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Long-term spatiotemporal stability and dynamic changes in helminth infracommunities of bank voles (Myodes glareolus) in NE Poland

Published online by Cambridge University Press:  07 October 2015

MACIEJ GRZYBEK ,
ANNA BAJER ,
MAŁGORZATA BEDNARSKA ,
MOHAMMED AL-SARRAF ,
JOLANTA BEHNKE-BOROWCZYK ,
PHILIP D. HARRIS ,
STEPHEN J. PRICE ,
GABRIELLE S. BROWN ,
SARAH-JANE OSBORNE  and
EDWARD SIŃSKI
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MACIEJ GRZYBEK
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK Department of Parasitology and Invasive Diseases, Faculty of Veterinary Medicine, University of Life Sciences in Lublin, 12 Akademicka Street, 20-950 Lublin, Poland
ANNA BAJER
Affiliation:
Department of Parasitology, Faculty of Biology, Institute of Zoology, University of Warsaw, 1 Miecznikowa Street, 02-096 Warsaw, Poland
MAŁGORZATA BEDNARSKA
Affiliation:
Department of Parasitology, Faculty of Biology, Institute of Zoology, University of Warsaw, 1 Miecznikowa Street, 02-096 Warsaw, Poland
MOHAMMED AL-SARRAF
Affiliation:
Department of Parasitology, Faculty of Biology, Institute of Zoology, University of Warsaw, 1 Miecznikowa Street, 02-096 Warsaw, Poland
JOLANTA BEHNKE-BOROWCZYK
Affiliation:
Department of Forest Pathology, Faculty of Forestry, Poznań University of Life Sciences, 71C Wojska Polskiego Street, 60-625 Poznan, Poland
PHILIP D. HARRIS
Affiliation:
National Centre for Biosystematics, Natural History Museum, University of Oslo, N-0562 Oslo 5, Norway
STEPHEN J. PRICE
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
GABRIELLE S. BROWN
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
SARAH-JANE OSBORNE
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
EDWARD SIŃSKI
Affiliation:
Department of Parasitology, Faculty of Biology, Institute of Zoology, University of Warsaw, 1 Miecznikowa Street, 02-096 Warsaw, Poland
JERZY M. BEHNKE*
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
*
* Corresponding author. School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK. E-mail: [email protected]
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Summary

Parasites are considered to be an important selective force in host evolution but ecological studies of host-parasite systems are usually short-term providing only snap-shots of what may be dynamic systems. We have conducted four surveys of helminths of bank voles at three ecologically similar woodland sites in NE Poland, spaced over a period of 11 years, to assess the relative importance of temporal and spatial effects on helminth infracommunities. Some measures of infracommunity structure maintained relative stability: the rank order of prevalence and abundance of Heligmosomum mixtum, Heligmosomoides glareoli and Mastophorus muris changed little between the four surveys. Other measures changed markedly: dynamic changes were evident in Syphacia petrusewiczi which declined to local extinction, while the capillariid Aonchotheca annulosa first appeared in 2002 and then increased in prevalence and abundance over the remaining three surveys. Some species are therefore dynamic and both introductions and extinctions can be expected in ecological time. At higher taxonomic levels and for derived measures, year and host-age effects and their interactions with site are important. Our surveys emphasize that the site of capture is the major determinant of the species contributing to helminth community structure, providing some predictability in these systems.

