Hostname: page-component-89b8bd64d-z2ts4 Total loading time: 0 Render date: 2026-05-12T03:37:47.177Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of photosynthesis on the survival and weight retention of two kleptoplastic sacoglossan opisthobranchs

Published online by Cambridge University Press:  25 May 2012

Shoko Yamamoto ,
Yayoi M. Hirano ,
Yoshiaki J. Hirano ,
Cynthia D. Trowbridge ,
Ayana Akimoto ,
Atsushi Sakai  and
Yoichi Yusa
Shoko Yamamoto
Affiliation:
Faculty of Science, Nara Women's University, Kitauoya-nishi 630-8506, Japan
Yayoi M. Hirano
Affiliation:
Graduate School of Science, Chiba University, 1-33 Yayoi-cho, Inage, Chiba 263-8522, Japan
Yoshiaki J. Hirano
Affiliation:
Graduate School of Science, Chiba University, 1-33 Yayoi-cho, Inage, Chiba 263-8522, Japan
Cynthia D. Trowbridge
Affiliation:
Oregon Institute of Marine Biology, University of Oregon, Charleston, OR 97420, USA
Ayana Akimoto
Affiliation:
Faculty of Science, Nara Women's University, Kitauoya-nishi 630-8506, Japan
Atsushi Sakai
Affiliation:
Faculty of Science, Nara Women's University, Kitauoya-nishi 630-8506, Japan
Yoichi Yusa*
Affiliation:
Faculty of Science, Nara Women's University, Kitauoya-nishi 630-8506, Japan
*
Correspondence should be addressed to: Y. Yusa, Faculty of Science, Nara Women's University, Kitauoya-nishi 630-8506, Japan email: yusa@cc.nara-wu.ac.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

Many sacoglossan sea slugs utilize chloroplasts ingested from food algae for photosynthesis (functional kleptoplasty), and the extent and duration of kleptoplast retention differs greatly among sacoglossan species. Although most recent studies focus on the genetic, microscopic, or physiological mechanisms responsible for this unique phenomenon, its effects on the life history traits of sacoglossans have not been fully explored. To study the effects of light conditions on survival and weight retention, adult individuals of two sacoglossan species, Elysia trisinuata and Plakobranchus ocellatus (‘black type'), were reared under light conditions (a 14-hour light: 10-hour dark photoperiod with an irradiance level of 28 µmol m−2s−1) or complete darkness for 21 days. There was no significant difference in the survival rate between the light and dark treatments for E. trisinuata, and its wet weight relative to the initial weight was smaller in the light than in the dark. However, both the survival and relative weights were greater in the light than dark for P. ocellatus. Based on the fluorescent yield measurement using pulse-amplitude-modulated fluorometry, the retention duration of functional chloroplasts was longer (>17 days) for P. ocellatus than E. trisinuata (<4 days). These results indicate that P. ocellatus benefits from photosynthesis for survival and growth, whereas E. trisinuata does not under starved conditions. This interspecific difference is likely related to the period of functional chloroplast retention.

Keywords

animalchloroplast symbiosisElysia trisinuatakleptoplastyMolluscaPlakobranchus ocellatussolar-powered sea slug

