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Factors affecting the component community structure of haemoparasites in common voles ( Microtus arvalis) from the Mazury Lake District region of Poland

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Abstract

The prevalence and abundance of infections with haemoparasites were studied over a 4-year period in Microtus arvalis (common vole, n =321) sampled from fallow grassland sites in north-eastern Poland. Total species richness was five (prevalence= Haemobartonella sp. 63.9%, Bartonella spp. 27.7%, Babesia microti 9.0%, Trypanosoma sp. 8.4% and and Hepatozoon lavieri 3.1%) with 76.9% of the voles carrying at least one species and a mean infracommunity species richness of 1.1. Variation in species richness was determined primarily by season and year, the interaction of these factors, and that of year with host age. The observed frequency distribution of infracommunity species richness did not differ from that predicted by a null model, suggesting that there were no marked associations between the species. Analyses of prevalence and abundance of infection with each species in turn, revealed that overall the principal causes of variation were temporal and seasonal, their interaction, and interactions with intrinsic factors (age and sex), the latter playing only a minor role in their own right. However, the relative importance of these combinations varied and was distinct for each of the species in the study. Prevalence data revealed eight sets of two- and three-way associations between species, mostly dependent to some extent on one of the intrinsic and extrinsic factors in the model. Analysis of quantitative associations suggested two sets of positive two-way interactions, none of which remained after controlling for the effect of extrinsic and intrinsic factors on the abundance of each species. These data are discussed in the context of the changing ecological profiles in this region of Eastern Europe and, in a wider context, in relation to current understanding of the factors that shape component community structures of haemoparasites in wild rodents.

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References

  • Adamczewska-Andrzejewska KD (1973) The lens weight as indicator of age in the wild Microtus arvalis populations. Bull Acad Pol Sci Cl 2 21:331–336

    Google Scholar 

  • Aeschliemann A, Burgdorfer W, Matile H, Peter O, Wyler R (1979) Aspects nouveaux du role de vecteur joue par Ixodes ricinus L. en Suisse. Acta Trop 36:181–191

    PubMed  Google Scholar 

  • Albright JW, Albright JF (1991) Rodent trypanosomes: their conflict with the immune system of the host. Parasitol Today 7:137–140

    Article  Google Scholar 

  • Anderson BE, Neuman MA (1997) Bartonella spp. as emerging human pathogens. Clin Microbiol Rev 10:203–219

    CAS  PubMed  Google Scholar 

  • Bajer A (2002) Gryzonie różnych siedlisk jako źródło zarażeń Cryptosporidium: biologiczna i molekularna charakterystyka izolatów. PhD thesis. Department of Parasitology, University of Warszawa, Warszawa

  • Bajer A, Pawełczyk A, Behnke JM. Gilbert FS, Siński E (2001) Factors affecting the component community structure of haemoparasites in bank voles ( Clethrionomys glareolus) from the Mazury lake district region of Poland. Parasitology 122:43–54

    Article  PubMed  Google Scholar 

  • Bajer A, Bednarska M, Pawelczyk A, Behnke JM, Gilbert FS, Sinski E (2002) Prevalence and abundance of Cryptosporidium parvum and Giardia spp. in wild rural rodents from the Mazury Lake District region of Poland. Parasitology 125:21–34

    Article  CAS  PubMed  Google Scholar 

  • Baker JR (1974) Protozoan parasites of the blood of British wild birds and mammals. J Zool 172:169–190

    Google Scholar 

  • Baker JR, Chitty D, Phipps E (1963) Blood parasites of wild voles, Microtus agrestis , in England. Parasitology 53:297–301

    Google Scholar 

  • Balashov JS (1995) The interrelationship of Ixodid ticks ( Ixodidae) with the causative agents of transmissible vertebrate infections. Parazitologiia 29:337–352

    PubMed  Google Scholar 

  • Behnke JM, Lewis JW, Mohd Zain SN, Gilbert FS (1999) Helminth infections in Apodemus sylvaticus in southern England:interactive effects of host-age, sex and year on prevalence and abundance of infections. J Helminthol 73:31–44

    CAS  PubMed  Google Scholar 

  • Birtles RJ, Harrison TG, Molyneux DH (1994) Grahamella in small woodland mammals in the U.K.:isolation, prevalence and host specificity. Ann Trop Med Parasitol 88:317–327

    CAS  PubMed  Google Scholar 

  • Birtles RJ, Harrison TG, Saunders NA, Molyneux DH (1995) Proposal to unify the genera Grahamella and Bartonella, with descriptions of Bartonella talpae comb. nov., and three new species, Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and Bartonella doshiae sp. nov. Int J Syst Bacteriol 45:1–8

