Abstract
Coral bleaching events are often associated with higher levels of coral mortality but when this occurs in the chronology of individual bleaching events is poorly documented. Knowing when mortality occurs is important for understanding molecular mechanisms and the putative adaptive significance of the response (the Adaptive Bleaching Hypothesis). In a detailed study of a coral bleaching event on the Great Barrier Reef, involving weekly and twice weekly repetitive observations of >200 individually marked corals over an 18 month period (∼16,000 observations), it is shown that bleaching in Acropora latistella, A. subulata and Turbinaria mesenterina was an acute, rapid response, occurring within days of a peak in seawater temperatures exceeding previously described thresholds. Subsurface light levels, measured over the duration of the event, were not anomalous. Full bleaching (i.e. whole colonies turning bone-white) and partial bleaching (white patches) was observed in the Acropora spp. whilst the T. mesenterina colonies typically paled to a light brown colour. Algal densities in bleached corals were 10–30% of those of normally pigmented corals (∼2.5 × 106 algae per cm2), and in this instance bleaching was clearly a sudden, isolated, stress event and not an extreme low-point in the seasonal fluctuation of the density of symbiotic algae. Bleached corals were associated with high levels of partial and whole-colony mortality, but mortality was exclusively limited to the two Acropora spp. Importantly, most of this mortality was recorded in surveys conducted 1 and 2 weeks after bleaching was first observed, and for A. latistella as little as 1 week after bleaching was first observed. This suggests that in this particular bleaching event, for the Acropora species, that bleaching and mortality were intimately linked: this in turn suggests it was a pathological phenomenon. The study highlights a problem in the adaptive bleaching hypothesis, whereby significant levels of mortality can occur in a bleaching event before any chance for subsequent recombination of the host-symbiont unit. It is argued that in order to further evaluate the significance of bleaching as a potentially adaptive mechanism, bleaching-induced and bleaching-related mortality have to be fully considered. It is necessary to incorporate the cost (in terms of mortality) of a bleaching event, the recurring cost of reverting to the original, mortal, stress–prone combination after the event, and the higher cost associated with forming a maladaptive combination.
Similar content being viewed by others
References
Aronson RB, Koltes KH, Precht WF, Toscano MA (2002) The 1998 bleaching event and its aftermath on a coral reef in Belize. Coral Reefs 141:435–447
Atwood DK, Hendee JC, Mendez A (1992) An assessment of global warming stress on Caribbean coral reef ecosystems. Bull Mar Sci 51:118–130
Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Progress Ser 237:133–141
Baker AC (2001) Reef corals bleach to survive change. Nature (Lond) 411:765–766
Baker AC (2003) Flexibility and specificity in coral–algal symbiosis: diversity, ecology and biogeography of Symbiodinium. Annu Rev Ecol Syst 34:661–689
Berkelmans R, Oliver JK (1999) Large scale bleaching of corals on the Great Barrier Reef. Coral Reefs 18:55–60
Berkelmans R, De’ath G, Kininmonth S, Skirving W (2004) A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns and predictions. Coral Reefs 23:74–83
Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138
Brown BE, Le Tissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals during a natural bleaching event. Mar Biol 122:655–663
Brown BE, Dunne RP, Ambarsari I, LeTissier MDA, Satapoomin U (1999) Seasonal fluctuations in environmental factors and their influence on symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Mar Ecol Progress Ser 191:53–69
Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism: a testable hypothesis. Bioscience 43:320–326
Buddemeier RW, Baker AC, Fautin DG, Jacobs JR (2004) The adaptive hypothesis of bleaching. In: Rosenberg E (ed) Coral health and disease. Springer, Berlin, pp 427–444
Castillo KD, Helmuth BST (2005) Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure. Mar Biol (NY) 148:261–270
Coffroth MA, Lasker HR, Oliver JK (1990) Coral mortality outside of the eastern Pacific during 1982–1983: relationship to El Niño. In: Glynn PW (eds) Global ecological consequences of the 1982–1983 El Niño-Southern Oscillation. Elsevier, Amsterdam, pp 141–182
Coles SL, Jokiel PL, Lewis CR (1976) Thermal tolerance in tropical versus subtropical Pacific reef corals. Pac Sci 30:159–166
