Coral bleaching--capacity for acclimatization and adaptation.

Coral bleaching, i.e., loss of most of the symbiotic zooxanthellae normally found within coral tissue, has occurred with increasing frequency on coral reefs throughout the world in the last 20 years, mostly during periods of El Nino Southern Oscillation (ENSO). Experiments and observations indicate that coral bleaching results primarily from elevated seawater temperatures under high light conditions, which increases rates of biochemical reactions associated with zooxanthellar photosynthesis, producing toxic forms of oxygen that interfere with cellular processes. Published projections of a baseline of increasing ocean temperature resulting from global warming have suggested that annual temperature maxima within 30 years may be at levels that will cause frequent coral bleaching and widespread mortality leading to decline of corals as dominant organisms on reefs. However, these projections have not considered the high variability in bleaching response that occurs among corals both within and among species. There is information that corals and their symbionts may be capable of acclimatization and selective adaptation to elevated temperatures that have already resulted in bleaching resistant coral populations, both locally and regionally, in various areas of the world. There are possible mechanisms that might provide resistance and protection to increased temperature and light. These include inducible heat shock proteins that act in refolding denatured cellular and structural proteins, production of oxidative enzymes that inactivate harmful oxygen radicals, fluorescent coral pigments that both reflect and dissipate light energy, and phenotypic adaptations of zooxanthellae and adaptive shifts in their populations at higher temperatures. Such mechanisms, when considered in conjunction with experimental and observational evidence for coral recovery in areas that have undergone coral bleaching, suggest an as yet undefined capacity in corals and zooxanthellae to adapt to conditions that have induced coral bleaching. Clearly, there are limits to acclimatory processes that can counter coral bleaching resulting from elevated sea temperatures, but scientific models will not accurately predict the fate of reef corals until we have a better understanding of coral-algal acclimatization/adaptation potential. Research is particularly needed with respect to the molecular and physiological mechanisms that promote thermal tolerance in corals and zooxanthellae and identification of genetic characteristics responsible for the variety of responses that occur in a coral bleaching event. Only then will we have some idea of the nature of likely responses, the timescales involved and the role of 'experience' in modifying bleaching impact.

[1]  O. Hoegh-Guldberg,et al.  Major colour patterns of reef-building corals are due to a family of GFP-like proteins , 2001, Coral Reefs.

[2]  R. Berkelmans Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef , 2002 .

[3]  R. Aronson,et al.  The 1998 bleaching event and its aftermath on a coral reef in Belize , 2002 .

[4]  Y. Loya,et al.  Penetration of the Coral-Bleaching BacteriumVibrio shiloi into Oculina patagonica , 2000, Applied and Environmental Microbiology.

[5]  W. Fitt,et al.  Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea , 2002 .

[6]  R. Aronson,et al.  Ecosystems: Coral bleach-out in Belize , 2000, Nature.

[7]  Tomas Tomascik,et al.  The Ecology of the Indonesian Seas , 1997 .

[8]  R. Berkelmans Bleaching, upper thermal limits and temperature adaptation in reef corals , 2001 .

[9]  R. Buddemeier,et al.  CORAL BLEACHING AS AN ADAPTIVE MECHANISM : A TESTABLE HYPOTHESIS , 1993 .

[10]  N. Gassman,et al.  The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis , 1990, Coral Reefs.

[11]  Peter W. Glynn,et al.  Crisis on coral reefs linked to climate change , 2001 .

[12]  H. Lasker,et al.  Bleaching of reef coelenterates in the San Blas Islands, Panama , 1984, Coral Reefs.

[13]  M. Pigllucci,et al.  How organisms respond to environmental changes: from phenotypes to molecules (and vice versa). , 1996, Trends in ecology & evolution.

[14]  S. Coles Species Diversity of Decapods Associated with Living and Dead Reef Coral Pocillopora meandrina , 1980 .

[15]  M. Meekan,et al.  Catastrophic loss of coral cover from reefs in the southern Great Barrier Reef and the impact on fish recruitment , 1997 .

[16]  B. Willis,et al.  Impacts of bleaching on the soft coral Lobophytum compactum. II. Biochemical changes in adults and their eggs , 2001, Coral Reefs.

