Opecoelidae (Digenea) in northern Great Barrier Reef goatfishes (Perciformes: Mullidae)

Abstract

The Opecoelidae (Digenea) of eight species of goatfishes (Perciformes: Mullidae) were studied off Lizard Island on the northern Great Barrier Reef (GBR). Host species included Mulloidichthys flavolineatus (Lacépède), M. vanicolensis (Valenciennes), Parupeneus barberinus (Lacépède), P. ciliatus (Lacépède), P. cyclostomus (Lacépède), P. indicus (Shaw), P. multifasciatus (Quoy & Gaimard), P. spilurus (Bleeker) and P. trifasciatus (Lacépède). Seven opecoelid species were found, of which Paropecoelus corneliae n. sp., Pa. leonae n. sp. and Pseudopecoeloides engeleri n. sp. are described as new. Paropecoelus elongatus (Ozaki, 1928), Pa. sogandaresi Pritchard, 1966 and Podocotyloides parupenei (Manter, 1963) are recorded and a description is provided for each. A second species of Pseudopecoeloides remains unnamed for want of sufficient morphological material. The seven species were distinguished on the basis of morphology and molecular analysis of 56 ITS2 rDNA sequences. Sequences differed by nine to 68 base pairs between species combinations recognised by morphology; no intraspecific variation was detected. Each opecoelid species infected between two and five mullid species, but none of the species has been found in non-mullid hosts. Every mullid species was infected with at least one species of opecoelid and Parupeneus ciliatus had all seven species. The Opecoelidae of GBR goatfishes are consistent with the typical pattern of stenoxenicity seen for trematodes of GBR fishes.

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References

  1. Aken’Ova, T. O. (2003). A new species of Podocotyloides Yamaguti, 1934 (Digenea: Opecoelidae) from a Western Australian temperate marine fish. Systematic Parasitology, 55, 127–133.

    PubMed  Article  Google Scholar 

  2. Aken’Ova, T. O., Cribb, T. H., & Bray, R. A. (2003). A new species of Dactylostomum Woolcock, 1935 (Digenea: Opecoelidae) from the goatfish Upeneichthys lineatus (Bloch & Schneider) (Mullidae) in Western Australian waters. Systematic Parasitology, 56, 63–68.

    PubMed  Article  Google Scholar 

  3. Aken’Ova, T. O., Cribb, T. H., & Bray, R. A. (2009). Seven species of Pseudopecoeloides Yamaguti, 1940 (Digenea, Opecoelidae) from temperate marine fishes of Australia, including five new species. ZooKeys, 5, 1–32.

    Google Scholar 

  4. Allen, G. (1997). Marine fishes of the Great Barrier Reef and south-east Asia. Perth: Western Australian Museum, 292 pp.

  5. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    PubMed  CAS  Google Scholar 

  6. Bray, R. A., & Cribb, T. H. (1989). Digeneans of the family Opecoelidae Ozaki, 1925 from the southern Great Barrier Reef, including a new genus and three new species. Journal of Natural History, 23, 429–473.

    Article  Google Scholar 

  7. Bray, R. A., Justine, J. L., & Cribb, T. H. (2007). Homalometron moraveci n. sp (Digenea: Apocreadiidae) in the yellowfin goatfish, Mulloidichthys vanicolensis (Valenciennes, 1831) (Perciformes : Mullidae), from New Caledonia and the Great Barrier Reef, with a checklist of digeneans of Mulloidichthys species. Zootaxa, 1525, 41–49.

    Google Scholar 

  8. Colwell, R. K. (2005). EstimateS: Statistical estimation of species richness and shared species from samples; Version 7.5, The University of Connecticut.

  9. Cribb, T. H. (2005). Opecoelidae, Ozaki 1925. In: Jones, A., Bray, R. A., & Gibson, D. I. (Eds) Keys to the Trematoda. Vol. 2. Wallingford: CAB International, pp. 443–532.

  10. 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.