    CAS  PubMed  Google Scholar 

  • Crawley MT (1993) GLIM for ecologists. Blackwell, Oxford

  • Dash KM, Hall E, Barger IA (1988) The role of arithmetic and geometric mean worm egg counts in faecal egg count reduction tests and in monitoring strategic drenching programs in sheep. Aust Vet J 65:66–68

    CAS  Google Scholar 

  • Elliott JM (1977) Some methods for the statistical analysis of samples of benthic invertebrates. Freshwater Biological Association, Cumbria, UK

  • Franca C (1912) Sur la classification des piroplasmes et description de deux formes de ces parasites. Arq Inst Bacteriol Camara Pestana Lisbon 3:11–18

    Google Scholar 

  • Gothe R, Kreier JP (1977) Aegyptianella, Eperythrozoon and Haemobartonella. In: Kreier JP (ed) Parasitic protozoa, vol IV. Academic Press, New York, pp 251–294

  • Grunwaldt E (1977) Babesiosis on Shelter Island. NY State J Med 8:1320–1321

    Google Scholar 

  • Healing TD (1981) Infections with blood parasites in small British rodents Apodemus sylvaticus, Clethrionomys glareolus and Microtus agrestis. Parasitology 83:179–189

    CAS  PubMed  Google Scholar 

  • Hoyte HMD (1954) Grahamella (Rickettsiales) in the common shrew Sorex araneus. Parasitology 46:224–234

    Google Scholar 

  • Humiczewska M, Kuzna-Grygiel W (1997) Przypadek importowanej ludzkiej babesiozy w Polsce. Wiad Parazytol 43:227–229

    CAS  PubMed  Google Scholar 

  • Janovy J Jr, Clopton RE, Clopton DA, Snyder SD, Eftin A, Krebs L (1995) Species density distributions as null models for ecologically significant interactions of parasite species in an assemblage. Ecol Model 77:189–196

    Article  Google Scholar 

  • Karbowiak G, Sinski E (1996a) The finding of Babesia microti in bank vole Clethrionomys glareolus in the district of Mazury Lakes (Poland). Acta Parasitol 41:50–51

    Google Scholar 

  • Karbowiak G, Sinski E (1996b) Occurrence and morphological characteristics of a Trypanosma evotomys strain from North Poland. Acta Parasitol 41:105–107

    Google Scholar 

  • Karbowiak G, Wita I (2000) Rola krwiopijnych stawonogów jako przenosicieli niepatogenicznych swidrowców z rodzaju Trypanosoma, grupy Stercoraria, w Europie. In: Buczek A, Blaszak C (eds) Stawonogi pasozytnicze i alergogenne. KGM, Lublin, pp 151–169

  • Karbowiak G, Stanko M, Rychlik L, Nowakowski W, Siuda K (1999) The new data about zoonotic reservoir of Babesia microti in small mammals in Poland. Acta Parasitol 44:142–144

    Google Scholar 

  • Karbowiak G, Wita I, Czaplinska U (2002) Protozoan parasites in the blood of the social vole ( Microtus socialis) in Askania Nova reserve, Ukraine. Proceedings of the 12th Conference of the Ukraine Scientific Society for Parasitology (UNTP). UNTP, Kijev, p 131

  • Krampitz HE (1962) Weitere intersuchungen an Grahamella, Brumpt, 1911. Z Tropmed Parasitol 13:34–53

    CAS  Google Scholar 

  • Krampitz HE (1964) Uber das Vorkommen und Verhalten von Haemococcidien der Gattung Hepatozoon, Miller 1908 (Protozoa, Adeleida) in mittel- und sudeuropaischen Saugern. Acta Trop 21:114–154

    CAS  PubMed  Google Scholar 

  • Krampitz HE (1981) Development of Hepatozoon erhardovae Krampitz, 1964 (Protozoa:Haemogregarinidae) in experimental mammalian and arthropod hosts. II. Sexual development in fleas and sporozoite indices in xenodiagnosis. J Trop Med Hyg 75:155–157

    CAS  Google Scholar 

  • Krampitz HE, Haberkorn A (1988) Experimental treatment of Hepatozoon infections with anticoccidial agent toltrazuril. J Vet Med B 35:131–137

    CAS  Google Scholar 

  • Krampitz HE, Kleinschmidt A (1960) Grahamella Brumpt 1911. Biologische und morphologische untersuchungen. Z Tropenmed Parasitol 11:336–352

