Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T22:10:11.377Z Has data issue: false hasContentIssue false
  • English
  • Français

Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from N.E. Poland. 2. The infracommunity level

Published online by Cambridge University Press:  02 June 2008

J. M. BEHNKE ,
A. BAJER ,
P. D. HARRIS ,
L. NEWINGTON ,
E. PIDGEON ,
G. ROWLANDS ,
C. SHERIFF ,
K. KULIŚ-MALKOWSKA ,
E. SIńSKI  and
F. S. GILBERT
...Show all authors
J. M. BEHNKE*
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
A. BAJER
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warsaw, ul. Miecznikowa 1, 02-096 Warszawa, Poland
P. D. HARRIS
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
L. NEWINGTON
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
E. PIDGEON
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
G. ROWLANDS
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
C. SHERIFF
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
K. KULIŚ-MALKOWSKA
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warsaw, ul. Miecznikowa 1, 02-096 Warszawa, Poland
E. SIńSKI
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warsaw, ul. Miecznikowa 1, 02-096 Warszawa, Poland
F. S. GILBERT
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
C. J. BARNARD
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
*
*Corresponding author: School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK. Tel: 0044 (0) 115 951 3208. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The relative importance of temporal and spatial effects was assessed in helminth communities of bank voles (Myodes glareolus) in 3 woodland sites in N.E. Poland in the late summers of 1999 and 2002. Among common species the rank order of sites in relation to prevalence and abundance of infection was maintained between surveys. Site effects accounted for most of the deviance (in statistical models), and time was less important, so the exact location from which voles were sampled was of critical importance. The only exception was Syphacia petrusewiczi. In contrast, for derived measures such as species richness and diversity, most deviance was accounted for by host age, and the interaction between site and year was significant, implying that rank order of sites changed between years. Temporal effects on derived measures were generated primarily by a combination of relatively small changes in prevalence and abundance of the common, rather than the rare, species between the years of the study. In the medium-term, therefore, helminth communities of bank voles in N.E. Poland had a stable core, suggesting a substantial strong element of predictability.

Keywords

infracommunitiesbank volesMyodes glareolusClethrionomyshelminthsnematodescestodessite-specific parasite variation
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 8 , July 2008 , pp. 999 - 1018
Copyright
Copyright © 2008 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

Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. S. (2000). Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 74, 7–16.CrossRefGoogle ScholarPubMed
Alexander, J. and Stimson, W. H. (1988). Sex hormones and the course of parasitic infections. Parasitology Today 4, 189–193.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Bajer, A., Behnke, J. M., Pawełczyk, A., Kuliś, K., Sereda, M. J. and Siński, E. (2005). Medium-term temporal stability of the helminth component community structure in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland. Parasitology 130, 213–228.CrossRefGoogle ScholarPubMed
Bangs, E. E. (1985). Occurrence of the nematode Protospirura muris in Alaskan Northern red-backed voles, Clethrionomys rutilus. Canadian Field Naturalist 99, 386–388.CrossRefGoogle Scholar
Beaucournu, J. C. and Chabaud, A. G. (1963). Infestation spontanée de Puces par le spiruride Mastophorus muris (Gmelin). Annales de Parasitologie (Paris) 38, 931–934.Google Scholar
