Acta Parasitologica

, Volume 57, Issue 3, pp 221–227 | Cite as

Occurrence of blood parasites and intensity of infection in Prunella modularis in the montane and subalpine zone in the Slovak Carpathians

  • Martina Haas
  • Martin Lukáň
  • Jana Kisková
  • Zuzana Hrehová
Original Paper
  • 105 Downloads

Abstract

The objective of this study was to obtain primary information on the occurrence of blood parasites and intensity of infection in the Dunnock Prunella modularis in the montane region of Slovakia. Altogether 109 birds were examined during the years 2006–2010. The occurrence of Haemoproteus sp., Leucocytozoon fringillinarum and Trypanosoma sp. was documented. Blood parasite prevalences of 45% by microscopic examination and 55% by PCR diagnostics were found. The prevalence of Leucocytozoon sp. was found to be dependent on host sex with males showing a significantly higher intensity of infection with Leucocytozoon. Adult birds showed significantly higher infection prevalence than subadults. The prevalences of both Leucocytozoon sp. and Haemoproteus sp. were significantly dependent on bird age. The intensity of infection with Haemoproteus and Leucocytozoon was positively correlated and higher intensity of infection was confirmed in adult birds then in subadults birds. The prevalence of blood parasites in our samples was significantly higher in comparison to most other studies from different countries of Europe conducted at lower altitudes, indicating that the montane zone is especially favourable for the transmission of Leucocytozoon and Haemoproteus species.

