper epidemic in the Serengeti: are lions victims of a new highly virulent canine distemper virus strain, or is pathogen circulation stochasticity to blame? Journal of the Royal Society Interface, 17, 1127-1134.
20. Haas, L., Hofer, H., East, M., Wohlsein, P., Liess, B. & Barrett, T. (1996) Canine distemper virus infection in Serengeti spotted hyaenas. Veterinary Microbiology, 49, 147-152.
21. Hampson, K., Dobson, A., Kaare, M., Dushoff, J., Magoto, M., Sindoya, E. & Cleaveland, S. (2008) Rabies exposures, post-exposure prophylaxis and deaths in a region of endemic canine rabies. PLoS Neglected Tropical Diseases, 2, e339.
22. Harrison, T.M., Mazet, J.K., Holekamp, K.E., Dubovi, E., Engh, A.E., Nelson, K., Van Horn, R.C. & Munson, L. (2004) Antibodies to canine and feline viruses in spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve. Journal of Wildlife Diseases, 40, 1-10.
23. Hawkins, C.E., Baars, C., Hesterman, H., Hocking, G.J., Jones, M.E., Lazenby, B., Mann, D., Mooney, N., Pemberton, D., Pyecroft, S., Restani, M. & Wiersma, J. (2006) Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii. Biological Conservation, 131, 307-324.
24. Hofer, H. & East, M.L. (1993) The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. II. Intrusion pressure and commuters' space use. Animal Behaviour, 46, 559-574.
25. Hofer, H. & East, M.L. (2003) Behavioral processes and costs of co-existence in female spotted hyenas: a life history perspective. Evolutionary Ecology, 17, 315-331.
26. Höner, O.P., Wachter, B., East, M.L. & Hofer, H. (2002) The response of spotted hyaenas to long-term changes in prey populations: functional response and interspecific kleptoparasitism. Journal of Animal Ecology, 71, 236-246.
27. Höner, O.P., Wachter, B., East, M.L., Runyoro, V.A. & Hofer, H. (2005) The effect of prey abundance and foraging tactics on the population dynamics of a social, territorial carnivore, the spotted hyena. Oikos, 108, 544-554.
28. Höner, O.P., Wachter, B., Speck, S., Wibbelt, G., Ludwig, A., Fyumagwa, R.D., Wohlsein, P., Lieckfeldt, D., Hofer, H. & East, M.L. (2006) Severe Streptococcus infection in spotted hyenas in the Ngorongoro Crater, Tanzania. Veterinary Microbiology, 115, 223-228.
29. Höner, O.P., Wachter, B., East, M.L., Streich, W.J., Wilhelm, K., Burke, T. & Hofer, H. (2007) Female mate-choice drives the evolution of male-biased dispersal in a social mammal. Nature, 448, 798-801.
30. Höner, O.P., Wachter, B., Hofer, H., Wilhelm, K., Thierer, D., Trillmich, F., Burke, T. & East, M.L. (2010) The fitness of dispersing spotted hyaena sons is influenced by maternal social status. Nature Communications, 1, 60.
31. Hudson, P.J., Dobson, A.P. & Newborn, D. (1998) Prevention of population cycles by parasite removal. Science, 282, 2256-2258.
32. Jones, M.E., Cockburn, A., Hamede, R., Hawkins, C., Hesterman, H., Lachish, S., Mann, D., McCallum, H. & Pemberton, D. (2008) Life-history change in disease-ravaged Tasmanian devil populations. Proceedings of the National Academy of Sciences of the United States of America, 105, 10023-10027.
33. Jorm, L.R. (1990) Strangles in horse studs: incidence, risk factors and effect of vaccination. Australian Veterinary Journal, 67, 436-439.
34. Kalinowski, S.T., Taper, M.L. & Marshall, T.C. (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology, 16, 1099-1106.
35. Kissui, B.M. & Packer, C. (2004) Top-down population regulation of a top predator: lions in the Ngorongoro Crater. Proceedings of the Royal Society of London B, 271, 1867-1874.