Behnke, J. M., Bajer, A., Harris, P. D., Newington, L., Pidgeon, E., Rowlands, G., Sheriff, C., Kuliś-Malkowska, K., Siński, E., Gilbert, F. S. and Barnard, C. J. (2008). Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from N.E. Poland. 1. Regional fauna and component community levels. Parasitology 135.Google ScholarPubMed
Behnke, J. M., Barnard, C. J., Bajer, A., Bray, D., Dinmore, J., Frake, K., Osmond, J., Race, T. and Siński, E. (2001). Variation in the helminth community structure in bank voles (Clethrionomys glareolus) from three comparable localities in the Mazury Lake District region of Poland. Parasitology 123, 401–414.CrossRefGoogle ScholarPubMed
Behnke, J. M., Harris, P. D., Bajer, A., Barnard, C. J., Sherif, N., Cliffe, L., Hurst, J., Lamb, M., Rhodes, A., James, M., Clifford, S., Gilbert, F. S. and Zalat, S. (2004). Variation in the helminth community structure in spiny mice (Acomys dimidiatus) from four montane wadis in the St. Katherine region of the Sinai Peninsula in Egypt. Parasitology 129, 379–398.CrossRefGoogle ScholarPubMed
Behnke, J. M., Lewis, J. W., Mohd Zain, S. N. and Gilbert, F. S. (1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host-age, sex and year on prevalence and abundance of infections. Journal of Helminthology 73, 31–44.CrossRefGoogle ScholarPubMed
Booth, M. (2006). The role of residential location in apparent helminth and malaria associations. Trends in Parasitology 22, 359–362.CrossRefGoogle ScholarPubMed
Brooks, D. R. and Hoberg, E. P. (2007). How will global climate change affect parasite-host assemblages? Trends in Parasitology 23, 571–574.CrossRefGoogle ScholarPubMed
Bugmyrin, S. V., Ieshko, E. P., Anikanova, V. A. and Bespyatova, L. A. (2005). Patterns of host-parasite interactions between the nematode Heligmosomum mixtum (Schulz, 1952) and the bank vole (Clethrionomys glareolus Schreber, 1780). Parasitologia 39, 414–422.Google Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Calvete, C., Blanco-Aguiar, J. A., Virgós, E., Cabezas-Diaz, S. and Villafuerte, R. (2004). Spatial variation in helminth community structure in the red-legged partridge (Alectoris rufa L.): effects of definitive host density. Parasitology 129, 101–113.CrossRefGoogle Scholar
Campos, M. Q. and Vargas, M. V. (1977). Biologia de Protospirura muricola Gedoelst, 1916 y Mastophorus muris (Gmelin, 1790) (Nematoda: Spiruridae), en Costa Rica. I. Huespedes intermediarios. Revista de Biologia Tropical 25, 191–207.Google Scholar
Campos, Q. M. and Vargas, E. M. (1978). The biology of Protospirura muricola and Mastophorus muris (Nematoda: Spiruridae) in Costa Rica II. Definitive hosts. Revista de Biologia Tropica 26, 199–211.Google Scholar
Carleton, M. D., Musser, G. G. and Pavlinov, I. Å. (2003). Myodes Pallas, 1811, is the valid name for the genus of red-backed voles. In Systematics, Phylogeny and Paleontology of Small Mammals. Proceedings of the International Conference devoted to the 90th anniversary of Prof. I. M. Gromov, November 2003, Saint Petersburg (ed. Averianov, A. and Abramson, N.), pp. 96–98.Google Scholar
Dyer, W. G. and Olsen, O. W. (1967). Biology of Mastophorus numidica (Seurat, 1914) Read and Millemann, 1953 (Nematoda: Spiruridae) with a description of the juvenile stages. Proceedings of the Helminthological Society of Washington 34, 98–103.Google Scholar
Eira, C., Torres, J., Vingada, J. and Miquel, J. (2006). Ecological aspects influencing the helminth community of the wood mouse Apodemus sylvaticus in Dunas de Mira, Portugal. Acta Parasitologica 51, 300–308.CrossRefGoogle Scholar
Elliott, J. M. (1977). Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates. Freshwater Biological Association, Cumbria, UK.Google Scholar
Ferrari, N., Cattadori, I. M., Nespereira, J., Rizzoli, A. and Hudson, P. J. (2004). The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecology Letters 7, 88–94.CrossRefGoogle Scholar
Gipps, J. H. W. (1985). The behaviour of bank voles. In The Ecology of Woodland Rodents Bank Voles and Wood Mice. Symposia of the Zoological Society of London, 55, 61–87. The Zoological Society of London, Clarendon Press, Oxford, UK.Google Scholar
