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Systematic Parasitology

, Volume 86, Issue 2, pp 125–151 | Cite as

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

  • Sarah R. CatalanoEmail author
Article

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.

Keywords

Peripheral Cell Axial Cell South Australia Mantle Length Infusoriform Embryo 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

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.

References

  1. 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.CrossRefGoogle Scholar
  2. Bogolepova-Dobrokhotova, I. I. (1962). Dicyemidae of far-eastern seas II. New species of the genus Dicyemennea. Zoologicheskii Zhurnal, 41, 503–518.Google Scholar
  3. Catalano, S. R. (2012). A review of the families, genera and species of Dicyemida Van Beneden, 1876. Zootaxa, 3479, 1–32.Google Scholar
  4. 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
  5. 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.PubMedCrossRefGoogle Scholar
  6. 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.PubMedCrossRefGoogle Scholar
  7. 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
  8. 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
  9. Furuya, H. (2008). A new dicyemid from Sepiella japonica (Mollusca: Cephalopoda: Decapoda). Journal of Parasitology, 94, 223–229.PubMedCrossRefGoogle Scholar
  10. Furuya, H. (2009). Two new dicyemid from Sepia longipes (Mollusca: Cephalopoda: Decapoda). Journal of Parasitology, 95, 681–689.PubMedCrossRefGoogle Scholar
  11. Furuya, H. (2010). A new dicyemid from Benthoctopus sibiricus (Mollusca: Cephalopoda: Octopoda). Journal of Parasitology, 96, 1,123–1,127.Google Scholar
  12. 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
  13. 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.CrossRefGoogle Scholar
  14. 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
  15. 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
  16. Furuya, H., Hochberg, F. G., & Tsuneki, K. (2003a). Calotte morphology in the phylum Dicyemida: Niche separation and convergence. Journal of Zoology, 259, 361–373.CrossRefGoogle Scholar
  17. Furuya, H., Hochberg, F. G., & Tsuneki, K. (2003b). Reproductive traits in dicyemids. Marine Biology, 142, 693–706.Google Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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
  22. 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.CrossRefGoogle Scholar
  23. 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
  24. Hochberg, F. G. (1982). The “kidneys” of cephalopods: A unique habitat for parasites. Malacologia, 23, 121–134.Google Scholar
  25. Hochberg, F. G. (1983). The parasites of cephalopods: A review. Memoirs of the National Museum Victoria, 44, 108–145.Google Scholar
  26. 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.Google Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.PubMedCrossRefGoogle Scholar
  30. Kearn, G. C. (1967). Experiments on host-finding and host-specificity in the monogenean skin parasite Entobdella soleae. Parasitology, 57, 585–605.PubMedCrossRefGoogle Scholar
  31. Kobayashi, M., Furuya, H., & Holland, P. W. H. (1999). Dicyemids are higher animals. Nature, 401, 762.PubMedCrossRefGoogle Scholar
  32. 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.PubMedCrossRefGoogle Scholar
  33. Lapan, E. A., & Morowitz, H. J. (1972). The Mesozoa. Scientific American, 227, 94–101.PubMedCrossRefGoogle Scholar
  34. Lapan, E. A., & Morowitz, H. J. (1974). Characterization of mesozoan DNA. Experimental Cell Research, 83, 143–151.PubMedCrossRefGoogle Scholar
  35. McConnaughey, B. H. (1949a). Dicyema sullivani, a new mesozoan from lower California. Journal of Parasitology, 35, 122–124.PubMedCrossRefGoogle Scholar
  36. McConnaughey, B. H. (1949b). Mesozoa of the family Dicyemidae from California. University of California Publications in Zoology, 2, 1–33.Google Scholar
  37. McConnaughey, B. H. (1951). The life cycle of the dicyemid mesozoa. University of California Publications in Zoology, 55, 295–336.Google Scholar
  38. McConnaughey, B. H. (1960). The rhombogen phase of Dicyema sullivani McConnaughey (Mesozoa: Dicyemidae). Journal of Parasitology, 46, 608–610.PubMedCrossRefGoogle Scholar
  39. 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
  40. 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.PubMedCrossRefGoogle Scholar
  41. Nouvel, H. (1948). Les dicyémides II. Infusoriforme, tératologie, spécificité du parasitisme, affinités. Archives de Biologie, 59, 147–224.PubMedGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. 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
  44. Pascual, S., & Hochberg, F. G. (1996). Marine parasites as biological tags of cephalopod hosts. Parasitology Today, 12, 324–327.PubMedCrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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
  47. 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
  48. Poulin, R. (1997). Species richness of parasite assemblages: Evolution and patterns. Annual Review of Ecology and Systematics, 28, 341–358.CrossRefGoogle Scholar
  49. 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.Google Scholar
  50. Short, R. B., & Damian, R. T. (1966). Morphology of the infusoriform larva of Dicyema aegira (Mesozoa: Dicyemidae). Journal of Parasitology, 52, 746–751.PubMedCrossRefGoogle Scholar
  51. 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.PubMedCrossRefGoogle Scholar
  52. 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
  53. 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.Google Scholar
  54. 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

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Marine Parasitology Laboratory, School of Earth and Environmental Sciences DX 650 418University of AdelaideAdelaideAustralia
  2. 2.Southern Seas Ecology LaboratoriesUniversity of AdelaideAdelaideAustralia
  3. 3.Evolutionary Biology UnitSouth Australian MuseumAdelaideAustralia
  4. 4.Australian Centre for Evolutionary Biology and BiodiversityUniversity of AdelaideAdelaideAustralia

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