[17]  M. Olaizola,et al.  SHORT‐TERM RESPONSE OF THE DIADINOXANTHIN CYCLE AND FLUORESCENCE YIELD TO HIGH IRRADIANCE IN CHAETOCEROS MUELLERI (BACILLARIOPHYCEAE) 1 , 1994 .

[18]  Barbara E. Brown,et al.  Adaptations of Reef Corals to Physical Environmental Stress , 1997 .

[19]  W. Fitt,et al.  Diurnal changes in photochemical efficiency and xanthophyll concentrations in shallow water reef corals : evidence for photoinhibition and photoprotection , 1999, Coral Reefs.

[20]  E. Rosenberg,et al.  A novel Vibrio sp. pathogen of the coral Pocilloporadamicornis , 2002 .

[21]  J. Wiedenmann,et al.  Molecular diversity of symbiotic algae at the latitudinal margins of their distribution: dinoflagellates of the genus Symbiodinium in corals and sea anemones , 2002 .

[22]  W. Fitt,et al.  Bleaching Patterns of Four Species of Caribbean Reef Corals. , 1995, The Biological bulletin.

[23]  S. Coles,et al.  Thermal Tolerance in Tropical Versus Subtropical Pacific Reef Corals , 1976 .

[24]  F. Rodríguez-Zaragoza,et al.  Coral bleaching and mortality in the Mexican Pacific during the 1997-98 El Niño and prediction from a remote sensing approach , 2001 .

[25]  Y. Loya,et al.  Role of endosymbiotic zooxanthellae and coral mucus in the adhesion of the coral-bleaching pathogen Vibrio shiloi to its host. , 2001, FEMS microbiology letters.

[26]  S. Coles,et al.  Effects of Heated Effluent on Hermatypic Corals at Kahe Point, Oahu , 1974 .

[27]  R. Gates,et al.  The biology of larvae from the reef coral Poritesastreoides, and their response to temperature disturbances , 2001 .

[28]  B. Brown,et al.  The influence of solar radiation on bleaching of shallow water reef corals in the Andaman Sea, 1993–1998 , 2001, Coral Reefs.

[29]  Guy Cox,et al.  Fluorescent pigments in corals are photoprotective , 2000, Nature.

[30]  A. Logan,et al.  Elevated temperatures and bleaching on a high latitude coral reef: the 1988 Bermuda event , 1990, Coral Reefs.

[31]  John C. Field,et al.  The Potential Consequences of Climate Variability and Change on Coastal Areas and Marine Resources , 2000 .

[32]  C. Downs,et al.  Exploring the basis of thermotolerance in the reef coral Goniastrea aspera , 2002 .

[33]  C. Yonge,et al.  STUDIES ON THE PHYSIOLOGY OF CORALS: V. THE EFFECT OF STARVATION IN LIGHT AND IN DARKNESS ON THE RELATIONSHIP BETWEEN CORALS AND ZOOXANTHELLAE , 1931 .

[34]  Y. Loya,et al.  Bleaching effect on regeneration and resource translocation in the coral Oculina patagonica , 2002 .

[35]  S. Coles,et al.  Effects of temperature on the mortality and growth of Hawaiian reef corals , 1977 .

[36]  B. Riegl,et al.  Corals in a non-reef setting in the southern Arabian Gulf (Dubai, UAE): fauna and community structure in response to recurring mass mortality , 1999, Coral Reefs.

[37]  P. W. Glynn,et al.  Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality , 1990, Coral Reefs.

[38]  K. Yamazato,et al.  Coral bleaching: the winners and the losers , 2001 .

[39]  J. Bythell,et al.  Mechanisms of bleaching deduced from histological studies of reef corals sampled during a natural bleaching event , 1995 .

[40]  R. P. Dunne,et al.  Marine ecology: Bleaching patterns in reef corals , 2000, Nature.

[41]  O. Hoegh‐Guldberg,et al.  Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific , 2001 .

[42]  A. A. Roth,et al.  Effect of temperature and temperature adaptation on calcification rate in the hermatypic coral Pocillopora damicornis , 1975 .

[43]  P. Glynn Widespread Coral Mortality and the 1982–83 El Niño Warming Event , 1984, Environmental Conservation.

[44]  Y. Loya,et al.  Bacterial infection and coral bleaching , 1996, Nature.

[45]  E. Stackebrandt,et al.  Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. , 2001, International journal of systematic and evolutionary microbiology.

