Abstract
We discuss the systematic position of five species of the Heligmonellidae (Skrjabin & Schikhobalova, 1952 tribe) Durette-Desset & Chabaud, 1977 described in arvicoline rodents “Eothenomys” (sensu lato) from Japan and Thailand, classified up to now in the genera Yatinema Asakawa & Ohbayashi, 1986, Carolinensis (Travassos, 1937), Morganiella Travassos, 1937 and Neoheligmonella Durette-Desset, 1971. The species are analysed, rediagnosed and their systematic position reviewed. A new generic arrangement is proposed mainly based on characters of the synlophe such as: the presence or absence of a careen; the relative size of the ridges of the careen with respect to the right ridge; the relative sizes of the left and right ridge; the size and position of ridge 1’; the presence or absence of gradients in ridge size; and the number of ridges. The taxa analysed are rearranged in three genera and six species, of which two genera and three species are new. The new classification proposed includes: Yatinema (sensu stricto) with Yatinema japonicum Asakawa & Ohbayashi, 1986 (type-species) and Y. niigatae n. sp. (syn. Y. japonicum sensu Asakawa & Ohbayashi, 1986 pro parte); Asakawanema n. g. with Asakawanema siamense n. comb. (syn. Yatinema siamensis Asakawa, Kamiya & Ohbayashi. 1986) as the type- and only species; and Fukumotonema n. g. with Fukumotonema orientale n. comb. (syn. Neoheligmonella orientalis Asakawa, Kamiya & Ohbayashi. 1986) (type-species), Fukumotonema deborahae n. sp. (syn. Yatinema japonicum sensu Asakawa, 1989 nec Asakawa & Ohbayashi. 1986), and Fukumotonema myodesi n. sp. (syn. Morganiella cricetuli sensu Asakawa et al., 1989 nec Yin & Zhang, 1981). Carolinensis eothenomysi Asakawa, Kamiya & Ohbayashi, 1986 and Morganiella cricetuli Yin & Zhang, 1981 are considered Nippostrongylinae incertae sedis. A key to the genera and species is provided.
Similar content being viewed by others
References
Asakawa, M. (1989). Studies on heligmonellid nematodes from the Japanese Microtidae. I. A study on heligmonellids and other helminths from the Japanese red-backed vole. Eothenomys andersoni (Thomas) [syn. Wakayama-Miyama-Nezumi, Aschizomys imaizumii (Jameson)] in Kii Peninsula, Japan. Journal of Rakuno Gakuen University, 13, 253–262.
Asakawa, M., & Ohbayashi, M. (1986). A new nematode, Yatinema japonicum gen. et sp. n. (Heligmonellidae: Nematoda), from voles, Eothenomys smithii (Thomas) and E. niigatae (Anderson). Japanese Journal of Veterinary Research, 34, 7–23.
Asakawa, M., Hasegawa, H., & Fukumoto, S. (1988). A taxonomical note on Longistriata wolgaensis sensu Yamaguti, 1954 (Nematoda: Heligmonellidae: Nippostrongylinae) from Clethrionomys smithii. Journal of the College of Dairying, 12, 367–370.
Asakawa, M., Kamiya, M., & Ohbayashi, M. (1986). Studies on the parasite fauna of Thailand. 6. Three new heligmonellid nematodes from Père David’s vole, Eothenomys melanogaster (Milne-Edwards). Japanese Journal of Veterinary Research, 34, 219–231.
Asakawa, M., Durette-Desset, M.-C., Fukumoto, S., & Ohbayashi, M. (1989). Studies on heligmonellid nematodes from the Japanese Microtidae. II- First record of Morganiella cricetuli Yin & Zhang, 1981 from Eothenomys smithii. Journal of Rakuno Gakuen University, 14, 43–47.
Asakawa, M., Tenora, F., Fukumoto, S., Kano, K., & Tomonari, T. (1992). Faunal and zoogeographical study on the parasitic helminths of voles and field mice in Shikoku, Japan. Bulletin of the Tokushima Prefectural Museum, 2, 51–75.
Beveridge, I., Durette-Desset, M.-C., & Spratt, D. (2012). 7-18 Order Strongylida (Railliet & Henry, 1913). In: Schmidt-Rhaesa, A. (Ed.), Handbook of zoology. A natural history of the phyla of the animal kingdom: 2 Nematoda. Berlin: De Gruyter, pp. 557–612.
Chabaud, A. G., Puylaert, F., Bain, O., Petter, A. J., & Durette- Desset, M.-C. (1970). Remarques sur l’homologie entre les papilles cloacales des Rhabditides et les côtes dorsales des Strongylida. Comptes Rendus de l’Académie des Sciences de Paris, 271, 1771–1774.
