Coral Reefs

, Volume 12, Issue 1, pp 1–17 | Cite as

Coral reef bleaching: ecological perspectives

  • P. W. Glynn


Coral reef bleaching, the whitening of diverse invertebrate taxa, results from the loss of symbiotic zooxanthellae and/or a reduction in photosynthetic pigment concentrations in zooxanthellae residing within the gastrodermal tissues of host animals. Of particular concern are the consequences of bleaching of large numbers of reef-building scleractinian corals and hydrocorals. Published records of coral reef bleaching events from 1870 to the present suggest that the frequency (60 major events from 1979 to 1990), scale (co-occurrence in many coral reef regions and often over the bathymetric depth range of corals) and severity (>95% mortality in some areas) of recent bleaching disturbances are unprecedented in the scientific literature. The causes of small scale, isolated bleaching events can often be explained by particular stressors (e.g., temperature, salinity, light, sedimentation, aerial exposure and pollutants), but attempts to explain large scale bleaching events in terms of possible global change (e.g., greenhouse warming, increased UV radiation flux, deteriorating ecosystem health, or some combination of the above) have not been convincing. Attempts to relate the severity and extent of large scale coral reef bleaching events to particular causes have been hampered by a lack of (a) standardized methods to assess bleaching and (b) continuous, long-term data bases of environmental conditions over the periods of interest. An effort must be made to understand the impact of bleaching on the remainder of the reef community and the long-term effects on competition, predation, symbioses, bioerosion and substrate condition, all factors that can influence coral recruitment and reef recovery. If projected rates of sea warming are realized by mid to late AD 2000, i.e. a 2°C increase in high latitude coral seas, the upper thermal tolerance limits of many reef-building corals could be exceeded. Present evidence suggests that many corals would be unable to adapt physiologically or genetically to such marked and rapid temperature increases.


Coral Reef Bleaching Event Coral Recruitment Symbiotic Zooxanthella Photosynthetic Pigment Concentration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andrews JC, Pickard GL (1990) The physical oceanography of coral-reef systems. In: Dubinsky Z (ed) Coral reefs, ecosystems of the world 25. Elsevier, Amsterdam, pp 11–48Google Scholar
  2. Atwood DK, Sylvester JC, Corredor JE, Morell JM, Mendez A, Nodal WJ, Huss BE, Foltz C (1988) Sea surface temperature anomalies for the Caribbean, Gulf of Mexico, Florida reef tract and the Bahamas considered in light of the 1987 regional coral bleaching event. Proc Assoc Mar Lab Caribbean 21:47Google Scholar
  3. Atwood DK, Hendee JC (in press) An assessment of global warming stress on Caribbean coral reef ecosystems. Proc Gulf Carib Fish Inst 44Google Scholar
  4. Ayre DJ, Willis BL (1988) Population structure in the coral Pavona cactus: clonal genotypes show little phenotypic plasticity. Mar Biol 99:495–505Google Scholar
  5. Babcock RC (1991) Comparative demography of three species of sclearactinian corals using age- and size-dependent classifications. Ecol Monogr 61:225–244Google Scholar
  6. Birkeland C (1988) Second-order ecological effects of nutrient input into coral communities. Galaxea 7:91–100Google Scholar
  7. Birkeland C, Lucas JS (1990) Acanthaster planci: major management problem of coral reefs. CRC, Boca Raton, Fla, p 257Google Scholar
  8. Blank RJ (1987) Evolutionary differentiation in gymnodinoid zooxanthellae. Ann N Y Acad Sci 503:530–533Google Scholar
  9. Blank RJ, Trench RK (1985) Speciation and symbiotic dinoflagellates. Science 229:656–658Google Scholar
  10. Blaustein AR, Wake DB (1990) Declining amphibian populations: a global phenomenon? Trends Ecol Evol 5:203–204Google Scholar
  11. Blumthaler M, Ambach W (1990) Indication of increasing solar UV-B radiation and flux in Alpine regions. Science 248:206–208Google Scholar
  12. Bottomley M, Folland CK, Hsiung J, Newell RE, Parker DE (1990) Global ocean surface temperature atlas. Massachusetts Institute of Technology Press, Cambridge, Mass, p 337Google Scholar
  13. Brongersma-Sanders M (1957) Mass mortality in the sea. In: Hedgpeth JW (ed) Treatise on marine ecology and paleoecology, vol 1: Ecology. Geol Soc Am Mem 67. Waverly, Baltimore, Md, pp 941–1,010Google Scholar
  14. Brown BE (1987) Worldwide death of corals-natural cyclical events or man-made pollution? Mar Poll Bull 18:9–13Google Scholar
