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Detection of a new Clytia species (Cnidaria: Hydrozoa: Campanulariidae) with DNA barcoding and life cycle analyses

Published online by Cambridge University Press:  07 August 2013

Konglin Zhou ,
Lianming Zheng ,
Jinru He ,
Yuanshao Lin ,
Wenqing Cao  and
Wenjing Zhang
Konglin Zhou
Affiliation:
College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China
Lianming Zheng*
Affiliation:
College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, China Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies (CEES), Xiamen University, Xiamen 361005, China
Jinru He
Affiliation:
College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China
Yuanshao Lin
Affiliation:
College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, China
Wenqing Cao
Affiliation:
College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, China
Wenjing Zhang
Affiliation:
College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361005, China
*
Correspondence should be addressed to: L. Zheng, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361005, China email: [email protected].
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Abstract

The genus Clytia is distributed worldwide, but most accepted species in this genus have been examined either only at the hydroid or medusa stage. The challenge in identifying Clytia species reflects their complex life cycles and phenotypic plasticity. In this study, molecular and morphological investigations of Clytia specimens from the coastal waters of China revealed an as yet unreported species, designated C. xiamenensis sp. nov., that was considered as conspecific to two nearly cosmopolitan species, C. hemisphaerica and C. gracilis. DNA barcoding based on partial mitochondrial cytochrome c oxidase subunit I (COI) and large subunit ribosomal RNA gene (16S) confirmed the highly distinct lineage of C. xiamenensis sp. nov. These results were corroborated by the detailed observations of its mature medusae and its colonies, which showed that C. xiamenensis sp. nov. was morphologically distinct from other species of Clytia. Thus, based on our findings, the nearly cosmopolitan distribution attributed to some species of Clytia might rather be due to the misidentification, and it is necessary to elucidate their whole life cycle in order to establish the systematic validity of all species within the genus Clytia.

Keywords

Clytianew speciesDNA barcodinglife cycle
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 8 , December 2013 , pp. 2075 - 2088
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

