Identification of a new species of digenean Notocotylus malhamensis n. sp. (Digenea: Notocotylidae) from the bank vole (Myodes glareolus) and the field vole (Microtus agrestis) | Parasitology | Cambridge Core (original) (raw)

Summary

Notocotylus malhamensis n. sp. is described from the caecum of the bank vole (Myodes glareolus) and the field vole (Microtus agrestis) from Malham Tarn Nature Reserve in North Yorkshire, UK. In total, 581 specimens were collected from rodents trapped at a wetland site (Tarn Fen) between July 2010 and October 2011 with a prevalence of 66·7% and mean intensity of 94·6 in the bank vole and 50% prevalence and a mean intensity of 4·3 in the field vole. This species appears to be most closely related to other previously described Notocotylus species infecting rodents in Europe but differs principally by the metraterm to cirrus sac ratio (1:1·5–1:1·2) in combination with a densely spinulated cirrus, simple caeca and a greater number of ventral glands in the lateral rows (14–17). The use of molecular differentiation was of limited use in this study due to a paucity of relevant information in the DNA sequence databases. However, the complete ITS1-5.8S rDNA-ITS2 and partial 28S gene sequences have been generated to provide a definitive tool for identification of this species in future studies. As far as we know this is the first report of a notocotylid infection in M. glareolus in the UK.

References

Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. S. (2000). Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 74, 7–15.CrossRefGoogle ScholarPubMed

Allan, J. C., Craig, P. S., Sherington, J., Rogan, M. T., Storey, D. M., Heath, S. and Iball, K. (1999). Helminth parasites of the wild rabbit Oryctolagus cuniculus near Malham Tarn, Yorkshire, UK. Journal of Helminthology 73, 289–294.CrossRefGoogle ScholarPubMed

Barker, F. D. (1915). Parasites of the American Muskrat (Fiber zibethicus). Journal of Parasitology 1, 184–197.CrossRefGoogle Scholar

Barton, D. P. and Blair, D. (2005). Family Notocotylidae Lühe, 1909. In Keys to the Trematoda, Vol. 2 (ed. Jones, A., Bray, R. A. and Gibson, D. I.), pp. 383–396. Cabi Publishing: Wallingford, Oxon, London, UK.CrossRefGoogle Scholar

Baylis, H. A. (1928 a). A new species of Notocotylus (Trematoda), with some remarks on the genus. The Annals and Magazine of Natural History, 10th Series 2, 582–585.CrossRefGoogle Scholar

Baylis, H. A. (1928 b). Records of some parasitic Worms from British Vertebrates. The Annals and Magazine of Natural History, 10th Series 3, 329–343.CrossRefGoogle Scholar

Baylis, H. A. (1936). A new species of Notocotylus (Trematoda), from the water rail. Annals and Magazine of Natural History, 10th Series 17, 474–477.CrossRefGoogle Scholar

Baylis, H. A. (1939). Further records of Parasitic Worms from British Vertebrates. The Annals and Magazine of Natural History, 11th Series 23, 473–798.CrossRefGoogle Scholar

Behnke, J. M., Eira, C., Rogan, M., Gilbert, F. S., Torres, J., Miquel, J. and Lewis, J. W. (2009). Helminth species richness in wild wood mice, Apodemus sylvaticus, is enhanced by the presence of the intestinal nematode Heligmosomoides polygyrus. Parasitology 136, 793–804.CrossRefGoogle Scholar

Behnke, J. M., Lewis, J. W., Mohd Zain, S. N. and Gilbert, F. S. (1999). Helminth infections in Apodemus sylvaticus in Southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 31–44.CrossRefGoogle ScholarPubMed

Beverley-Burton, M. (1961). Studies on the trematoda of British freshwater birds. Proceedings of the Zoological Society of London 137, 13–39.CrossRefGoogle Scholar

Bhalerao, G. D. (1935). On two new monostomes (Trematoda) from avian hosts in British India. Indian Journal of Veterinary Science and Animal Husbandry 5, 49–63.Google Scholar

Bhutta, M. S. and Khan, D. (1975). Digenetic trematodes of vertebrates from Pakistan. Bulletin of the Department of Zoology, University of the Panjab (new series), article 8: Lahore, Pakistan.Google Scholar

Bisset, S. (1977). Notocotylus tadornae n.sp. and Notocotylus gippyensis (Beverley-Burton, 1958) (Trematoda: Notocotylidae) from waterfowl in New Zealand: morphology, life history and systematic relations. Journal of Helminthology 51, 365–372.CrossRefGoogle Scholar