    PubMed  Article  Google Scholar 

  11. Cribb, T. H., Bray, R. A., & Barker, S. C. (1992). A review of the family Transversotrematidae (Trematoda: Digenea) with the description of a new genus, Crusziella. Invertebrate Taxonomy, 6, 909–935.

    Article  Google Scholar 

  12. Essafi, K., Raibaut, A., & Boudaoudkrissat, K. (1983). Colobomatus steenstrupi (Richiardi, 1876) and Colobomatus mulli n. sp. (Copepoda, Philichthyidae), parasitic on fish of the genus Mullus (Mullidae) in the western Mediterranean. Systematic Parasitology, 5, 135–142.

    Article  Google Scholar 

  13. Gosline, W. A. (1984). Structure, function, and ecology in the goatfishes (family Mullidae). Pacific Science, 38, 312–323.

    Google Scholar 

  14. Grant, E. M. (2004). Grant’s guide to fishes. Scarborough: E.M Grant Pty Limited, 880 pp.

  15. Hafeezullah, M. (1971). Opecoelid trematodes of marine fishes of India. Parasitology, 62, 321–329.

    Article  Google Scholar 

  16. Holland, K. (1978). Chemosensory orientation to food by a Hawaiian goatfish (Parupeneus porphyreus, Mullidae). Journal of Chemical Ecology, 4, 173–186.

    Article  CAS  Google Scholar 

  17. Hunter, J. A., Hall, K. A., & Cribb, T. H. (2012). A complex of Transversotrematidae (Platyhelminthes: Digenea) associated with mullid fishes of the Indo-West Pacific Region, including the descriptions of four new species of Transversotrema. Zootaxa, 3266, 1–22.

    Google Scholar 

  18. Jousson, O., & Bartoli, P. (2000). The life cycle of Opecoeloides columbellae (Pagenstecher, 1863) n. comb. (Digenea, Opecoelidae): evidence from molecules and morphology. International Journal for Parasitology, 30, 747–760.

    PubMed  Article  CAS  Google Scholar 

  19. Jousson, O., & Bartoli, P. (2001). Molecules, morphology and morphometrics of Cainocreadium labracis and Cainocreadium dentecis n. sp. (Digenea: Opecoelidae) parasitic in marine fishes. International Journal for Parasitology, 31, 706–714.

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  21. 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.

    Article  Google Scholar 

  22. Kim, B.-J. (2002). Comparative anatomy and phylogeny of the family Mullidae (Teleostei: Perciformes). Memoirs of the Graduate School of Fisheries Sciences Hokkaido University, 49, 1–74.

    Google Scholar 

  23. Kirino, M., Ikenaga, T., Tsukahara, J., Lamb, C. F., & Kiyohara, S. (2006). Primary taste center in the goatfish of genus Parupeneus. Fisheries Science, 72, 461–468.

    Article  CAS  Google Scholar 

  24. Kiyohara, S., & Tsukahara, J. (2005) Barbel taste system in catfish and goatfish. In: Reutter, K., & Kapoor, B. (Eds) Fish chemosenses. Enfield, New Hampshire: Science Publishers Inc, pp. 175–209.

  25. Koetschan, C., Hackl, T., Müller, T., Wolf, M., Förster, F., & Schultz, J. (2012). ITS2 database IV: interactive taxon sampling for internal transcribed spacer 2 based phylogenies. Molecular Phylogenetics & Evolution, 63, 585–588.

    Article  CAS  Google Scholar 

  26. Krajewski, J. P., & Bonaldo, R. M. (2006). Plankton-picking by the goatfish Pseudupeneus maculatus (Mullidae), a specialized bottom forager. Journal of Fish Biology, 68, 925–930.

    Article  Google Scholar 

  27. Kuiter, R. (1996). Guide to sea fishes of Australia – a comprehensive reference for divers and fishermen. Sydney: New Holland Publishers, 433 pp.

