Coral bleaching: causes and consequences

Abstract It has been over 10 years since the phenomenon of extensive coral bleaching was first described. In most cases bleaching has been attributed to elevated temperature, but other instances involving high solar irradiance, and sometimes disease, have also been documented. It is timely, in view of our concern about worldwide reef condition, to review knowledge of physical and biological factors involved in bleaching, the mechanisms of zooxanthellae and pigment loss, and the ecological consequences for coral communities. Here we evaluate recently acquired data on temperature and irradiance-induced bleaching, including long-term data sets which suggest that repeated bleaching events may be the consequence of a steadily rising background sea temperature that will in the future expose corals to an increasingly hostile environment. Cellular mechanisms of bleaching involve a variety of processes that include the degeneration of zooxanthellae in situ, release of zooxanthellae from mesenterial filaments and release of algae within host cells which become detached from the endoderm. Photo-protective defences (particularly carotenoid pigments) in zooxanthellae are likely to play an important role in limiting the bleaching response which is probably elicited by a combination of elevated temperature and irradiance in the field. The ability of corals to respond adaptively to recurrent bleaching episodes is not known, but preliminary evidence suggests that phenotypic responses of both corals and zooxanthellae may be significant.

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

[2]  United Kingdom. Global Ocean Surface Temperature Atlas (GOSTA), and Land Surface Atlas , 1991 .

[3]  William J. Emery,et al.  On the bulk‐skin temperature difference and its impact on satellite remote sensing of sea surface temperature , 1990 .

[4]  R. Steen,et al.  LOW TEMPERATURE EVOKES RAPID EXOCYTOSIS OF SYMBIOTIC ALGAE BY A SEA ANEMONE , 1987 .

[5]  J. Stone Climate change 1995: The science of climate change. Contribution of working group I to the second assessment report of the intergovernmental panel on climate change , 1997 .

[6]  D. Gleason Differential effects of ultraviolet radiation on green and brown morphs of the Caribbean coral Porites astreoides , 1993 .

[7]  M. Lesser,et al.  Depth-dependent responses to solar ultraviolet radiation and oxidative stress in the zooxanthellate coral Acropora microphthalma , 1995 .

[8]  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 .

[9]  D. Gleason,et al.  Variation in UVB sensitivity of planula larvae of the coral Agaricia agaricites along a depth gradient , 1995 .

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

[11]  M. Lesser,et al.  Effects of ultraviolet radiation on corals and other coral reef organisms , 1996 .

[12]  T. Goreau Mass Expulsion of Zooxanthellae from Jamaican Reef Communities after Hurricane Flora , 1964, Science.

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

[14]  R. Woesik,et al.  Effects of Cyclone 'Joy' on nearshore coral communities of the Great Barrier Reef , 1995 .

[15]  C. Roberts,et al.  Coral reefs: Health, hazards and history. , 1993, Trends in ecology & evolution.

[16]  Raymond L. Hayes,et al.  Coral Bleaching and Ocean "Hot Spots" , 1994 .

[17]  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 .

[18]  B. Brown,et al.  Dynamics of solar bleaching in the intertidal reef coral Goniastrea aspera at Ko Phuket, Thailand , 1996 .

[19]  R. Dunne Radiation and coral bleaching , 1994, Nature.

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

[21]  N. Mimura,et al.  Coastal Zones and Small Islands , 1995 .

[22]  N. Knowlton,et al.  Intraspecific diversity and ecological zonation in coral-algal symbiosis. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[23]  D. Bachelet,et al.  LATITUDINAL AND SEASONAL VARIATION IN CALCULATED ULTRAVIOLET‐B IRRADIANCE FOR RICE‐GROWING REGIONS OF ASIA * , 1991 .

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

[25]  R. Iglesias-Prieto,et al.  Macromolecules Associated with the Cell Walls of Symbiotic Dinoflagellates , 1992 .

[26]  Suharsono,et al.  Cellular and ultrastructural changes in the endoderm of the temperate sea anemone Anemonia viridis as a result of increased temperature , 1993 .

[27]  Dunne Rp,et al.  Penetration of solar UVB radiation in shallow tropical waters and its potential biological effects on coral reefs; results from the central Indian Ocean and Andaman Sea , 1996 .

