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North-west Pacific sacoglossan guild associated with filamentous green algae (Family Cladophoraceae and Family Boodleaceae)

Published online by Cambridge University Press:  13 September 2011

Cynthia D. Trowbridge*
Affiliation:
Oregon Institute of Marine Biology, Charleston, Oregon, USA
Yayoi M. Hirano
Affiliation:
Marine Biosystems Research Center, Chiba University, Japan Department of Biology, Graduate School of Science, Chiba University, Japan
Yoshiaki J. Hirano
Affiliation:
Marine Biosystems Research Center, Chiba University, Japan Department of Biology, Graduate School of Science, Chiba University, Japan
Kazuki Nishida
Affiliation:
Department of Biology, Faculty of Science, Chiba University, Japan
Kosuke Sudo
Affiliation:
Department of Biology, Graduate School of Science and Technology, Chiba University, Japan
*
Correspondence should be addressed to: C.D. Trowbridge, Oregon Institute of Marine Biology, Mail: PO Box 1995, Newport, OR 97365, USA email: [email protected]
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Abstract

On temperate and tropical shores around the world, a guild of sacoglossan opisthobranchs associates with filamentous green algae. This guild of four genera in three different families (Hermaeidae: Aplysiopsis; Limapontiidae: Ercolania, Limapontia; Plakobranchidae: Elysia) has been well studied in many geographical regions. Despite detailed information for Hong Kong, there is comparatively little information for Japanese shores. From 2000 to 2010, this guild of sacoglossans was investigated in two regions of Japan. On the Pacific shores of Honshu, Japan, at least ten species occupy this guild including Aplysiopsis minor, A. toyamana, A. nigra, A. orientalis, Ercolania boodleae, E. subviridis, Elysia hamatanii and E. abei. Two described species (Elysia nigrocapitata and E. hirasei) were not recorded but also occupy this temperate guild in Japan. On the west-coast shores of Okinawa (East China Sea), at least three species occur in this guild: Ercolania subviridis and two undescribed or unrecognized species of Ercolania. We quantified the size–frequency and abundance of specimens, characterized their spawn masses, and conducted feeding preference experiments. Many of the sacoglossans were seasonally frequent to abundant, their feeding activities were concentrated on uniseriate filaments of green algae (Order Cladophorales: Family Cladophoraceae and/or Order Siphonocladales: Family Boodleaceae), and their larvae were typically planktotrophic; yet, many of these species are regional endemics. Our results complement the wealth of ecological information available for other, more depauperate geographical regions.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

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References

REFERENCES

Baba, K. (1938) Opisthobranchia of Kii, Middle Japan. Journal of the Department of Agriculture, Kyushu Imperial University 6, 119.CrossRefGoogle Scholar
Baba, K. (1947) Illustrated encyclopedia of the fauna of Japan, exclusive of insects. Tokyo: Hokuryukan Co.Google Scholar
Baba, K. (1949) Opisthobranchia of Sagami Bay collected by His Majesty the Emperor of Japan. Tokyo: Iwanami Shoten.Google Scholar
Baba, K. (1955) Opisthobranchia of Sagami Bay. Supplement. Tokyo: Iwanami Shoten.Google Scholar
Baba, K. (1957) The species of the genus Elysia from Japan. Publications of the Seto Marine Biological Laboratory 6, 6974.CrossRefGoogle Scholar
Baba, K. (1959) The family Stiligeridae from Japan (Opisthobranchia–Sacoglossa). Publications of the Seto Marine Biological Laboratory 7, 327334.CrossRefGoogle Scholar
Baba, K. and Hamatani, I. (1952) Observations on the spawning habits of some of the Japanese Opisthobranchia (1). Publications of the Seto Marine Biological Laboratory 2, 8790.CrossRefGoogle Scholar