[46]  M. Öhman,et al.  The 1997/1998 mass mortality of corals: effects on fish communities on a Tanzanian coral reef. , 2001, Marine pollution bulletin.

[47]  M. Gleason,et al.  Effects of disturbance on coral communities: bleaching in Moorea, French Polynesia , 1993, Coral Reefs.

[48]  A. Edwards,et al.  Coral bleaching and mortality on artificial and natural reefs in Maldives in 1998, sea surface temperature anomalies and initial recovery. , 2001, Marine pollution bulletin.

[49]  D. J. Kinsman,et al.  Reef Coral Tolerance of High Temperatures and Salinities , 1964, Nature.

[50]  B. Willis,et al.  Impacts of bleaching on the soft coral Lobophytum compactum. I. Fecundity, fertilization and offspring viability , 2001, Coral Reefs.

[51]  P. Glynn,et al.  The 1997-98 El Niño event in Panama and Galápagos: An update of thermal stress indices relative to coral bleaching , 2001 .

[52]  Peter J. Mumby,et al.  Bleaching and hurricane disturbances to populations of coral recruits in Belize , 1999 .

[53]  R. Lindzen,et al.  Reconciling observations of global temperature change , 2002 .

[54]  Y. Loya,et al.  Effect of Temperature on Adhesion ofVibrio Strain AK-1 to Oculina patagonica and on Coral Bleaching , 1998, Applied and Environmental Microbiology.

[55]  T. McClanahan Bleaching Damage and Recovery Potential of Maldivian Coral Reefs , 2000 .

[56]  B. Ames,et al.  The free radical theory of aging matures. , 1998, Physiological reviews.

[57]  A. Douglas,et al.  On the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance , 2002 .

[58]  H. Kayanne,et al.  Recovery of coral populations after the 1998 bleaching on Shiraho Reef, in the southern Ryukyus, NW Pacific , 2002 .

[59]  B. Riegl Effects of the 1996 and 1998 positive sea-surface temperature anomalies on corals, coral diseases and fish in the Arabian Gulf (Dubai, UAE) , 2002 .

[60]  J. West,et al.  Management of bleached and severely damaged coral reefs , 2000 .

[61]  R. Cogdell,et al.  Carotenoids in Photosynthesis , 1996, Photochemistry and photobiology.

[62]  G. Schmidt,et al.  Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Zachos,et al.  Palaeoclimatology (Communication arising): Tropical temperatures in greenhouse episodes , 2002, Nature.

[64]  R. Bak,et al.  Effects of coral bleaching on tissue regeneration potential and colony survival , 1993 .

[65]  G. Sarazin,et al.  Proceedings of the sixth international coral reef symposium , 1988 .

[66]  A. Mayer Ecology of the Murray Island Coral Reef. , 1915, Proceedings of the National Academy of Sciences of the United States of America.

[67]  S. Lindquist,et al.  The heat-shock proteins. , 1988, Annual review of genetics.

[68]  R. Voellmy,et al.  Heat Shock Protein Induction in Montastraea faveolata and Aiptasia pallida Exposed to Elevated Temperatures. , 1995, The Biological bulletin.

[69]  G. Duineveld,et al.  RNA/DNA ratios of scleractinian corals suggest acclimatisation/adaptation in relation to light gradients and turbidity regimes , 2002 .

[70]  L. Fang,et al.  High temperature induces the synthesis of heat-shock proteins and the elevation of intracellular calcium in the coral Acropora grandis , 1997, Coral Reefs.

[71]  B. Brown,et al.  Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species , 1999 .

[72]  S. Coles Colonization of Hawaiian reef corals on new and denuded substrata in the vicinity of a Hawaiian power station , 1984, Coral Reefs.

[73]  S. Motoda The environment and the life of massive reef coral, Goniastrea aspera Verrill, Inhabiting the reef flat in Palao , 1940 .

[74]  R. Gates,et al.  The Physiological Mechanisms of Acclimatization in Tropical Reef Corals , 1999 .

[75]  T. Goulet,et al.  Early ontogenetic expression of specificity in a cnidarian-algal symbiosis , 2001 .

[76]  S. Coles,et al.  Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature , 1990, Coral Reefs.

[77]  Y. Loya,et al.  Effect of temperature on bleaching of the coral Oculina patagonica by Vibrio AK-1 , 1998 .

