R E S E A R C H A R T I C L E
T. R. McClanahan
The relationship between bleaching and mortality of common corals
Received: 12 July 2002 / Accepted: 10 November 2003 / Published online: 30 January 2004
Springer-Verlag 2004
AbstractReef corals are likely to have many subtle but four gross responses to anomalous warm water. These are (1) not bleach and live (mortality <10%), (2) not bleach and die (mortality >20%), (3) bleach and live, and (4) bleach and die. The frequency of these four possible gross responses was determined for 18 common coral taxa over an exceptionally warm 1998 El Nin˜o where intense bleaching was observed, and mortality determined from line transects averaged 41.2±34.7 (±SD). Field studies included (1) recording the loss of color (bleaching) and observing recently dead in-dividuals among 6,803 colonies during five sampling periods and (2) estimating mortality based on 180 m of line-intercept transects completed 4 months before and near the end of the bleaching episode. There was no clear relationship between the loss of color and either direct observation or transect-based estimates of mor-tality for the 18 taxa. The morphology of the taxa did not influence color loss but branching and encrusting taxa had higher mortality than massive and submassive taxa. Loss of color and mortality are the most common responses to warm water as only Pavona did not lose color or die and only two taxa, Cyphastrea and Mille-pora, did not significantly lose color but died. Of the 15 taxa that lost color, five taxa,Astreopora,Favia,Favites,
Goniopora, and Leptoria, did not die. These taxa are those most likely to have reduced potential mortality by the loss of pigments and associated algal symbionts. Death of the branching taxa was detected reasonably by direct field observation but some taxa were underesti-mated when compared with mortality estimates based on line transects. Death of encrusting and massive taxa includingEchinopora,Galaxea,Hydnophora,Montipora,
Platygyra, and massivePoriteswas poorly detected from direct observations but they proved to have modest to high mortality (20–80%) based on line transects. There
was no single response of these common corals to warm water but these data, collected during an extreme warm-water anomaly, indicate that the loss of color is most frequently a sign of morbidity, particularly for branch-ing and encrustbranch-ing taxa.
Introduction
Bleaching and mortality of hard corals has become increasingly frequent and is expected to increase with global climate change (Goreau 1990; Glynn 1996; Brown 1997; Hoegh-Guldberg 1999; Douglas 2003). Some investigators see bleaching or the loss of pigments and Symbiodinium, the endosymbiotic dinoflagellate living in the scleractinian corals, as a symptom of morbidity caused by warm-water stress that leads to mortality and associated ecological change (Glynn 1984; Goreau and Macfarlane 1990; Goreau 1992; Guldberg and Salvat 1995; Jones et al. 1998; Hoegh-Guldberg 1999). Other investigators view coral bleaching as a healthy but high-risk adaptation to reduce coral host mortality. Bleaching represents an interim period where switching of theSymbiodiniumtowards clades or species that have different thermal optima occurs and this may lead to improved host survival (Jokiel and Coles 1977; Buddemeier and Fautin 1993; Ware et al. 1996; Kinzie 1999; Gates and Edmunds 1999; Rowan et al. 1997). The loss of Symbiodinium occurs, often without obvious visual detection, on a seasonal basis (Fagoonee et al. 1999; Fitt et al. 2000), and bleaching events that are easily observed may simply represent the more extreme deviations from these cyclical patterns (Fitt et al. 2001). A test of the adaptive bleaching hypothesis, relying on an experimental reciprocal transplant study with depth, found that bleaching and a switch in the dominant Symbiodinium clades improved individuals’ chances for survival compared to individu-als that did not bleach (Baker 2001) but other environmental factors associated with depth may have Communicated by P.W. Sammarco, Chauvin
T. R. McClanahan
Wildlife Conservation Society, Bronx, NY 10460, USA E-mail: [email protected]
confounded a direct test of the hypothesis (Hoegh-Guldberg et al. 2002). Bleaching has, however, been associated with a large-scale loss of coral cover (Glynn 2000; Goreau et al. 2000; Mumby et al. 2001; Riegl 2002; Aronson et al. 2002). In many cases this may be due to the loss of fast-growing branching or encrusting taxa that often dominate coral cover, but there could be variable responses to warm water based on growth forms, metabolism, environmental history, or the evo-lutionary history of the coral taxa (Gates and Edmunds 1999; Coles and Brown 2003).
