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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)

Published online by Cambridge University Press:  19 July 2012

K. BOYCE
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
G. HIDE
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
P. S. CRAIG
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
P. D. HARRIS
Affiliation:
National Centre for Biosystematics, Natural History Museum, University of Oslo, PO Box 1172, N-0318, Oslo, Norway
C. REYNOLDS
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
A. PICKLES
Affiliation:
Field Studies Council at Malham Tarn Field Centre, North Yorkshire BD24 9PU
M. T. ROGAN*
Affiliation:
Centre for Parasitology and Disease Research, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK
*
*Corresponding author: Centre for Parasitology and Disease, School of Environment and Life Sciences, University of Salford, Salford M5 4WT, UK. Tel: 0044 161 295 4083. Fax: 0044 161 295 5015. E-mail: m.t.rogan@salford.ac.uk

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.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Ablasov, N. A. and Iksanov, K. I. (1958). Trematode fauna of piscivorous birds of Kirgizia. Rab. Gelm. 80-let. Skrjabin. Izd. AN SSSR, Moskva, 15–22 (in Russian).Google Scholar
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, 715.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, 289294.CrossRefGoogle ScholarPubMed
Barker, F. D. (1915). Parasites of the American Muskrat (Fiber zibethicus). Journal of Parasitology 1, 184197.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. 383396. 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, 582585.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, 329343.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, 474477.CrossRefGoogle Scholar
Baylis, H. A. (1939). Further records of Parasitic Worms from British Vertebrates. The Annals and Magazine of Natural History, 11th Series 23, 473798.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, 793804.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, 3144.CrossRefGoogle ScholarPubMed
Beverley-Burton, M. (1961). Studies on the trematoda of British freshwater birds. Proceedings of the Zoological Society of London 137, 1339.CrossRefGoogle Scholar
Beverley-Burton, M. (1972). Helminths from wild Anatids in Great Britain. Journal of Helminthology 46, 345355.CrossRefGoogle ScholarPubMed
Bhalerao, G. D. (1935). On two new monostomes (Trematoda) from avian hosts in British India. Indian Journal of Veterinary Science and Animal Husbandry 5, 4963.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, 365372.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, 6365.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, 3538.CrossRefGoogle Scholar
Cribb, T. H. (1991). Notocotylidae (Digenea) from the Australian water rat Hydromys chrysogaster Geoffroy, 1804 (Muridae). Systematic Parasitology 18, 227237.CrossRefGoogle Scholar
Deshmukh, A. L. (1985). A new species of Notocotylus (Trematoda: Notocotylidae) from a Cattle Egret, Bubulcus ibis. Indian Journal of Parasitology 9, 251252.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, 4276.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, 251255.Google Scholar
Duthoit, C. M. G. (1931). A new species of the trematode genus Notocotylus. Annals and Magazine of Natural History 7, 290293.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, 247252.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, 657721.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, 207214.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. 99108. 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, 14.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, 133135.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, 2735.Google Scholar
Gupta, P. D. (1970). Fauna of Rajastan, India. Part 8. Trematoda. Records of the Zoological Survey of India 62, 171190.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, 1326.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, 242243.CrossRefGoogle ScholarPubMed
Harrah, E. C. (1922). Notocotylus urbanensis. North American monostomes primarily from freshwater hosts. Illinois Biological monographs 7, 5153.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, 421437.Google Scholar
Herber, E. C. (1942). Life history studies of two trematodes of the sub family Notocotylinae. Journal of Parasitology 28, 179196.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, 255260.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, 2936.CrossRefGoogle ScholarPubMed
Hsu, P. K. (1954). A new species of Notocotylus from Canton (Trematoda: Notocotylidae). Acta Zoologica Sinica 6, 117122.Google Scholar
I-ping, S. (1965). On some digenetic trematodes from small mammals including descriptions of two new species. Acta Zootaxonomica Sinica (04). Available internet: http://en.cnki.com.cn/Article_en/CJFDTOTAL-DWFL196504003.htm [Accessed: 31/07/11].Google Scholar
Joyeux, C. H. (1922). Recherches sur les Notocotyles. Bulletin de la Societe de Pathologie Exotique 15, 331339.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, 133148.CrossRefGoogle Scholar
Kinsella, J. M. (1971). Growth, development, and intraspecific variation of Quinqueserialis quinqueserialis (Trematoda: Notocotylidae) in rodent hosts. The Journal of Parasitology 57, 6270.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, 194198.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, 113122.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, 457466.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, 419423.Google Scholar
Lange, R. and Staaland, H. (1970). Adaptations of the caecum-colon structure of rodents. Comparative Biochemistry and Physiology 35, 905919.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, 161166.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, 4548.CrossRefGoogle Scholar
Noble., A. E. (1933). Two new trematodes from the American coot. Transactions of the American microscopical Society 52, 353360.CrossRefGoogle Scholar
Odening, K. (1964). Zur trematoden fauna von Nettapus C. moromandelianus in Indien. Angewandte Parasitologie 5, 228241.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, 12771286.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, 145165.CrossRefGoogle Scholar
Qiongzhang, L. (1988). On the trematode fauna from the domestic geese and ducks in Lianhua County, Jiangxi Province. Chinese Journal of Animal and Veterinary Sciences. http://en.cnki.com.cn/articleen/CJFDTOTAL-XMSY198802013.htmGoogle Scholar
Qiongzhang, L. (1992). A new species and two new records of the genus Notocotylus (Trematoda: Notocotylidae). Acta Veterinaria et Zootechnica Sinica 23, 262266.Google Scholar
Read, C. P. (1951). The crowding effect in tapeworm infections. The Journal of Parasitology 37, 174178.CrossRefGoogle 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, 5762.CrossRefGoogle ScholarPubMed
Rudolphi, C. A. (1809). Entozoorum sive vermium intestinalium historia naturalis, vol 2. Amstelaedami: Sumtibus tabernae librariae et atrium. P328-329. http://www.biodiversitylibrary.org/item/50355#page/334/mode/1upGoogle Scholar
Rudolphi, C. A. (1819). Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Berolini: Sumtibusa Rucker. http://www.archive.org/stream/entozoorumsynops00rudo#page/86/mode/2upCrossRefGoogle Scholar
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, 93105 (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, 2133.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, 101111.Google Scholar
Singh, K. S. (1954). Some trematodes collected in India. Transactions of the American Microscopical Society 73, 202210.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, 803809.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, 501515.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, 266276.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, 3745.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, 11171123.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, 8393.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. 186193. 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, 922.CrossRefGoogle ScholarPubMed
Tubangui, M. A. (1932). Trematode parasites of Philippine vertebrates. V. Flukes from birds. Philippine Journal of Science 47, 369404.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. 6674. 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, 23462348.CrossRefGoogle Scholar
Yamaguti, S. (1934). Studies on the helminth fauna of Japan. Part 3. Avian trematodes II. Japanese Journal of Zoology 5, 543583.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
Ye, Y., Qiu, M., Wen, T., Li, S. and Li, G. (1956). Shanghai mice, a parasitic new species of trematode Notocotylus ratti sp. n. (Trematoda) a description of the form. Available internet: http://wenku.baidu.com/view/54455ec1d5bbfd0a79567383.html [Accessed: 31/07/11] (in Chinese with additional Russian description).Google Scholar