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Type: Articles
Published: 2012-07-04
Page range: 211–228
Abstract views: 69
PDF downloaded: 54

Two newly recorded invasive alien ascidians (Chordata, Tunicata, Ascidiacea) based on morphological and molecular phylogenetic analysis in Korea

Department of Life Science, Sahmyook University, Seoul 139-742
Department of Biotechnology, Korea University, Seoul 136-701
Department of Life Science, Sahmyook University, Seoul 139-742
Hemichordata Ascidians Ascidiella aspersa Molgula manhattensis invasive alien species Korea morphological characters 18S rDNA mt-COI molecular phylogenetic analysis

Abstract

We report five alien ascidians with some distinct features that were investigated from August 2009 to October 2011 in Korea, among which Ascidiella aspersa (Müller, 1776) belonging to family Ascidiidae of order Phlebobranchia and Molgula manhattensis (De Kay, 1843) belonging to family Molgulidae of order Stolidobranchia are newly discovered invasive species. These ascidians were identified and their phylogenetic relationships were clarified through molecular analysis using about 680 bp of nuclear 18S rDNA and about 670 bp of mt-COI genes along with detailed morphological characteristics, and reported for the first time in Korea. It was discovered that A. aspersa was widespread three coastlines of Korea except Jeju Island, and M. manhattensis first found in Mokpo, Gunsan, and Incheon in June 2010 extended into Busan of Korea Strait in 2011.

References

  1. Alder, J. & Hancock, A. (1905) The British Tunicata an unfinished monograph. volume I, edited by J. Hopkinson. Ray Society, London. 146 pp.

    Alder, J. & Hancock, A. (1907) The British Tunicata an unfinished monograph. volume II, edited by J. Hopkinson. Ray Society, London, 164 pp.

    Avise, J.C. (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, Massachusetts, 447 pp.

    Baker, P., Baker, S.M. & Fajans, J. (2004) Nonindigenous marine species in the greater Tampa Bay ecosystem. Tampa Bay Estuary Program Technical Publication, 1–123.

    Berrill, N.J. (1928) The Identification and Validity of Certain Species of Ascidians. Journal of the Marine Biological Association of the United Kingdom, 159–175.

    Byrne, M., Morrice, M.G. & Wolf, B. (1997) Introduction of the northern Pacific asteroid Asterias amurensis to Tasmania: reproduction and current distribution. Marine Biology, 127, 673–685.

    Carman, M.R. & Grunden, D.W. (2010) First occurrence of the invasive tunicate Didemnum vexillum in eelgrass habitat. Aquatic Invasions, 5, 23–29.

    Carman, M.R., Bullard, S.G. & Donnelly J.P. (2007) Water quality, nitrogen pollution, and ascidian diversity in coastal waters of southern Massachusetts, USA, Journal of Experimental Marine Biology and Ecology, 342, 175–178.

    Carver, C.E., Mallet, A.L. & Vercaemer, B. (2006) Biological Synopsis of the Solitary Tunicate Ciona intestinalis. Canadian Manuscript Report of Fisheries and Aquatic Science, 2746, 1–55.

    Carreras-Carbonell, J., Macpherson, E. & Pascual, M. (2005) Rapid radiation and cryptic speciation in mediterranean triplefin blennies (Pisces: Tripterygiidae) combining multiple genes. Molecular Phylogenetics and Evolution, 37, 751–761.

    Castilla, J.C., Uribe, M., Bahamonde, N., Clarke, M., Desqueyroux-Faúndez, R., Kong, I., Moyano, H., Rozbaczylo, N., Santelices, B., Valdovinos, C. & Zavala, P. (2005) Down under the southeastern Pacific: marine non-indigenous species in Chile. Biological Invasions, 7, 213–232.

    Cohen, A.N., Harris, L.H., Bingham, B.L., Carlton, J.T. & Chapman, J.W. (2005) Rapid assessment survey for exotic organisms in southern California bays and harbors, and abundance in port and non-port areas. Biological Invasions, 7, 995–1002.

    Cohen, A.N. & Carlton, J.T. (1996) Nonindigenous aquatic species in a United States estuary: a case study of the biological invasions of the San Francisco Bay and Delta. United States Fish and Wildlife service, Washington D.C. & the National Sea Grant College Program, Connecticut Sea Grant (NOAA Grant Number NA36RG0467), 1–218.

    Coles, S.L., DeFelice, R.C., Eldredge, L.G. & Carlton. J.T. (1999) Historical and recent introductions of non-indigenous marine species into Pearl harbor, Oahu, Hawaiian Islands. Marine Biology, 135, 147–158.

    Currie, D.R., McArthur, M.A. & Cohen, B.F. (1998) Exotic marine pests in the port of Geelong, Victoria. Marine and Freshwater Resources Institute, 8, 1–72.

