Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-19T12:00:15.665Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasitic nematodes of the genus Syphacia Seurat, 1916 infecting Muridae in the British Isles, and the peculiar case of Syphacia frederici

Published online by Cambridge University Press:  23 August 2017

ALEX STEWART ,
ANN LOWE ,
LESLEY SMALES ,
ANNA BAJER ,
JAN BRADLEY ,
DOROTA DWUŻNIK ,
FRITS FRANSSEN ,
JACK GRIFFITH ,
PETER STUART  and
CYAN TURNER
...Show all authors
ALEX STEWART
Affiliation:
Faculty of Health and Medical Sciences, University of Surrey, Guildford GU2 7XH, UK
ANN LOWE
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
LESLEY SMALES
Affiliation:
Parasitology Section, South Australian Museum, North Terrace, Adelaide 5000, Australia
ANNA BAJER
Affiliation:
Department of Parasitology, Institute of Zoology, Faculty of Biology, University of Warsaw, 1 Miecznikowa Street, Warsaw 02-096, Poland
JAN BRADLEY
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
DOROTA DWUŻNIK
Affiliation:
Department of Parasitology, Institute of Zoology, Faculty of Biology, University of Warsaw, 1 Miecznikowa Street, Warsaw 02-096, Poland
FRITS FRANSSEN
Affiliation:
National Reference Laboratory for Parasites, National Institute for Public Health and Environment (RIVM), Laboratory for Zoonoses and Environmental Microbiology Antonie van Leeuwenhoeklaan 9, Bilthoven 3721 MA, The Netherlands
JACK GRIFFITH
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
PETER STUART
Affiliation:
Department of Zoology, School of Natural Sciences, Trinity College Dublin, Ireland
CYAN TURNER
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
GRZEGORZ ZALEŚNY
Affiliation:
Department of Invertebrate Systematics and Ecology, Wrocław University of Environmental and Life Sciences, Kożuchowska 5B, Wrocław 51-631, Poland
JERZY M. BEHNKE*
Affiliation:
School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
*
*Corresponding author: School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK. E-mail: jerzy.behnke@nottingham.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Syphacia stroma (von Linstow, 1884) Morgan, 1932 and Syphacia frederici Roman, 1945 are oxyurid nematodes that parasitize two murid rodents, Apodemus sylvaticus and Apodemus flavicollis, on the European mainland. Only S. stroma has been recorded previously in Apodemus spp. from the British Isles. Despite the paucity of earlier reports, we identified S. frederici in four disparate British sites, two in Nottinghamshire, one each in Berkshire and Anglesey, Wales. Identification was based on their site in the host (caecum and not small intestine), on key morphological criteria that differentiate this species from S. stroma (in particular the tail of female worms) and by sequencing two genetic loci (cytochrome C oxidase 1 gene and a section of ribosomal DNA). Sequences derived from both genetic loci of putative British S. frederici isolates formed a tight clade with sequences from continental worms known to be S. frederici, clearly distinguishing these isolates from S. stroma which formed a tight clade of its own, distinct from clades representative of Syphacia obvelata from Mus and S. muris from Rattus. The data in this paper therefore constitute the first record of S. frederici from British wood mice, and confirm the status of this species as distinct from both S. obvelata and S. stroma.

