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Differences in the ecology of Bartonella infections of Apodemus flavicollis and Myodes glareolus in a boreal forest

Published online by Cambridge University Press:  16 February 2012

A. PAZIEWSKA ,
P. D. HARRIS ,
L. ZWOLIŃSKA ,
A. BAJER  and
E. SIŃSKI
A. PAZIEWSKA*
Affiliation:
National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172, Blindern, Oslo, Norway Department of Parasitology, Institute of Zoology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland
P. D. HARRIS
Affiliation:
National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172, Blindern, Oslo, Norway
L. ZWOLIŃSKA
Affiliation:
Department of Pathomorphology, Central Clinical Hospital of the Ministry of the Interior and Administration, Wołoska 137, 02–507 Warsaw, Poland
A. BAJER
Affiliation:
Department of Parasitology, Institute of Zoology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland
E. SIŃSKI
Affiliation:
Department of Parasitology, Institute of Zoology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland
*
*Corresponding author: National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172, Blindern, Oslo, Norway. E-mail: [email protected]
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Summary

The epidemiology of Bartonella species infecting Apodemus flavicollis and Myodes glareolus in a forest in Eastern Poland was followed for 2 years using mark-recapture. Infections could be acquired in any month, but prevalence, and probability of infection, peaked in the summer. There were significant differences in the pattern of infections between the two species. Both hosts were primarily infected as juveniles, but the probability of infection was highest for A. flavicollis, which, evidence suggests, experienced longer-lasting infections with a wider range of Bartonella genotypes. There was no evidence of increased host mortality associated with Bartonella, although the infection did affect the probability of recapture. Animals could become re-infected, generally by different Bartonella genotypes. Several longer lasting, poorly resolved infections of A. flavicollis involved more than 1 genotype, and may have resulted from sequential infections. Of 22 Bartonella gltA genotypes collected, only 2 (both B. grahamii) were shared between mice and voles; all others were specific either to A. flavicollis or to M. glareolus, and had their nearest relatives infecting Microtus species in neighbouring fields. This heterogeneity in the patterns of Bartonella infections in wild rodents emphasizes the need to consider variation between both, host species and Bartonella genotypes in ecological and epidemiological studies.