    Da Rocha, R.M. & Kremer, L.P. (2005) Introduced Ascidians in Paranagua Bay, Parana, southern Brazil. Revista Brasileira de Zoologia, 22, 1170–1184.

    De Barros, R.C., Da Rocha, R.M. & Pie, M.R. (2009) Human-mediated global dispersion of Styela plicata (Tunicata, Ascidiacea). Aquatic Invasions, 4, 45–57.

    De Caralt, S., López-Legentil, S., Tarjuelo, I., Uriz, M.J. & Turon, X. (2002) Contrasting biological traits of Clavelina lepadiformis (Ascidiacea) populations from inside and outside harbours in the western Mediterranean. Marine Ecology Progress Series, 244, 125–137.

    De Kay, J.E. (1843) Zoology of New York, or the New York fauna, part. 5, Mollusca. Albany, 271 pp.

    Delsuc, F., Brinkmann, H., Chourrout, D. & Philippe, H. (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature, 439, 965–968.

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & 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.

    Fuller, F. (2012) Styela plicata. USGS Nonindigenous Aquatic Species Database, Gainesville, FL. Available from http://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=1293 (access-ed: 8/21/2010)

    Hadfield, K.A., Swalla, B.J. & Jeffery, W.R. (1995) Multiple origins of anural development in ascidians inferred from rDNA sequences. Journal of Molecular Evolution, 40, 413–427.

    Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    Haydar, D., Hoarau, G., Olsen, J.L., Stam, W.T. & Wolff, W.J. (2011) Indroduced or glacial relict? phylogeography of the cryptogenic tunicate Molgula mangattensis (Ascidiacea, Pleurogona). Diversity and Distributions, 17, 68–80.

    Herdman, W.A. (1899) Descriptive catalogue of the Tunicata in the Australian museum. Liverpool by T. Dobb and Company, 139 pp.

    Hewitt, C.L., Campbell, M.L., Thresher, R.E., Martin, R.B., Boyd, S., Cohen, B.F., Currie, D.R., Gomon, M.F., Keough, M.J., Lewis, J.A., Lockett, M.M., Mays, N., McArthur, M.A., O’Hara, T.D., Poore, G.C.B., Ross, D.J., Storey, M.J., Watson, J.E. & Wilson, R.S. (2004) Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Marine Biology, 144, 183–202.

    Hiscock, K. (2008) Molgula manhattensis. Sea grapes. Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme. Plymouth: Marine Biological Association of the United Kingdom. Available from http://www.marlin.ac.uk/speciesfullr eview.php?speciesID=3823/ (accessed 10/01/2011)

    Howes, S., Herbinger, C.M., Darnell, P., Vercaemer, B. (2007) Spatial and temporal patterns of recruitment of the tunicate Ciona intestinalis on a mussel farm in Nova Scotia, Canada. Journal of Experimental Marine Biology and Ecology, 342, 85–92.

    Huber, J.L., Burke da Silva, K., Bates, W.R. & Swalla, B.J. (2000) The ecolution of anural larvae in molgulid ascidians. Cell & Developmental Biology, 11, 419–426.

    Inglis, G., Gust, N., Fitridge, I., Floerl, O., Woods, C., Kospartov, M., Hayden, B. & Fenwick, G. (2008) Port of Lyttelton Second baseline survey for non-indigenous marine species (Research Profext ZBS2000-04). Ministry of Agriculture and Forestry Biosecurity New Zealand Technical Paper, 1–139.

    Kott, P. (1972) The ascidians of the South Australia. 2. Eastern sector of the Great Australian Bight and investigator strast. Transactions of the Royal Society of South Australia, 96, 165–196.

    Lahille, F. (1886) Sur la classification des Tuniciers. The French Academy of Sciences, 102, 1573–1575.

    Lambert, C.C. & Lambert, G. (1998) Non-indigenous ascidians in southern California harbours and marinas. Marine Biology, 130, 675–688.

    Lambert, G. (2002) Nonindigenous ascidians in tropical waters. Pacific Science, 56, 291–298.

    Lesueur, C.A. (1823) Descriptions of several new species of Ascidia. Journal of the Academy of Natural Sciences of Philadelphia, 3, 2–8.

    Millar, R.H. (1952) The Annual Growth and Reproductive Cycle in Four Ascidians. Journal of the Marine Biological Association of the United Kingdom, 31, 41–61.

    Milne-Edwards, M. (1841) Observation sur les Ascidies composées des cotes de la Manche. Member of the Academy of Sciences of the Institute, France, 18, 217–326.

    Monniot, C. (1969) Les Molgulidae des mers Européennes. Mémoires du Muséum National d’Histoire Naturelle - Série A, Zoologie, 60, 172–272.

