Skip to main content
Log in

Opistholobetines (Digenea: Opecoelidae) in Australian tetraodontiform fishes

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

Opistholebetine opecoelids are reported following examination of 1,041 individual tetraodontiform fishes, comprising 60 species and seven families, collected in Australian waters between 1986 and 2018. Nine species consistent with Opistholebes Nicoll, 1915, Heterolebes Ozaki, 1935 or Maculifer Nicoll, 1915 were recovered. However, phylogenetic analysis of sequence data, generated for some of these species, suggested that five genera, not three, are required to adequately accommodate these taxa. Thus, the concept and composition for each is revised, Pseudoheterolebes Yamaguti, 1959 nec Gupta, 1968 is resurrected and Parallelolebes n. g. is proposed. Of the nine species examined, five are new. Four new species are from fishes endemic to subtropical and temperate Australian waters for which no trematodes have previously been reported: Pa. australis n. sp. and Ps. corazonae n. sp. from the slender-spined porcupinefish Diodon nicthemerus Cuvier (Diodontidae) off Stanley, Tasmania; Pa. virilis n. sp. from the horse-shoe leatherjacket Meuschenia hippocrepis (Quoy & Gaimard) (Monacanthidae) off Stanley; and Ps. stellaglobulus n. sp. from the threebar pocupinefish Dicotylichthys punctulatus Kaup (Diodontidae) in Moreton Bay, south-east Queensland. The fifth new species is M. diodontis n. sp., collected from the spotted porcupinefish Diodon hystrix Linnaeus and the blackblotched porcupinefish D. liturosus Shaw, in tropical waters on the Great Barrier Reef. Species reported previously include the type-species of Opistholebes, O. amplicoelus Nicoll, 1915 from the rough golden puffer Lagocephalus lunaris (Bloch & Schneider) (Tetraodontidae) and the common toadfish Tetractenos hamiltoni (Richardson) (Tetraodontidae) in Moreton Bay, and three species reported for the first time from fishes in Australian waters: H. maculosus Ozaki, 1935, Pa. elongatus Ozaki, 1937 n. comb. and Ps. diodontis (Cable, 1956) n. comb., each from both D. hystrix and D. liturosus on the Great Barrier Reef. Following the revisions, Opistholebes is recognised for two species, Heterolebes for five, Maculifer for eight, Pseudoheterolebes for five and Parallelolebes for three.

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.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Andres, M. J., Ray, C. L., Pulis, E. E., Curran, S. S., & Overstreet, R. M. (2014). Molecular characterization of two opecoelid trematodes from fishes in the Gulf of Mexico, with a description of a new species of Helicometra. Acta Parasitologica, 59, 405–412.

    Article  CAS  Google Scholar 

  • Antar, R., Georgieva, S., Gargouri, L., & Kostadinova, A. (2015). Molecular evidence for the existence of species complexes within Macvicaria Gibson & Bray, 1982 (Digenea: Opecoelidae) in the western Mediterranean, with descriptions of two new species. Systematic Parasitology, 91, 211–229.

    PubMed  Google Scholar 

  • Bilqees, F. M. (1972). Marine fish trematodes of West Pakistan. VIII. Description of thirteen new species including a new genus Pseudocoitocaecum from fishes of Karachi coast. In: Bilqees, F. M., Saeed, R., Rehana, R., Khatoon, A. & Kaikabad, S. H. (Eds). Helminth Parasites of Some Vertebrates Chiefly from Fishes of West Pakistan. Karachi: Agricultural Research Council, Government of Pakistan, pp. 1–40.

  • Bilqees, F. M. (1981). Digenetic Trematodes Fishes of Karachi Coast. Karachi: Kifayat Academy, 207 pp.

    Google Scholar 

  • Bilqees, F. M., & Nighat, Y. (1982). Two species of the genus Opistholebes Nicoll, 1915 from the fish Diodon hystrix of Karachi Coast (Trematoda: Opistholebetidae). Pakistan Journal of Zoology, 14, 33–37.

