Chloroplast symbiosis

Here is a list of published work on animals, mainly sacoglossan opisthobranchs, which have evolved symbiotic relationships with chloroplasts they have removed from plant tissue. The papers cover all aspects of the symbiosis, from morphological changes in the animal to physiological chnages in the plastid. Any additional references are welcome.

See Solar-powered Sea Slugs.

• Brandley, B (1984): Aspects of the ecology and physiology of Elysia cf. furvacauda (Mollusca: Sacoglossa). Bull. Mar. Sci. 34(2), 207-219.
• Clark, KB; 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. J. Moll. Stud. 44, 272-282,Figs1-3.
• Clark, KB; Jensen, KR; Stirts, HM; Fermin, C (1981): Chloroplast symbiosis in a non-elysiid mollusc, Costasiella lilianae Marcus (Hermaeidae: Ascoglossa (=Sacoglossa)): Effects of temperature, light intensity, and starvation on carbon fixation rate. Biol. Bull. 160(1), 43-54.
• Clark, K.B., Jensen, K.R. & Stirts, H.M. (1990) Survey for functional kleptoplasty among west Atlantic Ascoglossa (=Sacoglossa) (Mollusca: Opisthobranchia). The Veliger, 33: 339-345.
• Clark, K.B. 1992. Plant-like animals and animal-like plants: symbiotic coevolution of ascoglossan (=sacoglossan) molluscs, their algal prey, and algal plastids. pp. 515-530 [In] (W. Reisser, ed.) Algae and symbioses: plants, animals, fungi, viruses, interactions explored. Biopress Ltd., Bristol, U.K.
• Graves, DA; Gibson, MA; Bleakney, JS (1979): The digestive diverticula of Alderia modesta and Elysia chlorotica (Opisthobranchia: Sacoglossa). The Veliger 21(4), 415-422. (Figs 1-15)
• Green, B.J., Li, W-Y., Manhart, J.R., Fox, T.C., Summer, E.J., Kennedy, R.A., Pierce, S.K. & Rumpho, M.E. (2000) Mollusc-Algal Chloroplast Endosymbiosis. Photosynthesis, Thylakoid Protein Maintenance, and Chloroplast Gene Expression Continue for Many Months in the Absence of the Algal Nucleus. Plant Physiology, 124: 331-342.
• Hanten, J.J. and S.K. Pierce. (2001) Synthesis of several light-harvesting complex I polypeptides is blocked by cycloheximide in symbiotic chloroplasts in the sea slug, Elysia chlorotica (Gould): A case for horizontal gene transfer between alga and animal? Biological Bulletin, 201: 33-44.
• Hinde, R; Smith, DC (1974): `Chloroplast symbiosis' and the extent to which it occurs in Sacoglossa (Gastropoda: Mollusca). Biol. J. Linn. Soc. 6(4), 349-356.
• Hinde, R; Smith, DC (1975): The role of photosynthesis in the nutrition of the mollusc Elysia viridis. Biol. J. Linn. Soc. 7, 161-171.
• Ireland, C; Scheuer, PJ (1979): Photosynthetic marine mollusks: In vivo Carbon 14 incorporation into metabolites of the sacoglossan Placobranchus ocellatus. Science 205(4409), 922-923.
• Jensen, KR (1985): Annotated checklist of Hong Kong Ascoglossa (Mollusca: Opisthobranchia), with descriptions of four new species. In: Proceedings of the 2nd International Workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong, 1983. (Eds: Morton,B; Dudgeon,D) Hong Kong University Press, Hong Kong, 77-107.
• Kawaguti, S; Yamasu, T (1965): Electron microscopy on the symbiosis between an elysioid gastropod and chloroplasts of a green alga. Biol. J. Okayama Univ. 11(3-4), 57-65.
• Marin, A; Ros, JD (1988): The Sacoglossa (Mollusca, Opisthobranchia) of the South East Iberian peninsula. A Catalogue of species and presence of algal chloroplasts in them. Iberus 8(1), 25-49.
• Marin, A; Ros, JD (1992): Dynamics of a peculiar plant-herbivore relationship: the photosynthetic ascoglossan Elysia timida and the chlorophycean Acetabularia acetabulum. Marine Biology 112, 677-682,Figs1-10.
• Monselise, EB; Rahat, M (1980): Photobiology of Elysia timida (Mollusca: Opisthobranchia): observations in the sea. Isr. J. Zool. 29(1-3), 125-128.
• Mujer CV, Andrews DL, Manhart JR, Pierce SK, Rumpho ME (1996) Chloroplast genes are expressed during intracellular symbiotic association of Vaucheria litorea plastids with the sea slug Elysia chlorotica. Proc Natl Acad Sci U S A, 93(22):12333-8