    Müller, O.F. (1776) Zoologiae Danicae Prodromus, seu animalium Daniae et Norvegiae Indigenarum characteres, nomina, et synonyma imprimis popularum. Typis Hallageriis, Havniae, Copenhagen, 282 pp.

    NIMPIS (2012) Ascidiella aspersa general information, National Introduced Marine Pest Information System. Available from http://adl.brs.gov.au/marinepests/index.cfm?fa=main. spDetailsDB&sp=6000005711 (accessed 20 January 2010)

    Nydam, M.L. & Harrison, R.G. (2007) Genealogical relationships within and among shallow-water Ciona species (Ascidiacea). Marine Biology, 151, 1839–1847.

    Passamaneck, Y.J. & Gregorio, A.D. (2005) Ciona intestinalis: Chordate development made simple. Developmental Dynamics, 233, 1–19.

    Perrier, E. (1898) Note sur la Classification des Tuniciers. Comptes Rendus Academic Science Paris, 126, 1758–1762.

    Petersen, J.K. (2007) Ascidian suspension feeding. Journal of Experimental Marine Biology and Ecology, 342, 127–137.

    Picton, B.E. & Morrow, C.C. (2010a) Ascidiella aspersa general information. Available from (accessed 13 April 2010)

    Picton, B.E. & Morrow, C.C. (2010b) Ciona intestinalis general information. Available from (accessed 9 June 2010)

    Pineda, M.C., López-Legentil, S. & Turon, X. (2011) The Whereabouts of an Ancient Wanderer: Global Phylogeography of the Solitary Ascidian Styela plicata. PLoS ONE, 6, e25495.

    Posada, D. (2008) jModeltest: phylogenetic model averaging. Molecular Biology and Evolution, 25: 1253–1256.

    Pyo, J. & Shin, S. (2011) A New Record of Invasive Alien Colonial Tunicate Clavelina lepadiformis (Ascidiacea: Aplousobranchia: Clavelinidae) in Korea. Korean Journal of Systematic Zoology, 27, 197–200.

    Reinhardt, J.F., Stefaniak, L.M., Hudson, D.M., Mangiafico, J., Gladych, R. & Whitlatch, R.B. (2010) First record of the non-native light bulb tunicate Clavelina lepadiformis (Müller, 1776) in the northwest Atlantic. Aquatic Invasions, 5, 185–190.

    Rho, B.J. & Lee, J.E. (1991) A Systematic Study on the Ascidians in Korea. The Korean Journal of Systematic Zoology, 7, 195–220.

    Rho, B.J. (1977) Illustrated flora and fauna of Korea (Porifera, Hydrozoa and Ascidiacea). Ministry of Education, Seoul, 20, pp.101–136, 289–374.

    Rho, B.J., Choe, B.L., Song, J.I. & Lee, Y.J. (2000) Ascidians of Tangsa and its Adjacent Waters in Korea Strait. The Korean Journal of Systematic Zoology, 16: 39–53.

    Riley, K. (2008) Clavelina lepadiformis. Light bulb sea squirt. Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme. Plymouth: Marine Biological Association of the United Kingdom. Available from http://www.marlin.ac.uk/ speciesinformation.php?speciesID=3009 (accessed 20 June 2010)

    Ronquist, F. & Huelsenbeck, J.P. (2003) Mrbayes: bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Sanamyan, K. (2010) Asicidia lepadiformis Mueller, 1776. Available from http://www. marinespecies.org/ascidiacea/aphia.php?p=taxdetails&id=252057 (accessed 2 June 2010)

    Sanamyan, K. & Monniot, C. (2011a) Clavelina lepadiformis (Müller, 1776). Available from http://www.marinespecies.org/ascidiacea/aphia.php?p=taxdetails&id=103552 (accessed 4 June 2010)

    Sanamyan, K. & Monniot, C. (2011b) Ascidiella aspersa (Müller, 1776). Available from http://www.marinespecies.org/ascidiacea/aphia.php?p=taxdetails&id=103718 (accessed 10 July 2010)

    Sanamyan, K. & Monniot, C. (2011c) Molgula manhattensis (De Kay, 1843). Available from http://www. marinespecies.org/ascidiacea/aphia.php?p=taxdetails&id=103788 (accessed 15 January 2011)

    Sanamyan, K. & Monniot, C. (2011d) Styela plicata (Lesueur, 1823). Available from http://www.marinespecies.org/ascidiacea/aphia.php?p=taxdetails&id=103936 (accessed 28 March 2011)

    Shenkar, N. & Swalla, B.J. (2011) Global diversity of Ascidiacea. PLoS ONE, 6(6), 1–12

    Shenkar, N., Gittenberger, A., Lambert, G., Rius, M., Da Rocha, R.M., Swalla, B.J. & Turon, X (2012) World Ascidiacea Database. Available online at http://www.marinespecies. org/ascidiacea.