The relationship between bleaching, coral health, and mortality is poorly understood but this under-standing is critical to determining the adaptability or acclimatization of corals to global climate change (Fitt et al. 2001; Douglas 2003; Coles and Brown 2003). It has been uncommon to measure the concentration of pigment or Symbiodinium loss, coral health, and death for many taxa. Fitt et al. (2001) suggest there may be no clear relationship as the visual threshold for detecting bleaching may be arbitrary. Although losses of less than 30% of the Symbiodinium may be difficult to detect (Fitt et al. 2000) the most severe bleaching, when corals appear white, is easier to detect and fre-quently associated with a 75% reduction in Symbiodi-nium densities (Brown et al. 1995; Edmunds et al. 2003). Nonetheless, a recent study indicates that sub-jective rankings of bleaching based on coral color are strongly associated with Symbiodinium density, chlo-rophyll a concentrations, and the intensity of green, blue, and red color spectrums (Edmunds et al. 2003). Subjective rankings may, therefore, be a good indicator of disruption of the symbiosis for severe bleaching events although less useful for determining the health of the coral tissue, as there may be a significant time lag between the loss of Symbiodinium and effects on coral health (Edmunds et al. 2003). Many studies have focused on bleaching or mortality but only seldom has the interrelationship between the two factors been examined (Brown and Suharsono 1990; Davies et al. 1997; Marshall and Baird 2000; McClanahan 2000; Loya et al. 2001; Baird and Marshall 2002). Studies of both factors have often been restricted to a few of the dominant or most temperature-sensitive species (Glea-son 1993; Hoegh-Guldberg and Salvat 1995; Berkel-mans and Willis 1999; Glynn et al. 2001). Both recovery and high levels of mortality have been re-ported and this may depend on the temperature anomaly and the studied taxa.
Coral reef ecologists may be recording and reporting the more obvious response of bleaching and mortality (Fitt et al. 2001). There may be multiple causes, re-sponses, and outcomes to bleaching and anomalous warm water that either receive less attention or are difficult to quantify during limited field observations. There are also many physiological but four gross pos-sible responses to warm water: these are (1) not bleach and live, (2) not bleach and die, (3) bleach and live, and (4) bleach and die. Because bleaching is such a visual
phenomenon, bleaching and death are likely to have received more attention than the other possible out-comes (Fitt et al. 2001). The hypothesis tested here is that all of the above four outcomes occur during warm-water events and the response will vary with taxa and morphology. To test this hypothesis, observations on the color changes of 18 common coral taxa and two different estimates of death were made in the Mombasa Marine National Park (MNP) during the 1998 El Nin˜o, one of the warmest years in the past century (McPhaden 1999; Webster et al. 1999; Sheppard and Rayner 2002). These data were used to determine (1) if there is a clear relationship between the loss of coral color and mor-tality and (2) which of the four major outcomes is most represented by the studied taxa during these extreme warm water events.
Materials and methods
Study sites
The study was undertaken along a continuous fringing back-reef lagoon of the Mombasa MNP (359¢N; 395¢E) between November 1997 and September 1998. The study area included hard bottom areas between 1- and 6-m depths, depending on the tide, on the leeward side of Kenya’s fringing reef. The site is approximately 1 km from shore and protected from all forms of resource extrac-tion. The park protects a 6-km strip of this fringing reef and sampling was undertaken within a 2-km strip in the center of the park (see map in McClanahan and Mangi 2000). The reef contains a high diversity of coral and other benthic invertebrates and is typical of Kenyan back-reef fauna. The mean annual seawater temperature for the past 17 years is 27C (McClanahan et al. 2001), with warm-season temperatures averaging 28C. The anomaly during the peak warming was 1–1.5C above previous recorded years for the warmest months of March and April (McClanahan and Maina 2003).
