Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-23T21:27:59.891Z Has data issue: false hasContentIssue false

Life history traits and population dynamics of the invasive ascidian, Ascidiella aspersa, on cultured scallops in Funka Bay, Hokkaido, northern Japan

Published online by Cambridge University Press:  11 April 2016

Makoto Kanamori*
Affiliation:
Hakodate Fisheries Research Institute, Fisheries Research Department, Hokkaido Research Organization, 20-5, Benten, Hakodate, Hokkaido 040-0051, Japan Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato, Hakodate, Hokkaido 041-8611, Japan
Katsuhisa Baba
Affiliation:
Fisheries Research Department, Hokkaido Research Organization, 38, Hamamachi, Yoichi, Hokkaido 046-8555, Japan
Masafumi Natsuike
Affiliation:
Graduate School of Science and Engineering, Tokyo Institute of Technology, 2-12-1 Ookayama, Meguro, Tokyo 152-8550, Japan
Seiji Goshima
Affiliation:
Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato, Hakodate, Hokkaido 041-8611, Japan
*
Correspondence should be addressed to:M. Kanamori, Fisheries Research Department, Hakodate Fisheries Research Institute, Hokkaido Research Organization, 20-5, Benten, Hakodate, Hokkaido 040-0051, Japan email: [email protected]

