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Long-term trends in helminth infections of wood mice (Apodemus sylvaticus) from the vicinity of Malham Tarn in North Yorkshire, England

Published online by Cambridge University Press:  01 December 2020

Jerzy M. Behnke Open the ORCID record for Jerzy M. Behnke [Opens in a new window] ,
Michael T. Rogan ,
Philip S. Craig ,
Joseph A. Jackson  and
Geoff Hide Open the ORCID record for Geoff Hide [Opens in a new window]
Jerzy M. Behnke*
Affiliation:
School of Life Sciences, University of Nottingham, University Park, NottinghamNG7 2RD, UK
Michael T. Rogan
Affiliation:
Biomedical Research Centre, School of Science, Engineering and Environment, University of Salford, SalfordM5 4WT, UK
Philip S. Craig
Affiliation:
Biomedical Research Centre, School of Science, Engineering and Environment, University of Salford, SalfordM5 4WT, UK
Joseph A. Jackson
Affiliation:
Biomedical Research Centre, School of Science, Engineering and Environment, University of Salford, SalfordM5 4WT, UK
Geoff Hide
Affiliation:
Biomedical Research Centre, School of Science, Engineering and Environment, University of Salford, SalfordM5 4WT, UK
*
Author for correspondence: Jerzy M. Behnke, E-mail: [email protected]
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Abstract

Helminth infections in wood mice (n = 483), trapped over a period of 26 years in the woods surrounding Malham Tarn in North Yorkshire, were analysed. Although 10 species of helminths were identified, the overall mean species richness was 1.01 species/mouse indicating that the helminth community was relatively depauperate in this wood mouse population. The dominant species was Heligmosomoides polygyrus, the prevalence (64.6%) and abundance (10.4 worms/mouse) of which declined significantly over the study period. Because of the dominance of this species, analyses of higher taxa (combined helminths and combined nematodes) also revealed significantly declining values for prevalence, although not abundance. Helminth species richness (HSR) and Brillouin's index of diversity (BID) did not show covariance with year, neither did those remaining species whose overall prevalence exceeded 5% (Syphacia stroma, Aonchotheca murissylvatici and Plagiorchis muris). Significant age effects were detected for the prevalence and abundance of all higher taxa, H. polygyrus and P. muris, and for HSR and BID, reflecting the accumulation of helminths with increasing host age. Only two cases of sex bias were found; male bias in abundance of P. muris and combined Digenea. We discuss the significance of these results and hypothesize about the underlying causes.

Keywords

AbundanceagecestodesDigeneaHeligmosomoides polygyrushelminthsnematodesPlagiorchis murisprevalencesexSyphacia stroma
Type
Research Article
Information
Parasitology , Volume 148 , Issue 4 , April 2021 , pp. 451 - 463
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Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Abu-Madi, MA, Behnke, JM, Lewis, JW and Gilbert, FS (1998) Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 72, 93–100.CrossRefGoogle Scholar
Abu-Madi, MA, Behnke, JM, Lewis, JW and Gilbert, FS (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
Altizer, S, Ostfeld, RS, Johnson, PTJ, Kutz, S and Harvell, CD (2013) Climate change and infectious diseases: from evidence to a predictive framework. Science (New York, N.Y.) 341, 514–519.CrossRefGoogle ScholarPubMed
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
Asakawa, M and Tenora, F (1996) A checklist of epidemiology of nematode parasites of the genus Apodemus (Murinae: Rodentia) throughout the world excluding Japan. Journal of the Rakuno Gakuen University 20, 181–213.Google Scholar
Babayan, SA, Liu, W, Hamilton, G, Kilbride, E, Rynkiewicz, EC, Clerc, M and Pedersen, AB (2018) The immune and non-immune pathways that drive chronic gastrointestinal helminth burdens in the wild. Frontiers in Immunology 9, 56.CrossRefGoogle ScholarPubMed
