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Diversity of nematodes in the yellow-necked field mouse Apodemus flavicollis from the Peripannonic region of Serbia

Published online by Cambridge University Press:  02 October 2014

B. Čabrilo ,
V.M. Jovanović ,
O. Bjelić-Čabrilo ,
I. Budinski ,
J. Blagojević  and
M. Vujošević
B. Čabrilo*
Affiliation:
Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Trg Dositeja Obradovića 2, 21000Novi Sad, Serbia Institute for Biological Research ‘Siniša Stanković’, University of Belgrade, Blvd. despota Stefana 142, 11060Belgrade, Serbia
V.M. Jovanović
Affiliation:
Institute for Biological Research ‘Siniša Stanković’, University of Belgrade, Blvd. despota Stefana 142, 11060Belgrade, Serbia
O. Bjelić-Čabrilo
Affiliation:
Department of Biology and Ecology, Faculty of Sciences, University of Novi Sad, Trg Dositeja Obradovića 2, 21000Novi Sad, Serbia
I. Budinski
Affiliation:
Institute for Biological Research ‘Siniša Stanković’, University of Belgrade, Blvd. despota Stefana 142, 11060Belgrade, Serbia
J. Blagojević
Affiliation:
Institute for Biological Research ‘Siniša Stanković’, University of Belgrade, Blvd. despota Stefana 142, 11060Belgrade, Serbia
M. Vujošević
Affiliation:
Institute for Biological Research ‘Siniša Stanković’, University of Belgrade, Blvd. despota Stefana 142, 11060Belgrade, Serbia
*
* E-mail: borislav.cabrilo@dbe.uns.ac.rs
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Abstract

Up to six nematode species were identified from 86 specimens of the yellow-necked field mouse Apodemus flavicollis from three mountainous localities known as Avala, Cer and Liškovac in Serbia. The highest prevalence of infection of 97% was recorded from Mt. Avala. Only one nematode species, Syphacia frederici, occurred in all three localities. There was complete overlap in nematode species from Mts. Avala and Liškovac, whereas the taxonomic distinctness of Mt. Cer was seen in the presence of the insect-transmitted species Rictularia proni. Locality was a statistically significant factor in all the best-fitted generalized linear models of variation in abundances. The highest level of both species richness and parasite alpha diversity (Shannon's H= 1.47) was found in the easternmost Mt. Liškovac, whereas the diversity indices were lowest for the westernmost Mt. Cer (Shannon's H= 0.48). In view of this geographical difference, the beta diversity indices were calculated along a west to east longitudinal gradient.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 1 , January 2016 , pp. 14 - 20
Copyright
Copyright © Cambridge University Press 2014 

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References

Abt, K.F. & Bock, W.F. (1998) Seasonal variations of diet composition in farmland field mice (Apodemus spp.) and bank voles (Clethrionomys glareolus). Acta Theriologica 43, 379–389.CrossRefGoogle Scholar
Adnadević, T., Bugarski-Stanojević, V., Blagojević, J., Stamenković, G. & Vujošević, M. (2012) Genetic differentiation in populations of the yellow-necked field mouse, Apodemus flavicollis, harbouring B chromosomes in different frequencies. Population Ecology 54, 537–548.CrossRefGoogle Scholar
Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.CrossRefGoogle Scholar
Anderson, R.C. (2000) Nematode parasites of vertebrates: their development and transmission. 2nd edn.Oxon, UK, CABI Publishing.CrossRefGoogle Scholar
