Acta Parasitologica

, Volume 55, Issue 4, pp 369–378 | Cite as

The helminth parasites of two sympatric species of the genus Apodemus (Rodentia, Muridae) from south-eastern Slovakia

  • Jarmila Ondríková
  • Dana Miklisová
  • Alexis Ribas
  • Michal Stanko
Article

Abstract

The helminths of two sympatric species of rodents, the striped field mouse Apodemus agrarius and the yellow-necked mouse, Apodemus flavicollis from Slovakia were studied to determine whether there are similarities in the composition of the helminth fauna of two closely related host species living in the same area. A total of twelve species of helminths were identified in these rodent populations, including Brachylaima sp. (Trematoda); Hymenolepis diminuta (Rudolphi, 1819), Mesocestoides sp. larvae, Rodentolepis fraterna (Stiles, 1906), Rodentolepis straminea (Goeze, 1782), Skrjabinotaenia lobata (Baer, 1925), Taenia taeniaeformis larvae (Batsch, 1786) (Cestoda); Aonchotheca annulosa (Dujardin, 1845), Heligmosomoides polygyrus (Dujardin, 1845), Heterakis spumosa Schneider, 1866, Mastophorus muris (Gmelin, 1790) and Syphacia stroma (Linstow, 1884) (Nematoda). In A. agrarius, H. polygyrus was the most prevalent, as well as the most abundant helminth, but R. fraterna was the species with the highest mean intensity. In contrast, S. stroma dominated the A. flavicollis helminth fauna with the highest prevalence, mean abundance and mean intensity. Both rodent populations harboured nine helminth species, although the mean individual species richness was significantly higher in A. agrarius than in A. flavicollis. The analysis of helminth diversity at both component and infracommunity levels revealed differences between the two rodent populations, which are most likely attributable to the specific host ecology.

