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A re-evaluation of diversity of the Aporocotylidae Odhner, 1912 in Siganus fuscescens (Houttuyn) (Perciformes: Siganidae) and associated species

Abstract

The aporocotylid fauna of the mottled spinefoot, Siganus fuscescens (Houttuyn), from Moreton Bay, Queensland, Australia, was characterised using a combined morphological and molecular approach. Four aporocotylid species were identified, three belonging to the genus Ankistromeces Nolan & Cribb, 2006 and one to Cardicola Short, 1953. Specimens of Cardicola matched an undescribed species from the same host and locality; this species is described as Cardicola mogilae n. sp. Phylogenetic analyses of ITS2 and 28S data showed that C. mogilae n. sp. forms a strongly supported clade with other Cardicola species from siganid fishes. We record Ankistromeces olsoni Nolan & Cribb, 2006 in Moreton Bay for the first time, redescribe A. dunwichensis Nolan & Cribb, 2006 on the basis of new specimens and sequence data and re-report Ankistromeces sp. X from Moreton Bay based on molecular data. We review the status of the ten putative species of aporocotylids reported from siganids. Small variation in ITS2 rDNA sequences, in association with different geographic localities, was previously used to separate Cardicola lafii Nolan & Cribb, 2006 from C. parilus Nolan & Cribb, 2006, C. bartolii Nolan & Cribb, 2006 from C. watsonensis Nolan & Cribb, 2006, C. tantabiddii Nolan & Cribb, 2006 from Cardicola sp. 2, Ankistromeces sp. Y from A. olsoni and Ankistromeces sp. X from Ankistromeces sp. Z. These five combinations are reinterpreted as each representing a single species; Cardicola lafii is recognised as the senior synonym of C. parilus and C. bartolii as the senior synonym of C. watsonensis. This study thus suggests that six, rather than ten, species should be recognised as infecting S. fuscescens. This richness remains greater than is known for any other fish species and siganids are, so far, unique among fishes in harbouring two strongly radiated lineages of aporocotylids.

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References

  1. Agatsuma, T., Iwagami, M., Liu, C.-X., Saitoh, Y., Kawanaka, M., Upatham, S., et al. (2001). Molecular phylogenetic position of Schistosoma sinensium in the genus Schistosoma. Journal of Helminthology, 75, 215–221.

  2. 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 (Geoffrey Saint-Hilaire, 1817) (Teleostei: Sparidae): Description, molecular phylogeny, habitat and pathology. Parasitology International, 60, 34–44.

  3. 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.

  4. Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K.-L., Meier, R., Winker, K., et al. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 149–155.

  5. Blasco-Costa, I., Cutmore, S. C., Miller, T. L., & Nolan, M. J. (2016). Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Systematic Parasitology, 93, 295–306.

  6. Bott, N. J., Miller, T. L., & Cribb, T. H. (2013). Bucephalidae (Platyhelminthes: Digenea) of Plectropomus (Serranidae: Epinephelinae) in the tropical Pacific. Parasitology Research, 112, 2561–2584.

  7. 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.

  8. Bray, R. A., Cribb, T. H., & Littlewood, D. T. J. (2012). Sasala nolani gen. n., sp. n. (Digenea: Aporocotylidae) from the body-cavity of the guineafowl puffer fish Arothron meleagris (Lacepède) (Tetraodontiformes: Tetraodontidae) from off Moorea. French Polynesia. Zootaxa, 3334, 29–41.

  9. 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.

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

  11. Cribb, T. H., Bott, N. J., Bray, R. A., McNamara, M. K., Miller, T. L., Nolan, M. J., & Cutmore, S. C. (2014). Trematodes of the Great Barrier Reef, Australia: Emerging patterns of diversity and richness in coral reef fishes. International Journal for Parasitology, 44, 929–939.

