Gastrointestinal helminths of pipistrelle bats (Pipistrellus pipistrellus/Pipistrellus pygmaeus) (Chiroptera: Vespertilionidae) of England | Parasitology | Cambridge Core (original) (raw)

Summary

Although bats are one of the most successful and diverse of mammalian orders, studies that focus upon bat endoparasites are limited. To further knowledge of bat parasitology, pipistrelle bats (Pipistrellus pipistrellus and P. pygmaeus) were acquired from across the Greater Manchester and Lancashire region of England and examined for gastrointestinal helminths using morphological and molecular analyses†. Sixty-eight of 90 adult/juvenile bats (76% prevalence) were infected with at least 1 species of helminth and mean helminth abundance was 48·2 (+/−7·0). All helminths were digenean trematodes and the following species were identified in 51 P. pipistrellus specimens (prevalence in parentheses): Lecithodendrium linstowi (80·4%), L. spathulatum (19·6%), Prosthodendrium sp. (35·3%), Plagiorchis koreanus (29·4%) and Pycnoporus heteroporus (9·8%). Statistical analyses, incorporating multifactorial models, showed that male bats exhibited a significantly more aggregated helminth distribution and lower abundance than females. Positive associations were observed between L. linstowi and L. spathulatum, Prosthodendrium sp. and P. heteroporus and between L. spathulatum and P. koreanus. A revised phylogeny of bat-associated Lecithodendriidae, incorporating novel L. spathulatum and Prosthodendrium sp. 28S rRNA sequences, separated the controversial clade formed by L. linstowi and P. hurkovaae. Further studies are likely to assist the understanding of bat-parasite/pathogen relationships, helminth infracommunity structures and phylogenetics.

References

Anthony, E. (1988). Age determination in bats. In Ecological and Behavioural Methods for the Study of Bats (ed. Kunz, T. H.), pp. 47–58. Smithsonian Institution Press, Washington D.C., USA.Google Scholar

Barratt, E. M., Deaville, R., Burland, T. M., Bruford, M. W., Jones, G., Racey, P. A. and Wayne, R. K. (1997). DNA answers the call of pipistrelle bat species. Nature, London 387, 138–139.CrossRefGoogle ScholarPubMed

Behnke, J. M. (2008). Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions …. or pure randomness? Parasitology 135, 751–766.CrossRefGoogle ScholarPubMed

Blankespoor, H. D. and Ulmer, M. J. (1970). Helminths from six species of Iowa bats. Proceedings of the Iowa Academy of Sciences 77, 200–206.Google Scholar

Blehert, D. S., Hicks, A. C., Behr, M., Meteyer, C. U., Berlowski-Zier, B. M., Buckles, E. L., Coleman, J. T., Darling, S. R., Gargas, A., Niver, R., Okoniewski, J. C., Rudd, R. J. and Stone, W. B. (2009). Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227.CrossRefGoogle ScholarPubMed

Bliss, C. I. and Fisher, R. A. (1953). Fitting the negative binomial distribution to biological data. Biometrics 9, 176–200.Google Scholar

Botella, P., Sanchez, L. and Esteban, J. (1993). Helminthfauna of bats in Spain. III. Parasites of Pipistrellus pipistrellus (Schreber, 1774) (Chiroptera: Vespertilionidae). Research and Reviews in Parasitology 53, 63–70.Google Scholar

Bush, O. A., Aho, J. M. and Kennedy, C. R. (1990). Ecological versus phylogenetic determinants of helminth parasite community richness. Evolutionary Ecology 4, 1–20.Google Scholar

Butler, J. E., Wertz, N., Zhao, Y., Zhang, S., Bao, Y., Bratsch, S., Kunz, T. H., Whitaker, J. O. Jr. and Schountz, T. (2011). The two suborders of chiropterans have the canonical heavy-chain immunoglobulin (Ig) gene repertoire of eutherian mammals. Developmental and Comparative Immunology 35, 273–284.CrossRefGoogle ScholarPubMed

Calisher, C. H., Childs, J. E., Field, H. E., Holmes, K. V. and Schountz, T. (2006). Bats: important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19, 531–545.CrossRefGoogle ScholarPubMed

Cattadori, I. M., Haukisalmi, V., Henttonen, H. and Hudson, P. J. (2006). Transmission ecology and the structure of parasite communities in small mammals. In Micromammals and Macroparasites: From Evolutionary Ecology to Management (ed. Morand, S., Krasnov, B. R. and Poulin, R.), pp. 349–370. Springer, Tokyo, Japan.Google Scholar

