Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 4514 No. 1: 6 Nov. 2018
Type: Article
Published: 2018-11-05
DOI: 10.11646/zootaxa.4514.1.5
Page range: 65–76
Abstract views: 82
PDF downloaded: 99

Description of Enterobius (Colobenterobius) emodensis sp. n. (Nematoda: Oxyuridae) collected from Central Himalayan langur, Semnopithecus schistaceus, in Uttarakhand, India

Department of Biomedicine / Department of Infectious Disease Control, Faculty of Medicine, Oita University, Hasama, Yufu, Oita 879–5593, Japan.
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido 078-8510, Japan.
Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
Nematoda Pinworm Primates Coevolution Phylogeny Cox1

Abstract

A new pinworm species, Enterobius (Colobenterobius) emodensis sp. n. (Nematoda: Oxyuridae) is described from the Central Himalayan langur, Semnopithecus schistaceus, in Mandal Valley, Chamoli District, Uttarakhand, India, based on mature and immature adults and fourth-stage larvae. This species closely resembles Enterobius (Colobenterobius) zakiri parasitic in Tarai langur, Semnopithecus hector, recorded from Uttarakhand and Uttar Pradesh, India, but is readily distinguished by having a shorter esophagus and a shorter spicule. It is surmised that this pinworm has co-speciated with the host langur. The new species is also characterized in that the posterior 1/3 of the esophageal corpus is much darker. Phylogenetic analysis based on the sequences of partial Cox1 gene of mtDNA suggested a basal position of diversification of Colobenterobius from the Enterobius lineage.

 

References

  1. Ashalakshmi, N.C., Chetan Nag, K.S. & Karanth, K.P. (2014) Molecules support morphology: species status of South Indian populations of the widely distributed Hanuman langur. Conservation Genetics, 16, 43–58.
    https://doi.org/10.1007/s10592-014-0638-4

    Brooks, D.R. & Glen, D.R. (1982) Pinworms and primates: a case study in coevolution. Proceedings of the Helminthological Society of Washington, 49, 76–85.

    Cameron, T.W.M. (1929) The species of Enterobius Leach, in primates. Journal of Helminthology, 7, 161–182.
    https://doi.org/10.1017/S0022149X00018770

    Chabaud, A.G. (1974) No. 1. Keys to Subclass, Orders and Superfamilies. In: Anderson, S.R., Chabaud, A.G. & Willmott, S. (Eds.), CIH Keys to the Nematode Parasites of Vertebrates. Commonwealth Agricultural Bureaux, Farnham Royal, Buckinghamshire, pp. 6–17.

    Felsenstein, J. (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791.
    https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    Floyd, R.M., Rogers, A.D., Lambshead, P.J.D. & Smith, C.R. (2005) Nematode-specific PCR primers for the 18S small subunit rRNA gene. Molecular Ecology Notes, 5, 611–612.
    https://doi.org/10.1111/j.1471-8286.2005.01009.x

    Hasegawa, H. (2009) Methods of collection and identification of minute nematodes from the feces of primates, with special application to coevolutionary study of pinworms. In: Huffman. M.H. & Chapman, C.A. (Eds.), Primate Parasite Ecology. Cambridge University Press, Cambridge, pp. 29–46.

    Hasegawa, H., Murata, K. & Asakawa, M. (2002) Enterobius (Colobenterobius) pygatrichus sp. n. (Nematoda: Oxyuridae) collected from a golden monkey Pygathrix roxellana (Milne-Edwards, 1870) (Primates: Cercopithecidae: Colobinae). Comparative Parasitology, 69, 62–65.
    https://doi.org/10.1654/1525-2647(2002)069[0062:ECPSNN]2.0.CO;2

    Hasegawa, H., Matsuo, K. & Onuma, M. (2003) Enterobius (Colobenterobius) serratus sp. nov. (Nematoda: Oxyuridae) from the proboscis monkey, Nasalis larvatus (Wurmb, 1787) (Primates: Cercopithecidae: Colobinae), in Sarawak, Borneo, Malaysia. Comparative Parasitology, 70, 128–131.
    https://doi.org/10.1654/4078

    Hasegawa, H., Greiner, E.C. & Gillespie, T.R. (2008) Morphology of Enterobius (Colobenterobius) colobis Vuylstéke, 1964 (Nematoda: Oxyuridae: Enterobiinae) collected from an ashy red colobus, Procolobus rufomitratus tephrosceles (Elliot, 1907) (Primates: Cercopithecidae: Colobinae) in Uganda. Journal of Parasitology, 94, 1082–1086.
    https://doi.org/10.1645/GE-1442.1

    Hugot, J.P. (1984) Etude morphologique de Zenkoxyuris mabokensis (Oxyuridae: Nematoda) parasite de Zenkerella insignis (Anomaluridae, Rongeur). Systematic Parasitology, 6, 131–137.
    https://doi.org/10.1007/BF02185520

    Hugot, J.P. (1986) Etude morphologique d’Helminthoxys urichi (Oxyurata, Nematoda) parasite de Dasyprocta aguti (Caviomorpha, Rodentia). Bulletin du Muséum National d’Histoire Naturelle, Paris, 4éme Série, 8, Section A, no 1, 133–138.

