Skip to main content
Log in

First molecular description of Neorhadinorhynchus nudus (Acanthocephala: Cavisomidae) from fish in the pacific coast of Vietnam, with notes on biogeography

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

Neorhadinorhynchus nudus (Harada, 1938) Yamaguti, 1939 (Cavisomidae) was morphologically described from the frigate tuna Auxis thazard (Lacépède) (Scombridae) in Nha Trang, Pacific south Vietnam. Females of N. nudus were fully described for the first time in the Pacific. Its original inadequate description as Rhadinorhynchus nudus (Harada, 1938) was corrected in material from Fiji Island, the Red Sea and Pacific Vietnam and errors in the text and line drawings of Harada were repeated in subsequent major publications where it underwent considerable nomenclature changes. New descriptive and biogeographical notes are included. We also provided here the molecular characterization of the nuclear gene (18S) and the mitochondrial cytochrome c oxidase subunit 1 (cox1) sequence data of N. nudus. Furthermore, to elucidate the phylogenetic relationship of N. nudus within the family Cavisomidae and with other isolates were performed incorporating nuclear (18S) and mitochondrial (cox1) sequence data using maximum likelihood (ML) and Bayesian inference (BI). The phylogenetic results showed that N. nudus has a relationship with other isolates of the same species and the median-joining network showed the pattern of haplotypes that reflected the structure of the populations.

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.

Similar content being viewed by others

References

  • Amin, O. M. (1975). Variability in Acanthocephalus parksidei Amin, 1974 (Acanthocephala: Echinorhynchidae). The Journal of Parasitology, 61, 307–317.

    Article  CAS  PubMed  Google Scholar 

  • Amin, O. M. (1984). Variability and redescription of Acanthocephalus dirus (Acanthocephala: Echinorhynchidae) from freshwater fishes in North America. Proceedings of the Helminthological Society of Washington, 51, 225–237. https://doi.org/10.1007/s11230-022-10041-9

    Google Scholar 

  • Amin, O. M. (2013). Classification of the Acanthocephala. Folia Parasitologica, 60, 273–305. https://doi.org/10.14411/fp.2013.031

    Article  PubMed  Google Scholar 

  • Amin, O. M., Chaudhary, A., & Singh, H. S. (2022). New perspectives of Microsentis wardae Martin & Multani, 1966 (Acanthocephala: Neoechinorhynchidae) from Gillichthys mirabilis Cooper in California, with scanning electron microscopy images and energy dispersive X-ray analysis. Journal of Helminthology, 96, e42. https://doi.org/10.1017/S0022149X22000347

    Article  CAS  PubMed  Google Scholar 

  • Amin, O. M., & Ha, N. V. (2011). On four species of Echinorhynchid acanthocephalans from marine fish in Halong Bay, Vietnam, including the description of three new species and a key to species of Gorgorhynchus. Parasitology Research, 109, 841–847. https://doi.org/10.1007/s00436-011-2310-y

    Article  PubMed  Google Scholar 

  • Amin, O. M., Heckmann, R. A., & Ha, N. V. (2018). Descriptions of Neorhadinorhynchus nudum (Cavisomidae) and Heterosentis paraholospinus n. sp. (Arhythmacanthidae) (Acanthocephala) from fish along the pacific coast of Vietnam, with notes on biogeography. Journal of Parasitology, 104, 486–495. https://doi.org/10.1645/17-176

    Article  PubMed  Google Scholar 

  • Amin, O. M., & Nahhas, F. M. (1994). Acanthocephala of marine fishes off Fiji Islands, with descriptions of Filisoma longcementglandus n. sp., Neorhadinorhynchus macrospinosus n. sp. (Cavisomidae), and gravid females of Rhadinorhynchus johnstoni (Rhadinorhynchidae); and keys to species of the genera Filisoma and Neorhadinorhynchus. Journal of Parasitology, 80, 768–774.

    Article  CAS  PubMed  Google Scholar 

  • Amin, O. M., & Redlin, M. J. (1980). The effect of host species on growth and variability of Echinorhynchus salmonis Müller, 1784 (Acanthocephala: Echinorhynchidae), with special reference to the status of the genus. Systematic Parasitology, 2, 9–22.

    Article  Google Scholar 

  • Awachie, J. B. E. (1966). The development and life history of Echinorhynchus truttae Schrank, 1788 (Acanthocephala). Journal of Helminthology, 40, 11–32. https://doi.org/10.1017/s0022149x00034040

    Article  CAS  PubMed  Google Scholar 

  • Ayling, T., & Cox, G. (1982). Collings guide to sea fishes of New Zealand. William Collins Publishers., Ltd., Aukland, New Zealand. ISBN 0-00-216987-8.

  • Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

    Article  CAS  PubMed  Google Scholar 

  • Brown, A. F. (1987). Anatomical variability and secondary sexual characteristics in Pomphorhynchus laevis (Müller, 1776) (Acanthocephala). Systematic Parasitology, 9, 213–219. https://doi.org/10.1007/BF00010856

    Article  Google Scholar 

  • Buckner, S. C., & Nickol, B. B. (1975). Morphological variation of Moniliformis moniliformis (Bremser, 1811) Travassos, 1915 and Moniliformis clarki (Ward, 1917) Chandler 1921. Journal of Parasitology, 61, 996–998.

    Article  CAS  PubMed  Google Scholar 

  • FAO. (1997). Review of the state of world fishery resources: Marine fisheries. FAO Corporate Document Repository. FAO Fisheris Circular N. 920 FIRM/C920. Marine Resource Service, FAO, Rome, Italy. Provide the total number of pages in this article. ISSN 0429-9329.

  • Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.

    CAS  PubMed  Google Scholar 

  • Froese, R., & Pauly, D. (2004). Myctophidae in FishBase. December, 2004 version.

  • Gaevskaya, A. V. (1977). The helminth fauna of the Atlantic squid Stenoteuthis pteropus (Steenstrup). Nauchnye Doklady Vyshei Shkoly, Biologicheskie Nauki, 8, 47–52.

    Google Scholar 

  • García-Varela, M., Hernández-Orts, J. S., López-Jiménez, A., & González-García, M. T. (2023). Molecular and morphological characterization of Andracantha gravida (Alegret, 1941) (Acanthocephala: Polymorphidae) in piscivorous birds from the Gulf of Mexico. Journal of Helminthology, 97, e31. https://doi.org/10.1017/S0022149X22000955

    Article  PubMed  Google Scholar 

  • García-Varela, M., & Pinacho-Pinacho, C. (2020). Molecular characterization of Neoechinorhynchus cylindratus Van Cleave, 1913 (Acanthocephala: Neoechinorhynchidae), a parasite of the largemouth bass (Micropterus salmoides) in northern Mexico. Journal of Helminthology, 94, e18. https://doi.org/10.1017/S0022149X18001104

    Article  Google Scholar 

  • Gartner, Jr. J. V., Hopkins, T. L., Baird, R. C., & Millken, D. M. (1987). The lanternfishes (Pisces: Myctophidae) of the eastern Gulf of Mexico. Fishery Bulletin, 85, 81–98.

    Google Scholar 

  • Golvan, Y. J. (1969). Systématique des Acanthocéphales (Acanthocephala Rudolphi, 1801). Premiére Partie. L’Ordre des Palaeacanthocephala Meyer, 1931. Premier fascicule. La Superfamille des Echinorhynchoidae (Cobbold, 1876) Golvan et Houin, 1963. Mémoires du Museum National d’Histoire Naturelle, 57, 1–373. https://biostor.org/reference/249582

    Google Scholar 

  • Harada, I. (1938). Acanthocephalen aus Formosa. Annotationes Zoologicae Japanense, 17, 419–427.

    Google Scholar 

  • Hassanine, R. M. E. L.-S. (2006). Acanthocephalans from Red Sea fishes. Family Cavisomidae Meyer, 1932: seasonal cycle of Diplosentis nudus (Harada, 1938) Pichelin et Cribb, 2001 in a definitive fish host, and a comment on Sclerocollum Schmidt et Paperna, 1978. Acta Parasitologica, 51, 123–129. https://doi.org/10.2478/s11686-006-0019-3

    Article  Google Scholar 

  • Huston, D. C., Cribb, T. H., & Smales, L. R. (2020). Molecular characterisation of acanthocephalans from Australian marine teleosts: proposal of a new family, synonymy of another and transfer of taxa between orders. Systematic Parasitology, 97, 1–23. https://doi.org/10.1007/s11230-019-09896-2

    Article  PubMed  Google Scholar 

  • Li, L., Chen, H. X., Amin, O. M., & Yang, Y. (2017). Morphological variability and molecular characterization of Pomphorhynchus zhoushanensis sp. nov. (Acanthocephala: Pomphorhynchidae), with comments on the systematic status of Pomphorhynchus monticelli, 1905. Parasitology International, 66, 693–698. https://doi.org/10.1016/j.parint.2017.05.010

    Article  CAS  PubMed  Google Scholar 

  • Li, L., Wayland, M. T., Chen, H. X., & Yang Y. (2018a). Remarkable morphological variation in the proboscis of Neorhadinorhynchus nudus (Harada, 1938) (Acanthocephala: Echinorhynchida). Parasitology, 146, 348–355. https://doi.org/10.1017/S003118201800166X