Chowdhury, N. and Aquirre, A. A. (2001). Helminths of Wildlife. Science Publishers, Inc., Enfield, New Hampshire, USA.Google Scholar

Coggins, J. R., Tedesco, J. L. and Rupprecht, C. E. (1982). Seasonal changes and overwintering of parasites in the bat, Myotis lucifugus (Le Conte), in a Wisconsin hibernaculum. American Midland Naturalist 107, 305–315.CrossRefGoogle Scholar

Crawley, M. J. (2005). Statistics: An Introduction Using R. John Wiley & Sons Ltd, Chichester, UK.CrossRefGoogle Scholar

Dawes, B. (1956). The Trematoda: With special reference to British and other European forms. Cambridge University Press, Cambridge, UK.Google Scholar

Esteban, J. G., Amengual, B. and Cobo, J. S. (2001). Composition and structure of helminth communities in two populations of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) from Spain. Folia Parasitologica 48, 143–148.CrossRefGoogle ScholarPubMed

Esteban, J. G., Oltra Ferrero, J. L. and Mas-coma, S. (1990). Helmintofauna de los murcielagos de Espana. II. Parasitos de Miniopterus schreibersi (Kuhl, 1819) (Chiroptera: Vespertilionidae). Revista Iberica Parasitologia 50, 199–209.Google Scholar

Feliu, C., Torres, J., Miquel, J., Segovia, J. M. and Fons, R. (2006). Digenean trematodes. In Micromammals and Macroparasites: From Evolutionary Ecology to Management (ed. Morand, S., Krasnov, B. R. and Poulin, R.), pp. 13–28. Springer, Tokyo, Japan.CrossRefGoogle Scholar

Gibson, D. I., Bray, R. A. and Harris, E. A. (2005). Host-Parasite Database of the Natural History Museum. London, UK.Google Scholar

Harris, S., Morris, P., Wray, S. and Yeldon, D. (1995). A Review of British Mammals: Population Estimates and Conservation Status of British Mammals other than Cetaceans. Joint Nature Conservation Committee, Peterborough, UK.Google Scholar

Haukisalmi, V., Henttonen, H. and Tenora, F. (1988). Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807–825.CrossRefGoogle Scholar

Junker, K., Bain, O. and Boomker, J. (2008). Helminth parasites of Natal long-fingered bats, Miniopterus natalensis (Chiroptera: Miniopteridae), South Africa. Onderstepoort Journal of Veterinary Research 75, 261–265.CrossRefGoogle ScholarPubMed

Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247–264.Google Scholar

Koski, K. G. and Scott, M. E. (2001). Gastrointestinal nematodes, nutrition and immunity: breaking the negative spiral. Annual Review of Nutrition 21, 297–321.Google Scholar

Lotz, J. M. and Font, W. F. (1985). Structure of enteric helminth communities in two populations of Eptesicus fuscus (Chiroptera). Canadian Journal of Zoology 63, 2969–2978.CrossRefGoogle Scholar

Lotz, J. M. and Font, W. F. (1991). The role of positive and negative interspecific associations in the organization of communities of intestinal helminths of bats. Parasitology 103, 127–138.Google Scholar

Lotz, J. M. and Font, W. F. (1994). Excess positive associations in communities of intestinal helminths of bats: a refined null hypothesis and a test of the facilitation hypothesis. Journal of Parasitology 80, 398–413.Google Scholar

Macy, R. W. (1960). The life cycle of Plagiorchis vespertilionis parorchis. n. ssp., (Trematoda: Plagiorchidae), and observations on the effects of light on the emergence of the cercaria. Journal of Parasitology 46, 337–345.CrossRefGoogle ScholarPubMed

Maizels, R. M. and Yazdanbakhsh, M. (2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733–744.Google Scholar

Marshall, M. and Miller, G. (1979). Some digenetic trematodes from Ecuadorian bats including five new species and one new genus. Journal of Parasitology 65, 909–917.Google Scholar

Mayer, F. and von Helversen, O. (2001). Cryptic diversity in European bats. Proceedings of the Royal Society of London, B 268, 1825–1832.CrossRefGoogle ScholarPubMed

McAllister, C. T., Bursey, C. R. and Burns, A. D. (2005). Gastrointestinal helminths of Rafinesque's Big-Eared Bat, Corynorhinus rafinesquii (Chiroptera: Vespertilionidae), from Southwestern Arkansas, U.S.A. Comparative Parasitology 72, 121–123.Google Scholar

