Coral Bleaching: Causes and Mechanisms

  • Michael P. LesserEmail author


Unprecedented changes in coral reef systems have focused attention on a wide range of stressors on local, regional, and global spatial scales but global climate change resulting in elevated seawater temperatures is widely accepted as having contributed to the major declines in coral cover or phase shifts in community structure on time scales never previously observed or recorded in the geological record. The major mechanism of scleractinian mortality as a result of global climate change is “coral bleaching,” the loss of the endosymbiotic dinoflagellates (=zooxanthellae) that occurs as part of the coral stress response to temperature perturbations in combination with several other synergistic factors. Over several years many studies have shown that the common mechanism underlying the stress response of corals to elevated temperatures is oxidative stress that is exacerbated when exposure to high irradiances of solar radiation accompanies the thermal insult. Oxidative stress, the production and accumulation of reduced oxygen intermediates such as superoxide radicals, singlet oxygen, hydrogen peroxide, and hydroxyl radicals can cause damage to lipids, proteins, and DNA. Reactive oxygen species are also important signal transduction molecules and mediators of damage in cellular processes, such as apoptosis, autophagy, and cell necrosis all of which are believed to have roles in coral bleaching depending on the intensity and duration of the environmental insult. This chapter examines the current evidence supporting the hypothesis that the production and accumulation of reactive oxygen species leads to oxidative stress and is the proximal cause of coral bleaching.


Corals zooxanthellae coral bleaching seawater temperature global climate change 



The author thanks numerous colleagues for engaging in many conversations on the subject. Many funding agencies, including NOAA, NSF, and ONR, have supported this work over the years. In particular, the Coral Reef Targeted Research (CRTR) Program provided funding to support this review.


  1. Anderson S, Zepp R, Machula J, Santavy D, Hansen L, Mueller D (2001) Indicators of UV exposure in corals and their relevance to global climate change and coral bleaching. Human Ecol Risk Assess 7:1271–1282CrossRefGoogle Scholar
  2. Angilletta MJ Jr, Wilson RS, Navas CA, James RS (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240CrossRefGoogle Scholar
  3. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105:17442–17446CrossRefGoogle Scholar
  4. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Ann Rev Plant Physiol Mol Biol 50:601–639CrossRefGoogle Scholar
  5. Bailey S, Melis A, Mackey KRM, Cardol P, Finazzi G, van Dijken G, Berg GM, Arrigo K, Shrager J, Grossman A (2008) Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim Biophys Acta 1777:269–276CrossRefGoogle Scholar
  6. Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2008) Coral bleaching: the role of the host. Trends Ecol Evol 24:16–20CrossRefGoogle Scholar
  7. Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766CrossRefGoogle Scholar
  8. Banaszak AT, Lesser MP (2009) Effects of ultraviolet radiation on coral reef organisms. Photochem Photobiol Sci 8:1276–1294CrossRefGoogle Scholar
  9. Baruch R, Avishai N, Rabinowitz C (2005) UV incites diverse levels of DNA breaks in different cellular compartments of a branching coral species. J Exp Biol 208:843–848CrossRefGoogle Scholar
  10. Bayne BL (2004) Phenotypic flexibility and physiological tradeoffs in the feeding and growth of marine bivalve mollusks. Integr Comp Biol 44:425–432CrossRefGoogle Scholar
  11. Beere HM, Green DR (2001) Stress management-heat shock protein-70 and the regulation of apoptosis. Trends Cell Biol 11:6–10CrossRefGoogle Scholar
  12. Bellwood DR, Hughes TP, Folke C, Nystrom N (2004) Confronting the coral reef crisis. Nature 429:827–833CrossRefGoogle Scholar