[78]  Jordan M. West,et al.  Resistance and Resilience to Coral Bleaching: Implications for Coral Reef Conservation and Management , 2003 .

[79]  S. Coles,et al.  Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa , 1978 .

[80]  Suharsono,et al.  Damage and recovery of coral reefs affected by El Niño related seawater warming in the Thousand Islands, Indonesia , 1990, Coral Reefs.

[81]  B. Brown,et al.  Coral bleaching: causes and consequences , 1997, Coral Reefs.

[82]  Serge Andréfouët,et al.  Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event , 2001 .

[83]  A. Cohen,et al.  Coral Bleaching on Johnston Atoll, Central Pacific Ocean. , 1997, The Biological Bulletin.

[84]  R. Gates,et al.  Temperature Stress Causes Host Cell Detachment in Symbiotic Cnidarians: Implications for Coral Bleaching. , 1992, The Biological bulletin.

[85]  T. McShane The Devil in the Detail of Biodiversity Conservation , 2003 .

[86]  K. Fabricius Tissue loss and mortality in soft corals following mass-bleaching , 1999, Coral Reefs.

[87]  P. Falkowski,et al.  Non-photochemical fluorescence quenching and the diadinoxanthin cycle in a marine diatom , 1994, Photosynthesis Research.

[88]  E. Rosenberg,et al.  Growth, differentiation and death of Vibrio shiloi in coral tissue as a function of seawater temperature , 2001 .

[89]  O. Hoegh‐Guldberg Climate change, coral bleaching and the future of the world's coral reefs , 1999 .

[90]  T. McClanahan,et al.  Coral and algal changes after the 1998 coral bleaching: interaction with reef management and herbivores on Kenyan reefs , 2001, Coral Reefs.

[91]  A. Douglas,et al.  Experience shapes the susceptibility of a reef coral to bleaching , 2002, Coral Reefs.

[92]  A. Baker Ecosystems: Reef corals bleach to survive change , 2001, Nature.

[93]  C. Birkeland,et al.  High temperatures tolerated by a diverse assemblage of shallow-water corals in American Samoa , 2001, Coral Reefs.

[94]  R. Berkelmans,et al.  Large-scale bleaching of corals on the Great Barrier Reef , 1999, Coral Reefs.

[95]  David Miller,et al.  Heat shock protein (hsp 70) expression in the tropical reef coral Goniopora djiboutiensis , 1997 .

[96]  R. Warwick,et al.  Serial patterns of biodiversity change in corals across shallow reef flats in Ko Phuket, Thailand, due to the effects of local (sedimentation) and regional (climatic) perturbations , 2002 .

[97]  H. R. Bonilla Effects of the 1997-1998 El Niño-Southern Oscillation on coral communities of the Gulf of California, Mexico , 2001 .

[98]  R Gomulkiewicz,et al.  Adaptive phenotypic plasticity: consensus and controversy. , 1995, Trends in ecology & evolution.

[99]  G. Yohe,et al.  A globally coherent fingerprint of climate change impacts across natural systems , 2003, Nature.

[100]  F. Hartl Molecular chaperones in cellular protein folding , 1996, Nature.

[101]  Hayes Rl,et al.  Induction of 70-kD heat shock protein in scleractinian corals by elevated temperature: significance for coral bleaching. , 1995 .

[102]  O. Hoegh‐Guldberg,et al.  Temperature‐induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae , 1998 .

[103]  L. McCook,et al.  The fate of bleached corals: patterns and dynamics of algal recruitment , 2002 .

[104]  P. Glynn,et al.  Coral reef bleaching in the 1980s and possible connections with global warming. , 1991, Trends in ecology & evolution.

[105]  B. Brown Worldwide death of corals—Natural cyclical events or man-made pollution? , 1987 .

[106]  J. Feingold Responses of Three Coral Communities to the 1997–98 El Niño–Southern Oscillation: Galápagos Islands, Ecuador , 2001 .

[107]  S. W. Jeffrey,et al.  PHOTOSYNTHETIC PIGMENTS OF SYMBIOTIC DINOFLAGELLATES (ZOOXANTHELLAE) FROM CORALS AND CLAMS , 1968 .

[108]  M. Ashburner,et al.  The induction of gene activity in drosophila by heat shock , 1979, Cell.

[109]  S. Heckathorn,et al.  Small Heat Shock Proteins Protect Electron Transport in Chloroplasts and Mitochondria During Stress , 1999 .