Brooks, D. R. and Heard, R. W. III (1977). Parasites of the Clapper Rail, Rallus longirostris Boddaert. III. Description of Notocotylus schmidti sp. n. Proceedings of the Helminthological Society of Washington 44, 63–65.Google Scholar

Chaisiri, K., Morand, S. and Ribas, A. (2011). Notocotylus loeiensis N. sp. (Trematoda: Notocotylidae) from Rattus losea (Rodentia: Muridae) in Thailand. Parasite (Paris: France) 18, 35–38.CrossRefGoogle Scholar

Cribb, T. H. (1991). Notocotylidae (Digenea) from the Australian water rat Hydromys chrysogaster Geoffroy, 1804 (Muridae). Systematic Parasitology 18, 227–237.CrossRefGoogle Scholar

Deshmukh, A. L. (1985). A new species of Notocotylus (Trematoda: Notocotylidae) from a Cattle Egret, Bubulcus ibis. Indian Journal of Parasitology 9, 251–252.Google Scholar

Dubois, G. (1951). Etude des trematodes nord-americains de la collection E. L. Schiller et revision de genre Notocotylus Diesing, 1839. Bulletin de la Societe Neuchateloise des Sciences Naturelles 74, 42–76.Google Scholar

Dubois, G. and Vigueras, J. P. (1953). Notocotylus lopezneyrai n. sp. (Trematoda, Notocotylidae), parasito del intestino des Rosthramus sociabilis levis Friedmann (Aves). Memorias de la Sociedad Cubana Hisoria Natural 21, 251–255.Google Scholar

Duthoit, C. M. G. (1931). A new species of the trematode genus Notocotylus. Annals and Magazine of Natural History 7, 290–293.CrossRefGoogle Scholar

El-Naffar, M. K. and Khalifa, R. (1983). Notocotylus gallinulae sp.n. (Trematoda, Notocotylidae), a new digenetic trematode from the Egyptian moorhen Gallinula Chloropus Chloropus (L.) Acta Parasitologica polonica 28, 247–252.Google Scholar

Elton, C., Ford, E. B. and Baker, J. R. (1931). The health and parasites of a Wild Mouse population. Proceedings of the Zoological Society of London 101, 657–721.CrossRefGoogle Scholar

Flores, V. and Brugni, N. (2005). Notocotylus biomaphalariae n. sp (Digenea: Notocotylidae) from Biomphalaria peregrine (Gastropoda: Pulmonata) in Patagonia, Argentina. Systematic Parasitology 61, 207–214.CrossRefGoogle Scholar

Gibson, D. I., Bray, R. A. and Harris, E. A. (Compilers) (2005). Host-Parasite Database of the Natural History Museum, London. Available Internet: www.nhm.ac.uk [Accessed 08/08/2011].Google Scholar

Ginetsinskaya, T. A. and Naumov, D. V. (1958). The helminth fauna of some species of Charadriiformes in the white sea. In Papers on Helminthology Presented to Academician K. I. Skryabin on his 80th Birthday. pp. 99–108. Moscow, USSR.Google Scholar

Gupta, P. C. and Gupta, S. P. (1976). On two trematodes of the genus Notocotylus Diesing, 1839, from avian hosts of Kanpur. U. P. Indian Journal of Zootomy 17, 1–4.Google Scholar

Gupta, P. C. and Gupta, S. P. (1977). Two new avian trematodes. Psilotrema nettapusi n. sp. and Notocotylus kanpurensis n. sp. from Kanpur. Indian Journal of Parasitology 1, 133–135.Google Scholar

Gupta, P. C. and Singh, R. B. (1983). On four new species of the genus Notocotylus Diesing, 1839 (Digenea: Notocotylidae) from avian hosts of Uttar Pradesh. Kanpur University Research Journal 4, 27–35.Google Scholar

Gupta, P. D. (1970). Fauna of Rajastan, India. Part 8. Trematoda. Records of the Zoological Survey of India 62, 171–190.CrossRefGoogle Scholar

Gupta, V. and Jehan, A. (1977). Some trematodes from avian hosts of India. Anales del Instituto de Biologia, Universidad Nacional Autonoma de Mexico, Serie Zoologia 48, 13–26.Google Scholar

Gurr, G. T. (1963). Biological Staining Methods, 7th Edn.George T. Gurr Ltd, London, UK.Google Scholar

Hanelt, B. (2009). Hyperparasitism by Paragordius varius (Nematomorpha: Gordiida) Larva of Monostome Redia (Trematoda: Digenea). Journal of Parasitology 95, 242–243.CrossRefGoogle ScholarPubMed

Harrah, E. C. (1922). Notocotylus urbanensis. North American monostomes primarily from freshwater hosts. Illinois Biological monographs 7, 51–53.Google Scholar