Baba, K. and Hamatani, I. (1970) The anatomy of Ercolania boodleae (Baba, 1938) from Seto, Kii, Middle Japan (Opisthobranchia: Sacoglossa). Publications of the Seto Marine Biological Laboratory 18, 215222.CrossRefGoogle Scholar
Baumgartner, F.A., Motti, C.A., de Nys, R. and Paul, N.A. (2009) Feeding preferences and host associations of specialist marine herbivores align with quantitative variation in seaweed secondary metabolites. Marine Ecology Progress Series 396, 112.CrossRefGoogle Scholar
Behrens, D.W. (1991) Pacific coast nudibranchs, a guide to the opisthobranchs Alaska to Baja California. 2nd edition. Monterey, CA: Sea Challengers.Google Scholar
Burn, R. (1974) Notes on some benthonic opisthobranchs from Port Phillip Bay, Victoria. Journal of the Malacological Society of Australia 3, 4357.CrossRefGoogle Scholar
Burn, R. (2006) A checklist and bibliography of the Opisthobranchia (Mollusca: Gastropoda) of Victoria and the Bass Strait area, south-eastern Australia. Museum Victoria Science Reports 10, 142.CrossRefGoogle Scholar
Carlson, C. and Hoff, P.J. (2003) The opisthobranchs of the Mariana Islands. Micronesica 35–36, 272295.Google Scholar
Chia, F.S. (1971) Oviposition, fecundity, and larval development of three sacoglossan opisthobranchs from the Northumberland coast, England. Veliger 13, 319325.Google Scholar
Clark, K.B. (1975) Nudibranch life cycles in the northwest Atlantic and their relationship to the ecology of fouling communities. Helgoländer Wissenschaftliche Meeresuntersuchungen 27, 2869.CrossRefGoogle Scholar
Clark, K.B. (1982) A new Aplysiopsis (Opisthobranchia: Hermaeidae) from central Florida, with a brief summary of the ceratiform families of the order Ascoglossa (= Sacoglossa). Bulletin of Marine Science 32, 213219.Google Scholar
Cockerell, T.D.A. and Eliot, C. (1905) Notes on a collection of Californian nudibranchs. Journal of Malacology 12, 3153.Google Scholar
Eliot, C. (1903) Nudibranchiata, with some remarks on the families and genera and description of a new genus, Doridomorpha. In Gardiner, J.S. (ed.) The fauna and geography of the Maldive and Laccadive Archipelagoes 2. Cambridge: Cambridge University Press, pp. 540573.Google Scholar
Eliot, C. (1904) On some nudibranchs from East Africa and Zanzibar. Part VI. Proceedings of the Zoological Society of London 1904, 268298.CrossRefGoogle Scholar
Eliot, C. (1916) Mollusca Nudibranchiata, fauna of the Chilka Lake. Memoirs of the Indian Museum 5, 375380.Google Scholar
Eliot, C. (1917) Zoological results of a tour in the Far East. Mollusca Nudibranchiata (Ascoglossa). Memoirs of the Asiatic Society of Bengal 6, 179182.Google Scholar
Eliot, C.N.E. (1907) Nudibranchs from New Zealand and the Falkland Islands. Proceedings of the Malacological Society of London 7, 327360.Google Scholar
Ferreira, A.J. and Bertsch, H. (1975) Anatomical and distributional observations of some opisthobranchs from the Panamic faunal province. Veliger 17, 323330.Google Scholar
Gascoigne, T. (1978) The internal anatomy of Stiliger fuscatus (A. Gould, 1870) (Opisthobranchia: Sacoglossa). Zoological Journal of the Linnean Society 63, 265274.CrossRefGoogle Scholar
Gonor, J.J. (1961) Observations on the biology of Hermaeina smithi, a sacoglossan opisthobranch from the west coast of North America. Veliger 4, 8598.Google Scholar
Gosliner, T.M., Behrens, D.W. and Valdés, A. (2008) Indo-Pacific nudibranchs and sea slugs: a field guide to the world's most diverse fauna. Gig Harbor and San Francisco: Sea Challengers and California Academy of Sciences.Google Scholar
Hamatani, I. (1960) Notes on veligers of Japanese opisthobranchs (1). Publications of the Seto Marine Biological Laboratory 8, 5970.CrossRefGoogle Scholar
Hamatani, I. (2000) Sacoglossa. In Okutani, T. (ed.) Marine mollusks in Japan. Tokyo: Tokai University Press, pp. 760765.Google Scholar
Hirano, Y.J. (1991) Opisthobranch molluscs from Kominato, Boso Peninsula. (1) Hermaeidae (Ascoglossa). Annual Report of the Marine Ecosystems Research Center 11, 57.Google Scholar