Bajer, A, Behnke, JM, Pawełczyk, A, Kulis, K, Sereda, MJ 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
Behnke, JM, Barnard, CJ and Wakelin, D (1992) Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology 22, 861–907.CrossRefGoogle ScholarPubMed
Behnke, JM, Lewis, JW, Mohd Zain, SN and Gilbert, FS (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.CrossRefGoogle ScholarPubMed
Behnke, JM, Barnard, CJ, Bajer, A, Bray, D, Dinmore, J, Frake, K, Osmond, J, Race, T and Sinski, 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, JM, Bajer, A, Harris, PD, Newington, L, Pidgeon, E, Rowlands, G, Sheriff, C, Kuliś-Malkowska, K, Siński, E, Gilbert, FS and Barnard, C (2008a) 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.CrossRefGoogle Scholar
Behnke, JM, Bajer, A, Harris, PD, Newington, L, Pidgeon, E, Rowlands, G, Sheriff, C, Kuliś-Malkowska, K, Siński, E, Gilbert, FS and Barnard, CJ (2008b) Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from N.E. Poland. 2. The infracommunity level. Parasitology 135, 999–1018.CrossRefGoogle Scholar
Behnke, JM, Eira, C, Rogan, M, Gilbert, FS, Torres, J, Miquel, J and Lewis, JW (2009) Helminth species richness in wild wood mice, Apodemus sylvaticus, is enhanced by the presence of the intestinal nematode Heligmosomoides polygyrus. Parasitology 136, 793–804.CrossRefGoogle ScholarPubMed
Behnke, JM, Bajer, A, Behnke-Borowczyk, J, Clisham, N, Gilbert, FS, Glover, A, Jeffery, L, Kirk, J, Mierzejewska, EJ, Mills, SC, Mohallal, EME, Padget, O, Wainer, R and Zalat, S (2019) Long-term spatiotemporal stability and dynamic changes in helminth infracommunities of spiny mice (Acomys dimidiatus) in St. Katherine's Protectorate, Sinai, Egypt. Parasitology 146, 50–73.CrossRefGoogle Scholar
Bordes, F, Ponlet, N, de Bellocq, JG, Ribas, A, Krasnov, BR 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.CrossRefGoogle ScholarPubMed
Boyce, K (2013) Transmission Ecology of Gastrointestinal Trematodes of Small Mammals, Malham Tarn (PhD thesis). University of Salford, UK.Google Scholar
Boyce, K, Hide, G, Craig, PS, Harris, PD, Reynolds, C, Pickles, A and Rogan, MT (2012) Identification of a new species of digenean Notocotylus malhamensis n. sp. (Digenea: Notocotylidae) from the bank vole (Myodes glareolus) and the field vole (Microtus agrestis). Parasitology 139, 1630–1639.CrossRefGoogle Scholar
Boyce, K, Hide, G, Craig, PS, Reynolds, C, Hussain, M, Bodell, AJ, Bradshaw, H, Pickles, A and Rogan, MT (2014) A molecular and ecological analysis of the trematode Plagiorchis elegans in the wood mouse Apodemus sylvaticus from a periaquatic ecosystem in the UK. Journal of Helminthology 88, 310–320.CrossRefGoogle ScholarPubMed
Brooks, DR and Hoberg, EP (2007) How will global climate change affect parasite-host assemblages? Trends in Parasitology 23, 571–574.CrossRefGoogle ScholarPubMed
Čabrilo, B, Jovanović, VM, Bjelić Čabrilo, O, Budinski, I, Blagojević, J and Vujošević, M (2018) Is there a host sex bias in intestinal nematode parasitism of the yellow-necked mouse (Apodemus Fl avicollis) at Obedska Bara pond, Serbia? Helminthologia 55, 247–250.CrossRefGoogle Scholar
Carlson, CJ, Burgio, KR, Dougherty, ER, Phillips, AJ, Bueno, VM, Clements, CF, Castaldo, G, Dallas, TA, Cizauskas, CA, Cumming, GS, Doña, J, Harris, NC, Jovani, R, Mironov, S, Muellerklein, OC, Proctor, H and Getz, WM (2017) Parasite biodiversity faces extinction and redistribution in a changing climate. Science Advances 3, e1602422.CrossRefGoogle Scholar
Diamond, JM (1975) The island dilemma: lessons of modern biogeographic studies for the design of natural reserves. Biological Conservation 7, 129–146.CrossRefGoogle 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, JM (1977) Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates. Cumbria, UK: Freshwater Biological Association.Google Scholar
Elton, C, Ford, EB, Baker, JR and Gardiner, AD (1931) The health and parasites of a wild mouse population. Proceedings of the Zoological Society of London 1931, 657–721.Google Scholar