  13. Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc R Soc Lond B 273:2305–2312CrossRefGoogle Scholar
  14. Bhagooli R, Hidaka M (2004) Photoinhibition, bleaching susceptibility and mortality in two scleractinian corals, Platygyra ryukyuensis and Stylophora pistillata, in response to thermal and light stress. Comp Biochem Physiol A 137:547–555CrossRefGoogle Scholar
  15. Bidle KD, Falkowski PG (2004) Cell death in planktonic, photosynthetic microorganisms. Nat Rev Microbiol 2:643–655CrossRefGoogle Scholar
  16. Black NA, Voellmy R, Szmant AM (1995) Heat shock protein induction in Montastraea faveolata and Aiptasia pallida to elevated temperatures. Biol Bull 188:234–240CrossRefGoogle Scholar
  17. Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim et Biophys Acta (General Subjects) 1760:1690–1695CrossRefGoogle Scholar
  18. Bouchard JN, Yamasaki H (2008) Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: a possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol 49:641–652CrossRefGoogle Scholar
  19. Broadbent AD, Jones GB, Jones RJ (2002) DMSP in corals and benthic algae from the Great Barrier Reef. East Coast Shelf Sci 55:547–555CrossRefGoogle Scholar
  20. Brown BE (1997a) Coral bleaching: causes and consequences. Coral Reefs 16(Suppl):S129–S138CrossRefGoogle Scholar
  21. Brown BE (1997b) Adaptations of reef corals to physical environmental stress. Adv Mar Biol 31:222–299Google Scholar
  22. Brown BE, Dunne RP (2008) Solar radiation modulates bleaching and damage protection in a shallow water coral. Mar Ecol Prog Ser 362:99–107CrossRefGoogle Scholar
  23. Brown BE, Ambarsari I, Warner ME, Fitt WK, Dunne RP, Gibb SW, Cummings DG (1999) Diurnal changes in photochemical efficiency and xanthophylls concentrations in shallow water reef corals: evidence for photoinhibition and photoprotection. Coral Reefs 18:99–105CrossRefGoogle Scholar
  24. Brown BE, Downs CA, Dunne RP, Gibbs SW (2002) Exploring the basis of thermotolerance in the reef coral Goniastrea aspera. Mar Ecol Prog Ser 242:119–129CrossRefGoogle Scholar
  25. Büchell C, Wilhelm C (1993) In vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: progress, problems, and perspectives. Photochem Photobiol 58:137–148CrossRefGoogle Scholar
  26. Carpenter KE, Abrar M, Aeby G et al (2008) One-third of reef building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563CrossRefGoogle Scholar
  27. Castillo KD, Helmuth BST (2005) Influence of thermal history o the response of Montastraea annularis to short-term temperature exposure. Mar Biol 148:261–270CrossRefGoogle Scholar
  28. Cikala M, Wilm B, Hobmayer E, Böttger A, David CN (1999) Identification of caspases and apoptosis in the simple metazoan Hydra. Current Biol 9:959–962CrossRefGoogle Scholar
  29. Coles SL, Brown BE (2003) Coral bleaching-capacity for acclimatization and adaptation. Adv Mar Biol 46:184–223Google Scholar
  30. Crafts-Brandner S, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci U S A 97:13430–13435CrossRefGoogle Scholar
  31. Crawley A, Kline DI, Dunn S, Anthony K, Dove S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora Formosa. Global Change Biol 16:851–863CrossRefGoogle Scholar
  32. Crossland CJ, Barnes DJ (1977) Gas-exchange studies with the staghorn coral Acropora acuminata and its zooxanthellae. Mar Biol 40:185–194CrossRefGoogle Scholar
  33. Császár NBM, Seneca FO, van Oppen MJH (2009) Variation in antioxidant gene expression in the scleractinian coral Acropora millepora under laboratory thermal stress. Mar Ecol Prog Ser 392:93–102CrossRefGoogle Scholar
  34. D’Aoust BG, White R, Wells JM, Olsen DA (1976) Coral-algal association: capacity for producing and sustaining elevated oxygen tensions in situ. Undersea Biomed Res 3:35–40Google Scholar
  35. Desalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, Szmant AM, Medina M (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17:3952–3971CrossRefGoogle Scholar