• Pierce S, Biron R, Rumpho M. (1996) Endosymbiotic chloroplasts in molluscan cells contain proteins synthesized after plastid capture. J Exp Biol, 199(10):2323-30
• Pierce, S. K., Maugel, T. K., Rumpho, M. E., Hanten, J. J., Mondy, W. L. (1999). Annual viral expression in a sea slug population: Life cycle control and symbiotic chloroplast maintenance. Biological Bulletin, 196: 197: 1-6.
• Pierce, S.K., Massey, S.E., Hanten, J.J. &. Curtis, N.E. (2003). Horizontal Transfer of Functional Nuclear Genes Between Multicellular Organisms. Biological Bulletin, 204: 237-240.
• Rahat, M; Ben-Izhak Monselise, E (1979): Photobiology of the chloroplast hosting mollusc Elysia timida (Opisthobranchia). J. Exp. Biol. 79, 225-233.
• Roller, RA; Bianchi, TS (1995): HPLC analysis of chloroplast pigments from the marine ascoglossan Tridachia crispata (Morch, 1863) (Mollusca: Opisthobranchia). American Malacological Bulletin 11(2), 139-143.
• Ros, J; Rodriguez, J (1985): La simbiosis algal en Elysia timida Risso 1818. Primeros resultados. Anales de Biologia 4(Biologia Ambiental, 1), 37-47.
• Ros, J (1978): Distribucion en l'espai i en el temps dels opistobranquis Iberics, amb especial referencia als del litoral Catal…. Butllet¡ de la Institucio Catalana d'Historia Natural 42(Sec. Zool., 2), 23-32.
• Rumpho, M.E., Summer, E.J. & Manhart, J.R. (2000)
Solar-Powered Sea Slugs. Mollusc/Algal Chloroplast Symbiosis. Plant Physiology, 123: 29-38.
• Taylor, DL (1967): The occurrence and significance of endosymbiotic chloroplasts in the digestive glands of herbivorous opisthobranchs. Journal of Phycology, 3, 234-235.
• Taylor, DL (1971): Symbiosis between the chloroplasts of Griffithsia flosculosa and Hermaea bifida. Publicaziones della Stazione Zoologia Napoli 39, 116-120.
• Trench, ME; Trench, RK; Muscatine, L (1970): Utilization of photosynthetic products of symbiotic chloroplasts in mucus synthesis by Placobranchus ianthobapsus (Gould), Opisthobranchia, Sacoglossa. Comp. Biochem. Physiol. 37, 113-117.
• Trench, RK; Smith, DC (1970): Synthesis of pigment in symbiotic chloroplasts. Nature 227, 196-197.
• Trench, RK; Boyle, JE; Smith, DC (1973): The association between chloroplasts of Codium fragile and the mollusc Elysia viridis. I. Characteristics of isolated Codium chloroplasts. Proceedings of the Royal Society, London B, 184, 51-61.
• Trench, RK; Boyle, JE; Smith, DC (1973): The association between chloroplasts of Codium fragile and the mollusc Elysia viridis. II. Chloroplast ultrastructure and photosynthetic carbon fixation in E. viridis. Proceedings of the Royal Society, London B, 184, 63-81.
• Trench, RK; Boyle, JE; Smith, DC (1974): The association between chloroplasts of Codium fragile and the mollusc Elysia viridis. III. Movement of photosynthetically fixed Carbon 14 in tissues of intact living E. viridis and in Tridachia crispata. Proceedings of the Royal Society, London B, 185, 453-464.
• Waugh, GR; Clark, KB (1986): Seasonal and geographic variation in chlorophyll level of Elysia tuca (Ascoglossa: Opisthobranchia). Marine Biology 92, 483-487.
• Weaver, S; Clark, KB (1981): Light intensity and color preferences of five ascoglossan (=sacoglossan) Molluscs (Gastropoda: Opisthobranchia): a comparision of chloroplast-symbiotic and aposymbiotic species. Marine Behaviour and Physiology, 7, 297-306.
• Williams, S.I. & Walker, D.I. (1999) Mesoherbivore-macroalgal interactions: Feeding ecology of sacoglossan sea slugs (Mollusca, Opisthobranchia) and their effects on their food algae. Oceanography and Marine Biology Annual Review, 37: 87-128.
• Yonge, CM; Nicholas, HM (1940): Structure and function of the gut and symbiosis with zooxanthellae in Tridachia crispata (Oerst.) Bgh. Papers from Tortugas Laboratory 32(14 September), 289-301.

Authorship details
Rudman, W.B., 1998 (October 11) Chloroplast symbiosis . [In] Sea Slug Forum. Australian Museum, Sydney. Available from

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