Color response
The color response is based on observations of 6,803 coral colonies selected during five sampling periods between March and Sep-tember 1998 (Table 1). Colonies were sampled by swimming with eyes closed above the reef in a randomly chosen direction, kicking a random number of kicks between three and seven, and upon opening the eyes, selecting all corals colonies within a 2-m radius for color categorization. This process was continued until no less than 650 coral colonies were sampled, but in most cases more than 1,600 colonies were sampled per period (Table 1). Data were only analyzed for taxa having greater than 60 individual observations over the five sampling periods.
Each colony was identified to the genus and categorized into the following six categories: (1) unbleached (normal coloration), (2) pale (lighter color than usual for the time of year), (3) 0–20% of the surface bleached, (4) 20–50% bleached, (5) 50–80% bleached, and (6) 80–100% bleached (Fig. 1). This method of categorizing or ranking color changes was originally described by Gleason (1993), more recently used by Marshall and Baird (2000), and validated by Edmunds et al. (2003). A bleaching index (BI) was calculated from the percentage of observations in each of the above six bleaching categories over the five sampling periods as
whereciis the percentage of observations in each of the above six bleaching categories. Percentage data were tested for normality along with arcsin and square root transformed data. Data were normally distributed and transformations did not improve mea-sures of normality and, therefore, the untransformed data were used in the analyses.
Death estimates
Estimates of death due to warm water are based on two methods: (1) direct observations of dead corals in the color surveys above, which are referred to as observed dead, and (2) line-intercept transects undertaken 4 months before and at the end of the
Table 1 Number of individual
coral colonies sampled for each taxon during each sampling period in the Mombasa Marine National Park in 1998
Genus Growth form March May June July September Total
Poritesmassive Massive 139 363 387 215 141 1,245 Poritesbranching Branching 502 205 103 136 106 1,052 Montipora Encrusting 177 382 262 100 45 966 Acropora Branching 118 230 185 59 74 666 Pocillopora Branching 215 113 75 65 30 498 Galaxea Submassive 79 131 147 76 42 475 Favia Submassive 65 154 111 52 33 415 Platygyra Massive 49 58 56 32 20 215 Astreopora Massive 29 52 32 15 13 141 Favites Submassive 31 34 43 31 24 163 Stylophora Branching 73 37 23 29 10 172 Pavona Branching 24 17 40 41 46 168 Goniopora Submassive 26 17 51 25 14 133 Echinopora Encrusting 18 36 37 14 8 113 Millepora Branching 37 20 19 16 25 117 Cyphastrea Submassive 29 20 18 19 21 107 Leptoria Massive 3 26 15 37 9 90 Hydnophora Massive 16 26 9 9 7 67 Total 1,630 1,921 1,613 971 668 6,803
Fig. 1a–d Bleaching categories
used in this study using examples ofPorites lutea.aThe coral on the left is classified as pale and is a gray or blue type of paling, whereas the one on the right is classified as normal.
bThis coral is also pale but has a yellow coloration.cAn example of a 20–50% partially bleached coral.dA fully bleached coral on the left and one of normal color on the right
bleaching event, which is referred to as mortality. During the above five sampling periods individual corals were placed in a seventh category of recently dead. These corals had white exposed skeletons with no living tissue on the surface. Skeletons that were being colonized by filamentous microscopic algae lost their white color-ation, and turning green, were not classified as recently dead. The time between death and colonization by filamentous turf algae and the green coloration is <20 days (McClanahan 1997). Conse-quently, by the end of the sampling period many dead corals were no longer distinguishable from the turf algae community and the dead category was, therefore, sensitive to the sampling period and how protracted the period of death was for each taxa. To minimize this sampling effect, the period when mortality for each taxon was the highest was identified among the five sampling periods and used to estimate mortality by direct observation. Direct observation of mortality or observed dead was therefore calculated as the per-centage of recently dead individuals divided by the total number of corals sampled for the respective taxa during the chosen sampling date.
