Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-06-06T23:52:52.533Z Has data issue: false hasContentIssue false

Numerical response of a helminth community in the course of a multi-annual abundance cycle of the Water Vole (Arvicola terrestris)

Published online by Cambridge University Press:  19 January 2007

D. CERQUEIRA
Affiliation:
Centre de Biologie et Gestion des Populations, Institut National de la Recherche Agronomique, CS 30016 Montferrier sur Lez, 34988 Saint Gély du Fesc, France
P. DELATTRE*
Affiliation:
Centre de Biologie et Gestion des Populations, Institut National de la Recherche Agronomique, CS 30016 Montferrier sur Lez, 34988 Saint Gély du Fesc, France
B. DE SOUSA
Affiliation:
Centre de Biologie et Gestion des Populations, Institut National de la Recherche Agronomique, CS 30016 Montferrier sur Lez, 34988 Saint Gély du Fesc, France
C. GABRION
Affiliation:
Laboratoire de Parasitologie Fonctionnelle et Evolutive, Université du Languedoc Roussillon, Perpignan, France
S. MORAND
Affiliation:
Centre de Biologie et Gestion des Populations, Institut National de la Recherche Agronomique, CS 30016 Montferrier sur Lez, 34988 Saint Gély du Fesc, France
J. P. QUERE
Affiliation:
Centre de Biologie et Gestion des Populations, Institut National de la Recherche Agronomique, CS 30016 Montferrier sur Lez, 34988 Saint Gély du Fesc, France
*
*Corresponding author: Centre de Biologie et Gestion des Populations, Institut National de la Recherche Agronomique, CS 30016 Montferrier sur Lez, 34988 Saint Gély du Fesc, France. Tel: +33 (0)4 99 62 33 10. Fax: +33 (0)4 99 62 33 45. E-mail: delattre@ensam.inra.fr

