Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-24T04:53:30.268Z Has data issue: false hasContentIssue false
  • English
  • Français

Interaction webs of marine specialist herbivores on Japanese shores

Published online by Cambridge University Press:  03 March 2009

Cynthia D. Trowbridge ,
Yayoi M. Hirano  and
Yoshiaki J. Hirano
Cynthia D. Trowbridge*
Affiliation:
Department of Zoology, Oregon State University, PO Box 1995, Newport, OR 97365, USA
Yayoi M. Hirano
Affiliation:
Marine Biosystems Research Center, Chiba University, Uchiura 1, Kamogawa, 299-5502, Japan
Yoshiaki J. Hirano
Affiliation:
Marine Biosystems Research Center, Chiba University, Uchiura 1, Kamogawa, 299-5502, Japan Graduate School of Science, Chiba University, Yayoi-cho, Inage-ku, Chiba, 263-8522, Japan
*
Correspondence should be addressed to: C.D. Trowbridge, Department of Zoology, Oregon State University, PO Box 1995, Newport, OR 97365, USA email: sacoglossans@ymail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Marine specialist herbivores inhabiting Japanese rocky shores are significantly more diverse than in other biogeographical regions at comparable latitudes. The interaction webs of specialist sacoglossans were investigated on the Pacific shore of Honshu, Japan. The host use of the small stenophagous sacoglossan opisthobranch Placida sp. (sensu Baba, 1986) was investigated in association with the green macroalgae Codium spp. Based on field associations, Placida sp. attacked six congeneric algal host species out of eight investigated (75%) in and around Sagami Bay and ten of 20 species (50%) in Japan. In pairwise-choice feeding experiments, Placida sp. preferred the algal host from which it was collected (source alga) to alternate host and non-host algae. Preference rankings, however, could be altered based on the condition or identity of the choices (e.g. old versus young fronds of C. fragile). Connectance values were lower in these high-diversity assemblages than in their low-diversity counterparts on other temperate shores (but these values may increase with additional study). The sacoglossan occasionally coexisted with two other common sacoglossan species (Elysia trisinuata and E. setoensis) and several other less common ones. However, interspecific feeding interactions appeared minor, with no discernible evidence of interference or exploitation competition. Despite the diverse assemblage of specialist sacoglossans feeding on Codium spp., these Japanese sacoglossans (1) had low niche differentiation, (2) were weak interactors with their hosts, and (3) had negligible intra-guild interactions.

Keywords

interaction webJapansacoglossanCodiumPlacidaElysia
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 89 , Issue 2 , March 2009 , pp. 277 - 286
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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

