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Eimeria-parasites are associated with a lowered mother's and offspring's body condition in island and mainland populations of the bank vole

Published online by Cambridge University Press:  04 September 2006

H. HAKKARAINEN ,
E. HUHTA ,
E. KOSKELA ,
T. MAPPES ,
T. SOVERI  and
P. SUORSA
H. HAKKARAINEN
Affiliation:
Section of Ecology, Department of Biology, University of Turku, FIN-20014 Turku, Finland
E. HUHTA
Affiliation:
Finnish Forest Research Institute, Kolari Research Station, FIN-95900 Kolari, Finland
E. KOSKELA
Affiliation:
University of Jyväskylä, Department of Biological and Environmental Science, P.O. Box 35, FIN-40014 Jyväskylä, Finland
T. MAPPES
Affiliation:
University of Jyväskylä, Department of Biological and Environmental Science, P.O. Box 35, FIN-40014 Jyväskylä, Finland
T. SOVERI
Affiliation:
University of Helsinki, Department of Clinical Veterinary Sciences, FIN-04920 Saarentaus, Finland
P. SUORSA
Affiliation:
Section of Ecology, Department of Biology, University of Turku, FIN-20014 Turku, Finland
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Abstract

This study, based on correlative data, tests the hypothesis that infections with Eimeria spp. parasites exert a significant loss of fitness of bank voles (Clethrionomys glareolus) reflected in lower reproductive success and survival, declining host population densities and are associated positively with population size. The study was conducted in 20 mainland and 27 island populations in central Finland during May–September in 1999. Faecal samples showed that 28% of 767 individuals were infected with Eimeria spp. The presence of Eimeria parasites was higher in dense mainland populations than in sparsely populated islands. Eimerian infections increased during the course of the breeding season, probably as a result of the high infection rate of young individuals. Accordingly, the body masses of bank voles were negatively related to the presence of Eimeria spp. Reproductive output, as measured by the breeding probability of females and litter size, was not associated with the presence of eimerian infection. Interestingly, the body condition of the infected mothers appeared to be low. Moreover, mother's body condition was the single most important variable studied that showed a positive correlation to pup's body condition at birth. On small islands ([les ]3·2 ha) that were comprehensively trapped, the mean number of Eimeria spp. in the bank vole population was negatively related to density changes of the bank vole population during the study. Our data are consistent with the idea that infection with coccidian parasites may be one of the factors responsible for declining host populations in small, isolated populations.