[110]  R. Salm,et al.  Coral Bleaching and Marine Protected Areas , 2001 .

[111]  N. Phongsuwan Extensive coral mortality as a result of bleaching in the Andaman Sea in 1995 , 1998, Coral Reefs.

[112]  O. Hoegh‐Guldberg,et al.  Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora , 2001 .

[113]  M. P. Lesser,et al.  Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen , 1990, Coral Reefs.

[114]  E. Williams,et al.  The World-Wide Coral Reef Bleaching Cycle and Related Sources of Coral Mortality , 1990 .

[115]  T. Done Coral Community Adaptability to Environmental Change at the Scales of Regions, Reefs and Reef Zones , 1999 .

[116]  C. Downs,et al.  A Molecular Biomarker System for Assessing the Health of Coral (Montastraea faveolata) During Heat Stress , 2000, Marine Biotechnology.

[117]  H. Guzman,et al.  Changes in reef community structure after fifteen years of natural disturbances in the eastern Pacific (Costa Rica) , 2001 .

[118]  Richard I. Morimoto,et al.  1 Progress and Perspectives on the Biology of Heat Shock Proteins and Molecular Chaperones , 1994 .

[119]  C. Yonge,et al.  STUDIES ON THE PHYSIOLOGY OF CORALS: IV. THE STRUCTURE, DISTRIBUTION AND PHYSIOLOGY OF THE ZOOXANTHELLAE , 1931 .

[120]  O. Hoegh‐Guldberg,et al.  Changes in quantum efficiency of Photosystem II of symbiotic dinoflagellates of corals after heat stress, and of bleached corals sampled after the 1998 Great Barrier Reef mass bleaching event , 2000 .

[121]  O. Hoegh‐Guldberg,et al.  Periodic mass-bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia , 1995 .

[122]  M. Lesser Oxidative stress causes coral bleaching during exposure to elevated temperatures , 1997, Coral Reefs.

[123]  O. Hoegh‐Guldberg,et al.  Ecology (Communication arising): Is coral bleaching really adaptive? , 2002, Nature.

[124]  A. Pittock,et al.  Coral Reefs and Environmental Change: Adaptation to What? , 1999 .

[125]  G. Britton,et al.  Fluctuations in algal chlorophyll and carotenoid pigments during solar bleaching in the coral Goniastrea aspera at Phuket, Thailand , 1997 .

[126]  R. Buddemeier,et al.  Coral Adaptation and Acclimatization: A Most Ingenious Paradox , 1999 .

[127]  J. Woodley,et al.  Effect of the 1995-1996 bleaching event on polyp tissue depth, growth, reproduction and skeletal band formation in Montastraea annularis , 2002 .

[128]  J. R. Bowyer,et al.  Photoinhibition of photosynthesis : from molecular mechanisms to the field , 1994 .

[129]  P. Glynn Extensive ‘Bleaching’ and Death of Reef Corals on the Pacific Coast of Panamá , 1983, Environmental Conservation.

[130]  F. Zapata,et al.  Coral and coral reef responses to the 1997-98 El Niño event on the Pacific coast of Colombia , 2001 .

[131]  T. Wigley,et al.  The observed global warming record: what does it tell us? , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[132]  O. Hoegh‐Guldberg,et al.  The Effect of Sudden Changes in Temperature, Light and Salinity On the Population-Density and Export of Zooxanthellae From the Reef Corals Stylophora-Pistillata Esper and Seriatopora-Hystrix Dana , 1989 .

[133]  F. Rougerie,et al.  1994 Coral Bleaching Event, Society Islands, French Polynesia , 1994 .

[134]  Olof Lindén,et al.  Ecological and socioeconomic impacts of 1998 coral mortality in the Indian Ocean: an ENSO impact and a warning of future change? , 1999 .

[135]  W. Fitt,et al.  Damage and recovery of Photosystem II during a manipulative field experiment on solar bleaching in the coral Goniastrea aspera , 2000 .

[136]  A. Baird,et al.  Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa , 2000, Coral Reefs.

[137]  Mark E. Warner,et al.  Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals , 2001, Coral Reefs.

[138]  H. Boschma The Nature of the Association between Anthozoa and Zooxanthellae. , 1925, Proceedings of the National Academy of Sciences of the United States of America.