  15. Brown BE, Howard LS (1985) Assessing the effects of “stress” on reef corals. Adv Mar Biol 22:1–63Google Scholar
  16. Brown BE, Suharsono (1990) Damage and recovery of coral reefs affected by El Niño related seawater warming in the Thousand Islands, Indonesia. Coral Reefs 8:163–170Google Scholar
  17. Bryan PG (1973) Growth rate, toxicity and distribution of the encrusting sponge Terpios sp. (Hadromerida: Suberitidae) in Guam, Mariana Islands. Micronesica 9:237–242Google Scholar
  18. Buddemeier RW, Hopley D (1988) Turn-ons and turn-offs: causes and mechanisms of the initiation and termination of coral reef growth. Proc 6th Int Coral Reef Symp 1:253–261Google Scholar
  19. Buddemeier RW, Smith SV (1988) Coral reef growth in an era of rapidly rising sea level: predictions and suggestions for long-tern research. Coral Reefs 7:51–56Google Scholar
  20. Bunkley-Williams L, Morelock J, Williams EH Jr (1991) Lingering effects of the 1987 mass bleaching on Puerto Rican coral reefs in mid to late 1988. J Aquat Anim Health 3:242–247Google Scholar
  21. Causey BD (1988) Observations of environmental conditions preceding the coral bleaching event of 1987-Looe Key National Marine Sanctuary. Proc Assoc Is Mar Labs Carib 21:48Google Scholar
  22. Clausen CD, Roth AA (1975) Effect of temperature and temperature adaptation on calcification rate in the hermatypic coral Pocillopora damicornis. Mar Biol 33:93–100Google Scholar
  23. Coffroth MA, Lasker HR, Oliver JK (1990) Coral mortality outside of the eastern Pacific during 1982–1983: relationship to El Niño. In: Glynn PW (ed) Global ecological consequences of the 1982–83 El Niño-Southern Oscillation. Elsevier, Amsterdam, pp 141–182Google Scholar
  24. Coles SL (1988) Limitations on reef coral development in the Arabian Gulf: temperature or algal competition? Proc 6th Int Coral Reef Symp 3:211–216Google Scholar
  25. Coles SL, Jokiel PL (1977) Effects of temperature on photosynthesis and respiration in hermatypic corals. Mar Biol 43:209–216Google Scholar
  26. Coles SL, Jokiel PL (1978) Synergistic effects of temperature, salinity and light on the hermatypic coral Montipora verrucosa. Mar Biol 49:187–195Google Scholar
  27. Coles SL, Jokiel PL, Lewis CR (1976) Thermal tolerance in tropical versus subtropical Pacific reef corals. Pac Sci 30:159–166Google Scholar
  28. Colgan MW (1987) Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster. Ecology 68:1592–1605Google Scholar
  29. Colin PL (1980) A brief history of the Tortugas Marine Laboratory and the Department of Marine Biology, Carnegie Institution of Washington. In: Sears M, Merriman D (eds) Oceanography, the past. Springer, Berlin Heidelberg New York, pp 138–147Google Scholar
  30. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310Google Scholar
  31. Cortes J (1990) The coral reefs of Golfo Dulce, Costa Rica: distribution and community structure. Atoll Res Bull 344:1–37Google Scholar
  32. Cortes J, Risk MJ (1984) El arrecife coralino del Parque Nacional Cahuita, Costa Rica. Rev Biol Trop 32:109–121Google Scholar
  33. Cortes J, Murillo MM, Guzman HM, Acuña J (1984) Perdida de zooxantelas y muerte de corales y otros organismos arrecifales en el Caribe y Pacifico de Costa Rica. Rev Biol Trop 32:227–231Google Scholar
  34. Crowley TJ, North GR (1991) Paleoclimatology. Oxford University Press, New York, p 339Google Scholar
  35. Dawydoff MC (1952) Contribution a l'etude des invertebres de la faune marine benthique de l'Indochine. Bull Biol Fr Belg 37:1–158Google Scholar
  36. D'Elia CF, Webb KL, Porter JW (1981) Nitrate-rich groundwater inputs to Discovery Bay, Jamaica: a significant source of N to local reefs? Bull Mar Sci 31:903–910Google Scholar
  37. D'Elia CF, Buddemeier RW, Smith SV (1991) Workshop on coral bleaching, coral reef ecosystems and global change: report of proceedings. Maryland Sea Grant College Pub, College Park, Md, pp 1–49Google Scholar
  38. Done TJ, Dayton PK, Dayton AE, Steger R (1991) Regional and local variability in recovery of shallow coral communities: Moorea, French Polynesia and central Great Barrier Reef. Coral Reefs 9:183–192Google Scholar
  39. Dunlap WC, Chalker BE (1986) Identification and quantification of near-UV absorbing compounds (S-320) in a hermatypic scleractinian. Coral Reefs 5:155–159Google Scholar
  40. Dunlap WC, Chalker BE, Oliver JK (1986) Bathymetric adaptations of reef-building corals at Davies Reef, Great Barrier Reef, Australia. III. UV-B absorbing compounds. J Exp Mar Biol Ecol 104:239–248Google Scholar