Gregory, R. D., Montgomery, S. S. J. and Montgomery, W. I. (1992). Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749–757.CrossRefGoogle Scholar
Guernier, V., Hochberg, M. E. and Guegan, J.-F. (2004). Ecology drives the worldwide distribution of human diseases. PLoS Biology 2, 740–746.CrossRefGoogle ScholarPubMed
Haukisalmi, V. (1986). Frequency distributions of helminths in microtine rodents in Finnish Lapland. Annales Zoologici Fennici 23, 141–150.Google 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 ScholarPubMed
Haukisalmi, V. and Henttonen, H. (2000). Variability of helminth assemblages and populations in the bank vole Clethrionomys glareolus. Polish Journal of Ecology 48 (Suppl.) 219–231.Google Scholar
Haukisalmi, V., Henttonen, H. and Tenora, F. (1987). Parasitism by helminths in the grey-sided vole (Clethrionomys rufocanus) in northern Finland: influence of density, habitat and sex of the host. Journal of Wildlife Diseases 23, 233–241.CrossRefGoogle ScholarPubMed
Haukisalmi, V., Henttonen, H. and Tenora, F. (1988). Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807–825.CrossRefGoogle Scholar
Hudson, P. J., Cattadori, I. M., Boag, B. and Dobson, A. P. (2006). Climate disruption and parasite-host dynamics: patterns and processes associated with warming and the frequency of extreme climatic events. Journal of Helminthology 80, 175–182.CrossRefGoogle ScholarPubMed
Janovy, J. Jr., Clopton, R. E., Clopton, D. A., Snyder, S. D., Efting, A. and Krebs, L. (1995). Species density distributions as null models for ecologically significant interactions of parasite species in an assemblage. Ecological Modelling 77, 189–196.CrossRefGoogle Scholar
Kennedy, C. R., Bush, A. O. and Aho, J. M. (1986). Patterns in helminth communities: why are birds and fish different? Parasitology 93, 205–215.CrossRefGoogle ScholarPubMed
Kennedy, C. R. and Hartvigsen, R. A. (2000). Richness and diversity of intestinal metazoan communities in brown trout Salmo trutta compared to those of eels Anguilla anguilla in their European heartlands. Parasitology 121, 55–64.CrossRefGoogle ScholarPubMed
Keymer, A. E. and Dobson, A. P. (1987). The ecology of helminths in populations of small mammals. Mammal Review 17, 105–116.CrossRefGoogle Scholar
Kisielewska, K. (1970 a). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). 1. Structure and seasonal dynamics of helminth groupings in a host population in the Białowieża National Park. Acta Parasitologica Polonica 18, 121–147.Google Scholar
Kisielewska, K. (1970 b). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). IV. Spatial structure of a helminth grouping within the host population. Acta Parasitologica Polonica 18, 177–196.Google Scholar
Kisielewska, K. (1971). Intestinal helminths as indicators of the age structure of Microtus arvalis Pallas, 1778 population. Bulletin de L'Academie Polonaise des Sciences. Serie des Sciences Biologiques Cl.II, 19, 275–282.Google Scholar
Korslund, L. and Steen, H. (2006). Small rodent winter survival: snow conditions limit access to food resources. Journal of Animal Ecology 75, 156–166.CrossRefGoogle ScholarPubMed
Langley, R. and Fairley, J. S. (1982). Seasonal variations in infestations of parasites in a wood mouse Apodemus sylvaticus population in the west of Ireland. Journal of Zoology, London 198, 249–261.CrossRefGoogle Scholar
Lewis, J. W. (1968). Studies on the helminth parasites of voles and shrews from Wales. Journal of Zoology, London 154, 313–331.CrossRefGoogle Scholar
Lowrie, F. M. (2003). Host-Parasite Relationship of Protospirura muricola, a Spirurid Nematode. M.Phil thesis, University of Nottingham, UK.Google Scholar
Margolis, L., Esch, G. W., Holmes, J. C., Kuris, A. M. and Schad, G. A. (1982). The use of ecological terms in parasitology (report of an ad hoc committee of The American Society of Parasitologists). Journal of Parasitology 68, 131–133.CrossRefGoogle Scholar
