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Five new species of dicyemid mesozoans (Dicyemida: Dicyemidae) from two Australian cuttlefish species, with comments on dicyemid fauna composition

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Abstract

Five new species of dicyemid mesozoans in two genera are described from two Australian cuttlefish species, Sepia apama Gray (giant Australian cuttlefish) and S. novaehollandiae Hoyle (nova cuttlefish): Dicyema coffinense n. sp. from S. apama collected from Coffin Bay, South Australia (SA), Australia; D. koinonum n. sp. from S. apama and S. novaehollandiae collected from Gulf St Vincent (GSV) and Spencer Gulf (SG), SA, Australia; D. multimegalum n. sp. from S. apama collected from Cronulla and North Bondi, New South Wales, Australia; D. vincentense n. sp. from S. novaehollandiae collected from GSV, SA, Australia; and Dicyemennea spencerense n. sp. from S. novaehollandiae and S. apama collected from SG, SA, Australia. Totals of 51 S. apama and 27 S. novaehollandiae individuals were examined, of which all except for four S. apama were infected by at least one dicyemid species. Dicyemid parasites were also observed in host individuals that were held in tanks for 2–3 months prior to examination, including nematogen-exclusive infections, leading to questions about persistence of dicyemids after host death and the mechanism responsible for the switch between a nematogen phase and a rhombogen phase. Variations in host size, calotte shape and collection locality are explored as predictors of differences in observed composition of the parasite fauna. In particular, dicyemid parasite fauna varied with host collection locality. As these parasites are highly host-species specific, their use as biological tags to assess cephalopod population structure using a combined morphological and molecular approach is discussed. This study increases the number of dicyemid species described from Australian cephalopods from five to ten, and from 117 to 122 species described worldwide.

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References

  • Aruga, J., Odaka, Y. S., Kamiya, A., & Furuya, H. (2007). Dicyemid Pax6 and Zic: tool-kit genes in a highly simplified bilaterian. BMC Evolutionary Biology, 7, 1–16.

    Article  Google Scholar 

  • Bogolepova-Dobrokhotova, I. I. (1962). Dicyemidae of far-eastern seas II. New species of the genus Dicyemennea. Zoologicheskii Zhurnal, 41, 503–518.

    Google Scholar 

  • Catalano, S. R. (2012). A review of the families, genera and species of Dicyemida Van Beneden, 1876. Zootaxa, 3479, 1–32.

    Google Scholar 

  • Catalano, S. R. (2013). First descriptions of dicyemid mesozoans (Dicyemida: Dicyemidae) from Australian octopus (Octopodidae) and cuttlefish (Sepiidae) species, including a new record of Dicyemennea in Australian waters. Folia Parasitologica, 60, 306–320.

    Google Scholar 

  • Catalano, S. R., & Furuya, H. (2013). Two new species of dicyemid (Dicyemida: Dicyemidae) from two Australian cephalopod species: Sepioteuthis australis (Mollusca: Cephalopoda: Loliginidae) and Sepioloidea lineolata (Mollusca: Cephalopoda: Sepiadariidae). Journal of Parasitology, 99, 203–211.

    Article  PubMed  Google Scholar 

  • Criscione, C. D., Cooper, B., & Blouin, M. S. (2006). Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecology, 87, 823–828.

    Article  PubMed  Google Scholar 

  • Finn, J. K., Hochberg, F. G., & Norman, M. D. (2005). Phylum Dicyemida in Australian waters: First record and distribution across diverse cephalopod hosts. Phuket Marine Biology Research Center Bulletin, 66, 83–96.

    Google Scholar 

  • Furuya, H. (1999). Fourteen new species of dicyemid Mesozoans from six Japanese cephalopods, with comments on host specificity. Species Diversity, 4, 257–319.

    Google Scholar 

  • Furuya, H. (2008). A new dicyemid from Sepiella japonica (Mollusca: Cephalopoda: Decapoda). Journal of Parasitology, 94, 223–229.

    Article  PubMed  Google Scholar 

  • Furuya, H. (2009). Two new dicyemid from Sepia longipes (Mollusca: Cephalopoda: Decapoda). Journal of Parasitology, 95, 681–689.