    Article  PubMed  Google Scholar 

  • Li, L., Chen, H. X., Yang, Y. (2018b). Morphological and molecular study of Neorhadinorhynchus nudus (Harada, 1938) (Acanthocephala: Cavisomidae) from Auxis thazard Lacépède (Perciformes: Scombridae) in the South China Sea. Acta Parasitologica, 63, 479–485. https://doi.org/10.1515/ap-2018-0057

    Article  CAS  PubMed  Google Scholar 

  • Lisitsyna, O., Xi, B. W., Orosova, M., Bark, D., & Oros, M. (2022). The erection of a new genus, Neotegorhynchus n. g. (Palaeacanthocephala, Illiosentidae), with a redescription of Neotegorhynchus cyprini n. comb. from Cyprinus carpio from the Yangtze River basin, China. Zootaxa, 5150, 83–96. https://doi.org/10.11646/zootaxa.5150.1.4

    Article  PubMed  Google Scholar 

  • Milne, I., Lindner, D., Bayer, M., Husmeier, D., McGuire, G., Marshall, D. F., & Wright, F. (2009). TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics, 25, 126–127. https://doi.org/10.1093/bioinformatics/btn575

    Article  CAS  PubMed  Google Scholar 

  • Mordinova, T. N. (1988). Neorhadinorhynchus myctophumi (Acanthocephala) a new acanthocephalan species from Atlantic myctophid fish. Zoologicheskii Zhurnal, 67, 1411–1414. (In Russian)

    Google Scholar 

  • Near, T. J., Garey, J. R., Nadler, S. A. (1998). Phylogenetic relationships of the Acanthocephala inferred from 18S ribosomal DNA sequences. Molecular Phylogenetics and Evolution, 10, 287–298. https://doi.org/10.1006/mpev.1998.0569

    Article  CAS  PubMed  Google Scholar 

  • Nguyen, T. H., Dorny, P., Nguyen, T. H. G., & Dermauw, V. (2021). Helminth infections in fish in Vietnam: a systematic review. International Journal for Parasitology: Parasites and Wildlife, 14, 13-32. https://doi.org/10.1016/j.ijppaw.2020.12.001

    PubMed  Google Scholar 

  • Ortega-Olivares, M. P., Velázquez-Urrieta, Y., Sereno-Uribe, A. L., Harvey, M. B., & García-Varela, M. (2023). A molecular and ecological study of Macracanthorhynchus ingens (von Linstow, 1879) (Acanthocephala: Archiacanthocephala), in its paratenic and definitive hosts in southeastern Mexico and the Eastern USA. Systematic Parasitology, 100, 543–556. https://doi.org/10.1007/s11230-023-10104-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Pigliucci, M., Murren, C. J., & Schlichting, C. D. (2006). Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology, 209, 2362–2367. https://doi.org/10.1242/jeb.02070

    Article  PubMed  Google Scholar 

  • Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256. https://doi.org/10.1093/molbev/msn083

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez, S. M., Amin, O. M., Heckmann, R. A., Sharifdini, M., & D'Elía, G. (2022). Phylogeny and Life Cycles of the Archiacanthocephala with a Note on the Validity of Mediorhynchus gallinarum. Acta Parasitologica, 67, 369–379. https://doi.org/10.1007/s11686-021-00472-7

    Article  PubMed  Google Scholar 

  • Rozas, J., Sánchez-DelBarrio, J. C., Messeguer, X., & Rozas R. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19, 2496–2497. https://doi.org/10.1093/bioinformatics/btg359

    Article  CAS  PubMed  Google Scholar 

  • Ru, S. S., Yang, R. J., Chen, H. X., Kuzmina, T. A., Spraker, T. R., & Li, L. (2022). Morphology, molecular characterization and phylogeny of Bolbosoma nipponicum Yamaguti, 1939 (Acanthocephala: Polymorphidae), a potential zoonotic parasite of human acanthocephaliasis. International Journal for Parasitology: Parasites and Wildlife, 18, 212–220. https://doi.org/10.1016/j.ijppaw.2022.06.003

    PubMed  PubMed Central  Google Scholar 

  • Santoro, M., Palomba, M., Gili, C., Marcer, F., Marchiori, E., & Mattiucci, S. (2021). Molecular and morphological characterization of Bolbosoma balaenae (Acanthocephala: Polymorphidae), a neglected intestinal parasite of the fin whale Balaenoptera physalus. Parasitology, 148, 1293–1302. https://doi.org/10.1017/S0031182021000925

    Article  CAS  PubMed  Google Scholar 

  • Schmidt, G. D. (1985). Development and life cycles. In D.W.T. Crompton, & B.B. Nickol (Eds.), Biology of the Acanthocephala (pp. 273–286). Cambridge University Press, Cambridge.