  41. Eakin CM (1991) The damselfish-algal lawn symbiosis and its influence on the bioerosion of an El Niño impacted coral reef. Uva Island, Pacific Panama. Ph D dissertation, University of Miami, Coral Gables, Fla, pp 1–158Google Scholar
  42. Emiliani C, Kraus EB, Shoemaker EM (1981) Sudden death at the end of the Mesozoic. Earth Planet Sci Lett 55:317–334Google Scholar
  43. Endean R (1976) Destruction and recovery of coral reef communities. In: Jones OA, Endean R (eds) Biology and geology of coral reefs 3, Biology 2. Academic Press, New York, pp 215–254Google Scholar
  44. Endean R, Stablum W (1973) The apparent extent of recovery of reefs of Australia's Great Barrier Reef devastated by the crownof-thorns starfish (Acanthaster planci). Atoll Res Bull 168:1–26Google Scholar
  45. Endean R, Cameron AM (1990) Acanthaster planci population outbreaks. In: Dubinsky Z (ed) Coral reefs, ecosystems of the world 25. Elsevier, Amsterdam, pp 419–437Google Scholar
  46. Fagerstrom JA (1987) The evolution of reef communities. Wiley, New York, p 600Google Scholar
  47. Falkowski PG, Jokiel PL, Kinzie RA III (1990) Irradiance and corals. In: Dubinsky Z (ed) Coral reefs, ecosystems of the world 25. Elsevier, Amsterdam, pp 89–107Google Scholar
  48. FAO (1986) Report of the expert consultation on ulcerative fish diseases in the Asia-Pacific region. FAO, Reg Off Asia and Pacific, Bangkok, DOC. FAO/TCP/RAS/4508, p 38Google Scholar
  49. Fischer AG, Arthur MA (1977) Secular variations in the pelagic realm. In: Cook HE, Enos P (eds) Deep water carbonate environments. Soc Econ Paleontol Mineral Spec Publ 25:19–50Google Scholar
  50. Fishelson L (1973) Ecological and biological phenomena influencing coral species composition on the reef tables at Eilat (Gulf of Aqaba, Red Sea). Mar Biol 19:183–196Google Scholar
  51. Fisk D, Done T (1985) Taxonomic and bathymetric patterns of bleaching in corals, Myrmidon Reef (Queensland). Proc 5th Int Coral Reef Symp 6:149–154Google Scholar
  52. Fleischmann EM (1989) The measurement and penetration of ultraviolet radiation into tropical marine water. Limnol Oceanogr 34:1623–1629Google Scholar
  53. Folland CK, Karl TR, Vinnikov KYA (1990) Observed climate variations and change. In: Houghton JT, Jenkins GJ, Ephraums JJ (eds) Climate change, the IPCC scientific assessment. Cambridge University Press, Cambridge, pp 195–238Google Scholar
  54. Frederick JE, Lubin D (1988) Possible long-term changes in biologically active ultraviolet radiation reaching the ground. Photochem Photobiol 47:571–578Google Scholar
  55. Frost SH (1977) Miocene to Holocene evolution of Caribbean province reef-building corals. Proc 3rd Int Coral Reef Symp 2:353–359Google Scholar
  56. Gates RD (1990) Seawater temperature and sublethal coral bleaching in Jamaica. Coral Reefs 8:193–197Google Scholar
  57. Ghiold J, Smith SH (1990) Bleaching and recovery of deep-water, reef-dwelling invertebrates in the Cayman Islands, BWI. Caribb J Sci 26:52–61Google Scholar
  58. Gilmartin M, Revelante N (1974) The “island mass” effect on the phytoplankton and primary production of the Hawaiian Islands. J Exp Mar Biol Ecol 16:181–204Google Scholar
  59. Glynn PW (1976) Some physical and biological determinants of coral community structure in the eastern Pacific. Ecol Monogr 46:431–456Google Scholar
  60. Glynn PW (1984) Widespread coral mortality and the 1982/83 El Niño warming event. Environ Conserv 11:133–146Google Scholar
  61. Glynn PW (1985a) Corallivore population sizes and feeding effects following El Niño (1982–1983) associated coral mortality in Panama. Proc 5th Int Coral Reef Symp 4:183–188Google Scholar
  62. Glynn PW (1985b) El Niño-associated disturbance to coral reefs and post disturbance mortality by Acanthaster planci. Mar Ecol Prog Ser 26:295–300Google Scholar
  63. Glynn PW (1988a) Coral bleaching and mortality in the tropical eastern Pacific during the 1982–83 El Niño warming event. In: Ogden J, Wicklund R (eds) Mass bleaching of coral reefs in the Caribbean: a research strategy. NOAA's Undersea Res Prog, St Croix, US Virgin Islands, Res Rpt 88-2:42–45Google Scholar
  64. Glynn PW (1988b) El Niño-Southern Oscillation 1982–1983: nearshore population, community, and ecosystem responses. Ann Rev Ecol Syst 19:309–345Google Scholar
  65. Glynn PW (1988c) El Niño warming, coral mortality and reef framework destruction by echinoid bioerosion in the eastern Pacific. Galaxea 7:129–160Google Scholar
  66. Glynn PW (1990) Coral mortality and disturbances to coral reefs in the tropical eastern Pacific. In: Glynn PW (ed) Global ecological consequences of the 1982–83 El Niño-Southern Oscillation. Elsevier, Amsterdam, pp 55–126Google Scholar