  36. Donner SD, Knutson TR, Oppenheimer M (2007) Model-based assessment of the role of human-induced climate change in the 2005 Caribbean coral bleaching event. Proc Natl Acad Sci U S A 104:5483–5488CrossRefGoogle Scholar
  37. Douglas AE (2003) Coral bleaching-how and why? Mar Poll Bull 46:385–392CrossRefGoogle Scholar
  38. Dove S (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar Ecol Prog Ser 272:99–116CrossRefGoogle Scholar
  39. Dove S, Ortiz JC, Enríquez S, Fine M, Fisher P, Iglesias-Prieto R, Thornhill D, Hoegh-Guldberg O (2006) Respone of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol Ocenogr 51:1149–1158CrossRefGoogle Scholar
  40. Downs CA, Mueller E, Phillips S, Fauth JE, Woodley CM (2000) A molecular biomarker system for assessing the health of coral (Montastraea faveolata) during heat stress. Mar Biotechnol 2:533–544CrossRefGoogle Scholar
  41. Downs CA, Fauth JE, Halas JC, Dustan P, Bemiss J, Woodley CM (2002) Oxidative stress and seasonal coral bleaching. Free Radic Biol Med 33:533–543CrossRefGoogle Scholar
  42. Dunlap WC, Shick JM, Yamamoto Y (2000) UV protection in marine organisms. I. sunscreens, oxidative stress and sntioxidants. In: Yoshikawa T, Toyokuni S, Yamamoto Y, Naito Y (eds) Free radicals in chemistry, biology and medicine. OICA International, LondonGoogle Scholar
  43. Dunn SR, Bythell JC, Le Tessier DA, Burnett WJ, Thomason JC (2002) Programmed cell death and necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272:29–53CrossRefGoogle Scholar
  44. Dunn SR, Thomason JC, Le Tessier MDA, Bythell JC (2004) Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death Differ 11:1213–1232CrossRefGoogle Scholar
  45. Dunn SR, Phillips WS, Spatafora JW, Green DR, Weis VM (2006) Highly conserved caspase and Bcl-2 homologues from the sea anemone Aiptasia pallida: lower metazoans as models for the study of apoptosis evolution. Mol Evol 63:95–107CrossRefGoogle Scholar
  46. Dunn SR, Philips WS, Green DR, Weis VM (2007a) Knockdown of actin and caspase gene expression by RNA interference in the symbiotic anemone Aiptasia pallida. Biol Bull 212:250–258CrossRefGoogle Scholar
  47. Dunn SR, Schnitzler CE, Weis VM (2007b) Apoptosis and autophagy as mechanisms of dinoflagellate symbiont release during cnidarian bleaching: every which way you lose. Proc R Soc Lond B 274:3079–3085CrossRefGoogle Scholar
  48. Dunne RP (1994) Radiation and coral bleaching. Nature 368:697CrossRefGoogle Scholar
  49. Dunne R, Brown B (2001) The influence of solar radiation on bleaching of shallow water reef corals in the Andaman sea, 1993–1998. Coral Reefs 20:201–210Google Scholar
  50. Dykens JA, Shick JM (1982) Oxygen production by endosymbiotic algae controls superoxide dismutase activity in their animal host. Nature 297:579–580CrossRefGoogle Scholar
  51. Dykens JA, Shick JM, Benoit C, Buettner GR, Winston GW (1992) Oxygen radical production in the sea anemone Anthopleura elegantissima: and its symbiotic algae. J Exp Biol 168:219–241Google Scholar
  52. Edmunds PJ, Gates RD (2008) Acclimatization in tropical reef corals. Mar Ecol Prog Ser 361:307–310CrossRefGoogle Scholar
  53. Enriquéz S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50:1025–1032CrossRefGoogle Scholar
  54. Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845CrossRefGoogle Scholar
  55. Fang L, Huang S, Lin K (1997) High temperature induces the synthesis of heat –shock proteins and the elevation of intracellular calcium in the coral Acropora grandis. Coral Reefs 16:127–131CrossRefGoogle Scholar
  56. Feder ME, Walser J-C (2005) The biological limitations of transcriptomics in elucidating stress and stress responses. J Evol Biol 18:901–910CrossRefGoogle Scholar
  57. Fitt WK, Spero HJ, Halas J, White MW, Porter JW (1993) Recovery of the coral Montastrea annularis in the Florida Keys after the 1987 Caribbean “bleaching event”. Coral Reefs 12:57–64CrossRefGoogle Scholar
