Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-22T22:45:03.575Z Has data issue: false hasContentIssue false

Gongylonema infection of wild mammals in Japan and Sardinia (Italy)

Published online by Cambridge University Press:  20 November 2018

A. Setsuda
Affiliation:
Laboratory of Parasitology, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8515, Japan
A. Varcasia
Affiliation:
Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100 Sassari, Sardinia, Italy
A. Scala
Affiliation:
Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100 Sassari, Sardinia, Italy
S. Ozawa
Affiliation:
Oshima Park Station, Tokyo Metoropolian Oshima Island Branch Office, 2 Fukuju, Senzu, Oshima-machi, Tokyo 100-0103, Japan
M. Yokoyama
Affiliation:
Nature and Environment Division, Institute of Natural and Environmental Sciences, University of Hyogo, 940 Sawano, Aogaki-cho, Tanba, Hyogo 669-3842, Japan
H. Torii
Affiliation:
Nara University of Education, Takabatake-cho, Nara 630-8528, Japan
K. Suzuki
Affiliation:
Hikiiwa Park Center, 1629 Inari-cho, Tanabe, Wakayama 646-0051, Japan
Y. Kaneshiro
Affiliation:
NPO Shikoku Institute of Natural History, 470-1 Shimobu-otsu, Susaki, Kochi 785-0023, Japan
A. Corda
Affiliation:
Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100 Sassari, Sardinia, Italy
G. Dessì
Affiliation:
Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100 Sassari, Sardinia, Italy
C. Tamponi
Affiliation:
Laboratory of Parasitology, Veterinary Teaching Hospital, Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100 Sassari, Sardinia, Italy
P.A. Cabras
Affiliation:
Istituto Zooprofilattico Sperimentale della Sardegna, Tortolì, Via Aresu 2, 08048 Tortolì, Ogliastra, Sardinia, Italy
H. Sato*
Affiliation:
Laboratory of Parasitology, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi 753-8515, Japan
*
Author for correspondence: H. Sato, E-mail: [email protected]

Abstract

The gullet worms, classical Gongylonema pulchrum and newly differentiated Gongylonema nepalensis, are prevalent in various mammals in Japan and Sardinia, Italy, respectively. The former species is cosmopolitan in distribution, dwelling in the mucosa of the upper digestive tract of a variety of domestic and wild mammals, and also humans. At present, the geographical distribution of G. nepalensis is known in Nepal and Sardinia, with the nematode having been recorded from the oesophagus of water buffaloes (Nepal), cattle, sheep, goats and wild mouflon (Sardinia). To clarify their natural transmission cycles among domestic and wild mammals, the present study analysed the ribosomal RNA gene (rDNA) and mitochondrial cytochrome c oxidase subunit 1 gene (cox1) of worms of various origins: G. pulchrum worms from sika deer, wild boars, Japanese macaques, and feral alien Reeves's muntjacs in Japan, and G. nepalensis worms from a red fox and a wild boar in Sardinia. Although the internal transcribed spacer (ITS) regions of rDNA and partial cox1 nucleotide sequences of G. pulchrum from native wild mammals in Japan were distinct from those of the worms in cattle, the worms from feral alien Reeves's muntjacs showed the cattle-type ITS genotype and cox1 cattle-I and II haplotypes. The rDNA and cox1 nucleotide sequences of G. nepalensis from a red fox in Sardinia were almost identical to those of the worms from domestic and wild ruminants on the island. The ecological interaction between domestic and wild mammals and their susceptibility to different Gongylonema spp. must be considered when trying to elucidate this spirurid's transmission dynamics in nature.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2018 