Feliu, C, Renaud, F, Catzeflis, F, Hugot, J-P, Durand, P and Morand, S (1997) A comparative analysis of parasite species richness of Iberian rodents. Parasitology 115, 453–466.CrossRefGoogle ScholarPubMed
Ferrari, N, Cattadori, IM, Nespereira, J, Rizzoli, A and Hudson, PJ (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
Friberg, IM, Little, S, Ralli, C, Lowe, A, Hall, A, Jackson, JA and Bradley, JE (2013) Macroparasites at peripheral sites of infection are major and dynamic modifiers of systemic antimicrobial pattern recognition responses. Molecular Ecology 22, 2810–2826.CrossRefGoogle ScholarPubMed
Gehman, A-LM, Hall, RJ and Byers, JE (2018) Host and parasite thermal ecology jointly determine the effect of climate warming on epidemic dynamics. Proceedings of the National Academy of Sciences of the United States of America 115, 744–749.CrossRefGoogle ScholarPubMed
Gethings, OJ, Rose, H, Mitchell, S, Van Dijk, J and Morgan, ER (2015) Asynchrony in host and parasite phenology may decrease disease risk in livestock under climate warming: Nematodirus battus in lambs as a case study. Parasitology 142, 1306–1317.CrossRefGoogle ScholarPubMed
Gregory, RD (1992) On the interpretation of host-parasite ecology: Heligmosomoides polygyrus (Nematoda) in wild wood mouse (Apodemus sylvaticus) populations. Journal of Zoology, London 226, 109–121.CrossRefGoogle Scholar
Gregory, RD, Montgomery, SSJ and Montgomery, WI (1992) Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749–757.CrossRefGoogle Scholar
Grzybek, M, Bajer, A, Bednarska, M, Alsarraf, M, Behnke-Borowczyk, J, Harris, PD, Price, S, Brown, GS, Osborne, S-J, Siński, E and Behnke, JM (2015a) Long-term spatiotemporal stability and dynamic changes in helminth infracommunities of bank voles (Myodes glareolus) in NE Poland. Parasitology 142, 1722–1743.CrossRefGoogle Scholar
Grzybek, M, Bajer, A, Behnke-Borowczyk, J, Alsarraf, M and Behnke, JM (2015b) Female host sex-biased parasitism with the rodent stomach nematode Mastophorus muris in wild bank voles (Myodes glareolus). Parasitology Research 114, 523–533.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 ScholarPubMed
Haukisalmi, V and Henttonen, H (1993) Population dynamics of Taenia polyacantha metacestodes in the bank vole Clethrionomys glareolus. Annales Zoologici Fennici 30, 81–84.Google Scholar
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 (1988) Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807–825.CrossRefGoogle Scholar
Hominick, WM and Aston, AJ (1981) Association between Pelodera strongyloides (Nematoda: Rhabditidae) and wood mice, Apodemus sylvaticus. Parasitology 83, 67–75.CrossRefGoogle ScholarPubMed
Houghton, J (2009) Global Warming: The Complete Briefing, 4th Edn. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Hudson, PJ, Cattadori, IM, Boag, B and Doson, AP (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
Jackson, JA, Friberg, IM, Bolch, L, Lowe, A, Ralli, C, Harris, PD, Behnke, JM and Bradley, JE (2009) Immunomodulatory parasites and toll-like receptor-mediated tumour necrosis factor alpha responsiveness in wild mammals. BMC Biology 7, 16.CrossRefGoogle ScholarPubMed
Jackson, JA, Hall, AJ, Friberg, IM, Ralli, C, Lowe, A, Zawadzka, M, Turner, AK, Stewart, A, Birtles, RJ, Paterson, S, Bradley, JE and Begon, M (2014) An immunological marker of tolerance to infection in wild rodents. PLoS Biology 12, e1001901.CrossRefGoogle ScholarPubMed
Jackson, JA, Friberg, IM, Hablützel, PI, Masud, N, Stewart, A, Synnott, R and Cable, J (2020) Partitioning the environmental drivers of immunocompetence. Science of the Total Environment 747, 141152.CrossRefGoogle ScholarPubMed
Kisielewska, K (1970) 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 (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
Knowles, SCL, Fenton, A, Petchey, OL, Jones, TR, Barber, R and Pedersen, AB (2015) Stability of within-host-parasite communities in a wild mammal system. Proceedings of the Royal Society B 280, 20130598.CrossRefGoogle Scholar
