Abstract
Examinations of some deep-sea hydrothermal vent fishes from the western and eastern regions of the Pacific Ocean revealed the presence of three new species of Ascarophis van Beneden, 1871 (Nematoda: Cystidicolidae), all gastrointestinal parasites, namely: A. justinei n. sp. from Thermarces cerberus Rosenblatt & Cohen (type host) and Thermichthys hollisi Cohen, Rosemblatt & Moser (both Zoarcidae, Perciformes) and A. globuligera n. sp. from T. cerberus from the Northern East Pacific Rise, and A. monofilamentosa n. sp. from Pyrolicus manusanus Machida & Hashimoto (Zoarcidae, Perciformes) from the Manus Basin near Papua New Guinea. Specimens are described and illustrated based on light and scanning electron microscopical examinations. In addition to other morphological differences, all the three new species differ from each other by the structure of eggs: eggs bearing a lateral superficial swelling (A. globuligera n. sp.), eggs with one conspicuously long filament on one pole (A. monofilamentosa n. sp.) and eggs smooth, without any filaments or swellings (A. justinei n. sp.). The egg morphology of the two first-named species is unique within all species of Ascarophis, which indicates that all the three newly described species of Ascarophis are probably endemic to the respective hydrothermal vents as their fish hosts.
Similar content being viewed by others
Data Availability
All samples used in this study have been deposited in the relevant curated, internationally recognised museum collection as outlined in this paper.
References
Aguilar-Aguilar, R., Ruiz-Campos, G., Martorelli, S., Montes, M. M., & Martínez-Aquino, A. (2019) A new species of Ascarophis (Nematoda: Cystidicolidae) parasitizing Clinocottus analis (Pisces: Cottidae) from Baja California, Mexico. Journal of Parasitology, 105, 524–532. https://doi.org/10.1645/19-14
Anderson, R. C. (2000) Nematode parasites of vertebrates. Their development and transmission. Second edition. CABI Publishing, Wallingford.
Appy, R. G. (1981) Species of Ascarophis van Beneden, 1870 (Nematoda: Cystidicolidae) in North Atlantic fishes. Canadian Journal of Zoology, 59, 2193–2205.
Appy, R. G., & Butterworth, E. W. (2011) Development of Ascarophis sp. (Nematoda: Cystidicolidae) to maturity in Gammarus deubeni (Amphipoda). Journal of Parasitology, 97, 1035–1048. https://doi.org/10.1645/GE-2878.1
Arai, H. P., & Smith, J. W. (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
Beveridge, I., & Moravec, F. (2020) Ascarophisnema hoiae n. sp. (Nematoda: Cystidicolidae), from the stomach of the trumpeter whiting, Sillago maculata Quoy & Gaimard (Perciformes: Sillaginidae) from Moreton Bay, Queensland, Australia. Systematic Parasitology, 97, 297–304. https://doi.org/10.1007/s11230-020-09910-A.y
Boomker, J., & Puylaert, F. A. (1994) Eight new Afrotropical Spinitectus spp. (Nematoda: Cystidicolidae) from freshwater fishes with a key to the members of the genus in the region. Onderstepoort Journal of Veterinary Research, 61, 127–142.
Brugni, N. L., & Viozzi, G. (2008) New cystidicolid species (Nematoda) from Galaxias platei (Osmeriformes: Galaxiidae) in Patagonian freshwater environments. Journal of Parasitology, 94, 841–846. https://doi.org/10.1645/GE-1367.1
Buckman, K. L. (2009) Biotic and abiotic interactions of deep-sea hydrothermal vent-endemic fish on the East Pacific Rise. Technical report, Massachusetts Institute of Technology, Cambridge.
