Skip to main content
Log in

Some nematodes from eels (Anguilliformes: Anguillidae) in Japan, with descriptions of two new species

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

Recent occasional examinations of two species of eels (Anguilliformes: Anguillidae) in Japan, the Japanese eel Anguilla japonica Temminck & Schlegel from central Japan and the giant mottled eel Anguilla marmorata Quoy & Gaimard from southern Japan, respectively, revealed the following four species of gastrointestinal parasitic nematodes: Cucullanus filiformis Yamaguti, 1935 (Cucullanidae) from A. japonica; Paraquimperia japonica n. sp. (Quimperiidae) from A. japonica (type-host) and A. marmorata; Heliconema anguillae Yamaguti, 1935 (Physalopteridae) from A. marmorata (new host record); and Spinitectus anguillae n. sp. (Cystidicolidae) from A. japonica (type-host) and A. marmorata. Specimens of all species are described based on light and scanning electron microscopical examinations. Paraquimperia japonica n. sp. is mainly characterised by the presence of a ventral sucker, spicules 210–231 µm long and by narrow cervical alae, whereas S. anguillae n. sp. by the number (29–36) of cuticular spines in the first ring, the length of the left spicule (351 µm) and the structure (without polar caps, filaments or lateral swellings), and the size of eggs (36–42 × 21–27 µm).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Baylis, H. A. (1934). A little-known nematode parasite of the eel. Annals and Magazine of Natural History, Series 10, 13, 235–240.

    Article  Google Scholar 

  • Froese, R., & Pauly, D. (Eds) (2020). FishBase. World Wide Web electronic publication. http://www.fishbase.org, version 06/2020.

  • Fujita, T. (1927). On new species of nematodes from fishes of Lake Biwa. Japanese Journal of Zoology, 1, 169–176.

    Google Scholar 

  • Hasegawa, H., & Yoshimura, K. (2003). [Nematoda. In: Nishida, M., Shikatani, S. & Shokita, S. (Eds), The flora and fauna of inland waters in the Ryukyu Islands.] Hadano: Tokai University Press, pp. 160–165 (in Japanese).

  • ICZN (2012). International Commission on Zoological Nomenclature: Amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Bulletin of Zoological Nomenclature, 69, 161–169.

    Article  Google Scholar 

  • Ishii, S. (1916). [On a new species of Nematoda, Filaria anguillae n. sp., from the orbit of Japanese eels.] Zoological Magazine, 28, 214–220 (in Japanese).

  • Ishii, S. (1931). [Parasites of fishes of Japan. In: Anonymous (Ed.), Biology, Vol. 18 (supplement).] Tokyo: Iwanami Shoten, pp. 179–207 (in Japanese).

  • Kan, K., Sato, M., & Nagasawa, K. (2016). Tidal-flat macrobenthos as diets of the Japanese eel Anguilla japonica in western Japan, with a note on the occurrence of a parasitic nematode Heliconema anguillae in eel stomachs. Zoological Science, 33, 50–62.

    Article  Google Scholar 

  • Karve, J. N. (1941). Some parasitic nematodes of fishes. I. Journal of the University of Bombay, New Series, Part 3, Biological Sciences No. 10, 10, 9–42.

  • Katahira, H., & Nagasawa, K. (2015). Heliconema anguillae Yamaguti, 1935, a physalopterid nematode found in Japanese eels: taxonomic resurrection with a note on the third-stage larva from intertidal crabs in western Japan. Folia Parasitologica, 62: 028.

    Article  Google Scholar 

  • Kuwahara, A., Niimi, A., & Itagaki, H. (1974). Studies on a nematode parasitic in the air bladder of the eel. I. Description of Anguillicola crassa n. sp. (Philometridea, Anguillicolidae). Japanese Journal of Parasitology, 23, 275–279.

    Google Scholar 

  • Lefebvre, F., Wielgoss, S., Nagasawa, K., & Moravec, F. (2012). On the origin of Anguillicoloides crassus, the invasive nematode of anguillid eels. Aquatic Invasions, 7, 443–453.

    Article  Google Scholar 

  • Li, H.C. (1934). Report on a collection of parasitic nematodes, mainly from North China. Part II. Spiruroidea. Transactions of the American Microscopical Society, 53, 174–195.

    Article  Google Scholar 

  • Li, L., Liu, Y.-Y., Liu, B.-C., & Zhang, L.-P. (2013). Morphological and molecular characterization of Heliconema hainanensis [sic] sp. nov. (Spirurina: Physalopteridae) from congers in the South China Sea, with a key to the species of Heliconema. Memórias do Instituto Oswaldo Cruz, 108, 41–47.

    Article  Google Scholar 

  • Linstow, O., von (1878). Neue Beobachtungen an Helminthen. Archiv für Naturgeschichte, 44, 218–245.

    Google Scholar 

  • Moravec, F. (1966). On the systematics of the genus Paraquimperia Baylis, 1934 (Nematoda; Quimperiidae). Helminthologia, 7, 353–364.