Nahhas, F. A., Yang, P. and Uch, S. (2005). Digenetic trematodes of Tadarida brasiliensis mexicana (Chiroptera: Molossidae) and Myotis californicus (Chiroptera: Vespertilionidae) from Northern California, U.S.A. Comparative Parasitology 72, 196–199.Google Scholar

Nickel, P. A. and Hansen, M. F. (1967). Helminths of bats collected in Kansas, Nebraska and Oklahoma. American Midland Naturalist 78, 481–486.Google Scholar

Olsen, O. W. (1937). A systematic study of the Trematode sub-family Plagiorchiinae Prat, 1902. Transactions of the American Microscopical Society 56, 311–339.Google Scholar

Page, R. D. (1996). TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google ScholarPubMed

Poulin, R. (1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937–944.Google Scholar

Poulin, R. (1996). Helminth growth in vertebrate hosts: does host sex matter? International Journal for Parasitology 26, 1311–1315.Google Scholar

Prendergast, B. J., Freeman, D. A., Zucker, I. and Nelson, R. J. (2002). Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 282, 1054–1062.Google Scholar

Pusterla, N., Johnson, E. M., Chae, J. S. and Madigan, J. E. (2003). Digenetic trematodes, Acanthatrium sp. and Lecithodendrium sp., as vectors of Neorickettsia risticii, the agent of Potomac horse fever. Journal of Helminthology 77, 335–339.CrossRefGoogle Scholar

R Development Core Team (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.Google Scholar

Reiczigel, J. (2003). Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine 22, 611–621.CrossRefGoogle ScholarPubMed

Reiczigel, J., Zakarias, D. and Rozsa, L. (2005). A bootstrap test of stochastic equality of two populations. The American Statistician 59, 1–6.CrossRefGoogle Scholar

Ricci, M. (1995). Trematode parasites of Italian bats. Parassitologia 37, 199–214.Google ScholarPubMed

Rogan, M. T., Craig, P. S., Hide, G., Heath, S., Pickles, A. and Storey, D. M. (2007). The occurrence of the trematode Plagiorchis muris in the wood mouse Apodemus sylvaticus in North Yorkshire, UK. Journal of Helminthology 81, 57–62.CrossRefGoogle ScholarPubMed

Rozsa, L., Reiczigel, J. and Majoros, G. (2000). Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232.CrossRefGoogle ScholarPubMed

Sambrook, J. and Russell, D. (2000). Molecular Cloning: A Laboratory Manual, 3rd Edn.Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.Google Scholar

Shimalov, V. V., Demyanchik, M. G. and Demyanchik, V. T. (2002). A study on the helminth fauna of the bats (Mammalia, Chiroptera: Vespertilionidae) in Belarus. Parasitology Research 88, 1011.Google Scholar

Stebbings, R. E., Yalden, D. W. and Herman, J. S. (2007). Which Bat Is It?: A Guide to Bat Identification in Great Britain and Ireland, 3rd Edn.The Mammal Society, Southampton, UK.Google Scholar

Swofford, D. L. (2004). PAUP 4.0: Phylogenetic Analysis Using Parsimony (and Other Methods): User's Book. Sinauer Associates Incorporated, Sunderland, MA, USA.Google Scholar

Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar

Tkach, V., Pawlowski, J. and Mariaux, J. (2000 a). Phylogenetic analysis of the suborder plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal for Parasitology 30, 83–93.Google Scholar

Tkach, V. V., Pawlowski, J. and Sharpilo, V. P. (2000 b). Molecular and morphological differentiation between species of the Plagiorchis vespertilionis group (Digenea, Plagiorchiidae) occurring in European bats, with a re-description of P. vespertilionis (Muller, 1780). Systematic Parasitology 47, 9–22.CrossRefGoogle ScholarPubMed

Tkach, V. V., Littlewood, D. T., Olson, P. D., Kinsella, J. M. and Swiderski, Z. (2003). Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.Google Scholar

Venables, W. N. and Ripley, B. D. (2002). Modern Applied Statistics with S, 4th Edn.Springer, New York, USA.Google Scholar

Webster, W. A. and Casey, G. A. (1973). Studies on the parasites of Chiroptera. III. Helminths from various bat species collected in British Columbia. Canadian Journal of Zoology 51, 633–636.Google Scholar

Wedekind, C. and Jacobsen, P. J. (1998). Male-biased susceptibility to helminth infection: an experimental test with a copepod. Oikos 81, 458–462.Google Scholar

Zdzitowiecki, K. (1969). Helminths of bats in Poland II. Trematodes of the subfamily Lecithodendriinae. Acta Parasitologica Poloni 16, 207–225.Google Scholar