[139]  B. Willis,et al.  Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef , 1999, Coral Reefs.

[140]  T. Goreau Bleaching and reef community change in Jamaica: 1951-1991 , 1992 .

[141]  Robert W. Buddemeier,et al.  Patterns of coral bleaching: modeling the adaptive bleaching hypothesis , 1996 .

[142]  B. Brown,et al.  Coral bleaching relative to elevated seawater temperature in the Andaman Sea (Indian Ocean) over the last 50 years , 1996, Coral Reefs.

[143]  Peter W. Glynn,et al.  Coral bleaching and mortality in Panama and Ecuador during the 1997-1998 El Niño-Southern Oscillation event : Spatial/temporal patterns and comparisons with the 1982-1983 event , 2001 .

[144]  B. Halliwell,et al.  Free radicals in biology and medicine , 1985 .

[145]  J. Jaubert,et al.  Unprecedented bleaching-induced mortality in Porites spp. at Rangiroa Atoll, French Polynesia , 2001 .

[146]  C. H. Edmondson,et al.  The ecology of an Hawaiian coral reef , 1974 .

[147]  P. W. Glynn,et al.  Coral reef bleaching: ecological perspectives , 1993, Coral Reefs.

[148]  A. Baird,et al.  Mass bleaching of corals on the Great Barrier Reef , 1998, Coral reefs.

[149]  S. Neudecker Growth and survival of scleractinian corals exposed to thermal effluents at Guam , 1981 .

[150]  A. S. Evans,et al.  The Evolution of Plant Ecophysiological Traits: Recent Advances and Future Directions , 2000 .

[151]  S. R. Santos,et al.  The Adaptive Bleaching Hypothesis: Experimental Tests of Critical Assumptions , 2001, The Biological Bulletin.

[152]  Steven L. Miller,et al.  Florida's mystery coral-killer identified , 1998, Nature.

[153]  V. Harriott Mortality rates of scleractinian corals before and during a mass bleaching event , 1985 .

[154]  Y. Loya,et al.  Ultraviolet radiation prevents bleaching in the mediterranean coral Oculina patagonica , 2002 .

[155]  J. Bruno,et al.  El Niño related coral bleaching in Palau, Western Caroline Islands , 2001, Coral Reefs.

[156]  J. Reeve,et al.  Origin of the Eukaryotic Nucleus , 1998, Science.

[157]  D. R. Robertson,et al.  The Effect of the El Niño–southern Oscillation Event On the Distribution of Reef-associated Labrid Fishes In the Eastern Pacific Ocean , 2001 .

[158]  W. W. Adams,et al.  The xanthophyll cycle , 1993 .

[159]  M. Spalding,et al.  Coral Bleaching in the Southern Seychelles During the 1997–1998 Indian Ocean Warm Event , 2000 .

[160]  R. D. Gates,et al.  Seawater temperature and sublethal coral bleaching in Jamaica , 1990, Coral Reefs.

[161]  Clive Wilkinson,et al.  Status of Coral Reefs of the World: 2020 , 2000 .

[162]  S. Coles A Comparison of Effects of Elevated Temperature versus Temperature Fluctuations on Reef Corals at Kahe Point, Oahu , 1975 .

[163]  G. Somero,et al.  Heat-Shock Protein Expression in Mytilus californianus: Acclimatization (Seasonal and Tidal-Height Comparisons) and Acclimation Effects. , 1997, The Biological bulletin.

[164]  S. Coles,et al.  Effects of temperature on photosynthesis and respiration in hermatypic corals , 1977 .

[165]  Paul Marshall,et al.  Mortality, growth and reproduction in scleractinian corals following bleaching on the Great barrier Reef , 2002 .

[166]  G. Wellington,et al.  El Niño mass coral mortality: a test of resource limitation in a coral reef damselfish population , 1985, Oecologia.

[167]  R. Iglesias-Prieto,et al.  Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[168]  Mark E. Warner,et al.  The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach , 1996 .

[169]  J. Cortés,et al.  Coral bleaching and mortality associated with the 1997-98 El Niño in an upwelling environment in the eastern Pacific (Gulf of Papagayo, Costa Rica) , 2001 .

[170]  R. Berkelmans,et al.  Recurrent bleaching of corals at Magnetic Island (Australia) relative to air and seawater temperature , 1997 .