Summary

The impact of parasitism on population dynamics is determined in part by the numerical responses of parasites during population fluctuations of their hosts. Vole populations fluctuate in multi-annual cycles allowing such responses to be studied over successive phases of population growth, abundance and decline. We investigate how a helminth community (5 nematode and 7 cestode species) evolved over a full 6-year Water Vole (Arvicola terrestris) population cycle. Brillouin and individual parasite species richness (IPSR) indices were used to measure the numerical response of the parasite community. We report a correlation between levels of parasite intensity and vole population cycle phases. Both indices were consistently higher during pre-decline and decline phases for male and female voles alike. The numerical response of the parasite community suggests that populations may be regulated by parasitism and that studies of this mechanism should allow both for the cyclic or non-cyclic character of the host populations and for the response of the broadest possible set of the local parasite community.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Arneberg, P. (2002). Host population density and body mass as determinants of species richness in parasite communities: comparative analysis of directly transmitted nematodes of mammals. Echography 25, 8894.CrossRefGoogle Scholar
Boonstra, R. (1994). Population cycles in microtines: the senescence hypothesis. Evolutionary Ecology 8, 196219.CrossRefGoogle Scholar
Boonstra, R. (1977). Effect of the parasite Wohlfahrtia vigil on Microtus townsendii populations. Canadian Journal of Zoology 55, 10571060.CrossRefGoogle ScholarPubMed
Boonstra, R., Krebs, C. J. and Beacham, T. D. (1980). Impact of botfly parasitism on Microtus townsendii populations. Canadian Journal of Zoology 58, 16831692.CrossRefGoogle Scholar
Cavanagh, R., Lambin, X., Bennett, M., Ergon, T., Graham, I. M., Van Soolingen, D., Telfer, S. and Begon, M. (2003). Disease dynamics in cyclic populations of field voles, Microtus agrestis: cowpox virus and vole tuberculosis, Mycobacterium microti. Proceedings of The Royal Society, B 271, 1541, 859867.CrossRefGoogle Scholar
Cerqueira, D. (2001). Implications des communautés parasitaires dans les cinétiques des populations de rongeurs: application aux populations sympatriques de deux espèces de campagnols, Arvicola terrestris sherman Shaw, 1801, et Microtus arvalis Pallas, 1779. Thèse de Doctorat, Université de Montpellier.Google Scholar
Cerqueira, D., De Sousa, B., Gabrion, C., Giraudoux, P., Quéré, J.-P. and Delattre, P. (2006). Cyclic changes in the population structure and reproductive pattern of the water vole, Arvicola terrestris L. 1758. Mammalian Biology 71, 193202. doi: 10.1016/j.mambio.2006.01.004.CrossRefGoogle Scholar
Delattre, P., Damange, J.-P., Pascal, M. and Habert, M. (1988). Rôle de la prédation et influence de la structure du paysage agraire sur le développement des cycles d'abondance des populations d'Arvicola terrestris scherman. OEPP Bulletin 18, 415422.CrossRefGoogle Scholar
Delattre, P., Giraudoux, P., Baudry, J., Quéré, J.-P. and Fichet, E. (1996). Effect of landscape structure on Common Vole, Microtus arvalis, distribution and abundance at several space scales. Landscape Ecology 11, 279288.CrossRefGoogle Scholar
Descoteaux, J.-P. and Mihok, S. (1986). Serologic study on the prevalence of murine viruses in a population of wild meadow voles, Microtus pennsylvanicus. Journal of Wildlife Diseases 22, 314319.CrossRefGoogle Scholar
Duhamel, R., Quéré, J.-P., Delattre, P. and Giraudoux, P. (2000). Landscape effects on the population dynamics of the fossorial form of the water vole, Arvicola terrestris sherman. Landscape Ecology 15, 8998.CrossRefGoogle Scholar
Fichet-Calvet, E., Jomâa, I., Ben Ismail, R. and Ashford, R. W. (2000). Patterns of infection of haemoparasites in the fat sand rat, Psammomys obesus, in Tunisia, and effect on the host. Annals of Tropical Medicine and Parasitology 94, 5568.CrossRefGoogle ScholarPubMed
Fichet-Calvet, E., Giraudoux, P., Quéré, J.-P., Ashford, R. W. and Delattre, P. (2003). Is the prevalence of Taenia taeniaeformis in Microtus arvalis dependent on population density? Journal of Parasitology 89, 11471152.CrossRefGoogle ScholarPubMed
Fichet-Calvet, E., Kia, E.-B., Giraudoux, P., Quéré, J.-P., Delattre, P. and Ashford, R. W. (2004). Frenkelia parasites in a small mammal community: dynamics of infection and effect on the host. Parasite 11, 301310.CrossRefGoogle Scholar
Giraudoux, P., Delattre, P., Habert, M., Quéré, J.-P., Deblay, S., Defaut, R., Duhamel, R., Moissenet, M.-F., Salvi, D. and Truchetet, D. (1997). Population dynamics of fossorial water vole, Arvicola terrestris scherman: a land use and landscape perspective. Agriculture, Ecosystem and Environment 66, 4760.CrossRefGoogle Scholar
Gregory, R. D. (1991). Parasite epidemiology and host population growth: Heligmosomoïdes polygyrus (Nematoda) in an enclosed wood mouse population. Journal of Animal Ecology 60, 805821.CrossRefGoogle Scholar
Gulland, F. M. (1992). The role of nematode parasites in Soay sheep, Ovis aries L., mortality during a population crash. Parasitology 105, 493503.CrossRefGoogle ScholarPubMed
Gulland, F. M. and Fox, M. (1992). Epidemiology of nematode infections of Soay sheep, Ovies aries L., on St Kilda. Parasitology 105, 481492.CrossRefGoogle Scholar
Hansson, L. (2001). Dynamics and trophic interactions of small rodents: landscape or regional effects on spatial variation? Oecologia 130, 259266.CrossRefGoogle Scholar
Hansson, L. (2002). Rodent dynamics, population regulation and predation in changeable landscapes: importance for Echinococcus transmission. In Cestode Zoonoses: Echinococcosis and Cysticercosis (ed. Craig, P. and Pawlowski, Z.),pp. 267285. IOS Press, Amsterdam.Google Scholar
Haukisalmi, V., Henttonen, H. and Tenora, F. (1988). Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807825.CrossRefGoogle Scholar
Haukisalmi, V. and Henttonen, H. (1990). The impact of climatic factors and host density on the long-term population dynamics of vole helminths. Oecologia 83, 309315.CrossRefGoogle ScholarPubMed