Keywords

Syphacia fredericiSyphacia stromaSyphacia obvelataSyphacia murisoxyurid nematodesApodemus sylvaticusApodemus flavicollis
Type
Research Article
Information
Parasitology , Volume 145 , Issue 3 , March 2018 , pp. 269 - 280
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel-Gaber, R. (2016). Syphacia obvelata (Nematode Oxyuridae) infecting laboratory mice Mus musculus (Rodentia, Muridae):phylogeny and host-parasite relationship. Parasitology Research 115, 975–985.CrossRefGoogle ScholarPubMed
Abu-Madi, M. A., Behnke, J. M., Lewis, J. W. and Gilbert, F. S. (1998). Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 72, 93–100.CrossRefGoogle 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, 7–16.CrossRefGoogle ScholarPubMed
Adamson, M. (1994). Evolutionary patterns in the life histories of Oxyurida. International Journal for Parasitology 24, 1167–1177.CrossRefGoogle ScholarPubMed
Araujo, S. B. L., Braga, M. P., Brooks, D. R., Agosta, S. J., Hoberg, E. P., von Hartenthal, F. W. and Boeger, W. A. (2015). Understanding host-switching by ecological fitting. PLoS ONE 10, 1371.CrossRefGoogle ScholarPubMed
Baruš, V., Tenora, F. and Wiger, R. (1979). Scanning electron microscopy of eggs of European species of the genus Syphacia Seurat, 1916 (Nematoda). Folia Parasitologica 26, 21–26.Google 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
Behnke, J. M., Stewart, A., Bajer, A., Grzybek, M., Harris, P. D., Lowe, A., Ribas, A., Smales, L. and Vandegrift, K. J. (2015). Bank voles (Myodes glareolus) and house mice (Mus musculus/domesticus) in Europe are each parasitized by their own distinct species of Aspiculuris . Parasitology 142, 1493–1505.CrossRefGoogle ScholarPubMed
Bernard, J. (1966). Les Syphacia spp. parasites des rongeurs de la fauna belge: Syphacia vandenbrueli de Micromys minutus Pal. Bulletin de Recherche Agronomiques de Gembloux 1, 345–358.Google Scholar
Berry, R. J. (1973). Chance and change in British long-tailed field mice. Journal of Zoology 170, 351–366.CrossRefGoogle Scholar
Cable, J., Harris, P. D., Lewis, J. W. and Behnke, J. M. (2006). Molecular evidence that Heligmosomoides polygyrus from laboratory mice and wood mice are separate species. Parasitology 133, 111–122.CrossRefGoogle ScholarPubMed
Čabrilo, B., Jovanović, V. M., Bjelić-Čabrilo, O., Budinski, I., Blagojević, J. and Vujošević, M. (2016). Diversity of nematodes in the yellow-necked field mouse Apodemus sylvaticus from the Peripannonic region of Serbia. Journal of Helminthology 90, 14–20.CrossRefGoogle Scholar
Canning, E. U., Cox, F. E. G., Croll, N. A. and Lyons, K. M. (1973). The natural history of Slapton Ley Nature Reserve: VI Studies on the parasites. Field Studies 3, 681–718.Google Scholar
Chabaud, A. G., Rausch, R. L. and Desset, M. C. (1963). Nèmatodes parasites de rongeurs et insectivores japonais. Bulletin de la Société Zoologique de France 88, 489–512.Google Scholar
Cobbold, T. S. (1864). Entozoa: An Introduction to the Study of Helminthology, with References More Particularly to the Internal Parasites of Man. Groombridge, London, UK, p. 480.Google Scholar
Dewi, K., Mitsuhiko, A. and Fitrana, Y. S. (2014). Syphacia (Syphacia) semiadii n. sp. (Nematoda: Oxyuridae) from Halmaheramys bokimekot Fabre et al., 2013 (Rodentia: Muridae) on Halmahera Island Indonesia and a key to the species present in Sulawesi and the Australian Bioregion. Transactions of the Royal Society of South Australia 138, 98–104.CrossRefGoogle Scholar