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References

REFERENCES

Adamík, P., Gallager, S.M., Horgan, E., Madin, L.P., McGillis, W.R., Govindarajan, A. and Alatalo, P. (2006) Effects of turbulence on the feeding rate of a pelagic predator: the planktonic hydroid Clytia gracilis . Journal of Experimental Marine Biology Ecology 333, 159–165.Google Scholar
Amiel, A., Chang, P., Momose, T. and Houliston, E. (2010) Clytia hemisphaerica: a cnidarian model for studying oogenesis. In Verlhac, M.H. and Villeneuve, A. (eds) Oogenesis: the universal process. Chichester: John Wiley & Sons, pp. 81–102.Google Scholar
Avent, S.R., Bollens, S.M., Butler, M., Horgan, E. and Rountree, R. (2001) Planktonic hydroids on Georges Bank: ingestion and selection by predatory fishes. Deep-Sea Research Part II: Topical Studies in Oceanography 48, 673–684.Google Scholar
Boero, F., Camillo, C.D. and Gravili, C. (2005) Aquatic invasions: phantom aliens in Mediterranean waters. MarBEF Newsletter 3, 21–22.Google Scholar
Bouillon, J. and Boero, F. (2000) Synopsis of the families and genera of the Hydromedusae of the world, with a list of the worldwide species. Thalassia Salentina 24, 47–296.Google Scholar
Bouillon, J., Gravili, C., Pagés, F., Gili, J.M. and Boero, F. (2006) An introduction to Hydrozoa. Paris: Publications Scientifiques du Muséum, 591pp.Google Scholar
Bucklin, A., Steinke, D. and Blanco-Bercial, L. (2011) DNA barcoding of marine metazoa. Annual Review of Marine Science 3, 471–508.Google Scholar
Calder, D.R. (1991) Shallow-water hydroids of Bermuda: the Thecatae, exclusive of Plumularioidea. Toronto: Royal Ontario Museum.Google Scholar
Calder, D.R., Mallinson, J.J., Collins, K. and Hickman, C.P. (2003) Additions to the hydroids (Cnidaria) of the Galápagos, with a list of species from the islands. Journal of Natural History 37, 1173–1218.Google Scholar
Cheng, F.P., Wang, M.X., Wang, Y.T., Zhang, F., Li, C.L. and Sun, S. (2012) DNA barcoding of common medusozoa in northern China based on mtCOI sequence. Oceanologia et Limnologia Sinica 43, 451–459. [In Chinese.]Google Scholar
Cornelius, P.F.S. (1982) Hydroids and medusae of the family Campanulariidae recorded from the eastern North Atlantic, with a world synopsis of the genera. Bulletin of the British Museum (Natural History): Zoology 42, 37–148.Google Scholar
Cornelius, P.F.S. (1987) The hydranths of Clytia linearis (Cnidaria, Hydrozoa) and related species. In Bouillon, J., Boero, F., Cicogna, F. and Cornelius, P.F.S. (eds) Modern trends in the systematics, ecology and evolution of Hydroids and Hydromedusae. Oxford: Clarendon Press, pp. 291–297.Google Scholar
Cornelius, P.F.S. (1990) European Obelia (Cnidaria, Hydroida): systematics and identification. Journal of Natural History 24, 535–578.Google Scholar
Cornelius, P.F.S. (1995) North-west European thecate hydroids and their medusa, part 2, Sertulariidae to Campanulariidae. In Barnes, R.S.K. and Crothers, J.H. (eds) Synopses of the British fauna (new series), No. 50. London: Linnean Society of London.Google Scholar
Ender, A. and Schierwater, B. (2003) Placozoa are not derived cnidarians: evidence from molecular morphology. Molecular Biology and Evolution 20, 130–134.Google Scholar
Gao, C.S. (1956) On the hydroids along Shantung coast. Journal of Shandong University 4, 70–103. [In Chinese.]Google Scholar
Gao, C.S., Li, F.L., Chang, U.M. and Li, H.L. (1958) On the Hydromedusae from the Shantung coast. Journal of Shandong University 1, 75–118. [In Chinese.]Google Scholar
Govindarajan, A.F., Halanych, K.M. and Cunningham, C.W. (2005) Mitochondrial evolution and phylogeography in the hydrozoan Obelia geniculata (Cnidaria). Marine Biology 146, 213–222.Google Scholar
Govindarajan, A.F., Boero, F. and Halanych, K.M. (2006) Phylogenetic analysis with multiple markers indicates repeated loss of the adult medusa stage in Campanulariidae (Hydrozoa, Cnidaria). Molecular Phylogenetics and Evolution 38, 820–834.Google Scholar
Hebert, P.D.N. and Gregory, T.R. (2005) The promise of DNA barcoding for taxonomy. Systematic Biology 54, 852–859.Google Scholar