  58. Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef corals and relation to coral bleaching. Limnol Oceanogr 45:677–685CrossRefGoogle Scholar
  59. Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65CrossRefGoogle Scholar
  60. Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkar A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo-Pacific corals, Porites cylindrical and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J Exp Mar Biol Ecol 373:102–110CrossRefGoogle Scholar
  61. Flores-Ramírez LA, Liñán-Cabello MA (2007) Relationships among thermal stress, bleaching and oxidative damage in the hermatypic coral, Pocillopora capitata. Com Biochem Physiol C 146:194–202CrossRefGoogle Scholar
  62. Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Prog Ser 272:117–130CrossRefGoogle Scholar
  63. Fridovich I (1998) Oxygen toxicity: a radical explanation. J Exp Biol 201:1203–1209Google Scholar
  64. Gates RD, Edmunds PJ (1999) The physiological mechanisms of acclimatization in tropical reef corals. Am Zool 39:30–43Google Scholar
  65. Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implications for coral bleaching. Biol Bull 182:324–332CrossRefGoogle Scholar
  66. Gleason DF, Wellington GM (1993) Ultraviolet radiation and coral bleaching. Nature 365:836–838CrossRefGoogle Scholar
  67. Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17CrossRefGoogle Scholar
  68. Gniadecki R, Thorn T, Vicanova J, Petersen A, Wulf HC (2000) Role of mitochondria in ultraviolet-induced oxidative stress. J Cell Biochem 80:216–222CrossRefGoogle Scholar
  69. Gorbunov M, Kolber ZS, Lesser MP, Falkowski PG (2001) Photosynthesis and photoprotection in symbiotic corals. Limnol Oceanogr 46:75–85CrossRefGoogle Scholar
  70. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312CrossRefGoogle Scholar
  71. Grottoli AG, Rodrigues LJ, Palardy JE (2007) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189CrossRefGoogle Scholar
  72. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press Inc., New York, p 936Google Scholar
  73. Harriot VJ (1985) Mortality rates of scleractinian corals before and during a mass bleaching event. Mar Ecol Prog Ser 21:81–88CrossRefGoogle Scholar
  74. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770–776CrossRefGoogle Scholar
  75. Hildeman DA, Mitchell T, Aronow B, Wojciechowski S, Kappler J (2003) Control of Bcl-2 expression by reactive oxygen species. Proc Natl Acad Sci U S A 100:15035–15040CrossRefGoogle Scholar
  76. Hill R, Ralph PJ (2005) Diel and seasonal changes in fluorescence rise kinetics of three scleractinian corals. Funct Plant Biol 32:549–559CrossRefGoogle Scholar
  77. Hill R, Ralph PJ (2006) Photosystem II heterogeneity of in hospite zooxanthellae in scleractinian corals exposed to bleaching condition. Photochem Photobiol 82:1577–1585Google Scholar
  78. Hill R, Ralph PJ (2008) Impact of bleaching stress on the function of the oxygen evolving complex of zooxanthellae from scleractinian corals. J Phycol 44:299–310CrossRefGoogle Scholar
  79. Hill R, Ulstrup KE, Ralph PJ (2009) Temperature induced changes in thylakoid membrane thermostability of cultured, freshly isolated, and expelled zooxanthellae from scleractinian corals. Bull Mar Sci 85:223–244Google Scholar
  80. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshwater Res 50:839–866CrossRefGoogle Scholar
  81. Hoegh-Guldberg O, Jones RJ (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183:73–86CrossRefGoogle Scholar
  82. Hoegh-Guldberg O, Smith GJ (1989) 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. J Exp Mar Biol Ecol 129:279–303CrossRefGoogle Scholar
  83. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthinga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742CrossRefGoogle Scholar
  84. Hofmann GE, Burnaford JL, Fielman KT (2005) Genomics-fueled approaches to current challenges in marine ecology. Trends Ecol Evol 20:305–311CrossRefGoogle Scholar
