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Chabaudstrongylus ninhae (Trichostrongylidae: Cooperiinae) and Oesophagostomum muntiacum (Chabertiidae: Oesophagostominae) in feral alien Reeves's muntjacs on Izu-Oshima Island, Tokyo, Japan

Published online by Cambridge University Press:  11 April 2019

A. Setsuda ,
E. Kato ,
S. Sakaguchi ,
S. Tamemasa ,
S. Ozawa  and
H. Sato Open the ORCID record for H. Sato [Opens in a new window]
A. Setsuda
Affiliation:
Laboratory of Parasitology, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8515, Japan
E. Kato
Affiliation:
Laboratory of Parasitology, Joint Faculty of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8515, Japan
S. Sakaguchi
Affiliation:
Laboratory of Parasitology, Joint Faculty of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8515, Japan
S. Tamemasa
Affiliation:
Laboratory of Parasitology, Joint Faculty of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8515, Japan
S. Ozawa
Affiliation:
Oshima Park Station, Tokyo Metropolitan Oshima Island Branch Office, 2 Fukuju, Senzu, Oshima-machi, Tokyo 100-0103, Japan
H. Sato*
Affiliation:
Laboratory of Parasitology, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8515, Japan Laboratory of Parasitology, Joint Faculty of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8515, Japan
*
Author for correspondence: H. Sato, Fax: +81-83-933-5902, E-mail: [email protected]
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Abstract

The naturalization of alien Reeves's muntjacs (Muntiacus reevesi) on Izu-Oshima Island, Tokyo, Japan, has proceeded intensively over the last five decades. To clarify whether the gastrointestinal helminths of these animals were brought from their original endemic area or were newly acquired in Japan, 32 Reeves's muntjacs trapped on the island were parasitologically examined. In addition to Gongylonema pulchrum in the oesophagus (34.4% prevalence), Chabaudstrongylus ninhae (Dróżdż, 1967) (Trichostrongylidae: Cooperiinae) and Oesophagostomum muntiacum Jian, 1989 (Chabertiidae: Oesophagostominae) were prevalent in the small (28.1%) and large (46.9%) intestines, respectively. For the first time, these trichostrongylid or chabertiid worms were genetically characterized based on partial nucleotide sequences of the nuclear ribosomal RNA gene (rDNA) and mitochondrial DNA cytochrome c oxidase subunit 1 gene (cox-1), and the phylogenetic relationships with other members of their family were explored. Since these two intestinal nematode species are inherent in muntjacs, this study demonstrates a new distribution of exotic helminth species in Japan in accordance with the naturalization of alien mammalian hosts. The molecular genetic data collected here could assist the taxonomic assessment of morphological variants in different Muntiacus spp. and/or of different geographical origins. Furthermore, our data may help to define the phylogenetic relationships among such isolates.

Keywords

Chabaudstrongylus ninhaecox-1Japan: morphologyMuntiacus reevesiOesophagostomum muntiacumrDNA
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e48
Copyright
Copyright © Cambridge University Press 2019 