Hebert, P.D.N., Ratnasingham, S. and deWaard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit I divergences among closely related species. Proceedings of the Royal Society, B 270, S96–S99.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. and Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator . Proceedings of the National Academy of Science of the United States of America 101, 14812–14817.Google Scholar
Hincks, T. (1868) A history of the British hydroid zoophytes. Volume 1. London: John van Voorst, 112 pp.CrossRefGoogle Scholar
Houliston, E., Momose, T. and Manuel, M. (2010) Clytia hemisphaerica: a jellyfish cousin joins the laboratory. Trends in Genetics 26, 159–167.CrossRefGoogle ScholarPubMed
Huang, Z.G. (2008) Marine species and their distributions in China's Seas. Beijing: China Ocean Press. [In Chinese.]Google Scholar
Kramp, P.L. (1968) The hydromedusae of the Pacific and Indian Oceans: Sections II and III. Copenhagen: A.F. Host.Google Scholar
Krishnamurthy, P.K. and Francis, R.A. (2012) A critical review on the utility of DNA barcoding in biodiversity conservation. Biodiversity and Conservation 21, 1901–1919.Google Scholar
Kubota, S. (1978a) The life-history of Clytia edwardsi (Hydrozoa; Campanulariidae) in Hokkaido, Japan. Journal of the Faculty of Science Hokkaido University Series VI. Zoology 21, 317–354.Google Scholar
Kubota, S. (1978b) Notes on Clytia and Phialidium (Hydrozoa; Campanulariidae) from Shimoda, Japan. Proceeding of the Japanese Society of Systematic Zoology 15, 1–7.Google Scholar
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. and Higgins, D.G. (2007) Clustal W and clustal X version 2.0. Bioinformatics 23, 2947–2948.Google Scholar
Licandro, P., Conway, D.V.P., Yahia, M.N.D., de Puelles, M.L.F., Gasparini, S., Hecq, J.H., Tranter, P. and Kirby, R.R. (2010) A blooming jellyfish in the northeast Atlantic and Mediterranean. Biology Letters 6, 688–691.Google Scholar
Lindner, A. and Migotto, A.E. (2002) The life cycle of Clytia linearis and Clytia noliformis: metagenic campanulariids (Cnidaria: Hydrozoa) with contrasting polyp and medusa stages. Journal of the Marine Biological Association of the United Kingdom 82, 541–553.Google Scholar
Lindner, A., Govindarajan, A.F. and Migotto, A.E. (2011) Cryptic species, life cycles, and the phylogeny of Clytia (Cnidaria: Hydrozoa: Campanulariidae). Zootaxa 2980, 23–36.Google Scholar
Madin, L.P., Bollens, S.M., Horgan, E., Butler, M., Runge, J., Sullivan, B.K., Klein-Macphee, G., Durbin, E., van Keuren, D., Plourde, S., Bucklin, A. and Clarke, M.E. (1996) Voracious planktonic hydroids: unexpected predatory impact on a costal marine ecosystem. Deep-Sea Research Part II: Topical Studies in Oceanography 43, 1823–1829.Google Scholar
Mariscal, R.N. (1974) Nematocysts. In Muscatine, L. and Lenhoff, H.M. (eds) Coelenterate biology: reviews and new perspectives. New York: Academic Press, pp. 129–178.Google Scholar
Mayer, A.G. (1910) Medusae of the world. The Hydromedusae. Washington, DC: Carnegie Institution of Washington, 498 pp.Google Scholar
Millard, N.A.H. (1966) The Hydrozoa of the south and west coasts of South Africa. Part III. The Gymnoblastea and small families of Calyptoblastea. Annals of the South African Museum 48, 426–487.Google Scholar
Moritz, C. and Cicero, C. (2004) DNA barcoding: promise and pitfalls. Plos Biology 2, 1529–1531.Google Scholar
Moura, C.J., Cunha, M.R., Porteiro, F.M. and Rogers, A.D. (2011) Polyphyly and cryptic diversity in the hydrozoan families Lafoeidae and Hebellidae (Cnidaria: Hydrozoa). Invertebrate Systematics 25, 454–470.Google Scholar
Moura, C.J., Harris, D.J., Cunha, M.R. and Rogers, A.D. (2008) DNA barcoding reveals cryptic diversity in marine hydroids (Cnidaria, Hydrozoa) from coastal and deep-sea environments. Zoologica Scripta 37, 93–108.Google Scholar
Nutting, C.C. (1915) American hydroids. Part III. The Campanularidae and the Bonneviellidae. Washington, DC: Smithsonian Institution, Special Bulletin 4.Google Scholar