Keywords

helminth infracommunitiesbank volesMyodes glareolusClethrionomyshelminthsnematodescestodessite-specific parasite variation
Type
Research Article
Information
Parasitology , Volume 142 , Issue 14 , December 2015 , pp. 1722 - 1743
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Copyright © Cambridge University Press 2015 

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References

REFERENCES

Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. S. (1998). Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 72, 93–100.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, 7–16.Google Scholar
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 (ed. Flowerdew, J. R., Gurnell, J. and Gipps, J. H. W.), pp. 277–313. Clarendon Press, Oxford. Symposia of the Zoological Society of London Vol. 55.Google Scholar
Anderson, R. M. (1982). The population dynamics and control of hookworm and roundworm infections. In Population Dynamics of Infectious Diseases. Theory and Applications (ed. Anderson, R. M.), pp. 67–108. Chapman and Hall, London.Google Scholar
Arneberg, P. (2001). An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography 24, 352–358.CrossRefGoogle Scholar
Bajer, A., Behnke, J. M., Pawelczyk, A., Kulis, 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.Google Scholar
Bajer, A., Welc-Falęciak, R., Bednarska, M., Alsarraf, M., Behnke-Borowczyk, J., Siński, E. and Behnke, J. M. (2014). Long-term spatiotemporal stability and dynamic changes in the haemoparasite community of bank voles (Myodes glareolus) in NE Poland. Microbial Ecology 68, 196–211.Google Scholar
Baker, D. G. (2007). Parasites of rats and mice. In Flynn's Parasites of Laboratory Animals, 2nd Edn (ed. Baker, D. G.), pp. 339–340. Blackwell Publishing, Ames, IA.Google Scholar
Barnard, C. J., Behnke, J. M., Bajer, A., Bray, D., Race, T., Frake, K., Osmond, J., Dinmore, J. and Siński, E. (2002). Local variation in endoparasite intensities of bank voles (Clethrionomys glaroelus) from ecologically similar sites: morphometric and endocrine correlates. Journal of Helminthology 76, 103–112.Google Scholar
Barnard, C. J., Kuliś, K., Behnke, J. M., Bajer, A., Gromadzka-Ostrowska, J., Stachon, M. and Siński, E. (2003). Local variation in helminth burdens of bank voles (Clethrionomys glareolus) from ecologically similar sites: temporal stability and relationships with hormone concentrations and social behaviour. Journal of Helminthology 77, 185–195.Google Scholar
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.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, 401–414.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 a). 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, 985–997.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 b). Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from NE Poland. 2. The infracommunity level. Parasitology 135, 999–1018.CrossRefGoogle ScholarPubMed
Behnke, J. M., Stewart, A., Bajer, A., Grzybek, M., Harris, P. D., Lowe, A., Ribas, A., Smales, L. and Vandegrift, K. J. (2016). Bank voles (Myodes glareolus) and house mice (Mus musculus musculus/domesticus) in Europe are each parasitized by their own distinct species of Aspiculuris (Nematoda, Oxyurida). Parasitology (Epub ahead of print) doi:10.1017/S0031182015000864.Google Scholar
Boag, B., Lello, J., Fenton, A., Tompkins, D. M. and Hudson, P. J. (2001). Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus). International Journal for Parasitology 31, 1421–1428.Google Scholar
Booth, M. (2006). The role of residential location in apparent helminth and malaria associations. Trends in Parasitology 22, 359–362.Google Scholar
Bordes, F., Ponlet, N., de Bellocq, J. G., Ribas, A., Krasnov, B. R. and Morand, S. (2012). Is there sex-biased resistance and tolerance in Mediterranean wood mouse (Apodemus sylvaticus) populations facing multiple helminth infections? Oecologia 170, 123–135.Google Scholar
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
Bujalska, G. (2000). The bank vole population in Crab-apple Island. Polish Journal of Ecology 48 (Suppl.), 97–106.Google Scholar
