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Morphology and molecular analyses of a new Clytia species (Cnidaria: Hydrozoa: Campanulariidae) from the East China Sea

Published online by Cambridge University Press:  27 June 2014

Jinru He ,
Lianming Zheng ,
Wenjing Zhang ,
Yuanshao Lin  and
Wenqing Cao
Jinru He
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361102, China
Lianming Zheng*
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361102, China Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies (CEES), Xiamen University, Xiamen 361102, China College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China
Wenjing Zhang
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361102, China Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies (CEES), Xiamen University, Xiamen 361102, China
Yuanshao Lin
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361102, China Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies (CEES), Xiamen University, Xiamen 361102, China
Wenqing Cao
Affiliation:
Marine Biodiversity and Global Change Research Center, Xiamen University, Xiamen 361102, China Fujian Provincial Key Laboratory for Coastal Ecology and Environmental Studies (CEES), Xiamen University, Xiamen 361102, China
*
Correspondence should be addressed to: L. Zheng, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, China email: [email protected]
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Abstract

The near-cosmopolitan genus Clytia is abundantly found in coastal waters, but difficulties of identification in this genus make nearly all species records of medusae suspect. Complex life histories, ambiguous taxonomic characters, and phenotypic plasticity pose serious problems for accurate species-level identifications and future revisions of Clytia species. In the present study, morphological investigations and molecular analyses of Clytia specimens from the coastal waters of the East China Sea revealed Clytia gulangensis sp. nov. as a new species. DNA barcoding based on the mitochondrial cytochrome oxidase I (COI) gene supported the new species as a separate species within Clytia, and phylogenetic analyses based on mitochondrial 16S rDNA and nuclear 18S rDNA further confirmed this new species to be a distinct lineage. Moreover, detailed observation of medusae and polyps of this species showed sufficient morphological differences from other Clytia species for a diagnosis. Our results indicated that life cycle and DNA-based studies should be a standard approach in future biodiversity investigations of Clytia species.