    Google Scholar 

  • Blend, C. K., & Dronen, N. O. (2015). A review of the genus Helicometra Odhner, 1902 (Digenea: Opecoelidae: Plagioporinae) with a key to species including Helicometra overstreeti n. sp. from the cusk-eel Luiobrotula corethromycter Cohen, 1964 (Ophidiiformes: Ophidiidae) from the Gulf of Mexico. Marine Biodiversity, 45, 183–270.

    Article  Google Scholar 

  • Born-Torrijos, A., Kostadinova, A., Raga, J. A., & Holzer, A. S. (2012). Molecular and morphological identification of larval opecoelids (Digenea: Opecoelidae) parasitising prosobranch snails in a Western Mediterranean lagoon. Parasitology International, 61, 450–460.

    Article  CAS  Google Scholar 

  • Bray, R. A. (1986). Some helminth parasites of marine fishes of South Africa: families Enenteridae, Opistholebetidae and Pleorchiidae (Digenea). Journal of Natural History, 20, 471–488.

    Article  Google Scholar 

  • Bray, R. A., Cribb, T. H., Littlewood, T. J., & Waeschenbach, A. (2016). The phylogeny of the digenean family Opecoelidae Ozaki, 1925: molecular phylogenetic inference and the value of morphological characters. Parasitology International, 1, 1–10.

    Google Scholar 

  • Bravo-Hollis, M. (1954). Trematodos de peces marinos de aguas Mexicanas. VII. Anales del Instituto de Biología. Universidad Nacional Autónoma de México, 25, 219–252.

    Google Scholar 

  • Cable, R. M. (1954). The development of a species of Opistholebes in the final host, the affinities of some amphistomatous trematodes from marine fishes, and the allocreadioid problem. Journal of Parasitology, 40, 38.

    Google Scholar 

  • Cable, R. M. (1956). Opistholebes diodontis n. sp., its development in the final host, the affinities of some amphistomatous trematodes from marine fishes and the allocreadioid problem. Parasitology, 46, 1–13.

    CAS  PubMed  Google Scholar 

  • Cribb, T. H., Bray, R. A., Littlewood, D. T. J., Pichelin, S., & Herniou, E. A. (2001). The Digenea. In: Littlewood, D. T. J. & Bray, R. A. (Eds), Interrelationships of the Platyhelminthes. London: Taylor & Francis, pp. 185–186.

    Google Scholar 

  • Cribb, T. H. (1998). The diversity of the Digenea of Australian animals. International Journal for Parasitology, 28, 899–911.

    Article  CAS  Google Scholar 

  • Cribb, T. H. (2005). Family Opistholebetidae Fukui, 1929. In: Jones, A., Bray, R. A., & Gibson, D. I. (Eds), Keys to the Trematoda Volume 2. Wallingford: CAB International, pp. 533–539

  • Cribb, T. H., & Bray, R. A. (2010). Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology, 76, 1–7.

    Article  Google Scholar 

  • Dyer, W. G., Williams, E. H., & Bunkley-Williams, L. (1985). Digenetic trematodes of marine fishes of the western an southwestern coasts of Puerto Rico. Proceedings of the Helminthological Society of Washington, 52, 85–94.

    Google Scholar 

  • Dyer, W. G., Williams, E. H., & Bunkley-Williams, L. (1988). Digenetic trematodes of marine fishes of Okinawa, Japan. Journal of Parasitology, 74, 638–645.

    Article  CAS  Google Scholar 

  • Dyer, W. G., Williams, E. H., & Bunkley-Williams, L. (1992). Homalometron dowgialloi sp. n. (Homalometridae) from Haemulon flavolineatum and additional records of digenetic trematodes of marine fishes in the West Indies. Journal of the Helminthological Society of Washington, 59, 182–189.

    Google Scholar 

  • Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    Article  CAS  Google Scholar 

  • Froese, R., & Pauly, D. (2018). FishBase. 2018. www.fishbase.org. Accessed on 11 July 2018.

  • Gibson, D. I. (2014). Pycnadena pyriformis Price, 1934. Accessed through: World Register of Marine Species. http://www.marinespecies.org/aphia.php?p=taxdetails&id=757513. Accessed on 11 July 2018.

  • Gu, C. D., & Shen, J. (1979). Ten new species of digenetic trematodes of marine fishes. Acta Zoologica Sinica, 4, 342–355.