Keywords

Helminth community Apodemus agrarius Apodemus flavicollis Rodentia Muridae south-eastern Slovakia 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abu-Madi M.A., Behnke J.M., Lewis J.W., Gilbert F.S. 1998. Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in southeast England. Journal of Helminthology, 72, 93–100. DOI: 10.1017/S0022149X00016254.CrossRefGoogle Scholar
  2. Abu-Madi M.A., Behnke J.M., Lewis J.W., 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, 7–15. DOI: 10.1017/S0022149X00000020.PubMedGoogle Scholar
  3. Babinska-Werka J., Gliwicz J., Goszczynski J. 1981. Demographic processes in a urban population of the striped mouse. Acta Theriologica, 26, 275–283.Google Scholar
  4. 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. 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, 985–997. DOI: 10.1017/S0031182008004393.PubMedGoogle Scholar
  5. 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 (Clethrionomys glareolus) from three comparable localities in the Mazury Lake District region of Poland. Parasitology, 123, 401–414. DOI: 10.1017/S0031182001008605.CrossRefPubMedGoogle Scholar
  6. Behnke J.M., Lewis J.W., Mohd Zain S.N., Gilbert F.S. 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. DOI: 10.1017/S0022149X99000049.PubMedGoogle Scholar
  7. Bergstedt B. 1966. Home ranges and movements of the rodent species Clethrionomys glareolus (Schreber), Apodemus flavicollis (Melchior) and Apodemus sylvaticus (Linné) in southern Sweden. Oikos, 17, 150–157.CrossRefGoogle Scholar
  8. Bordes F., Morand S., Kelt D.A., Van Vuren D.H. 2009. Home range and parasite diversity in mammals. American Naturalist, 173, 467–474. DOI: 10.1086/597227.CrossRefPubMedGoogle Scholar
  9. Brown E.D., MacDonald D.W., Tew T.E., Todd I.A. 1994. Apodemus sylvaticus infected with Heligmosomoides polygyrus (Nematoda) in an arable ecosystem: epidemiology and effects of infection on the movement of male mice. Journal of Zoology, 234, 623–640. DOI: 10.1111/j.1469-7998.1994.tb04869.x.CrossRefGoogle Scholar
  10. Bryja J., Rehák Z. 2002. Další doklady součansné expanze areálu myšice temnopásé (Apodemus agrarius) na Moravě. Lynx, 33, 69–77.Google Scholar
  11. 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. DOI: 10.2307/3284227.CrossRefPubMedGoogle Scholar
  12. Corbet G., Ovenden D. 1980. The Mammals of Britain and Europe. William Collins Sons and Co., Ltd, Glasgow, 253 pp.Google Scholar
  13. Cislakova L., Stanko M., Fricova J., Mosansky L., Travnicek M., Halanova M., Mardzinova S., Stefancikova A. 2004. Small mammals (Insectivora, Rodentia) as a potential source of chlamydial infection in East Slovakia. Annals of Agricultural and Environmental Medicine, 11, 139–143.PubMedGoogle Scholar
  14. Craig P., Ito A. 2007. Intestinal cestodes. Current Opinion in Infectious Diseases, 20, 524–532. DOI: 10.1097/QCO.0b013e3282ef579e.CrossRefPubMedGoogle Scholar
  15. Eira C., Torres J., Vingada J., 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. DOI: 10.2478/s11686-006-0046-0.CrossRefGoogle Scholar
  16. Erhardova B. 1956. Parazitičti červi našich myšovitých hlodavců II. Československá Parasitologie, 3, 49–66.Google Scholar
  17. Erhardova B. 1958. Parazitičti červi hlodavců ČSSR. Československá Parasitologie, 5(1), 27–103.Google Scholar
  18. Erhardova B., Rysavy B. 1955. Přípěvek k poznání cizopasních červů našich myši a hrabošů. Zoologické a Entomologické Listy, 4, 71–83.Google Scholar
  19. Filippucci M.G., Macholan M., Michaux J.R. 2002. Genetic variation and evolution in the genus Apodemus (Muridae: Rodentia). Biological Journal of the Linnean Society, 75, 395–419. DOI: 10.1046/j.1095-8312.2002.00032.x.CrossRefGoogle Scholar
  20. Fuentes M.V., Sáez S., Trelis M., Galán-Puchades M.T., Esteban J.G. 2004. The helminth community of the wood mouse, Apodemus sylvaticus, in the Sierra Espuña, Murcia, Spain. Journal of Helminthology, 78, 219–223. DOI: 10.1079/JOH2003226.CrossRefPubMedGoogle Scholar
  21. Fuentes M.V., Sainz-Elipe S., Galán-Puchades M.T. 2007. Ecological study of the wood mouse helminth community in a burned Mediterranean ecosystem in regeneration five years after a wildfire. Acta Parasitologica, 52, 403–413. DOI: 10.2478/s11686-007-0056-6.CrossRefGoogle Scholar
  22. Gliwicz J., Kryštufek B. 1999. Apodemus agrarius (Pallas, 1771). In: (Eds. A. Mitchell-Jones, G. Amori, W. Bogdanowicz, B. Kryštufek, P.J.H. Reinders, F. Spitzenberger, M. Stubbe, J.B.M. Thissen, V. Vohralík and J. Zima) The atlas of European Mammals. Academic Press, London, 266–267.Google Scholar