Keywords

Clytianew speciesmorphologymolecular analysis
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 2 , March 2015 , pp. 289 - 300
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Agassiz, A. and Mayer, A.G. (1899) Acalephs from the Fiji Islands. Bulletin of the Museum of Comparative Zoology 32, 157–189.Google Scholar
Agassiz, L. (1862) Hydroids of the family Cytaeidae. Bulletin of the British Museum (Natural History) Zoology 8, 379–400.Google Scholar
Bigelow, H.B. (1904) Medusae from the Maldive Islands. Bulletin of the Museum of Comparative Zoology 39, 245–269.Google Scholar
Boero, F., Bouillon, J. and Piraino, S. (1996) Classification and phylogeny in the Hydroidomedusae (Hydrozoa, Cnidaria). Scientia Marina 60, 17–33.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. (1984) Révision de la famille des Phialuciidae (Kramp, 1955) (Leptomedusae, Hydrozoa, Cnidaria), avec un essai de classification des Thecatae—Leptomedusae. Indo-Malayan Zoology 1, 1–24.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.Google Scholar
Bouillon, J., Medel, M.D., Pagès, F., Gili, J.M., Boero, F. and Gravili, C. (2004) Fauna of the Mediterranean Hydrozoa. Scientia Marina 68, 5–449.CrossRefGoogle Scholar
Bridge, D., Cunningham, C.W., DeSalle, R. and Buss, L.W. (1995) Class-level relationships in the phylum Cnidaria: molecular and morphological evidence. Molecular Biology and Evolution 12, 679–689.Google ScholarPubMed
Bucklin, A., Hopcroft, R.R., Kosobokova, K.N., Nigro, L.M., Ortman, B.D., Jennings, R.M. and Sweetman, C.J. (2010a) DNA barcoding of Arctic Ocean holozooplankton for species identification and recognition. Deep-Sea Research Part II: Topical Studies in Oceanography 57, 40–48.CrossRefGoogle Scholar
Bucklin, A., Ortman, B.D., Jennings, R.M., Nigro, L.M., Sweetman, C.J., Copley, N.J., Sutton, T. and Wiebe, P.H. (2010b) A “Rosetta Stone” for metazoan zooplankton: DNA barcode analysis of species diversity of the Sargasso Sea (Northwest Atlantic Ocean). Deep-Sea Research Part II: Topical Studies in Oceanography 57, 2234–2247.CrossRefGoogle Scholar
Bucklin, A., Steinke, D. and Blanco-Bercial, L. (2011) DNA barcoding of marine metazoa. Annual Review of Marine Science 3, 471–508.CrossRefGoogle ScholarPubMed
Calder, D.R. (1991) Shallow-water hydroids of Bermuda: the Thecatae, exclusive of Plumularioidea. Toronto: Royal Ontario Museum.Google Scholar
Collins, A.G., Schuchert, P., Marques, A.C., Jankowski, T., Medina, M. and Schierwater, B. (2006) Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Systematic Biology 55, 97–115.CrossRefGoogle Scholar
Collins, A.G., Winkelmann, S., Hadrys, H. and Schierwater, B. (2005) Phylogeny of Capitata and Corynidae (Cnidaria, Hydrozoa) in light of mitochondrial 16S rDNA data. Zoologica Scripta 34, 91–99.CrossRefGoogle Scholar
Cornelius, P.F.S. (1982) Hydroids and medusae of the family Campanulariidae recorded from the eastern North Atlantic, with a world synopsis of genera. Bulletin of the British Museum of Natural History 42, 37–148.Google Scholar
Cornelius, P.F.S. (1995) North-west European thecate hydroids and their medusae: part 1 introduction, Laodiceidae to Haleciidae: keys and notes for identification of the species. In Barnes, R.S.K. and Crothers, J.H. (eds) Synopses of the British fauna (New Series). London: Linnean Society of London, pp. 1–347.Google Scholar
Du, F.Y., Xu, Z.Z., Huang, J.Q. and Guo, D.H. (2012) Studies on the medusae (Cnidaria) from the Beibu Gulf in the Northern South China Sea, with description of three new species. Acta Zootaxonomica Sinica 37, 506–519.Google Scholar
Ender, A. and Schierwater, B. (2003) Placozoa are not derived cnidarians: evidence from molecular morphology. Molecular Biology and Evolution 20, 130–134.CrossRefGoogle Scholar
Evans, N.M., Lindner, A., Raikova, E.V., Collins, A.G. and Cartwright, P. (2008) Phylogenetic placement of the enigmatic parasite, Polypodium hydriforme, within the Phylum Cnidaria. BMC Evolutionary Biology 9, 165.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Fraser, C.M. (1944) Hydroids of the Atlantic coast of North America. Toronto: The University of Toronto Press.Google Scholar
Galea, H.R. (2010) Additional shallow-water thecate hydroids (Cnidaria: Hydrozoa) from Guadeloupe and Les Saintes, French Lesser Antilles. Zootaxa 2570, 1–40.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.CrossRefGoogle ScholarPubMed
Gravili, C., D'Ambrosio, P., Di Camillo, C., Renna, G., Bouillon, J. and Boero, F. (2008) Clytia hummelincki (Hydroidomedusae: Leptomedusae) in the Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 88, 1547–1553.CrossRefGoogle Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. and deWaard, J.R. (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society B—Biological Sciences 270, 313–321.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Ratnasingham, S. and deWaard, J.R. (2003b) Barcoding animal life: cytochrome c oxidase subunit I divergences among closely related species. Proceedings of the Royal Society B—Biological Sciences 270, S96–S99.CrossRefGoogle ScholarPubMed
Hiro, F. (1939) Notes on the animals found on Macrocheira kaempferi de Haan. III. Hydroids. Annotations Zoologicae Japonenses 18, 167–176.Google Scholar
Houliston, E., Momose, T. and Manuel, M. (2010) Clytia hemisphaerica: a jellyfish cousin joins the laboratory. Trends in Genetics 26, 159–167.Google ScholarPubMed
Huang, Z.G. (2008) Marine species and their distributions in China's Seas. Beijing: China Ocean Press. [In Chinese.]Google Scholar
Huang, Z.G. and Lin, M. (2012) The living species and their illustrations in China's Seas. Beijing: China Ocean Press. [In Chinese.]Google Scholar
Kelmo, F. and Attrill, M.J. (2003) Shallow-water Campanulariidae (Hydrozoa, Leptothecatae) from Northern Bahía, Brazil. Revista de biologia tropical 51, 123–146.Google ScholarPubMed
Kramp, P.L. (1961) Synopsis of the Medusae of the World. Journal of the Marine Biological Association of the United Kingdom 40, 1–469.CrossRefGoogle Scholar