  85. Huang S-P, Lin K-L, Fang L-S (1998) The involvement of calcium in heat-induced coral bleaching. Zool Stud 37:89–94Google Scholar
  86. Hughes T (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551CrossRefGoogle Scholar
  87. Hughes L (2000) Biological consequences of global warming: is the signal already apparent. Trends Ecol Evol 15:56–61CrossRefGoogle Scholar
  88. Hughes TP, Connell JH (1999) Multiple stressors on coral reefs: a long-term perspective. Limnol Oceanogr 44:932–940CrossRefGoogle Scholar
  89. Iglesias-Prieto R, Matta JL, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci U S A 89:10302–10305CrossRefGoogle Scholar
  90. Jamieson D, Chance B, Cadenas E, Boveris A (1986) The relation of free radical production to hyperoxia. Ann Rev Physiol 48:703–719CrossRefGoogle Scholar
  91. Johnson TM, Yu Z, Ferrans VJ, Lowenstein RA, Finkel T (1996) Reactive oxygen species are downstream mediators of p53-dependent apoptosis. Proc Natl Acad Sci U S A 93:11848–11852CrossRefGoogle Scholar
  92. Jokiel PL, Coles SL (1990) Responses of Hawaiian and other Indo-Pacific reef corals to elevated temperatures. Coral Reefs 8:155–162CrossRefGoogle Scholar
  93. Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation, and the relationship to coral bleaching. Plant Cell Environ 24:89–99CrossRefGoogle Scholar
  94. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230CrossRefGoogle Scholar
  95. Jones AM, Berkelmans R, van Oppen MJH, Mioeg JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc R Soc Lond B 275:1359–1365CrossRefGoogle Scholar
  96. Kerswell AP, Jones RJ (2003) Effects of hypo-osmosis on the coral Stylophora pistillata: nature and cause of ‘low-salinity bleaching’. Mar Ecol Prog Ser 253:145–154CrossRefGoogle Scholar
  97. Kinzie RA III (1993) Effects of ambient levels of solar ultraviolet radiation on zooxanthellae and photosynthesis of the reef coral Montipora verrucosa. Mar Biol 116:319–327CrossRefGoogle Scholar
  98. Kleypas JA, Buddemeier RR, Archer D, Gattuso JP, Langdon C, Opdyke BN (1999) Geochemical consequences of increased atmospheric CO2 on corals and coral reefs. Science 284:118–120CrossRefGoogle Scholar
  99. Kramarenko GG, Hummel SG, Martin SM, Buettner GR (2006) Ascorbate reacts with singlet oxygen to produce hydrogen peroxide. Photochem Photobiol 82:1634–1637Google Scholar
  100. Kühl M, Cohen Y, Dalsgaard T, Jørgensen BB, Revsbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH, and light. Mar Ecol Prog Ser 117:159–172CrossRefGoogle Scholar
  101. Leggat W, Hoegh-Guldberg O, Dove S (2007) Analysis of an ESt library from the dinoflagellate (Symbiodiniumi sp.) symbiont of reef-building corals. J Phycol 43:1010–1021CrossRefGoogle Scholar
  102. Lesser MP (1996) Exposure of symbiotic dinoflagellates to elevated temperatures and ultraviolet radiation causes oxidative stress and photosynthesis. Limnol Oceanogr 41:271–283CrossRefGoogle Scholar
  103. Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192CrossRefGoogle Scholar
  104. Lesser MP (2000) Depth-dependent effects of ultraviolet radiation on photosynthesis in the Caribbean coral, Montastraea faveolata. Mar Ecol Prog Ser 192:137–151CrossRefGoogle Scholar
  105. Lesser MP (2004) Experimental coral reef biology. J Exp Mar Biol Ecol 300:217–252CrossRefGoogle Scholar
  106. Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Ann Rev Physiol 68:253–278CrossRefGoogle Scholar
  107. Lesser MP (2007) Coral reef bleaching and global climate change: can coral survive the next century? Proc Natl Acad Sci U S A 104:5259–5260CrossRefGoogle Scholar
  108. Lesser MP, Farrell J (2004) Solar radiation increases the damage to both host tissues and algal symbionts of corals exposed to thermal stress. Coral Reefs 23:367–377CrossRefGoogle Scholar
  109. Lesser MP, Gorbunov MY (2001) Diurnal and bathymetric changes in chlorophyll fluorescence yields of reef corals measured in situ with a fast repetition rate fluorometer. Mar Ecol Prog Ser 212:69–77CrossRefGoogle Scholar