Abstract

The European sea squirt, Ascidiella aspersa was first found as an alien species in 2008 from Funka Bay, Hokkaido, northern Japan, causing serious damage to the scallop aquaculture industry. We investigated A. aspersa on cultured scallops and larval occurrence from July 2010 to June 2014 to clarify life history traits and population dynamics, and consider the relation between the life history of A. aspersa and the process of scallop aquaculture. Larvae of A. aspersa were found from June to December, and recruitment on cultured scallops occurred mainly between July and October. The ascidians grew well and their weights increased until February. We found that 60–80% of A. aspersa that had settled in summer had eggs or sperm in autumn, and 90–100% of A. aspersa matured early the following summer. Maturity size in September was 17–20 mm as male, 22–24 mm as female. Scallops in Funka Bay are hung in the spring and harvested from winter to the next spring. Ascidiella aspersa settle as larvae in early summer, and grow well until winter, resulting in overgrowth on scallops in the harvest season. The linking of the process of scallop aquaculture and the life history of A. aspersa explains why this invasive ascidian has caused serious damage to the aquaculture industry in the bay. In comparison to the earlier descriptions of the native population, A. aspersa in Funka Bay has longer reproductive and growth periods, earlier initiation of reproduction, and possibly smaller maturity size.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Berrill, N.J. (1950) The tunicata with an account of the British species. London: Ray Society.Google Scholar
Blossey, B. and Nötzold, R. (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology 83, 887889.Google Scholar
Bourque, D., Davidson, J., MacNair, N.G., Arsenault, G., LeBlanc, A.R., Landry, T. and Miron, G. (2007) Reproduction and early life history of an invasive ascidian Styela clava Herdman in Prince Edward Island, Canada. Journal of Experimental Marine Biology and Ecology 342, 7884.CrossRefGoogle Scholar
Brewin, B.I. (1946) Ascidians in the vicinity of the Portobello Marine Biological Station, Otago Harbour. Transactions of the Royal Society of New Zealand 76, 87131.Google Scholar
Carlton, J.T. (2000) Quo Vadimus Eotica Oceanica? Marine bioinvasion ecology in the twenty-first century. In Pederson, J. (ed.) Marine bioinvasions: Proceedings of the First National Conference, January 24–27, 1999. Cambridge, MA: Massachusetts Institute of Technology, pp. 610.Google Scholar
Carman, M.R., Morris, J.A., Karney, R.C. and Grunden, D.W. (2010) An initial assessment of native and invasive tunicates in shellfish aquaculture of the North American east coast. Journal of Applied Ichthyology 26, 811.Google Scholar
Colautti, R.I., Ricciardi, A., Grigorovich, I.A. and Maclsaac, H.J. (2004) Is invasion success explained by the enemy release hypothesis? Ecology Letters 7, 721733.Google Scholar
Currie, D.R., McArthur, M.A. and Cohen, B.F. (1998) Exotic marine pests in the port of Geelong, Victoria. Marine and Freshwater Resources Institute Report 8, 57 pp.Google Scholar
Daigle, R.M. and Herbinger, C.M. (2009) Ecological interactions between the vase tunicate (Ciona intestinalis) and the farmed blue mussel (Mytilus edulis) in Nova Scotia, Canada. Aquatic Invasions 4, 177187.CrossRefGoogle Scholar
de Kluijver, M.J. and Ingalsuo, S.S. (2004) Ascidiella aspersa, Macrobenthos of the North Sea-Tunicata, Zoological Museum, University of Amsterdam. Available at http://wbd.etibioinformatics.nl/bis/tunicata.php?selected=beschrijving&menuentry=soorten&id=17 Google Scholar
Dybern, B.I. (1969) Distribution and ecology of ascidians in Kviturdvikpollen and Vågsböpollen on the west coast of Norway. Sarsia 37, 2140.CrossRefGoogle Scholar
Goodbody, I. (2004) Diversity and distribution of ascidians (Tunicata) at Twin Cays, Belize. Atoll Research Bulletin 524, 119.Google Scholar
Hakodate Fisheries Research Institute (2010) 12th Scallop News in Funka Bay (2010). Available at http://www.fishexp.hro.or.jp/cont/hakodate/section/zoushoku/tpc05300000007ut-att/tpc053000000080h.pdf Google Scholar
Hokkaido Government (2012) Hokkaido fisheries today 2012. Sapporo: Hokkaido Government, 125 pp.Google Scholar
Howes, S., Herbinger, C.M., Darnell, P. and Veraemer, 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, 8592.Google Scholar
Imai, I., Shimada, H., Shinada, A., Baba, K., Kanamori, M., Sato, M., Kuwahara, Y., Miyoshi, K., Tada, M., Hirano, K., Miyazono, A. and Itakura, S. (2014) Prediction of toxic algal bloom occurrences and adaptation to toxic blooms to minimize economic loss to the scallop aquaculture industry in Hokkaido, Japan. PICES Scientific Report 47, 716.Google Scholar
Japan Meteorological Agency (2010a) The weather of summer (June–August). Available at http://www.jma.go.jp/jma/press/1009/01c/tenko100608.html Google Scholar
Japan Meteorological Agency (2010b) The weather of autumn (September–December). Available at http://www.jma.go.jp/jma/press/1012/01b/tenko100911.html Google Scholar
Japan Meteorological Agency (2012) Report on the 2011 off the Pacific coast of Tohoku earthquake. Technical report of the Japan Meteorological Agency 133, 479 pp.Google Scholar
Kanamori, M., Baba, K., Hasegawa, N. and Nishikawa, T. (2012) Biological characteristics, distinction and identification of Ascidiella aspersa (Müller, 1776), as an alien ascidian in northern Japan (Technical Report). Scientific Reports of Hokkaido Fisheries Research Institutes 81, 151156.Google Scholar
Kanamori, M., Baba, K., Konda, Y. and Goshima, S. (2014) Distribution of the invasive ascidian Ascidiella aspersa (Müller, 1776) (Urochordata, Ascidiacea) in Hokkaido, Japan. Japanese Journal of Benthology 69, 2331.Google Scholar
Keane, R.M. and Crawley, M.J. (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17, 164170.Google Scholar
Kosaka, Y. and Ito, H. (2006) Japan. In Shumway, S.E. and Parsons, G.J. (eds) Scallops: biology, ecology and aquaculture, 2nd edition. Tokyo: Elsevier, pp. 10931141.Google Scholar