    Hugot, J.P. (1987a) Sur le genre Enterobius (Oxyuridae, Nematoda): s. g. Colobenterobius. I. Parasites de primates Colobinae en région éthiopienne. Bulletin du Muséum National d’Histoire Naturelle, Paris, 4éme Série, 9, Section A, no 2, 341–352.

    Hugot, J.P. (1987b) Sur le genre Enterobius (Oxyuridae, Nematoda): s. g. Colobenterobius. II. Parasites de primates Colobinae en région orientale. Bulletin du Muséum National d’Histoire Naturelle, Paris, 4éme Série, 9, Section A, no 4, 799–813.

    Hugot, J.P. (1999) Primates and their pinworm parasites: The Cameron hypothesis revisited. Systematic Biology, 48, 523–546.
    https://doi.org/10.1080/106351599260120

    Hugot, J.P., Gardner, S.L. & Morand, S. (1996) The Enterobiinae subfam. nov. (Nematoda, Oxyurida) pinworm parasites of primates and rodents. International Journal for Parasitology, 26, 147–159.
    https://doi.org/10.1016/0020-7519(95)00108-5

    IUCN (2017) The IUCN Red List of Threatened Species. 2017–3. Available from http://www.iucnredlist.org/details/39840/0 (accessed 30 June 2018)

    Katayama, T., Yamamoto, H., Wada, H. & Satoh, N. (1993) Phylogenetic position of acoel turbellarians inferred from partial 18S rDNA sequences. Zoological Science, 10, 529–36.

    Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
    https://doi.org/10.1007/BF01731581

    Kuze, N., Kanamori, T., Peter Malim, T., Bernard, H., Zamma, K., Kooriyama, T., Morimoto, A. & Hasegawa, H. (2010) Parasites found from the feces of Bornean orangutans in Danum Valley, Sabah, Malaysia, with a redescription of Pongobius hugoti and the description of a new species of Pongobius (Nematoda: Oxyuridae). Journal of Parasitology, 96, 954–960.
    https://doi.org/10.1645/GE-2379.1

    Osterholtz, M., Walter, L. & Roos, C. (2008) Phylogenetic position of the langur genera Semnopithecus and Trachypithecus among Asian colobines, and genus affiliations of their species groups. BMC Evolutionary Biology, 8, 58.
    https://doi.org/10.1186/1471-2148-8-58

    Petter, A.J. & Quentin, J.C. (1976) No. 4. Keys to Genera of the Oxyuroidea. In: Anderson, S.R., Chabaud, A.G. & Willmott, S. (Eds.), CIH Keys to the Nematode Parasites of Vertebrates. Commonwealth Agricultural Bureaux, Farnham Royal, Buckinghamshire, pp. 1–30.

    Quentin, J.C., Betterton, C. & Krishnasamy, M. (1979) Oxyures nouveaux ou peu connus, parasites de primates de rongeurs et de dermoptères en Malaisie. Création du sous-genre Colobenterobius n. subgen. Bulletin du Muséum National d’Histoire Naturelle, Paris, Série 4 (Zoologie), 1, 1031–1050.

    Saitou, N. & Nei, M. (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.

    Siddiqi, A.H. & Mirza, M.B. (1954) On a new oxyurid worm, Enterobius zakiri n. sp. from the rectum of Semnopithecus entellus schistaceus (Tarai langur). Indian Journal of Helminthology, 6, 24–26.

    Springer, M.S., Meredith, R.W., Gatesy, J., Emerling, C.A., Park, J., Rabosky, D.L., Stadler, T., Steiner, C., Ryder, O.A., Janečka, J.E., Fisher, C.A., William J. & Murphy, W.J. (2012) Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLoS ONE, 7 (11), e49521.
    https://doi.org/10.1371/journal.pone.0049521

    Stevens N.J., Seiffert E.R., O’Connor, P.M., Roberts, E.M., Schmitz, M.D., Krause, C., Gorscak, E., Ngasala S., Hieronymus, T.L. & Temu, J. (2013) Palaeontological evidence for an Oligocene divergence between Old World monkeys and apes. Nature, 497, 611–614.
    https://doi.org/10.1038/nature12161

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
    https://doi.org/10.1093/molbev/mst197

    Vuylstéke, C. (1964) Mission de zoologie médicale au Maniema (Congo Léopoldville). 3. Vermes—Nématoda. Annales du Musée Royal de l’Afrique Centrale, en-8°, Zoologie, 132, 41–66.

    Wahid, S. (1961) On two new species of the genus Enterobius Leach, 1853, from a Colobus monkey. Journal of Helminthology, 35, 345–352.
    https://doi.org/10.1017/S0022149X00004727

    Wilkinson, R.D., Steiper, M.E., Soligo, C., Martin, R.D., Yang, Z. & Tavaré, S. (2011) Dating primate divergences through an integrated analysis of paleontological and molecular data. Systematic Biology, 60,16–31.
    https://doi.org/10.1093/sysbio/syq054

    Wilson, D.E. & Reeder, D.M. (2005) Mammal Species of the World. 3rd Edition. Johns Hopkins University Press, Baltimore, Maryland, 2142 pp.