    Article  PubMed  Google Scholar 

  • Furuya, H. (2010). A new dicyemid from Benthoctopus sibiricus (Mollusca: Cephalopoda: Octopoda). Journal of Parasitology, 96, 1,123–1,127.

    Google Scholar 

  • Furuya, H., & Hochberg, F. G. (1998). Three new species of Dicyema (Phylum Dicyemida) from cephalopods in the western Mediterranean. Vie et Milieu, 49, 117–128.

    Google Scholar 

  • Furuya, H., & Hochberg, F. G. (2002). New species of Dicyemennea (Phylum: Dicyemida) in deep-water Graneledone (Mollusca: Cephalopoda: Octopoda) from the Antarctic. Journal of Parasitology, 88, 326–330.

    Article  Google Scholar 

  • Furuya, H., & Tsuneki, K. (2005). A new species of dicyemid mesozoan (Dicyemida: Dicyemidae) from Sepioteuthis lessoniana (Mollusca: Cephalopoda), with notes on Dicyema orientale. Species Diversity, 10, 45–62.

    Google Scholar 

  • Furuya, H., Tsuneki, K., & Koshida, Y. (1992). Two new species of the genus Dicyema (Mesozoa) from octopuses of Japan with notes on D. misakiense and D. acuticephalum. Zoological Science, 9, 423–437.

    Google Scholar 

  • Furuya, H., Hochberg, F. G., & Tsuneki, K. (2003a). Calotte morphology in the phylum Dicyemida: Niche separation and convergence. Journal of Zoology, 259, 361–373.

    Article  Google Scholar 

  • Furuya, H., Hochberg, F. G., & Tsuneki, K. (2003b). Reproductive traits in dicyemids. Marine Biology, 142, 693–706.

    Google Scholar 

  • Furuya, H., Hochberg, F. G., & Tsuneki, K. (2007). Cell number and cellular composition in vermiform larvae of dicyemid mesozoans. Journal of Zoology, 272, 284–298.

    Article  Google Scholar 

  • Furuya, H., Ota, M., Kimura, R., & Tsuneki, K. (2004). Renal organs of cephalopods: A habitat for dicyemids and chromidinids. Journal of Morphology, 262, 629–643.

    Article  PubMed  Google Scholar 

  • Gonzalez, A. F., Pascual, S., Gestal, C., Abollo, E., & Guerra, A. (2003). What makes a cephalopod a suitable host for parasite? The case of Galician waters. Fisheries Research, 60, 177–183.

    Article  Google Scholar 

  • Guegan, J. F., Lambert, A., Leveque, C., Combes, C., & Euzet, L. (1992). Can host body size explain the parasite species richness in tropical freshwater fishes? Oecologia, 90, 197–204.

    Google Scholar 

  • Hall, K. C., & Hanlon, R. T. (2002). Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Marine Biology, 140, 533–545.

    Article  Google Scholar 

  • Ho, J. S. (1991). Two species of chondracanthid copepods parasitic on commercial fishes in the Pacific. Publications of the Seto Marine Biological Laboratory, 31, 1–10.

    Google Scholar 

  • Hochberg, F. G. (1982). The “kidneys” of cephalopods: A unique habitat for parasites. Malacologia, 23, 121–134.

    Google Scholar 

  • Hochberg, F. G. (1983). The parasites of cephalopods: A review. Memoirs of the National Museum Victoria, 44, 108–145.

    Google Scholar 

  • Hochberg, F. G. (1990). Diseases caused by protists and mesozoans. In: Kinne, O. (Ed) Diseases of Marine Animals, Volume III. Hamburg, Germany: Biologische Anstalt Helgoland, pp. 47–202.

  • Kalavati, C., Narasimhamurti, C. C., & Suseela, T. (1984). Four new species of mesozoan parasites (Mesozoa: Dicyemidae) from cephalopods of Bay of Bengal. Proceedings of the Indian Academy of Science (Animal Science), 93, 639–654.

