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A complex of Cardicola Short, 1953 (Digenea: Aporocotylidae) species infecting the milkfish Chanos chanos Forsskål (Gonorynchiformes), with descriptions of two new species

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Abstract

Two new species of Cardicola Short, 1953 are described from the milkfish, Chanos chanos Forsskål (Gonorynchiformes: Chanidae), obtained from off Lizard Island on the northern Great Barrier Reef (GBR) and North Stradbroke Island in southeast Queensland. These are the first known blood flukes from this order of fishes. Cardicola suni n. sp. differs from all other Cardicola spp. by a combination of a large ovoid oral sucker surrounding a subterminal mouth, recurved tegumental spines up to 16 μm long, anterior caeca occupying 25.1–31.3% (28.7%) of total body length and a mostly-intercaecal ovary. Cardicola jiigurru n. sp. differs from C. suni n. sp. and all other species of Cardicola by a combination of a narrowly lanceolate body, weakly-muscularised and poorly-demarcated oral sucker, minute tegumental spines <1 µm in length, and anterior caeca occupying 15.9–22.0% (19.4%) of total body length, an almost entirely post-caecal ovary and the male genital pore terminal on a dorsolateral protuberance. A third species, closely resembling C. suni n. sp., was also discovered off Wangetti Beach, north Queensland, but is not described due to lack of material. Molecular phylogenetic analysis, based on both ITS2 and partial 28S rDNA regions, shows that these three species form a clade nested within that formed by existing species of Cardicola.

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References

  • Alama-Bermejo, G., Montero, F. E., Raga, J. A., & Holzer, A. S. (2011). Skoulekia meningialis n. gen., n. sp. (Digenea: Aporocotylidae Odhner, 1912) a parasite surrounding the brain of the Mediterranean common two-banded seabream Diplodus vulgaris (Geoffroy Saint-Hilaire, 1817) (Teleostei: Sparidae): Description, molecular phylogeny, habitat and pathology. Parasitology International, 60, 34–44.

    Article  PubMed  Google Scholar 

  • Allen, G. R., Midgley, S. H., & Allen, M. (2002). Field Guide to the Freshwater Fishes of Australia. Perth, WA: Western Australian Museum, 394 pp.

  • Anderson, G. R., & Barker, S. C. (1998). Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spacer (ITS2) of ribosomal DNA. Systematic Parasitology, 41, 87–94.

    Article  Google Scholar 

  • Arthur, J. R., & Lumanlan-Mayo, S. (1997). Checklist of the Parasites of Fishes of the Philippines. FAO Fisheries Technical Paper, No. 369, Rome, Italy, 102 pp.

  • Baliao, D. (1984). Milkfish nursery pond and pen culture in the Indo-Pacific region. In: Juario, J. V., Ferraris, R. P. & Benitez, L. P. (Eds). Proceedings of the Second International Milkfish Aquaculture Conference, 4–8 October 1983. Iloilo City, pp. 97–106.

  • Braicovich, P. E., Etchegoin, J. A., Timi, J. T., & Sardella, N. H. (2006). A new species of Cardicola Short, 1953 (Digenea: Sanguinicolidae) parasitizing the Brazilian flathead, Percophis brasiliensis Quoy et Gaimard, 1824, from the coasts of Mar del Plata, Argentina. Parasitology International, 55, 175–177.

    Article  PubMed  Google Scholar 

  • Brant, S. V., Morgan, J. A., Mkoji, G. M., Snyder, S. D., Rajapakse, R. P., & Loker, E. S. (2006). An approach to revealing blood fluke life cycles, taxonomy and diversity: provision of key reference data including DNA sequence from single life cycle stages. Journal of Parasitology, 92, 77–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bullard, S. A. (2010). A new species of Cardicola Short, 1953 (Digenea: Aporocotylidae) from the heart and branchial vessels of two surfperches (Perciformes: Embiotocidae) in the eastern Pacific Ocean off California. Journal of Parasitology, 96, 382–388.