Bundy, D. A. P. (1990). Is the hookworm just another geohelminth? Chapter 10. In Hookworm Disease. Current Status and New Directions (ed. Schad, G. A. and Warren, K. S.), pp. 147–164. Taylor and Francis, London.Google Scholar
Calvete, C., Blanco-Aguiar, J. A., Virgós, E., Cabezas-Díaz, 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.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, Saint Petersburg, November 2003 (ed. Averianov, A. and Abramson, N.), p. 96.Google Scholar
Carleton, M. D., Gardner, A. L., Pavlinov, I. Y. and Musser, G. G. (2014). The valid generic name for red-backed voles (Muroidea: Cricetidae: Arvicolinae): restatement of the case for Myodes Pallas, 1811. Journal of Mammology 95, 943–959.CrossRefGoogle Scholar
Cattadori, I. M., Boag, B. and Hudson, P. J. (2008). Parasite co-infection and interaction as drivers of host heterogeneity. International Journal for Parasitology 38, 371–380.Google Scholar
Cornell, S. J., Bjornstad, O. N., Cattadori, I. M., Boag, B. and Hudson, P. J. (2008). Seasonality, cohort-dependence and the development of immunity in a natural host-nematode system. Proceedings of the Royal Society B 275, 511–518.CrossRefGoogle Scholar
Elliott, J. M. (1977). Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates. Freshwater Biological Association, Cumbria, UK.Google Scholar
Elton, C., Ford, E. B., Baker, J. R. and Gardner, A. D. (1931). The health and parasites of a wild mouse population. Proceedings of the Royal Zoological Society, London 101, 657–721.Google Scholar
European Environment Agency (2014). http://www.eea.europa.eu/themes/climate.Google Scholar
Ghazal, A. M. and Avery, R. A. (1974). Population dynamics of Hymenolepis nana in mice: fecundity and the ‘crowding effect’. Parasitology 69, 403–415.Google Scholar
Grear, D. A. and Hudson, P. (2011). The dynamics of macroparasite host-self-infection: a study of the patterns and processes of pinworm (Oxyuridae) aggregation. Parasitology 138, 619–627.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.Google Scholar
Grzybek, M., Bajer, A., Behnke-Borowczyk, J., Al-Sarraf, M. and Behnke, J. M. (2015). Female host sex-biased parasitism with the rodent stomach nematode Mastophorus muris in wild bank voles (Myodes glareolus). Parasitology Research 114, 523–533.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.Google Scholar
Haukisalmi, V. and Henttonen, H. (2000). The 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.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, 807–825.CrossRefGoogle Scholar
Haukisalmi, V., Henttonen, H. and Vikman, P. (1996). Variability of sex ratio, mating probability and egg production in an intestinal nematode in its fluctuating host population. International Journal for Parasitology 26, 755–764.Google Scholar
Hill, W. A., Randolph, M. M. and Mandrell, T. D. (2009). Sensitivity of perianal tape impressions to diagnose pinworm (Syphacia spp.) infections in rats (Rattus norvegicus) and mice (Mus musculus). Journal of the American Association for Laboratory Animal Science 48, 378–380.Google Scholar
Hudson, P. J., Cattadori, I. M., Boag, B. and Dobson, A. P. (2006). Climatic disruption and parasite-host dynamics: patterns and processes associated with warming and frequency of extreme climatic events. Journal of Helminthology 80, 175–182.Google Scholar
Huntley, J. W., Fürsich, F. T., Alberti, M., Hethke, M. and Liu, C. (2014). A complete Holocene record of trematode-bivalve infection and implications for the response of parasitism to climate change. Proceedings of the National Academy of Sciences, USA 111, 18150–18155.CrossRefGoogle ScholarPubMed
Institute of Meteorology and Water Management (Instytut Meteorologii i Gospodarki Wodnej) National Research Institute of Poland (Państwowy Instytut Badawczy) (2013). Climate change and climate variability in Poland. In COP19/CMP9 United Nations Climate Change Conference, Warsaw, Poland, 11–22 November 2013.Google Scholar
Jackson, J. A., Hal, A. J., Friber, I. M., Ralli, C., Lowe, A., Zawadzka, M., Turner, A. K., Stewart, A., Birtles, R. J., Paterson, S., Bradley, J. E. and Begon, M. (2014). An immunological marker of tolerance to infection in wild rodents. PLoS Biology 12, e1001901.Google Scholar