  110. Lesser MP, Lewis S (1996) Action spectrum for the effects of UV radiation on photosynthesis in the hermatypic coral Pocillopora damicornis. Mar Ecol Prog Ser 134:171–177CrossRefGoogle Scholar
  111. Lesser MP, Shick JM (1989) Effects of irradiance and ultraviolet radiation on photoadaptation in the zooxanthellae of Aiptasia pallida: primary production, photoinhibition, and enzymic defenses against oxygen toxicity. Mar Biol 102:243–255CrossRefGoogle Scholar
  112. Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8:225–232CrossRefGoogle Scholar
  113. Lesser MP, Cullen JJ, Neale PJ (1994) Photoinhibition of photosynthesis in the marine diaton Thalassiosira pseudonana during acute exposure to ultraviolet B radiation: relative importance of damage and repair. J Phycol 30:183–192CrossRefGoogle Scholar
  114. Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Invest 115:2679–2688CrossRefGoogle Scholar
  115. Levy O, Achituv Y, Yacobi YZ, Dubinsky Z, Stambler N (2006) Diel ‘tuning” of coral metabolism: physiological responses to light cues. J Exp Biol 209:273–283CrossRefGoogle Scholar
  116. Liu K, Sun J, Song Y, Liu B, Xu Y, Zhang S, Tian Q, Liu Y (2004) Superoxide, hydrogen peroxide, and hydroxyl radical in D1/D2/cytochrome b-559 photosystem II reaction center complex. Photosynth Res 81:41–47CrossRefGoogle Scholar
  117. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Ann Rev Plant Physiol Mol Biol 45:633–662CrossRefGoogle Scholar
  118. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131CrossRefGoogle Scholar
  119. Lum JJ, DeBerardinis RJ, Thompson CB (2005) Autophagy in metazoans: cell survival in the land of plenty. Nat Rev Mol Cell Biol 6:439–448CrossRefGoogle Scholar
  120. Macpherson AN, Telfer A, Barber J, Truscott GT (1993) Direct detection of singlet oxygen from isolated photosystem II reaction centers. Biochim Biophys Acta 1143:301–309CrossRefGoogle Scholar
  121. Marla SS, Lee J, Groves JT (1997) Peroxynitrite rapidly permeates phopholipid membranes. Proc Natl Acad Sci U S A 94:14243–14248CrossRefGoogle Scholar
  122. Martindale JL, Holbrook NJ (2002) Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol 192:1–15CrossRefGoogle Scholar
  123. Matta JL, Govind NS, Trench RK (1992) Polyclonal antibodies against iron-superoxide dismutase from Escherichia coli B cross react with superoxide dismutases from Symbiodinium microadriaticum (Dinophyceae). J Phycol 28:343–346CrossRefGoogle Scholar
  124. Mayfield AB, Gates RD (2007) Osmoregulation and osmotic stress in coral dinoflagellate symbiosis: role in coral bleaching. Comp Biochem Physiol A 147:1–10Google Scholar
  125. Maynard JA, Anthony KRN, Marshall PA, Masiri I (2008) Major bleaching events can lead to increased thermal tolerance in corals. Mar Biol 155:173–182CrossRefGoogle Scholar
  126. Mazel C, Lesser MP, Gorbunov M, Barry T, Farrell J, Wyman K, Falkowski PG (2003) Green fluorescent proteins in Caribbean corals. Limnol Oceanogr 48:402–411CrossRefGoogle Scholar
  127. Middlebrook R, Hoegh-Guldberg O, Leggat W (2008) The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J Exp Biol 211:1050–1056CrossRefGoogle Scholar
  128. Morrall CE, Galloway TS, Trapido-Rosenthal HG, Depledge MH (2000) Characterization of nitric oxide synthase activity in the tropical sea anemone Aiptasia pallida. Comp Biochem Physiol B 125:483–491CrossRefGoogle Scholar
  129. Murata N, Takahashi S, Nishyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421CrossRefGoogle Scholar
  130. Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition. I. δ13C of zooxanthellae and animal tissue vs depth. Mar Biol 100:185–193CrossRefGoogle Scholar
  131. Nakamura T, van Woesik R (2001) Water-flow rates and passive diffusion partially explain differential survival of corals during the 1998 bleaching event. Mar Ecol Prog Ser 212:301–304CrossRefGoogle Scholar