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

Alicata, JE (1935) Early developmental stages of nematodes occurring in swine. U.S. Department of Agriculture Technical Bulletin 489, 196.Google Scholar
Anderson, RC (1992) Nematode Parasites of Vertebrates: Their Development and Transmission. Wallingford: CABI Publishing.Google Scholar
Anisimova, M and Gascuel, O (2006) Approximate likelihood–ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539552.Google Scholar
Brack, M (1996) Gongylonematiasis in the common marmoset (Callithrix jacchus). Laboratory Animal Science 46, 266270Google Scholar
Cappucci, DT Jr, Augsburg, JK and Klinck, PC (1982) Gongylonemiasis. In Steele, JH (ed.), Handbook Series in Zoonoses, Section C: Parasitic Zoonoses, Vol. II. Boca Raton, CRC Press, pp. 181192.Google Scholar
Chabaud, AG (2009) Spirurida: Spiruroidea, Habronematoidea and Acuarioidea. In Anderson, RC, Chabaud, AG and Willmott, S (eds), Keys to the Nematode Parasites of Vertebrates. Archival volume. Wallingford: CABI Publishing, pp. 361448.Google Scholar
Dereeper, A et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non–specialist. Nucleic Acids Research 36, 465469.Google Scholar
Duncan, M et al. (1995) Lingual gongylonemiasis and pasterurellosis in Goeldi's monkeys (Callimico goeldii). Journal of Zoo and Wildlife Medicine 26, 102108.Google Scholar
Eslami, A and Farsad-Hamdi, S (1992) Helminth parasites of wild boars, Sus scrofa, in Iran. Journal of Wildlife Diseases 28, 316318.Google Scholar
Frankham, R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78, 311327.Google Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.Google Scholar
Haruki, K et al. (2005) Gongylonema infection in man: a first case of gongylonemosis in Japan. Helminthologia 42, 6366.Google Scholar
Inukai, T (1952) The sika deer on Hokkaido and its prosperity and decline. Hoppo Bunka Kenkyu Houkoku (The Report of Northern Cultural Research of Hokkaido Univ.) 7, 145 (in Japanese).Google Scholar
Kirkpatrick, CE et al. (1986) Gongylonema pulchrum Molin (Nematoda: Gongylonematidae) in black bears (Ursus americanus Pallas) from Pennsylvania. Journal of Wildlife Diseases 22, 119121.Google Scholar
Kitamura, E et al. (1997) Metazoan parasites of sika deer from east Hokkaido, Japan and ecological analyses of their abomasal nematodes. Journal of Wildlife Diseases 33, 278284.Google Scholar
Kudo, N et al. (1996) Intermediate hosts of Gongylonema pulchrum Molin, 1957, in Aomori Prefecture, Japan. Japanese Journal of Parasitology 45, 222229 (in Japanese, with English summary).Google Scholar
Lichtenfels, JR (1971) Morphological variation in the gullet nematode, Gongylonema pulchrum Molin,1857, from eight species of definitive hosts with a consideration of Gongylonema from Macaca spp. Journal of Parasitology 57, 348355.Google Scholar
Makouloutou, P et al. (2013a) Genetic variation of Gongylonema pulchrum from wild animals and cattle in Japan based on ribosomal RNA and mitochondrial cytochrome c oxidase I genes. Journal of Helminthology 87, 326335.Google Scholar
Makouloutou, P et al. (2013b) A distinct genetic population of Gongylonema pulchrum from water buffaloes in Nepal. Journal of Parasitology 99, 669676.Google Scholar
Nabata, D, Masuda, R and Takahashi, O (2004) Bottle-neck effects on the sika deer Cervus nippon population in Hokkaido, revealed by ancient DNA analysis. Zoological Science 21, 473481.Google Scholar
Nei, M, Maruyama, T and Chakraborty, R (1975) The bottleneck effect and genetic variability in populations. Evolution 29, 110.Google Scholar
Sato, H (2009) Biology and transmission of the gullet worm (Gongylonema pulchrum Molin, 1857). Yamaguchi Journal of Veterinary Medicine 36, 3154 (in Japanese, with English summary).Google Scholar
Sato, H, Une, Y and Takada, M (2005) High incidence of the gullet worm, Gongylonema pulchrum, in a squirrel monkey colony in a zoological garden in Japan. Veterinary Parasitology 127, 131137.Google Scholar
Setsuda, A et al. (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, 787795.Google Scholar
Setsuda, A et al. (2018) Molecular genetic diversity of Gongylonema neoplasticum (Fibiger & Ditlevsen, 1914) (Spirurida: Gongylonematidae) from rodents in Southeast Asia. Systematic Parasitology 95, 235247.Google Scholar
Skrjabin, KI, Sobolev, AA and Ivashkin, VM (1967) Spirurata of animals and man and the diseases caused by them. Part 4. Thelazioidea. In Skrjabin, KI (ed.), Akademiya Nauk SSSR, Gel'mintologicheskaya Laboratoriya Osnovy Nematodologii, Tom XVI, Translated from Russian to English by Israel Program for Scientific Translations, Jerusalem, 1971.Google Scholar
Suzuki, K et al. (1992) Gongylonema pulchrum Molin, 1857 from cattle in Hokkaido. Journal of Japanese Veterinary Medical Association 45, 120124 (in Japanese, with English summary).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, 46734680.Google Scholar
Tokyo Municipal Office (2017) Control plan of feral alien Reeves's muntjac on Oshima Island, Tokyo in 2017. Available at http://www.kankyo.metro.tokyo.jp/nature/animals_plants/kyon.files/kyon_29biz_plan.pdf (accessed 9 June 2018).Google Scholar
Varcasia, A et al. (2017) First record of Gongylonema nepalensis in domestic and wild ruminants in Europe. Veterinary Parasitology 246, 1118.Google Scholar
Ward, HB (1916) Gongylonema in the role of a human parasite. Journal of Parasitology 2, 119125.Google Scholar
Xu, L–Q, Yu, S–H and Xu, S–H (2000) Distribution and pathogenic impact of human parasites in China. Beijing: People's Medical Publishing House.Google Scholar
Yamaguti, S (1961) Systema Helminthum. Vol. III. The Nematodes of Vertebrates. New York, NY: Interscience Publishers.Google Scholar
Zinter, DE and Migaki, G (1970) Gongylonema pulchrum in tongues of slaughtered pigs. Journal of the American Veterinary Medical Association 157, 301303.Google Scholar