    Google Scholar 

  • Moravec, F. (1975). Some remarks on the development of Paraquimperia tenerrima (Linstow, 1878) (Nematoda: Quimperiidae). Scripta Facultatis Scientiarum Naturalium Universitatis Purkynianae Brunensis, Biologia 5, 4 (Year 1974), 135–142.

  • Moravec, F. (1979). Redescription of the nematode Spinitectus inermis parasitic in eels, Anguilla anguilla, of Europe. Acta Societatis Zoologicae Bohemoslovenicae, 43, 35–42.

    Google Scholar 

  • Moravec, F. (1996). Some new data on the morphology of Spinitectus inermis (Nematoda: Cystidicolidae), a rare parasite of eels, as revealed by SEM. Parasite, 3, 169–174.

    Article  Google Scholar 

  • Moravec, F. (2013). Parasitic nematodes of freshwater fishes of Europe. Revised second edition. Prague: Academia, 601 pp.

    Google Scholar 

  • Moravec, F., Boomker, J., & Taraschewski, H. (2000). Paraquimperia africana n. sp. (Nematoda: Quimperiidae), a new intestinal parasite of the eel Anguilla mossambica Peters, in South Africa. Journal of Parasitology, 86, 113–117.

    Article  CAS  Google Scholar 

  • Moravec, F., Chaudhary, A., & Singh, H. S. (2019). Heliconema monopteri n. sp. (Nematoda: Physalopteridae) from Monopterus cuchia (Hamilton) (Osteichthyes: Synbranchidae) in India, with notes on the taxonomy of Heliconema spp. Helminthologia, 56, 124–131.

    Article  CAS  Google Scholar 

  • Moravec, F., & Justine, J.-L. (2018). Three new species of Cucullanus (Nematoda: Cucullanidae) from marine fishes off New Caledonia, with a key to species of Cucullanus from Anguilliformes. Parasite, 25, 51.

    Article  Google Scholar 

  • Moravec, F., & Nagasawa, K. (2018). Rhabdochona angusticaudata sp. n. (Nematoda: Rhabdochonidae) from the Japanese eel Anguilla japonica, and new records of some other nematodes from inland fishes in Japan. Folia Parasitologica, 65, 016.

  • Moravec, F., Nie, P., & Wang, G. (2004). New data on the morphology and systematic status of Spinitectus petrowi and Spinitectus gigi (Nematoda: Cystidicolidae) parasitic in catfishes in central China. Folia Parasitologica, 51, 346–358.

    Article  Google Scholar 

  • Moravec, F., Pachanawan, A., & Kamchoo, K. (2016). Redescription of two species of cystidicolid nematodes (Spirurina: Cystidicolidae) from Notopterus notopterus (Osteichthyes) in Thailand. Acta Parasitologica, 61, 278–280.

    PubMed  Google Scholar 

  • Moravec, F., & Scholz, T. (2015). Macroparasites and their communities of the European eel Anguilla anguilla (Linnaeus) in the Czech Republic. Folia Parasitologica, 62, 033.

    Google Scholar 

  • Moravec, F., & Sey, O. (1988). Nematodes of freshwater fishes from North Vietnam. Part 1. Camallanoidea and Habronematoidea. Acta Societatis Zoologicae Bohemoslovenicae, 52, 128–148.

    Google Scholar 

  • Moravec, F., & Yooyen, T. (2011). Observations on two nematode species parasitizing freshwater fishes in Thailand, including Spinitectus thaiensis sp. nov. (Cystidicolidae) from Pseudomystus siamensis (Bagridae). Acta Parasitologica, 56, 58–66.

    Google Scholar 

  • Morishita, K. (1926). Studies on some nematode parasites of frogs and toads in Japan, with notes on their distribution and frequency. Journal of the Faculty of Science, the Imperial University of Tokyo, Section 4, 1, 1–32 + 5 Plates.

  • Nagasawa, K. (2016). A checklist of the parasitic nematodes of freshwater fishes of Japan (1905–2016) – Part 1. Bulletin of the Hiroshima University Museum, 8, 61–90 (In Japanese with English abstract).

    Google Scholar 

  • Nagasawa, K., & Katahira, H. (2017). A revised and updated checklist of the parasites of eels (Anguilla spp.) (Anguilliformes: Anguillidae) in Japan (1915–2017). Biosphere Science, 56, 33–69.

    Google Scholar 

  • Nagasawa, K., Kim, Y.-G., & Hirose, H. (1994). Anguillicola crassus and A. globiceps (Nematoda: Dracunculoidea) parasitic in the swimbladder of eels (Anguilla japonica and A. anguilla) in East Asia: a review. Folia Parasitologica, 41, 127–137.

    Google Scholar 

  • Nakabo, T. (2018). The natural history of the fishes of Japan. Tokyo: Shogakukan, 524 pp. (In Japanese).

  • Odening, K. (1976). Conception and terminology of hosts in parasitology. Advances in Parasitology, 14, 1–93.

    Article  CAS  Google Scholar 

  • Ogden, C. G. (1969). A revision of the genus Heliconema Travassos, 1919, Physalopteridae (Nematoda). Journal of Natural History, 3, 423–431.

