Hostname: page-component-84b7d79bbc-dwq4g Total loading time: 0 Render date: 2024-07-27T23:31:41.318Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of geographical scale on the detection of density dependence in the host-parasite system, Arvicola terrestris and Taenia taeniaeformis

Published online by Cambridge University Press:  05 December 2005

J. DETER ,
K. BERTHIER ,
Y. CHAVAL ,
J. F. COSSON ,
S. MORAND  and
N. CHARBONNEL
J. DETER
Affiliation:
INRA, UMR Centre de Biologie et de Gestion des Populations (CBGP), Campus international de Baillarguet, CS 30 016 – 34 988 Montferrier sur Lez, France
K. BERTHIER
Affiliation:
INRA, UMR Centre de Biologie et de Gestion des Populations (CBGP), Campus international de Baillarguet, CS 30 016 – 34 988 Montferrier sur Lez, France
Y. CHAVAL
Affiliation:
INRA, UMR Centre de Biologie et de Gestion des Populations (CBGP), Campus international de Baillarguet, CS 30 016 – 34 988 Montferrier sur Lez, France
J. F. COSSON
Affiliation:
INRA, UMR Centre de Biologie et de Gestion des Populations (CBGP), Campus international de Baillarguet, CS 30 016 – 34 988 Montferrier sur Lez, France
S. MORAND
Affiliation:
INRA, UMR Centre de Biologie et de Gestion des Populations (CBGP), Campus international de Baillarguet, CS 30 016 – 34 988 Montferrier sur Lez, France
N. CHARBONNEL
Affiliation:
INRA, UMR Centre de Biologie et de Gestion des Populations (CBGP), Campus international de Baillarguet, CS 30 016 – 34 988 Montferrier sur Lez, France
Get access Rights & Permissions [Opens in a new window]

Abstract

Infection by the cestode Taenia taeniaeformis was investigated within numerous cyclic populations of the fossorial water vole Arvicola terrestris sampled during 4 years in Franche-Comté (France). The relative influence of different rodent demographic parameters on the presence of this cestode was assessed by considering (1) the demographic phase of the cycle; (2) density at the local geographical scale (<0·1 km2); (3) mean density at a larger scale (>10 km2). The local scale corresponded to the rodent population (intermediate host), while the large scale corresponded to the definitive host population (wild and feral cats). General linear models based on analyses of 1804 voles revealed the importance of local density but also of year, rodent age, season and interactions between year and season and between age and season. Prevalence was significantly higher in low vole densities than during local outbreaks. By contrast, the large geographical scale density and the demographic phase had less influence on infection by the cestode. The potential impacts of the cestode on the fitness of the host were assessed and infection had no effect on the host body mass, litter size or sexual activity of voles.

Keywords

Arvicola terrestrisTaenia taeniaeformiscestodedensity-dependencegeographical scalehost reproductioncyclic demography
Type
Research Article
Information
Parasitology , Volume 132 , Issue 4 , April 2006 , pp. 595 - 605
Copyright
2005 Cambridge University Press