  23. Goüy de Bellocq J., Sarà M., Casanova J.C., Feliu C., Morand S. 2003. A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitology Research, 90, 64–70. DOI: 10.1007/s00436-002-0806-1.Google Scholar
  24. Hildebrand J., Zalesny G., Okulewicz A., Baszkiewicz K. 2009. Preliminary studies on the zoonotic importance of rodents as a reservoir of toxocariasis from recreation grounds in Wroclaw (Poland). Helminthologia, 46, 80–84. DOI: 10.2478/s11687-009-0016-9.CrossRefGoogle Scholar
  25. Horvath G., Trocsanyi B. 1998. Home range size of Apodemus agrarius and small mammal population dynamics in the rodent assemblage of a Querco-robori-carpinetum forest habitat. Tiscia, 31, 63–69.Google Scholar
  26. Holisova V. 1967. The food of Apodemus agrarius (Pall.). Zoologické Listy, 16, 1–14.Google Scholar
  27. Klempa B., Stanko M., Labuda M., Ulrich R., Meisel H., Krüger D.H. 2005. Central European Dobrava Hantavirus isolate from striped field mouse (Apodemus agrarius). Journal of Clinical Microbiology, 43, 2756–2763. DOI: 10.1128/JCM.43.6.2756-2763.2005.CrossRefPubMedGoogle Scholar
  28. Klimpel S., Förster M., Schmahl G. 2007a. Parasites of two abundant sympatric rodent species in relation to host phylogeny and ecology. Parasitology Research, 100, 867–875. DOI: 10.1007/s00436-006-0368-8.CrossRefPubMedGoogle Scholar
  29. Klimpel S., Förster M., Schmahl G. 2007b. Parasite fauna of the bank vole (Clethrionomys glareolus) in an urban region of Germany: reservoir host of zoonotic metazoan parasites? Parasitology Research, 102, 69–75. DOI: 10.1007/s00436-007-0725-2.CrossRefPubMedGoogle Scholar
  30. Kozakiewicz M., Gortat T., Kozakiewicz A., Barkowska M. 1999. Effects of habitat fragmentation on four rodent species in Polish farm landscape. Landscape Ecology, 14, 391–400. DOI: 10.1023/A:1008070610187.CrossRefGoogle Scholar
  31. Lefkovitch L.P. 1966. An index of spatial distribution. Researches on Population Ecology, 8, 89–92.CrossRefGoogle Scholar
  32. Magurran A.E. 1988. Ecological Diversity and Its Measurement. Croom Helm, London, 179 pp.Google Scholar
  33. Magurran A.E. 2004. Measuring Biological Diversity. Wiley-Blackwell, 256 pp.Google Scholar
  34. Marangi M., Zechini B., Fileti A., Quaranta G., Aceti A. 2003. Hymenolepis diminuta infection in a child living in the urban area of Rome, Italy. Journal of Clinical Microbiology, 41, 3994–3995. DOI: 10.1128/JCM.41.8.3994-3995.2003.CrossRefPubMedGoogle Scholar
  35. Michaux J.R., Chevret P., Filippucci M.G., Macholan M. 2002. Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Molecular Phylogenetics and Evolution, 23, 123–136. DOI: 10.1016/S1055-7903(02)00007-6.CrossRefPubMedGoogle Scholar
  36. Milazzo C., Aloise G., Cagnin M., Di Bella C., Geraci F., Feliu C., Casanova J.C. 2005. Helminths of Apodemus sylvaticus (Muridae) distributed on the southern European border (Italian peninsula). Vie et Milieu, 55, 45–51.Google Scholar
  37. Mituch J. 1975. Helmintocenózy cicavcov masívu Poľany. Záverečná správa, HELú SAV, Košice, 150 pp.Google Scholar
  38. Mituch J., Hovorka J., Hovorka I., Tenkacova I. 1987. Helminty a helmintocenózy cicavcov karpatského oblúka. Záverečná správa, HELú SAV, Košice, 145 pp.Google Scholar
  39. Montgomery W. 1985. The behaviour of Apodemus. Symposia of the Zoological Society of London, 55, 89–115.Google Scholar
  40. Mongomery W. 1999. Apodemus flavicollis (Melchior, 1834). In: (Eds. A. Mitchell-Jones, G. Amori, W. Bogdanowicz, B. Kryštufek, P.J.H. Reinders, F. Spitzenberger, M. Stubbe, J.B.M. Thissen, V. Vohralík and J. Zima) The atlas of European Mammals. Academic Press, London, 270–271.Google Scholar
  41. Montgomery S.S.J., Montgomery W.I. 1990. Structure, stability and species interactions in helminth communities of wood mice, Apodemus sylvaticus. International Journal for Parasitology, 20, 225–242. DOI: 10.1016/0020-7519(90)90105-V.CrossRefPubMedGoogle Scholar
  42. Morand S. 2000. Wormy word: comparative tests of theoretical hypotheses on parasite species richness. In: (Eds. R. Poulin, S. Morand and A. Skorping) Evolutionary biology of host parasite: theory meets reality. Elsevier Science, Amsterdam, 63–79.Google Scholar
  43. Musser G.G., Carleton M.D. 1993. Family Muridae. In: (Eds. D.E. Wilson and D.M. Reeder) Mammal Species of the World. 2nd Edition, Smithsonian Institute Press, Washington D.C. and London, 501–806.Google Scholar
