Abstract
Exposure of the temperate sea anemone Anemonia viridis Forskål to increased seawater temperature (from 16 to 26°C) reduced the lysosomal latency of coelenterate tissues. Lysosomes in the mesenterial filaments of anemones were destabilised by increased temperature, with greater destabilisation in heat-shocked symbiotic anemones than in heat-shocked aposymbiotic anemones in the early stages of the experiment. Lysosomal enzyme activity in zooxanthellae from heat-shocked symbiotic anemones was associated with the algal membranes and the cytoplasm of degenerate algal cells. While the relationship between host coelenterate and symbiotic alga may confer many benefits under “normal” conditions, comparison of the responses of symbiotic and aposymbiotic anemones to heat shock suggests that there may be disadvantages for symbiotic anemones under stress.
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Literature cited
Brown, B. E., Suharsono (1990). Damage and recovery of coral reefs affected by El Niño related seawater warming in the Thousand Islands, Indonesia. Coral Reefs 8: 163–170
Coles, S. L., Jokiel, P. L. (1977). Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar. Biol. 43: 209–216
Douglas, A. E., Smith, D. C. (1989). Are endosymbioses mutualistic? Trends Ecol. Evol. 4: 23–26
Fankboner, P. V. (1971). Intracellular digestion of symbiotic zooxanthellae by host amoebocytes in giant clams (Bivalvia: Tridacnidae) with a note on the nutritional role of the hypertrophied siphonal epidermis. Biol. Bull. mar. biol. Lab., Woods Hole 141: 222–234
Fisk, D. A., Done, T. J. (1985). Taxonomic and bathymetric patterns of bleaching corals, Myrmidon Reef, Queensland. Proc. 5th int. coral Reef Congr. 6: 149–154. [Gabrie, C., Toffart, J. L., Salvat, B. (eds.) Antenne Museum-EPHE, Moorea, French Polynesia]
Fitt, W. K., Trench, R. K. (1983). Endocytosis of the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal, by endodermal cells of the scyphistomae of Cassiopeia xamachana and resistance of the algae to host digestion. J. Cell Sci. 64: 195–212
Glynn, P. W. (1983). Extensive bleaching and death of reef corals on the Pacific Coast of Panama. Envir. Conserv. 10: 149–154
Glynn, P. W. (1991). Coral reef bleaching in the 1980s and possible connections with global warming. Trends Ecol. Evol. 6: 175–179
Glynn, P. W., D'Croz, L. (1990). Experimental evidence for high temperature stess as the cause of El Niño-coincident coral mortality. Coral Reefs 8: 181–191
Harland, A. D., Fixter, L. M., Spencer Davies, P., Anderson, R. A. (1992). Effects of light on the total lipid content and storage lipids of the symbiotic sea anemone Anemonia viridis. Mar. Biol. 112: 253–258
Hoegh-Guldberg, O., Smith, G. J. (1989). The effect of temperature, light and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata and Seriatopora hystrix J exp. mar. Biol. Ecol. 129: 279–303
Hohman, T. C., McNeil, P. L., Muscatine, L. (1982). Phagosomelysosome fusion inhibited by algal symbionts of Hydra viridis. J. Cell Biol. 94: 56–63
Hopsu-Havu, V. K., Helminen H. (1974) Sulfatases. In: Hayat, M. A. (ed.) Electron microscopy of enzymes principles and methods. 2. Van Nostrand Reinhold, New York, Toronto, London, p. 90–109
Jeon, K. W. (1983). Integration of bacterial endosymbionts in Amoebae. Int. Rev. Cytol. (Suppl.) 14: 29–47
Lesser, M. P., Stochaj, W. J., Tapley, D. W., Shick, J. M. (1990). Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8: 225–232
Lorch, I. J., Jeon, K. W. (1980). Resuscitation of amoebae deprived of essential symbiotes: micrurgical studies. J. Protozool. 27: 423–426
Lowe, D. M. (1981). Alterations in cellular structure of Mytilus edulis resulting from exposure to environmental contaminants under field and experimental conditions. Mar. Ecol. Prog. Ser. 46: 91–100
Lowe, D. M., Clarke, K. R. (1989). Contaminant-induced changes in the structure of the digestive epithelium of Mytilus edulis. Aquat. Toxic. 15: 345–358
Lowe, D. M., Moore, M. N., Clarke, K. R. (1981). Effects of oil on digestive cells in mussels: quantitative alterations in cellular and lysosomal structure. Aquat. Toxic. 1: 213–226
McNeil, P. L., McAuley, P. J. (1984). Lysosomes fuse with one half of algae bearing phagosomes during the reestablishment of the European green Hydra symbiosis. J. exp. Zool. 230: 377–385