Hirano, Y.J. and Hirano, Y.M. (1991) Food preference of five species of Hermaeidae (Opisthobranchia: Ascoglossa) from Kominato, Boso Peninsula (preliminary report). Annual Report of the Marine Ecosystems Research Center 11, 912.Google Scholar
Hirano, Y.M., Trowbridge, C.D. and Hirano, Y.J. (2007) Unrecognized diversity of the genus Ercolania (Mollusca, Gastropoda, Sacoglossa) on Japanese shores. 43rd Annual Meeting of the Japanese Society of Systematic Zoology, Kitakyushu, Kyushu, 9–10 June 2007.Google Scholar
Hirasé, S. (1927) Figuraro de Japanaj Bestoj, Moluskoj de Hirasé S. et al. Tokyo: Hokuryukwan & Co. Ltd.Google Scholar
Hutton, F.W. (1882a) Notes on some branchiate Gastropoda. Transactions and Proceedings of the New Zealand Institute 15, 118131.Google Scholar
Hutton, F.W. (1882b) Additions to the molluscan fauna of New Zealand. Transactions and Proceedings of the New Zealand Institute 15, 131133.Google Scholar
Jensen, K. (1975) Food preference and food consumption in relation to growth of Limapontia capitata (Opisthobranchia, Sacoglossa). Ophelia 14, 114.CrossRefGoogle Scholar
Jensen, K. (1976) The importance of Limapontia capitata (Mueller) (Opisthobranchia, Sacoglossa) as a primary consumer in the Cladophora-belt. Tenth European Symposium on Marine Biology 2, 339350.Google Scholar
Jensen, K.R. (1983) Factors affecting feeding selectivity in herbivorous Ascoglossa (Mollusca: Opisthobranchia). Journal of Experimental Marine Biology and Ecology 66, 135148.CrossRefGoogle Scholar
Jensen, K.R. (1985) Annotated checklist of Hong Kong Ascoglossa (Mollusca: Opisthobranchia), with descriptions of four new species. In Morton, B. and Dudgeon, D. (eds) Proceedings of the Second International Workshop on the Malacofauna of Hong Kong and Southern China. Hong Kong: Hong Kong University Press, pp. 77107.Google Scholar
Jensen, K.R. (1990) Three new species of Ascoglossa (Mollusca, Opisthobranchia) from Hong Kong, and a description of the internal anatomy of Costasiella pallida Jensen, 1985. In Morton, B. (ed.) Proceedings of the Second International Marine Biological Workshop. The marine flora and fauna of Hong Kong and southern China, Hong Kong, 2–24 April 1986. Hong Kong: Hong Kong University Press, pp. 419432.Google Scholar
Jensen, K.R. (1993) Sacoglossa (Mollusca, Opisthobranchia) from Rottnest Island and central Western Australia. In Wells, F.E., Walker, D.I., Kirkman, H. and Lethbridge, R. (eds) Proceedings of the Fifth International Marine Biological Workshop. The marine flora and fauna of Rottnest Island, Western Australia. Perth: Western Australian Museum, pp. 207253.Google Scholar
Jensen, K.R. (1995) Anatomy and biology of Aplysiopsis formosa Pruvot-Fol (Mollusca, Opisthobranchia, Sacoglossa) from the Azores. Açoreana, Supplement, 217230.Google Scholar
Jensen, K.R. (1997) Sacoglossa (Mollusca, Opisthobranchia) from the Darwin Harbour area, Northern Territory, Australia. In Hanley, J.R., Caswell, G., Megírian, D. and Larson, H.K. (eds) Proceedings of the Sixth International Marine Biological Workshop 1993. The marine flora and fauna of Darwin Harbour, Northern Territory, Australia. Darwin: Museums and Art Galleries of the Northern Territory, pp. 163186.Google Scholar
Jensen, K.R. (2001) Review of reproduction in the Sacoglossa (Mollusca, Opisthobranchia). Bollettino Malacologico 37, 8198.Google Scholar
Jensen, K.R. (2003) Distributions, diets and reproduction of Hong Kong Sacoglossa (Mollusca: Opisthobranchia): a summary of data, 1980–2001. In Morton, B. (ed.) Perspectives on marine environmental change in Hong Kong and Southern China, 1977–2001. Hong Kong: Hong Kong University Press, pp. 347365.Google Scholar
Jensen, K.R. (2007) Biogeography of the Sacoglossa (Mollusca, Opisthobranchia). Bonner Zoologische Beiträge 55, 255281.Google Scholar