[28]  M. Lesser,et al.  Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defenses against oxygen toxicity , 1989 .

[29]  M. Lesser Photobiology of natural populations of zooxanthellae from the sea anemone Aiptasia pallida: assessment of the host's role in protection against ultraviolet radiation. , 1989, Cytometry.

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

[31]  L. Muscatine,et al.  Coral tissue microstructure and necrosis: relation to catastrophic coral mortality in Panama , 1985 .

[32]  A. Banaszak,et al.  Effects of ultraviolet (UV) radiation on marine microalgal-invertebrate symbioses. I. Response of the algal symbionts in culture an in hospite , 1995 .

[33]  A. Bradshaw,et al.  Evolution and stress-genotypic and phenotypic components , 1989 .

[34]  A. Tudhope,et al.  EVALUATION OF THE ENVIRONMENTAL-IMPACT OF DREDGING ON INTERTIDAL CORAL REEFS AT KO-PHUKET, THAILAND, USING ECOLOGICAL AND PHYSIOLOGICAL-PARAMETERS , 1990 .

[35]  T. P. Scoffin,et al.  Solar damage in intertidal corals , 1994 .

[36]  A. Strong,et al.  APPLYING MCSST TO CORAL REEF BLEACHING , 1995 .

[37]  S. Madronich,et al.  Changes in ultraviolet-radiation reaching the earths surface , 1994 .

[38]  R. Gates,et al.  Free amino acids exhibit anthozoan "host factor" activity: they induce the release of photosynthate from symbiotic dinoflagellates in vitro. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Ogden,et al.  A Long-Term Interdisciplinary Study of the Florida Keys Seascape , 1994 .

[40]  R. Kinzie Effects of ambient levels of solar ultraviolet radiation on zooxanthellae and photosynthesis of the reef coral Montipora verrucosa , 1993 .

[41]  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.

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

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

[44]  D. Powers,et al.  A Molecular Genetic Classification of Zooxanthellae and the Evolution of Animal-Algal Symbioses , 1991, Science.

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

[46]  L. Muscatine,et al.  Release of symbiotic algae by tropical sea anemones and corals after cold shock , 1991 .

[47]  J. Vaisnys,et al.  Temperature stress induces dynamical chaos in a cnidarian gastrovascular system , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[49]  D. Lubin,et al.  Effects of clouds and stratospheric ozone depletion on ultraviolet radiation trends , 1995, Nature.

[50]  D. Gleason,et al.  Ultraviolet radiation and coral bleaching , 1993, Nature.

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

[52]  E. Peters,et al.  A new and unusual species of coccidium (Apicomplexa: Agamococcidiorida) from Caribbean scleractinian corals , 1986 .

[53]  Ming-chin Liu,et al.  Pigment Composition in Different-colored Scleractinian Corals before and during the Bleaching Process , 1995 .

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

[55]  P. Edmunds Evidence that reef-wide patterns of coral bleaching may be the result of the distribution of bleaching-susceptible clones , 1994 .

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

[57]  T. Hughes Catastrophes, Phase Shifts, and Large-Scale Degradation of a Caribbean Coral Reef , 1994, Science.

[58]  David Miller,et al.  Expression of low molecular weight HSP 70 related polypeptides from the symbiotic sea anemone Anemonia viridis forskall in response to heat shock , 1994 .

[59]  D. R. Kobluk,et al.  «Ring» bleaching in southern Caribbean Agaricia agaricites during rapid water cooling , 1994 .

[60]  D. Parker,et al.  Marine surface temperature: Observed variations and data requirements , 1995 .

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

[62]  T. Done,et al.  The effects of Cyclone Sadie on coral communities of nearshore reefs in the central Great Barrier Reef , 1997 .

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

[64]  R. K. Trench,et al.  Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density , 1994 .

[65]  David Miller,et al.  A novel environmentally-regulated 33 kDa protein from tropical and temperate cnidarian zooxanthellae , 1995 .

[66]  T. Done,et al.  Taxonomic and bathymetric patterns of bleaching in corals, Myrmidon reef , 1985 .

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