Haukisalmi, V. and Henttonen, H. (1993). Population dynamics of Taenia polyacantha metacestodes in the bank vole, Clethrionomys glareolus. Annals of Zoology Fennici 30, 8184.Google Scholar
Hixon, M. A., Pacala, S. W. and Sandin, S. A. (2002). Population regulation: historical context and contemporary challenges of open versus closed systems. Ecology 83, 14901508.CrossRefGoogle Scholar
Hoogenboom, I. and Dijkstra, C. (1987). Sarcocystis cernae: a parasite increasing the risk of predation of its intermediate host, Microtus arvalis. ɶcologia 74, 8692.Google ScholarPubMed
Holmes, J. C. (1995). Population regulation: a dynamic complex of interactions. Wildlife Research 22, 1119.CrossRefGoogle Scholar
Hudson, P. J., Dobson, A. P. and Newborn, D. (1992). Do parasites make prey vulnerable to predation? Red grouse and parasites. Journal of Animal Ecology 61, 681692.CrossRefGoogle Scholar
Hudson, P. J. and Dobson, A. P. (1998). Prevention of population cycles by parasite removal. Science 282, 22562258.CrossRefGoogle ScholarPubMed
Ives, A. and Murray, D. L. (1997). Can sublethal parasitism destabilize predator–prey population dynamics. A model of snowshoe hares, predators and parasites. Journal of Animal Ecology 66, 265278.CrossRefGoogle Scholar
Keymer, A. E. and Dobson, A. P. (1987). The ecology of helminths in a population of small mammals. Mammal Review 17, 105116.CrossRefGoogle Scholar
Kisielewska, K. and Zubczewska, Z. (1973). Intestinal helminths as indexes of reproduction dynamics in the host population Common Vole. Acta Theriologica 18, 237246.CrossRefGoogle Scholar
Korpimaki, E., Klemola, T., Norrdahl, K., Oksanen, L., Oksanen, T., Banks, P. B., Batzli, G. O. and Henttonen, H. (2003). Vole cycles and predation. Trends in Ecology and Evolution 18, 494495.CrossRefGoogle Scholar
Korpimaki, E., Brown, P. R., Jacob, J. and Pech, R. P. (2004). The puzzles of population cycles and outbreaks of small mammals solved? Bioscience 54, 10711079.CrossRefGoogle Scholar
Kovalchuk, E. S. (1984). Dynamics of infestation of the water vole, Arvicola terrestris, with helminths during population fluctuations. Soviet Journal of Ecology 14, 179183.Google Scholar
Krebs, C. J. and Myers, J. H. (1974). Population cycles in small mammals. Advances in Ecological Research 8, 267399.CrossRefGoogle Scholar
Krebs, C. J. (1996). Population cycles revisited. Journal of Mammalogy 77, 824.CrossRefGoogle Scholar
Lidicker, W. Z. (1988). Solving the enigma of microtine cycles. Journal of Mammalogy 69, 225235.CrossRefGoogle Scholar
Lidicker, W. Z. (1991). In defense of a multifactor perspective in population ecology. Journal of Mammalogy 72, 631635.CrossRefGoogle Scholar
Lidicker, W. Z. (2002). From dispersal to landscapes: progress in the understanding of population dynamics. Acta Theriologica 47, 2337.CrossRefGoogle Scholar
Magurran, A. E. (1988). Ecological Diversity and Measurement. Princeton University Press, Princeton, USA.CrossRefGoogle Scholar
Morand, S. and Poulin, R. (1998). Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology 12, 717727.CrossRefGoogle Scholar
Munger, J. C. and Karasov, W. H. (1991). Sublethal parasites in white-footed mice: impact on survival and reproduction. Canadian Journal of Zoology 69, 398404.CrossRefGoogle Scholar
Nicholson, A. J. (1933). The balance of animal populations. Journal of Mammalogy 2, 132178.Google Scholar
Oksanen, L. and Ericson, L. (1987). Preface: why should we care about predation and parasitism? Oikos 50, 274275.Google Scholar
Piélou, E. C. (1975). Ecological Diversity. Wiley-Interscience, New York.Google Scholar
Poulin, R. (1999). The functional importance of parasites in animal communities: many roles at many levels. International Journal for Parasitology 29, 903914.CrossRefGoogle ScholarPubMed
Scherrer, B. (1984). Biostatistique. Gaetan Morin, Paris.Google Scholar
Scott, M. (1987). Regulation of mouse colony abundance by Heligmosomoïdes polygyrus. Parasitology 95, 111124.CrossRefGoogle ScholarPubMed
Scott, M. and Dobson, A. (1989). The role of parasites in regulating host abundance. Parasitology Today 5, 176183.CrossRefGoogle ScholarPubMed
Sokal, R. and Rohlf, F. J. (1995). Biometry. Freeman and Company, New York.Google Scholar
Soveri, T., Henttonen, H., Rudback, E., Schildt, R., Tanskanen, R., Husu-Kallio, J., Haukisalmi, V., Sukura, A. and Laakkonen, J. (2000). Disease patterns in field and bank vole populations during a cyclic decline in central Finland. Comparative Immunology Microbiology and Infectious Diseases 23, 7389.CrossRefGoogle ScholarPubMed
Stenseth, N. C., Bjornstadt, O. N. and Falck, W. (1996). Is spacing behaviour coupled with predation causing the microtine density cycle? A synthesis of current process-oriented and pattern-oriented studies. Proceedings of The Royal Society of London, B 263, 14231435.Google ScholarPubMed
Stenseth, N. C., Saitoh, T. and Yoccoz, G. (1998). Frontiers in population ecology of microtine rodents: a pluralistic approach to the study of population ecology. Research in Population Ecology 40, 520.CrossRefGoogle Scholar
Stenseth, N. C., Viljugrein, H., Saitoh, T., Hansen, T. F., Kittilsen, M., Bolviken, E. and Glöckner, F. (2003). Seasonality, density dependence and population cycles in Hokkaido voles. Proceedings of the National Academy of Sciences, USA 100, 1147811483.CrossRefGoogle ScholarPubMed
Telfer, S., Bennett, M., Bown, K., Cavanagh, R., Crespin, L., Hazel, S., Jones, T. and Begon, M. (2002). The effects of cowpox virus on survival in natural rodent populations: increases and decreases. Journal of Animal Ecology 71, 558568.CrossRefGoogle Scholar
Telfer, S., Bennett, 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, 317322.CrossRefGoogle Scholar
Tenora, F. and Murray, E. (1980). The genera Anoplocephaloides and Paranoplocephala (Cestoda) parasites of Rodentia in Europe. Acta Zoologica Hungaria 26, 263284.Google Scholar
Tompkins, D. M. and Begon, M. (1999). Parasites can regulate wildlife populations. Parasitology Today 15, 311313.CrossRefGoogle ScholarPubMed