  67. Glynn PW (1991) Coral reef bleaching in the 1980s and possible connections with global warming. Trends Ecol Evol 6:175–179Google Scholar
  68. Glynn PW, D'Croz L (1990) Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8:181–191Google Scholar
  69. Glynn PW, Weerdt WH de (1991) Elimination of two reef-building hydrocorals following the 1982–83 El Niño warming event. Science 253:69–71Google Scholar
  70. Glynn PW, Stewart RH (1973) Distribution of coral reefs in the Pearl Islands (Gulf of Panama) in relation to thermal conditions. Limnol Oceanogr 18:367–379Google Scholar
  71. Glynn PW, Perez M, Gilchrist SL (1985a) Lipid decline in stressed corals and their crustacean symbionts. Biol Bull 168:276–284Google Scholar
  72. Glynn PW, Peters EC, Muscatine L (1985b) Coral tissue microstructure and necrosis: relation to catastrophic coral mortality in Panama. Dis Aquat Org 1:29–37Google Scholar
  73. Glynn PW, Cortes J, Guzman HM, Richmond RH (1988) El Niño (1982–83) associated coral mortality and relationship to sea surface temperature deviations in the tropical eastern Pacific. Proc 6th Int Coral Reef Symp 3:237–243Google Scholar
  74. Goreau TF (1959) The ecology of Jamaican coral reefs 1. Species composition and zonation. Ecology 40:67–90Google Scholar
  75. Goreau TF (1964) Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane Flora. Science 145:383–386Google Scholar
  76. Goreau TJ, Macfarlane AH (1990) Reduced growth rate of Montastrea annularis following the 1987–1988 coral-bleaching event. Coral Reefs 8:211–215Google Scholar
  77. Goreau TJ, Hayes RL, Clark JW, Basta DJ, Robertson CN (in press) Elevated sea surface temperatures correlate with Caribbean coral reef bleaching. In: Geyer RA (ed) A global warming forum: scientific, economic, and legal overview, vol II, chap 4. CRC Press, Boca Raton, FloridaGoogle Scholar
  78. Grigg RW (1982) Darwin point: a threshold for atoll formation. Coral Reefs 1:29–34Google Scholar
  79. Grigg RW (1983) Community structure, succession and development of coral reefs in Hawaii. Mar Ecol Prog Ser 11:1–14Google Scholar
  80. Grigg RW, Maragos JE (1974) Recolonization of hermatypic corals on submerged lave flows in Hawaii. Ecology 55:387–395Google Scholar
  81. Grigg RW, Epp D (1989) Critical depth for the survival of coral islands: effects on the Hawaiian archipelago. Science 243:638–641Google Scholar
  82. Grigg RW, Dollar SJ (1990) Natural and anthropogenic disturbance on coral reefs. In: Dubinsky Z (ed) Coral reefs, ecosystems of the world 25. Elsevier, Amsterdam, pp 439–452Google Scholar
  83. Guzman HM, Cortes J (in press) Cocos Island (Pacific of Costa Rica) coral reefs after the 1982–83 El Niño disturbance. Rev Biol TropGoogle Scholar
  84. Guzman HM, Cortes J, Glynn PW, Richmond RH (1990) Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Mar Ecol Prog Ser 60:299–303Google Scholar
  85. Hallock P, Schlager W (1986) Nutrient excess and the demise of coral reefs and carbonate platforms. Palaios 1:389–398Google Scholar
  86. Hansen J, Lebedeff S (1987) Global trends of measured surface air temperature. J Geophys Res 92:13345–13372Google Scholar
  87. Harmelin-Vivien ML, Laboute P (1986) Catastrophic impact of hurricanes on atoll outer reef slopes in the Tuamotu (French Polynesia). Coral Reefs 5:55–62Google Scholar
  88. Harriott VJ (1985) Mortality rates of scleractinian corals before and during a mass bleaching event. Mar Ecol Prog Ser 21:81–88Google Scholar
  89. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Coral reefs, ecosystems of the world 25. Elservier, Amsterdam, pp 133–207Google Scholar
  90. Hatai S (1937) The Palao Tropical Biological Station. Palao Trop Biol Sta Stud 1:1–15Google Scholar
  91. Hay ME (1984) Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical? Ecology 65:446–454Google Scholar
  92. Hayes RL, Bush PG (1990) Microscopic observations of recovery in the reef-building scleractinian coral, Montastrea annularis, after bleaching on a Cayman reef. Coral Reefs 8:203–209Google Scholar
  93. Highsmith RC (1980) Geographic patterns of coral bioerosion: a productivity hypothesis. J Exp Mar Biol Ecol 46:177–196Google Scholar
  94. Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226Google Scholar
  95. Hoegh-Guldberg O, Smith GJ (1989) Light, salimity, and temperature and the population density, metabolism and export of zooxanthellae from Stylophora pistillata and Seriatopora hystrix. J Exp Mar Biol Ecol 129:279–303Google Scholar