  28. Lo, C. F., Morgan, J. A. T., Galzin, R., & Cribb, T. H. (2001). Identical digeneans in coral reef fishes from French Polynesia and the Great Barrier Reef (Australia) demonstrated by morphology and molecules. International Journal for Parasitology, 31, 1573–1578.

    PubMed  Article  CAS  Google Scholar 

  29. Lucas, T., O’Brien, E. K., Cribb, T. H., & Degnan, B. M. (2005). Digenean trematodes infecting the tropical abalone Haliotis asinina have species-specific cercarial emergence patterns that follow daily or semilunar spawning cycles. Marine Biology, 148, 285–292.

    Article  Google Scholar 

  30. Madhavi, R. (1975). Digenetic trematodes from marine fishes of Waltair Coast, Bay of Bengal. Family Opecoelidae. Rivista di Parassitologia, 36, 153–164.

    Google Scholar 

  31. 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 

  32. McCormick, M. I. (1993). Development and changes at settlement in the barbel structure of the reef fish, Upeneus tragula (Mullidae). Environmental Biology of Fishes, 37, 269–282.

    Article  Google Scholar 

  33. McCormick, M. I. (1995). Fish feeding on mobile benthic invertebrates – influence of spatial variability in habitat associations. Marine Biology, 121, 627–637.

    Article  Google Scholar 

  34. Meenakshi, M., Madhavi, R., & Swarnakumari, V. G. M. (1993). The life-cycle of Helicometra gibsoni n. sp. (Digenea: Opecoelidae). Systematic Parasitology, 25, 63–72.

    Article  Google Scholar 

  35. Miller, T. L., Bray, R. A., & Cribb, T. H. (2011). Taxonomic approaches to and interpretation of host-specificity of trematodes of fishes: lessons from the Great Barrier Reef. Parasitology, 138, 1710–1722.

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  37. Moravec, F., Justine, J. L., & Rigby, M. C. (2006a). Some camallanid nematodes from marine perciform fishes off New Caledonia. Folia Parasitologica, 53, 223–239.

    PubMed  Google Scholar 

  38. Moravec, F., Ternengo, S., & Levron, C. (2006b). Three species of Philometra (Nematoda, Philometridae) from marine fishes off Corsica, France. Acta Parasitologica, 51, 111–118.

    Article  Google Scholar 

  39. Nelson, J. S. (2006) Fishes of the world. New Jersey: John Wiley & Sons Inc, 601 pp.

  40. Nolan, M. J., & Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology, 60, 101–163.

    PubMed  Article  Google Scholar 

  41. Nolan, M. J., & Cribb, T. H. (2006). 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.

    Google Scholar 

  42. Palm, H. W. (1997). Trypanorhynch cestodes of commercial fishes from Northeast Brazilian coastal waters. Memórias do Instituto Oswaldo Cruz, 92, 69–79.

    Article  Google Scholar 

  43. Paperna, I. (1972). Monogenea from Red Sea fishes. 2. Monogenea of Mullidae. Proceedings of the Helminthological Society of Washington, 39, 39–45.

    Google Scholar 

  44. Platell, M. E., & Potter, I. C. (2001). Partitioning of food resources amongst 18 abundant benthic carnivorous fish species in marine waters on the lower west coast of Australia. Journal of Experimental Marine Biology and Ecology, 261, 31–54.

    PubMed  Article  Google Scholar 

  45. Platell, M. E., Potter, I. C., & Clarke, K. R. (1998). Do the habitats, mouth morphology and diets of the mullids Upeneichthys stotti and U. lineatus in coastal waters of south-western Australia differ? Journal of Fish Biology, 52, 398–418.

    Google Scholar 

  46. Pritchard, M. H. (1966). Studies on digenetic trematodes of Hawaiian fishes: Family Opecoelidae Ozaki, 1925. Zoologische Jahrbücher. Abteilung für Systematik, Ökologie und Geographie der Tiere, 93, 173–202.