  132. Nii CM, Muscatine L (1997) Oxidative stress in the symbiotic sea anemone Aiptasia pulchella (Calgren, 1943): contribution of the animal to superoxide ion production at elevated temperature. Biol Bull 192:444–456CrossRefGoogle Scholar
  133. Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587–5594CrossRefGoogle Scholar
  134. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749CrossRefGoogle Scholar
  135. Niyogi KK (1999) Photoprotection revisted: genetic and molecular approaches. Ann Rev Plant Physiol Plant Mol Biol 50:333–359CrossRefGoogle Scholar
  136. Palmer CV, Modi CK, Mydlarz LD (2009) Coral fluorescent proteins as antioxidants. PLoS ONE 4:e7298CrossRefGoogle Scholar
  137. Peltier G, Cournac L (2002) Chororespiration. Ann Rev Plant Biol 53:523–550CrossRefGoogle Scholar
  138. Perez S, Weis V (2006) Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. J Exp Biol 209:2804–2810CrossRefGoogle Scholar
  139. Perez S, Weis V (2008) Cyclophyllin and the regulation of symbiosis in Aiptasia pallida. Biol Bull 215:63–72CrossRefGoogle Scholar
  140. Plantivaux A, Furla P, Zoccola D, Garello G, Forcioli D, Richier S, Merle P-L, Tambutté S, Alemand D (2004) Molecular characterization of two CuZn-superoxide dismutases in a sea anemone. Free Radic Biol Med 37:1170–1181CrossRefGoogle Scholar
  141. Pourzand C, Tyrell RM (1999) Apoptosis, the role of oxidative stress and the example of solar UV radiation. Photochem Photobiol 70:380–390CrossRefGoogle Scholar
  142. Rands ML, Douglas AE, Loughman BC, Ratcliff RG (1992) Avoidance of hypoxia in a cnidarian symbiosis by algal photosynthetic oxygen. Biol Bull 182:159–162CrossRefGoogle Scholar
  143. Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci U S A 105:13674–13678CrossRefGoogle Scholar
  144. Rich T, Allen RL, Wyllie AH (2000) Defying death after DNA damage. Nature 407:777–783CrossRefGoogle Scholar
  145. Richier S, Sabourault C, Courtiade J, Zucchini N, Allemand D, Furla P (2006) Oxidative stress and apoptotic events in the symbiotic sea anemone, Anemonia viridis. FEBS J 273:4186–4198CrossRefGoogle Scholar
  146. Richier S, Rodriguez-Lanetty M, Schnitzler CE, Weis VM (2008) Response of the symbiotic cnidarian Anthopleura elegantissima transcriptome to temperature and UV increase. Comp Biochem Physiol D 3:283–289Google Scholar
  147. Richter M, Rüle W, Wild A (1990) Studies on the mechanism of photosystem II photoinhibition II. The involvement of toxic oxygen species. Photosynth Res 24:237–243CrossRefGoogle Scholar
  148. Rong Y, Distelhorst CW (2008) Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival. Ann Rev Physiol 70:73–91CrossRefGoogle Scholar
  149. Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci U S A 105:10444–10449CrossRefGoogle Scholar
  150. Sandeman I (2006) Fragmentation of the gastrodermis and detachment of zooxanthellae in symbiotic cnidarians: a role for hydrogen peroxide and Ca2+ in coral bleaching and algal density control. Rev Biol Trop (Int J Trop Biol) 54:79–96Google Scholar
  151. Saragosti E, Tchernov D, Katsir A, Shaked Y (2010) Extracellular production and degradation of superoxide in the coral Stylophora pistillata and cultured Symbiodinium. PLoS ONE 9:e12508Google Scholar
  152. Sawyer SJ, Muscatine L (2001) Cellular mechanisms underlying temperature-induced bleaching in the tropical sea anemone Aiptasia pulchella. J Exp Biol 204:3443–3456Google Scholar
  153. Segovia M, Haramaty L, Berges JA, Falkowski PG (2003) Cell death in the unicellular chlorophyte Dunaliella tertiolecta. A hypothesis on the evolution of apoptosis in higher plants and metazoans. Plant Physiol 132:99–105CrossRefGoogle Scholar
  154. Sharp VA, Brown BE, Miller D (1997) Heat shock protein (HSP 70) expression in the tropical reef coral Goniopora djiboutiensis. J Therm Biol 22:11–19CrossRefGoogle Scholar
  155. Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461CrossRefGoogle Scholar
  156. Sheppard CRC (2003) Predicted recurrences of mass coral mortality in the Indian Ocean. Nature 425:294–297CrossRefGoogle Scholar