    Google Scholar 

  • Gupta, A. N. (1968a). Heterolebes spindalis sp. n., family Opistholebetidae Fukui, 1929 (Trematoda: Digenea) from Tetradon immaculatus (Cantor) and discussion on the status of the genus Heterolebes Ozaki, 1935. Acta Parasitologica Polonica, 15, 361–365.

    Google Scholar 

  • Gupta, A. N. (1968b). On three new species of Opistholebes (Opistholebetidae Fukui, 1929) from the globe fish, Tetraodon viridipunctatus (Gunther) from India. Journal of Helminthology, 42, 283–288.

    Article  Google Scholar 

  • Gupta, A. N. (1968c). Studies on Pseudoheterolebes g. n. (Trematoda: Digenea) from Tetradon viridipunctatus (Gunther) from Madras, India with the description of P. indicus sp. n. as its type-species and key to the genera of family Opistholebetidae Fukui, 1929. Acta Parasitologica Polonica, 15, 355–359.

    Google Scholar 

  • Hafeezullah, M. (1971). On some new and known digenetic trematodes from marine fishes of India. Journal of Helminthology, 45, 73–88.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Jousson, O., Bartoli, P., & Pawlowski, J. (1999). Molecular identification of developmental stages in Opecoelidae (Digenea). International Journal for Parasitology, 29, 1853–1858.

    Article  CAS  Google Scholar 

  • Krishna, P. V., & Sreeramulu, K. (1993). Ophistholebes tetrodontis (Trematoda: Digenea) a new record from Waltair Coast. Uttar Pradesh Journal of Zoology, 13, 89–90.

    Google Scholar 

  • Ku, G. T., & Shen, C.-W. (1965). Studies on some digenetic trematodes from marine fishes in China. Acta Parasitologica Sinica, 2, 355–365 (In Chinese).

    Google Scholar 

  • Lanfear, R., Calcott, B., Ho, S. Y. W., & Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.

    Article  CAS  Google Scholar 

  • Layman, E. M. (1930). Parasitic worms from the fishes of Peter The Great Bay. Bulletins of the Pacific Scientific Fishery Research Station, 3, 1–120.

    Google Scholar 

  • Liu, S. F. (1999). Description of three new species of Opistholebetidae (Trematodes: Digenea). Acta Zootaxonomica Sinica, 24, 265–271 (In Chinese).

    CAS  Google Scholar 

  • Machida, M., Ichihara, A., & Kamegai, S. (1970). Digenetic trematodes collected from the fishes in the sea north of the Tsushima Islands. Memoirs of the National Science Museum, Tokyo, 3, 101–112.

    Google Scholar 

  • Machida, M., & Kuramochi, T. (1999). Digenean trematodes from tetraodontiform fishes from Japanese and adjacent waters. Bulletin of the National Science Museum, Tokyo, Series A, Zoology, 25, 1–25.

    Google Scholar 

  • Manter, H. W. (1947). The digenetic trematodes of marine fishes of Tortugas, Florida. American Midland Naturalist, 38, 257–416.

    Article  Google Scholar 

  • Manter, H. W. (1963). Studies on digenetic trematodes of fishes of Fiji. II. Families Lepocreadiidae, Opistholebetidae, and Opecoelidae. Journal of Parasitology, 49, 99–113.

    Article  Google Scholar 

  • Manter, H. W., & Pritchard, M. H. (1962). Studies on digenetic trematodes of Hawaiian fishes: Families Fellodistomatidae, Opistholebetidae and Gyliauchenidae. Transactions of the American Microscopical Society, 81, 113–123.

    Article  Google Scholar 

  • Martin, S. B., Cutmore, S. C., & Cribb, T. H. (2017a). An updated concept and revised composition for Hamacreadium Linton, 1910 (Opecoelidae: Plagioporine) clarifies a previously obscured pattern of host-specificity among species. Zootaxa, 4254-, 151–187.

    Article  Google Scholar 

  • Martin, S. B., Cutmore, S. C., & Cribb, T. H. (2017b). Revision of Neolebouria Gibson, 1976 (Digenea: Opecoelidae), with Trilobovarium n. g., for species infecting tropical and subtropical shallow-water fishes. Systematic Parasitology, 94, 307–338.