    Article  Google Scholar 

  • Park, J.-K., & Moravec, F. (2008). Redescription of Cucullanus robustus (Nematoda: Cucullanidae) from the conger eel Conger myriaster off Korea. Zootaxa, 1729, 1–7.

    Article  Google Scholar 

  • Peng, W., Liu, S., Wang, B., & Wei, M. (2011). A checklist of parasitic nematodes from marine fishes of China. Systematic Parasitology, 79, 17–40.

    Article  Google Scholar 

  • Poinar, G., Jr., Weinstein, S. B., Garcia-Vedrenne, A. E., & Kuris, A. M. (2014). First description of a nematode, Spinitectus gabata n. sp. (Spirurina: Cystidicolidae), from the deep sea oarfish, Regalecus russelii (Regalecidae) in Japan. International Journal of Nematology, 24, 117–123.

    Google Scholar 

  • Saraiva, A. M., Moravec, F., Pereira, A., & Cruz, C. (2002). Development of Spinitectus inermis (Nematoda: Cystidicolidae), a parasite of eel, Anguilla anguilla, in Europe. Folia Parasitologica, 49, 118–126.

    Article  Google Scholar 

  • Shears, J. A., & Kennedy, C. R. (2005). The life cycle of Paraquimperia tenerrima: a parasite of the European eel Anguilla anguilla. Journal of Helminthology, 79, 169–176.

    Article  CAS  Google Scholar 

  • Taraschewski, H., Moravec, F., Lamah, T., & Anders, K. (1987). Distribution and morphology of two helminths recently introduced into European eel populations: Anguillicola crassus (Nematoda, Dracunculoidea) and Paratenuisentis ambiguus (Acanthocephala, Tenuisentidae). Diseases of Aquatic Organisms, 3, 167–176.

    Article  Google Scholar 

  • Tsukamoto, K., & Arai, T. (2001). Facultative catadromy of the eel Anguilla japonica between freshwater and seawater habitats. Marine Ecology Progress Series, 220, 265–276.

    Article  Google Scholar 

  • Tzeng, W. N., Shiao, J. C., & Iizuka, Y. (2002). Use of otolith SR:Ca ratios to study the riverine migratory behaviors of Japanese eel Anguilla japonica. Marine Ecology Progress Series, 245, 213–221.

    Article  Google Scholar 

  • Wang, P., & Ling, X. (1975). Some nematodes of the suborder Camallanata from Fujian Province, with notes on their life histories. Acta Zoologica Sinica, 21, 350–358 (In Chinese with English abstract).

    Google Scholar 

  • Wang, P., & Zhao, Y. (1980). Observations on the life history of Anguillicola globiceps (Nematoda: Anguillicolidae). Acta Zoologica Sinica, 26, 243–249 (In Chinese with English abstract).

    Google Scholar 

  • Yamaguti, S. (1935). Studies on the helminth fauna of Japan. Part 9. Nematodes of fishes, 1. Japanese Journal of Zoology, 6, 337–386.

    Google Scholar 

  • Yamaguti, S. (1941). Studies on the helminth fauna of Japan. Part 33. Nematodes of fishes, II. Japanese Journal of Zoology, 9, 343–395 + Plates IV–VI.

  • Yamaguti, S. (1961). The nematodes of vertebrates. Part I, II. Systema helminthum III. New York-London: Interscience Publishers, 1261 pp.

Download references

Acknowledgements

We thank Takeshi Sasaki (University Museum, University of the Ryukyus, Fujukan) and Toru Naruse (Tropical Biosphere Research Center, Iriomote Station, University of the Ryukyus) for providing laboratory facilities. We are grateful to Hirotaka Katahira (Azabu University) for help and support during the study and to Yasuhiro Fujioka (Shiga Prefectural Fisheries Experiment Station), Daisuke Uyeno (Kagoshima University) and Masato Nitta (Kobe University) for assistance with fish sampling. Thanks are also due to the Laboratory of Electron Microscopy, Institute of Parasitology, Biology Centre CAS, institution supported by the MEYS CR (LM2015062 Czech-BioImaging) for their support with obtaining scientific data presented in this paper, and to Blanka Škoríková of the same Institute for help with the illustrations. The Japanese eels examined were captured with a special permission from the Yamaguchi Prefecture Government and the Fisheries Cooperative Associations for Fishes of the Nishiki and Shimata Rivers.

Funding

This study was partly supported by the institutional support of the Institute of Parasitology, BC AS CR, 585110/9500 to FM and by JSPS (Japan Society for the Promotion of Science) KAKENHI Grant Number JP 24580267 to KN.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to František Moravec.

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

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article was registered in the Official Register of Zoological Nomenclature (ZooBank) as urn:lsid:zoobank.org:pub:D0694D29-95AB-4442-855E-62252D106A97. This article was published as an Online First article on the online publication date shown on this paper. The article should be cited by using the doi number. This is the Version of Record.

This article is part of the Topical Collection Nematoda.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moravec, F., Nagasawa, K. & Hatama, T. Some nematodes from eels (Anguilliformes: Anguillidae) in Japan, with descriptions of two new species. Syst Parasitol 97, 691–712 (2020). https://doi.org/10.1007/s11230-020-09945-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-020-09945-1

Navigation