    CAS  PubMed  Google Scholar 

  • Krampitz HE, Buschmann H, Münchhoff P (1986) Gibt es latente Babesien-infektionen beim Menschen in Süddeutschland? Mitt Oesterr Gese Tropenmed Parasitol 8:233–243

    Google Scholar 

  • Laakkonen J, Sukura A, Oksanen A, Henttonen H, Soveri T (2001) Haemogregarines of the genus Hepatozoon (Apicomplexa:Adeleina) in rodents from northern Europe. Folia Parasitol (Prague) 48:263–267

    Google Scholar 

  • Laakkonen J, Henttonen H, Hastriter MW, Niemimaa J, Jarrell GH (2002) Hemoparasites and fleas of shrews and rodents from Alaska. Acta Parasitol 47:254–257

    Google Scholar 

  • Mahnert V (1972) Grahamella und Sporozoa als Blutparasiten alpiner Kleinsauger. Acta Trop 29:88–100

    CAS  PubMed  Google Scholar 

  • Margolis L, Esch GW, Holmes JC, Kuris AM, Schad GA (1982) The use of ecological terms in parasitology (report of an ad hoc committee of The American Society of Parasitologists). J Parasitol 68:131–133

    Google Scholar 

  • Molyneux DH (1969) The morphology and biology of Trypanosoma (Herpetosoma) evotomys of the bank-vole, Clethrionomys glareolus. Parasitology 59:843–857

    CAS  PubMed  Google Scholar 

  • Morris P (1972) A review of mammalian age determination methods. Mammal Rev 2:69–104

    Google Scholar 

  • Neimark H, Johansson K-E, Rikihisa Y, Tully JG (2001) Proposal to transfer members of the genera Haemobartonella and Eperythrozoon to the genus Mycoplasma with descriptions of Candidatus Mycoplasma haemofelis, Candidatus Mycoplasma haemomuris, Candidatus Mycoplasma haemosuis and Candidatus Mycoplasma wenyonii. Int J Syst Evol Microbiol 51:891–899

    CAS  PubMed  Google Scholar 

  • Neimark H, Barnaud A, Gounon,P, Michel JC, Contamin H (2002) The putative haemobartonella that influences Plasmodium falciparum parasitaemia in squirrel monkeys is a haemotrophic mycoplasma. Microbes Infect 4:693–698

    Article  CAS  PubMed  Google Scholar 

  • Noyes HA, Ambrose P, Barker F, Begon M, Bennet M, Bown KJ, Kemp SJ (2002) Host specificity of Trypanosoma ( Herpetosoma) species:evidence that bank voles ( Clethrionomys glareolus) carry only one T.( H.) evotomys 18S rRNA genotype but wood mice ( Apodemus sylvaticus) carry at least two polyphyletic parasites. Parasitology 124:185–190

    Article  CAS  PubMed  Google Scholar 

  • Parry MF, Fox M, Burka SA, Richar WJ (1977) Babesia microti infection in man. J Am Med Assoc 238:1282–1283

    Article  CAS  Google Scholar 

  • Pawelczyk A (2003) Rola dziko zyjacych gryzoni w utrzymywaniu w przyrodzie zrodel infekcji Borrelia burgdorferi sensu lato. PhD thesis. Department of Parasitology, University of Warszawa, Warszawa

  • Pawełczyk A, Siński E (2000) Prevalence of IgG antibodies response to Borrelia burgdorferi s.l. in populations of wild rodents from Mazury Lakes District, Poland. Ann Agric Environ Med 7:79–83

    PubMed  Google Scholar 

  • Poulin R (1993) The disparity between observed and uniform distributions: a new look at parasite aggregation. Int J Parasitol 23:937–944

    CAS  PubMed  Google Scholar 

  • Rogozinska M (1997) Sukcesja w zgrupowaniu drobnych ssaków ugorowanego pola uprawnego. Stan w 4 lata po rozpoczęciu ugorowania. (Changes in the population structures of small mammals on fallow fields, previously cultivated. Appraisal 4 years after the cessation of cultivation.) MSc thesis. Department of Ecology, University of Warszawa, Warszawa

  • Sebek Z (1978) Blood parasites of small mammals in Western Hungary. Parasitol Hung 11:17–21

    Google Scholar 

  • Sebek Z, Rosicky B, Sixl W (1977) The occurrence of babesiasis affecting small terrestrial mammals and the importance of this zoonosis in Europe. Folia Parasitol (Prague) 24:221–228

    Google Scholar 

  • Sebek Z, Sixl W, Stunzner D, Valova M, Hubalek Z, Troger H (1980) Zur Kenntnis der Blutparasiten wildlebender Kleinsauger in der Steiermark und im Burgenland. Folia Parasitol (Prague) 27:295–301

    Google Scholar 

  • Sinski E, Pawelczyk A (1999) Detection of reservoirs for Lyme borreliosis in the Mazury Lake district, Poland. Zentralbl Bakteriol 289:689–703

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, San Francisco, Calif.