    Article  Google Scholar 

  • Martin, S. B., Crouch, K., Cutmore, S. C., & Cribb, T. H. (2018a). Expansion of the concept of the Opistholebetinae Fukui, 1929 (Digenea: Opecoelidae Ozaki, 1925), with Magnaosimum brooksae n. g., n. sp. from Tripodichthys angustifrons (Hollard) (Tetradontiformes: Triacanthidae) in Moreton Bay, Australia. Systematic Parasitology, 95, 121–132.

    Article  CAS  Google Scholar 

  • Martin, S. B., Cutmore, S. C., & Cribb, T. H. (2018b). Revision of Podocotyloides Yamaguti, 1934 (Digenea: Opecoelidae), resurrection of Pedunculacetabulum Yamaguti, 1934 and the naming of a cryptic opecoelid species. Systematic Parasitology, 95, 1–31.

    Article  Google Scholar 

  • Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 20120, New Orleans, LA, 1–8.

  • Moravec, F., & Barus, V. (1971). Studies on parasitic worms from Cuban fishes. Vestník Ceskoslovenské Spolecnosti Zoologické, 35, 56–74.

    Google Scholar 

  • Nahhas, F. M., & Cable, R. M. (1964). Digenetic and aspidogastrid trematodes from marine fishes of Curaçao and Jamaica. Tulane Studies in Zoology, 11, 169–228.

    Article  Google Scholar 

  • Nicoll, W. (1915). The trematode parasites of north Queensland. III. Parasites of fishes. Parasitology, 8, 22–41.

    Article  Google Scholar 

  • Nikolaeva, V. M., & Kovaleva, A. A. (1966). [Parasite fauna of Trachurus from the Mediterranean Basin.] In: Delyamure, S. L. (Ed.) [Helminth fauna of animals of the southern seas.] Kiev: Naukova Dumka, pp. 67–79 (In Russian).

  • Ogawa, K., & Inouye, K. (1997). Parasites of cultured tiger puffer (Takifugu rubripes) and their seasonal occurrences, with descriptions of two new species of Gyrodactylus. Fish Pathology, 32, 7–14.

    Article  Google Scholar 

  • Olson, P. D., Cribb, T. H., Tkach, V. V., Bray, R. A., & Littlewood, D. T. J. (2003). Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755.

    Article  CAS  Google Scholar 

  • Ozaki, Y. (1935). Two new trematodes of the family Opistholebetidae Travassos. Proceedings of the Imperial Academy of Tokyo, 11, 244–246.

    Article  Google Scholar 

  • Ozaki, Y. (1937a). Studies on the trematode families Gyliauchenidae and Opistholebetidae, with special reference to lymph system. I. Journal of Science of the Hiroshima University, 5, 125–165.

    Google Scholar 

  • Ozaki, Y. (1937b). Studies on the trematode families Gyliauchenidae and Opistholebetidae, with special reference to lymph system. II. Journal of Science of the Hiroshima University, 5, 167–244.

    Google Scholar 

  • Palm, H. W., & Bray, R. A. (2014). Marine Fish Parasitology in Hawaii. Hohenwarsleben: Westarp & Partner Digitaldruck, 302 pp.

    Google Scholar 

  • Parukhin, A. M. (1970). [New species of trematodes in fish from the Red Sea.] Biologiya Morya. Kiev, 20, 267–272 (In Russian).

    Google Scholar 

  • Pérez-Ponce de León, G., Garcia-Prieto, L., & Mendoza-Garfias, B. (2007). Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa, 1534, 1–247.

    Google Scholar 

  • Prasad, B., & Radhakrishnan, S. (2010). Metazoan parasites of smooth-backed blow fish Lagocephalus inermis from Kerala, south-west coast of India. Indian Journal of Fisheries, 57, 71–76.

    Google Scholar 

  • Rigby, M. C., Lo, C. M., Cribb, T. H., Euzet, L., Faliex, E., Galzin, R., et al. (1999). Checklist of the parasites of coral reef fishes from French Polynesia, with considerations on their potential role in these fish communities. Cybium, 23, 273–284.