    Article  PubMed  Google Scholar 

  • Bullard, S. A. (2012). Cardicola langeli sp. n. (Digenea: Aporocotylidae) from heart of sheepshead, Archosargus probatocephalus (Actinopterygii: Sparidae) in the Gulf of Mexico, with an updated list of hosts, infection sites and localities for Cardicola spp. Folia Parasitologica, 60, 17–27.

    Article  Google Scholar 

  • Bullard, S. A., & Overstreet, R. M. (2004). Two new species of Cardicola (Digenea: Sanguinicolidae) in drums (Sciaenidae) from Mississippi and Louisiana. Journal of Parasitology, 90, 128–136.

    Article  PubMed  Google Scholar 

  • Bullard, S. A. (2013). Cardicola langeli sp. n. (Digenea: Aporocotylidae) from heart of sheepshead, Archosargus probatocephalus (Actinopterygii: Sparidae) in the Gulf of Mexico, with an updated list of hosts, infection sites and localities for Cardicola spp. Folia Parasitologica, 60, 17–27.

    Article  PubMed  Google Scholar 

  • Bullard, S. A., Baker, T., & de Buron, I. (2012). New species of Cardicola (Digenea: Aporocotylidae) from heart of Atlantic croaker, Micropogonias undulatus (Perciformes: Sciaenidae) of the South Atlantic Bight. Journal of Parasitology, 98, 328–332.

    Article  PubMed  Google Scholar 

  • Bullard, S. A., & Overstreet, R. M. (2002). Potential pathological effects of blood flukes (Digenea: Sanguinicolidae) on pen-reared marine fishes. In: Creswell, R. L. (Ed). Proceedings of the 53rd Gulf & Caribbean Fisheries Institute, November 2000. Biloxi, Mississippi, pp. 10–25.

  • Colquitt, S. E., Munday, B. L., & Daintith, M. (2001). Pathological findings in southern bluefin tuna, Thunnus maccoyii (Castelnau), infected with Cardicola forsteri (Cribb, Daintith & Munday, 2000) (Digenea: Sanguinicolidae), a blood fluke. Journal of Fish Diseases, 24, 225–229.

    Article  Google Scholar 

  • Cribb, T. H., Anderson, G. R., Adlard, R. D., & Bray, R. A. (1998). A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). International Journal for Parasitology, 28, 1791–1795.

    Article  CAS  PubMed  Google Scholar 

  • Cribb, T. H., & Bray, R. A. (2011). Trematode families and genera: have we found them all? Trends in Parasitology, 27, 149–154.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fink, S. V., & Fink, W. L. (1996). Interrelationships of Ostariophysian Fishes (Teleostei). San Diego, CA: Academic Press, 496 pp.

  • Hernández-Orts, J. S., Alama-Bermejo, G., Carillo, J. M., García, N. A., Crespo, E. A., Raga, J. A., & Montero, F. E. (2012). Aporocotyle mariachristinae n. sp., and A. ymakara Villalba & Fernández, 1986 (Digenea: Aporocotylidae) of the pink cusk-eel Genypterus blacodes (Ophidiiformes: Ophidiidae) from Patagonia, Argentina. Parasite, 19, 319–330.

    Article  PubMed  PubMed Central  Google Scholar 

  • Holzer, A. S., Montero, F. E., Repullés, A., Nolan, M. J., Sitja-Bobadilla, A., Alvarez-Pellitero, P., et al. (2008). Cardicola aurata sp. n. (Digenea: Sanguinicolidae) from Mediterranean Sparus aurata L. (Teleostei: Sparidae) and its unexpected phylogenetic relationship with Paradeontacylix McIntosh, 1934. Parasitology International, 57, 472–482.

    Article  CAS  PubMed  Google Scholar 

  • Lebedev, B. I., & Mamaev, Yu. L. (1968). Two new species of the genus Cardicola Short, 1953 (Trematoda: Sanguinicolidae) from fish in the South China Sea. In: Skryabin, K. I. & Mamaev, Yu. L. (Eds). Helminths of animals of the Pacific Ocean. Moscow: Izdatelstvo “Nauka”, pp. 72–75.