Adrianov, A.V. and Kussakin, O.G. (1998) A check-list of biota of the Peter the Great Bay, the Sea of Japan. Vladivostock, Dalnauka: Russian Academy of Sciences, Far East Branch, Institute of Marine Biology.Google Scholar
Baba, K. (1959) The family Stiligeridae from Japan (Opisthobranchia–Sacoglossa). Publications of the Seto Marine Biological Laboratory 7, 327–334.CrossRefGoogle Scholar
Baba, K. (1986) Anatomical information on Placida sp. =  Hermaea dendritica of Baba, 1937 and 1955, from Japan. Shells and Sea Life 18, 21–22.Google 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, 87–90.CrossRefGoogle Scholar
Bleakney, J.S. (1989) Morphological variation in the radula of Placida dendritica (Alder & Hancock, 1843) (Opisthobranchia: Ascoglossa/Sacoglossa) from Atlantic and Pacific populations. Veliger 32, 171–181.Google Scholar
Brodie, J., Maggs, C.A. and John, D.M. (2007) Green seaweeds of Britain and Ireland. London: British Phycological Society.Google Scholar
Chang, J.-S., Dai, C.-F. and Chang, J. (2002) A taxonomic and karyological study of the Codium geppiorum complex (Chlorophyta) in southern Taiwan, including the description of Codium nanwanense sp. nov. Botanical Bulletin of Academia Sinica 43, 161–170.Google Scholar
Clark, K.B. (1975) Nudibranch life cycles in the Northwest Atlantic and their relationship to the ecology of fouling communities. Helgoländer Wissenschaftliche Meeresuntersungen 27, 28–69.CrossRefGoogle Scholar
Clark, K.B. (1994) Ascoglossan (=Sacoglossa) molluscs in the Florida Keys: rare marine invertebrates at special risk. Bulletin of Marine Science 54, 900–916.Google Scholar
Dyer, L.A., Singer, M.S., Lill, J.T., Stireman, J.O., Gentry, G.L., Marquis, R.J., Ricklefs, R.E., Greeney, H.F., Wagner, D.L. Morais, H.C., Diniz, I.R., Kursar, T.A. and Coley, P.G. (2007) Host specificity of Lepidoptera in tropical and temperate forests. Nature 448, 696–699.CrossRefGoogle ScholarPubMed
Hirano, Y.J., Hirano, Y.M. and Trowbridge, C.D. (2006a) Cryptic species of a common Japanese sacoglossan, “Midoriamamo-umiushi”. Venus 65, 272–273. [In Japanese.]Google Scholar
Hirano, Y.J., Hirano, Y.M. and Trowbridge, C.D. (2006b) Placida sp. (sensu Baba, 1986) and its cryptic species. Umiushi-Tsushin 51, 10–12. [In Japanese.]Google Scholar
Jensen, K.R. (1989) Learning as a factor in diet selection by Elysia viridis (Montagu) (Opisthobranchia). Journal of Molluscan Studies 55, 79–88.CrossRefGoogle Scholar
Jensen, K.R. (1993a) Evolution of buccal apparatus and diet radiation in the Sacoglossa (Opisthobranchia). Bollettino Malacologico 29, 147–172.Google Scholar
Jensen, K.R. (1993b) Morphological adaptations and plasticity of radular teeth of the Sacoglossa (=Ascoglossa) (Mollusca: Opisthobranchia) in relation to their food plants. Biological Journal of the Linnean Society 48, 135–155.CrossRefGoogle Scholar
Jensen, K.R. (1993c) Sacoglossa (Mollusca: Opisthobranchia)–specialist herbivores and partial predators: integrating ecological, physiological and morphological data. In Morton, B. (ed.) The marine biology of the South China Sea. Proceedings of the First International Conference on the Marine Biology of Hong Kong and the South China Sea, Hong Kong, 28 October–3 November 1990. Hong Kong: Hong Kong University Press, pp. 437–458.Google Scholar
Jensen, K.R. (1994) Behavioural adaptations and diet specificity of sacoglossan opisthobranchs. Ethology Ecology and Evolution 6, 87–101.CrossRefGoogle Scholar
Jensen, K.R. (1999) Aggregative behaviour in the sacoglossan opisthobranch Stiliger aureomarginatus Jensen, 1993 in Rottnest Island, Western Australia. In Walker, D.I. and Wells, F.E. (eds) The seagrass flora and fauna of Rottnest Island: Proceedings of the Ninth International Marine Biological Workshop, Rottnest Island, Western Australia, January 1996. Perth: Western Australian Museum, pp. 275–280.Google Scholar
Macnae, W. (1954) On four sacoglossan molluscs new to South Africa. Annals of the Natal Museum 13, 51–64.Google Scholar
MMBS website (2007) Available at http://www.mmbs.s.u-tokyo.ac.jp/overview/overview-e.htmlGoogle Scholar
Nakano, R. (2004) Opisthobranchs of Japan Islands. Tokyo: Rutles, Inc.Google Scholar
Novotny, V., Basset, Y., Miller, S.E., Drozd, P. and Cizek, L. (2002) Host specialization of leaf-chewing insects in a New Guinea rainforest. Journal of Animal Ecology 71, 400–412.CrossRefGoogle Scholar
Olesen, J.M. and Jordano, P. (2002) Geographic patterns in plant-pollinator mutualistic networks. Ecology 83, 2416–2424.Google Scholar
Ono, A. (1999) Opisthobranchs of Kerama Islands. Tokyo: TBS–Britannica Co., Ltd.Google Scholar
Ono, A. (2004) Opisthobranchs of Ryukyu Islands. Tokyo: Rutles, Inc.Google Scholar