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References

Anisimova, M and Gascuel, O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539–552.Google Scholar
Asada, M (2014) Body weight and reproductive status in Reeves's muntjac for FY2008 to 2012 in Chiba Prefecture, Japan. Report of the Chiba Biodiversity Center 8, 37–40.Google Scholar
Atkinson, IAE (2001) Introduced mammals and models for restoration. Biological Conservation 99, 81–96.Google Scholar
Chabaud, AG and Durette-Desset, MC (1973) Description d'un nouveau Nématode Oesophagostome, parasite d’Hyemoschus au Gabon, et remarques sur le genre Oesophagostomum. Bulletin du Museum National d'Histoire Naturelle, Paris, 3e série, No. 184, Zoologie 123, 1415–1424.Google Scholar
Chapman, N, Harris, S and Stanford, A (1994) Reeves’ muntjac Muntiacus reevesi in Britain: their history, spread, habitat selection, and the role of human intervention in accelerating their dispersal. Mammal Review 24, 113–160.Google Scholar
Chiba Prefectural Office (2013) Control plan of feral alien Reeves's muntjac in Boso Peninsula, Chiba in 2013. 13 pp. Available at https://www.pref.chiba.lg.jp/shizen/choujuu/kyon/documents/kyonkeikaku.pdf (accessed 2 July 2018).Google Scholar
Chiba Prefectural Office (2017) Implementation report of control measures of feral alien Reeves's muntjac in Boso Peninsula, Chiba in 2016. 13 pp. Available at https://www.pref.chiba.lg.jp/shizen/jouhoukoukai/shingikai/shingikai/shizen-choujuu/documents/h29-kyon-shiryou1.pdf (accessed 2 July 2018).Google Scholar
Courchamp, F, Chapuis, JL and Pascal, M (2003) Mammal invaders on islands: impact, control and control impact. Biological Reviews 78, 347–383.Google Scholar
Dereeper, A, Guignon, V, Blanc, G, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36, 465–469.Google Scholar
Dróżdż, J (1965) Studies on helminths and helminthiases in Cervidae. I. Revision of the subfamily Ostertagiinae Sarwar, 1956 and an attempt to explain the phylogenesis of its representatives. Acta Parasitologica Polonica 13, 445–481.Google Scholar
Dróżdż, J (1967) Cooperia ninhae sp. n. (Nematoda: Trichostrongylidae), a parasite of Muntjacus muntjak in Vietnam. Acta Parasitologica Polonica 14, 209–211.Google Scholar
Dróżdż, J (1970) Ashworthius tuyenguangi sp. n. (Nematoda: Trichostrongylidae), from Muntiacus muntjak Zimm. from Vietnam. Acta Parasitologica Polonica 17, 253–258.Google Scholar
Dróżdż, J (1973) Materials contributing to the knowledge of the helminth fauna of Cervus (Russa) unicolor Kerr and Muntjacus muntjak Zimm. of Vietnam, including two new nematode species: Oesophagostomum labiatum sp. n. and Trichocephalus muntjaci sp. n. Acta Parasitologica Polonica 21, 465–477.Google Scholar
Durette-Desset, MC (1983) CIH keys to the nematode parasites of vertebrates. No. 10. Keys to genera of the superfamily Trichostrongyloidea. 86 pp. Farnham Royal, Commonwealth Agricultural Bureaux.Google Scholar
Durette-Desset, MC and Chabaud, AG (1974) Trois nouveax Nématodes parasites du Chevrotain aquatique: Hyemoschus aquaticus au Gabon (collection G. Dubost). Bulletin du Museum National d'Histoire Naturelle, Paris, 3e série, No. 205, Zoologie 135, 75–87.Google Scholar
Durette-Desset, MC and Denké, M (1978) Description de nouveaux Nématodes parasites d'un Lièvre Africain et compléments à l’étude morphologique de quelques Trichostrongylidae. Bulletin du Museum National d'Histoire Naturelle, Paris, 3e série, No. 515, Zoologie 354, 331–347.Google Scholar
Giao, PM, Tuoc, D, Dung, VV, Wikramanayake, ED, Amato, G, Arctander, P and MacKinnon, JR (1998) Description of Muntiacus truongsonensis, a new species of muntjac (Artiodactyla: Muntiacidae) from Central Vietnam, and implications of conservation. Animal Conservation 1, 61–68.Google Scholar
Gibbons, LM and Kan, SKP (1987) Neorhabditostomum yeni n. g., n. sp. (Nematoda, Strongyloidea) from Muntiacus muntjak in Sabah, Malaysia. Systematic Parasitology 9, 173–178.Google Scholar
Gibbons, LM and Khalil, LF (1983) Morphology of the genital cone in the nematode family Trichostrongylidae and its value as a taxonomic character. pp. 261–271 in Stone, AR, Platt, HM and Khalil, LF (Eds) Concepts in nematode systematics. London, Academic Press.Google Scholar