Choudhury, A., & Nadler, S. A. (2018) Phylogenetic relationships of spiruromorph nematodes (Spirurina: Spiruromorpha) in North American freshwater fishes. Journal of Parasitology, 104, 496–504. https://doi.org/10.1645/17-195
Cohen, D. M., & Haedrich, R. L. (1983) The fish fauna of the Galápagos thermal vent region. Deep Sea Research Part A: Oceanographic Research Papers, 30, 371–379. https://doi.org/10.1016/0198-0149(83)90072-9
Černotíková, E., Horák, A., & Moravec, F. (2011) Phylogenetic relationships of some spirurine nematodes (Nematoda: Chromadorea: Rhabditida: Spirurina) parasitic in fishes inferred from SSU rRNA gene sequences. Folia Parasitologica, 58, 135–148. https://doi.org/10.14411/fp.2011.014
de Buron, I., & Morand, S. (2004) Deep-sea hydrothermal vent parasites: why do we not find more? Parasitology, 128, 1–6. https://doi.org/10.1017/s0031182003004347
Dollfus, R. Ph., & Campana-Rouget, Y. (1956) Une nouvelle espèce d’Ascarophis (Nematoda, Spirurinae) chez Gadus luscus L. Révision du genre. Annales de Parasitologie Humaine et Comparée, 31, 385–404.
Dykman, L. N., Tepolt, C. K., Kuris, A. M., Solow, A. R., & Mullineaux, L. S. (2023) Parasite diversity at isolated, disturbed hydrothermal vents. Proceedings of the Royal Society B, 290, 20230877. https://doi.org/10.1098/rspb2023.0877
Fagerholm, H.-P., & Berland, B. (1988) Description of Ascarophis arctica Poljansky, 1952 (Nematoda: Cystidicolidae) in Baltic Sea fishes. Systematic Parasitology, 11, 151–158.
Fagerholm, H-P., & Butterworth, E. W. (1988) Ascarophis sp. (Nematoda: Spirurida) attaining sexual maturity in Gammarus spp. (Crustacea). Systematic Parasitology, 12, 123–139.
Ferrer, E., Aznar, F. J., Balbuena, J. A., Kostadinova, A., Raga, J. A., & Moravec, F. (2005) A new cystidicolid nematode from Mullus surmuletus (Perciformes: Mullidae) from the western Mediterranean. Journal of Parasitology, 91, 335–344. https://doi.org/10.1645/GE-366R
Froese, R., & Pauly, D. (Eds.) (2023). FishBase. World Wide Web electronic publication. http://www.fishbase.org, version 05/2023
ICZN (2012) International Commision 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. https://doi.org/10.21805/bzn.v69i3.a8.161
Justine, J.-L., Cassone, J., & Petter, A. (2002) Moravecnema segonzaci gen et sp. n. (Nematoda: Cystidicolidae) from Pachycara thermophilum (Zoarcidae), a deep-sea hydrothermal vent fish from the Mid-Atlantic Ridge. Folia Parasitologica, 49, 299–303. https://doi.org/10.14411/fp.2002.055
Ko, R. C. (1986) A preliminary review of the genus Ascarophis van Beneden, 1871 (Nematoda: Cystidicolidae) of the gastrointestinal tract of fishes. Department of Zoology, University of Hong Kong, Hong Kong.
Machida, M. (1981) Two new species of Ascarophis (Nematoda, Spirurida) from marine fishes of Japan and Palau. Bulletin of the National Science Museum, Series A (Zoology), 7, 1–5.
Machida, M., & Syahailatua, A. (1994) A new species of cystidicolid nematode from driftfish of Indonesia. Proceedings of the Japanese Society of Systematic Zoology, No. 50, 1–5.
