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Molecular characterization of haemoparasites infecting bats (Microchiroptera) in Cornwall, UK

Published online by Cambridge University Press:  28 June 2005

R. CONCANNON ,
K. WYNN-OWEN ,
V. R. SIMPSON  and
R. J. BIRTLES
R. CONCANNON
Affiliation:
Department of Veterinary Pathology, University of Liverpool, Leahurst, Chester High Road, Neston, Cheshire CH64 7TE
K. WYNN-OWEN
Affiliation:
Department of Veterinary Pathology, University of Liverpool, Leahurst, Chester High Road, Neston, Cheshire CH64 7TE
V. R. SIMPSON
Affiliation:
The Wildlife Veterinary Investigation Centre, Jollys Bottom Farm, Chacewater, Truro, Cornwall TR4 8PB
R. J. BIRTLES
Affiliation:
Department of Veterinary Pathology, University of Liverpool, Leahurst, Chester High Road, Neston, Cheshire CH64 7TE
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Abstract

The presence of haemoparasites from the Order Piroplasmida and the genera Bartonella and Trypanosoma was assessed in the blood of 60 bats, belonging to 7 species, inhabiting sites across Cornwall in southwest England. DNA extracted from macerated heart tissue was incorporated into taxon-specific polymerase chain reactions (PCRs) and amplification products were sequenced as a means of identifying, or assigning an identity, to detected haemoparasites. A Piroplasmida species was detected in 6 Pipistrellus spp., whereas Bartonella infections were detected in 5 bats belonging to 4 different species. Trypanosoma dionisii was detected in 1 Pipistrellus spp. Phylogenetic inference from alignment of a partial 18S rRNA-encoding gene sequence of the pipistrelle-associated Piroplasmida species with homologous sequences available for other members of the Order indicated that this organism was unique but specifically related to members of the genus Babesia, a phylogeny that would be in keeping with the organism being Babesia vesperuginis. Alignment of partial citrate synthase gene sequences from the bat-associated bartonellae revealed 5 distinct genotypes that were probably derived from 2 distinct Bartonella species. The study demonstrates the utility of molecular methods for detecting haemoparasites in dead bats and provides, for the first time, tangible identities for bat-associated Babesia and Bartonella species.

Keywords

HaemoparasitePiroplasmidaTrypanosomaBabesiaBartonellaMicrochiropterabats
Type
Research Article
Information
Parasitology , Volume 131 , Issue 4 , October 2005 , pp. 489 - 496
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