  96. Hoeksema BW (1991) Control of bleaching in mushroom coral populations (Scleractinia: Fungiidae) in the Java Sea: stress tolerance and interference by life history strategy. Mar Ecol Prog Ser 74:225–237Google Scholar
  97. Hoffman JS, Keyes D, Titus JG (1983) Projecting future sea level rise: methodology, estimates to the year 2100, and research needs. Strategic Studies Staff, US Environmental Protection Agency, Washington, DCGoogle Scholar
  98. Hopley D, Kinsey DW (1988) The effects of rapid short-term sea-level rise on the Great Barrier Reef. In: Pearman GI (ed) Greenhouse, planning for climate change. Brill, Leiden, pp 189–201Google Scholar
  99. Houghton JT, Jenkins GJ, Ephraums JJ (eds) (1990) Climate change, the IPCC scientific assessment. Cambridge University Press, Cambridge, Mass, p 365Google Scholar
  100. Hudson JH (1981) Response of Montastrea annularis to environmental change in the Florida Keys. Proc 4th Int Coral Reef Symp 2:233–240Google Scholar
  101. Hughes TP (1985) Life histories and population dynamics of early successional corals. Proc 5th Int Coral Reef Symp 4:101–106Google Scholar
  102. Hughes TP (1989) Community structure and diversity of coral reefs: the role of history. Ecology 70:275–279Google Scholar
  103. Hughes TP, Jackson JBC (1985) Population dynamics and life histories of foliaceous corals. Ecol Monogr 55:141–166Google Scholar
  104. Hughes TP, Reed DC, Boyle M-J (1987) Herbivory on coral reefs: community structure following mass mortalities of sea urchins. J Exp Mar Biol Ecol 113:39–59Google Scholar
  105. Hunter CL (1985) Assessment of clonal diversity and population structure of Porites compressa (Cnidaria, Scleractinia). Proc 5th Int Coral Reef Symp 6:69–74Google Scholar
  106. IUCN Bull (1990) Hot news from the Gulf. 21:9Google Scholar
  107. Jaap WC (1988) The 1987 zooxanthellac expulsion event at Florida reefs. NOAA's Undersea Res Prog Res Rpt 88-2:24–29Google Scholar
  108. Jablonski D (1991) Extinctions: a paleontological perspective. Science 253:754–757Google Scholar
  109. Jackson JBC, Cubit JD, Keller BD, Batista V, Burns K, Caffey HM, Caldwell RL, Garrity SD, Getter CD, Gonzalez C, Guzman HM, Kaufmann KW, Knap AH, Levings SC, Marshall MJ, Steger RS, Thompson RC, Weil E (1989) Ecological effects of a major oil spill on Panamanian coastal marine communities. Science 243:37–44Google Scholar
  110. Jaenike J (1991) Mass extinction of European fungi. Trends Ecol Evol 6:174–175Google Scholar
  111. Jerlov NG (1968) Optical oceanography. Elsevier, Amsterdam, p 194Google Scholar
  112. Johannes RE (1975) Pollution and degradation of coral reef communities. In: Ferguson Wood EJ, Johannes RE (eds) Tropical marine pollution. Elsevier Oceanogr Ser 12:13–51Google Scholar
  113. Jokiel PL (1980) Solar ultraviolet radiation and coral reef epifauna. Science 207:1069–1071Google Scholar
  114. Jokiel PL (1988) Is photoadaptation a critical process in the developmentm function and maintenance of reef communities? Proc 6th Int Coral Reef Symp 1:187–192Google Scholar
  115. Jokiel PL, Guinther EB (1978) Effects of temperature on reproduction in the hermatypic coral Pocillopora damicornis. Bull Mar Sci 28:786–789Google Scholar
  116. Jokiel PL, York RH (1982) Solar ultraviolet photobiology of the reef coral Pocillopora damicornis and symbiotic zooxanthellae. Bull Mar Sci 32:301–315Google Scholar
  117. Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155–162Google Scholar
  118. Kerr RA (1988) The weather in the wake of El Niño. Science 239:883Google Scholar
  119. Kleppel GS, Dodge RE, Reese CJ (1989) Changes in pigmentation associated with the bleaching of stony corals. Limnol Oceanogr 34:1331–1335Google Scholar
  120. Knowlton N, Lang JC, Keller BD (1990) Case study of natural population collapse: post-hurricane predation on Jamaican staghorn corals. Smithson Contrib Mar Sci 31:1–25Google Scholar
  121. Knowlton N, Weil E, Weigt LA, Guzman HM (1992) Sibling species in Montastraea annularis, coral bleaching, and the coral climate record. Science 255:330–333Google Scholar
  122. Kojis BL, Quinn NJ (1985) Puberty in Goniastrea favulus. Age or size limited? Proc 5th Int Coral Reef Symp 4:289–293Google Scholar
  123. Lamberts AE (1983) Coral kill and recolonization in American Samoa. Nat Geogr Soc Res Rep 15:359–377Google Scholar
  124. Jang JC (1988) Apparent differences in bleaching responses by zooxanthellate cnidarians on Colombian and Bahamian reefs. NOAA's Undersea Res Prog. Res Rpt 88-2:30–32Google Scholar