  • Lee, C. S., & Banno, J. E. (1988). Milkfish culture and production in Southeast Asia present and future. In: Tanaka, H., Uwate, K. R., Juario, J. V., Lee, C. S. & Foscarini, R. (Eds). Proceedings of the Regional Workshop on Milkfish Culture Development in the South Pacific, South Pacific Aquaculture Development Project/Food and Agriculure Organisation of the United Nations, 21–25 November 1988. Tarawa, Kiribati, pp. 43–65.

  • Littlewood, D. T. J. (1994). Molecular phylogenetics of cupped oysters based on partial 28S rRNA gene sequences. Molecular Phylogenetics and Evolution, 3, 221–229.

    Article  CAS  PubMed  Google Scholar 

  • Littlewood, D. T. J., Curini-Galletti, M., & Herniou, E. A. (2000). The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466.

    Article  CAS  PubMed  Google Scholar 

  • Littlewood, D. T. J., Rohde, K., & Clough, K. A. (1997). Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology, 27, 1289–1297.

    Article  CAS  PubMed  Google Scholar 

  • Lockyer, A. E., Olson, P. D., & Littlewood, D. T. (2003a). Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society, 78, 155–171.

    Article  Google Scholar 

  • Lockyer, A. E., Olson, P. D., Ostergaard, P., Rollinson, D., Johnston, D. A., Attwood, S. W., et al. (2003b). The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology, 126, 203–224.

    Article  CAS  PubMed  Google Scholar 

  • Maddison, W. P., & Maddison, D. R. (2015). Mesquite: a modular system for evolutionary analysis. Version 3.04. http://mesquiteproject.org.

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

  • Morgan, J. A., & Blair, D. (1995). Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology, 111, 609–615.

    Article  CAS  PubMed  Google Scholar 

  • Nelson, J. S. (2006). Fishes of the World (4th ed.). New York: Wiley, 601 pp.

  • Nolan, M. J., & Cribb, T. H. (2006). Cardicola Short, 1953 and Braya n. gen. (Digenea: Sanguinicolidae) from five families of tropical Indo-Pacific fishes. Zootaxa, 1265, 1–80.

    Google Scholar 

  • Nolan, M. J., Miller, T. L., Cutmore, S. C., Cantacessi, C., & Cribb, T. H. (2014). Cardicola beveridgei n. sp. (Digenea: Aporocotylidae) from the mangrove jack, Lutjanus argentimaculatus (Perciformes: Lutjanidae), and C. bullardi n. sp. from the Australian spotted mackerel, Scomberomorus munroi (Perciformes: Scombridae), from the northern Great Barrier Reef. Parasitology International, 63, 735–745.

    Article  PubMed  Google Scholar 

  • Ogawa, K., Tanaka, S., Sugihara, Y., & Takami, I. (2009). A new blood fluke of the genus Cardicola (Trematoda:Sanguinicolidae) from Pacific bluefin tuna Thunnus orientalis (Temminck & Schlegel, 1844) cultured in Japan. Parasitology International, 59, 44–48.

    Article  PubMed  Google Scholar 

  • Ogawa, K., Ishimaru, K., Shirakashi, S., Takami, I., & Grabner, D. (2011). Cardicola opisthorchis n. sp. (Trematoda: Aporocotylidae) from the Pacific bluefin tuna, Thunnus orientalis (Temminck & Schlegel, 1844), cultured in Japan. Parasitology International, 60, 307–312.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Orélis-Ribeiro, R., & Bullard, S. A. (2015). Blood flukes (Digenea: Aporocotylidae) infecting body cavity of South American catfishes (Siluriformes: Pimelodidae): two new species from rivers in Bolivia, Guyana and Peru with a re-assessment of Plehniella Szidat, 1951. Folia Parasitologica, 62, 050.