Information

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 93 , Issue 1 , February 2013 , pp. 209 - 215
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Adachi, A. (1991) Morphological study on sacoglossan opisthobranch Plakobranchus spp. MSc thesis. University of Ryukyus, Nishihara, Okinawa, Japan. [In Japanese].Google Scholar
Barneah, O., Brickner, I., Hooge, M., Weis, V.M., LaJeunesse, T.C. and Benayahu, Y. (2007) Three party symbiosis: acoelomorph worms, corals and unicellular algal symbionts in Eilat (Red Sea). Marine Biology 151, 1215–1223.CrossRefGoogle Scholar
Clark, K.B. and Busacca, M. (1978) Feeding specificity and chloroplast retention in four tropical Ascoglossa, with a discussion of the extent of chloroplast symbiosis and the evolution of the order. Journal of Molluscan Studies 44, 272–282.Google Scholar
Clark, K.B., Busacca, M. and Stirts, H. (1979) Nutritional aspects of development of the ascoglossan, Elysia cauze. In Stancyk, S.E. (ed.) Reproductive ecology of marine invertebrates. Columbia, SC: University of South Carolina Press, pp. 11–24.Google Scholar
Clark, K.B. and DeFreese, D. (1987) Population ecology of Caribbean Ascoglossa (Mollusca: Opisthobranchia): a study of specialized algal herbivores. American Malacological Bulletin 5, 259–280.Google Scholar
Clark, K.B., Jensen, K.R. and Stirts, H.M. (1990) Survey for functional kleptoplasty among West Atlantic Ascoglossa (= Sacoglossa) (Mollusca: Opisthobranchia). Veliger 33, 339–345.Google Scholar
Dunlap, M.F.S. (1975) Symbiosis between algal chloroplasts and the mollusk Plakobranchus ocellatus van Hasselt (Sacoglossa: Opisthobranchia). PhD thesis. University of Hawaii, Honolulu, USA.Google Scholar
Evertsen, J. and Johnsen, G. (2009) In vivo and in vitro differences in chloroplast functionality in the two North Atlantic sacoglossans (Gastropoda, Opisthobranchia) Placida dendritica and Elysia viridis. Marine Biology 156, 847–859.CrossRefGoogle Scholar
Evertsen, J., Burghardt, I., Johnsen, G. and Wägele, H. (2007) Retention of functional chloroplasts in some sacoglossans from the Indo-Pacific and Mediterranean. Marine Biology 151, 2159–2166.CrossRefGoogle Scholar
Gallop, A., Bartrop, J. and Smith, D.C. (1980) The biology of chloroplast acquisition by Elysia viridis. Proceedings of the Royal Society of London, B 207, 335–349.Google Scholar
Giménez Casalduero, F. and Muniain, C. (2006) Photosynthetic activity of the solar-powered lagoon mollusc Elysia timida (Risso, 1818) (Opisthobranchia: Sacoglossa). Symbiosis 41, 151–158.Google Scholar
Giménez Casalduero, F. and Muniain, C. (2008) The role of kleptoplasts in the survival rates of Elysia timida (Risso, 1818): (Sacoglossa: Opisthobranchia) during periods of food shortage. Journal of Experimental Marine Biology and Ecology 357, 181–187.CrossRefGoogle Scholar
Händeler, K., Grymbowski, P.Y., Krug, P. and Wägele, H. (2009) Functional chloroplasts in metazoan cells—a unique evolutionary strategy in animal life. Frontiers in Zoology 6, 1–18.CrossRefGoogle ScholarPubMed
Hoegh-Guldberg, O., Hinde, R. and Muscatine, L. (1986) Studies on a nudibranch that contains zooxanthellae II. Contribution of zooxanthellae to animal respiration (CZAR) in Pteraeolidia ianthina with high and low densities of zooxanthellae. Proceedings of the Royal Society of London, B 228, 511–521.Google Scholar
Hinde, R. and Smith, D.C. (1972) Persistence of functional chloroplasts in Elysia viridis (Opisthobranchia, Sacoglossa). Nature New Biology 239, 30–31.CrossRefGoogle ScholarPubMed
Hinde, R. and Smith, D.C. (1975) The role of photosynthesis in the nutrition of the mollusc Elysia viridis. Biological Journal of the Linnean Society 7, 161–171.CrossRefGoogle Scholar
Jesus, B., Ventura, P. and Calado, G. (2010) Behaviour and a functional xanthophyll cycle enhance photo-regulation mechanisms in the solar-powered sea slug Elysia timida (Risso, 1818). Journal of Experimental Marine Biology and Ecology 395, 98–105.CrossRefGoogle Scholar
Kawaguti, S. and Yamasu, T. (1965) Electron microscopy on the symbiosis between an elysioid gastropod and chloroplasts of a green alga. Biological Journal of Okayama University 11, 57–65.Google Scholar