Martorelli, S. R., Navone, G. T., & Ivanov, V. (2000) Proposed life cycle of Ascarophis marina (Nematoda: Cystidicolidae) in Argentine waters. Journal of Parasitology, 86, 1047–1050. https://doi.org/10.1645/0022-3395(2000)086[1047:PLCOAM]2.0.CO;2
Moravec, F. (2007) Some aspects of the taxonomy and biology of adult spirurine nematodes parasitic in fishes: a review. Folia Parasitologica, 54, 239–257. https://doi.org/10.14411/fp.2007.033
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 Parasitologica, 55, 144–160. https://doi.org/10.2478/s11686-010-0017-3
Moravec, F., & González-Solís, D. (2007) Structure of the cephalic end of Ascarophis mexicana (Nematoda: Cystidicolidae), as revealed by SEM. Folia Parasitologica, 54, 155–156. https://doi.org/10.14411/fp.2007.021
Moravec, F., & Justine, J.-L. (2007) A new species of Ascarophis (Nematoda, Cystidicolide) from the stomach of the marine scorpaeniform fish Hoplichthys citrinus from a seamount off the Chesterfield Islands, New Caledonia. Acta Parasitologica, 52, 238–246. https://doi.org/10.2478/s11686-007-0026-z
Moravec, F., & Justine, J.-L. (2009) Two cystidicolids (Nematoda, Cystidicolidae) from marine fishes off New Caledonia. Acta Parasitologica, 54, 341–349. https://doi.org/10.2478/s11686-009-0058-7
Moravec, F., & Klimpel, S. (2009) Two new species of cystidicolid nematodes from the digestive tract of the deep-sea fish Coryphaenoides mediterraneus (Giglioli) (Macrouridae) from the Mid-Atlantic Ridge. Systematic Parasitology, 73, 37–47. https://doi.org/10.1007/s11230-009-9182-x
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. https://doi.org/10.14411/fp.2018.016
Moravec, F., & Nagasawa, K. (2021) Some spirurid nematodes (Spirurida) from freshwater and brackish-water fishes in Okinawa Prefecture, Japan, with descriptions of two new species. Acta Parasitologica, 66, 163–177. https://doi.org/10.1007/s11686-020-00268-1
Moravec, F., Shamsi, S., & Justine, J.-L. (2021) Redescription of Ascarophis distorta Fusco et Overstreet, 1978 (Nematoda, Cystidicolidae) from the stomach of some butterflyfishes off New Caledonia. Acta Parasitologica, 66, 907–914. https://doi.org/10.1007/s11686-021-00359-7
Moravec, F., Yooyen, T., & Sanprick, A. (2018) Two nematode species from freshwater and marine fishes in Thailand, including Ascarophia scatophagi sp. nov. (Cystidicolidae) from Scatophagus argus (Scatophagidae). Acta Parasitologica, 63, 89–98. https://doi.org/10.1515/ap-2018-0010
Muñoz, G., & George-Nascimento, M. (2007) Two new species of Ascarophis (Nematoda: Cystidicolidae) in marine fishes from Chile. Journal of Parasitology, 93, 1178–1188. https://doi.org/10.1645/GE-1169R1.1
Odening, K. (1976) Conception and terminology of hosts in parasitology. Advances in Parasitology, 14, 1–93.
Parukhin, A. M. (1978) [New species of nematodes from fish in the Indian Ocean.] Materialy Nauchnoy Konferentsii Vsesoyuznogo Obshchestva Gel’mintologii (VOG), Moscow, pp. 125–129. (in Russian)
Pereira, A. N., Timi, J. T., Vieira, F. M., & Luque, J. L. (2012) A new species of Neoascarophis (Nematoda: Cystidicolidae) parasitic in Mullus argentinae (Perciformes: Mullidae) from the Atlantic coast of South America. Folia Parasitologica, 59, 64–70. https://doi.org/10.14411/fp.2012.010
Pereira, F. B., Pereira, A. N., Timi, J. T. & Luque, J. L. (2013) Pseudascarophis brasiliensis sp. nov. (Nematoda: Cystidicolidae) parasitic in the Bermuda chub Kyphosus sectatrix (Perciformes: Kyphosidae) from southeastern Brazil. Memórias do Instituto Oswaldo Cruz, 108, 476–480. https://doi.org/10.1590/0074-02761080420130
Pinto, R. M., Vicente, J. J., & Noronha, D. (1984) First report of Ascarophis van Beneden, 1871: A. brasiliensis n. sp. (Nematoda, Ascarophidinae) and Procamallanus (Spirocamallanus) pereirai Annereaux, 1946 (Nematoda, Procamallaninae) in South America. Memórias do Instituto Oswaldo Cruz, 79, 491–494. https://doi.org/10.1590/S0074-02761984000400015