    Article  Google Scholar 

  • Orélis-Ribeiro, R., & Bullard, S. A. (2016). Two new genera of fish blood flukes (Digenea: Aporocotylidae) from catfishes in the Peruvian Amazon. Journal of Parasitology, 102, 357–368.

    Article  PubMed  Google Scholar 

  • Padrós, F., Zarza, C., & Crespo, S. (2001). Histopathology of cultured sea bream Sparus aurata infected with sanguinicolid trematodes. Diseases of Aquatic Organisms, 44, 47–52.

    Article  PubMed  Google Scholar 

  • Parukhin, A. M. (1976). New species of trematodes from fish of the South Atlantic. Biologiya Morya, 2, 28–30.

    Google Scholar 

  • Regidor, S. E., & Arthur, J. R. (1986). Parasites of juvenile milkfish, Chanos chanos. In: Maclean, J. L., Dizon, L. B. & Hosillos, L. V. (Eds). The First Asian Fisheries Forum. Proceedings of the First Asian Fisheries Forum, 26–31 May 1986. Manila, Philippines, pp. 261–264.

  • Regidor, S. E., & Arthur, J. R. (1992). A survey of the parasite fauna of milkfish (Chanos chanos Forskal) in the Philippines. In: Shariff, M., Subasinghe, R. P. & Arthur, J. R. (Eds). Diseases in Asian Aquaculture. I. Fish Health Section, Vol. 1. Manila: Asian Fisheries Society, pp. 313–322.

    Google Scholar 

  • Repullés-Albelda, A., Montero, F. E., Holzer, A. S., Ogawa, K., Hutson, K. S., & Raga, J. A. (2008). Speciation of the Paradeontacylix spp. (Sanguinicolidae) of Seriola dumerili. Two new species of the genus Paradeontacylix from the Mediterranean. Parasitology International, 57, 405–414.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Saitoh, K., Miya, M., Inoue, J. G., Ishiguro, N. B., & Nishida, M. (2003). Mitochondrial genomics of ostariophysian fishes: perspectives on phylogeny and biogeography. Journal of Molecular Evolution, 56, 464–472.

    Article  CAS  PubMed  Google Scholar 

  • Sambrook, J., & Russell, D. W. (2001). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2344 pp.

  • Shirakashi, S., Kishimoto, Y., Kinami, R., Katano, H., Ishimaru, K., Murata, O., et al. (2012). Morphology and distribution of blood fluke eggs and associated pathology in the gills of cultured Pacific bluefin tuna, Thunnus orientalis. Parasitology International, 61, 242–249.

    Article  PubMed  Google Scholar 

  • Shirakashi, S., Tsunemoto, K., Webber, C., Rough, K., Ellis, D., & Ogawa, K. (2013). Two species of Cardicola (Trematoda: Aporocotylidae) found in southern bluefin tuna Thunnus maccoyii ranched in South Australia. Fish Pathology, 48, 1–4.

    Article  Google Scholar 

  • Short, R. B. (1953). A new blood fluke, Cardicola laruei n. g., n. sp., (Aporocotylidae) from marine fishes. Journal of Parasitology, 39, 304–309.

    Article  CAS  PubMed  Google Scholar 

  • Smith, J. W. (2002). Family Sanguinicolidae von Graff, 1907. In: Gibson, D. I., Bray, R. A. & Jones, A. (Eds). Keys to the Trematoda, Volume 1. Wallingford, UK: CABI Publishing, pp. 433–452.

    Google Scholar 

  • Snyder, S. D., & Tkach, V. V. (2001). Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology, 87, 1433–1440.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugihara, Y., Yamada, T., Tamaki, A., Yamanishi, R., & Kanai, K. (2014). Larval stages of the bluefin tuna blood fluke Cardicola opisthorchis (Trematoda: Aporocotylidae) found from Terebella sp. (Polychaeta: Terebellidae). Parasitology International, 63, 295–299.