Klochkova, T.A., Han, J.W., Kim, J.H., Kim, K.Y. and Kim, G.H. (2010) Feeding specificity and photosynthetic activity of Korean sacoglossan mollusks. Algae 25, 217–227.CrossRefGoogle Scholar
Little, A.F., van Oppen, M.J.H. and Willis, B.L. (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304, 1492–1494.CrossRefGoogle ScholarPubMed
Maeda, T., Kajita, T., Maruyama, T. and Hirano, Y. (2010) Molecular phylogeny of the Sacoglossa, with a discussion of gain and loss of kleptoplasty in the evolution of the group. Biological Bulletin. Marine Biological Laboratory, Woods Hole 219, 17–26.CrossRefGoogle ScholarPubMed
Marin, A. and Ros, J. (1993) Ultrastructural and ecological aspects of the development of chloroplast retention in the sacoglossan gastropod Elysia timida. Journal of Molluscan Studies 59, 95–104.CrossRefGoogle Scholar
Pelletreau, K.N., Bhattacharya, D., Price, D.C., Worful, J.M., Moustafa, A. and Rumpho, M.E. (2011) Sea slug kleptoplasty and plastid maintenance in a metazoan. Plant Physiology 155, 1561–1565.CrossRefGoogle Scholar
Rumpho, M.E., Pelletreau, K.N., Moustafa, A. and Bhattacharya, D. (2011) The making of a photosynthetic animal. Journal of Experimental Biology 214, 303–311.CrossRefGoogle ScholarPubMed
Rumpho, M.E., Worful, J.M., Lee, J., Kannan, K., Tyler, M.S., Bhattacharya, D., Moustafa, A. and Manhart, J.R. (2008) Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proceedings of the National Academy of Sciences of the United States of America 105, 17867–17871.CrossRefGoogle Scholar
Schwartz, J.A., Curtis, N.E. and Pierce, S.K. (2010) Using algal transcriptome sequences to identify transferred genes in the sea slug, Elysia chlorotica. Evolutionary Biology 37, 29–37.CrossRefGoogle Scholar
Serôdio, J., Silva, R., Ezequiel, J. and Calado, R. (2011) Photobiology of the symbiotic acoel flatworm Symsagittifera roscoffensis: algal symbiont photoacclimation and host photobehaviour. Journal of the Marine Biological Association of the United Kingdom 91, 167–171.CrossRefGoogle Scholar
Trowbridge, C.D. (1991) Diet specialization limits herbivorous sea slug's capacity to switch among food species. Ecology 72, 1880–1888.CrossRefGoogle Scholar
Trowbridge, C.D. (2000) 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, 1087–1094.CrossRefGoogle Scholar
Trowbridge, C.D., Hirano, Y.J. and Hirano, Y.M. (2008) Sacoglossan opisthobranchs associated with the green macroalgae Codium spp. on Pacific rocky shores of Japan. Venus 66, 175–190.Google Scholar
Venn, A.A., Loram, J.E. and Douglas, A.E. (2008) Photosynthetic symbioses in animals. Journal of Experimental Botany 59, 1069–1080.CrossRefGoogle ScholarPubMed
Vieira, S., Calado, R., Coelho, H. and Serôdio, J. (2009) Effects of light exposure on the retention of kleptoplastic photosynthetic activity in the sacoglossan mollusc Elysia viridis. Marine Biology 156, 1007–1020.CrossRefGoogle Scholar
Wägele, H. and Johnsen, G. (2001) Observations on the histology and photosynthetic performance of ‘solar-powered’ opisthobranchs (Mollusca, Gastropoda, Opisthobranchia) containing symbiotic chloroplasts or zooxanthellae. Organisms Diversity and Evolution 1, 193–210.CrossRefGoogle Scholar
Wägele, H., Deusch, O., Händeler, K., Martin, R., Schmitt, V., Christa, G., Pinzger, B., Gould, S.B., Dagan, T., Klussmann-Kolb, A. and Martin, W. (2011) Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Molecular Biology and Evolution 28, 699–706.CrossRefGoogle Scholar
Warner, M.E., Fitt, W.K. and Schmidt, G.W. (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proceedings of the National Academy of Sciences of the United States of America 96, 8007–8012.CrossRefGoogle ScholarPubMed
Waugh, G.R. and Clark, K.B. (1986) Seasonal and geographic variation in chlorophyll level of Elysia tuca (Ascoglossa: Opisthobranchia). Marine Biology 92, 483–487.CrossRefGoogle Scholar
Williams, S.I. (2000) Plant-animals: a study of sacoglossan sea slugs. PhD thesis. University of Western Australia, Perth, Australia.Google Scholar
Yamamoto, Y.Y., Yusa, Y., Yamamoto, S., Hirano, Y., Hirano, Y., Motomura, T., Tanemura, T. and Obokata, J. (2009) Identification of photosynthetic sacoglossans from Japan. Endocytobiosis and Cell Research 19, 112–119.Google Scholar