Skip to main content
Log in

Retroporomonorchis pansho n. g., n. sp., an unusual monorchiid trematode exploiting an atypical host

  • Published:
Systematic Parasitology Aims and scope Submit manuscript

Abstract

The Monorchiidae Odhner, 1911 are well represented in tropical and subtropical marine fishes worldwide but rarely reported from the Lutjanidae, an important family of tropical fishes that prey mainly on demersal fishes, decapods and cephalopods. Here, we report the first monorchiid from a lutjanid in Australian waters, Retroporomonorchis pansho n. g., n. sp. in Lutjanus fulvus (Forster), off Lizard Island on the northern Great Barrier Reef. It is morphologically and phylogenetically distinct among known monorchiids, resolves within the Monorchiinae Odhner, 1911, and is characterised by a relatively large ventral sucker, a sinistral genital pore immediately posterior to the ventral sucker, unfilamented eggs, a single testis, and vitelline follicles restricted to the level of the gonads. We assessed all previous records of monorchiids from lutjanid fishes and found only one to be convincing, that of Infundiburictus overstreeti (Gupta & Gupta, 1990) Wee, Cutmore, Pérez-del-Olmo & Cribb, 2020 from Lutjanus monostigma (Cuvier) in the Bay of Bengal. Another, Monorcheides xishaensis Shen, 1985, from Lutjanus argentimaculatus (Forsskål) in the Paracel Islands, South China Sea, is here recognised as a cryptogonimid, and is synonymised with Siphoderina asiatica Gu & Shen, 1979. In the remaining reports, the identity of the host is either ambiguous or doubtful, or the identity of the worm is not supported with sufficient evidence.

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

  • Allen, G. R. (1985). FAO species catalogue: Vol. 6 Snappers of the world: An annotated and illustrated catalogue of lutjanid species known to date. Rome: Food and Agricultural Organization of the United Nations.

  • Amato, J. F. R. (1982). Digenetic trematodes of percoid fishes of Florianópolis, southern Brasil - Monorchiidae, with the description of two new species. Revista Brasileira de Biologia, 42, 701–719.

  • Andres, M. J., Pulis, E. E., Curran, S. S., & Overstreet, R. M. (2018). On the systematics of some marine haploporids (Trematoda) with the description of a new species of Megasolena Linton, 1910. Parasitology International, 67, 805–815.

  • Ankenbrand, M. J., Keller, A., Wolf, M., Schultz, J., & Förster, F. (2015). ITS2 Database V: Twice as much. Molecular Biology and Evolution, 32, 3030–3032.

  • Atopkin, D. M., Besprozvannykh, V. V., Ngo, H. D., Van Ha, N., Van Tang, N., Ermolenko, A. V., et al. (2017). Morphometric and molecular data of the two digenean species Lasiotocus lizae Liu, 2002 (Monorchiidae) and Paucivitellosus vietnamensis sp. n. (Bivesiculidae) from mullet fish in Tonkin Bay, Vietnam. Journal of Helminthology, 91, 346–355.

  • Bagnato, E., Gilardoni, C., Pina, S., Rodrigues, P., & Cremonte, F. (2016). Redescription and life cycle of the monorchiid Postmonorcheides maclovini Szidat, 1950 (Digenea) from the Southwestern Atlantic Ocean: Morphological and molecular data. Parasitology International, 65, 44–49.

  • Bartoli, P. (1965). Lasiotocus longicystis n. sp. (Trematoda, Digenea, Monorchiidae), metacercaire parasite de Lamellibranches marins; recherches experimentales sur son development. Bulletin de la Societe Zoologique de France, 90, 119–129.

  • Bartoli, P., Jousson, O., & Russell-Pinto, F. (2000). The life cycle of Monorchis parvus (Digenea: Monorchiidae) demonstrated by developmental and molecular data. Journal of Parasitology, 86, 479–489.

  • Besprozvannykh, V. V., Ermolenko, A. V., & Atopkin, D. M. (2012). The life cycle of Asymphylodora percotti sp. n. (Trematoda: Lissorchiidae) in the Russian Southern Far East. Parasitology International, 61, 235–241.

  • Bravo-Hollis, M. (1956). Trematodes de peces marinos de aguas Mexicanas. XI. Estudio de 17 digeneoss de las costas del Pacifico, incluyendo seis especies nuevas y un genero nuevo. Anales del Instituto de Biologia, Universidad Nacional Autonoma de Mexico, 27, 245–275.

  • Bray, R. A., Cribb, T. H., & Cutmore, S. C. (2018a). Lepocreadiidae Odhner, 1905 and Aephnidiogenidae Yamaguti, 1934 (Digenea: Lepocreadioidea) of fishes from Moreton Bay, Queensland, Australia, with the erection of a new family and genus. Systematic Parasitology, 95, 479–498.