  12. Cribb, T. H., Bray, R. A., Diaz, P. E., Huston, D. C., Kudlai, O., Martin, S. B., et al. (2016). Trematodes of fishes of the Indo-West Pacific: Told and untold richness. Systematic Parasitology, 93, 237–247.

  13. Cutmore, S. C., Diggles, B. K., & Cribb, T. H. (2016). Transversotrema Witenberg, 1944 (Trematoda: Transversotrematidae) from inshore fishes of Australia: Description of a new species and significant range extensions for three congeners. Systematic Parasitology, 93, 639–652.

  14. Daniel, B., Piro, S., Charbonnel, E., Francour, P., & Letourneur, Y. (2009). Lessepsian rabbitfish Siganus luridus reached the French Mediterranean coasts. Cybium, 33, 163–164.

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

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

  17. Froese, R., & Pauly, D. (Eds) (2017). FishBase, World Wide Web electronic publication. http://www.fishbase.org. 2017; accessed 02/2017.

  18. Herbert, B. W., Shaharom-Harrison, F. M., & Overstreet, R. M. (1994). Description of a new blood-fluke, Cruoricola lates n. g., n. sp. (Digenea: Sanguinicolidae), from sea-bass Lates calcarifer (Bloch, 1790) (Centropomidae). Systematic Parasitology, 29, 51–60.

  19. 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.

  20. 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.

  21. 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. Zootaxa, 3450, 1–7.

  22. Jousson, O., Bartoli, P., & Pawlowski, J. (2000). Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). Journal of Evolutionary Biology, 13, 778–785.

  23. 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.

  24. Kuriiwa, K., Hanzawa, N., Yoshino, T., Kimura, S., & Nishida, M. (2007). Phylogenetic relationships and natural hybridization in rabbitfishes (Teleostei: Siganidae) inferred from mitochondrial and nuclear DNA analyses. Molecular Phylogenetics and Evolution, 45, 69–80.

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

  26. Maddison, W. P., & Maddison, D. R. (2017). Mesquite: A modular system for evolutionary analysis. Version 3.2. http://mesquiteproject.org.

  27. McNamara, M. K., Miller, T. L., & Cribb, T. H. (2014). Evidence for extensive cryptic speciation in trematodes of butterflyfishes (Chaetodontidae) of the tropical Indo-West Pacific. International Journal for Parasitology, 44, 37–48.

  28. 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 Nov. 2010. New Orleans, LA, pp. 1–8.

  29. Montero, F. E., Aznar, F. J., Fernández, M., & Raga, J. A. (2003). Girdles as the main infection site for Paradeontacylix kampachi (Sanguinicolidae) in the greater amberjack Seriola dumerili. Diseases of Aquatic Organisms, 53, 271–272.

  30. Nolan, M. J., & Cribb, T. H. (2004). Ankistromeces mariae n. g., n. sp (Digenea: Sanguinicolidae) from Meuschenia freycineti (Monacanthidae) off Tasmania. Systematic Parasitology, 57, 151–157.

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

  32. Nolan, M. J., & Cribb, T. H. (2006b). An exceptionally rich complex of Sanguinicolidae von Graff, 1907 (Platyhelminthes: Trematoda) from Siganidae, Labridae and Mullidae (Teleostei: Perciformes) from the Indo-west Pacific region. Zootaxa, 1218, 1–80.

  33. Nolan, M. J., Cantacessi, C., Cutmore, S. C., Cribb, T. H., & Miller, T. L. (2016). High-intensity cardiac infections of Phthinomita heinigerae n. sp. (Digenea: Aporocotylidae) in the orangelined cardinalfish, Taeniamia fucata (Cantor), off Heron Island on the Great Barrier Reef. Parasitology International, 65, 371–377.

  34. Ogawa, K., Akiyama, K., & Grabner, D. (2015). Paradeontacylix buri n. sp. (Trematoda: Aporocotylidae) from Seriola quinqueradiata cultured in Japan with a description of unidentified Paradeontacylix sp. from S. lalandi. Fish Pathology, 50, 183–191.