Eira, C., Torres, J., Vingada, J. and Miquel, J. (2006). Ecological aspects influencing the helminth community of the wood mouse Apodemus sylvaticus in Dunas de Mira, Portugal. Acta Parasitologica 51, 300–308.CrossRefGoogle Scholar
Elton, C., Ford, E. B., Baker, J. R. and Gardiner, A. D. (1931). The health and parasites of a wild mouse population. Proceedings of the Zoological Society of London 1931, 657–721.CrossRefGoogle Scholar
Franssen, F., Swart, A., van Knapen, F. and van der Giessen, J. (2016). Helminth parasites in black rats (Rattus rattus) and brown rats (Rattus norvegicus) from different environments in the Netherlands. Infection Ecology and Epidemiology 6, 31413.CrossRefGoogle Scholar
Grear, D. and Hudson, P. (2011). The dynamics of macroparasite host-self-infection: a study of the patterns and processes of pinworm (Oxyuridae) aggregation. Parasitology 138, 619–627.CrossRefGoogle ScholarPubMed
Hasegawa, H. (1981). Two nematode species of the genus Syphacia (Oxyuridae) collected from rodents in Niigata Prefecture, Japan. Japanese Journal of Parasitology 30, 325–329.Google Scholar
Hasegawa, H. (1991). Syphacia (Syphacia) ohtaorum n. sp. (Nematoda: Oxyuridae) from Mus caroli on Okinawa Island, Japan. Systematic Parasitology 18, 221–226.CrossRefGoogle Scholar
Hasegawa, H., Asakawa, M., Yagi, K. and Takao, Y. (1994). Descriptions of three species of the genus Syphacia (Nematoda: Oxyuridae from the murids of Japan. Biological Magazine of Okinawa 32, 7–15.Google Scholar
Hasegawa, H. and Tarore, D. (1996). Syphacia (Syphacia) sulawesiensis n. sp. and S. (S.) muris (Yamaguti 1935) (Nematoda Oxyuridae) collected from Rattus xanthurus (Gray 1867) (Rodentia Muridae) in North Sulawesi, Indonesia. Tropical Zoology 9, 165–173.CrossRefGoogle Scholar
Hugot, J. P. (1988). Les nématodes Syphaciinae, parasites de Rongeurs et de Lagomorphes. Taxonomie, Zoogéographie, Évolution. Mémoires du Muséum National d'Histoire, Paris Ser. A Zoologie 141, 1–153.Google Scholar
Hussey, K. L. (1957). Syphacia muris vs S. obvelata in laboratory rats and mice. Journal of Parasitology 43, 555–559.CrossRefGoogle Scholar
Kerboeuf, D. and Lewis, J. W. (1987). Rhythmic behaviour of intestinal helminths in rodents. Mammal Review 17, 127–134.CrossRefGoogle Scholar
Khera, S. (1956). Nematode parasites of some Indian vertebrates. Indian Journal of Helminthology 6, 27–133.Google Scholar
Lewis, J. W. (1968). Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology, London 154, 287–312.CrossRefGoogle Scholar
Lewis, J. W. (1987). Helminth parasites of British rodents and insectivores. Mammal Review 17, 81–93.CrossRefGoogle Scholar
Lewis, J. W. and D'Silva, J. (1986). The life-cycle of Syphacia muris Yamaguti (Nematoda:Oxyuroidea) in the laboratory rat. Journal of Helminthology 60, 39–46.CrossRefGoogle ScholarPubMed
Loxton, K. C., Lawton, C., Stafford, P. and Holland, C. V. (2016). Reduced helminth parasitism in the introduced bank vole (Myodes glareolus): more parasites lost than gained. International Journal for Parasitology: Parasites and Wildlife 5, 175–183.Google ScholarPubMed
Meade, T. M. and Watson, J. (2014). Characterization of rat pinworm (Syphacia muris) epidemiology as a means to increase detection and elimination. Journal of the American Association for Laboratory Animal Science 53, 661–667.Google ScholarPubMed
Mészáros, F. and Murai, E. (1979). Contribution to the knowledge of helminths of rodents in Roumania. Parasitologia Hungarica 12, 55–70.Google Scholar