Östman, C. (1979a) Two types of nematocysts in Campanulariidae (Cnidaria, Hydrozoa) studied by light and scanning electron microscopy. Zoologica Scripta 8, 5–12.Google Scholar
Östman, C. (1979b) Nematocysts in the Phialidium medusae of Clytia hemisphaerica (Hydrozoa, Campanulariidae) studied by light and scanning electron microscopy. Zoon 7, 125–142.Google Scholar
Östman, C. (1982) Nematocysts and taxonomy in Laomedea, Gonothyraea and Obelia (Hydrozoa, Campanulariidae). Zoologica Scripta 11, 227–241.CrossRefGoogle Scholar
Östman, C. (1987) New techniques and old problems in hydrozoan systematics. In Bouilon, J., Boero, F., Cicogna, F. and Cornelius, P.F.S. (eds) Modern trends in the systematics, ecology and evolution of Hydroids and Hydromedusae. Oxford: Clarendon Press, pp. 67–82.Google Scholar
Östman, C. (1999) Nematocysts and their value as taxonomic parameters within the Campanulariidae (Hydrozoa). A review based on light and scanning electron microscopy. In Stepanjants, S.D. (ed.) Obelia (Cnidaria, Hydrozoa): phenomenon, aspects of investigations, perspectives of employment. St Petersburg: Russian Academy of Sciences, pp. 17–28.Google Scholar
Östman, C., Piraino, S. and Roca, I. (1987) Nematocyst comparisons between some Mediterranean and Scandinavian campanulariids (Cnidaria, Hydrozoa). In Bouilon, J., Boero, F., Cicogna, F. and Cornelius, P.F.S. (eds) Modern trends in the systematics, ecology and evolution of Hydroids and Hydromedusae. Oxford: Clarendon Press, pp. 299–310.Google Scholar
Pagliara, P., Bouillon, J. and Boero, F. (2000) Photosynthetic planulae and planktonic hydroids contrasting strategies of propagule survival. Scientia Marina 64, 173–178.Google Scholar
Ralph, P.M. (1956) Variation in Obelia geniculata (Linnaeus, 1758) and Silcularia bilabiata (Coughtrey, 1875) (Hydroida, F. Campanulariidae). Transactions of the Royal Society of New Zealand 84, 279–296.Google Scholar
Roosen-Runge, E.C. (1970) Life cycle of the Hydromedusa Phialidium gregarium (A. Agassiz, 1862) in the laboratory. Biological Bulletin. Marine Biological Laboratory, Woods Hole 139, 203–221.Google Scholar
Russell, F.S. (1953) The medusae of the British Isles Vol. I: Anthomedusae, Leptomedusae, Limnomedusae, Trachymedusae and Narcomedusae. Cambridge: Cambridge University Press.Google Scholar
Schuchert, P. (2003) Hydroids (Cnidaria, Hydrozoa) of the Danish expedition to the Kei Islands. Steenstrupia 27, 137–256.Google Scholar
Schuchert, P. (2012) World Hydrozoa database. Available at: http://www.marinespecies.org/hydrozoa/aphia.php?p=taxdetails&id=117030 (accessed 2 July 2013).Google Scholar
Schuchert, P. and Reiswig, H.M. (2006) Brinckmannia hexactinellidophila, n. genera, n. sp. a hydroid living in tissues of glass sponges of the reefs, fjords, and seamounts of Pacific Canada and Alaska. Canadian Journal of Zoology 84, 564–572.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Uchida, T. (1947) Some medusa from the central pacific. Journal of the Faculty of Science. Hokkaido University 9, 297–319.Google Scholar
Wang, W.Q. and Xu, Z.Z. (1990) Nematocysts of some species of Siphonophores and Scyphomedusae in Xiamen Harbour. Journal of Xiamen University (Natural Science) 29, 85–88. [In Chinese.]Google Scholar
Weill, R. (1934) Contribution à l’étude des cnidaries et leurs nématocysts. I, II. Travaux de la Station Zoologique de Wimereux, 10/11, 1–701.Google Scholar
West, D.L. and Renshaw, R.W. (1970) The life cycle of Clytia attenuata (Calyptoblastea: Campanulariidae). Marine Biology 7, 332–339.Google Scholar
Xu, Z.Z., Huang, J.Q. and Wang, W.Q. (1985) On new species and records of Hydromedusae from the Jiulong river estuary of Fujian, China. Journal of Xiamen University (Natural Science) 24, 102–110. [In Chinese.]Google Scholar
Zheng, L.M., Lin, Y.S., Li, S.J., Cao, W.Q., Xu, Z.Z. and Huang, J.Q. (2009) Aequorea taiwanensis n. sp. (Hydrozoa, Leptomedusae) and mtCOI sequence analysis for the genus Aequorea . Acta Oceanologica Sinica 28, 109–115.Google Scholar
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