The second measure of mortality was calculated from the eighteen 10-m line transects completed in mid-November 1997 and repeated 9 months later in mid-August 1998. Line transects were haphazardly placed along the fringing reef in the same areas where the bleaching observations were made. Along the 10-m line all corals >3 cm were identified to the genus and the colony convex crown diameter measured. Branching was distinguished from massivePoritesand all sampledMontiporawere encrusting forms in this survey. Percent mortality is based on the difference between the taxa-specific cover in the pre- and post-bleaching period divided by the pre-bleaching period. From frequent observations during this period, mortality is almost exclusively attributable to bleaching or interactions with bleaching, as no other sources of large-scale mortality, such as diseases, storms, freshwater, sediments, or physical damage, were observed during this 9-month period. The BI was compared with the two estimates of death for each taxon with scatterplots of the relationships between the three variables. The 18 taxa were pooled into three growth forms, (1) branching (n=6), (2) encrusting (n=2), and (3) submassive and massive (n=10) (Table 1), and the BI and the two estimates of mortality were compared by single-factor analysis of variance and Tukey tests (Sall et al. 2001).
Results
The average of the observed dead for the 18 taxa was significantly lower [F=6.2,P<0.02; 17.0±5.2% (±SEM)] than mortality estimated from the line trans-ects (41.2±8.2%). There are further differences based on coral taxa and morphologies as indicated by the scat-terplot of the relationship between the two estimates of mortality (Fig. 2). The highest correspondence between the observed dead and mortality was for taxa that experienced mortality of <10%. These taxa were Ast-reopora,Favia,Favites,Goniopora,LeptoriaandPavona. An additional two branching taxa, Millepora and
Acropora, were not far from the 1:1 line, but mortality of all other taxa was underestimated by the direct obser-vation method. The difference was less pronounced for three branching taxa, branchingPorites,Stylophora, and
Pocillopora, but the difference was large for the remaining seven encrusting, submassive, and massive taxa that bleached and died. This analysis suggests that, on average, direct observation during a single peak time of bleaching mortality is likely to underestimate mor-tality by more than half and I, therefore, used the line-transect method as the best estimate of mortality.
The average BI for the 18 taxa was 26.2±3.8. Scat-terplots of the BI and the best estimate of mortality indicate that there was no clear relationship between the color response and mortality for all the taxa by either estimate of mortality (Fig. 3). All taxa with the excep-tion ofPavonaexperienced either bleaching or mortality during this warm-water event. Two taxa,Milleporaand
Cyphastrea, did not bleach appreciably but nonetheless died. Mortality ofCyphastreaby direct observation was probably highly underestimated but was 54% by the line-transect method. The taxa Astreopora, Favia,
Favites,Goniopora, andLeptoriableached but lived. The remaining 10 taxa were found to have bleached and died when the more accurate line-transect estimate of mor-tality was used. The highest estimate of mormor-tality was found for the three branching taxa, branching Porites,
Stylophora, and Pocillopora, but their BI was not appreciably higher than other nonbranching taxa such as Galaxea,Montipora, and massive Porites. Branching
Acropora had an intermediate BI and mortality. Consequently, for 10 of the 18 taxa, bleaching was a sign of morbidity.
Analyses of the taxa pooled into the three morpho-logies indicated no statistical differences for the BI but
Fig. 2 Scatterplot of the relationship between percentage mortality
based on line transects before and after the bleaching episode and observed dead from field observations during the peak mortality period for each of the 18 taxa. The 1:1 line is that expected for a perfect correlation
Fig. 3 Scatter plot of the relationship between the Bleaching Index
and the percentage mortality based on line transects before and after the warm-water anomaly for the 18 studies coral taxa
significant differences for both mortality estimates (Table 2). The percentage of branching morphologies that were observed dead was considerably higher than both encrusting and massive taxa. Mortality estimates based on line transects indicate that branching taxa died at three times the rate of massive taxa, but the small sample size of the encrusting taxa (n=2) resulted in no statistical differences. Mortality estimates of the massive and encrusting taxa were more than six times higher by the line transect method than direct observation during peak mortality periods, but the difference in branching taxa was only 1.5 times higher.