Langley, R and Fairley, JS (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, JW (1968) Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology, London 154, 287–312.CrossRefGoogle Scholar
Lewis, JW and Twigg, GI (1972) A study of the internal parasites of small rodents from woodland areas in Surrey. Journal of Zoology (London) 166, 61–77.CrossRefGoogle Scholar
Loxton, KC, Lawton, C, Stafford, P and Holland, CV (2016) Reduced helminth parasitism in the introduced bank vole (Myodes glareolus); more parasites lost than gained. International Journal for Parasitology: Parasites and Wildlife 5, 175–183.Google ScholarPubMed
Loxton, KC, Lawton, C, Stafford, P and Holland, CV (2017) Parasite dynamics in an invaded ecosystem: helminth communities of native wood mice are impacted by the invasive bank vole. Parasitology 144, 1476–1489.CrossRefGoogle Scholar
Luong, LT, Perkins, SE, Grear, DA, Rizzoli, A and Hudson, PJ (2010) The relative importance of host characteristics and co-infection in generating variation in Heligmosomoides polygyrus fecundity. Parasitology 137, 1003–1012.CrossRefGoogle ScholarPubMed
Maizels, RM, Balic, A, Gomez-Escobar, N, Nair, M, Taylor, MD and Allen, JE (2004) Helminth parasites-masters of regulation. Immunological Reviews 201, 89–116.CrossRefGoogle Scholar
Margolis, L, Esch, GW, Holmes, JC, Kuris, AM and Schad, GA (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
Mas-Coma, S, Esteban, JG, Fuentes, MV, Bargues, MD, Valero, M and Galan-Puchades, MT (1998) Helminth parasites of small mammals (insectivores and rodents) on the Pityusic Island of Formentera (Baleartic Archipelago). Research and Reviews in Parasitology 58, 125–133.Google Scholar
Mayr, E (1959) Isolation as an evolutionary factor. Proceedings of the American Philosophical Society 103, 221–230.Google Scholar
Milazzo, C, Aloise, G, Cagnin, M, Di Bella, C, Geraci, F, Feliu, C and Casanova, JC (2005) Helminths of Apodemus sylvaticus (Muridae) distributed on the Southern European border (Italian Peninsula). Vie et Milieu 55, 45–51.Google Scholar
Montgomery, SSJ and Montgomery, WI (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, SSJ and Montgomery, WI (1989) Spatial and temporal variation in the infracommunity structure of helminths of Apodemus sylvaticus (Rodentia: Muridae). Parasitology 98, 145–150.CrossRefGoogle Scholar
Montgomery, SSJ and Montgomery, WI (1990) Structure, stability and species interactions in helminth communities of wood mice Apodemus sylvaticus. International Journal for Parasitology 20, 225–242.CrossRefGoogle ScholarPubMed
Moore, SL and Wilson, K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science (New York, N.Y.) 297, 2015–2018.CrossRefGoogle ScholarPubMed
Moravec, F (2000) Review of capillariid & trichosomoidid nematodes from mammals in the Czech Republic and the Slovak Republic. Acta Societatis Zoologicae Bohemicae 64, 271–304.Google Scholar
Moravec, F, Prokopic, P and Shilkas, AV (1987) The biology of nematodes of the family Capillariidae Neveu-Lemaire, 1936. Folia Parasitologica 34, 39–56.Google ScholarPubMed
Muller-Graf, CDM, Durand, P, Feliu, C, Hugot, J-P, O'Callighan, CJO, Renaud, F, Santalla, F and Morand, S (1999) Epidemiological and genetic variability of two species of nematodes (Heligmosomoides polygyrus and Syphacia stroma) of Apodemus spp. Parasitology 118, 425–432.CrossRefGoogle ScholarPubMed
Murúa, RE (1978) Studies on the ecology of parasites of Apodemus sylvaticus (L.) and Clethrionomys glareolus (Schreb.) (Rodentia): analysis of the parasite populations and their seasonal variation in the Bristol area. Acta Parasitologica Polonica 25, 149–161.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.CrossRefGoogle ScholarPubMed
Orr, HA (2005) The genetic basis of reproductive isolation: insights from Drosophila. Proceedings of the National Academy of Sciences of the United States of America 102, 6522–6526.CrossRefGoogle ScholarPubMed
