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Some Spirurid Nematodes (Spirurida) from Freshwater and Brackish-Water Fishes in Okinawa Prefecture, Japan, with Descriptions of Two New Species

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Abstract

Purpose

Despite the fact that Okinawa Prefecture represents a very interesting subtropical region of Japan, its fauna of nematodes parasitizing fishes is still little-known. Therefore, new data are needed to recognize the species composition of these parasites in this zoogeographically remarkable region.

Methods

Helminthological examinations of some freshwater and brackish-water fishes in Okinawa Prefecture carried out in the years 2010, 2016 and 2018, revealed two new and four insufficiently known species of spirurid nematodes (Spirurida), all gastrointestinal parasites. These were studied with the use of light and scanning electron microscopy.

Results

All nematode species recorded are described: Rhabdochonidae: Rhabdochona honshuensis Moravec et Nagasawa, 1989 from Glossogobius celebius (Valenciennes) (Gobiidae, Perciformes) (new host), Rhabdochona iriomotensis sp. nov. from Ophieleotris sp. (Eleotridae, Perciformes) and Rhabdochona sp. (only females) from Eleotris acanthopoma Bleeker and E. fusca (Forster) (both Eleotridae, Perciformes); Cystidicolidae: Spinitectus mirabilis sp. nov. from Kuhlia rupestris (Lacepède) (Kuhliidae, Perciformes) and Spinitectus sp. larvae from E. acanthopoma; and Camallanidae: Procamallanus (Spirocamallanus) sp. (fourth-stage larva) from Yongeichthys criniger (Valenciennes) (Gobiidae, Perciformes). Rhabdochona iriomotensis sp. nov. is very similar to R. honshuensis, but differs from it in the presence of well-developed ventral precloacal ridges. Spinitectus mirabilis sp. nov. differs from its congeners and all other cystidicolids in having eggs provided with both lateral swellings and polar filaments.

Conclusions

In addition to the discovery of two new nematode species, Rhabdochona iriomotensis sp. nov. and Spinitectus mirabilis sp. nov., the findings of all other species represent new host and geographical records. Rhabdochona denudata honshuensis Moravec et Nagasawa, 1989 is elevated to the level of an independent species R. honshuensis.

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References

  1. Hasegawa H, Williams EH, Bunkley-Williams L (1991) Nematode parasites from marine fishes of Okinawa, Japan. J Helminthol Soc Wash 58:186–197

    Google Scholar 

  2. 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. Tokai Univ Press, Hadano, pp 160–165 (In Japanese)

    Google Scholar 

  3. Moravec F, Cutmore SC, Yong RQ-Y (2018) Redescription of Philometra pellucida (Jägerskiöld, 1893) (Nematoda: Philometridae) parasitic in the abdominal cavity of the blackspotted puffer Arothron nigropunctatus (Bloch & Schneider) (Teleostei: Tetraodontidae) off Australia and Japan. Syst Parasitol 95:665–671. https://doi.org/10.1007/s11230-018-9806-0

    Article  PubMed  Google Scholar 

  4. Moravec F, Nagasawa K, Hatama T (2020) Some nematodes from eels (Anguilla spp.) in Japan, with descriptions of two new species. Syst Parasitol, in press.

  5. Froese R, Pauly D (eds.) (2020) FishBase. World Wide Web electronic publication. https://www.fishbase.org. Accessed 15 June 2020

  6. Nakabo T (ed) (2013) Fishes of Japan with pictorial keys to the species, 3rd edn. Tokai Univ Press, Hadano (In Japanese)

    Google Scholar 

  7. Moravec F (2010) Some aspects of the taxonomy, biology, possible evolution and biogeography of nematodes of the spirurine genus Rhabdochona Railliet, 1916 (Rhabdochonidae, Thelazioidea). Acta Parasitol 55:144–160. https://doi.org/10.2478/s11686-010-0017-3

    Article  Google Scholar 

  8. Moravec F (2013) Parasitic nematodes of freshwater fishes of Europe. Revised second edition, Academia, Prague

    Google Scholar 

  9. Ali SM (1956) Studies on the nematode parasites of fishes and birds found in Hyderabat State. Ind J Helminthol 8:1–83

    Google Scholar 

  10. Caspeta-Mandujano JM, Aguilar-Aguilar R, Salgado-Maldonado G (2002) Rhabdochona guerreroensis n. sp. (Nematoda: Rhabdochonidae) from the intestine of the gobiid Sicydium multipunctatum from freshwaters in Mexico. J Parasitol 88:746–749. https://doi.org/10.1645/0022-3395(2002)088[0746:RGNSNR]2.0.CO