    Google Scholar 

  • Schmidt, G. D., & Paperna, I. (1978). Sclerocollum rubrimaris gen. and sp. n. (Rhadinorhynchidae: Gorgorhynchinae), and other Acanthocephala of marine fishes from Israel. Journal of Parasitology, 64, 846–850.

    Article  Google Scholar 

  • Shostak, A. W., Dick, T. A., Szalai, A. J., & Bernier, L. M. J. (1986). Morphological variability in Echinorhynchus gadi, E. leidyi, and E. salmonis (Acanthocephala: Echinorhynchidae) from fishes in northern Canadian waters. Canadian Journal of Zoology, 64, 985–995. https://doi.org/10.1139/z86-148

    Article  Google Scholar 

  • Shotton, R. (1995). Deepwater fisheries. In Review of the state of world marine fishery resources. FAO Fisheries technical paper 457, FAO, Rome.

  • Smales, L. R., Al Hasson, H. A. H., Al-Niaeem, K. S., Al-Azizz, S. A. (2015). A new species of Neorhadinorhynchus (Acanthocephala: Cavisomidae) from Platax teira (Ephippidae) from Iraqi marine waters. Transactions of the Royal Society of South Australia, 140, 1–6. https://doi.org/10.1080/03721426.2015.1115458

    Google Scholar 

  • Sobecka, E., Szostakowska, B., MacKenzie, K., Hemmingsen, W., Prajsnar, S., & Eydal, M. (2012). Genetic and morphological variation in Echinorhynchus gadi Zoega in Müller, 1776 (Acanthocephala: Echinorhynchidae) from Atlantic cod Gadus morhua L. Journal of Helminthology, 86, 16–25. https://doi.org/10.1017/S0022149X10000891

    Article  CAS  PubMed  Google Scholar 

  • Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38, 3022–3027. https://doi.org/10.1093/molbev/msab120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tkach, V. V., Lisitsyna, O. I., Crossley, J. L., Binh, T. T., & Bush, S. E. (2013). Morphological and molecular differentiation of two new species of Pseudoacanthocephalus petrochenko, 1958 (Acanthocephala: Echinorhynchidae) from amphibians and reptiles in the Philippines, with identification key for the genus. Systematic Parasitology, 85, 11–26. https://doi.org/10.1007/s11230-013-9409-8

    Article  PubMed  Google Scholar 

  • Truong, T. V., Ngo, H. T. T., Bui, T. Q., Palm, H. W., & Bray, R. A. (2022). Marine fish parasites of Vietnam: a comprehensive review and updated list of species, hosts, and zoogeographical distribution. Parasite, 29, 36. https://doi.org/10.1051/parasite/2022033

    Article  PubMed  PubMed Central  Google Scholar 

  • Wayland, M. T., Gibson, D. I., & Sommerville, C. (2005). Morphometric discrimination of two allozymically diagnosed sibling species of the Echinorhynchus gadi Zoega in Muller complex (Acanthocephala) in the North Sea. Systematic Parasitology, 60, 139–149.

    Article  PubMed  Google Scholar 

  • Yamaguti, S. (1939). Studies on the helminth fauna of Japan. Part 29. Acanthocephala II. Japanese Journal of Zoology, 13, 317–351.

    Google Scholar 

Download references

Acknowledgements

This project was supported by an Institutional Grant from the Parasitology Center, Inc. (PCI), Scottsdale, Arizona. The authors thank the Head, Department of Zoology, Chaudhary Charan Singh University, Meerut, for providing laboratory facilities.

Author information

Authors and Affiliations

Authors

Contributions

OA. Wrote the manuscript except the molecular part. AC. Contributed the molecular text and figures. MS. Initial molecular analysis HS. Provided lab. support.

Corresponding author

Correspondence to Omar M. Amin.

Ethics declarations

Competing interests

The authors declare no conflicts of interest and that they have observed all applicable ethical standards.

Additional information

Publisher's Note

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

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amin, O.M., Chaudhary, A., Sharifdini, M. et al. First molecular description of Neorhadinorhynchus nudus (Acanthocephala: Cavisomidae) from fish in the pacific coast of Vietnam, with notes on biogeography. Syst Parasitol 101, 23 (2024). https://doi.org/10.1007/s11230-023-10139-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11230-023-10139-8

Navigation