Keywords

BartonellaApodemusMyodesrodentsrodent epidemiologyparasite communities
Type
Research Article
Information
Parasitology , Volume 139 , Issue 7 , June 2012 , pp. 881 - 893
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Amori, G. and Luiselli, L. (2011). Growth patterns in free-ranging yellow-necked wood mice, Apodemus flavicollis. Mammalian Biology 76, 129–132. doi: 10.1016/j.mambio.2010.03.008.CrossRefGoogle Scholar
Anderson, B., Lu, E., Jones, D. and Regnery, R. (1995). Characterisation of a 17 kilodalton antigen of Bartonella henselae reactive with sera from patients with cat scratch disease. Journal of Clinical Microbiology 33, 2358–2365.CrossRefGoogle Scholar
Bai, Y., Calisher, C. H., Kosoy, M. Y., Root, J. J. and Doty, J. B. (2011). Persistent infection or successive reinfection of deer mice with Bartonella vinsonii subsp. arupensis. Applied and Environmental Microbiology 77, 1728–1731.CrossRefGoogle ScholarPubMed
Bajer, A., Pawełczyk, A., Behnke, J. M., Gilbert, F. S. and Siński, E. (2001). Factors affecting the component community structure of haemoparasites in bank voles (Clethrionomys glareolus) from the Mazury lake district of Poland. Parasitology 122, 43–54. doi: 10.1007/s00436-003-1040-1.CrossRefGoogle ScholarPubMed
Bajer, A., Bednarska, M., Pawełczyk, A., Behnke, J. M., Gilbert, F. S. and 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. doi: 10.1017/S0031182002001865.CrossRefGoogle ScholarPubMed
Berglund, E. C., Frank, A. C., Calteau, A., Pettersson, O. V., Granberg, F., Eriksson, A.-S., Näslund, K., Holmberg, M., Lindroos, H. and Andersson, S. G. E. (2009). Run-off replication of host adaptability genes is associated with gene transfer agents in the genome of the mouse infecting Bartonella grahamii. PloS Genetics 5, e100546. doi: 10.1371/journal.pgen.1000546.CrossRefGoogle Scholar
Berglund, E. C., Ehrenborg, C., Pettersson, O. V., Granberg, F., Näslund, K., Holmberg, M. and Andersson, S. G. E. (2010). Genome dynamics of Bartonella grahamii in micro-populations of woodland rodents. BMC Genomics 11, 152. doi: 10.1186/1471-2164-11-152.CrossRefGoogle ScholarPubMed
Birtles, R. J., Harrison, T. G. and Molyneux, D. H. (1994). Grahamella in small woodland rodents in the UK: isolation, prevalence and host specificity. Annals of Tropical Medicine and Parasitology 88, 317–327.CrossRefGoogle ScholarPubMed
Birtles, R. J., Hazel, S. M., Bennett, M., Bown, K., Raoult, D. and Begon, M. (2001). Longitudinal monitoring of the dynamics of infection due to Bartonella species in UK woodland rodents. Epidemiology and Infection 126, 323–329.CrossRefGoogle ScholarPubMed
Bown, K., Bennett, M. and Begon, M. (2004). Flea-borne Bartonella grahamii and Bartonella taylorii in bank voles. Emerging Infectious Diseases 10, 684–687. doi: 10.3201/eid1004.030455.CrossRefGoogle ScholarPubMed
Bown, K. J., Begon, M., Bennett, M., Birtles, R. J., Burthe, S., Lambin, X., Telfer, S., Woldehiwet, Z. and Ogden, N. H. (2006). Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom? Vector Borne and Zoonotic Diseases 6, 404–410. doi: 10.1089/vbz.2006.6.404.CrossRefGoogle ScholarPubMed
Breitschwerdt, E. B., Maggi, R. G., Cadenas, M. B. and de Paiva Diniz, P. P. (2009). A groundhog, a novel Bartonella sequence, and my father's death. Emerging Infectious Diseases 15, 2080–2086. doi: 10.3201/eid1512.090206.CrossRefGoogle ScholarPubMed
Cooch, E. and White, G. (2010). Program Mark. A gentle introduction. Avaliable at http://www.phidot.org/software/mark/docs/book/.Google Scholar
Dehio, C. (2008). Infection-associated type IV secretion systems of Bartonella and their diverse roles in host cell interaction. Cellular Microbiology 10, 1591–1598. doi: 10.1111/j.1462-5822.2008.01171.x.CrossRefGoogle ScholarPubMed
Flowerdew, J. R. (1984). Woodmice and yellow necked mice. Mammal Society, London.Google Scholar
Flowerdew, J. R. (1985). The population dynamics of wood mice and yellow necked mice. Symposia of the Zoological Society of London 55, 315–338.Google Scholar
Harris, P. D., Paziewska, A., Zwolińska, L. and Siński, E. (2009). Seasonality of the ectoparasite community of woodland rodents in a Mazurian forest, Poland. Wiadomości Parazitologiczne 55, 377–388.Google Scholar
Healing, T. D. (1981). Infections with blood parasites in the small British rodents Apodemus sylvaticus, Clethrionomys glareolus and Microtus agrestis. Parasitology 83, 179–189.CrossRefGoogle ScholarPubMed
Holmberg, M., Mills, J. N., McGill, S., Benjamin, G. and Ellis, B. A. (2003). Bartonella infection in sylvatic small mammals in Sweden. Epidemiology and Infection 130, 149–157. doi: 10.1017/S0950268802008075.CrossRefGoogle Scholar
Inoue, K., Maruyama, S., Kabeya, H., Yamada, N., Ohashi, N., Sato, Y., Yukawa, M., Masuzawa, T., Kawamori, F., Kadosaka, T., Takada, N., Fujita, H. and Kawabata, H. (2008). Prevalence and genetic diversity of Bartonella species isolated from wild rodents in Japan. Applied and Environmental Microbiology 74, 5086–5092. doi: 10.1128/AEM.00071-08.CrossRefGoogle ScholarPubMed
Iralu, J., Bai, Y., Crook, L., Tempest, B., Simpson, G., McKenzie, T. and Koster, F. (2006). Rodent-associated Bartonella febrile illness, Southwestern United States. Emerging Infectious Diseases 12, 1081–1086.CrossRefGoogle ScholarPubMed
