Keywords
coral bleaching
Hydrogen peroxide
Ca2
algal density
algal detachment
gastrodermal fragmentation
zooxantela
blanquamiento de corales
peróxido de hidrógeno
Ca2
densidad algal
desprendimiento algal
fragmentación gastrodermal
How to Cite
Abstract
Coral bleaching involves the detachment of zooxanthellae and the simultaneous fragmentation of the gastrodermis. Results obtained with a cell permeant fluorescent probe for calcium ions (Ca2+) indicates that “thermal” bleaching is the result of a temperature related breakdown of the Ca2+ exclusion system. “Solar” bleaching, which takes place at lower temperatures and is driven by light, is the result of a build-up of photosynthetically produced hydrogen peroxide in the tissues. Gastrodermal tissue with its symbionts, scraped from between septa of corals, was observed under controlled conditions of high light and temperature. Pieces of gastrodermis round off, zooxanthellae move to the surface, protrude from the surface and after a delay, detach, surrounded by a thin layer of host cytoplasm, inclusions and plasma membrane. The higher the temperature and light level the shorter the delay and higher the rate of algal detachment. Fragmentation by the ballooning-out and detachment of small spheres of cytoplasm (bleb formation) takes place simultaneously. This is likely to be due to oxidation, by hydrogen peroxide (H2O2), of -SH groups on the cytoskeleton and its attachment to the plasma membrane. Ground, polished and stained thin acrylic resin sections reveal similar processes taking place in artificially bleached corals. Isolated zooxanthellae and whole corals are shown to release H2O2 in the light. This process of algal detachment and fragmentation that takes place at normal sea temperatures may underlie the mechanism limiting algal populations in the gastrodermis and may be localized to areas with a concentration of algae near the membrane. At above-normal temperatures under the synergistic effect of light and temperature, the rate of production of H2O2 exceeds the rate at which can it be lost by diffusion or destroyed and H2O2 accumulates. This results in damage to the calcium exclusion system, detachment of zooxanthellae into the coelenteron and fragmentation of the gastrodermis. Rev. Biol. Trop. 54 (Suppl. 3): 79-96. Epub 2007 Jan. 15.References
Andreae, W.A. 1955. A sensitive method for the estimation of hydrogen peroxide in biological materials. Nature 175: 859-860.
Banin, E., T. Israely, A. Kushmaro, Y. Loya, E. Orr & E. Rosenberg. 2000. Penetration of the coral-bleaching bacterium Vibrio shiloi into Oculina patagonica. Appl. Env. Microbiol. 66: 3031-3036.
Blackstone, N.W. 2001. Redox state, Reactive oxygen species and adaptive growth in colonial hydroids. J. Exp. Biol. 204: 1845-1853.
Brown, B.E., M.D.A. Le Tissier & J.C. Bythell. 1995. Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event. Mar. Biol. 122: 655-663.
Brown, B.E., R.P. Dunne, M.S. Goodson & A.E. Douglas. 2000a. Bleaching pattern in reef corals. Nature 404: 142-143.
Brown, B.E., R.P. Dunne, M.E. Warner, I. Ambarsari, W.K. Fitt, S.W. Gibb & D.G. Cummings. 2000b. Damage and recovery of Photosystem II during a manipulative field experiment on solar bleaching in the coral Goniastra aspera. Mar. Ecol. Prog. Ser. 195: 117-124.
Downs, C.A., E. Mueller, S. Phillips, J.E. Fauth & C.M. Woodley. 2000. Oxidative stress and seasonal coral bleaching. Mar. Biotechnol. 2: 533-544.
Downs, C.A., J.E. Fauth, J.C. Halas, P. Dustan, J. Bemiss & C.M. Woodley. 2002. Oxidative stress and seasonal coral bleaching. Free Radical Biol. Med. 33: 533-543.
Drollet, J.H., M. Faucon & P.M.V. Martin. 1995. Elevated sea water temperatures and solar Uv-B flux associated with two successive coral mass bleaching events in Tahiti. Mar. Freshwater Res. 46: 1153-1157.
Dunn, S.R., J.C. Bythell, M.D.A. Le Tissier, W.J. Burnett & J.C. Thomason. 2002. Programmed cell death and cell necrosis activity during hyperthermic stressinduced bleaching of the symbiotic sea anemone Aiptasia sp. J. Exp. Mar. Biol. Ecol. 272: 29-53.