Digiani, M. C., & Durette-Desset, M.-C. (2013). Taxonomic revision of the genus Neoheligmonella Durette-Desset, 1971 (Nematoda, Heligmonellidae), parasitic in Muridae mainly from the Ethiopian region. Zoosystema, 35, 479–488.
Digiani, M. C., & Durette-Desset, M.-C. (2014). Taxonomic revision of the Nippostrongylinae (Nematoda, Heligmonellidae) parasitic in Oriental Muridae. The genus Paraheligmonelloides Fukumoto, Kamiya & Suzuki, 1980. Zootaxa, 3884, 81–88.
Durette-Desset, M.-C. (1971). Essai de classification des Nématodes Héligmosomes. Corrélation avec la paléobiogéographie des hôtes. Mémoires du Muséum National d’Histoire Naturelle, Série A, Zoologie, 49, 1–126.
Durette-Desset, M.-C. (1983). Keys to genera of the Superfamily Trichostrongyloidea. In: Anderson, R. C. & Chabaud, A. G. (Eds), CIH Keys to the Nematode Parasites of Vertebrates. Farnham Royal: CAB, pp. 1–68.
Durette-Desset, M.-C. (1985). Trichostrongyloid nematodes and their vertebrate hosts: reconstruction of the phylogeny of a parasitic group. Advances in Parasitology, 24, 239–306.
Durette-Desset, M.-C., & Chabaud, A. G. (1977). Essai de classification des Nématodes Trichostrongyloidea. Annales de Parasitologie Humaine et Comparée, 52, 539–558.
Durette-Desset, M.-C., & Digiani, M. C. (2005). The axis of orientation of the synlophe in the Heligmosomoidea (Nematoda, Trichostrongylina): a new approach. Parasite, 12, 195–202.
Durette-Desset, M.-C., & Digiani, M.-C. (2012). The caudal bursa in the Heligmonellidae (Nematoda: Trichostrongylina). Characterization and hypothesis on its evolution. Parasite, 19, 3–18.
Durette-Desset, M.-C., & Digiani, M. C. (2015). Taxonomic revision of the Nippostrongylinae (Nematoda, Heligmonellidae) parasites of Muridae from the Australasian region. The genus Odilia Durette-Desset, 1973. Parasite, 22, 1–12.
Durette-Desset, M.-C., & Vaucher, C. (1974). Nématodes Héligmosomes parasites d’Insectivores Talpidés de la région holarctique. Annales de Parasitologie Humaine et Comparée, 49, 191–200.
Durette-Desset, M.-C., Digiani, M. C., Kilani, M., & Geffard-Kuriyama, D. (2017). Critical revision of the Heligmonellidae (Nematoda: Trichostrongylina: Heligmosomoidea). Paris: Muséum national d’Histoire naturelle.
Musser, G. G., & Carleton, M. D. (2005). Subfamily Arvicolinae. In: Wilson, D. E. & Reeder, D. A. M. (Eds), Mammal species of the world. A taxonomic and geographic reference. 3rd Edition. Baltimore: Johns Hopkins University Press, pp. 956–1039.
Travassos, L. (1937). Revisão da familia Trichostrongylidae Leiper, 1912. Monographias do Instituto Oswaldo Cruz, 1, 1–512.
Yamaguti, S. (1954). Studies on the helminth fauna of Japan. Part 51. Mammalian nematodes, V. Acta Medicinae Okayama, 9, 105–121.
Yin, W.-Z., & Zhang, N.-X. (1981). On some parasitic nematodes from rodents and insectivora in Peking, China. Acta Zootaxonomica Sinica, 6, 16–21.
Acknowledgements
We are grateful to Dr Ryo Nakao (Laboratory of Parasitology, Graduate School of Veterinary Medicine, Hokkaido University, Japan) for providing information on the deposited material of some of the species studied and Didier Geffard-Kuriyama (Muséum national d’Histoire naturelle, Paris, France) for the scanning and graphic editing of the figures.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable institutional, national and international guidelines for the care and use of animals were followed.
Additional information
This article is part of the Topical Collection Nematoda.
Rights and permissions
About this article
Cite this article
Durette-Desset, MC., Digiani, M.C. Taxonomic revision of the Heligmonellidae (Skrjabin & Schikhobalova, 1952 tribe) Durette-Desset & Chabaud, 1977 (Nematoda) parasitic in arvicoline rodents “Eothenomys” (sensu lato) (Cricetidae) from Japan and Thailand. Syst Parasitol 96, 1–13 (2019). https://doi.org/10.1007/s11230-018-9836-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11230-018-9836-7