Karem, K. L., Dubois, K. A., McGill, S. L., and Regnery, R. L. (1999). Characterisation of Bartonella-henselae specific humoral immunity in BALB/c mice. Immunology 97, 352–358.CrossRefGoogle ScholarPubMed
Koesling, J., Aebischer, T., Falch, C., Schülein, R. and Dehio, C. (2001). Antibody mediated cessation of hemotropic infection by the intraerythrocytic mouse pathogen Bartonella grahamii. Journal of Immunology 167, 11–14.CrossRefGoogle ScholarPubMed
Kosoy, M., Mandel, E., Green, D., Marston, E., Jones, D. and Childs, E. (2004). Prospective studies of Bartonella of rodents. Part II. Diverse infections in a single rodent community. Vector Borne and Zoonotic Diseases 4, 296–305. doi: 10.1089/vbz.2004.4.296.CrossRefGoogle Scholar
Kozakiewicz, M. (1976). The weight of eye lens as the proposed age indicator of the bank vole. Acta Theriologica 21, 314–316.CrossRefGoogle Scholar
Maurin, M. and Raoult, D. (1996). Bartonella (Rochalimea) quintana infections. Clinical Microbiological Reviews 9, 273–292.CrossRefGoogle ScholarPubMed
Morick, D., Krasnov, B. R., Khokhlova, I. R., Gottlieb, Y. and Harrus, S. (2011). Investigation of Bartonella acquisition and transmission in Xenopsylla ramesis fleas (Siphonaptera: Pulicidae). Molecular Ecology 20, 2864–2870. doi: 10.1111/j.1365-294X.2011.05033.x.CrossRefGoogle ScholarPubMed
Norman, A. F., Regnery, R., Jameson, P., Greene, C. and Krause, D. C. (1995). Differentiation of Bartonella-like isolates at the species level by PCR-restriction fragment length polymorphism in the citrate synthase gene. Journal of Clinical Microbiology 33, 1797–1803.CrossRefGoogle ScholarPubMed
Paziewska, A., Harris, P. D., Zwolińska, L., Bajer, A. and Siński, E. (2011). Recombination within and between species of the alpha-proteobacterium Bartonella infecting rodents. Microbial Ecology 61, 134–145. doi: 10.1007/s00248-010-9735-1.CrossRefGoogle ScholarPubMed
Paziewska, A., Zwolińska, L., Harris, P. D., Bajer, A., and Siński, E. (2010). Utilisation of rodent species by larvae and nymphs of hard ticks (Ixodidae) in two habitats in NE Poland. Experimental and Applied Acarology 50, 79–91. doi: 10.1007/s10493-009-9269-8.CrossRefGoogle ScholarPubMed
Perkins, S. E., Cagnacci, F., Stradiotto, A., Arnoldi, D. and Hudson, P. J. (2009). Comparison of social networks derived from ecological data: implications for inferring infectious disease dynamics. Journal of Animal Ecology 78, 1015–1022. doi: 10.1111/j.1365-2656.2009.01557.x.CrossRefGoogle ScholarPubMed
Richner, H., Oppliger, A. and Christe, P. (1993). Effect of an ectoparasite on reproduction in great tits. Journal of Animal Ecology 62, 703–710.CrossRefGoogle Scholar
Schwarz, C. J. and Arnason, A. N. (1996). A general methodology for the analysis of capture recapture experiments in open populations. Biometrics 52, 860–873.CrossRefGoogle Scholar
Schwarz, C. J. and Arnason, A. N. (2006). Jolly-Seber models in Mark. In Program Mark: A Gentle Introduction (ed. Cooch, E. and White, G.), pp. 401–452. Available at http://www.phidot.org/software/mark/docs/book.Google Scholar
Siński, E., Bajer, A., Welc, R., Pawełczyk, A., Ogrzewalska, M. and Behnke, J. M. (2006). Babesia microti: Prevalence in wild rodents and Ixodes ricinus ticks from the Mazury lake district of NE Poland. International Journal of Medical Microbiology 296, 137–143. doi: 10.1016/j.ijmm.2006.01.015.CrossRefGoogle Scholar
Stenseth, N. Chr., Viljugrein, H., Jędrzejewski, W., Mysterud, A. and Pucek, Z. (2002). Population dynamics of Clethrionomys glareolus and Apodemus flavicollis: seasonal components of density dependence and density independence. Acta Theriologica 47 (Suppl. 1), 39–67.CrossRefGoogle Scholar
Sweger, D., Resto-Ruiz, S., Johnson, D. P., Schmiederer, M., Hawke, N. and Anderson, B. (2000). Conservation of the 17-kilodalton antigen gene within the genus Bartonella. Clinical and Diagnostic Laboratory Immunology 7, 251–257.CrossRefGoogle ScholarPubMed
Telfer, S., Bennett, M., Bown, K., Cavanagh, R., Crespin, L., Hazel, S., Jones, T. and Begon, M. (2002). The effects of cowpox virus on survival in natural rodent populations: increases and decreases. Journal of Animal Ecology 71, 558–568.CrossRefGoogle Scholar
Telfer, S., Birtles, R., Bennett, M., Lambin, X., Paterson, S. and Begon, M. (2008). Parasite interactions in natural populations: insights from longitudinal data. Parasitology 135, 767–781. doi: 10.1017/S0031182008000395.CrossRefGoogle ScholarPubMed
Telfer, S., Lambin, X., Birtles, R., Beldomenico, P., Burthe, S., Paterson, S. and Begon, M. (2010). Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243–246. doi: 10.1126/science.1190333.CrossRefGoogle Scholar
Welc-Falęciak, R., Bajer, A., Behnke, J. and Siński, E. (2008). Effects of host diversity and the community composition of hard ticks (Ixodidae) on Babesia microti infection. International Journal of Medical Microbiology 298 (Suppl. 1), 235–242. doi: 10.1016/j.ijmm.2007.12.002.CrossRefGoogle Scholar
White, G. C. and Burnham, K. P. (1999). Program MARK: survival estimation from populations of marked animals. Bird Study 46 (Suppl.), 120–138. doi: 10.1080/00063659909477239.CrossRefGoogle Scholar
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