Harwood, P. D. (1939). Notes on Tennessee helminths. IV. North American trematodes of the subfamily Notocotylinae. Journal of the Tennessee Academy of Science 14, 421–437.Google Scholar

Herber, E. C. (1942). Life history studies of two trematodes of the sub family Notocotylinae. Journal of Parasitology 28, 179–196.CrossRefGoogle Scholar

Hughes, J. M., Thomasson, D. T., Craig, P. S., Georgin, S., Pickles, A. and Hide, G. (2008). Neospora caninum: detection in wild rabbits and coinfection with Toxoplasma gondii by PCR analysis. Experimental Parasitology 120, 255–260.CrossRefGoogle ScholarPubMed

Hughes, J. M., Williams, R. H., Morley, E. K., Cook, D. A. N., Terry, R. S., Murphy, R. G., Smith, J. E. and Hide, G. (2006). The prevalence of Neospora caninum and co-infection with Toxoplasma gondii by PCR analysis in naturally occurring mammal populations. Parasitology 132, 29–36.CrossRefGoogle ScholarPubMed

Hsu, P. K. (1954). A new species of Notocotylus from Canton (Trematoda: Notocotylidae). Acta Zoologica Sinica 6, 117–122.Google Scholar

Joyeux, C. H. (1922). Recherches sur les Notocotyles. Bulletin de la Societe de Pathologie Exotique 15, 331–339.Google Scholar

Kanev, I., Vassilev, I., Dimitrov, V. and Radev, V. (1994). Life cycle delimitation and redescription of Catatropis verrucosa (Frolich, 1789) Odhner, 1905 (Trematoda, Notocotylidae). Systematic Parasitology 29, 133–148.CrossRefGoogle Scholar

Kinsella, J. M. (1971). Growth, development, and intraspecific variation of Quinqueserialis quinqueserialis (Trematoda: Notocotylidae) in rodent hosts. The Journal of Parasitology 57, 62–70.CrossRefGoogle Scholar

Kinsella, J. M. and Tkach, V. V. (2005). Notocotylus fosteri sp. Nov. (Trematoda, Notocotylidae) from the rice rat, Oryzomys palustris in Florida. Acta Parasitologica 50, 194–198.Google Scholar

Ku, C. (1937). Two new trematodes of the genus Notocotylus, with a key to the species of the genus. Peking Natural History Bulletin 12, 113–122.Google Scholar

Lal, M. B. (1935 a). A review of the genus Notocotylus with description of a new trematode parasite of Mareca Penelope from Lucknow. Proceedings of the Indian Academy of Sciences, Section B 2, 457–466.Google Scholar

Lal, M. B. (1935 b). On the morphology of a new species of monostome of the genus Notocotylus Diesing, 1839. Proceedings of the Indian Academy of Sciences, Section B 2, 419–423.Google Scholar

Lange, R. and Staaland, H. (1970). Adaptations of the caecum-colon structure of rodents. Comparative Biochemistry and Physiology 35, 905–919.CrossRefGoogle Scholar

Murrills, R. J., Southgate, V. R. and Reader, T. A. J. (1988). Studies on the invasion of Notocotylus attenuatus (Notocotylidae: Digenea) into its snail host Lymnaea peregra: in vivo observations 1 and 7 days post infection. International Journal for Parasitology 18, 161–166.CrossRefGoogle Scholar

Nath, D. and Pande, B. P. (1963). On a monostome of Indian Domestic Fowl with remarks on the genus Notocotylus Diesing 1839. Parasitology 53, 45–48.CrossRefGoogle Scholar

Noble., A. E. (1933). Two new trematodes from the American coot. Transactions of the American microscopical Society 52, 353–360.CrossRefGoogle Scholar

Odening, K. (1964). Zur trematoden fauna von Nettapus C. moromandelianus in Indien. Angewandte Parasitologie 5, 228–241.Google Scholar

Pfunder, M., Holzgang, O. and Frey, J. E. (2004). Development of microarray-based diagnosis of voles and shrews for use in biodiversity monitoring studies, and evaluation of mitochondrial cytochrome oxidase I vs. cytochrome b as genetic markers. Molecular Ecology 13, 1277–1286.CrossRefGoogle Scholar

Pike, A. W. (1969). Observations on the life cycles of Notocotylus triserialis Diesing, 1839, and N. imbricatus (Looss, 1839) sensu Szidat, 1935. Journal of Helminthology 43, 145–165.CrossRefGoogle Scholar

Qiongzhang, L. (1992). A new species and two new records of the genus Notocotylus (Trematoda: Notocotylidae). Acta Veterinaria et Zootechnica Sinica 23, 262–266.Google Scholar