Kubota, S. (1978a) Notes on Clytia and Phialidium (Hydrozoa; Campanulariidae) from Shimoda, Japan. Proceedings of the Japanese Society of Systematic Zoology 15, 1–7.Google Scholar
Kubota, S. (1978b) 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
Laakmann, S. and Holst, S. (2014) Emphasizing the diversity of North Sea hydromedusae by combined morphological and molecular methods. Journal of Plankton Research 36, 64–76.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Leclère, L., Schuchert, P., Cruaud, C., Couloux, A. and Manuel, M. (2009) Molecular phylogenetics of Thecata (Hydrozoa, Cnidaria) reveals long-term maintenance of life history traits despite high frequency of recent character changes. Systematic Biology 58, 509–526.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle Scholar
Lucas, C.H., Williams, D.W., Williams, J.A. and Sheader, M. (1995) Seasonal dynamics and production of the hydromedusan Clytia hemisphaerica (Hydromedusa: Leptomedusa) in Southampton Water. Estuaries 18, 362–372.CrossRefGoogle Scholar
Madin, L.P., Bollens, S.M., Horgan, E., Butler, M., Runge, J., Sullivan, B.K., Klein-Macphee, G., Durbin, E., Durbin, A.G., Keuren, D.V., 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.CrossRefGoogle Scholar
Mayer, A.G. (1910) Medusae of the world. II. The hydromedusae. Washington: Carnegie Institution.CrossRefGoogle Scholar
Medina, M., Collins, A.G., Silberman, J.D. and Sogin, M.L. (2001) Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proceedings of the National Academy of Sciences of the United States of America 98, 9707–9712.CrossRefGoogle ScholarPubMed
Meyer, C.P. and Paulay, G. (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3, 2229–2238.CrossRefGoogle ScholarPubMed
Miglietta, M.P., Rossi, M. and Collin, R. (2008) Hydromedusa blooms and upwelling events in the Bay of Panama, Tropical East Pacific. Journal of Plankton Research 30, 783–793.CrossRefGoogle Scholar
Millard, N.A.H. (1975) Monograph on the Hydroida of southern Africa. Annals of the South African Museum 68, 1–513.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.CrossRefGoogle Scholar
Ortman, B.D., Bucklin, A., Pagès, F. and Youngbluth, M. (2010) DNA Barcoding the Medusozoa using mtCOI. Deep-Sea Research Part II: Topical Studies in Oceanography 57, 2148–2156.CrossRefGoogle Scholar
Östman, C. (1979a) Nematocysts in the Phialidium medusae of Clytia hemisphaerica (Hydrozoa, Campanulariidae) studied by light and scanning electron microscopy. Zoon Uppsala 7, 125–142.Google Scholar
Östman, C. (1979b) Two types of nematocysts in Campanulariidae (Cnidaria, Hydrozoa) studied by light and scanning electron microscopy. Zoologica Scripta 8, 5–12.CrossRefGoogle 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. (2000) A guideline to nematocyst nomenclature and classification, and some notes on the systematic value of nematocysts. Scientia Marina 64, 31–46.CrossRefGoogle Scholar
Pagliara, P., Bouillon, J. and Boero, F. (2000) Photosynthetic planulae and planktonic hydroids contrasting strategies of propagule survival. Scientia Marina 64, 173–178.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Schierwater, B. and Ender, A. (2000) Sarsia marii n. sp. (Hydrozoa, Anthomedusae) and the use of 16S rDNA sequences for unpuzzling systematic relationships in Hydrozoa. Scientia Marina 64, 117–122.CrossRefGoogle Scholar
Schuchert, P. (1998) How many hydrozoan species are there? Zoologische Verhandelingen (Leiden) 323, 209–219.Google Scholar
Schuchert, P. (2003) Hydroids (Cnidaria, Hydrozoa) of the Danish expedition to the Kei Islands. Steenstrupia 27, 137–256.Google Scholar
Schuchert, P. (2013) World Hydrozoa database. Available at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=117030 (accessed 3 June 2014).Google Scholar
Schuchert, P. (2014) High genetic diversity in the hydroid Plumularia setacea: a multitude of cryptic species or extensive population subdivision? Molecular Phylogenetics and Evolution 76, 1–9.CrossRefGoogle ScholarPubMed
Swofford, D.L. (2002) PAUP* (Phylogenetic Analysis Using Parsimony). Sunderland, MA: Sinauer.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
Thornely, L.R. (1900) The hydroid zoophytes collected by Dr Willey in the southern seas. In Willey, A. (ed.) Zoological results based on material from New Britain, New Guinea, Loyalty Islands and elsewhere. Part IV. Cambridge: Cambridge University Press, pp. 451–457.Google Scholar
Torrey, H.B. (1909) The Leptomedusae of the San Diego region. Berkeley, CA: University of California Press.Google Scholar
Vervoort, W. and Watson, J.E. (2003) The marine fauna of New Zealand: Leptothecata (Cnidaria: Hydrozoa) (Thecate Hydroids). NIWA Biodiversity Memoir 119, 1–538.Google Scholar
West, D.L. and Renshaw, R.W. (1970) The life cycle of Clytia attenuata (Calyptoblastea: Campanulariidae). Marine Biology 7, 332–339.CrossRefGoogle Scholar
Xu, Z., Huang, J. and Chen, X. (1991) On new species and record of Hydromedusae in the upwelling region off the Minnan-Taiwan Bank fishing ground, China. In Hong, H., Qiu, S., Ruan, W. and Hong, G. (eds) Minnan-Taiwan bank fishing ground upwelling ecosystem study. Beijing: Science Press, pp. 469–486. [In Chinese with English abstract.]Google Scholar
Zheng, L., He, J., Lin, Y., Cao, W. and Zhang, W. (2014) 16S rRNA is a better choice than COI for DNA barcoding hydrozoans in the coastal waters of China. Acta Oceanologica Sinica 33, 55–76.CrossRefGoogle Scholar
Zheng, L., Lin, Y., Li, S., Cao, W., Xu, Z. and Huang, J. (2009) Aequorea taiwanensis n. sp. (Hydrozoa, Leptomedusae) and mtCOI sequence analysis for the genus Aequorea. Acta Oceanologica Sinica 28, 109–115.Google Scholar
Zhou, K., Zheng, L., He, J., Lin, Y., Cao, W. and Zhang, W. (2013) Detection of a new Clytia species (Cnidaria: Hydrozoa: Campanulariidae) with DNA barcoding and life cycle analyses. Journal of the Marine Biological Association of the United Kingdom 93, 2075–2088.CrossRefGoogle Scholar
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