Barnard, C.J., Kulis, K., Behnke, J.M., Bajer, A., Gromadzka-Ostrowska, J., Stachon, M. & Sinski, E. (2003) Local variation in helminth burdens of bank voles (Clehtrionomys glareolus) from ecologically similar sites: temporal stability and relationships with hormone concentrations and social behaviour. Journal of Helminthology 77, 185–195.CrossRefGoogle ScholarPubMed
Behnke, J.M., Lewis, J.W., Mohd Zain, S.N. & Gilbert, F.S. (1999) Helminth infections in Apodemus flavicollis 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 Scholar
Behnke, J.M., Barnard, C.J., Bajer, A., Bray, D., Dinmore, J., Frake, K., Osmond, J., Race, T. & Sinski, E. (2001) Variation in the helminth community structure in bank voles (Clethryonomys glareolus) from three comparable localities in the Mazury Lake District Region of Poland. Parasitology 123, 401–414.CrossRefGoogle Scholar
Behnke, J.M., Bajer, A., Harris, P.D., Newington, L., Pidgeon, E., Rowlands, G., Sheriff, C., Kulis-Malkowska, K., Sinski, E., Gilbert, F.S. & Barnard, C.J. (2008a) Temporal and between-site variation in helminth communities of the bank vole (Myodes glareolus) from N.E. Poland. 1. Regional fauna and component community levels. Parasitology 135, 985–997.CrossRefGoogle ScholarPubMed
Behnke, J.M., Bajer, A., Harris, P.D., Newington, L., Pidgeon, E., Rowlands, G., Sheriff, C., Kulis-Malkowska, K., Sinski, E., Gilbert, F.S. & Barnard, C.J. (2008b) Temporal and between-site variation in helminth communities of the bank vole (Myodes glareolus) from N.E. Poland. 2. The infracommunity level. Parasitology 135, 999–1018.CrossRefGoogle ScholarPubMed
Bjelić-Čabrilo, O., Popović, E., Kostić, D. & Šimić, S. (2009) Nematofauna of bank vole – Clethrionomys glareolus (Schreber, 1780) – from Mt. Fruška gora (Serbia). Archives of Biological Science 61, 555–561.CrossRefGoogle Scholar
Bjelić-Čabrilo, O., Kostić, D., Popović, E., Ćirković, M., Aleksić, N. & Lujić, J. (2011) Helminth fauna of the bank vole Myodes glareolus (Rodentia, Arvicolinae) on the territory of Fruska gora mountain (Serbia) – a potential source of zoonoses. Bulgarian Journal of Agricultural Science 17, 829–836.Google Scholar
Bordes, F., Morand, S., Krasnov, B.R. & Poulin, R. (2010) Parasite diversity and latitudinal gradients in terrestrial mammals. pp. 89–98in Morand, S. & Krasnov, B.R. (Eds) The biogeography of host–parasite interactions. New York, USA, Oxford University Press Inc.Google Scholar
Burnham, K.P. & Overton, W.S. (1978) Estimation of the size of a closed population when capture probabilities vary among animals. Biometrika 65, 623–633.CrossRefGoogle Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Ćirović, D., Pavlović, I., Kulišić, Z., Ivetić, V., Penezić, A. & Ćosić, N. (2012) Echinococcus multilocularis in the European beaver (Castor fibre L.) from Serbia: first report. Veterinary Record 171, 100.CrossRefGoogle ScholarPubMed
Colwell, R.K. (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9 and earlier. User's guide and application. Available athttp://purl.oclc.org/estimates (accessed accessed 17 January 2014).Google Scholar
Dobson, A.J. (1990) An introduction to generalized linear models. London, Chapman & Hall.CrossRefGoogle Scholar
European Environmental Agency. (2003) Biological diversity. pp. 230–249in Europe's environment: The third assessment. Copenhagen, Denmark, European Environmental Agency.Google Scholar
Feliu, C., Renaud, F., Catzeflis, F., Hugot, J.-P., Durand, P. & Morand, S. (1997) A comparative analysis of parasite species richness of Iberian rodents. Parasitology 115, 453–466.CrossRefGoogle ScholarPubMed