    Article  PubMed  Google Scholar 

  11. Chabaud AG (1970) Rhabdochona srivastavai n. sp., a parasitic nematode of a gobiid from Madagascar. H. D. Srivastava Commemorative Volume, Izatnagar, India, pp 307–310

  12. Wang P (1976) Notes on some new nematodes of the suborder Spirurata from Fujian, China. Acta Zool Sinica 22:393–402 (In Chinese, Engl abstract)

    Google Scholar 

  13. Yamaguti S (1941) Studies on the helminth fauna of Japan. Part 33. Nematodes of fishes, II. Jap J Zool 9:343–395 (Plts IV–VI)

    Google Scholar 

  14. Hirasawa R, Urabe M (2003) Ephemera strigata (Insecta: Ephemeroptera: Ephemeridae) is the intermediate host of the nematodes Rhabdochona denudata honshuensis and Rhabdochona coronacauda in Japan. J Parasitol 89:617–620. https://doi.org/10.1645/GE-3106RN

    Article  CAS  PubMed  Google Scholar 

  15. Hirasawa R, Yuma M (2003) Ephemera strigata imagoes are the likely source of a parasitic nematode infection of fish. Folia Parasitol 50:313–314. https://doi.org/10.14411/fp.2003.042

    Article  Google Scholar 

  16. Moravec F, Nagasawa K (1989) Observations on some nematodes parasitic in Japanese freshwater fishes. Folia Parasitol 36:127–141

    Google Scholar 

  17. Mori T, Urabe M, Nagoshi M (1998) Relationship between body size of dark chub, Zacco temmincki and number of parasitic nematode Rhabdochona denudata. Biol Inland Wat 13:67–70 (In Japanese)

    Google Scholar 

  18. Moravec F (1975) Reconstruction of the nematode genus Rhabdochona Railliet, 1916 with a review of the species parasitic in fishes of Europe and Asia. Studie ČSAV No. 8. Academia, Prague

  19. Moravec F, Sey O (1988) Nematodes of freshwater fishes from North Vietnam. Part 2. Thelazioidea, Physalopteroidea and Gnathostomatoidea. Acta Soc Zool Bohemoslov 52:176–191

    Google Scholar 

  20. González-Solís D, Soler-Jiménez LC, Aguirre-Macedo ML, McLaughlin JP, Shaw JC, James AK, Hechinger RF, Kuris AM, Lafferty KD, Vidal-Martínez VM (2019) Parasitic nematodes of marine fishes from Palmyra Atoll, East Indo-Pacific, including a new species of Spinitectus (Nematoda, Cystidicolidae). ZooKeys 892:1–26. https://doi.org/10.3897/zookeys.892.38447(27Nov2019)

    Article  PubMed  PubMed Central  Google Scholar 

  21. Moravec F, García-Magaña L, Salgado-Maldonado G (2002) Spinitectus tabascoensis sp. nov. (Nematoda, Cystidicolidae) from Ictalurus furcatus (Pisces) in southeastern Mexico. Acta Parasitol 47:224–227

    Google Scholar 

  22. 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 Parasitol 56:58–66. https://doi.org/10.2478/s11686-011-0014-1

    Article  Google Scholar 

  23. Skryabin KI, Sobolev AA, Ivashkin VM (1967) Spirurata of animals and man and the diseases caused by them. Part 4. Thelazioidea. Osnovy nematodologii 16. Nauka, Moscow (in Russian)

  24. Yamaguti S (1961) The nematodes of vertebrates. Part I, II Systema helminthum III. Interscience Publishers, New York, and London

    Google Scholar 

  25. Moravec F (1998) Nematodes of freshwater fishes of the Neotropical Region. Academia, Prague

    Google Scholar 

  26. Petter AJ (1984) Nématodes de poissons du Paraguay II. Habronematoidea (Spirurida). description de 4 espèces nouvelles de la famille des Cystidicolidae. Rev Suisse Zool 91:935–952

    Article  Google Scholar 

  27. Petter AJ (1987) Nématodes de poissons de l’Equateur. Rev Suisse Zool 94:61–76

    Article  Google Scholar 

  28. Travassos L, Artigas P, Pereira C (1928) Fauna helminthologica dos peixes do agua doce do Brasil. Arch Inst Biol 1:5–68 (14 Plts)

    Google Scholar 

  29. Arai HP, Smith JW (2016) Guide to the parasites of fishes of Canada Part V: Nematoda. Zootaxa 4185:1–274. https://doi.org/10.11646/zootaxa.4185.1.1

    Article  Google Scholar 

  30. Moravec F, Nagasawa K (1999) Morphology and taxonomy of Salvelinema species (Nematoda: Cystidicolidae), swimbladder parasites of Pacific area salmonids. Folia Parasitol 46:123–131