Miller, D., Brown B. E., Sharp, V. A., Nganro, N. (1992). Changes in expression of soluble proteins extracted from the symbiotic anemone Anemonia viridis accompany bleaching induced by hyperthermia and metal stressors. J. therm. Biol. 17: 217–223
Moore, M. N. (1988). Cytochemical responses of the lysosmal system and NADPH-ferrihemoprotein reductase in molluscan digestive cells to environmental and experimental exposure to xenobiotics. Mar. Ecol. Prog. Ser. 46: 81–89
Moore, M. N. (1991). Cellular reactions to toxic environmental contaminants in marine molluscs. In: Able, P. D., Axiak, V. (eds.) Ecotoxicology and the marine environment. Ellis Horwood, Chichester, p. 157–175
Moore, M. N., Koehn, P. K., Bayne, B. L. (1980). Leucine aminopeptidase (aminopeptidase-1): N-acetyl-β-hexaminidase and lysosomes in the mussel, Mytilus edulis, L. in response to salinity changes. J. exp. Zool. 214: 239–249
Moore, M. N., Stebbing, A. R. D. (1976). The quantitative cytochemical effects of three metal ions on a lysosomal hydrolase of a hydroid. J. mar. biol. Ass. UK. 56: 955–1005
Oesman, M. P. (1991). Ultrastructural changes in zooxanthellae of Anemonia viridis on heat-stress. MSc dissertation. University of Newcastle upon Tyne, England
Patton, J. S., Abraham, S., Benson, A. A. (1977). Lipogenesis in the intact coral Pocillopora capitata and its isolated zooxanthellae: evidence for a light-driven carbon cycle between symbiont and host. Mar. Biol. 44: 235–247
Pipe, R. K., Da Silveira, H. M. C. (1989). Arylsulphatase and acid phosphatase activity associated with developing and ripe spermatozoa of the mussel Mytilus edulis. Histochem. J. 21: 23–32
Pipe, R. K., Moore, M. N. (1985). The ultrastructural localization of lysosomal acid hydrolases in developing oocytes of the common marine mussel Mytilus edulis. Histochem. J. 17: 939–949
Pipe, R. K., Moore, M. N. (1986a) Arylsulphatase activity associated with phenanthrene induced digestive cell deletion in the marine mussel Mytilus edulis. Histochem. J. 18: 557–564
Pipe, R. K., Moore, M. N. (1986b). An ultrastructural study on the effects of phenanthrene on lysosomal membranes and distribution of the lysosomal enzyme β-glucuronidase in digestive cells of the periwinkle Littorina littorea. Aquat. Toxic. 8: 65–76
Suharsono (1990). Ecological and physiological implications of coral bleaching at Pari Island, Thousand Islands, Indonesia. PhD dissertation. University of Newcastle upon Tyne, England
Suharsono, Brown, B. E. (1992). Comparative measurements of mitotic index in zooxanthellae from a symbiotic cnidarian subject to temperature increase. J. exp. mar. Biol. Ecol. 158: 179–188
Tiffon, M. Y. (1971). Détection cytochemique d'hyrolases lysosmiales dans les cloisons septales stériles de Cerianthus lloydi (Coelentere Anthozoaire). C. r. hebd Séanc. Acad. Sci., Paris. 273: 1953–1967
Trench, R. K., Colley, N. J., Fitt, W. K. (1981). Recognition phenomana in symbiosis between marine invertebrates and zooxanthellae uptake; sequestration and persistence. Ber. dt. bot. Ges. 94: 568–629
Vandermeulen, J. H., Davis, N. D., Muscatine, L. (1972). The effect of inhibitors of photosynthesis on zooxanthellae in corals and other marine invertebrates. Mar. Biol. 16: 185–191
Williams, E. H., Goenaga, C., Vincente, V. (1987). Mass bleaching on Atlantic coral reefs. Science, N. Y. 237: 877–878
Wolfe, D. A., Clark, R. C., Foster, C. A., Hawkes, J. W., MacLoad, W. D. (1981). Hydrocarbon accumulation and histopathology in bivalve molluscs transplanted to the Baie de Morlaix and the Rade de Brest. In: Amoco Cadiz: fates and effects of the oil spill. Centre d'Océanologie de Bretagne, Brest, France, p. 599–616
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Communicated by J. Mauchline, Oban
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Suharsono, Pipe, R.K. & Brown, B.E. Cellular and ultrastructural changes in the endoderm of the temperate sea anemone Anemonia viridis as a result of increased temperature. Marine Biology 116, 311–318 (1993). https://doi.org/10.1007/BF00350021
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DOI: https://doi.org/10.1007/BF00350021