  44. Obrtel R., Holisova V. 1974. Trophic niches of Apodemus flavicollis and Clethrionomys glareolus in low-land forest. Acta Scientiarum Naturalium Academiae Scientiarum Bohemicae Brno, 8, 1–37.Google Scholar
  45. Orlov V.N., Bulatova N.S., Nadjafova R.S., Kozlovsky A.I. 1996. Evolutionary classification of European wood mice of the subgenus Sylvaemus based on allozyme and chromosome data. Bonner Zoologische Beiträge, 46, 191–202.Google Scholar
  46. Pelikan J. 1965. Reproduction, population structure and elimination of males in Apodemus agrarius (Pall.). Folia Zoologica, 14, 317–332.Google Scholar
  47. Pence D.B., Eason S. 1980. Comparison of the helminth faunas of two sympatric top carnivores from rolling plains of Texas. Journal of Parasitology, 66, 115–120. DOI: 10.2307/3280601.CrossRefPubMedGoogle Scholar
  48. Poulin R. 1993. The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology, 23, 937–944. DOI: 10.1016/0020-7519(93)90060-C.CrossRefPubMedGoogle Scholar
  49. Reiczigel J., Rózsa L. 2005. Quantitative Parasitology 3.0. Budapest.Google Scholar
  50. Rózsa L., Reiczigel J., Majoros G. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology, 86, 228–232. DOI: 10.1645/0022-3395(2000)086[0238:QPISOH]2.0.C0;2.CrossRefPubMedGoogle Scholar
  51. Shimalov V.V. 2002. Helminth fauna of the striped field mouse (Apodemus agrarius Pallas 1778) in ecosystems of Belorussian Polesie transformed as a result of reclamation. Parasitology Research, 88, 1009–1010. DOI: 10.1007/s004360100437.CrossRefPubMedGoogle Scholar
  52. Stanko M. 1994. Small mammals communities of windbreaks and adjacent fields in the Eastern Slovakia lowlands. Folia Zoologica, 43, 135–143.Google Scholar
  53. Stanko M., Fricova J., Schniererova E., Mosansky L., Mardzinova S. 2004. Fauna drobnych cicavcov (Insectivora, Rodentia, Carnivora) okolia Rozhanoviec (Košická kotlina). Natura Carpatica, 45, 107–116.Google Scholar
  54. Stanko M., Krasnov B.R., Miklisova D., Morand S. 2007. Simple epidemiological model predicts the relationships between prevalence and abundance in ixodid ticks. Parasitology, 134, 59–68. DOI: 10.1017/S0031182006001296.CrossRefPubMedGoogle Scholar
  55. Stanko M., Mosansky L., Fricova J. 1996. Small mammals in fragments of Robinia pseudoacacia stands in the East Slovakian lowlands. Folia Zoologica, 45, 145–152.Google Scholar
  56. Stefancikova A., Derdakova M., Lencakova D., Ivanova R., Stanko M., Cislakova L., Petko B. 2008. Serological and molecular detection of Borrelia burgdorferi sensu lato and Anaplasmataceae in rodents. Folia Microbiologica, 53, 493–499.CrossRefPubMedGoogle Scholar
  57. Stefancikova A., Gajdos O., Macko J., Tomasovicova K. 1994. Helminth fauna of small mammals in the urban and suburban area of Košice. Biologia, 49, 147–152.Google Scholar
  58. Stradiotto A., Cagnacci F., Delahay R., Tioli S., Nieder L., Rizzoli A. 2009. Spatial organization of the yellow-necked mouse: effects of density and resource availability. Journal of Mammalogy, 90, 704–714. DOI: 10.1644/08-MAMM-A-120R1.1.CrossRefGoogle Scholar
  59. Tena D., Purez Simon M., Gimeno C., Purez Pomata M.T., Illescas S., Amondarain I., Gonzalez A., Dominguez J., Bisquert J. 1998. Human infection with Hymenolepis diminuta: Case report from Spain. Journal of Clinical Microbiology, 36, 2375–2376.PubMedGoogle Scholar
  60. Tew T.E., MacDonald D.W. 1994. Dynamics of space use and male vigour amongst wood mice, Apodemus sylvaticus, in the cereal ecosystem. Behavioral Ecology and Sociobiology, 34, 337–345. DOI: 10.1007/BF00197004.CrossRefGoogle Scholar
  61. Vukicevic-Radic O., Matic R., Kataranovski D., Stamenkovic S. 2006. Spatial organization and home range of Apodemus flavicollis and A. agrarius on Mt. Avala, Serbia. Acta Zoologica Academiae Scientiarum Hungaricae, 52, 81–96.Google Scholar
  62. Zejda J. 1967. Habitat selection in Apodemus agrarius (Pallas, 1778) (Mammalia: Muridae) on the border of the area of its distribution. Folia Zoologica, 16, 15–30.Google Scholar

Copyright information

© © Versita Warsaw and Springer-Verlag Wien 2010

Authors and Affiliations

  • Jarmila Ondríková
    • 1
  • Dana Miklisová
    • 2
  • Alexis Ribas
    • 3
  • Michal Stanko
    • 1
    • 2
  1. 1.Institute of ZoologySlovak Academy of Sciences, Division of Medical ZoologyKošiceSlovakia
  2. 2.Parasitological InstituteSlovak Academy of SciencesKošiceSlovakia
  3. 3.Department of Population Biology, Institute of Vertebrate BiologyAcademy of Sciences of the Czech RepublicKoněšínCzech Republic

Personalised recommendations