Ferrari, N. (2005) Macroparasite transmission and dynamics in Apodemus flavicollis. PhD thesis, University of Stirling, Scotland, UK.Google Scholar
Ferrari, N., Cattadori, I.M., Nespereira, J., Rizzoli, A. & Hudson, P.J. (2004) The role of host sex on parasite dynamics: field experiments on the yellow-necked mouse (Apodemus flavicollis). Ecology Letters 7, 88–94.CrossRefGoogle Scholar
Genov, T. (1984) Helminths of insectivorous mammals and rodents in Bulgaria. Sofia, Publishing house of the Bulgarian Academy of Sciences (in Bulgarian).Google Scholar
Grear, D.A., Luong, L.T. & Hudson, P.J. (2012) Sex-biased transmission of a complex life-cycle parasite: why males matter. Oikos 121, 1446–1453.CrossRefGoogle Scholar
Grikieniene, J. (2005) Investigations into endoparasites of small mammals in the environs of lake Drukšiai. Acta Zoologica Lituanica 15, 109–114.CrossRefGoogle Scholar
Guégan, J.F., Morand, S. & Poulin, R. (2005) Are there general laws in parasite community ecology? The emergence of spatial parasitology and epidemiology. pp. 22–42in Thomas, F., Renaud, F. & Guegan, J.F. (Eds) Parasitism and ecosystems. New York, USA, Oxford University Press Inc.CrossRefGoogle Scholar
Habijan-Mikeš, V. (1990) Nematode vrste Apodemus flavicollis Melch. sa Fruške Gore. Magister Thesis, Faculty of Science, University of Novi Sad, Novi Sad (in Serbian).Google Scholar
Hammer, O., Harper, D.A.T. & Ryan, P.D. (2001) PAST: Paleontological Statistics software package for education and data analysis. Palaeontologia Electronica 4, 1–9.Google Scholar
Harrison, A., Scantlebury, M. & Montgomery, W.I. (2010) Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 119, 1099–1104.CrossRefGoogle Scholar
Heltsche, J. & Forrester, N.E. (1983) Estimating species richness using the jackknife procedure. Biometrics 39, 1–11.CrossRefGoogle Scholar
Kark, S., Allnutt, T.F., Levin, N., Manne, L.L. & Williams, P.H. (2007) The role of transitional areas as avian biodiversity centres. Global Ecology and Biogeography 16, 187–196.CrossRefGoogle Scholar
Kataranovski, D.S., Vukićević-Radić, O.D., Kataranovski, M.V., Radović, D.L. & Mirkov, I.I. (2008) Helminth fauna of Mus musculus Linnaeus 1758 from the suburban area of Belgrade, Serbia. Archives of Biological Science Belgrade 60, 609–617.CrossRefGoogle Scholar
Krasnov, B.R., Morand, S., Hawlena, H., Khokhlova, I.S. & Shenbrot, S.I. (2005) Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146, 209–217.CrossRefGoogle ScholarPubMed
Krasnov, B.R., Poulin, R. & Morand, S. (2006) Patterns of macroparasite diversity in small mammals. pp. 197–231in Morand, S., Krasnov, B.R. & Poulin, R. (Eds) Micromammals and macroparasites: From evolutionary ecology to management. Tokyo, Japan, Springer-Verlag.CrossRefGoogle Scholar
Krasnov, B.R., Bordes, F., Khokhlova, I.S. & Morand, S. (2012) Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia 76, 1–13.CrossRefGoogle Scholar
Magura, T., Tóthmérész, B. & Molnár, T. (2001) Forest edge and diversity: carabids along forest-grassland transects. Biodiversity and Conservation 10, 287–300.CrossRefGoogle Scholar
Magurran, A.E. (2004) Measuring biological diversity. London, Blackwell Science.Google Scholar
Marović, M., Đoković, I., Pešić, L., Radovanović, S., Toljić, M. & Gerzina, N. (2002) Neotectonics and seismicity of the southern margin of the Pannonian basin in Serbia. EGU Stephan Mueller Special Publication Series 3, 1–19.CrossRefGoogle Scholar
Marsh, A.C.W. & Harris, S. (2000) Partitioning of woodland habitat resources by two sympatric species of Apodemus: lessons for the conservation of the yellow-necked mouse (A. flavicollis) in Britain. Biological Conservation 92, 275–283.CrossRefGoogle Scholar