Jensen, K.R. and Wells, F.E. (1990) Sacoglossa (= Ascoglossa) (Mollusca, Opisthobranchia) from southern Western Australia. In Wells, F.E., Walker, D.I., Kirkman, H. and Lethbridge, R. (eds) Proceedings of the Third International Marine Biological Workshop. The marine flora and fauna of Albany, Western Australia. volume 1. Perth: Western Australian Museum, pp. 297331.Google Scholar
Lemche, H.M. (1935) On some nudibranchiate gastropods from the northern Atlantic. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening 99, 131148. [Note: although whole volume was not published until 1936, reprints were distributed in 1935.]Google Scholar
Linse, K. (1999) Mollusca of the Magellan region. A checklist of the species and their distribution. Scientia Marina 63, Suppl. 1, 399407.CrossRefGoogle Scholar
MacFarland, F.M. (1966) Studies of opisthobranchiate mollusks of the Pacific coast of North America. Memoirs of the California Academy of Sciences 6, 1546.Google Scholar
Macnae, W. (1954) On four sacoglossan molluscs new to South Africa. Annals of the Natal Museum 12, 5164.Google Scholar
Marcus, E. (1958) On western Atlantic opisthobranchiate gastropods. American Museum Novitates 1906, 182.Google Scholar
Marcus, E. (1959) Lamellariacea und Opisthobranchia. Reports of the Lund University Chile Expedition 1948–49, no. 36. Lunds Universitets Årsskrift (Ny Foljd), Avd. 2, 55(9), 1133.Google Scholar
Marcus, E. (1961) Opisthobranch mollusks from California. Veliger 3, Supplement, 184.Google Scholar
Marcus, E. du B.-R. and Marcus, E. (1970) Some gastropods from Madagascar and west Mexico. Malacologia 10, 181223.Google Scholar
Nakano, R. (2004) Opisthobranchs of Japan Islands. Tokyo: Rutles Inc.Google Scholar
Ono, A. (2004) Opisthobranchs of Ryukyu Islands. Tokyo: Rutles Inc.Google Scholar
Ortea, J., Bacallado, J.J. and Sanchez, J.M.P. (1990) Aplysiopsis formosa Pruvot-Fol, 1953 (Mollusca, Opisthobranchia, Ascoglossa) in the Canary Islands. Lavori della Societa Italiana di Malacologia, Napoli 23, 281285.Google Scholar
Ortea, J. and Espinosa, J. (2001) A new species of Ercolania Trinchese, 1872. Avicennia Suplemento 4, 4547. [Original title: Descripción de una nueva especie de Ercolania Trinchese, 1872.]Google Scholar
Pruvot-Fol, A. (1953) Étude de quelques opisthobranches de la côte Atlantique du Maroc et du Sénégal. Travaux de l'Institut Scientifique Chérifien, Zoologie 5, 1105.Google Scholar
Rao, K.V. (1937) Structure, habits and early development of a new species of Stiliger Ehrenberg. Records of the Indian Museum 39, 435464.Google Scholar
Rao, K.V. and Rao, K.P. (1963) Stiliger nigrovittatus sp. nov., a sacoglossan mollusc from the Gulf of Mannar. Journal of the Marine Biological Association of India 5, 232238.Google Scholar
Schmekel, L. and Portmann, A. (1982) Opisthobranchia des Mittelmeeres. Nudibranchia und Sacoglossa. Berlin/New York: Springer-Verlag.CrossRefGoogle Scholar
Sewell, R.B.S. and Annandale, N. (1922) Fauna of Chilka Lake: hydrography and invertebrate fauna of Rhambha Bay in an abnormal year. Stiliger pica Annandale & Prashad, sp. nov. Memoirs of the Indian Museum 5, 700702.Google Scholar
Swennen, C. (1998) [for 1997] Two new gastropods, Elysia bangtawaensis and E. siamensis from southern Thailand (Opisthobranchia, Sacoglossa, Elysiidae). Bulletin Zoölogisch Museum 16, 3338.Google Scholar
Thompson, T.E. (1973) Sacoglossan gastropod molluscs from eastern Australia. Proceedings of the Malacological Society of London 40, 239251.Google Scholar
Thompson, T.E. (1976) Biology of Opisthobranch Molluscs. Volume 1. London: The Ray Society.Google Scholar
Trinchese, S. (1872) Un nuovo genere della famiglia degli Eolididei. Annali del Museo Civico di Storia Naturale di Genova 2, 86132.Google Scholar
Trinchese, S. (1881) Per la fauna marittima italiana. Materiali raccolti ed illustrati dal Socio corrisp. T. Trinchese. Aeolididae e famiglie affini. Atti della Reale Accademia dei Lincei. Memoire della Classe di Scienze Fisiche, Matematiche e Naturali 11, 3142.Google Scholar