Keywords

Prunella modularis Leucocytozoon Haemoproteus blood parasites Slovakia 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ahmed F.E., Mohammed A.H. 1978. Haemoproteus columbae: course of infection, relapse and imunity to reinfection in the pigeon. Zeitschrift für Parasitenkunde, 57, 229–236. DOI: 10.1007/BF00928036.PubMedCrossRefGoogle Scholar
  2. Allander K., Bennett G.F. 1994. Prevalence and intensity of haematozoan infection in a population of Great Tits Parus major from Gotland, Sweden. Journal of Avian Biology, 25, 69–74. DOI: 10.2307/3677296.CrossRefGoogle Scholar
  3. Allander K., Bennett G.F. 1995. Retardation of breeding onset in Great Tits (Parus major) by blood parasites. Functional Ecology, 9, 677–682. DOI: 10.2307/2390160.CrossRefGoogle Scholar
  4. Appleby B.M., Anwar M.A., Petty S.J. 1999. Short-term and longterm effects of food supply on parasite burdens in tawny Owls, Strix aluco. Functional Ecology, 13, 315–321. DOI: 10.1046/j.1365-2435.1999.00319.x.CrossRefGoogle Scholar
  5. Atkinson C.T., van Riper C. 1991. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: (Eds. J.E. Loye and M. Zuk) Bird-Parasite Interactions: Ecology, Evolution and Behaviour. Oxford University Press, England, 19–48.Google Scholar
  6. Benedikt V. 2006. Krevní parazité volně Žijicích pěvců v pohnízdnim období v Podbeskydské pahorkatině. Thesis. Faculty of Veterinary Medicine and Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Czech Republic.Google Scholar
  7. Bensch S., Stjernman M., Hassequist D., Östman Ö., Hansson B., Westerdahl H., Pinheiro R.T. 2000. Host specificity in avian blood parasites: A study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London, Series B — Biological Sciences, 267, 1583–1589. DOI: 10.1098/rspb.2000.1181.CrossRefGoogle Scholar
  8. Bulanková E., Za’ovičová Z. 2006. Preimaginal stages of Diptera (excluding Chironomidae and Simuliidae) of mountain lakes, their inlets and outlets in the Tatra Mountains (Slovakia). Biologia, Bratislava, 61, (Suppl. 18), 185–190. DOI: 10.2478/s1156-006-0130-9.CrossRefGoogle Scholar
  9. Cichoñ M., Sendecka J., Gustafsson L. 2003. Age-related decline in humoral immune function in collared flycatchers. Journal of Evolutionary Biology, 16, 1205–1210. DOI: 10.1046/j.1420-9101.2003.00611.x.PubMedCrossRefGoogle Scholar
  10. Davies N.B. 1992. Dunnock Behaviour and Social Evolution. Oxford University Press, New York, pp. 272.Google Scholar
  11. Dawson R.D., Bortolotti G.R. 2000. Effects of hematozoan parasites on condition and return rates of American Kestrels. Auk, 117, 373–380.CrossRefGoogle Scholar
  12. Deviche P., Greiner E.C., Manteca X. 2001. Seasonal and Age-Related Changes in Blood Parasite Prevalence in Dark-Eyed Juncos (Junco hyemalis, Aves, Passeriformes). Journal of Experimental Zoology, 289, 456–466.PubMedCrossRefGoogle Scholar
  13. Dymowska Z., Żukowski K. 1968. Pierwotniaki krwi ptaków odłowionych na terenie Bieszczadow. Wiadomości Parazytologiczne, 14, 455–459.PubMedGoogle Scholar
  14. Dyrcz A., Wink M., Kruszewicz A., Leisler B. 2005. Male reproductive success is correlated with blood parasite levels and body condition in the promiscuous Aquatic Warbler (Acrocephalus paludicola). Auk, 122, 558–565. DOI: 10.1642/0004-8038(2005)122[0558:MRSICW]2.0.CO;2.CrossRefGoogle Scholar
  15. Feldman R.A., Freed L.A., Cann R.L. 1995. A PCR test for avian malaria in Hawaiian birds. Molecular Ecology, 4, 663–673. DOI: 10.1111/j.1365-294X.1995.tb00267.x.PubMedCrossRefGoogle Scholar
  16. Ferianc O. 1979. Vtáky Slovenska 2. Veda SAV, Bratislava, 471 pp.Google Scholar
  17. Folstad I., Karter A.J. 1992. Parasites, bright males, and the immunocompetence handicap. American Naturalist, 139, 603–622.CrossRefGoogle Scholar
  18. Garvin M.C., Greiner E.C. 2003. Epizootiology of Haemoproteus danilewskyi (Haemosporina: Haemoproteidae) in Blue Jays (Cyanocitta cristata) in southcentral Florida. Journal of Wildlife Diseases, 39, 1–9.PubMedGoogle Scholar
  19. Garvin M.C., Szell C.C., Moore F.R. 2006. Blood parasites of Nearctic-Neotropical migrant passerine birds during spring transgulf migration: impact on host body condition. Journal of Parasitology, 92, 990–996. DOI: 10.1645/GE-758R.1.PubMedCrossRefGoogle Scholar
