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Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from N.E. Poland. 1. Regional fauna and component community levels

Published online by Cambridge University Press:  04 July 2008

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 Warsaw, 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 Warsaw, Poland
E. SIŃSKI
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warsaw, ul. Miecznikowa 1, 02-096 Warsaw, 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: +44 (0) 115 951 3208. Fax: +44 (0) 115 951 3251. E-mail: [email protected]

Summary

Helminth infections were studied in bank voles (Myodes glareolus) from 3 woodland sites in N.E. Poland in the late summers of 1999 and 2002, to assess the temporal stability of derived statistics describing the regional helminth fauna and component community structure, and spatial influence on the latter. Regional helminth fauna changed dramatically between the two years, primarily due to a fall in the abundance of Syphacia petrusewiczi but was partially compensated for by an increase in Mesocestoides lineatus and Cladotaenia globifera. It was dominated by nematodes overall, but more so in 1999 than in 2002 when larval cestodes were more frequent. Most derived parameters for component community structure varied considerably between sites and the two surveys, the hierarchical order for sites not being maintained between surveys. They were susceptible to the disproportionate influence of three relatively rare, unpredictable species with the greatest overall aggregated distribution among hosts. Jaccard's similarity index was less influenced by the rare species, showing greater stability between sites and across years. In conclusion, temporal variation confounded any site-specific characteristics of the summary measures quantified in this study and their usefulness is therefore restricted to the years in which the surveys were conducted.