O'Sullivan, HM, Smal, CM and Fairley, JS (1984) A study of parasitic infestations in populations of small rodents (Apodemus sylvaticus and Clethrionomys glareolus) on Ross Island, Killarney. Journal Life Sciences Royal Dublin Society 5, 29–42.Google Scholar
Pisanu, B, Chapuis, J-L, Durette-Desset, M-C and Morand, S (2002) Epizootiology of Syphacia obvelata from a domestic mouse population on sub-Antarctic Kerguelen Archipelago. Journal of Parasitology 88, 645–649.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 of Ecology and Systematics 28, 341–358.CrossRefGoogle Scholar
Rogan, MT, Craig, PS, Hide, G, Heath, S, Pickles, A and Storey, DM (2007) The occurrence of the trematode Plagiorchis muris in the wood mouse Apodemus sylvaticus in North Yorkshire, UK. Journal of Helminthology 81, 57–62.CrossRefGoogle ScholarPubMed
Rohlf, FJ and Sokal, RR (1995) Statistical Tables. San Francisco: Freeman W.H. and Company.Google Scholar
Ryan, S and Holland, C (1996) The intestinal helminth community of wild woodmice Apodemus sylvaticus in County Wicklow. Proceedings of the Royal Irish Academy 96B, 45–48.Google Scholar
Sanchez, A, Devevey, G and Bize, P (2011) Female-biased infection and transmission of the gastrointestinal nematode Trichuris arvicolae infecting the common vole, Microtus arvalis. International Journal for Parasitology 41, 1397–1402.CrossRefGoogle ScholarPubMed
Schalk, G and Forbes, MR (1997) Male biases in parasitism of mammals: effects of study type, host age and parasite taxa. Oikos 78, 67–74.CrossRefGoogle Scholar
Sharpe, GI (1964) The helminth parasites of some small mammal communities. I. The parasites and their hosts. Parasitology 54, 145–154.CrossRefGoogle ScholarPubMed
Stewart, A, Hablützel, PI, Brown, M, Watson, HV, Parker-Norman, S, Tober, AV, Thomason, AG, Friberg, IM, Cable, J and Jackson, JA (2018 a) Half the story: thermal effects on within-host infectious disease progression in a warming climate. Global Change Biology 24, 371–386.CrossRefGoogle Scholar
Stewart, A, Lowe, A, Smales, L, Bajer, A, Bradley, J, Dwużnik, D, Franssen, F, Griffith, J, Stuart, P, Turner, C, Zaleśny, G and Behnke, JM (2018 b) Parasitic nematodes of the genus Syphacia Seurat, 1916 infecting Muridae in the British Isles, and the peculiar case of Syphacia frederici. Parasitology 145, 269–280.CrossRefGoogle ScholarPubMed
Stuart, P, Paredis, L, Henttonen, H, Lawton, C, Ochoa Torres, CA and Holland, CV (2020) The hidden faces of a biological invasion: parasite dynamics of invaders and natives. International Journal for Parasitology 50, 111–123.CrossRefGoogle ScholarPubMed
Tenora, F (2004) Corrections in the taxonomic position of the helminth-fauna of Apodemus spp. (Rodentia) in the Czech Republic. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 52, 7–14.CrossRefGoogle Scholar
Tenora, F and Staněk, M (1994) Changes of the helminthofauna in several Muridae and Arvicolidae at Lednice in Moravia. I. Systematics and taxonomy. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 42, 237–247.Google Scholar
Tenora, F and Zavadil, R (1967) A contribution to the evaluation of capillariid nematodes found in rodents in Czechoslovakia. Acta Universitatis Agriculturae 15, 357–368.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
Thomas, RJ (1953) On the nematodes and trematode parasites of some small mammals from the Inner Hebrides. Journal of Helminthology 28, 143–168.CrossRefGoogle Scholar
World Meteorological Organization (2019) WMO Statement on the State of the Global Climate in 2018. WMO-No. 1233. Geneva. ISBN 978-92-63-11233-0.Google Scholar
Xu, R (2003) Measuring explained variation in linear mixed effects models. Statistics in Medicine 22, 3527–3541.CrossRefGoogle ScholarPubMed
Zuk, M and McKean, KA (1996) Sex differences in parasitic infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.CrossRefGoogle ScholarPubMed
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