Janova, E., Skoric, M., Heroldova, M., Tenora, F., Fictum, P. and Pavlik, I. (2010). Determinants of the prevalence of Heligmosomum costellatum (Heligmosomidae: Trichostrongyloidea) in a common vole population in southern Moravia, Czech Republic. Journal of Helminthology 84, 410–414.CrossRefGoogle Scholar
Keith, L. B., Cary, J. R., Yuill, T. M. and Keith, I. M. (1985). Prevalence of helminths in a cyclic snowshoe hare population. Journal of Wildlife Diseases 21, 233–253.CrossRefGoogle Scholar
Keymer, A. E. and Hiorns, R. W. (1986). Faecal egg counts and nematode fecundity: Heligmosomoides polygyrus and laboratory mice. Parasitology 93, 189–203.Google Scholar
Kinsella, J. M. (1974). Comparison of helminth parasites of the cotton rat, Sigmodon hispidus, from several habitats in Florida. American Museum Novitates 2540, 1–11.Google Scholar
Kirschenblatt, N. I. (1938). Die Gesetzmaessigkeiten der Dynamik der Parasitenfauna bei den maeuseaehnlichen Nagetieren (Muriden) in Transkaukasien . Dissertation. University of Leningrad, pp. 5–92 (In Russian, with a German Summary).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 Bialowieża 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). III. Structure of the helminth groupings in C. glareolus populations of various forest biocoenoses in Poland. Acta Parasitologica Polonica 18, 163–176.Google Scholar
Kloch, A., Babik, W., Bajer, A., Siński, E. and Radwan, J. (2010). Effects of an MHC-DRB genotype and allele number on the load of gut parasites in the bank vole Myodes glareolus . Molecular Ecology 19, 255–265.Google Scholar
Knowles, S. C. L., Fenton, A., Petchey, O. L., Jones, T. R., Barber, R. and Pedersen, A. B. (2013). Stability of within-host-parasite communities in a wild mammal system. Proceedings of the Royal Society B 280, 20130598.Google Scholar
Krasnov, B. R., Mouillot, D., Shenbrot, G. I., Khokhlova, I. S., Vinarski, M. V., Korallo-Vinarskaya, N. P. and Poulin, R. (2010). Similarity in ectoparasite faunas of Palaearctic rodents as a function of host phylogenetic, geographic or environmental distances: which matters the most? International Journal for Parasitology 40, 807–817.Google Scholar
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.Google Scholar
Levecke, B., Behnke, J. M., Ajjampur, S. S. R., Albonico, M., Ame, S. M., Charlier, J., Geiger, S. M., Hoa, N. T. V., Kamwa Ngassam, R. I., Kotze, A. C., McCarthy, J. S., Montresor, A., Periago, M. V., Roy, S., Tchuem Tchuente, L.-A., Thach, D. T. C. and Vercruysse, J. (2011). A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and kato-katz thick smear methods for soil-transmitted helminths. PLoS Neglected Tropical Diseases 5, e1201.CrossRefGoogle ScholarPubMed
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, 287–312.Google Scholar
Lewis, J. W. and D'Silva, J. (1980). Rhythmic egg deposition by the oxyurid nematode Syphacia muris in the rat. Journal of Zoology, London 191, 429–433.Google Scholar
Lewis, J. W. and D'Silva, J. (1986). The life-cycle of Syphacia muris Yamaguti (Nematoda: Oxyuroidea) in the laboratory rat. Journal of Helminthology 60, 39–46.Google Scholar
Liu, B., Bu, Y. and Zhang, L. (2012). A new species of Aspiculuris Schulz, 1924 (Nematoda, Heteroxynematidae) from the gray-sided vole, Clethrionomys rufocanus (Rodentia, Cricetidae), from Tianjin, China. Acta Parasitologica 57, 311–315.Google Scholar
Martin, J. L. and Huffman, D. G. (1980). An analysis of the community and population dynamics of the helminths of Sigmodon hispidus (Rodentia: Cricetidae) from three central Texas vegetational regions. Proceedings of the Helminthological Society of Washington 47, 247–255.Google Scholar
Michalska, B. (2011). Tendencies of air temperature changes in Poland. Prace i Studia Geograficzne 47, 67–75.Google Scholar
Milazzo, C., Casanova, J. C., Aloise, G., Ribas, A. and Cagnin, M. (2003). Helminths of the bank vole Clethrionomys glareolus (Rodentia, Arvicolinae) in southern Italy. Italian Journal of Zoology 70, 333–337.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.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, 78–90.CrossRefGoogle ScholarPubMed