  125. Jang JC, Smith RC, Muller-Karger F (in press) Sea surface temperatures and coral bleaching in the tropical western Atlantic: 1979–1990. Proc Assoc Is Mar Labs Carib 24Google Scholar
  126. 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 102:243–255Google Scholar
  127. Lesser MP, Shick JM (1990) Effects of visible and ultraviolet radiation on the ultrastructure of zooxanthellae (Symbiodinium sp.) in culture and in sity. Cell Tissue Res 261:501–508Google Scholar
  128. Lesser MP, Stochaj WR, Tapley DW, Shick JM (1990) Physiological mechanisms of bleaching in coral reef anthozoans: effects of irradiance, ultraviolet radiation, and temperature on the activities of protective enzymes against active oxygen. Coral Reefs 8:225–232Google Scholar
  129. Lessios HA, Robertson DR, Cubit JD (1984) Spread of Diadema mass mortality through the Caribbean. Science 226:335–337Google Scholar
  130. Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Monogr 56:183–200Google Scholar
  131. Loya Y (1976) Recolonization of Red Sea corals affected by natural catastrophes and man-made perturbations. Ecology 57:278–289Google Scholar
  132. Loya Y, Rinkevich B (1980) Effects of oil pollution on coral reef communities. Mar Ecol Prog Ser 3:167–180Google Scholar
  133. MacCracken M (1990) Energy and climate change. Lewis, Chelsea, Mich, p 161Google Scholar
  134. Manabe S, Stouffer RJ, Spelman MJ, Bryan K (1991) Transient responses of a coupled ocean-atmosphere model to gradual changes of atmospheric CO2. Part I: Annual mean response. J Climate 4:785–818Google Scholar
  135. Mitchell JFB (1988) Local effects of greenhouse gases. Nature 332:399–400Google Scholar
  136. Moore HB (1972) Aspects of stress in the tropical marine environment. Adv Mar Biol 10:217–269Google Scholar
  137. Moran PJ (1986) The Acanthaster phenomenon. Oceanogr Mar Biol Ann Rev 24:379–480Google Scholar
  138. Moyer JT, Emerson WK, Ross M (1982) Massive destruction of scleractinian corals by the muricid gastropod, Drupella, in Japan and the Philippines. Nautilus 96:69–82Google Scholar
  139. Neumann AC, Macintyre IG (1985) Reef response to sea level rise: keep-up, catch-up or give-up. Proc 5th Int Coral Reef Symp 3:105–110Google Scholar
  140. Oliver J (1985) Recurrent seasonal bleaching and mortality of corals on the Great Barrier Reef. Proc 5th Int Coral Reef Symp 4:201–206Google Scholar
  141. Parker DE, Folland CK (1991) Worldwide surface temperature trends since the mid-19th century. In: Schlesinger ME (ed) Greenhouse-gas-induced climatic change: a critical appraisal of simulations and observations. Develop Atmos Sci 19. Elsevier, Amsterdam, pp 173–193Google Scholar
  142. Pastorok RA, Bilyard GR (1985) Effects of sewage pollution on coral-reef communities. Mar Ecol Prog Ser 21:175–189Google Scholar
  143. Pearson RG (1981) Recovery and recolonization of coral reefs. Mar Ecol Prog Ser 4:105–122Google Scholar
  144. Philander SG (1990) El Niño, La Niña, and the Southern Oscillation. Academic Press, New York, p 293Google Scholar
  145. Pirazzoli PA (1991) World atlas of Holocene sea-level changes. Elsevier Oceanogr Ser 58. Elsevier, Amsterdam, p 300Google Scholar
  146. Porter JW, Fitt WK, Spero HJ, Rogers CS, White MW (1989) Bleaching in reef corals: physiological and stable isotopic responses. Proc Natl Acad Sci USA 86:9342–9346Google Scholar
  147. Potts DC (1984) Natural selection in experimental populations of reef-building corals (Scleractinia). Evolution 38:1059–1078Google Scholar
  148. Potts DC (1985) Sea-level fluctuations and speciation in Scleractinia. Proc. 5th Int Coral Reef Symp 4:127–132Google Scholar
  149. Potts DC, Garthwaite RL (1991) Evolution of reef-building corals during periods of rapid global change. In: Dudley EC (ed) The unity of evolutionary biology. Proc 4th Int Congr Syst Evol Biol 1:170–178Google Scholar
  150. Quinn WH, Neal VT, Antunez de Mayolo SE (1987) El Niño occurrences over the past four and a half centuries. J Geophys Res 92:14449–14461Google Scholar
  151. Ricklefs RE, Buffetaut E, Hallam A, Hsu K, Jablonski D, Kauffman EG, Legendre S, Martin P, McLaren DJ, Myers N, Traverse A (1990) Biotic systems and diversity-report of working group 4, Interlaken workshop for past global changes. Palaeogeogr Palaeoclimatol Palacoecol 82:159–168Google Scholar
  152. Rinkevich B, Loya Y (1977) Harmful effects of chronic oil pollution on a Red Sea scleractinian coral population. Proc 3rd Int Coral Reef Symp 2:585–591Google Scholar
  153. Risk MJ, Murillo MM, Cortes J (1980) Observaciones biologicas preliminares sobre el arrecife coralino en el Parque Nacional de Cahuita, Costa Rica. Rev Biol Trop 28:361–382Google Scholar