Trowbridge, C.D. (1993a) Feeding ecology of the ascoglossan opisthobranch Aplysiopsis enteromorphae (Cockerell & Eliot): patterns of distribution and impact on tidepool-dwelling green algae. Journal of Experimental Marine Biology and Ecology 169, 233257.CrossRefGoogle Scholar
Trowbridge, C.D. (1993b) Population structure of two common species of ascoglossan (= sacoglossan) opisthobranchs on the central coast of Oregon, USA. Veliger 36, 99106.Google Scholar
Trowbridge, C.D. (1994) Life at the edge: population dynamics and salinity tolerance of a high intertidal, pool-dwelling ascoglossan opisthobranch on New Zealand rocky shores. Journal of Experimental Marine Biology and Ecology 182, 6584.CrossRefGoogle Scholar
Trowbridge, C.D. (1995) Hypodermic insemination, oviposition, and embryonic development of a pool-dwelling ascoglossan (= sacoglossan) opisthobranch: Ercolania felina (Hutton, 1882) on New Zealand shores. Veliger 38, 203211.Google Scholar
Trowbridge, C.D. (2000a) (25 September) Elysia cf. nigrocapitata from Sagami Bay. [Message in] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/find/3063Google Scholar
Trowbridge, C.D. (2000b) (5 July) Ercolania from Oregon, USA. [Message in] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/find/2652Google Scholar
Trowbridge, C.D. (2000c) The missing links: larval and post-larval development of the ascoglossan opisthobranch Elysia viridis. Journal of the Marine Biological Association of the United Kingdom 80, 10871094.CrossRefGoogle Scholar
Trowbridge, C.D. (2002) Northeastern Pacific sacoglossan opisthobranchs: natural history review, bibliography, and prospectus. Veliger 45, 124.Google Scholar
Trowbridge, C.D. (2005) (15 April) Unknown Ercolania sp. from Okinawa. [Message in] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/find/13437Google Scholar
Trowbridge, C.D., Hirano, Y.J. and Hirano, Y.M. (2008a) Sacoglossan opisthobranchs associated with the green macroalgae Codium spp. on Pacific rocky shores of Japan. Venus 66, 175190.Google Scholar
Trowbridge, C.D., Little, C., Stirling, P. and Farnham, W.F. (2008b) Sacoglossan gastropods on native and introduced hosts in Lough Hyne, Ireland: larval retention and population asynchrony? Journal of the Marine Biological Association of the United Kingdom 88, 771782.CrossRefGoogle Scholar
Trowbridge, C.D., Hirano, Y.M. and Hirano, Y.J. (2011) Inventory of Japanese sacoglossan opisthobranchs: historical review, current records, and unresolved issues. American Malacological Bulletin 29, 122.CrossRefGoogle Scholar
Trowbridge, C.D., Hirano, Y.M., Hirano, Y.J., Sudo, K., Shimadu, Y., Watanabe, T., Yorifuji, M., Maeda, T., Anetai, Y. and Kumagai, K. (2010) Subtropical sacoglossans in Okinawa—at ‘special risk’ or ‘predictably rare’? American Malacological Bulletin 28, 167181.CrossRefGoogle Scholar
Usuki, I. (1977) Effects of food algae on the nutrition of Ercolania boodleae (Baba), (Opisthobranchia, Gastropoda). Japanese Journal of Ecology 27, 103110.Google Scholar
Usuki, I. and Hayashi, S. (1975) A supplementary list of opisthobranch molluscs occurring in the coasts of Niigata Prefecture, faced on the Japan Sea. Bulletin of the Niigata Prefectural Biological Society for Education 10, 3336.Google Scholar
Valdés, A., Hamann, J., Behrens, D.W. and DuPont, A. (2006) Caribbean sea slugs, a field guide to the opisthobranch mollusks from the tropical northwestern Atlantic. Gig Harbor: Sea Challengers Natural History Books.Google Scholar
Wägele, H., Stemmer, K., Burghardt, I. and Händeler, K. (2010) Two new sacoglossan sea slug species (Opisthobranchia, Gastropoda): Ercolania annelyleorum sp. nov. (Limapontioidea) and Elysia asbecki sp. nov. (Plakobranchoidea), with notes on anatomy, histology and biology. Zootaxa 2676, 128.CrossRefGoogle Scholar
Yoshida, T. (1998) Marine algae of Japan. Tokyo: Uchida Rokakuho Publishing Co. Ltd.Google Scholar