Discussion
Coral bleaching is a visually striking response that is frequently associated with warm water and other envi-ronmental disturbances to coral reefs (Glynn 1996; Brown 1997; Fitt et al. 2001). Some investigators see coral bleaching as a symptom of environmental stress and an indicator of morbidity and eventual mortality whereas others see it as a risky adaptation to changing environmental conditions (Buddemeier and Smith 1999). This study suggests that there are multiple responses and outcomes to anomalous warm water that depend on the coral taxa and their morphologies (Tables 2, 3). There are, however, differences in the frequencies of the four possible responses and in general, bleaching is most of-ten a sign of morbidity. The least common response is not to bleach and survive and only one taxa, Pavona, exhibited it. Secondly, not to bleach and die was also uncommon with only two taxa, Cyphastrea and Mille-pora, exhibiting it. Bleaching was the most common response with 83% of the taxa bleaching and 55% dying in significant numbers from the bleaching. More death may have occurred for the taxa that bleached if they had not bleached, but it is not possible to test this response with these data. Experiments to determine this possi-bility, such as the transplantation of corals to different depth and light environments, are insightful (Baker 2001). Transplantation experiments cannot, however, distinguish differential acclimation and changes in sym-biont dominance in response to only changing light because other environmental cofactors associated with depth, such as levels of plankton, nutrients, and other stresses and food sources, can confound experimental conditions and associated conclusions (Hoegh-Guldberg et al. 2002).
Bleaching appears to be a common response of hard corals to warm water with only a few exceptions. It might be argued from the adaptive bleaching perspective that taxa that do not bleach and die do so as a consequence of not bleaching. In this study the mortality of the two taxa that did not bleach and died was 40%, very similar to the 41% mortality found for the taxa that did bleach. To be truly supportive of the adaptive bleaching hypothesis, mortality among non-bleaching taxa should be greater than for taxa that bleached. The adaptive bleaching hypothesis is better supported by the response of the five taxa that bleached moderately but experienced no net mortality, but this was only true for 28% of the studied taxa. It can also be reasoned that mortality might have been significantly higher if bleaching had not occurred, but the data can only test this possibility for between-taxa differences and not within between-taxa. Where within-between-taxa experiments have been done, they have been partially supportive of this hypothesis (Baker 2001). Given that taxa have different responses, experiments that both adjustSymbiodinumclades while holding environmental factors constant and that followSymbiodiniumchanges over changing environmental conditions will be required for many coral taxa to determine the degree of intra- and interspecific adaptation to warm-water anomalies.
Changes to total coral cover can be significantly greater than the average mortality by taxa, due to the differential cover of the various taxa (Marshall and Baird 2000). For instance, in this study area where the average taxa-specific mortality was 41%, the total hard coral cover decreased by 66% from 41 to 14% across the 9-month period. This is largely due the high abundance and mortality of branching Porites (37% of the hard
Table 2 Comparison of the bleaching index, percentage observed dead, and percentage mortality estimated from line transects based on
three coral morphologies. The massive category also includes submassive taxa;nnumber of taxa,SDstandard deviation
Branching Encrusting Massive ANOVA Tukey test
Mean SD Mean SD Mean SD FRatio P>F
Bleaching index 24.2 17.3 38.7 23.7 25.0 15.2 0.6 NS
Observed dead (%) 41.3 23.0 10.8 6.8 3.6 2.8 14.7 0.00 Branching >Massive, Encrusting Mortality (%) 61.7 42.0 73.7 2.8 22.5 19.6 5.0 0.02 Branching, Encrusting >Massive
Table 3 Summary of the four gross responses to the 1998
warm-water event and the outcomes of the studied taxa
Lived Died
No bleaching Pavona Cyphastrea
Millepora
Bleaching Astreopora Acropora
Favia Echinopora Favites Galcaea Goniopora Hydnophora Leptoria Montipora Platygyra Pocillopora Poritesbranching Poritesmassive Stylophora
coral cover) in the study area before 1998. Common to other study sites, where branching taxa such as Acro-pora,Stylophora,Pocillopora, and branchingPoritesare among the dominant taxa and susceptible to bleaching, the loss of total coral cover can be larger than the average taxa-specific mortality.