Poore, A.G., Hill, N.A. and Sotka, E.E. (2007) Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidea. Evolution 62, 21–38. DOI 10.1111/j.1558-5646.2007.00261.xGoogle Scholar
Provan, J., Booth, D., Todd, N.P., Beatty, G.E. and Maggs, C.A. (2007) Tracking biological invasions in space and time: elucidating the true invasive history of the green alga Codium fragile using old DNA. Diversity and Distributions, DOI 10.1111/j.1472-4642.2007.00420.Google Scholar
Shimada, S., Tadano, T. and Tanaka, J. (2007a) Codium tenuifolium (Codiales, Chlorophyta), a new species from Japan. Journal of Japanese Botany 82, 117–125.Google Scholar
Shimada, S., Ebata, H., Horiguchi, T., Kurihara, A. and Tanaka, J. (2007b) Molecular phylogenetic and morphological analyses of prostrate Codium (Chlorophyta) in Japan. Journal of Japanese Botany 82, 190–204.Google Scholar
Shimadu, Y. (2004) Food algae and life history of Placida sp. (sensu Baba, 1986) (Opisthobranchia: Sacoglossa). MSc thesis. Chiba University, Chiba, Japan [In Japanese.]Google Scholar
Shimadu, Y., Hirano, Y.M., Trowbridge, C.D. and Hirano, Y.J. (2006) Food algae and life history variation in Placida sp. (sensu Baba, 1986). In Abstracts of the Second Scientific Congress of East Asian Federation of Ecological Societies, Niigata, Japan, March 2006, p. 168. [In Japanese.]Google Scholar
Stegenga, H., Bolton, J.J. and Anderson, R.J. (1997) Seaweeds of the South African west coast. Contributions from the Bolus Herbarium, No. 18, University of Cape Town, South Africa.Google Scholar
Suzuki, K. (2000) Opisthobranchs of Izu Peninsula. Tokyo: TBS–Britannica Co., Ltd.Google Scholar
Thompson, T.E. (1976) Biology of opisthobranch molluscs, Volume 1. London: The Ray Society.Google Scholar
Trowbridge, C.D. (1991a) Diet specialization limits herbivorous sea slugs’ capacity to switch among food species. Ecology 72, 1880–1888.CrossRefGoogle Scholar
Trowbridge, C.D. (1991b) Group membership facilitates feeding of the herbivorous sea slug Placida dendritica. Ecology 72, 2193–2203.CrossRefGoogle Scholar
Trowbridge, C.D. (1992a) Mesoherbivory: the ascoglossan sea slug Placida dendritica may contribute to the restricted distribution of its algal host. Marine Ecology Progress Series 83, 207–220.CrossRefGoogle Scholar
Trowbridge, C.D. (1992b) Phenology and demography of a marine specialist herbivore: Placida dendritica (Gastropoda: Opisthobranchia) along the central coast of Oregon. Marine Biology 114, 443–452.CrossRefGoogle Scholar
Trowbridge, C.D. (1995) New Zealand opisthobranchs associated with the low intertidal, crustose green alga Codium convolutum: ascoglossans “Down Under”. Veliger 38, 116–125.Google Scholar
Trowbridge, C.D. (2002) Northeastern Pacific sacoglossan opisthobranchs: natural history review, bibliography, and prospectus. Veliger 45, 1–24.Google Scholar
Trowbridge, C.D. (2004) Emerging associations on marine rocky shores: specialist herbivores on introduced macroalgae. Journal of Animal Ecology 73, 294–308.CrossRefGoogle Scholar
Trowbridge, C.D. (2006) A global proliferation of non-native marine and brackish macroalgae. In Critchley, A.T., Ohno, M. and Largo, D.B. (eds). World seaweed resources—an authoritative reference system. DVD-ROM, version 1.0. Amsterdam: ETI Bioinformatics.Google Scholar
Trowbridge, C.D. and Todd, C.D. (2001) Host-plant changes of marine specialist herbivores: ascoglossan sea slugs on the introduced Codium fragile. Ecological Monographs 71, 219–243.CrossRefGoogle Scholar
Trowbridge, C.D., Little, C., Stirling, P. and Farnham, W.F. (2008a) 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, 771–782.CrossRefGoogle Scholar
Trowbridge, C.D., Hirano, Y.J. and Hirano, Y.M. (2008b) Sacoglossan opisthobranchs associated with the green macroalgae Codium spp. on Pacific rocky shores of Japan. Venus 66, 175–190.Google Scholar
Trowbridge, C.D., Hirano, Y.J. and Hirano, Y.M. (in press) Sacoglossan opisthobranchs on North-West Pacific shores: Stiliger berghi Baba, 1937 and Elysia sp. on filamentous red algae. Veliger 51.Google Scholar
Walsh, E.J. and Trowbridge, C.D. (2001) Genetic variation in oligophagous herbivores (Sacoglossa: Opisthobranchia) on native and introduced hosts. World Congress of Malacology, Vienna (Austria), 19–25 August 2001. (Abstract).Google Scholar
Vázquez, D.P. and Stevens, R.D. (2004) The latitudinal gradient in niche breadth: concepts and evidence. American Naturalist 164, E1–E19.CrossRefGoogle ScholarPubMed
Yoshida, T. (1998) Marine algae of Japan. Tokyo: Uchida Rokakuho Publishing Co., Ltd.Google Scholar
Yoshida, T., Shimada, S., Yoshinaga, K. and Nakajima, Y. (2005) Checklist of marine algae of Japan (revised in 2005). Japanese Journal of Phycology 53, 179–228.Google Scholar
Zar, J.H. (1984) Biostatistical analysis, 2nd edition. Englewood Cliffs, NJ: Prentice-Hall, Inc.Google Scholar