Groves, C and Grubb, P (2011) Ungulate taxonomy. 317 pp. Baltimore, Johns Hopkins University Press.Google Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Jian, S (1989) Description of a new species of parasitic nematode in the muntja (Strongylata: Trichonematidae). Acta Zootaxonomica Sinica 14, 20–23 (in Chinese with English summary).Google Scholar
Li, GG, Zhang, MX, Swa, K, Maung, KW and Quan, RC (2017) Complete mitochondrial genome of the leaf muntjac (Muntiacus putaoensis) and phylogenetics of the genus Muntiacus. Zoological Research 38, 310–316.Google Scholar
Lichtenfels, JR (1980) CIH keys to the Nematode parasites of Vertebrates. No. 7. Keys to genera of the superfamily Strongyloidea. 41 pp. Farnham Royal, Commonwealth Agricultural Bureaux.Google Scholar
Makouloutou, P, Setsuda, A, Yokoyama, M, et al. (2013) Genetic variation of Gongylonema pulchrum from wild animals and cattle in Japan based on ribosomal RNA and mitochondrial cytochrome c oxidase subunit I genes. Journal of Helminthology 87, 326–335.Google Scholar
Newton, LA, Chilton, NB, Beveridge, I and Gasser, RB (1998) Systematic relationships of some members of the genera Oesophagostomum and Chabertia (Nematoda: Chabertiidae) based on ribosomal DNA sequence data. International Journal for Parsitology 28, 1781–1789.Google Scholar
Ohdachi, SD, Ishibashi, Y, Iwasa, MA and Saitoh, T (2010) The wild mammals of Japan. 544 pp. Kyoto, Shoukadoh book Sellers.Google Scholar
Robertson, PA, Adriaens, T, Lambin, X, Mill, A, Roy, S, Shuttleworth, CM and Sutton-Croft, M (2017) The large-scale removal of mammalian invasive alien species in northern Europe. Pest Management Science 73, 273–279.Google Scholar
Sato, H and Suzuki, K (2006) Gastrointestinal helminthes of feral raccoons (Procyon lotor) in Wakayama Prefecture, Japan. Journal of Veterinary Medical Science 68, 311–318.Google Scholar
Sato, H, Suzuki, K, Osanai, A, Kamiya, H and Furuoka, H (2006) Identification and characterization of the threadworm, Strongyloides procyonis, from feral raccoons (Procyon lotor) in Japan. Journal of Parasitology 92, 63–68.Google Scholar
Sato, H, Torii, H, Une, Y and Ooi, HK (2007) A new rhabditoid nematode species in Asian sciurids, distinct from Strongyloides robustus in North American sciurids. Journal of Parasitology 93, 1476–1486.Google Scholar
Schaller, GB and Vrba, ES (1996) Description of the giant muntjac (Megamuntiacus vuquangensis) in Laos. Journal of Mammalogy 77, 675–683.Google Scholar
Setsuda, A, Da, N, Hasegawa, H, Behnke, JM, Rana, HB, Dhakal, IP and Sato, H (2016) Intraspecific and interspecific genetic variation of Gongylonema pulchrum and two rodent Gongylonema spp. (G. aegypti and G. neoplasticum), with the proposal of G. nepalensis n. sp. for the isolate in water buffaloes from Nepal. Parasitology Research 115, 787–795.Google Scholar
Setsuda, A, Varcasia, A, Scale, A, et al. (2018) Gongylonema infection of wild mammals in Japan and Sardinia (Italy). Journal of Helminthology 1–8. 2018 Nov 20. doi:10.1017/S0022149X18001001. [Epub ahead of print]Google Scholar
Sultan, K, Omar, M, Makouloutou, P, Kaneshiro, Y, Saita, E, Yokoyama, M, Suzuki, K, Hosoi, E and Sato, H (2014) Molecular genetic conspecificity of Spiculopteragia houdemeri (Schwartz, 1926) and S. andreevae (Dróżdż, 1965) (Nematoda: Ostertagiinae) from wild ruminants in Japan. Journal of Helminthology 88, 1–12.Google Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (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
Tokyo Municipal Office (2017) Control plan of feral alien Reeves's muntjac on Oshima Island, Tokyo in 2017. 14 pp. Available at http://www.kankyo.metro.tokyo.jp/nature/animals_plants/kyon.files/kyon_29biz_plan.pdf (accessed 9 June 2018).Google Scholar
Tran, BT, Sato, H and Luc, PV (2015) A new Cosmocercoides species (Nematoda: Cosmocercoidae), C. tonkinensis n. sp., in the scale-bellied tree lizard (Acanthosaura lepidogaster) from Vietnam. Acta Parasitologica 60, 407–416.Google Scholar
Wang, W and Lan, H (2000) Rapid and parallel chromosomal number reductions in muntjac deer inferred from mitochondrial DNA phylogeny. Molecular Biology and Evolution 17, 1326–1333.Google Scholar
Wildon, DE and Reeder, DM (2005) Mammal species of the world: a taxonomic and geographic reference. 3rd edn. 2142 pp. Baltimore, Johns Hopkins University Press.Google Scholar
Yen, W (1973) Helminthes of birds and wild animals from Lin-tsan Prefecture, Yunnan Province, China II. Parasitic nematodes of mammals. Acta Zoologica Sinica 19, 354–364 (in Chinese with English summary).Google Scholar