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

Anderson, R. M. and May, R. M. ( 1978). Regulation and stability of host-parasite population interactions. I. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Arneberg, P., Skorping, A., Grenfell, B. T. and Read, A. F. ( 1998). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London, B 265, 1283–1289. DOI: 10.1098/rspb.1998.0431.CrossRefGoogle Scholar
Bagge, A. M., Poulin, R. and Valtonen, E. T. ( 2004). Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology 128, 305–313.CrossRefGoogle Scholar
Behnke, J. M., Lewis, J. W., Zain, S. N. M. and Gilbert, F. S. ( 1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 31–44.Google Scholar
Beigom Kia, E. ( 1996). Patterns of infection of parasites of predators in small intermediate hosts. Ph. D. thesis, University of Liverpool, Liverpool, UK.
Boonstra, R. ( 1994). Population cycles in microtines: the senescence hypothesis. Evolutionary Ecology 8, 196–219.CrossRefGoogle Scholar
Boonstra, R., Krebs, C. J. and Stenseth, N. C. ( 1998). Population cycles in small mammals: the problem of explaining the low phase. Ecology 79, 1479–1488.CrossRefGoogle Scholar
Boujard, T. ( 1982). Contribution à l’étude de la structure et de la cinétique d'une population de la forme fouisseuse du campagnol terrestre (Arvicola terrestris Scherman (Shaw)) dans le Doubs (France) pendant la phase pullulante du cycle. Ph. D. thesis, Université Pierre et Marie Curie – Paris VI, Paris.
Bursten, S. N., Kimsey, R. B. and Owings, D. H. ( 1997). Ranging of male Oropsylla montana fleas via male California ground squirrel (Spermophilus beecheyi) juveniles. Journal of Parasitology 83, 804–809.CrossRefGoogle Scholar
Cavanagh, R. D., Lambin, X., Ergon, T., Bennett, 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
Cerqueira, D. ( 2001). Implication 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 l'Université Montpellier II, Montpellier, France.
Decker, K. H. D., Duszynski, 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
Delahay, R. J., Daniels, M. J., Macdonald, D. W., McGuire, K. and Balharry, D. ( 1998). Do patterns of helminth parasitism differ between groups of wild-living cats in Scotland? Journal of Zoology 245, 175–183.Google Scholar
Delattre, P., Duplantier, J. M., Fichet, E. and Giraudoux, P. ( 1998). Pullulations de rongeurs, agriculture et santé publique. Cahiers Agricultures 7, 285–298.Google Scholar
Dobson, A. P. and Hudson, P. J. ( 1992). Regulation and stability of a free-living host parasite-system: Trichostrongylus tenuis in red grouse. II. Population models. Journal of Animal Ecology 61, 487–498.Google Scholar
Duplantier, J. M. and Sene, M. ( 2000). Rodents as reservoir hosts in the transmission of Schistosoma mansoni in Richard-Toll, Senegal, West Africa. Journal of Helminthology 74, 129–135.Google Scholar
Dvorakova, L. and Prokopic, J. ( 1984). Hydatigera taeniaeformis (Batsch, 1786) as the cause of mass deaths of muskrats. Folia Parasitologica 31, 127–131.Google Scholar
Elton, C. and Nicholson, M. ( 1942). The ten-year cycle in numbers of the lynx in canada. Journal of Animal Ecology 11, 215–244.CrossRefGoogle Scholar
Fichet-Calvet, E., Giraudoux, P., Quere, J. P., Ashford, R. W. and Delattre, P. ( 2003 a). Is the prevalence of Taenia taeniaeformis in Microtus arvalis dependent on population density? Journal of Parasitology 89, 1147–1152.Google Scholar
Fichet-Calvet, E., Kia, E. B., Giraudoux, P., Quere, 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-Journal de La Société Francaise de Parasitologie 11, 301–310.Google Scholar
Fichet-Calvet, E., Wang, J. F., Jomaa, I., Ismail, R. B. and Ashford, R. W. ( 2003 b). Patterns of the tapeworm Raillietina trapezoides infection in the fat sand rat Psammomys obesus in Tunisia: season, climatic conditions, host age and crowding effects. Parasitology 126, 481–492.Google 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, Ecosystems and Environment 66, 47–60.CrossRefGoogle Scholar
Giraudoux, P., Delattre, P., Quéré, J.-P. and Damange, J.-P. ( 1994). Structure and kinetics of rodent populations, in a region under agricultural land abandonment. Acta Oecologia 15, 385–400.Google Scholar
Giraudoux, P., Pradier, B., Delattre, P., Deblay, S., Salvi, D. and Defaut, R. ( 1995). Estimation of water vole abundance by using surface indices. Acta Theriologica 40, 77–96.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, 309–315.CrossRefGoogle 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, 807–826.CrossRefGoogle Scholar