  157. Shick JM (1990) Diffusion limitation and hyperoxic enhancement of oxygen consumption in zooxanthellate sea anemones, zoanthids, and corals. Biol Bull 179:148–158CrossRefGoogle Scholar
  158. Shick JM, Lesser MP, Jokiel P (1996) Effects of ultraviolet radiation on corals and other coral reef organisms. Global Change Biol 2:527–545CrossRefGoogle Scholar
  159. Smith DJ, Suggett DJ, Baker NR (2005) Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals? Global Change Biol 11:1–11CrossRefGoogle Scholar
  160. Smith-Keune C, Dove S (2008) Gene expression of a green fluorescent protein homolog as a host-specific biomarker of heat stress within a reef-building coral. Mar Biotechnol 10:166–180CrossRefGoogle Scholar
  161. Somero GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integr Comp Biol 42:780–789CrossRefGoogle Scholar
  162. Sotka EE, Thacker RW (2005) Do some corals like it hot? Trends Ecol Evol 20:59–62CrossRefGoogle Scholar
  163. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker NR (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956CrossRefGoogle Scholar
  164. Sunda W, Kleber DJ, Klene RP, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320CrossRefGoogle Scholar
  165. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition. Trends Plant Sci 13:178–182CrossRefGoogle Scholar
  166. Takahashi S, Nakamura T, Sakamizu M, van Woesik R, Yamasaki H (2004) Repair machinery of symbiotic photosynthesis as the primary target of heat stress for reef-building corals. Plant Cell Physiol 45:251–255CrossRefGoogle Scholar
  167. Takahashi S, Whitney S, Itoh S, Maruyama T, Badger M (2008) Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured Symbiodinium. Proc Natl Acad Sci U S A 105:4203–4208CrossRefGoogle Scholar
  168. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Häggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci U S A 101:13531–13535CrossRefGoogle Scholar
  169. Trapido-Rosenthal H, Zielke S, Owen R, Buxton L, Boeing B, Bhagooli R, Archer J (2005) Increased zooxanthellae nitric oxide synthase activity is associated with coral bleaching. Biol Bull 208:3–6CrossRefGoogle Scholar
  170. Vincent WF (1980) Mechanisms of rapid photosynthetic adaptation in natural phytoplankton communities. 2. Changes in photochemical capacity as measured by DCMU-induced chlorophyll fluorescence. J Phycol 20:201–211CrossRefGoogle Scholar
  171. Warner ME, Berry-Lowe S (2006) Xanthophyll cycling and photochemical activity in symbiotic dinoflgellates in multiple locations of three species of Caribbean coral. J Exp Mar Biol Ecol 339:86–95CrossRefGoogle Scholar
  172. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci U S A 96:8007–80012CrossRefGoogle Scholar
  173. Warner ME, Chilcoat GC, McFarland FK, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates in the Caribbean reef-building coral Montastraea. Mar Biol 141:31–38CrossRefGoogle Scholar
  174. Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066CrossRefGoogle Scholar
  175. Weis VM, Davy SK, Hoegh-Guldber O, Rodriguez-Lanetty M, Pringle JR (2008) Cell Biology in model systems as the key to understanding corals. Trends Ecol Evol 23:369–376CrossRefGoogle Scholar
  176. Wilkinson CR (1999) Global and local threats to coral reef functioning and existence: review and predictions. Mar Freshwater Res 50:867–878Google Scholar
  177. Williams EH Jr, Bunkley-Williams L (1990) The world-wide coral reef bleaching cycle and related sources of coral mortality. Atoll Res Bull 335:1–67Google Scholar
  178. Yonge CM, Nichols AG (1931) The structure, distribution and physiology of the zooxanthellae. (Studies on the Physiology of Corals IV). Sci Rep Great Barrier Reef Exped 1928–29 1:135–176Google Scholar

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© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Molecular, Cellular and Biomedical SciencesUniversity of New HampshireDurhamUSA

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