    Shenkar, N., Sanamyan, K. & Monniot, C. (2011) Ciona intestinalis (Linnaeus, 1767). Available from http://www.marinespecies.org/ascidiacea/aphia.php?p=taxdetails&id=103732 (accessed 2 October 2010)

    Shirley, P.N. (2003) Aplousobranch ascidians (Tunicata: Ascidiacea) from southern Africa. PhD dissertation, University of Port Elizabeth, Port Elizabeth, South Africa, 199 pp.

    Stach, T. & Turbeville, J.M. (2002) Phylogeny of Tunicata inferred from molecular and morphological characters. Molecular Phylogenetics and Evolution, 25, 408–428.

    Stachowicz, J.J., Fried, H., Osman, R.W. & Whitlatch, B.B. (2002) Biodiversity, Invasion Resistance, and Marine Ecosystem Function: Reconcling Pattern and Process. The Ecological Society of America, 2575–2590.

    Swalla, B.J., Cameron, C.B., Corley, L.S. & Garey J.R. (2000) Urochordates Are Monophyletic Within the Deuterostomes. Sytematic Biology, 49, 52–64.

    Therriault, T.W., & Herborg L-M., (2008) A qualitative biologgical risk assessment for vas tunicate Ciona intestinalis in Canadian waters: using expert knowledge. ICES Journal of Marine Science, 65, 781–787.

    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.

    Tokioka, T. (1954) Contributions to Japanese Ascidian Fauna notes on some Ascidians Collected in Osaka Bay. Seto Marine Biological Laboratory, 75–98.

    Tokioka, T. (1960) Ascidians Found in The Benthonic Samples Dredged in the Ariake Sea 1957–58. Seto Marine Biological Laboratory, 205–218.

    Tokioka, T. & Kado, Y. (1972) The occurrence of Molgula manhattensis (de Kay) in brackish water near Hiroshima, Japan. Publications of the Seto Marine Biological Laboratory, Kyoto University, 21, 21–29.

    Tsagkogeorga, G., Turon, X., Hopcroft, R.R., Tilak, M., Feldstein, T., Shenkar, N., Loya, Y., Huchon, D., Douzery, E.J.P. & Delsuuc, F. (2009). An updated 18S rRNA phylogeny of tunicates based on mixture and secondary structure models. BMC Evolutionary Biology, 9, 1–187.

    Turon, X. & López-Legentil, S. (2004) Ascidian molecular phylogeny inferred from mtDNA data with emphasis on the Aplousobranchiata. Molecular Phylogenetics and Evolution, 33, 309–320.

    Turon, X., Tarjuelo, I., Duran, S. & Pascual, M. (2003) Characterising invasion processes with genetic data: an Atlantic clade of Clavelina lepadiformis (Ascidiacea) introduced into Mediterranean harbours. Hydrobiologia, 503, 29–35.

    Van Name, W.G. (1912) Simple ascidians of the coasts of New England and neighboring British provinces. Proceedings of the Boston Society of Natural History, 34, 439–619.

    Van Name, W.G. (1945) The North and South American ascidians. Bulletin of American Museum of Natural History, 84, 1–476.

    Veeman, M.T., Chiba, S. & Smith, W.C. (2011) Ciona Genetics. Methods Molecular Biology, 770, 401–422.

    Wada, H. (1998) Evolutionary History of Free-Swimming and Sessile Life styles in Urochordates as Deduced from 18S rDNA Molecular Phylogeny. The Society for Molecular Biology and Evolution, 1189–1194.

    Wada, H., Makabe, K.W., Nakauchi, M. & Satoh, N. (1992) Phylogenetic relationships between solitary and colonial ascidians, as inferred from the sequence of the central region of their respective 18S rDNAs. Biological Bulletin, 183, 448–445.

    Wirtz, P. (1998) Twelve invertebrate and eight fish species new to the marine fauna of Madeira, and a discussion of the zoogeography of the area. Helgoländer Meeresunters. 52, 197–207.

    Yamaguchi, M. (1975) Growth and reproductive cycles of the marine fouling ascidians Ciona intestinalis, Styela plicata, Botrylloides violaceus, and Leptoclinum mitsukurii at Aburatsubo-Moroiso Inlet (Central Japan). Ymrine Biology, 29, 253–259.

    Zeng, L. & Swalla, B.J. (2005) Molecular phylogeny of the protochordates: chordate evolution. Canadian Journal of Zoology, 83, 24–33.

    Zeng, L., Jacob, M.W. & Swalla, B.J. (2006). Coloniality has evolved once in stolidobranch ascidians. Intergrative and Comparative Biology, 46, 255–268.