Experimental studies suggest that the thresholds for bleaching can vary among these branching taxa based on background temperatures (Berkelmans and Willis 1999). Consequently, they do have some ability to acclimate but the ability is probably less than for mas-sive and submasmas-sive taxa. Loya et al. (2001) found warm-water-induced high mortality among branching taxa in Japan and suggested that thinner tissue common to branching taxa was the likely cause of the high mortality. Thinner tissue will provide less energy for corals that have reduced photosynthetic production and will result in a shorter time to die. Gates and Edmunds (1999) suggest that branching morphologies are unable to respire and metabolize proteins to the extent of taxa with other morphologies and slower skeletal growth. These studies indicate that physiological and morpho-logical characters of branching corals limit their adapt-ability to anomalous environmental change. Perhaps, over multiple generations, natural selection, physiologi-cal adaptations, and switches in their symbionts occur, but long-term studies will be required to test this pos-sibility. Nonetheless, the study indicates that it is not the greater bleaching response but rather the contribution of branching taxa to total coral cover and their high mor-tality that causes branching taxa to be frequently noted, recorded, and studied during bleaching events.
AcknowledgementsResearch was supported by the Wildlife
Con-servation Society and permission to undertake field work in Kenya and the parks was provided by Kenya’s Office of the President and Kenya Wildlife Services. I am grateful to R. Arthur, H. Machano Ali, and S. Mangi for assistance with the line transects and J. Maina for preparing the figures.
References
Aronson RB, Precht WF, Toscano MA, Koltes KH (2002) The 1998 bleaching event and its aftermath on a coral reef in Belize. Mar Biol 144:435–447
Baird AH, Marshall PA (2002) Mortality, growth and reproduc-tion in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141
Baker AC (2001) Reef corals bleach to survive change. Nature 411:765–766
Berkelmans R, Willis BL (1999) Seasonal and local spatial patterns in the upper thermal limits of corals on the inshore Central Great Barrier Reef. Coral Reefs 18:219–228
Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16:S129–S138
Brown BE, Suharsono (1990) Damage and recovery of coral reefs affected by El Nino related seawater warming in the Thousand Islands, Indonesia. Coral Reefs 8:163–170
Brown BE, Le Tissier MDA, Bythell JC (1995) Mechanisms of bleaching deduced from histological studies of reef corals sam-pled during a natural bleaching event. Mar Biol 122:655–663
Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism: a testable hypothesis. Bioscience 43:320–326 Buddemeier RW, Smith SV (1999) Coral adaptation and
acclima-tization: a most ingenious paradox. Am Zool 39:1–9
Coles SL, Brown BE (2003) Coral bleaching—capacity for ac-climitization and adaptation. Adv Mar Biol 46:183–223 Davies JM, Dunne RP, Brown BE (1997) Coral bleaching and
elevated sea-water temperature in Milne Bay Province, Papua New Guinea, 1996. Mar Freshw Res 48:513–516
Douglas AE (2003) Coral bleaching—how and why? Mar Pollut Bull 46:385–392
Edmunds PJ, Gates RD, Gleason DF (2003) The tissue composi-tion ofMontastraea franksiduring a natural bleaching event in the Florida Keys. Coral Reefs 22:54–62
Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long-term study in the field. Science 283:843–845
Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Sea-sonal patterns of tissue biomass and densities of symbiotic di-noflagellates 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 ther-mal thresholds in tropical corals. Coral Reefs 20:51–65 Gates RD, Edmunds PJ (1999) The physiological mechanisms of