  20. Graczyk T.K., Shaw M.L., Cranfield M.R., Beall F.B. 1994. Hematological characteristics of avian malaria cases in African blackfooted penguins (Spheniscus demersus) during the first outdoor exposure season. Journal of Parasitology, 80, 302–308.PubMedCrossRefGoogle Scholar
  21. Greiner E.C., Bennett G.F., White E.M., Coombs R.F. 1975. Distribution of the avian hematozoa of North America. Canadian Journal of Zoology, 53, 1762–1787. DOI: 10.1139/z75-211.PubMedCrossRefGoogle Scholar
  22. Griffiths R., Double M.C., Orr K., Dawson R.J.G. 1998. A DNA test to sex most birds. Molecular Ecology, 7, 1071–1075. DOI: 10.1046/j.1365-294x.1998.00389.x.PubMedCrossRefGoogle Scholar
  23. Haas M. 2011. Krvné parazity vtákov v predhniezdom období a výskyt hemopsporídií vtákov u rodu Prunella. PhD Thesis. Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic.Google Scholar
  24. Hauptmanová K., Benedikt V., Literák I. 2006. Blood Parasites in Passerine Birds in Slovakian East Carpathians. Acta Protozoologica, 45, 105–109.Google Scholar
  25. Hauptmanová K., Literák I., Bártová E. 2002. Haematology and leucocytozoonosis of great tits (Parus major L.) during winter. Acta Veterinaria (Brno), 7, 199–204.CrossRefGoogle Scholar
  26. Hellgren O., Walderstöm J., Bensch S. 2004. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium and Haemoproteus from avian blood. Journal of Parasitology, 90, 797–802.PubMedCrossRefGoogle Scholar
  27. Illéšová D., Halgoš J., Krno I. 2008. Blackfly communities (Diptera, Simuliidae) in mountain streams of the High Tatra Mts. Biologia, Bratislava, 55, 177–184. DOI: 10.1007/s10750-007-9148-4.Google Scholar
  28. Jarvi S.I., Farias M.E.M., Baker H., Freifeld H.B., Baker P.E., Van Gelder E., Massey J.G., Atkinson C.T. 2003. Detection of avian malaria (Plasmodium spp.) in native land birds of American Samoa. Conservation Genetics, 4, 629–637.CrossRefGoogle Scholar
  29. Jarvi S.I., Schultz J.J., Atkinson C.T. 2002. PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. Journal of Parasitology, 88, 153–158. DOI: 10.1645/0022-3395(2002)088 [0153:PDUTPO]2.0.CO;2.PubMedCrossRefGoogle Scholar
  30. Jurášek V., Dubinský P. (Eds.). 1993. Veterinárna parazitológia. Príroda, Bratislava, 383 pp.Google Scholar
  31. Križanauskienė A., Hellgren O., Kosarev V., Sokolov L., Bensch S., Valkiūnas G. 2006. Variation in host specificity between species of avian haemosporidian parasites: evidence from parasite morphology and cytochrome b gene sequences. Journal of Parasitology, 92, 1319–1324. DOI: 10.1645/GE-873R.1.PubMedCrossRefGoogle Scholar
  32. Kučera J. 1981a. Blood parasites of birds in Central Europe. 1. Survey of literature. The incidence in domestic birds and general remarks to the incidence in wild birds. Folia Parasitologica (Praha), 28, 13–22.Google Scholar
  33. Kučera J. 1981b. Blood parasites of birds in Central Europe. 2. Leucocytozoon. Folia Parasitologica (Praha), 28, 193–203.Google Scholar
  34. Kučera J. 1981c. Blood parasites of birds in Central Europe. 3. Plasmodium and Haemoproteus. Folia Parasitologica (Praha), 28, 303–312.Google Scholar
  35. Kučera J. 1982. Blood parasites of birds in Central Europe. 4. Trypanosoma, Atoxoplasma, microfilariae and other rare haematozoa. Folia Parasitologica (Praha), 29, 107–113.Google Scholar
  36. Lucas A.M., Jamroz C. 1961. Atlas of Avian Hematology. Agriculture Monograph 25, United States Department of Agriculture, Washington, USA, 271 pp.CrossRefGoogle Scholar
  37. Madsen V., Valkiūnas G., Iezova T.A., Mercade C., Sanchez M., Osorno J.L. 2007. Testosterone levels and gular pouch coloration in courting magnificent frigatebird (Fregata magnificens): Variation with age-class, visited status and blood parasite infection. Hormones and Behavior, 51, 156–163. DOI: 10.1016/j.yhbeh.2006.09.010.PubMedCrossRefGoogle Scholar
  38. Marzal A., Bensch S., Reviriego M., Balbontin J., de Lope F. 2008. Effects of malaria double infection in birds: one plus one is not two. Journal of Evolutionary Biology, 21, 979–987. DOI: 10.1111/j.1420-9101.2008.01545.x.PubMedCrossRefGoogle Scholar