    Google Scholar 

  • Rima, M., Marzoug, D., Pérez-del-Olmo, A., Kostadinova, A., Bouderbala, M., & Georgieva, S. (2017). New molecular and morphological data for opecoelid digeneans in two Mediterranean sparid fishes with descriptions of Macvicaria gibsoni n. sp. and M. crassigula (Linton, 1910) (sensu stricto). Systematic Parasitology, 94, 739–763.

    Article  Google Scholar 

  • Shen, J. (1986). [Digenetic trematodes of fishes from the east China Sea I. Species of the families Opistholebetidae, Lepocreadiidae and Cryptogonimidae.] Studia Marina Sinica, 27, 209–219 (In Chinese).

  • Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313.

    Article  CAS  Google Scholar 

  • Siddiqi, A. H., & Cable, R. M. (1960). Digenetic trematodes of marine fishes of Puerto Rico. Scientific Survey of Porto Rico and the Virgin Islands, 17, 257–369.

    Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    Article  CAS  Google Scholar 

  • Tkach, V. V., Pawlowski, J., Mariaux, J., & Swiderski, Z. (2001). Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In: Littlewood, D. T. J. & Bray, R. A. (Eds), Interrelationships of the Platyhelminthes. London: Taylor and Francis, pp. 186–193.

    Google Scholar 

  • Wang, P.-Q. (1982). Some digenetic trematodes of marine fishes from Fujian Province, China. Oceanologia et Limnologia Sinica, 13, 179–194.

    Google Scholar 

  • Wee, N. Q.-X., Cribb, T. H., Bray, R. A., & Cutmore, S. C. (2017). Two known and one new species of Proctoeces from Australian teleosts: variable host-specificity for closely related species identified through mult-locus mlecular data. Parasitology International, 66, 16–26.

    Article  CAS  Google Scholar 

  • Yamaguti, S. (1938). Studies on the Helminth Fauna of Japan. Part 21. Trematodes of Fishes, IV. Kyoto: S. Yamaguti, 139 pp., 1 pl.

  • Yamaguti, S. (1940). Studies on the helminth fauna of Japan, Part 31. Trematodes of fishes, VII. Japanese Journal of Zoology, 9, 35–108.

    Google Scholar 

  • Yamaguti, S. (1959). Studies on the helminth fauna of Japan. Part 54. Trematodes of fishes, XII. Publications of the Seto Marine Biological Laboratory, 7, 241–262.

    Article  Google Scholar 

  • Yamaguti, S. (1970). Digenetic Trematodes of Hawaiian Fishes. Tokyo: Keigaku Publishing Co., 436 pp.

    Google Scholar 

  • Zhukov, E. V. (1960). [Endoparasitic worms of the fishes in the Sea of Japan and South-Kuril shallow-waters.] Trudy Zoologicheskogo Instituta. Leningrad, 28, 3–146 (In Russian).

    Google Scholar 

Download references

Acknowledgements

The authors thank the staff of the Heron Island, Lizard Island, and Moreton Bay Research Stations for their support, the various students and colleagues who helped collect fishes and specimens, and two anonymous reviewers for improving the manuscript.

Funding

SBM is supported by a Holsworth Wildlife Research Endowment, administered by the Ecological Society of Australia (ESA), an Australian Postgraduate Award (APA) and an Australian Biological Resources Study (ABRS) National Taxonomy Research Grant Programme (NTRGP) Ph. D. scholarship (No. CT215-14). Collection within Moreton Bay was part of a larger effort to characterise the metazoan parasite fauna of fishes from that region, funded by an ABRS grant (RF215-40) awarded to SCC and THC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Storm B. Martin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was conducted in compliance with all institutional, national and international guidelines on the care and use of animals.

Additional information

This article was registered in the Official Register of Zoological Nomenclature (ZooBank) as DB4F4F85-4020-401E-96ED-A1C86474A7A9. This article was published as an Online First article on the online publication date shown on this page. The article should be cited by using the doi number. This is the Version of Record.

This article is part of the Topical Collection Digenea.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martin, S.B., Ribu, D., Cutmore, S.C. et al. Opistholobetines (Digenea: Opecoelidae) in Australian tetraodontiform fishes. Syst Parasitol 95, 743–781 (2018). https://doi.org/10.1007/s11230-018-9826-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-018-9826-9

Navigation