D’ Croz L, Maté JL (2004) Experimental responses to elevated water temperature in genotypes of the reef coral Pocillopora damicornis from upwelling and non-upwelling environments in Panama. Coral Reefs 23:473–483
Douglas AE (2003) Coral bleaching—how and why? Mar Poll Bull 46:385–392
Dunn S, Bythell JC, Le Tissier MDA, Burnett WJ, Thomason JC (2002) Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the symbiotic sea anemone Aiptasia sp. J Exp Mar Biol Ecol 272:29–53
Edmunds PJ, Gates RD, Gleason DF (2003) The tissue composition of Montastraea franksi during a natural bleaching event in the Florida Keys. Coral Reefs 22:54–62
English S, Wilkinson C, Baker V (1997) Survey manual for tropical marine resources, 2nd edn. Australian Institute of Marine Science, Townsville
Fagoonee I, Wilson HB, Hassell MP, Turner JF (1999) The dynamics of zooxanthellae populations: a long term study in the field. Science (Wash. DC) 283:843–845
Fautin DG, Buddemeier RW (2004) Adaptive bleaching: a general phenomenon. Hydrobiologia 530/531:459–467
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 45:677–685
Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20:51–65
Franklin DJ, Hoegh-Guldberg P, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching. Mar Ecol Progress Ser 272:117–130
Gates RD, Baghdasarian G, Muscatine L (1992) Temperature stress causes host cell detachment in symbiotic cnidarians: implication for coral bleaching. Biol Bull (Woods Hole) 182:324–332
Gleeson MW, Strong AE (1995) Applying MCSST to coral reef bleaching. Adv Space Res 16:151–154
Glynn PW (1985) El Nino-associated disturbances to coral reefs and post disturbance mortality by Acanthaster planci. Mar Ecol Progress Ser 26:295–300
Glynn PW (1988) El Nino warming, coral mortality and reef framework destruction by echinoid bioerosion in the eastern Pacific. Galaxea 7:129–160
Glynn PW (1993) Coral reef bleaching: ecological perspectives. Coral Reefs 12:1–17
Goreau TJ, Hayes RL (1994) Coral bleaching and ocean ‘Hot Spots’. Ambio 3:176–180
Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature (Lond) 440:1186–1189
Harvell D, Kim K, Quirolo C, Weir J, Smith G (2001) Coral bleaching and disease: contributors to 1998 mass mortality in Briareum asbetinum (Octocorallia, Gorgonacea). Hydrobiologia 460:97–104
Hendee JC (1998) An expert system for marine environmental monitoring in the Florida Keys National Marine Sanctuary and Florida Bay. In: Brebbia CA (ed) Proc 2nd int conf on environmental coastal regions computational mechanics publications. WIT Press, Southampton, pp 57–66
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–66
Hoegh-Guldberg O, Salvat B (1995) Periodic mass-bleaching and elevated sea temperatures: bleaching of outer reef slope communities in Moorea, French Polynesia. Mar Ecol Prog Ser 121:181–190
Hoegh-Guldberg O, Jones RJ, Ward S, Loh WK (2002) Is coral bleaching really adaptive? Nature 415:601–602
Hughes TP (1989) Community structure and diversity of coral reefs: the role of history. Ecology 70:275–279
Hughes TP, Jackson JBC (1980) Do corals lie about their age? Some demographic consequences of partial mortality, fission and fusion. Science 209:713–715
Jokiel PL (2004) Temperature stress and coral bleaching. In: Rosenberg E (ed) Coral health and disease. Springer, Berlin, pp 401–425
Jokiel PL, Coles SL (1990) Response of Hawaiian and other Indo-Pacific reef corals to elevated temperatures associated with global warming. Coral Reefs 9:155–162
Jones RJ (1997) Changes in zooxanthellar densities and chlorophyll concentrations in corals during and after a bleaching event. Mar Ecol Prog Ser 158:51–59
Jones RJ (2005) Testing the Photoinhibition model of coral bleaching using chemical inhibitors. Mar Ecol Prog Ser 284:133–145
Jones RJ, Yellowlees DY (1997) Algal (=zooxanthellae) regulation and control in hard corals. Philos Trans R Soc Lond B Biol Sci 352:457–468
Jones RJ, Berkelmans R, Oliver J (1997) The recurrent bleaching of corals at Magnetic Island (Australia) relative to air and seawater temperature. Mar Ecol Prog Ser 158:289–292
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 21:1219–1230
Jones RJ, Ward S, Amri AY, Hoegh-Guldberg O (2000) Changes in quantum efficiency of Photosystem II of symbiotic dinoflagellates of corals after heat stress and during the 1998 Great Barrier Reef mass bleaching event. Mar Freshw Res 51:63–71
Jones RJ, Bowyer J, Hoegh-Guldberg O, Blackall L (2004) Dynamics of a temperature-related coral disease outbreak. Mar Ecol Prog Ser 281:63–77
Kaufman KW, Thompson RC (2005) Water temperature variation and the meteorological and hydrographic environment of Bocas del Toro, Panama. Caribb J Sci 41:392–413
Kinzie R, Takayama M, Santos SR, Coffroth MA (2001) The adaptive bleaching hypothesis: experimental tests of critical assumptions. Biol Bull (Woods Hole) 200:51–58