Keywords

ProtozoacoccidiaEimeria spp.host–parasite interactionsbreeding successsurvivalpopulation densitybank voleisland and mainland populations
Type
Research Article
Information
Parasitology , Volume 134 , Issue 1 , January 2007 , pp. 23 - 31
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Anderson, R. M. and May, R. M. ( 1979). Population biology of infectious diseases: part I. Nature, London 280, 361–367.CrossRefGoogle Scholar
Ball, S. J. and Lewis, D. C. ( 1984). Eimeria (Protozoa: Coccidia) in wild populations of some British rodents. Journal of Zoology 202, 373–381.Google Scholar
Bertolino, S., Wauters, L. A., Debryun, L. and Canestri-Trotti, G. ( 2003). Prevalence of coccidian parasites (Protozoa) in red squirrels (Sciurus vulgaris): effects of host phenotype and environmental factors. Oecologia 137, 286–295.CrossRefGoogle Scholar
Bondrup-Nielsen, S. and Karlsson, F. ( 1985). Movements and spatial patterns in populations of Clethrionomys species: a review. Annales Zoologici Fennici 22, 385–392.Google Scholar
Boonstra, R., Krebs, C. J. and Beacham, T. D. ( 1980). Impact of botfly parasitism on Microtus townsendii populations. Canadian Journal of Zoology 58, 1683–1692.CrossRefGoogle Scholar
Booth, D. T., Clayton, D. H. and Block, B. A. ( 1993). Experimental demonstration of the costs of parasitism free-ranging hosts. Proceedings of the Royal Society of London, B 253, 125–129.CrossRefGoogle Scholar
Buchholz, R. ( 2004). Effects of parasitic infection on mate sampling by female wild turkeys (Meleagris gallopavo): should infected females be more or less choosy? Behavioral Ecology 15, 687–694.Google Scholar
Bujalska, G. ( 1970). Reproduction stabilizing elements in island populations of Clethrionomys glareolus. Acta Theriologica 15, 381–412.CrossRefGoogle Scholar
Catchpole, J., Norton, C. C. and Joyner, L. P. ( 1976). Experiments with defined multispecific coccidial infections in lambs. Parasitology 72, 137–147.CrossRefGoogle Scholar
Cavanagh, R. D., Lambin, X., Ergon, T., Bennet, M., Graham, I. M., van Soolingen, D. and Begon, M. ( 2004). Disease dynamics in cyclic populations of field voles (Microtus agrestis): cowpox virus and vole tuberculosis (Mycobacterium microti). Proceedings of the Royal Society of London, B 271, 859–867.CrossRefGoogle Scholar
Chapman, B. R. and George, J. E. ( 1991). The effects of ectoparasites on cliff swallow growth and survival. In Bird-Parasite Interactions: Ecology, Evolution, and Behaviour ( ed. Loye, J. E. and Zug, M.), pp. 69–92. Oxford University Press, Oxford, UK.
Connors, V. A. and Nickol, B. B. ( 1991). Effects of Plagiorhynchus cylinrageus (Acanthocephala) on the energy metabolism of adult starlings, Sturnus vulgaris. Parasitology 103, 395–402.CrossRefGoogle Scholar
Decker, K. H., Duszynski, D. W. and Patrick, M. J. ( 2001). Biotic and abiotic effects on endoparasites infecting Dipodomys and Perognathus species. Journal of Parasitology 87, 300–307.CrossRefGoogle Scholar
Duszynski, D. W. and Marquardt, W. C. ( 2003). Coccidia in the mammary glands of shrews (Order: Insectivora). Journal of Parasitology 89, 609–611.CrossRefGoogle Scholar
Fuller, C. A. and Blaustein, A. R. ( 1996). Effects of the parasite Eimeria arizonensis on survival of deer mice (Peromyscus maniculatus). Ecology 77, 2196–2202.CrossRefGoogle Scholar
Goater, T. M., Shostak, J. A., Williams, J. A. and Esch, G. W. ( 1989). A mark-recapture study of trematode parasitism in overwintered Helisoma anceps (Pulmonata), with special reference to Halipegus occidualis (Hemiuridae). Journal of Parasitology 75, 553–560.CrossRefGoogle Scholar
Gres, V., Voza, T., Chabaud, A. and Landau, I. ( 2003). Coccidiosis of the wild rabbit (Oryctolagus cuniculus) in France. Parasite 10, 51–57.CrossRefGoogle Scholar
Gulland, F. M. and Fox, M. ( 1992). Epidemology of nematode infections of Soya sheep (Ovis aries L.) on St Kilda. Parasitology 105, 481–492.Google Scholar
Higgs, S. and Nowell, F. ( 2000). Population biology of Eimeria (Protozoa: Apicomplexa) in Apodemus sylvaticus. A capture/recapture study. Parasitology 120, 355–363.Google Scholar
Hobbs, R. P., Twigg, L. E., Elliot, A. D. and Wheeler, A. G. ( 1999). Evaluation of the association of parasitism with mortality of wild European rabbits Oryctolagus cuniculus (L.) in southwestern Australia. Journal of Parasitology 85, 803–808.Google Scholar
Jonsson, P., Hartikainen, T., Koskela, E. and Mappes, T. ( 2002). Determinants of reproductive successs in voles: space use in relation to food and litter size manipulation. Evolutionary Ecology 16, 455–467.CrossRefGoogle Scholar
Keith, I. M., Keith, L. B. and Cary, J. R. ( 1986). Parasitism in a declining population of snowshoe hares. Journal of Wildlife Diseases 22, 349–363.CrossRefGoogle Scholar