  35. 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.

  36. Palacios-Abella, J. F., Rodríguez-Llanos, J., Mele, S., & Montero, F. E. (2015). Morphological characterisation and identification of four species of Cardicola Short, 1953 (Trematoda: Aporocotylidae) infecting the Atlantic bluefin tuna Thunnus thynnus (L.) in the Mediterranean Sea. Systematic Parasitology, 91, 101–117.

  37. Palacios-Abella, J. F., Georgieva, S., Mele, S., Raga, J. A., Isbert, W., Kostadinova, A., et al. (2017). Skoulekia erythrini n. sp. (Digenea: Aporocotylidae): a parasite of Pagellus erythrinus (L.) (Perciformes: Sparidae) from the western Mediterranean with an amendment of the generic diagnosis. Systematic Parasitology, 94, 669–688.

  38. Pichelin, S., Smales, L. R., & Cribb, T. H. (2016). A review of the genus Sclerocollum Schmidt & Paperna, 1978 (Acanthocephala: Cavisomidae) from rabbitfishes (Siganidae) in the Indian and Pacific Oceans. Systematic Parasitology, 93, 101–114.

  39. 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.

  40. 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.

  41. Santoro, M., Cipriani, P., Pankov, P., & Lawton, S. P. (2015). Aporocotyle michaudi n. sp. (Digenea: Aporocotylidae) from the emerald rock cod, Trematomus bernacchii (Teleostei: Perciformes) in Antarctica. Parasitology International, 64, 324–329.

  42. 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.

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

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

  45. 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.

  46. 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.

  47. Trieu, N., Cutmore, S. C., Miller, T. L., & Cribb, T. H. (2015). A species pair of Bivesicula Yamaguti, 1934 (Trematoda: Bivesiculidae) in unrelated great barrier reef fishes: Implications for the basis of speciation in coral reef fish trematodes. Systematic Parasitology, 91, 231–239.

  48. Woodland, D. J. (1990). Revision of the fish family Siganidae with descriptions of two new species and comments on distribution and biology. Indo-Pacific Fishes, 19, 136 pp.

  49. Yagishita, N., & Yamaguchi, A. (2016). Genetic population structure of the mottled spinefoot Siganus fuscescens in Japan. Fisheries Science, 82, 289–301.

  50. 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.

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

  52. Yong, R. Q.-Y., Cutmore, S. C., Wee, N. Q.-X., & Cribb, T. H. (2016b). A complex of Cardicola (Digenea: Aporocotylidae) species infecting the milkfish, Chanos chanos (Gonorynchiformes), with descriptions of two new species. Systematic Parasitology, 93, 831–846.

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Acknowledgements

The authors sincerely thank John Page, Dave Thompson, Daniel Huston, Storm Martin and Nicholas Wee for their assistance in the collection of fish in Moreton Bay. The authors thank the staff of Moreton Bay Research Station for their active and enthusiastic support of our research.

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. This work was further funded by Moreton Bay Research Station Research Scholarships awarded to RY and an ABRS Capacity-building Grant Honours Scholarship awarded to XB. RY acknowledges the support of the Australian government through an Australian Government Research Training Program Scholarship.

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Correspondence to Scott C. Cutmore.

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This article was registered in the Official Register of Zoological Nomenclature (ZooBank) as urn:lsid:zoobank.org:pub:5B490D2E-3ADF-4DD4-B881-8B82C73C7C9F. 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.

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Brooks, X., Cribb, T.H., Yong, R.Q. et al. A re-evaluation of diversity of the Aporocotylidae Odhner, 1912 in Siganus fuscescens (Houttuyn) (Perciformes: Siganidae) and associated species. Syst Parasitol 94, 717–737 (2017). https://doi.org/10.1007/s11230-017-9744-2

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