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.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, 225–242.Google Scholar
Moravec, F. (1982). Proposal of a new systematic arrangement of nematodes of the family Capillariidae. Folia Parasitologica 29, 119–132.Google Scholar
Moravec, F. (2000). Review of capillariid and trichosomoidid nematodes from mammals in the Czech Republic and the Slovak Republic. Acta Societatis Zoologicae Bohemicae 64, 271–304.Google Scholar
Nadleśnictwo Pisz (2014). Monitoring Stanu Lasu. Nadleśnictwo Pisz, Lasy Państwowe, Poland. http://www.pisz.bialystok.lasy.gov.pl/documents/62733/22275741/monitoring+stanu+lasu+24-03-2014.pdf.Google Scholar
Nakao, M., Lavikainen, A., Iwaki, T., Haukisalmi, V., Konyaev, S., Oku, Y., Okamoto, M. and Ito, A. (2013). Molecular phylogeny of the genus Taenia (Cestoda: Taeniidae): proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria . International Journal for Parasitology 43, 427–437.Google Scholar
O'Sullivan, H. M., Smal, C. M. and Fairley, J. S. (1984). A study of parasitic infestations in populations of small rodents (Apodemus sylvaticus and Clethrionomys glareolus) on Ross Island, Killarney. Journal of Life Sciences of the Royal Dublin Society 5, 29–42.Google Scholar
Paziewska, A., Harris, P. D., Zwolińska, L., Bajer, A. and Siński, E. (2012). Differences in the ecology of Bartonella infections of Apodemus flavicollis and Myodes glareolus in a boreal forest. Parasitology 139, 881–893.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.Google Scholar
Quinnell, R. J. (1992). The population dynamics of Heligmosomoides polygyrus in an enclosure population of wood mice. Journal of Animal Ecology 61, 669–679.Google Scholar
Rausch, R. and Tiner, J. D. (1949). Studies on the parasitic helminths of the North Central States. II. Helminths of voles (Microtus spp.). Preliminary report. American Midland Naturalist 41, 665–694.Google Scholar
Ribas, S. A., Guivier, E., Xuéreb, A., Chaval, Y., Cadet, P., Poulle, M.-L., Sironen, T., Voutilainen, L., Henttonen, H., Cosson, J.-F. and Charbonnel, N. (2011). Concomitant influence of helminth infection and landscape on the distribution of Puumala hantavirus in its reservoir, Myodes glareolus . BMC Microbiology 11, 30.Google Scholar
Rohlf, F. J. and Sokal, R. R. (1995). Statistical Tables. Freeman W.H. and Company, San Francisco.Google Scholar
Scott, M. E. and Gibbs, H. C. (1986). Long-term population dynamics of pinworms (Syphacia obvelata and Aspiculuris tetraptera) in mice. Journal of Parasitology 72, 652–662.CrossRefGoogle ScholarPubMed
Simões, R., Gentile, R., Rademaker, V., D'Andrea, P., Herrera, H., Freitas, T., Lanfredi, R. and Maldonado, A. Jr. (2010). Variation in the helminth community structure of Thrichomys pachyurus (Rodentia: Echimyidae) in two sub-regions of the Brazilian Pantanal: the effects of land use and seasonality. Journal of Helminthology 84, 266–275.Google Scholar
Tenora, F. and Stanĕk, 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
Tenora, F. and Zejda, J. (1974). The helminth synusy of Clethrionomys glareolus in a lowland forest and its changes. Acta Scientiarum Naturalium – Academiae Scientiarum Bohemoslovacae, Brno 6, 1–48.Google Scholar
Tenora, F., Wiger, R. and Barus, V. (1979). Seasonal and annual variations in the prevalence of helminths in a cyclic population of Clethrionomys glareolus . Holarctic Ecology 2, 176–181.Google Scholar
Tesakov, A. S., Lebedev, V. S., Bannikova, A. A. and Abramson, N. I. (2010). Clethrionomys Tilesius, 1850 is the valid generic name for red-backed voles and Myodes Pallas, 1811 is a junior synonym of Lemmus Link, 1795. Russian Journal of Theriology 9, 83–86.Google Scholar
Xu, R. (2003). Measuring explained variation in linear mixed effects models. Statistics in Medicine 22, 3527–3541.Google Scholar
Zajączkowski, G., Jabłoński, M., Jabłoński, T., Małecka, M., Kowalska, A., Małachowska, J. and Piwnicki, J. (2014). Raport o stanie lasów w Polsce 2013. Centrum Informacyjne Lasów Państwowych, Warszawa, Poland.Google Scholar