acclimatization in tropical reef corals. Am Zool 39:30–43 Gleason MG (1993) Effects of disturbance on coral communities:
bleaching in Moorea, French Polynesia. Coral Reefs 12:193– 201
Glynn PW (1984) Widespread coral mortality and the 1982/83 El Nino warming event. Environ Conserv 11:133–146
Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Global Change Biol 2:495–509
Glynn PW (2000) El Nino-Southern Oscillation mass mortalities of reef corals: a model of high temperature marine extinctions? In: Insalaco E, Skelton PW, Palmer TJ (eds) Carbonate platform systems: components and interactions. (Special Publications 178) Geological Society of London, London, pp 117–133 Glynn PW, Mate JL, Baker AC, Calderon MO (2001) Coral
bleaching and mortality in Panama and Ecuador during the 1997–98 El Nino-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 event. Bull Mar Sci 69:79–109
Goreau T, McClanahan T, Hayes R, Strong A (2000) Conservation of coral reefs after the 1998 global bleaching event. Conserv Biol 14:5–15
Goreau TJ (1990) Coral bleaching in Jamaica. Nature 343:417 Goreau TJ (1992) Bleaching and reef community change in
Jamaica: 1951–1991. Am Zool 32:683–695
Goreau TJ, Macfarlane AH (1990) Reduced growth rate of Mon-tastrea annularisfollowing the 1987–1988 coral-bleaching event. Coral Reefs 8:211–215
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866 Hoegh-Guldberg O, Salvat B (1995) Periodic mass-bleaching and
elevated sea temperatures: bleaching of outer reef slope com-munities in Moorea, French Polysnesia. 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
Jokiel PL, Coles SL (1977) Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar Biol 43:201–208 Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998)
Temperature-induced bleaching of corals begins with impair-ment of the CO2 fixation mechanism in zooxanthellae. Plant
Cell Environ 21:1219–1230
Kinzie RA (1999) Sex, symbiosis and coral communities. Am Zool 39:80–91
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 (1997) Primary succession of coral-reef algae: differing patterns on fished versus unfished reefs. J Exp Mar Biol Ecol 218:77–102
McClanahan TR (2000) Bleaching damage and recovery potential of Maldivian coral reefs. Mar Pollut Bull 40:587–597
McClanahan TR, Maina J (2003) Response of coral assemblages to the interaction between natural temperature variation and rare warm-water events. Ecosystems 6:551–563
McClanahan TR, Mangi S (2000) Spillover of exploitable fishes from a marine park and its effect on the adjacent fishery. Ecol Appl 10:1792–1805
McClanahan TR, Muthiga NA, Mangi S (2001) Coral and algal response to the 1998 coral bleaching and mortality: interaction with reef management and herbivores on Kenyan reefs. Coral Reefs 19:380–391
McPhaden MJ (1999) Genesis and evolution of the 1997–98 El Nino. Science 283:950–954
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 139:183–189
Riegl B (2002) Effects of the 1996 and 1998 positive sea-surface temperature anomalies on corals, coral diseases and fish in the Arabian Gulf (Dubai, UAE). Mar Biol 140:29–40
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
Sall J, Lehman A, Creighton L (2001) JMP start statistics. Dux-bury/Thomson Learning, Pacific Grove, Calif.
Sheppard C, Rayner NA (2002) Utility of the Hadley Centre sea ice and sea surface temperature data set (HadISST1) in two widely contrasting coral reef areas. Mar Pollut Bull 44: 303–308
Ware JR, Fautin DG, Buddemeier RW (1996) Patterns of coral bleaching: modeling the adaptive bleaching hypothesis. Ecol Model 84:199–214
Webster PJ, Moore AM, Loschnigg JP, Leben RR (1999) Coupled ocean-atmosphere dynamics in the Indian Ocean during 1997– 1998. Nature 401:356–360