    Article  Google Scholar 

  • Kassahn, K. S., Donnellan, S. C., Fowler, A. J., Hall, K. C., Adams, M., & Shaw, P. W. (2003). Molecular and morphological analyses of the cuttlefish Sepia apama indicate a complex population structure. Marine Biology, 143, 947–962.

    Article  Google Scholar 

  • Katayama, T., Wada, H., Furuya, H., Satoh, N., & Yamamoto, M. (1995). Phylogenetic position of the dicyemid Mesozoa inferred from 18S rDNA sequences. Biological Bulletin, 189, 81–90.

    Article  PubMed  CAS  Google Scholar 

  • Kearn, G. C. (1967). Experiments on host-finding and host-specificity in the monogenean skin parasite Entobdella soleae. Parasitology, 57, 585–605.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi, M., Furuya, H., & Holland, P. W. H. (1999). Dicyemids are higher animals. Nature, 401, 762.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi, M., Furuya, H., & Wada, H. (2009). Molecular markers comparing the extremely simple body plan of dicyemids to that of lophotrochozoans: insight from the expression patterns of Hox, Otx, and brachyury. Evolution and Development, 11, 582–589.

    Article  PubMed  CAS  Google Scholar 

  • Lapan, E. A., & Morowitz, H. J. (1972). The Mesozoa. Scientific American, 227, 94–101.

    Article  PubMed  CAS  Google Scholar 

  • Lapan, E. A., & Morowitz, H. J. (1974). Characterization of mesozoan DNA. Experimental Cell Research, 83, 143–151.

    Article  PubMed  CAS  Google Scholar 

  • McConnaughey, B. H. (1949a). Dicyema sullivani, a new mesozoan from lower California. Journal of Parasitology, 35, 122–124.

    Article  PubMed  CAS  Google Scholar 

  • McConnaughey, B. H. (1949b). Mesozoa of the family Dicyemidae from California. University of California Publications in Zoology, 2, 1–33.

    Google Scholar 

  • McConnaughey, B. H. (1951). The life cycle of the dicyemid mesozoa. University of California Publications in Zoology, 55, 295–336.

    Google Scholar 

  • McConnaughey, B. H. (1960). The rhombogen phase of Dicyema sullivani McConnaughey (Mesozoa: Dicyemidae). Journal of Parasitology, 46, 608–610.

    Article  PubMed  CAS  Google Scholar 

  • Norman, M., Finn, J., & Tregenza, T. (1999). Female impersonation as an alternate reproductive strategy in giant cuttlefish. Proceedings of the Royal Society of London, 266, 1,347–1,349.

    Google Scholar 

  • Noto, T., & Endoh, H. (2004). A “chimera” theory on the origin of dicyemid mesozoans: Evolution driven by frequent lateral gene transfer from host to parasite. BioSystems, 73, 73–83.

    Article  PubMed  CAS  Google Scholar 

  • Nouvel, H. (1948). Les dicyémides II. Infusoriforme, tératologie, spécificité du parasitisme, affinités. Archives de Biologie, 59, 147–224.

    PubMed  CAS  Google Scholar 

  • Ogino, K., Tsuneki, K., & Furuya, H. (2010). Unique genome of dicyemid mesozoan: Highly shortened spliceosomal introns in conservative exon/intron structure. Gene, 449, 70–76.

    Article  PubMed  CAS  Google Scholar 

  • Ohama, T., Kumazaki, T., Hori, H., & Osawa, S. (1984). Evolution of multicellular animals as deduced from 5S rRNA sequences: A possible early emergence of the Mesozoa. Nucleic Acids Research, 12, 5,101–5,108.

    Google Scholar 

  • Pascual, S., & Hochberg, F. G. (1996). Marine parasites as biological tags of cephalopod hosts. Parasitology Today, 12, 324–327.

    Article  PubMed  CAS  Google Scholar 

  • Pawlowski, J., Montoya-Burgos, J., Fahrni, J. F., Wuest, J., & Zaninetti, L. (1996). Origin of the Mesozoa inferred from 18S rRNA gene sequences. Molecular Biology and Evolution, 13, 1128–1132.