Michaux, J., Reyes, A. and Catzeflis, F. (2001). Evolutionary history of the most speciose mammals: molecular phylogeny of muroid rodents. Molecular Biology and Evolution 18, 2017–2031.CrossRefGoogle ScholarPubMed
Milazzo, C., Di Bella, C., Casanova, J. C., Ribas, A. and Cagnin, M. (2010). Helminth communities of wood mice (Apodemus sylvaticus) on the river Avena (Calabria, Southern Italy). Hystrix, the Italian Journal of Mammology 21, 171–176.Google Scholar
Montgomery, S. S. J. and Montgomery, W. I. (1990). Structure, stability and species interactions in helminth communities of wood mice Apodemus sylvaticus . International Journal for Parasitology 20, 225–242.CrossRefGoogle ScholarPubMed
Montgomery, W. I., Provan, J., McCabe, A. M. and Yalden, D. W. (2014). Origin of British and Irish mammals: disparate post- glacial colonisation and species introductions. Quaternary Science Reviews 98, 144–165.CrossRefGoogle Scholar
Morgan, D. O. (1932). Oxyuris stroma Linstow, 1886. Journal of Helminthology 10, 15–20.CrossRefGoogle Scholar
Murúa, R. E. (1978). Studies on the ecology of parasites of Apodemus sylvaticus (L.) and Clethrionomys glareolus (Schreb.)(Rodentia): analysis of the parasite populations and their seasonal variation in the Bristol area. Acta Parasitologica Polonica 25, 149–161.Google Scholar
Newton, L. A., Chilton, N. B., Beveridge, I., Hoste, H., Nansen, P. and Gasser, R. B. (1998). Genetic markers for strongylid nematodes of livestock defined by PCR-based restriction analysis of the spacer rDNA. Acta Tropica. 69, 1–15.CrossRefGoogle ScholarPubMed
Nieberding, C., Libois, R., Douady, C. J., Morand, S. and Michaux, J. R. (2005). Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palearctic region: persistence of northern cryptic populations during ice ages? Molecular Ecology 14, 765–779.CrossRefGoogle ScholarPubMed
Ogden, C. G. (1971). Observations on the systematics of nematodes belonging to the genus Syphacia Seurat, 1916. Bulletin of the British Museum of Natural History. (Zool.) 20, 253–280.Google Scholar
Okamoto, M., Urushima, H., Iwasa, M. and Hasegawa, H. (2007). Phylogenetic relationships of rodent pinworms (genus Syphacia) in Japan inferred from mitochondrial CO1 gene sequences. Journal of Veterinary Medical Science 69, 545–547.CrossRefGoogle ScholarPubMed
Parel, J. D., Galula, J. U. and Ooi, H. K. (2008). Characterization of rDNA sequences from Syphacia obvelata, Syphacia muris, and Aspiculuris tetraptera and development of a PCR-based method for identification. Veterinary Parasitology 153, 379–383.CrossRefGoogle ScholarPubMed
Quentin, J. C. (1971). Morphologie comparée des structures céphaliques et génitales des oxyures du genre Syphacia . Annales de Parasitologie 46, 15–60.Google ScholarPubMed
Rojas, H., Elba, J., Mino, H., Notarnicola, M. and del Rosario Robles, M. (2011). A new species of Syphacia (Nematoda: Oxyuridae) from Calomys laucha (Rodentia: Cricetidae) in an agroecosystem of Central Argentina. Journal of Parasitology 97, 676–681.Google Scholar
Roman, E. (1945). Spécificité parasitaire des Oxyurides du genre Syphacia chez les rats de l'Europe occidentale. Annales de Parasitology 20, 297–298.Google Scholar
Roman, E. (1951). Etude éclogique et morphologique sur les acanthocéphales et les nématodes parasites des rats de la région lyonnaise. Mémoires du Muséum National d'Histoire Naturelle (Serie A. Zoologie) 2, 49–270.Google Scholar