  154. Robinson G (1985) The influence of the 1982–83 El Niño on Galapagos marine life. In: Robinson G, del Pino EM (eds) El Niño in the Galapagos Islands: the 1982–1983 event. Fundacion Charles Darwin para las Islas Galapagos, Quito, Ecuador, pp 153–190Google Scholar
  155. Rogers CS (1985) Degradation of Caribbean and western Atlantic coral reefs and decline of associated fisheries. Proc 5th Int Coral Reef Symp 6:491–496Google Scholar
  156. Rogers CS (1990) Responses of coral reefs and reef organisms to sedimentation. Mar Ecol Prog Ser 62:185–202Google Scholar
  157. Rowan R, Powers DA (1991a) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1351Google Scholar
  158. Rowan R, Powers DA (1991b) Molecular genetic identification of symbiotic dinoflagellates (zooxanthellae). Mar Ecol Prog Ser 71:65–73Google Scholar
  159. Salm RV (1990) IUCN Coastal Zone Management Project 9571, Sultanate of Oman, CZMP4:F6Google Scholar
  160. Salvat B (1987) Human impacts on coral reefs: facts and recommendations. antenne de Tahiti Museum EPHE French Polynesia, p 253Google Scholar
  161. Scheibling RE, Stephenson RL (1984) Mass mortality of Strongylocentrotus droebachiensis (Echinodermata: Echinoidea) off Nova Scotia, Canada. Mar Biol 78:153–164Google Scholar
  162. Schoenberg DA, Trench RK (1976) Specificity of symbioses between marine cnidarians and zooxanthellae. In: GO Mackie (ed) Coelenterate ecology and behavior. Plenum, New York, p 423–432Google Scholar
  163. Schoenberg DA, Trench RK (1980) Genetic variation in Symbiodinium (=Gymnodinium) microadriaticum Freudenthal, and specificity in its symbiosis with marine invertebrates. III. Specificity and infectivity of Symbiodinium microadriaticum. Proc R Soc Lond 207B:445–460Google Scholar
  164. Scott PJB, Risk MJ, Carriquiry JD (1988) El Niño, bioerosion and the survival of east Pacific reefs. Proc 6th Int Coral Reef Symp 2:517–520Google Scholar
  165. Sheppard CRC, Salm RV (1988) Reef and coral communities of Oman, with a description of a new coral species (Order Scleactinia, genus Acanthastrea). J Nat Hist 22:263–279Google Scholar
  166. Shibata K (1969) Pigments and a UV-absorbing substance in corals and a blue-green alga living in the Great Barrier Reef. Plant Cell Physiol 10:325–335Google Scholar
  167. Siebeck O (1981) Photoreactivation and depth-dependent UV tolerance in reef coral in the Great Barrier Reef/Australia. Naturwissenschaften 68:426–428Google Scholar
  168. Siebeck O (1988) Experimental investigation of UV tolerance in hermatypic corals (Scleractinia). Mar Ecol Prog Ser 43:95–103Google Scholar
  169. Sindermann CJ (1988) Epizootic ulcerative syndromes in coastal/estuarine fish. NOAA Tech Memo, NMFS-F/NEC-54, Northeast Fisheries Center, Woods Hole, Mass, p 37Google Scholar
  170. Singer SF (1989) Global climate change: human and natural influences. Paragon House, New York, p 424Google Scholar
  171. Smith BL, Potts DC (1987) Clonal and solitary anemones (Anthopleura) of western North America: population genetics and systematics. Mar Biol 94:537–546Google Scholar
  172. Smith DB (1991) The reproduction and recruitment of Porites panamensis Verrill at Uva Island, Pacific Panama. MS thesis, University of Miami, Fla, p 64Google Scholar
  173. Smith RC, Calkins J (1976) The use of the Robertson meter to measure the penetration of solar middle-ultraviolet radiation (UVB) into natural waters. Limnol Oceanogr 21:746–749Google Scholar
  174. Smith SV, Kimmerer WJ, Laws EA, Brock RC, Walsh TW (1981) Kaneohe Bay sewage diversion experiment: perspectives on ecosystem responses to nutritional perturbation. Pac Sci 35:279–395Google Scholar
  175. Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn Freeman, San Francisco, p 859Google Scholar
  176. Somers LH (1972) Research Diver's manual. Rev and Exp end, Sea Grant Tech Rpt 16, Univ MichiganGoogle Scholar
  177. Soong K (1990) Reproduction of colonial reef corals: individuality of coral colonies and colony size related characters. PhD Dissertation, University of Texas, Austin, TX, p 137Google Scholar
  178. Sorokin YuI (1990) Plankton in the reef ecosystems. In: Dubinsky Z (ed) Coral reefs, ecosystems of the world 25. Elsevier, Amsterdam, pp 291–327Google Scholar
  179. Sournia A (1976) Abondance du phytoplancton et absence de récifs coralliens sur les côtes des îles Marquies. CR Acad Sci Ser D 282:553–555Google Scholar
  180. Stoddart DR (1969) Ecology and morphology of recent coral reefs. Biol Rev Cambridge Phil Soc 44:433–498Google Scholar