Type
Original Articles
Copyright
Copyright © 2008 Cambridge University Press

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References

Aars, J., Ims, R. A., Liu, H. P., Mulvey, M. and Smith, M. H. (1998). Bank voles in linear habitats show restricted gene flow as revealed by mitochondrial DNA (mtDNA). Molecular Ecology 7, 13831389.Google Scholar
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, 716.CrossRefGoogle ScholarPubMed
Alibhai, S. K. and Gipps, J. H. W. (1985). The population dynamics of bank voles. In The Ecology of Woodland Rodents Bank Voles and Wood Mice. Symposia of the Zoological Society of London, 55, 277313. The Zoological Society of London, Clarendon Press, Oxford.Google Scholar
Bajer, A., Pawełczyk, A., Behnke, J. M., Gilbert, F. S. and Siński, E. (2001). Factors affecting the haemoparasitic component community structure in bank voles (Clethrionomys glareolus) from the Mazury lake district region of Poland. Parasitology 122, 4354.Google 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, 213228.Google Scholar
Behnke, J. M. (1974). The Biology of Aspiculuris tetraptera (Schulz). Ph.D. thesis, University of London.Google Scholar
Behnke, J. M. (1975). Aspiculuris tetraptera in wild Mus musculus. The prevalence of infection in male and female mice. Journal of Helminthology 49, 8590.Google Scholar
Behnke, J. M. (1976). Aspiculuris tetraptera in wild Mus musculus. Age resistance and acquired immunity. Journal of Helminthology 50, 197202.Google Scholar
Behnke, J. M., Bajer, A., Harris, P., 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. 2. The infracommunity level. Parasitology 135.Google Scholar
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, 401414.Google Scholar
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, 379398.Google 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, 101113.Google Scholar
Carleton, M. D., Musser, G. G. and Pavlinov, I.A. (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. 9698.Google Scholar
Chernin, J. and McLaren, D. J. (1983). The pathology induced in laboratory rats by metacestodes of Taenia crassiceps and Mesocestoides corti (Cestoda). Parasitology 87, 279287.Google Scholar
Corbet, G. B. (1978). Mammals of the Palaearctic Region: A Taxonomic Review. British Museum (Natural History), London.Google Scholar
Dove, A. D. M. and Cribb, T. H. (2006). Species accumulation curves and their applications in parasite ecology. Trends in Parasitology 22, 568574.CrossRefGoogle ScholarPubMed
Esch, G. W., Bush, A. O. and Aho, J. M. (1990). Parasite Communities: Patterns and Processes. Chapman and Hall, London.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, 300308.Google Scholar
Ferrer, D., Molina, R., Adelantado, C. and Kinsella, J. M. (2004). Helminths isolated from the digestive tract of diurnal raptors in Catalonia, Spain. Veterinary Record 154, 1720.Google Scholar
Gerlach, G. and Musolf, K. (2000). Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conservation Biology 14, 10661074.CrossRefGoogle Scholar
Gliwicz, J. and Ims, R. A. (2000). Dispersal in the bank vole. Polish Journal of Ecology 48 (Suppl.) 5161.Google Scholar
Hartvigsen, R. and Kennedy, C. R. (1993). Patterns in the composition and richness of helminth communities in brown trout, Salmo trutta, in a group of reservoirs. Journal of Fish Biology 43, 603615.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, 309315.CrossRefGoogle ScholarPubMed
Haukisalmi, V. and Henttonen, H. (1993). Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. Journal of Animal Ecology 62, 221229.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, 233241.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, 5564.Google 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 Białowiea National Park. Acta Parasitologica Polonica 18, 121147.Google Scholar
Kisielewska, K. (1970 b). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). III. Structure of the helminth groupings in C. glareolus populations of various forest biocoenoses in Poland. Acta Parasitologica Polonica 18, 163176.Google Scholar
Lande, R. (1996). Statistics and partitioning of species diversity, and similarity among communities. Oikos 76, 513.Google Scholar
Le Pesteur, M. H., Giraudoux, P., Delattre, P., Damange, J. P. and Quere, J. P. (1992). Spatiotemporal distribution of four species of cestodes in a landscape of mid-altitude mountains (Jura, France). Annales de Parasitologie Humaine et Comparée 67, 155160.CrossRefGoogle Scholar
Lewis, J. W. (1968). Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology, London 154, 287312.Google Scholar
Lewis, J. W. (1987). Helminth parasites of British rodents and insectivores. Mammal Review 17, 8193.CrossRefGoogle Scholar
Loos-Frank, B. (1980 a). Mesocestoides leptothylaceus n.sp. und das nomenklatorische Problem in der Gattung Mesocestoides Vaillant, 1863 (Cestoda, Mesocestoididae). Tropenmedizin und Parasitologie 31, 214.Google Scholar
Loos-Frank, B. (1980 b). The common vole, Microtus arvalis Pall, as the intermediate host of Mesocestoides (Cestoda) in Germany. Zeitschrift für Parasitenkunde 63, 129136.CrossRefGoogle ScholarPubMed
Loos-Frank, B. (1991). One or two intermediate hosts in the life cycle of Mesocestoides (Cyclophyllidea, Mesocestoididae)? Parasitology Research 77, 726728.CrossRefGoogle ScholarPubMed
Loos-Frank, B. (2000). An up-date of Verster's (1969) ‘Taxonomic revision of the genus Taenia Linnaeus’ (Cestoda) in table format. Systematic Parasitology 45, 155183.Google Scholar
Montgomery, S. S. J. and Montgomery, W. I. (1988). Cyclic and non-cyclic dynamics in populations of the helminth parasites of wood mice Apodemus sylvaticus. Journal of Helminthology 62, 7890.Google 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, 145150.Google Scholar
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, 225242.Google Scholar
Poulin, R. (1997). Species richness of parasite assemblages: evolution and patterns. Annual Reviews in Ecology and Systematics 28, 341358.Google Scholar
Poulin, R. (2004). Macroecological patterns of species richness in parasite assemblages. Basic and Applied Ecology 5, 423434.Google Scholar
Poulin, R. (2007). Are there general laws in parasite ecology? Parasitology 134, 763776.CrossRefGoogle ScholarPubMed
Poulin, R. and Mouillot, D. (2004). The evolution of taxonomic diversity in helminth assemblages of mammalian hosts. Evolutionary Ecology 18, 231247.CrossRefGoogle Scholar
Premier, J. (1983). On the problem of European Mesocestoides species (Cestoda) from mammals. Helminthologia 20, 8995.Google Scholar
Pucek, Z., Ryszkowski, L. and Zejda, J. (1969). Estimation of average length of life in bank vole, Clethrionomys glareolus (Schreber, 1780). In Energy Flow Through Small Mammal Populations (ed. Petrusewicz, K. and Ryszkowski, L.), pp. 137210. Polish Scientific Publications, Warszawa.Google Scholar
Rohlf, F. J. and Sokal, R. R. (1995). Statistical Tables. W.H. Freeman and Company, San Francisco.Google Scholar
Sharpe, G. I. (1964). The helminth parasites of some small mammal communities. I. The parasites and their hosts. Parasitology 54, 145154.Google Scholar
Smal, C. M. and Fairley, J. S. (1984). The spread of the bank vole Clethrionomys glareolus in Ireland. Mammal Review 14, 7178.Google Scholar
Specht, D. and Voge, M. (1965). Asexual multiplication of Mesocestoides tetrathyridia in laboratory animals. Journal of Parasitology 51, 268272.CrossRefGoogle ScholarPubMed
Spitzenberger, F. (1999). Clethrionomys glareolus. In The Atlas of European Mammals (ed. Mitchell-Jones, A. J., Amori, G., Bogdanowicz, W., Krystufek, B., Reijnders, P. J. H., Spizenberger, F., Stubbe, M., Thissen, J. B. M., Vohralik, V. and Zima, J.), pp. 212213. Academic Press, London.Google Scholar
Taylor, L. R. (1961). Aggregation, variance and the mean. Nature, London 189, 732735.Google Scholar
Tenora, F. (2004). Notes to Mesocestoides Vaillant, 1863 (Cestoda) and findings of Mesocestoides sp. parasitizing Canis familiaris (Carnivora) in the Czech Republic. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 52, 2533.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, 5765.Google Scholar
Timi, J. T. and Poulin, R. (2003). Parasite community structure within and across host populations of a marine pelagic fish: how repeatable is it? International Journal for Parasitology 33, 13531362.Google Scholar
Van Apeldoorn, R. C., Oostenbrink, W. T., van Winden, A. and van der Zee, F. F. (1992). Effects of habitat fragmentation on the bank vole, Clethrionomys glareolus, in an agricultural landscape. Oikos 65, 265274.Google Scholar
Verster, A. (1969). A taxonomic revision of the genus Taenia Linnaeus, 1758 S. Str. Ondersteport Journal of Veterinary Research 36, 358.Google ScholarPubMed
Walther, B. A., Cotgreave, P., Gregory, R. D., Price, R. D. and Clayton, D. H. (1995). Sampling effort and parasite species richness. Parasitology Today 11, 306310.CrossRefGoogle ScholarPubMed
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