    Article  PubMed  Google Scholar 

  • Szidat, L. (1951). Neue Arten der Trematodenfamilie Aporocotylidae aus dem Blut und der Leibeshöhle von Süsswasserfischen des Rio de la Plata. Zeitschrift für Parasitenkunde, 15, 70–86.

    CAS  PubMed  Google Scholar 

  • Truong, T. N., & Bullard, S. A. (2013). Blood flukes (Digenea: Aporocotylidae) of walking catfishes (Siluriformes: Clariidae): new genus and species from the Mekong River (Vietnam) with comments on related catfish aporocotylids. Folia Parasitologica, 60, 237–247.

    Article  PubMed  Google Scholar 

  • Velasquez, C. C. (1984). Pests/parasites and diseases of milkfish in the Philippines. In: Juario, J. V., Ferraris, R. P. & Benitez, L. P. (Eds). Proceedings of the Second International Milkfish Aquaculture Conference, 4–8 October 1983. Iloilo City, pp. 155–159.

  • Winans, G. A. (1980). Geographic variation in the milkfish Chanos chanos. I. Biochemical Evidence. Evolution, 34, 558–574.

    Article  CAS  Google Scholar 

  • Yamaguti, S. (1970). Digenetic trematodes of Hawaiian fishes. Tokyo: Keigaku Publishing Co.

    Google Scholar 

  • Yong, R. Q-Y., Cutmore, S. C., Miller, T. L., Adlard, R. D., & Cribb, T. H. (2013). The ghosts of parasites past: Eggs of the blood fluke Cardicola chaetodontis (Aporocotylidae) trapped in the heart and gills of butterflyfishes (Perciformes: Chaetodontidae) of the Great Barrier Reef. Parasitology, 140, 1186–1194.

    Article  PubMed  Google Scholar 

  • Yong, R. Q.-Y., Cutmore, S. C., Bray, R. A., Miller, T. L., Semarariana, I. W. Y., Palm, H. W., & Cribb, T. H. (2016). Three new species of blood flukes (Digenea: Aporocotylidae) infecting pufferfishes (Teleostei: Tetraodontidae) from off Bali, Indonesia. Parasitology International, 65, 432–443.

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Drs Rodney Bray and Abigail Downie for their aid in obtaining and analysing specimens for this study. We also thank the staff of Moreton Bay and Lizard Island Research Stations, for their practical and enthusiastic support of our research. The authors acknowledge the Dingaal, Yirrganydji and Quandamooka people, the traditional custodians of Lizard Island, Wangetti and North Stradbroke Island respectively, and pay respects to elders past and present of those nations.

Funding

The authors acknowledge the Australian Biological Resources Study (ABRS) for their ongoing support. This study was funded by the ABRS National Taxonomy Research Grant RF215-40, awarded in support of research into the parasites of commercial fishes of Moreton Bay. This work was also supported by a Holsworth Wildlife Research Endowment, as well as a Moreton Bay Research Station (MBRS) research scholarship, both awarded to the first author.

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  1. School of Biological Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia

    Russell Q.-Y. Yong, Scott C. Cutmore, Nicholas Q.-X. Wee & Thomas H. Cribb

  2. Centre for Sustainable Tropical Fisheries and Aquaculture, College of Marine and Environmental Sciences, James Cook University, Cairns, QLD, 4870, Australia

    Terrence L. Miller

  3. Fish Health Laboratory, Department of Fisheries Western Australia, 3 Baron-Hay Court, South Perth, WA, 6151, Australia

    Terrence L. Miller

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  1. Russell Q.-Y. Yong
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Yong, R.QY., Cutmore, S.C., Miller, T.L. et al. A complex of Cardicola Short, 1953 (Digenea: Aporocotylidae) species infecting the milkfish Chanos chanos Forsskål (Gonorynchiformes), with descriptions of two new species. Syst Parasitol 93, 831–846 (2016). https://doi.org/10.1007/s11230-016-9673-5

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