Ryzhikov, K. M., Gvozdev, E. V., Tokobaev, M. M., Shaldybin, L. S., Matsaberidze, G. V., Merkusheva, I. V., Nadtochi, E. V., Khokhlova, I. G. and Sharpilo, L. D. (1979). Keys to the rodent helminth fauna of the USSR. Nematodes and Acanthocephalans. Academy of Science of the USSR. Helminth Laboratory. Izdatel'stvo Nauka, Moscow. pp. 157–179 (in Russian).Google Scholar
Rudolphi, C. A. (1802). Forsetzung der Beobachtungen über die Eingeweide würmer. Archiv fur Zoologie und Zootomie von Wiedemanns 2, 1–67.Google Scholar
Seurat, L. G. (1915). Sur deux nouveaux oxyures du Maroc. Bulletin de la Société d'Histoire Naturelle de l'Afrique du Nord 7, 24–31.Google Scholar
Seurat, L. G. (1916). Sur les Oxyures des mammiferes. Comptes Rendus des Séances de la Société de Biologie et de ses Filiales 79, 64–68.Google Scholar
Sharpe, G. I. (1964). The helminth parasites of some small mammal communities. I. The parasites and their hosts. Parasitology 54, 145–154.CrossRefGoogle ScholarPubMed
Sharpilo, L. D. (1973). Predstavitěli roda Syphacia (Nematoda, Syphaciidae), v fauně USSR. Vestnik Zoologii 5, 59–65 (in Russian).Google Scholar
Smales, L. R. (2011). Gastrointestinal nematodes of Coccymys ruemmleri (Rodentia, Muridae) with the description of Montistrongylus giluwensis sp. nov. (Heligmonellidae) and Syphacia coccymyos sp. nov. (Oxyuridae) from Papua New Guinea. Acta Parasitologica 56, 418–426.CrossRefGoogle Scholar
Taffs, L. F. (1976). Pinworm infections in laboratory rodents: a review. Laboratory Animals 10, 1–13.CrossRefGoogle ScholarPubMed
Tenora, F. and Meszaros, F. (1975). Nematodes of the genus Syphacia, Seurat, 1916 (Nematoda) – parasites of rodents (Rodentia) in Czechoslovakia and Hungary. Acta Universitatis Agriculturae, Brno 23, 537–554.Google Scholar
Tenora, F., Quentin, J. C. and Durette-Desset, M.-C. (1974). Some new findings of nematodes of the families Oxyuridae and Heligmosomidae (Nematoda) in Czechoslovakia and Poland. Vĕstnik Československé Společnosti Zoologické 38, 71–75.Google Scholar
Thomas, R. J. (1953). On the nematode and trematode parasites of some small mammals from the Inner Hebrides. Journal of Helminthology 27, 143–168.CrossRefGoogle Scholar
Tiner, J. D. (1948). Syphacia eutamii n.sp. from the least Chipmunk, Eutamias minimus, with a key to the genus (Nematoda: Oxyuridae). Journal of Parasitology 34, 87–92.CrossRefGoogle Scholar
von Linstow, O. (1884). Helminthologisches. Archiv fur Naturgeschichte 50, 125–145.Google Scholar
Weaver, H. J. and Smales, L. R. (2010). Three new species of Syphacia (Syphacia) (Oxyurida: Oxyuridae) from Queensland Australia, and a key to the species present in the Australian bioregion. Comparative Parasitology 77, 9–19.Google Scholar
Weaver, H. J., Monks, S. and Gardner, S. L. (2016). Phylogeny and biogeography of species of Syphacia Seurat 1916 (Nematoda: Oxyurida: Oxyuridae) from the Australian bioregion. Australian Journal of Zoology 64, 81–90.CrossRefGoogle Scholar
Wiger, R., Baruš, V. and Tenora, F. (1978). Scanning electron microscopical studies on four species of the genus Syphacia (Nematoda, Oxyuridae). Zoologica Scripta 7, 25–31.CrossRefGoogle Scholar
Yalden, D. W. (1999). The History of the British Mammals. Poyser Natural History, London, UK.Google Scholar
Yamaguti, S. (1935). Studies on the helminth fauna of Japan. Part 13. Mammalian Nematodes. Japanese Journal of Zoology 6, 433–457.Google Scholar
Zaleśny, G., Hildebrand, J., Paziewska-Harris, A., Behnke, J. M. and Harris, P. D. (2014). Heligmosomoides neopolygyrus Asakawa & Ohbayashi,1986, a cryptic Asian nematode infecting the striped field mouse Apodemus agrarius in Central Europe. Parasites and Vectors 7, 457.CrossRefGoogle ScholarPubMed