Baker, J. R. ( 1974). Protozoan parasites of the blood of British wild birds and mammals. Journal of Zoology 172, 169–190.CrossRefGoogle Scholar
Baker, J. R., Miles, M. A., Godfrey, D. G. and Barrett, T. V. ( 1978). Biochemical characterisation of some Trypanosoma (Schizotrypanum) from bats (Microchiroptera). American Journal of Tropical Medicine and Hygiene 27, 483–491.CrossRefGoogle Scholar
Baker, J. R. and Thompson, G. B. ( 1971). Two species of Trypanosoma from British Chiroptera (bats). Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 427.CrossRefGoogle Scholar
Birtles, R. J., Harrison, T. G. and Molyneux, D. H. ( 1994). Grahamella in small woodland mammals in the U.K.: isolation, prevalence and host specificity. Annals of Tropical Medicine and Parasitology 88, 317–327.Google Scholar
Bown, K. J., Begon, M., Bennett, M., Woldehiwet, Z. and Ogden, N. H. ( 2003). Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerging Infectious Diseases 9, 63–70.CrossRefGoogle Scholar
Coles, A. C. ( 1914). Blood parasites found in mammals, birds and fishes in England. Parasitology 7, 17–61.CrossRefGoogle Scholar
Cox, F. E. G. ( 1970). Parasitic protozoa of British wild mammals. Mammal Review 1, 1–28.CrossRefGoogle Scholar
Gardner, R. A., Molyneux, D. H. and Stebbings, R. E. ( 1987). Studies on the prevalence of haematozoa of British bats. Mammal Review 17, 75–80.CrossRefGoogle Scholar
Gardner, R. A. and Molyneux, D. H. ( 1987). Babesia vesperuginis: natural and experimental infections in British bats (Microchiroptera). Parasitology 95, 461–469.CrossRefGoogle Scholar
Gardner, R. A. and Molyneux, D. H. ( 1988 a). Trypanosoma (Megatrypanum) incertum from Pipistrellus pipistrellus: development and transmission by cimicid bugs. Parasitology 96, 433–447.Google Scholar
Gardner, R. A. and Molyneux, D. H. ( 1988 b). Schizotrypanum in British bats. Parasitology 97, 43–50.Google Scholar
Gardner, R. A. and Molyneux, D. H. ( 1988 c). Polychromophilus murinus: a malarial parasite of bats: life-history and ultrastructural studies. Parasitology 96, 591–605.Google Scholar
Goedbloed, E., Cremers-Hoyer, L. and Perie, N. M. ( 1964). Blood parasites of bats in The Netherlands. Annals of Tropical Medicine and Parasitology 58, 257–260.CrossRefGoogle Scholar
Gundi, V. A., Davoust, B., Khamis, A., Boni, M., Raoult, D. and La Scola, B. ( 2004). Isolation of Bartonella rattimassiliensis sp. nov. and Bartonella phoceensis sp. nov. from European Rattus norvegicus. Journal of Clinical Microbiology 42, 3816–3818.Google Scholar
Hamilton, P. B., Stevens, J. R., Gaunt, M. W., Gidley, J. and Gibson, W. C. ( 2004). Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. International Journal for Parasitology 34, 1393–1404.CrossRefGoogle Scholar
Harris, S., Morris, P., Wray, S. and Yaldon, D. ( 1995). A review of British mammals: population estimates and conservation status of British mammals other than cetaceans. Joint Nature Conservation Committee, Peterborough, UK.
Jones, G. and Barratt, E. M. ( 1999). Vespertilio pipistrellus Schreber, 1774 and V. pygmaeus Leach, 1825 (currently Pipistrellus pipistrellus and P. pygmaeus; Mammalia, Chiroptera): proposed designation of neotypes. Bulletin of Zoological Nomenclature 56, 182–186.Google Scholar
Kramptiz, H. E. and Kleinschmidt, A. ( 1960). Grahamella Brumpt 1911. Biologische und morphologische Untersuchungen. Zeitschrift für Tropenmedizin und Parasitologie 11, 336–352.Google Scholar
La Scola, B., Zeaiter, Z., Khamis, A. and Raoult, D. ( 2003). Gene-sequence-based criteria for species definition in bacteriology: the Bartonella paradigm. Trends in Microbiology 11, 318–321.CrossRefGoogle Scholar
Molyneux, D. H. and Bafort, J. M. ( 1971). Observations on the trypanosome of Pipistrellus pipistrellus in Britain, Trypanosoma (Schizotrypanum) vespertilionis. Annales de la Société Belge de Médecine Tropicale 51, 335–348.Google Scholar
Nathwani, D., McIntyre, P. G., White, K., Shearer, A. J., Reynolds, N., Walker, D., Orange, G. V. and Fooks, A. R. ( 2003). Fatal human rabies caused by European bat Lyssavirus type 2a infection in Scotland. Clinical Infectious Diseases 37, 598–601.CrossRefGoogle Scholar
Noyes, H. A., Stevens, J. R., Teixeira, M., Phelan, J. and Holz, P. ( 1999). A nested PCR for the ssrRNA gene detects Trypanosoma binneyi in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia. International Journal for Parasitology 29, 331–339.CrossRefGoogle Scholar
Page, R. D. M. ( 1996). TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google Scholar
Petrie, G. F. ( 1905). Observations relating to the structure and geographical distribution of certain trypanosomes. Journal of Hygiene 5, 191–200.CrossRefGoogle Scholar
Pretorius, A.-M., Beati, L. and Birtles, R. J. ( 2004). Diversity of bartonellae associated with small mammals inhabiting Free State province, South Africa. International Journal of Systematic and Evolutionary Microbiology 54, 1959–1967.CrossRefGoogle Scholar
Schmidt-Posthaus, H., Breitenmoser-Wursten, C., Posthaus, H., Bacciarini, L. and Breitenmoser, U. ( 2002). Causes of mortality in reintroduced Eurasian lynx in Switzerland. Journal of Wildlife Disease 38, 84–92.CrossRefGoogle Scholar
Schnittger, L., Yin, H., Gubbels, M. J., Beyer, D., Niemann, S., Jongejan, F. and Ahmed, J. S. ( 2003). Phylogeny of sheep and goat Theileria and Babesia parasites. Parasitology Research 91, 398–406.Google Scholar
Simpson, V. R., Panciera, R. J., Hargreaves, J., McGarry, J. W., Scholes, S. F. E., Bown, K. J. and Birtles, R. J. ( 2005). Myocarditis and myositis in pine martens (Martes martes) in Scotland due to infection with Hepatozoon sp. Veterinary Record 156, 442–446.CrossRefGoogle Scholar
Stebbings, R. E. ( 1988 a). Conservation of European Bats. Christopher Helm, London.
Stebbings, R. E. ( 1988 b). Identification of resident and vagrant Bats in Great Britain. The State Veterinary Journal 42, 130–139.Google Scholar
Stevens, J. R., Noyes, H. A., Dover, G. A. and Gibson, W. C. ( 1999). The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118, 107–116.CrossRefGoogle Scholar
Telfer, S., Bown, K. J., Sekules, R., Begon, M., Hayden, T. and Birtles, R. J. ( 2005). Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130, 661–668.CrossRefGoogle Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. ( 1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.CrossRefGoogle Scholar
Wenyon, C. M. ( 1926). Protozoology, a Manual for Medical Men, Veterinarians and Zoologists, Vols 1 and 2. Bailliere, Tindall and Cox, London.
Wickramasinghe, L. P., Harris, S., Jones, G. and Vaughan, N. ( 2003). Bat activity and species richness on organic and conventional farms: impact of agricultural intensification. Journal of Applied Ecology 40, 984–993.CrossRefGoogle Scholar
Young, A. S. ( 1970). Studies on the blood parasites of small mammals with special reference to piroplasms. PhD thesis, University of London.