  181. Stoddart JA (1984) Genetical structure within populations of the coral Pocillopora damicornis. Mar Biol 81:19–30Google Scholar
  182. Stoddart JA, Babcock RC, Heyward AJ (1988) Self-fertilization and maternal enzymes in the planulae of the coral Goniastrea favulus. Mar Biol 99:489–494Google Scholar
  183. Stouffer RJ, Manabe S, Bryan K (1991) Climatic response to a gradual increase of atmospheric carbon dioxide. In: Schlesinger ME (ed) Greenhouse-gas-induced climatic change: a critical appraisal of simulations and observations. Develop Atmos Sci 19. Elsevier, Amsterdam, p 129–136Google Scholar
  184. Szmant AM, Gassman NJ (1990) The effects of prolonged “bleaching” on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217–224Google Scholar
  185. Szmant-Froelich A (1985) The effect of colony size on the reproductive ability of the Caribbean coral Montastrea annularis (Ellis and Solander). Proc 5th Int Coral Reef Symp 4:295–300Google Scholar
  186. Thompson JB, Newton CR (1988) Late Devonian mass extinction: episodic climatic cooling or warming? Proc 2nd Int Symp Devonian Syst 3:29–34Google Scholar
  187. Tomascik T, Sander F (1985) Effects of eutrophication on reef-building corals. I. Growth rate of the reef-building coral Montastrea annularis. Mar Biol 87:143–155Google Scholar
  188. Tomascik T, Sander F (1987) Effects of eutrophication on reef-building corals III. Reproduction of the reef-building coral Porites porites. Mar Biol 94:77–94Google Scholar
  189. Tonguthai K (1985) A preliminary account of ulcerative fish diseases in the Indo-Pacific region. FAO, Reg Off Asia and Pacific, Bangkok, DOC FAO/TCP/RAS/4508, p 39Google Scholar
  190. Trench RK (1971) The physiology and biochemistry of zooxanthellae symbiotic with marine coelenterates II. Liberation of fixed 14C by zooxanthellae in vitro. Proc R Soc Lond B 177:237–250Google Scholar
  191. Trench RK (1992) Microalgal invertebrate symbiosis, current trends. In: Lederberg J (ed) Encyclopedia of microbiology, vol 3. Academic Press, New York, pp 2127–2146Google Scholar
  192. Tsonis AA, Elsner JB (1989) Testing the global warming hypothesis. Geophys Res Lett 16:795–797Google Scholar
  193. UNEP/FAO (1985) Directory of marine environmental centres in Caribbean. UNEP regional seas directories and bibliographies, 2nd edn FAO, Rome, p 214Google Scholar
  194. UNEP/IUCN (1988) Coral reefs of the world, vols 1–3. In: Wells SM, Jenkins MD (eds) UNEP regional seas directories and bibliographies. IUCN, Gland, Switzerland, Cambridge, UK/UNEP, Nairobi, KenyaGoogle Scholar
  195. Vernberg WB, Vernberg FJ (1972) Environmental physiology of marine animals. Springer-Verlag, New York, p 346Google Scholar
  196. Veron JEN, Kelley R (1988) Species stability in reef corals of Papua New Guinea and the Indo Pacific. Assoc Aust Palaeontol Mem 6:1–69Google Scholar
  197. Weerdt WH de, Glynn PW (1991) A new and presumably now extinct species of Millepora (Hydrozoa) in the eastern Pacific. Zool Med Leiden 65:267–276Google Scholar
  198. Wigley TML, Raper SCB (1992) Implications for climate and sea level of revised IPCC emissions scenarios. Nature 357:293–300Google Scholar
  199. Wilkerson FP, Kobayashi D, Muscatine L (1988) Mitotic index and size of symbiotic algae in Caribbean reef corals. Coral Reefs 7:29–36Google Scholar
  200. Williams EH Jr, Bunkley-Williams L (1990) The world-wide coral reef bleaching cycle and related sources of coral mortality. Atoll Res Bull 335:1–71Google Scholar
  201. Worrest RC (1982) Review of literature concerning the impact of UV-B radiation upon marine organisms. In: Calkins J (ed) The role of solar ultraviolet radiation in marine ecosystems. Plenum, New York, p 429–457Google Scholar
  202. Yamaguchi M (1975) Sea level fluctuations and mass mortalities of reef animals in Guam, Mariana Islands. Micronesica 11:227–243Google Scholar
  203. Yamazato K (1988) Proceedings of MAB/COMAR MICE IV meeting: Asian and Pacific regional workshop and international symposium on the conservation and management of coral reef and mangrove ecosystems, 25 September–3 October 1987, Okinawa, Japan. Galaxea 7:69–333Google Scholar
  204. Yonge CM (1930) A year on the Great Barrier Reef. Putnam, London, New York, p 246Google Scholar
  205. Yonge CM, Nicholls AG (1931) Studies on the physiology of corals. IV. The structure, distribution and physiology of the zooxanthellae. Sci Rep Gr Barrier Reef Exped 1928–29 1:135–176Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • P. W. Glynn
    • 1
  1. 1.Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric ScienceUniversity of MiamiMiamiUSA

Personalised recommendations