Miyata, J. (1939). Studies on the life history of the nematode Protospirura muris (Gmelin) parasitic in the stomach of the rat, especially on the relation of the intermediate hosts, cockroaches, skin moth and rat fleas. Volumen jubilare pro Professore Sadao Yoshida, Osaka, Japan 1, 101–136 (In Japanese.)Google Scholar
Mollhagan, T. (1978). Habitat influence on helminth parasitism of the cotton rat in western Texas, with remarks on some of the parasites. The Southwestern Naturalist 23, 401–407.CrossRefGoogle Scholar
Montgomery, S. S. J. and Montgomery, W. I. (1989). Spatial and temporal variation in the infracommunity structure of helminths of Apodemus sylvaticus (Rodentia: Muridae). Parasitology 98, 145–150.CrossRefGoogle ScholarPubMed
Montgomery, S. S. J. and Montgomery, W. I. (1990). Structure, stability and species interactions in helminth communities of wood mice Apodemus sylvaticus. International Journal for Parasitology 20, 225–242.CrossRefGoogle ScholarPubMed
Morand, S. and Guegan, J. F. (2000). Distribution and abundance of parasite nematodes: ecological specialization, phylogenetic constraints or simply epidemiology? Oikos 88, 563–573.CrossRefGoogle Scholar
Poulin, R. (1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937–944.CrossRefGoogle Scholar
Poulin, R. (1996). Sexual inequalities in helminth infections: a cost of being a male? The American Naturalist 147, 287–295.CrossRefGoogle Scholar
Poulin, R. (1997). Species richness of parasite assemblages: evolution and patterns. Annual Reviews in Ecology and Systematics 28, 341–358.CrossRefGoogle Scholar
Quentin, J. C. (1969). Cycle biologique de Protospirura muricola Gedoelst 1916 (Nematoda; Spiruridae). Annales de Parasitologie (Paris) 44, 485–504.Google Scholar
Quentin, J. C. (1970). Morphogenese larvaire du spiruride Mastophorus muris (Gmelin, 1790). Annales de Parasitologie (Paris) 45, 839–855.Google ScholarPubMed
Roberts, C. W., Satoskar, A. and Alexander, J. (1996). Sex steroids, pregnancy-associated hormones and immunity to parasitic infection. Parasitology Today 12, 382–388.CrossRefGoogle ScholarPubMed
Rohlf, F. J. and Sokal, R. R. (1995). Statistical Tables. W. H. Freeman and Company, San Francisco.Google Scholar
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111–S127.CrossRefGoogle ScholarPubMed
Shogaki, Y., Mizuno, S. and Itoh, H. (1972). On Protospirura muris (Gmelin) a parasic nematode of the brown rat in Nagoya City. Japanese Journal of Parasitology 21, 28–38.Google Scholar
Tenora, F. and Stanek, M. (1995). Changes of the helminthofauna in several Muridae and Arvicolidae at Lednice in Moravia. II. Ecology. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 43, 57–65.Google Scholar
Thul, J. E., Forrester, D. J. and Abercrombie, C. L. (1985). Ecology of parasitic helminths of wood ducks, Aix sponsa, in the Atlantic flyway. Proceedings of the Helminthological Society of Washington 52, 297–310.Google Scholar
Torres, J., Miquel, J. and Motje, M. (2001). Helminth parasites of the Eurasian badger (Meles meles L.) in Spain: a biogeographic approach. Parasitology Research 87, 259–263.CrossRefGoogle Scholar
Venables, W. N. and Ripley, B. D. (1997). Modern Applied Statistics with S-Plus. Springer, New York.CrossRefGoogle Scholar
Washington, H. G. (1984). Diversity, biotic and similarity indices. A review with special relevance to aquatic ecosystems. Water Research 18, 653–694.CrossRefGoogle Scholar
Wilson, D. E. and Reeder, D. M. (2005). Mammal Species of the World. A Taxonomic and Geographic Reference, 3rd Edn. Johns Hopkins University Press, Baltimore, USA.CrossRefGoogle Scholar
Xu, R. (2003). Measuring explained variation in linear mixed effects models. Statistics in Medicine 22, 3527–3541.CrossRefGoogle ScholarPubMed
Ylonen, H. and Viitala, J. (1991). Social overwintering and food distribution in the bank vole Clethrionomys glareolus. Hoarctic Ecology 14, 131–137.Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasitic infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.CrossRefGoogle ScholarPubMed