Dykens, J.A. 1984. Enzymic defences against oxygen toxicity in marine cnidarians containing endosymbiotic algae. Marine Biology Letters 5: 291-301.
Dykens, J.A. & J.M. Shick. 1984. Photobiology of the symbiotic sea anemone, Anthopleura elegantissima: Defences against photodynamic effects, and seasonal photoacclimatization. Biol. Bull. 167: 683-697.
Dykens, J.A., J.M. Shick, C. Benoit, G.R. Buettner & G.W. Winston. 1992. Oxygen radical production in the sea anemone Anthopleura elegantissima and its endosymbiotic algae. J. Exp. Biol. 168: 219-241.
Fang, L-S., J-T. Wang & K-L. Lin. 1998. The subcellular mechanism of the release of zooxanthellae during coral bleaching. Proc. Natl. Sci. Counc. Rep. China, Pt B, Life Sci 22: 150-158.
Fitt, W.K. & M.E. Warner. 1995. Bleaching patterns of four species of Caribbean reef corals. Biol. Bull. 189: 298-307.
Gates, R.D., G. Baghdasarian & L. Muscatine. 1992. Temperature stress causes host cell detachment in symbiotic cnidarians: Implications for coral bleaching. Biol. Bull. 182: 324-332.
Gleason, D.F. & G.M. Wellington. 1993. Ultraviolet radiation and coral bleaching. Nature 365: 836-838.
Glider, W.V. 1983. The biology of the association of Symbiodinium microadriaticum with Aiptasia pallida: an anemone-alga symbiosis. Ph.D. Diss., Univ. Nebraska, Lincoln, Nebraska. 102 p.
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. & L. D’Croz. 1990. Experimental evidence for high temperature stress as the cause of El Nino-coincidental coral mortality. Coral Reefs 8: 181-191.
Glynn, P.W., E.C. Peters & L. Muscatine. 1985. Coral tissue microstructure and necrosis: relation to catastrophic coral mortality in Panama. Dis. Aquat. Org. 1: 29-37.
Goreau, T.F. 1964. Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane Flora.. Science 145: 383-386.
Halliwell, B. & J.M.C. Gutteridge. 1999. Free Radicals in Biology and Medicine. (Third Edition) Oxford University Press, Oxford, England. 936 p.
Hoegh-Guldberg, O. 1999. Climate change and world’s coral reefs: Implications for the Great Barrier Reef. Mar. Freshw. Res. 50: 839-866.
Johannes, R.E. & W. J. Wiebe. 1970. A method for determination of coral tissue biomass and composition. Limnol. Oceanogr. 5: 822-824.
Jokiel, P.L. 1980. Solar ultraviolet radiation and coral reef epifauna. Science 207: 1069-1071.
Jokiel, P.L. & S.L. Coles. 1990. Responses of Hawaiian and other Indo-Pacific reef corals to elevated temperatures. Coral Reefs 8: 155-162.
Jones, R.J., O. Hoegh-Guldberg, A.W.D. Larkum & U. Schreiber. 1998. Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant, Cell Environ. 21: 1219-1230.
Kim, C.S., S.G. Lee, C.K. Lee, H.G. Kim & J. Jung. 1999. Reactive oxygen species as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium polykrikoides. J. Plankt. Res. 21: 2105-2115.
Kleppel, G.S., R.E. Dodge & C.J. Reese. 1989. Changes in pigmentation associated with the bleaching of stony corals. Limnol. Oceangr. 34: 1331-1335.
Kushmaro, A., Y. Loya, M. Fine & E. Rosenberg. 1996. Bacterial infection and coral bleaching. Nature 380: 396.
Kushmaro, A., E. Rosenberg, M. Fine, Y.B. Haim & Y. Loya. 1998. Effect of temperature on bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar. Ecol. Prog. Ser. 171: 131-137.
Lasker, H.R., E.C. Peters & M.A. Coffroth. 1984. Bleaching of reef coelenterates in the San Blas Islands, Panama. Coral Reefs 3: 183-190.
Lesser, M.P. 1996. Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol. Oceanogr. 41: 271-283.