    Google Scholar 

  47. Prudhoe, S., & Bray, R. A. (1973). Digenetic trematodes from fishes. B.A.N.Z. Antarctic Research Expedition Reports. Series B (Zoology and Botany), 8, 199–225.

    Google Scholar 

  48. Randall, J. E., Allen, G. R., & Steene, R. C. (1997). Fishes of the Great Barrier Reef and Coral Sea. Bathurst: Crawford House Press, 557 pp.

  49. Rigby, M. C., & Font, W. F. (1997). Redescription and range extension of Spirocamallanus istiblenni Noble, 1966 (Nematoda: Camallanidae) from coral reef fishes in the Pacific. Journal of the Helminthological Society of Washington, 64, 227–233.

    Google Scholar 

  50. Sambrook, J., Fritsch, E., & Maniatis, T. (2001). Molecular cloning: a laboratory manual. Third edition. New York: Cold Spring Harbor Laboratory Press, 2344 pp.

  51. Shimazu, T., & Machida, M. (1985). Two new and two known opecoelid trematodes from goatfishes in Japan. Bulletin of the National Science Museum, Tokyo, Series A, Zoology, 11, 1–6.

    Google Scholar 

  52. Stergiou, K. I., & Karpouzi, V. S. (2001). Feeding habits and trophic levels of Mediterranean fish. Reviews in Fish Biology and Fisheries, 11, 217–254.

    Article  Google Scholar 

  53. Swainston, R. (2010). Swainston’s fishes of Australia. The complete illustrated guide. Camberwell: Viking, 821 pp.

  54. Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    PubMed  Article  CAS  Google Scholar 

  55. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882.

    PubMed  Article  CAS  Google Scholar 

  56. Walther, B. A., & Morand, S. (1998). Comparative performance of species richness estimation methods. Parasitology, 116, 395–405.

    PubMed  Article  Google Scholar 

  57. Williams, E. H., Jr, & Bunkley-Williams, L. (1992). Renocila loriae and R. richardsonae (Crustacea: Isopoda: Cymothoidae), external parasites of coral reef fishes from New Guinea and the Philippines. Proceedings of the Biological Society of Washington, 105, 299–309.

    Google Scholar 

  58. Yamaguti, S. (1970). Digenetic trematodes of Hawaiian fishes. Tokyo: Keigaku Publishing Co., 436 pp.

  59. Youssef, E. M., & Ghobashy, M. A. (2009). Historical review and generic diagnosis of some trematodes infecting paruponi fish (Parupeneus forsskali) from Red Sea, Egypt. Abbassa International Journal for Aquaculture, Special Issue for Global Fisheries and Aquaculture Research Conference, 377–385.

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Acknowledgments

This work was supported by the Australian Biological Resources Study. The authors thank the CReefs Australia Project for providing support. The CReefs Australia Project was generously sponsored by BHP Billiton in partnership with the Australian Biological Resources Study, The Great Barrier Reef Foundation, the Australian Institute of Marine Science and the Alfred P. Sloan Foundation. CReefs is a field programme of the Census of Marine Life. We thank the staff of the Lizard Island Research Station for their support and Rob Adlard, Tane Sinclair-Taylor and Tony Byrne for assistance in the field. We also thank Terry Miller, Scott Cutmore, Mieke Burger, Ricky Gleeson, Abigail Downie, Nicole Gunter and Janet Hunter for their support in the lab. We thank Dr Takashi Iwaki of the Meguro Parasitological Museum, Tokyo, and Dr Toshiaki Kuramochi of the National Museum of Nature and Science, Tokyo, for examining specimens for us. Terry Miller provided useful comments on an early draft of the paper.

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Rohner, C.A., Cribb, T.H. Opecoelidae (Digenea) in northern Great Barrier Reef goatfishes (Perciformes: Mullidae). Syst Parasitol 84, 237–253 (2013). https://doi.org/10.1007/s11230-013-9404-0

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Keywords

  • Ventral Sucker
  • Oral Sucker
  • Genital Pore
  • Vitelline Follicle
  • Anterior Testis