  • Stanko M, Miklisova D (2002) Infestation trends of two rodent species (Rodentia, Muridae) on the East Slovakian Lowland. In:Buczek A, Błaszak C (eds) Stawonogi w medycynie. Wydawnictwo Drukarnia LIBER, Lublin, pp 105–114

  • Steketee RW, Eckman MR, Burgess EC, Kuritsky JN, Dickerson J, Schell WD, Godsey MS, Davis JD (1985) Babesiosis in Wisconsin:a new focus of disease transmission. J Am Med Assoc 253:2675–2678

    Article  CAS  Google Scholar 

  • Turner CMR (1986) Seasonal and age distributions of Babesia, Hepatozoon , Trypanosoma and Grahamella species in Clethrionomys glareolus and Apodemus sylvaticus populations. Parasitology 93:279–289

    PubMed  Google Scholar 

  • Turner CMR, Cox FEG (1985) Interspecific interactions between blood parasites in a wild rodent community. Ann Trop Med Parasitol 79:463–465

    CAS  PubMed  Google Scholar 

  • Tyzzer EE (1942) A comparative study of Grahamella, Haemobartonella and Eperythrozoa in small mammals. Proc Am Philos Soc 85:359–398

    Google Scholar 

  • Tyzzer EE, Weinman D (1939) Haemobartonella n.g. ( Bartonella olim. pro parte). H. microti n. sp. of the field vole. Am J Hyg 30:141–157

    Google Scholar 

  • Walter G, Liebisch A (1980) Studies of the ecology of some blood Protozoa of mammals in north Germany. Acta Trop 37:31–40

    CAS  PubMed  Google Scholar 

  • Watkins RA, Moshier SE, O’Dell WD, Pinter AJ (1991) Splenomegaly and reticulocytosis caused by Babesia microti infections in natural populations of the montane vole, Microtus montanus. J Protozool 38:573–576

    CAS  PubMed  Google Scholar 

  • Wiger R (1979) Seasonal and annual variations in the prevalence of blood parasites in cyclic species of small rodents in Norway with special reference to Clethrionomys glareolus. Holarct Ecol 2:169–175

    Google Scholar 

  • Wilson K, Grenfell BT (1997) Generalized linear modelling for parasitologists. Parasitol Today 13:33–38

    Article  Google Scholar 

  • Weinman D (1944) Infectious anaemia due to Bartonella and related red cell parasites. Trans Am Philos Soc 33:243–350

    Google Scholar 

  • Young A (1970) Studies on the blood parasites of small mammmals with special reference to piroplasms. PhD thesis. University of London, London

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Acknowledgements

We are grateful to the British Council UK, to the former State Committee for Scientific Research (KBN) Poland (KBN grants UM 855 and UM 930), and to the Ministry of Scientific Research and Information Technology (British-Polish Young Scientist Programme, 2003) for financial support for this study. We wish also to express our gratitude to Prof. Dr Hab. M. Kozakiewicz, Dr R. Halba and Mr. G. Gorecki for the use of, and hospitality at, the field station in Urwitalt.

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Authors and Affiliations

  1. Department of Parasitology, Institute of Zoology, University of Warszawa, Miecznikowa 1 Street, 02–096, Warszawa, Poland

    A. Pawelczyk, A. Bajer & E. Sinski

  2. School of Biology, University Park, University of Nottingham, Nottingham, NG7 2RD, UK

    J. M. Behnke & F. S. Gilbert

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  1. A. Pawelczyk
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  2. A. Bajer
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  3. J. M. Behnke
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  5. E. Sinski
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Correspondence to J. M. Behnke.

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Pawelczyk, A., Bajer, A., Behnke, J.M. et al. Factors affecting the component community structure of haemoparasites in common voles ( Microtus arvalis) from the Mazury Lake District region of Poland. Parasitol Res 92, 270–284 (2004). https://doi.org/10.1007/s00436-003-1040-1

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