Keymer, A. E. and Read, A. F. ( 1991). Behavioral ecology: the impact of parasitism. In Parasite-Host Associations: Coexistence or Conflict? ( ed. Toft, C. A., Aeschlimann, A. and Bolis, L.), pp. 37–61. Oxford University Press, Oxford, UK.
Koivula, M., Koskela, E., Mappes, T. and Oksanen, T. A. ( 2003). Costs of reproduction in the wild: manipulation of reproductive effort in the bank vole. Ecology 84, 398–405.CrossRefGoogle Scholar
Kruczek, M. and Marchlewska-Koj, A. ( 1986). Puberty delay of bank vole females in a high-density population. Biology of Reproduction 35, 537–541.CrossRefGoogle Scholar
Laakkonen, J., Oksanen, A., Soveri, T. and Henttonen, H. ( 1998). Dynamics of intestinal coccidia in peak density Microtus agrestis, Microtus oeconomus and Clethrionomus glareolus populations in Finland. Ecography 21, 135–139.CrossRefGoogle Scholar
Levine, N. D. and Ivens, V. ( 1990). The Coccidian Parasites of Rodents. CRC Press, Boca Raton, Florida, USA.
Lewis, D. C. and Ball, S. J. ( 1982). The life-cycle of Eimeria cernae Levine and Ivens, 1965 in the bank vole, Clethrionomys glareolus. Parasitology 85, 443–449.CrossRefGoogle Scholar
Mappes, T. and Koskela, E. ( 2004). Genetic basis of the trade-off between offspring number and quality in the bank vole. Evolution 58, 645–650.CrossRefGoogle Scholar
Mappes, T., Koskela, E. and Ylönen, H. ( 1995). Reproductive costs and litter size in the bank vole. Proceedings of the Royal Society of London, B 261, 19–24.CrossRefGoogle Scholar
May, R. M. and Anderson, M. ( 1979). Population biology of infectious diseases: part II. Nature, London 280, 455–461.CrossRefGoogle Scholar
Myllymäki, A., Paasikallio, A., Pankakoski, E. and Kanervo, V. ( 1971). Removal experiments on small quadrates as a means of rapid assesment of the abundance of small mammals. Annales Zoologici Fennici 8, 177–185.Google Scholar
Newman, C., Macdonald, D. W. and Anwar, M. A. ( 2001). Coccidiosis in the European badger, Meles meles in Wytham Woods: infection and consequences for growth and survival. Parasitology 123, 133–142.CrossRefGoogle Scholar
Palkovacs, E. P. ( 2003). Explaining adaptive shift in body size on islands. A life history approach. Oikos 103, 37–44.Google Scholar
Pellérdy, L. P. ( 1974). Coccidia and Coccidiosis. Paul Parey, Berlin, Germany.
Ross, J., Tittensor, A. M., Fox, A. P. and Sanders, M. F. ( 1989). Myxomatosis in farmland rabbit populations in England and Wales. Epidemology and Infection 103, 333–357.CrossRefGoogle Scholar
Schall, J., Bennet, A. F. and Putnam, R. W. ( 1982). Lizards infected with malaria: physiological and behavioural consequences. Science 217, 1057–1059.CrossRefGoogle Scholar
Schall, J. J. ( 1983). Lizard malaria: cost to vertebrate host's reproductive success. Parasitology 87, 1–6.CrossRefGoogle Scholar
Scott, M. E. ( 1987). Regulation of mouse colony abundance by Heligmosomoides polygyrus. Parasitology 95, 111–124.CrossRefGoogle Scholar
Scott, M. E. and Anderson, M. ( 1984). The population dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulate. Parasitology 89, 159–194.CrossRefGoogle Scholar
Smith, A. L. and Hayday, A. C. ( 2000). An alpha beta T-cell-independent immunoprotective response towards gut coccidian is supported by gamma delta cells. Immunology 101, 325–332.Google Scholar
Soulsby, E. J. L. ( 1982). Helminths, Arthropods and Protozoa of Domesticated Animals. Bailliére Tindall, London, UK.
Stanton, N. L., Shults, L. M., Parker, M. and Seville, R. S. ( 1992). Coccidan assemblages in the Wyoming ground squirrel, Spermophilus elegans elegans. Journal of Parasitology 78, 323–328.CrossRefGoogle Scholar
Stenseth, N. C. ( 1985). Geographic distribution of Clethrionomys species. Annales Zoologici Fennici 22, 215–219.Google Scholar
Tacconi, G., Piergili-Fioretti, D., Moretti, A., Nobilini, N. and Pasquali, P. ( 1995). Coccidia in hare (Lepus europaeus) reared in Umbria, Italy: bioepidemiological study. Journal of Protozoological Research 5, 77–85.Google Scholar
Telfer, S., Bennet, M., Bown, K., Carslake, D., Cavanagh, R., Hazel, S., Jones, T. and Begon, M. ( 2005). Infection with cowpox virus decreases female maturation rates in wild populations of woodland rodents. Oikos 109, 317–322.CrossRefGoogle Scholar
Thompson, S. N. ( 1990). Physiological alterations during parasitism and their effects on host behaviour. In Parasitism and Host Behaviour ( ed. Barnard, C. J. and Behnke, J. M.), pp. 64–94. Taylor and Francis, London, UK.
Toft, C. A. and Karter, A. J. ( 1990). Parasite-host coevolution. Trends in Ecology and Evolution 5, 326–329.CrossRefGoogle Scholar
Vorisek, P., Votypka, J., Zvara, K. & Svobodova, M. ( 1998). Heteroxenous coccidian increase the predation risk of parasitized rodents. Parasitology 117, 521–524.CrossRefGoogle Scholar
Yun, C. H., Lillehoj, H. S. and Lillehoj, E. P. ( 2000). Intestinal immune responses to coccidiosis. Developmental and Comparative Immunology 24, 303–324.CrossRefGoogle Scholar