Kott, P. (1985) The Australian Ascidiacea Part I, Phlebobranchia and Stolidobranchia. Memoirs of The Queensland Museum 23, 1440.Google Scholar
Lambert, G. (2005) Ecology and natural history of the protochordates. Canadian Journal of Zoology 83, 3450.Google Scholar
Lambert, G. (2007) Invasive sea squirts: a growing global problem. Journal of Experimental Marine Biology and Ecology 342, 34.Google Scholar
Locke, A. and Carman, M. (2009) An overview of the 2nd International Sea Squirt Conference: what we learned. Aquatic Invasions 4, 14.CrossRefGoogle Scholar
Mackenzie, A.B. (2011) Biological synopsis of the European sea squirt Ascidiella aspersa . Canadian Manuscript Report of Fisheries and Aquatic Sciences 2968, 15 pp.Google Scholar
MAFF (2015) The 89th Statistical Yearbook of Ministry of Agriculture, Forestry and Fisheries (2013–2014). Available at http://www.maff.go.jp/e/tokei/kikaku/nenji_e/89nenji/index.html Google Scholar
Millar, R.H. (1952) The annual growth and reproductive cycle in four ascidians. Journal of the Marine Biological Association of the United Kingdom 31, 4161.CrossRefGoogle Scholar
Millar, R.H. (1971) The biology of ascidians. Advances in Marine Biology 9, 1100.CrossRefGoogle Scholar
Nagabhushanam, A.K. and Krishnamoorthy, P. (1992) Occurrence and biology of the solitary ascidian Ascidiella aspersa in Tamil Nadu coastal waters. Journal of the Marine Biological Association of India 34, 19.Google Scholar
Natsuike, M., Kanamori, M., Baba, K., Moribe, K., Yamaguchi, A. and Imai, I. (2014) Changes in abundances of Alexandrium tamarense resting cysts after the tsunami caused by Great East Japan Earthquake in Funka Bay, Hokkaido, Japan. Harmful Algae 39, 271279.Google Scholar
Niermann-Kerkenberg, E. and Hoffman, D. K. (1989) Fertilization and normal development in Ascidiella aspersa (Tunicata) studied with Nomarski-optics. Helgoländer Meeresuntersuchungen 43, 245258.Google Scholar
Nishikawa, T., Kajiwara, Y. and Kawamura, K. (1993) Probable introduction of Polyandrocarpa zorritensis (Van Name) to Kitakyushu and Kochi, Japan. Zoological Science 10 (Supplement), 176.Google Scholar
Nishikawa, T., Oohara, I., Saitoh, K., Shigenobu, Y., Hasegawa, N., Kanamori, M., Baba, K., Turon, X. and Bishop, J.D.D. (2014) Molecular and morphological discrimination between an invasive ascidian, Ascidiella aspersa, and its congener A. scabra (Urochordata: Ascidiacea). Zoological Science 31, 180185.Google Scholar
Ohtani, K., Akiba, Y., Ito, E. and Onoda, M. (1971a) Studies on the change of the hydrographic conditions in the Funka Bay IV. Oceanographic conditions of the Funka Bay occupied by the Tsugaru Warm Waters. Bulletin of the Faculty of Fisheries Hokkaido University 22, 221230.Google Scholar
Ohtani, K., Akiba, Y., Yoshida, K. and Ohtuki, T. (1971b) Studies on the change of the hydrographic conditions in the Funka Bay III. Oceanographic conditions of the Funka Bay occupied by the Oyashio water. Bulletin of the Faculty of Fisheries Hokkaido University 22, 129142.Google Scholar
Osman, R.W. and Whitlatch, P.B. (2000) Ecological interactions of invading ascidians within epifaunal communities of southern New England. In Pederson, J. (ed.), Marine bioinvasions: Proceedings of the First National Conference, January 24–27, 1999. Cambridge, MA: Massachusetts Institute of Technology, pp. 164174.Google Scholar
Pyo, J., Lee, T. and Shin, S. (2012) Two newly recorded invasive alien ascidians (Chordata, Tunicata, Ascidiacea) based on morphological and molecular phylogenetic analysis in Korea. Zootaxa 3368, 211228.Google Scholar
R Development Core Team (2013) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at http://www.R-project.org/ Google Scholar
Rius, M., Carmen, M. and Turon, X. (2009) Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea. Biological Invasions 11, 21812194.Google Scholar
Robinson, T.B., Griffiths, C.L. and Kruger, N. (2004) Distribution and status of marine invasive species in and bordering the West Coast National Park. Koedoe 47, 7987.Google Scholar
Shenkar, N. and Loya, Y. (2008) The solitary ascidian Herdmani momus: native (Red Sea) versus non-indigenous (Mediterranean) populations. Biological Invasions 10, 14311439.Google Scholar
Shenkar, N. and Loya, Y. (2009) Non-indigenous ascidians (Chordata: Tunicata) along the Mediterranean coast of Israel. Marine Biodiversity Records 2, 17.Google Scholar
Shenkar, N. and Swalla, B.J. (2011) Global diversity of Ascidiacea. PLoS ONE 6, e20657.Google Scholar
Stachowicz, J.J., Terwin, J.R., Whitlatch, R.B. and Osman, R.W. (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proceedings of the National Academy of Sciences USA 99, 1549715500.CrossRefGoogle ScholarPubMed
Svane, I.B. and Young, C.M. (1989) The ecology and behaviour of ascidian larvae. In Barnes, M. (ed.) Oceanography and marine biology, an annual review 27. Aberdeen: Aberdeen University Press, pp. 4590.Google Scholar
Tatián, M., Schwindt, E., Lagger, C. and Varela, M.M. (2010) Colonization of Patagonian harbours (SW Atlantic) by an invasive sea squirt (Chordata, Ascidiacea). Spixiana 33, 111117.Google Scholar
The Plankton Society of Japan and The Japanese Association of Benthology (2009) Marine aliens introduced by human activities and their impacts on ecosystems and industries. Hadano: Tokai University Press.Google Scholar
Tokioka, T. and Kado, Y. (1972) The occurrence of Molgula manhattensis (De Kay) in brackish water near Hiroshima, Japan. Publications of the Seto Marine Biological Laboratory 21, 2129.Google Scholar
Vicente, C.S. and Sorbe, J.C. (2013) Comparative life-histories, population dynamics and productivity of Schistomysis population (Crustacea, Mysida) in European shelf environments. Journal of Sea Research 81, 1332.CrossRefGoogle Scholar
Whitlatch, R.B. and Bullard, S.G. (2007) Introduction to the Proceedings of the 1st International Invasive Sea Squirt Conference. Journal of Experimental Marine Biology and Ecology 342, 12.Google Scholar
World Sea Temperatures (2015) Saltcoats sea temperature. Available at http://www.seatemperature.org/europe/united-kingdom/saltcoats.htm Google Scholar