Lesser, M.P. 1997. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16: 187-192.
Lesser, M.P., W.R. Stochaj, D.W. Tapley & J.M. Shick. 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.
Marsh, J.A. 1970. Primary productivity of reef-building calcareous red algae. Ecology 51: 255-263.
McCarthy, N.J & G.I. Evans. 1998. Methods for detecting and quantifying apoptosis. Curr. Top. Develop. Biol. 36:259-278.
McCloskey, L.R., T.G. Cove & E.A. Verde. 1996. Symbiont expulsion from the anemone Anthopleura elegantissima (Brandt) Cnidaria; Anthozoa). J. Exp. Mar. Biol. Ecol. 195: 173-186.
Meltzar, S & M.C. Berman. 1984. Effects of pH, temperature, and calcium concentration on the stoichiometry of the calcium pump of sarcoplasmic reticulum. J. Biol. Chem. 259: 4244-4253.
Muscatine, L., D. Grossman & J. Doino. 1991. Release of symbiotic algae by tropical sea anemones and corals after cold shock. Mar. Ecol. Prog. Ser. 77: 233-243.
Nakamura, T. & R. Van Woesik. 1997. Water flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Mar. Ecol. Prog. Ser. 149: 163-171.
Nii, C.M. & L. Muscatine. 1997. Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943): Contribution of the animal to superoxide ion production at elevated temperature. Biol. Bull. 192: 444-456.
Ogden, J. & R. Wicklund. 1988. Introduction, p. 1-9. In J. Ogden & R. Wicklund (eds.). Mass Bleaching of Corals in the Caribbean: A Research Strategy. Natl. Undersea Res. Prog. Rep. 88-2, NOAA, Washington DC.
Patterson, C.O.P. & J. Myers. 1973. Photosynthetic production of hydrogen peroxide by Anacystis nidulans. Plant Physiol. 51: 104-109.
Perez, S.F., C.B. Cook & W.R. Brooks. 2001. The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. J. Exp. Mar. Biol. Ecol. 256: 1-14.
Ralph, P.J., R. Gademann & A.W.D. Larkum. 2001. Zooxanthellae expelled from bleached corals at 33 C are photosynthetically competent. Mar. Ecol. Prog. Ser. 220: 163-168.
Rega, A.F. 1986. Other properties and coupling of Ca2+ transport and ATP hydrolysis: p. 91-104. In: A.F. Rega & P.J. Garrahan, The Ca2+ pump of plasma membranes. CRC Press, Boca Raton, Florida, USA.
Searle, J., J.F.R. Kerr & C.J. Bishop. 1982. Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathol. Annu. 17: 229-259.
Slater, A.F.G., C. Stefan, I. Nobel, D.J. van den Dobbelsteen & S. Orrenius. 1995. Signalling mechanisms and oxidative stress in apoptosis. Toxicol. Lett. 82/83: 149-153.
Steen, R.G. & L. Muscatine. 1987. Low temperature evokes rapid exocytosis of symbiotic algae by a sea anemone. Biol. Bull. 172: 246-263.
Szmant, A. & N.J. Gassman. 1990. The effects of prolonged bleaching on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8: 217-224.
Tytler, E.M. & R.K. Trench. 1986. Activities of enzymes in ß-carboxylation reactions and of catalase in cellfree preparations from the symbiotic dinoflagellates Symbiodinium spp. from a coral, a clam, a zoanthid and two sea anemones. Proc. R. Soc. Lond. B 228: 483-492.
Vicente, V.P. 1990. Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs 8: 199-204.
Vogel, A.I. 1961. A text-book of quantitative inorganic analysis including elementary instrumental analysis. Longmans, Green, London. 363 p.
Warner, M.E., W.K. Fitt & G.W. Schmidt. 1999. Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proc. Natl. Acad. Sci. USA 96: 8007-8012.
Williams, E.H., Jr & L. Bunkley-Williams. 1990. The world wide coral bleaching cycle and related sources of coral mortality. Atoll Res. Bull. 335: 1-71.
Yonge, C.M. & A.G. Nicholls. 1931. Studies on the physiology of corals IV. The structure, distribution and physiology of the zooxanthellae. Great Barrier Reef Expedition 1928-29, Scient. Rep. 1: 135-176.
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