    Google Scholar 

  31. Holloway HL, Klewer HL (1969) Rhabdochona beatriceinsleyae n. sp. (Nematoda: Spiruridea: Rhabdochonidae), from the Antarctic zoarcid, Rhigophila dearborni. Trans Am Micr Soc 88:460–471

    Article  Google Scholar 

  32. Moravec F, Hanzelová V, Gerdeaux D (2007) New data on the morphology of Comephoronema oschmarini (Nematoda, Cystidicolidae), a little-known gastrointestinal parasite of Lota lota (Teleostei) in Palaearctic Eurasia. Acta Parasitol 52:135–141. https://doi.org/10.2478/s11686-007-0018-2

    Article  Google Scholar 

  33. Moravec F, Klimpel S (2007) A new species of Comephoronema (Nematoda: Cystidicolidae) from the stomach of the abyssal halosaur Halosauropsis macrochir (Teleostei) from the Mid-Atlantic Ridge. J Parasitol 93:901–906. https://doi.org/10.1645/ge-1065r.1

    Article  PubMed  Google Scholar 

  34. Pereira FB, Pereira AN, Luque JL (2014) A new species of Comephoronema (Nematoda: Cystidicolidae) from the squirrelfish Holocentrus adscensionis (Beryciformes: Holocentridae) off Brazil. Folia Parasitol 61:55–62. https://doi.org/10.14411/fp.2014.001

    Article  Google Scholar 

  35. Sokolov SG, Voropaeva EL, Malysheva SV (2019) Redescription and molecular characterisation of Comephoronema werestschagini Layman, 1933 (Nematoda: Cystidicolidae) from the endemic Baikal fish Cottocomephorus grewingkii (Dybowski, 1874) (Scorpaeniformes: Cottocomephoridae) with some comments on cystidicolid phylogeny. Russian J Nematol 27:57–66. https://doi.org/10.24411/0869-6918-2019-10007

    Article  Google Scholar 

  36. Boomker J, Puylaert FA (1994) Eight new Afrotropical Spinitectus spp. (Nematoda: Cystidicolidae) from freshwater fishes with a key to the members of the genus in the region. Onderstepoort J Vet Res 61:127–142

    CAS  PubMed  Google Scholar 

  37. Petter AJ, Golvan YJ, Tcheprakoff R (1977) Nématodes de poisons de rivière en Guadeloupe. Bull Mus Nat Hist Nat Zool 298:159–171

    Google Scholar 

  38. Moravec F (1979) Redescription of the nematode Spinitectus inermis parasitic in eels, Anguilla anguilla, of Europe. Acta Soc Zool Bohemoslov 43:35–42

    Google Scholar 

  39. Saraiva AM, Moravec F, Pereira A, Cruz C (2002) Development of Spinitectus inermis (Nematoda: Cystidicolidae), a parasite of eel, Anguilla anguilla, in Europe. Folia Parasitol 49:118–126. https://doi.org/10.14411/fp.2002.022

    Article  Google Scholar 

  40. Moravec F (2007) Some aspects of the taxonomy and biology of adult spirurine nematodes parasitic in fishes: a review. Folia Parasitol 54:239–257. https://doi.org/10.14411/fp.2007.003

    Article  Google Scholar 

  41. Moravec F, Justine JL (2019) New species and new records of camallanid nematodes (Nematoda, Camallanidae) from marine fishes and sea snakes in New Caledonia. Parasite 26:66. https://doi.org/10.1051/parasite/2019068

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Takeshi Sasaki (Fujukan, University Museum, UR), Toru Naruse (Tropical Biosphere Research Center, Iriomote Station, UR) and the staff of the Research Center for Subtropical Fisheries (Seikai National Fisheries Research Institute, Fisheries Research Agency) for providing laboratory facilities. We are grateful to Nobuhiko Shimadzu (Shimadzu Alien Fishes Laboratory), Daisuke Uyeno (Kagoshima University), Hirotaka Katahira (Azabu University) and Masato Nitta (Kobe University) for assistance with fish sampling and identification. 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) and ERDF (No. CZ.02.1.01/0.0/0.0/16_013/0001775, for their support with obtaining scientific data presented in this paper, and to Blanka Škoríková of the same Institute for help with the illustrations.

Funding

This study was partly supported by the institutional support of the Institute of Parasitology, BC AS CR (RVO: 60077344) to F.M. and by the Ocean Exposition Commemorative Park Management Foundation, Okinawa, to K.N.

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Correspondence to František Moravec.

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Moravec, F., Nagasawa, K. Some Spirurid Nematodes (Spirurida) from Freshwater and Brackish-Water Fishes in Okinawa Prefecture, Japan, with Descriptions of Two New Species. Acta Parasit. 66, 163–177 (2021). https://doi.org/10.1007/s11686-020-00268-1

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