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

Sargent, G. and Morris, P. (2003). How to find and identify Mammals. The Mammal Society, London, UK.Google Scholar

Shaldybin, L. S. (1965). A new trematode of Clethrionomys glareolus. Gelmintologia Sbornik 4, 93–105 (in Russian).Google Scholar

Simon-Vicente, F., Mas-Coma, S., Lopez-Roman, R., Tenora, F. and Gallego, J. (1985 a). Review of Notocotylus species (Trematoda: Notocotylidae) parasitizing rodents in Europe. Folia Parasitologica (Praha) 32, 21–33.Google Scholar

Simon-Vicente, F., Mas-Coma, S., Lopez-Roman, R., Tenora, F. and Gallego, J. (1985 b). Biology of Notocotylus neyrai Gonzalez-Castro, 1945 (Trematoda). Folia Parasitologica (Praha) 32, 101–111.Google Scholar

Singh, K. S. (1954). Some trematodes collected in India. Transactions of the American Microscopical Society 73, 202–210.CrossRefGoogle Scholar

Skrjabin, K. I. (1953). Trematodes of Animal and Man, Principles of Trematodology Vol. 8. Publishing House of the USSR Academy of Science, Moscow, USSR.Google Scholar

Stunkard, H. W. (1960). Studies on the morphology and life history of Notocotylus minutus n. sp. a digenetic trematode from ducks. Journal of Parasitology 46, 803–809.CrossRefGoogle Scholar

Stunkard, H. W. (1966). The morphology and life-history of Notocotylus atlanticus n. sp. A digenetic trematode of eider ducks, Somateria mollissima and the designation Notocotylus duboisi nom. nov for Notocotylus imbricatus (Looss, 1839) Szidat, 1935. The Biological Bulletin 131, 501–515.CrossRefGoogle Scholar

Stunkard, H. W. (1967). The morphology, life history, and systematic relations of the digenetic trematode, Uniserialis breviserialis sp. nov., (Notocotylidae), a parasite of the bursa fabricius of birds. The Biological Bulletin 132, 266–276.CrossRefGoogle ScholarPubMed

Sutton, R. and Shorrock, B. (2008). Checklist of the Birds of Malham Tarn. Malham Tarn Field Centre, UK.Google Scholar

Tenora, F., Henttonen, H. and Haukisalmi, V. (1983). On helminths of rodents in Finland. Annales Zoologici Fennici 20, 37–45.Google Scholar

Thomasson, D., Wright, E. A., Hughes, J. M., Dodd, N. S., Cox, A. P., Boyce, K., Gerwash, O., Abushahma, M., Lun, Z. R., Murphy, R. G., Rogan, M. T. and Hide, G. (2011). Prevalence and co-infection of Toxoplasma gondii and Neospora caninum in Apodemus sylvaticus in an area relatively free of cats. Parasitology 138, 1117–1123.CrossRefGoogle Scholar

Tkach, V., Pawlowski, J. and Mariaux, J. (2000 b). Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal for Parasitology 30, 83–93.CrossRefGoogle ScholarPubMed

Tkach, V., Pawlowski, J., Mariaux, J. and Swiderski, Z. (2001). Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In Interrelationships of the Platyhelminthes (ed. Littlewood, D. T. J. and Bray, R. A.), pp. 186–193. Systematics Association Special Publication, Taylor & Francis, London, UK.Google Scholar

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

Tubangui, M. A. (1932). Trematode parasites of Philippine vertebrates. V. Flukes from birds. Philippine Journal of Science 47, 369–404.Google Scholar

Vassilev, I. and Kanev, I. (1984). Morphology and biology of Notocotylus zduni Chiaberachvili and Djavelidze 1966 in Bulgaria. In Faunae, Taxonomy and Ecology of Helminths on Birds (ed. Vassilev, I.), pp. 66–74. Publishing House of the Bulgarian Academy of Sciences: Sofia.Google Scholar

Webber, R. A., Rau, M. E. and Lewis, D. J. (1987). The effects of Plagiorchis noblei (Trematoda: Plagiorchiidae) metacercariae on the susceptibility of Aedes aegypti larvae to predation by guppies (Poecilia reticulata) and meadow voles (Microtus pennsylvanicus). Canadian Journal of Zoology 65, 2346–2348.CrossRefGoogle Scholar

Yamaguti, S. (1934). Studies on the helminth fauna of Japan. Part 3. Avian trematodes II. Japanese Journal of Zoology 5, 543–583.Google Scholar

Yamaguti, S. (1958). Systema helminthum, Vol. 1, Parts 1 and 2. Digenetic Trematodes of Vertebrates. Interscience Publishers, New York, USA and London, UK.Google Scholar