  • Bray, R. A., Cutmore, S. C., & Cribb, T. H. (2018b). Lepotrema Ozaki, 1932 (Lepocreadiidae: Digenea) from Indo-Pacific fishes, with the description of eight new species, characterised by morphometric and molecular features. Systematic Parasitology, 95, 693–741.

  • Cole, A. J., & Pratchett, M. S. (2014). Diversity in diet and feeding behaviour of butterflyfishes: reliance on reef corals versus reef habitats. In: Pratchett, M. S., Berumen, M. L. & Kapoor, B. G. (Eds) Biology of Butterflyfishes. Boca Raton, Florida, USA: CRC Press, pp. 107–139.

  • 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.

  • Cribb, T. H., Wee, N. Q.-X., Bray, R. A., & Cutmore, S. C. (2018). Monorchis lewisi n. sp. (Trematoda: Monorchiidae) from the surf bream, Acanthopagrus australis (Sparidae), in Moreton Bay, Australia. Journal of Helminthology, 92, 100–108.

  • Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772.

  • DeMartini, J. D., & Pratt, I. (1964). The life cycle of Telolecithus pugetensis Lloyd & Guberlet, 1932 (Trematoda: Monorchiidae). Journal of Parasitology, 50, 101–105.

  • Duarte, L. O., & García, C. B. (1999). Diet of the mutton snapper Lutjanus analis (Cuvier) from the gulf of Salamanca, Colombia, Caribbean Sea. Bulletin of Marine Science, 65, 453–465

    Google Scholar 

  • Durio, W. O., & Manter, H. W. (1968). Some digenetic trematodes of marine fishes of New Caledonia. Part. 1. Bucephalidae, Monorchiidae, and some smaller families. Proceedings of the Helminthological Society of Washington, 35, 143–153.

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

  • Gobert, B., Guillou, A., Murray, P., Berthou, P., Oqueli Turcios, M. D., Lopez, E., et al. (2005). Biology of queen snapper (Etelis oculatus: Lutjanidae) in the Caribbean. Fishery Bulletin, 103, 417–425.

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

  • Gu, C. D., & Shen, J. (1983). Digenetic trematodes of fishes from the Xisha Islands, Guangdong Province, China. I. Studia Marina Sinica, 20.

  • Gupta, V. C., & Gupta, P. C. (1990). Lasiotocus overstreeti new species (Digenea: Monorchiide) from a marine fish, Lutianus lioglossus (Bleeker) at Deegha Coast, West Bengal, India. Rivista di Parassitologia, 6, 159–163.

  • Harmelin-Vivien, M. L., & Bouchon-Navaro, Y. (1983). Feeding diets and significance of coral feeding among chaetodontid fishes in Moorea (French Polynesia). Coral Reefs, 2, 119–127.

  • 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.

  • Keller, A., Schleicher, T., Schultz, J., Müller, T., Dandekar, T., & Wolf, M. (2009). 5.8S-28S rRNA interaction and HMM-based ITS2 annotation. Gene, 430, 50–57.

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549.

  • Linton, E. (1910). Helminth fauna of the Dry Tortugas. II. Trematodes. Papers from the Tortugas Laboratory of the Carnegie Institute of Washington, 4, 11–98.

  • Liu, S.-f. (1996). Two new species of trematodes parasitic in marine fishes from Fujian, China (Trematoda: Digenea: Cryptogonimidae). Acta Zootaxonomica Sinica, 21, 10–17.

  • Looss, A. (1907). Zur Kentnis der Distomenfamilie Hemiuridae. Zoologischer Anzeiger, 31, 585–620.

  • Machida, M. (2005). Monorchiidae (Trematoda, Digenea) from fishes of Japanese and adjacent waters. Bulletin of the National Science Museum Tokyo, Series A, 31, 123–136.

  • Machida, M., & Kuramochi, T. (2000). Digenean trematodes from halfbeaks and needlefishes of Japan and adjacent waters. Bulletin of the National Science Museum, Tokyo, Series A., 26, 203–218.

  • Madhavi, R. (1974). Digenetic trematodes from marine fishes of Waltair Coast, Bay of Bengal. Family Monorchiidae. Rivista di Parassitologia, 35, 87–98.

  • Manter, H. W. (1934). Some digenetic trematodes from deep-water fish of Tortugas, Florida. Papers from Tortugas Laboratory, 28, 257–345.

  • Manter, H. W. (1942). Monorchiidae (Trematoda) from fishes of Tortugas, Florida. Transactions of the American Microscopical Society, 61, 349–360.