36. Kruuk, H. (1972) The Spotted Hyena. A Study of Predation and Social Behavior. University of Chicago Press, Chicago, IL.
37. Lembo, T., Haydon, D.T., Velasco-Villa, A., Rupprecht, C.E., Packer, C., Brandão, P.E., Kuzmin, I.V., Fooks, A.R., Barrat, J. & Cleaveland, S. (2007) Molecular epidemiology identifies only a single rabies virus variant circulating in complex carnivore communities of the Serengeti. Proceedings of the Royal Society of London B, 274, 2123-2130.
38. Lloyd-Smith, J.O., Cross, P.C., Briggs, C.J., Daughterty, M., Getz, W.M., Latto, J., Sanchez, M.S., Smith, A.B. & Swei, A. (2005) Should we expect population thresholds for wildlife disease? Trends in Ecology and Evolution, 20, 511-519.
39. Manly, B.F.J., McDonald, L.L. & Thomas, D.L. (1993) Resource Selection by Animals. Statistical Design and Analysis for Field Studies. Chapman and Hall, London.
40. Martin, L.B., Weil, Z.M. & Nelson, R.J. (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 363, 321-339.
41. Munson, L., Terio, K.A., Kock, R., Mlengeya, T., Roelke, M.E., Dubovi, E., Summers, B., Sinclair, A.R.E. & Packer, C. (2008) Climate extremes promote fatal co-infections during canine distemper epidemics in African lions. PLoS ONE, 3, e2545.
42. Nelson, R.J. & Demas, G.E. (1996) Seasonal changes in immune function. Quarterly Review of Biology, 71, 511-548.
43. Parmar, M.K.B. & Machin, D. (1995) Survival Analysis: A Practical Approach. John Wiley and Sons, New York, NY.
44. Reif, J.S. (1979) Epidemiology of equine infectious respiratory disease. Veterinary Clinics of North America Large Animal Practice, 1, 3-15.
45. Robert, N., Walzer, C., Ruegg, S.R., Kaczensky, P., Ganbaatar, O. & Stauffer, C. (2005) Pathologic findings in reintroduced Przewalski's horses (Equus caballus przewalskii) in southwestern Mongolia. Journal of Zoo and Wildlife Medicine, 36, 273-285.
46. Runyoro, V.A., Hofer, H., Chausi, E.B. & Moehlman, P.D. (1995) Long-term trends in the herbivore populations of the Ngorongoro Crater, Tanzania. Serengeti II: Dynamics, Management, and Conservation of an Ecosystem (eds A.R.E. Sinclair & P. Arcese), pp. 146-168. University of Chicago Press, Chicago, IL.
47. Sahin, E. & DePinho, R.A. (2010) Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature, 464, 520-528.
48. Sapolsky, R.M. (2005) The influence of social hierarchy on primate health. Science, 308, 648-652.
49. Speck, S., Höner, O.P., Wachter, B. & Fickel, J. (2008) Characterization of Streptococcus equi subsp. ruminatorum isolated from spotted hyenas (Crocuta crocuta) and plains zebras (Equus burchelli), and identification of a M-like protein (SrM) encoding gene. Veterinary Microbiology, 128, 148-159.
50. Sweeney, C.R., Benson, C.E., Whitlock, R.H., Meirs, D.A., Barningham, S.O., Whitehead, S.C. & Cohen, D. (1989) Description of an epizootic and persistence of Streptococcus equi infections in horses. Journal of the American Veterinary Medical Association, 194, 1281-1286.
51. Timoney, J.F. (1999) Equine strangles: 1999. Proceedings of the American Association of Equine Practitioners, 45, 31-37.
52. Tompkins, D.M. & Begon, M. (1999) Parasites can regulate wildlife populations. Parasitology Today, 15, 311-313.
53. Weese, J.S., Jarlot, C. & Morley, P. (2008) Survival of Streptococcus equi in an outdoor environment. Journal of Veterinary Internal Medicine, 22, 819.