Polyanskiy, Yu. I. (1952) [Some new and little-known parasitic nematodes from the intestine of marine fishes.] Trudy Zoologicheskogo Instituta. Akademiya Nauk SSSR, 12, 133–147. (in Russian)
Sancho, G., Fisher, C. R., Mills, S., Micheli, F., Johnson, G. A., Lenihan, H. S., Peterson, C. H., & Mullineaux, L. S. (2005) Selective predation by the zoarcid fish Thermarces cerberus at hydrothermal vents. Deep Sea Reseach Part I: Oceanographic Research Papers, 52, 837-844. https://doi.org/10.1016/j.dsr.2004.12.002
Skryabin, K. I., Sobolev, A. A., & Ivashkin, V. M. (1967) [Spirurata of animals and man and the diseases caused by them. Part 4, Thelazioidea.] Nauka, Moscow (in Russian).
Van Dover, C. L., German, C. R., Speer, K. G., Parson, L. M., & Vrijenhoek, R. C. (2002) Evolution and biogeography of deep-sea vent and seep invertebrates. Science, 295, 1253–1257. https://doi.org/10.1126/science.1067361
Zhukov, E. V. (1960) [Endoparasitic worms of fishes of the Sea of Japan and the South-Kurile shallow waters.] Trudy Zoologicheskogo Instituta. Akademiya Nauk SSSR, 28, 3–146 (in Russian with English summary).
Acknowledgements
We thank Lauren Mullineaux at the Woods Hole Oceanographic Institution and Cindy Van Dover at Duke University for supporting research and cruises and for procuring samples. We thank Gorka Sancho at the College of Charleston, Kate Buckman at Dartmouth, and Timothy Shank at Woods Hole Oceanographic Institution for donating additional samples. Field samples from the East Pacific Rise were made possible by the captain and crew of the RV Atlantis and RV Roger Revelle and the operators of HOV Alvin and ROV Jason. The at-sea component of the Papua New Guinea Luk Luk Cruise to Manus Basin was made possible by the captain and crew of Global Marine’s Wawe Mercury, the UTEC suvey staff, the Helix Offshore staff, the ROV operators, and Nautilus Minerals personnel, especially S. Smith, in collaboration with Cindy Van Dover. The Manus Basin samples were analyzed on behalf of the people of Papua New Guinea. We are grateful to John Mike Kinsella at the HelmWet Laboratory, Missoula, MT, for his preliminary examination of the present nematodes and their generic 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 the 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, Biology Centre of the Czech Academy of Sciences (RVO: 60077344 awarded to FM). Research cruises to the East Pacific Rise were supported by National Science Foundation (NSF) grants OCE BIO-1829773, OCE BIO-1948580, OCE-9619605, and OCE-9711233 to LS Mullineaux, and OCE-988550 and OCE-9982999 to CL Van Dover. LND was supported by NSF grants OCE BIO-1829773 and OCE BIO-1948580 to LS Mullineaux.
Author information
Authors and Affiliations
Contributions
Lauren N. Dykman and Deiric B. Davis obtained the samples and undertook the processing for morphological identification of the nematodes. František Moravec carried out the identification and morphological analysis and drafted the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Conflict of interest
The authors declare that there is 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:45458B06-D58D-4722-A230-5E0EB81415F7” 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.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Moravec, F., Dykman, L.N. & Davis, D.B. Three new species of Ascarophis van Beneden, 1871 (Nematoda: Cystidicolidae) from deep-sea hydrothermal vent fishes of the Pacific Ocean. Syst Parasitol 101, 2 (2024). https://doi.org/10.1007/s11230-023-10130-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11230-023-10130-3