Huffaker, C. B. ( 1958). Experimental studies on predation: dispersion factors and predator-prey oscillations. Hilgardia 27, 343–383.CrossRefGoogle Scholar
Ilsoe, B., Kyvsgaard, N., Nansen, P. and Henriksen, S. A. ( 1990). A study on the survival of Taenia saginata eggs on soil in Denmark. Acta Veterinaria Scandinavica 31.Google Scholar
Johnson, J. B. and Omland, K. S. ( 2004). Model selection in ecology and evolution. Trends in Ecology and Evolution 19, 101–108. DOI: 10.1016/j.tree.2003.10.013.CrossRefGoogle Scholar
Krebs, C. J. and Myers, J. M. ( 1974). Population cycles in small mammals. Advances in Ecological Research 8, 267–299.CrossRefGoogle Scholar
Laws, G. F. ( 1968). Physical factors influencing survival of Taeniid eggs. Experimental Parasitology 22, 227–239.CrossRefGoogle Scholar
Le Louarn, H. and Quéré, J.-P. ( 2003). Les rongeurs de France, faunistique et biologie, INRA Editions. Paris.
Le Pesteur, M. H., Giraudoux, P., Delattre, P., Damange, J.-P. and Quéré, J.-P. ( 1992). Spatiotemporal distribution of four species of cestodes in a landscape of mid-altitude mountains (Jura, France). Annales de Parasitologie Humaine Comparée 67, 155–160.CrossRefGoogle Scholar
Legendre, P. and Legendre, L. ( 1998). Numerical Ecology. Elsevier, Amsterdam.
Lewis, J. W. and Twigg, G. I. ( 1972). A study of the internal parasites of small rodents from woodland areas in Surrey. Journal of Zoology, London 166, 61–77.CrossRefGoogle Scholar
Lin, Y. C., Rikihisa, Y., Kono, H. and Gu, Y. ( 1990). Effects of larval tapeworm (Taenia taeniaeformis) infection on reproductive functions in male and female host rats. Experimental Parasitology 70, 344–352.CrossRefGoogle Scholar
Lloyd, S. and Soulsby, E. J. L. ( 1978). The role of IgA immunoglobulins in the passive transfer of protection to Taenia taeniaeformis in the mouse. Immunology 34, 939–945.Google Scholar
Lucker, J. T. ( 1960). A test of resistance of Teania saginata eggs to freezing. Journal of Parasitology 46, 304.CrossRefGoogle Scholar
Martinet, L. ( 1966). Détermination de l’âge chez le campagnol des champs (Microtus arvalis) par la pesée du cristallin. Mammalia 30, 425–430.CrossRefGoogle Scholar
Montgomery, S. S. J. and Montgomery, W. I. ( 1988). Cyclic and non-cyclic dynamics in populations of the helminths parasites of wood mice, Apodemus sylvaticus. Journal of Helminthology 62, 78–90.CrossRefGoogle Scholar
Nelson, R. J., Demas, G. E., Klein, S. L. and Kriegsfeld, L. J. ( 2002). Seasonal Patterns of Stress, Immune Function and Disease. Cambridge University Press, Cambridge.CrossRef
Ostfeld, R. S., Canham, C. D. and Pugh, S. R. ( 1993). Intrinsic density-dependent regulation of vole populations. Nature, London 366, 259–261.CrossRefGoogle Scholar
Payne, R., Murray, D., Harding, S., Baird, D., Soutar, D. and Lane, P. ( 2003). GenStat® for Windows(tm) (7th Edition) – Introduction, VSN International, Wilkinson House, Jordon Hill Road, Oxford, UK.
Saucy, F. ( 1997). Juvenile dispersal in the vole (Arvicola terrestris) during rainy nights: a preliminary report. Bulletin de la Société Vaudoise des Sciences Naturelles 84, 333–345.Google Scholar
Schmidt, G. D. ( 1986). Handbook of Tapeworm Identification. CRC Press, Boca Raton, Florida, USA.
Stahl, P., Artois, M. and Aubert, M. F. ( 1988). Organisation spatiale et déplacements des chats forestiers adultes (Felis sylvestris, Shreber, 1777) en Lorraine. Revue d'Ecologie (Terre et Vie) 43, 113–131.Google Scholar
Stanko, M., Miklisova, D., De Bellocq, J. G. and Morand, S. ( 2002). Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131, 289–295. DOI: 10.1007/s00442-002-0889-5CrossRefGoogle Scholar
Theis, J. H. and Schwab, R. G. ( 1992). Seasonal prevalence of Teania taeniaeformis: relationship to age, sex, reproduction and abundance of an intermediate host (Peromyscus maniculatus). Journal of Wildlife Diseases 28, 42–50.CrossRefGoogle Scholar
Tompkins, D. M., Dobson, A. P., Arneberg, P., Begon, M., Cattadori, I. M., Greenman, J. V., Heesterbeek, J. A. P., Hudson, P. J., Newborn, D., Pugliese, A., Rizzoli, A., Rosà, R., Rosso, P. J. and Wilson, K. ( 2002). Parasites and host population dynamics. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 45–62. Oxford University Press, Oxford.