    Article  PubMed  CAS  Google Scholar 

  • Penchaszadeh, P. E. (1968). Diciemidos (Mesozoa) en cefalopodos de Argentina Dicyema australis sp. nov. parasito del pulpo Octopus tehuelchus D’Orb. Neotropica, 14, 127–131.

    Google Scholar 

  • Pickford, G. E., & McConnaughey, B. H. (1949). The Octopus bimaculatus problem: A study in sibling species. Bulletin of Bingham Oceanographic College, Peabody Museum of Natural History, Yale University, 12, 1–66.

    Google Scholar 

  • Poulin, R. (1997). Species richness of parasite assemblages: Evolution and patterns. Annual Review of Ecology and Systematics, 28, 341–358.

    Article  Google Scholar 

  • Reid, A., Jereb, P., & Roper, C. F. E. (2005). Family Sepiidae. In: Jereb, P. & Roper, C. F. E. (Eds.), Cephalopods of the world. An annotated and illustrated catalogue of species known to date. Volume 1. Chambered nautiluses and sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae). Rome: Food and Agriculture Organisation of the United Nations, pp. 57–152.

  • Short, R. B., & Damian, R. T. (1966). Morphology of the infusoriform larva of Dicyema aegira (Mesozoa: Dicyemidae). Journal of Parasitology, 52, 746–751.

    Article  PubMed  CAS  Google Scholar 

  • Suzuki, T. G., Ogino, K., Tsuneki, K., & Furuya, H. (2010). Phylogenetic analysis of dicyemid mesozoans (Phylum Dicyemida) from innexin amino acid sequences: Dicyemids are not related to Platyhelminthes. Journal of Parasitology, 96, 614–625.

    Article  PubMed  Google Scholar 

  • van Beneden, E. (1876). Recherches sur les Dicyemides, survivants actuels d’un embranchement des Mésozoaires. Bulletins de l’Academis Royale Des Sciences et Belles Lettres de Bruxelles, 41, 1160–1205.

    Google Scholar 

  • von Kölliker, A. (1849). Ueber Dicyema paradoxum, den Schmarotzer der Venenanhänge der Cephalopoden [in German]. Berichte von der Königlichen Zootomischen Anstalt zu Wurzburg, 59–66.

  • Whitman, C. O. (1883). A contribution to the embryology, life-history and classification of the dicyemids. Mittheilungen Zoologischen Station Zu Neapel, 4, 1–90.

    Google Scholar 

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Acknowledgements

I thank Kate Hutson, Richard Saunders, Brian Saunders and Kieran Brazell for assistance in sample collections from Coffin Bay, and Bernadette Saunders for keeping us all well nourished! Thanks are due to Cameron Dixon and Graham Hooper at the South Australian Research and Development Institute for organising prawn trawl survey trips in Spencer Gulf and Gulf St Vincent, and to Alex Schnell and Dave Barker for material from New South Wales and allowing me to visit the Cronulla Fisheries Research Centre. All research was conducted with approval from the University of Adelaide Animal Ethics Committee (# S-2010-116) and according to Primary Industries and Resources SA S115 Ministerial Exemptions (# 9902264 and # 9902398). Funding for this project has been provided by the Australian Society for Parasitology, Norman Wettenhall Foundation, Holsworth Wildlife Research Endowment, Sir Mark Mitchell Research Foundation, Lirabenda Endowment Fund, Nature Foundation South Australia, Nature Conservation Society of South Australia and Australian Federation of University Women South Australia. I am grateful to my supervisors Bronwyn Gillanders (University of Adelaide, UA), Steve Donnellan (The South Australian Museum, SAMA, and UA) and Ian Whittington (SAMA and UA) for their constructive comments on earlier drafts, and thanks are due to Tim Benson for his continual support. SRC is funded by an Australian Postgraduate Award.

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Catalano, S.R. Five new species of dicyemid mesozoans (Dicyemida: Dicyemidae) from two Australian cuttlefish species, with comments on dicyemid fauna composition. Syst Parasitol 86, 125–151 (2013). https://doi.org/10.1007/s11230-013-9443-6

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