  39. Merino S., Potti J., Fargallo J.A. 1997. Blood Parasites of Passerine Birds from Central Spain. Journal of Wildlife Diseases, 33, 638–641.PubMedGoogle Scholar
  40. Murdock C.C. 2009. Studies on the ecology of avian malaria in an Alpine ecosystem. PhD Thesis. Natural Resources and Environment, University of Michigan, USA.Google Scholar
  41. Palinauskas V., Markovets M.Y., Kosarev V.V., Efremov V.D., Sokolov L.V., Valkiūnas G. 2005. Occurrence of avian haematozoa in Ekaterinburg and Irkutsk districts of Russia. Ekologija, 4, 8–12.Google Scholar
  42. Perkins S.L., Osgood S.M., Schall J.J. 1998. Use of PCR for detection of subpatent infections in lizard malaria: Implications for epizootiology. Molecular Ecology, 7, 1587–1590. DOI: 10.1046/j.1365-294x.1998.00496.x.CrossRefGoogle Scholar
  43. Perkins S.L., Schall J.J. 2002. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology, 88, 972–978. DOI: 10.1645/0022-3395(2002)088[0972:AMPOMP]2.0.CO;2.PubMedCrossRefGoogle Scholar
  44. Peirce M.A. 1981. Distribution and host-parasite check-list of the haematozoa of birds in Western Europe. Journal of Natural History, 15, 419–458.CrossRefGoogle Scholar
  45. Peirce M.A., Mead C.J. 1976. Haematozoa of British birds I. Blood parasites of birds from Dumfries and Lincolnshire. Bulletin of British Ornithological Club, 96, 128–132.Google Scholar
  46. Peirce M.A., Mead C.J. 1977. Haematozoa of British birds II. Blood parasites of birds from Hertfordshire. Journal of Natural History, 11, 597–600.CrossRefGoogle Scholar
  47. Peirce M.A., Mead C.J. 1978. Haematozoa of British birds IV. Blood parasites of birds from Wales. Journal of Natural History, 12, 361–363.CrossRefGoogle Scholar
  48. Phalen D.N., Taylor C., Phalen S.W., Bennett G.F. 1995. Hemograms and hematozoa of Sharp-shinned (Accipiter striatus) and Cooper’s hawks (Accipiter cooperii) captured during spring migration in northern New York. Journal of Wildlife Diseases, 31, 216–222.PubMedGoogle Scholar
  49. R.Development.Core.Team. 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0.Google Scholar
  50. Ricklefs R.E., Fallon S.M. 2002. Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London B, Biology Sciences, 269, 885–892. DOI: 10.1098/rspb.2001.1940.CrossRefGoogle Scholar
  51. Rintamäki P.T., Huhta E., Jokimäki J., Squires-Parsons D. 1999. Leucocytozoonosis and trypanosomiasis in redstarts in Finland. Journal of Wildlife Diseases, 35, 603–607.PubMedGoogle Scholar
  52. Rintamäki P.T., Ojanen M., Pakkala H., Tynjälä A. 1998. Blood parasites of migrating Willow Warblers (Phylloscopus trochilus) at a stopover site. Canadian Journal of Zoology, 76, 984–988. DOI: 10.1139/z98-027.Google Scholar
  53. Scheuerlein A., Ricklefs R.E. 2004. Prevalence of blood parasites in European passerine birds. Proceedings of the Royal Society of London B, Biology Sciences, 271, 1363–1370. DOI: 10.1098/rspb.2004.2726.CrossRefGoogle Scholar
  54. Shurulinkov P., Golemansky V. 2003. Plasmodium and Leucocytozoon (Sporozoa: Haemosporida) of wild birds in Bulgaria. Acta Protozoologica, 42, 205–214.Google Scholar
  55. Svobodová M., Votýpka J. 1998. Výskyt krevních prvoků u dravců (Falconiformes). Buteo, 10, 51–56.Google Scholar
  56. Valkiūnas G. 2005. Avian Malaria Parasites and Other Haemosporidia. CRC Press, Boca Raton, Florida, 946 pp.Google Scholar
  57. Waldenström J., Bensch S., Kiboi S., Hasselquist D., Ottosson U. 2002. Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology, 11, 1545–1554. DOI: 10.1046/j.1365-294X.2002.01523.x.PubMedCrossRefGoogle Scholar
  58. Zuk M., McKean K.A. 1996. Sex differences in parasitic infections: patterns and processes. International Journal for Parasitology, 26, 1009–1024.PubMedGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Wien 2012

Authors and Affiliations

  • Martina Haas
    • 1
  • Martin Lukáň
    • 1
  • Jana Kisková
    • 1
  • Zuzana Hrehová
    • 1
  1. 1.Institute of the High Mountain BiologyUniversity of ŽilinaŽilinaSlovakia

Personalised recommendations