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

    Article  Google Scholar 

  • Martin, S. B., Cutmore, S. C., & Cribb, T. H. (2017). 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.

  • Martin, S. B., Cutmore, S. C., & Cribb, T. H. (2020a). The Pseudoplagioporinae, a new subfamily in the Opecoelidae Ozaki, 1925 (Trematoda) for a small clade parasitizing mainly lethrinid fishes, with three new species. Journal of Zoological Systematics and Evolutionary Research, 58, 79–113.

  • Martin, S. B., Downie, A. J., & Cribb, T. (2020b). A new subfamily for a clade of opecoelids (Trematoda: Digenea) exploiting marine fishes as second-intermediate hosts, with the first report of opecoelid metacercariae from an elasmobranch. Zoological Journal of the Linnean Society, 188, 455–472.

  • Martin, S. B., Sasal, P., Cutmore, S. C., Ward, S., Aeby, G. S., & Cribb, T. H. (2018). Intermediate host switches drive diversification among the largest trematode family: evidence from the Polypipapiliotrematinae n. subf. (Opecoelidae), parasites transmitted to butterflyfishes via predation of coral polyps. International Journal for Parasitology, 48, 1107–1126.

  • Martin, W. E. (1940). Studies on the trematodes of Woods Hole. III. The life cycle of Monorcheides cumingiae (Martin) with special reference to its effect on the invertebrate host. Biological Bulletin, 79, 131–144.

  • Miller, M. A., Pfeiler, E., & Schwartz, T. (2010). Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA, p. 1–8.

  • Miller, T. L., & Cribb, T. H. (2007a). Coevolution of Retrovarium n. gen. (Digenea: Cryptogonimidae) in Lutjanidae and Haemulidae (Perciformes) in the Indo-West Pacific. International Journal for Parasitology, 37, 1023–1045.

  • Miller, T. L., & Cribb, T. H. (2007b). Two new cryptogonimid genera Beluesca n. gen. and Chelediadema n. gen. (Digenea: Cryptogonimidae) from tropical Indo-West Pacific Haemulidae (Perciformes). Zootaxa, 1543, 45–60.

  • Miller, T. L., & Cribb, T. H. (2008). Eight new species of Siphoderina Manter, 1934 (Digenea, Cryptogonimidae) infecting Lutjanidae and Haemulidae (Perciformes) off Australia. Acta Parasitologica, 53, 344–364.

  • Miller, T. L., & Cribb, T. H. (2013). Dramatic phenotypic plasticity within species of Siphomutabilus n. g. (Digenea: Cryptogonimidae) from Indo-Pacific caesionines (Perciformes: Lutjanidae). Systematic Parasitology, 86, 101–112.

  • 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.

  • Nahhas, F. M., Powell, E. C. (1965). Monorchiidae (Trematoda) from fishes of Apalachee Bay, Gulf of Mexico. Journal of Parasitology, 51, 16–20

    Article  CAS  Google Scholar 

  • Nanami, A., & Shimose, T. (2013). Interspecific differences in prey items in relation to morphological characteristics among four lutjanid species (Lutjanus decussatus, L. fulviflamma, L. fulvus and L. gibbus). Environmental Biology of Fishes, 96, 591–602.

  • Osmanov, S. U. (1940). [Studies on the parasite fauna of fish from the Black Sea]. Uchenye Zapiski Leningradskogo Gosudarstvennogo Pedagogicheskogo Instituta im. A.I. Gertsena, 30, 187–265 (In Russian).

  • Overstreet, R. M. (1969). Digenetic trematodes of marine teleost fishes from Biscayne Bay, Florida. Tulane Studies in Zoology and Botany, 15, 119–180.

  • Panyi, A. J., Curran, S. S., & Overstreet, R. M. (2020). Phylogenetic affinity of Genolopa (Digenea: Monorchiidae) with descriptions of two new species. Diversity, 12, 51.

  • Parukhin, A. M. (1965). A new trematode species from the marine fish Rachycentron canadus from the South China Sea. Uchenye Zapiski Gorʼkovskogo Gosudarstvennogo Pedagogicheskogo Instituta im. M. Gorʼkogo, Seria Biologicheskikh Nauk, 56, 17–19.

  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. I., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.

  • Rooker, J. R. (1995). Feeding ecology of the schoolmaster snapper, Lutjanus apodus (Walbaum), from southwestern Puerto Rico. Bulletin of Marine Science, 56, 881–894.

  • Sano, M. (1989). Feeding habits of Japanese butterflyfishes (Chaetodontidae). Environmental Biology of Fishes, 25, 195–203.