Loya Y (1976) The Red Sea coral Stylophora pistillata is an r-strategist. Nature (Lond.) 259:478–480
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, Woesik R van (2001) Coral bleaching: the winners and losers. Ecol Lett 4:122–131
Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163
McClanahan TR (2004) The relationship between bleaching and mortality of common corals. Mar Biol (NY) 144:1239–1245
McClanahan TR, Baird AH, Marshall PA, Toscano MA (2004) Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Mar Pollut Bull 28:327–335
Mendes JM, Woodley JD (2002) Effect of the 1995–1996 bleaching event on polyp tissue depth, growth, reproduction and skeletal band formation in Montastraea annularis. Mar Ecol Prog Ser 235:93–102
Mumby PJ, Chisholm JRM, Edwards AJ, Clark CD, Roark EB, Andrefouet S, Jaubert J (2001) Unprecedented bleaching induced mortality in Porites spp at Rangiroa Atoll, French Polynesia. Mar Biol (NY) 139:183–189
Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinski Z (ed) Ecosystems of the world: coral reefs, vol 25. Elsevier, Amsterdam, pp 75–87
Nakamura T, van Woesik R (2001) Differential survival of corals during the 1998 bleaching event is partially explained by water-flow rates and passive diffusion. Mar Ecol Prog Ser 212:301–304
Oliver JK (1984) Intra-colony variation in the growth of Acroproa formosa: extension rates and skeletal structure of white (zooxanthellae-free) and brown tipped branches. Coral Reefs 3:139–147
Oliver J (1985) Recurrent seasonal bleaching and mortality of corals on the Great Barrier Reef. In: Proceedings of the 5th international coral reef symposium, vol 4, pp 201–206
Oren U, Benayahu Y, Loya Y (1997a) Effect of lesion size and shape on regeneration of the red Sea coral Favia favus. Mar Ecol Prog Ser 146:101–167
Oren U, Rinkevich B, Loya Y (1997b) Oriented intra-colonial transport of 14C labelled material during coral regeneration. Mar Ecol Prog Ser 161:119–122
Oren U, Benayahu Y, Lubinevsky H, Loya Y (2001) Colony integration during regeneration in the stony coral Favia favus. Ecology (N. Y.) 82:802–813
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 86:9342–9346
Rosenberg E, Ben-Haim Y (2002) Microbial diseases of corals and global warming. Environ Microbiol 4:318–326
Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269
Stimson J (1997) the annual cycle of density of zooxanthellae in the tissues of field and laboratopry-held Pocillopora damicornis. J Exp Mar Biol Ecol 214:35–48
Stimson J, Sakai K, Sembali H (2002) Interspecific comparison of the symbiotic relationship in with high and low rates of bleaching-induced mortality. Coral Reefs 21:409–421
Strong AE, Barrientos CS, Duda C, Sapper J (1997) Improved satellite techniques for monitoring coral reef bleaching. In: Proceedings of the 8th international coral reef symposium, vol 2, pp 1495–1498
Strychar KB, Coates M, Sammarco PW, Piva TJ (2004) Bleaching as a pathogenic response in scleractinian corals, evidenced by high concentrations of apoptotic and necrotic zooxanthellae. J Exp Mar Biol Ecol 304:99–121
Sweatman H, Cheal A, Coleman G, Fitzpatrick B (2000) Long-term monitoring of the great barrier reef. Status Report No 4. Australian Institute of Marine Science, Townsville
Szmant AM, Gassman NJ (1990) The effects of prolonged ‘bleaching’ on the tissue biomass and reproduction of the reef coral Montastraea annularis. Coral Reefs 8:217–224
Toller WW, Rowan R, Knowlton N (2001) Repopulation of zooxanthellae in the Caribbean corals Montastraea annularis and M. faveolata following experimental and disease associated bleaching. Biol Bull (Woods Hole) 201:360–373
Wallace CC (1999) Staghorn corals of the world: a revision of the genus Acropora. CSIRO Publishing, Collingwood
Ware JR, Fautin DG, Buddemeier RW (1996) Patterns of coral bleaching: modeling the adaptive bleaching hypothesis. Ecol Model 84:199–214
Warner ME, Chilcoat G, McFarland F, Fitt WK (2002) Seasonal fluctuations in the photosynthetic capacity of photosystem II in symbiotic dinoflagellates within the Caribbean reef-building coral Montastraea. Mar Biol (NY) 141:31–38
Wooldridge S, Done T (2004) Learning to predict large-scale coral bleaching from past events: a Bayesian approach using remotely sensed data, in-situ data, and environmental proxies. Coral Reefs 23:96–108
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P.W. Sammarco.
Rights and permissions
About this article
Cite this article
Jones, R.J. Coral bleaching, bleaching-induced mortality, and the adaptive significance of the bleaching response. Mar Biol 154, 65–80 (2008). https://doi.org/10.1007/s00227-007-0900-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-007-0900-0