Mažeika, V., Pailauskas, A. & Balčiauskas, L. (2003) New data on the helminth fauna of rodents of Lithuania. Acta Zoologica Lituanica 13, 41–47.CrossRefGoogle Scholar
Mészáros, F. & Murai, É. (1979) Contribution to the knowledge of helminths of rodents in Roumania. Parasitologia Hungarica 12, 55–70.Google Scholar
Mészáros, F., Habijan, V. & Mikes, M. (1983) Parasitic nematodes of rodents in Vojvodina (Yugoslavia). Parasitologia Hungarica 16, 103–110.Google Scholar
Milazzo, C., Di Bella, C., Casanova, J.C., Ribas, A. & Cagnin, M. (2010) Helminth communities of wood mouse (Apodemus sylvaticus) on the river Avena (Calabria, Southern Italy). Hystrix – The Italian Journal of Mammalogy 21, 171–176.Google Scholar
Nabaglo, L. & Pachinger, K. (1979) Eye lens weight as an age indicator in yellow-necked mice. Acta Theriologica 24, 119–122.CrossRefGoogle Scholar
Ondríková, J., Miklisová, D., Ribas, A. & Stanko, M. (2010) The helminth parasites of two sympatric species of the genus Apodemus (Rodentia, Muridae) from south-eastern Slovakia. Acta Parasitologica 55, 369–378.CrossRefGoogle Scholar
Petrov, B.M. (1992) Mammals of Yugoslavia: insectivores and rodents. Belgrade, Serbia, Natural History Museum in Belgrade.Google Scholar
Poulin, R. (1998) Comparison of three estimators of species richness in parasite component communities. Journal of Parasitology 84, 485–490.CrossRefGoogle ScholarPubMed
Poulin, R. (2001) Interactions between species and the structure of helminth communities. Parasitology 122 (Suppl.), S3–S11.CrossRefGoogle ScholarPubMed
Prokopic, J. & Mahnert, V. (1970) On the helminthofauna of small mammals (Insectivore, Rodentia) in Tirol (Austria). Berichte des naturwissenschaftlich-medizinischen Vereins in Innsbruck 58, 143–154.Google Scholar
R Core Team (2014) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available athttp://www.R-project.org/ (accessed accessed 1 May 2014).Google Scholar
Reiczigel, J. (2003) Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine 22, 611–621.CrossRefGoogle ScholarPubMed
Reiczigel, J., Abonyi-Tóth, Z. & Singer, J. (2008) An exact confidence set for two binomial proportions and exact unconditional confidence intervals for the difference and ratio of proportions. Computational Statistics and Data Analysis 52, 5046–5053.CrossRefGoogle Scholar
Risser, P.G. (1995) The status of the science examining ecotones. BioScience 45, 318–325.CrossRefGoogle Scholar
Rózsa, L., Reiczigel, J. & Majoros, G. (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232.CrossRefGoogle ScholarPubMed
Ryžikov, K.M. (1978) Key to rodent helminth fauna of the USSR. Tapeworms and flukes. USSR, Izdatelstvo ‘Nauka’ (in Russian).Google Scholar
Ryžikov, K.M. (1979) Key to rodent helminth fauna of the USSR. Roundworms and acanthocephalans. USSR, Izdatelstvo ‘Nauka’ (in Russian).Google Scholar
Tóthmérész, B. (1995) Comparison of different methods for diversity ordering. Journal of Vegetation Science 6, 283–290.CrossRefGoogle Scholar
Van Rensburg, B.J., Hugo, S., Levin, N. & Kark, S. (2013) Are environmental transitions more prone to biological invasions? Diversity and Distributions 19, 341–351.CrossRefGoogle Scholar
Venables, W.N. & Ripley, B.D. (2002) Modern Applied Statistics with S. 4th edn.New York, Springer.CrossRefGoogle Scholar
Wilson, M.V. & Shmida, A. (1984) Measuring beta diversity with presence–absence data. Journal of Ecology 72, 1055–1064.CrossRefGoogle Scholar