  • Searle, E. L., Cutmore, S. C., & Cribb, T. H. (2014). Monorchiid trematodes of the painted sweetlips, Diagramma labiosum (Perciformes: Haemulidae), from the southern Great Barrier Reef, including a new genus and three new species. Systematic Parasitology, 88, 195–211.

  • Shen, J. (1985). Digenetic trematodes of fishes from the Xisha Islands, II. Studia Marina Sinica, 24, 167–177.

  • Shen, J. (1986). Digenetic trematodes of fishes from the East China Sea I. Species of the families Opistholobetidae, Lepocreadiidae and Cryptogonimidae. Studia Marina Sinica, 27, 209–219.

  • Shen, J. (1990). Digenetic trematodes of marine fishes of Hainan Island. Beijing: Science Publications.

  • Sogandares-Bernal, F. (1959). Digenetic trematodes of marine fishes from the Gulf of Panama and Bimini, British West Indies. Tulane Studies in Zoology, 7, 71–117.

  • Sokolov, S., Voropaeva, & E., Atopkin, D. (2020). A new species of deropristid trematode from the sterlet Acipenser ruthenus (Actinopterygii: Acipenseridae) and revision of superfamily affiliation of the family Deropristidae. Zoological Journal of the Linnean Society. https://doi.org/10.1093/zoolinnean/zlaa015/5810955

  • Sokolov, S. G., & Gordeev, I. I. (2019). Asaccotrema vietnamiense n. gen.; n. sp. (Trematoa: Monorchioidea), a new aberrant representative of lissorchiid trematodes from the sidestripe rasbora, Rasbora paviana Tirant (Actinopterygii: Cyprinidae), Vietnam. Zootaxa, 4674, 451–462.

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

  • Takeuchi, N., Saeki, T., Sakai, Y., & Hashimota, H. (2007). Diets of 45 fish species from 17 families at Kuchierabu-jima Island. Journal of the Graduate School of Biosphere Science, Hiroshima University, 45, 5–13.

  • Tkach, V. V., Pawlowski, J., Mariauxc, 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 & Francis, pp. 186–193.

  • Vélez, E. I. (1987). Sobre la fauna de tremátodes en peces marinos de la familia Lutjanidae en el mar Caribe. Actualidades Biologicas, 16, 70–84

    Google Scholar 

  • Wallet, M., & Kohn, A. (1987). Trématodes parasites de poissons marins du littoral de Rio de Janeiro, Brésil. Memorias do Instituto Oswaldo Cruz, 82, 21–27s.

  • Wang, P.-q. (1991). Report on one new genus and six new species of digenetic trematodes from marine fishes in Pingtan, Fujian Province. Wuyi Science Journal, 8, 131–138.

  • 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 multi-locus molecular data. Parasitology International, 66, 16–26.

  • Wee, N. Q.-X., Cutmore, S. C., & Cribb, T. H. (2018). Two monorchiid species from the freckled goatfish, Upeneus tragula (Perciformes: Mullidae), in Moreton Bay, Australia, including a proposal of a new genus. Systematic Parasitology, 95, 353–365.

  • Wee, N. Q.-X., Cutmore, S. C., & Cribb, T. H. (2019). Four new monorchiids from the golden trevally, Gnathanodon speciosus (Forsskål) (Perciformes: Carangidae), in Moreton Bay, Australia. Systematic Parasitology, 96, 265–278.

  • Wee, N. Q.-X., Cutmore, S. C., Sasal, P., & Cribb, T. H. (2020). Three new species of Allobacciger Hafeezullah & Siddiqi, 1970 (Digenea: Monorchiidae) from Australia and French Polynesia. Marine Biodiversity, 50.

  • Yamaguti, S. (1971). Synopsis of Digenetic Trematodes of Vertebrates, Vol. 1. Tokyo: Keigaku Publishing.

Download references

Acknowledgements

We sincerely thank the members of the Marine Parasitology Laboratory for their support and assistance with the collection of host specimens. We also thank the staff of Lizard Island Research Station for their support of our work.

Funding

This project was supported by the Holsworth Wildlife Research Endowment & The Ecological Society of Australia, and the PADI Foundation through funds awarded to NW. NW is supported by a PhD scholarship from the University of Queensland (Research Training Program (RTP) Scholarship). SCC and THC are supported by the Australian Biological Resources Study (ABRS National Taxonomy Research Grant RG19-37).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicholas Q.-X. Wee.

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

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:1FE1714A-3A57-4E38-998E-7B1E4042A7B7. 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

Wee, N.QX., Cribb, T.H., Cutmore, S.C. et al. Retroporomonorchis pansho n. g., n. sp., an unusual monorchiid trematode exploiting an atypical host. Syst Parasitol 97, 441–454 (2020). https://doi.org/10.1007/s11230-020-09926-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11230-020-09926-4

Navigation