ACCELERATING IMPACTS OF TEMPERATURE-INDUCED CORAL BLEACHING IN THE CARIBBEAN
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1 Ecology, 86(8), 2005, pp by the Ecological Society of America ACCELERATING IMPACTS OF TEMPERATURE-INDUCED CORAL BLEACHING IN THE CARIBBEAN JOHN P. MCWILLIAMS, 1,2 ISABELLE M. CÔTÉ, 3,4 JENNIFER A. GILL, 2,3 WILLIAM J. SUTHERLAND, 3 AND ANDREW R. WATKINSON 1,2,3 1 Centre for Ecology, Evolution and Conservation, School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ UK 2 Tyndall Centre for Climate Change Research, Norwich NR4 7TJ UK 3 Centre for Ecology, Evolution and Conservation, School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ UK Abstract. Coral bleaching is a stress-related response that can be triggered by elevated sea surface temperatures (SST). Recent increases in the frequency of coral bleaching have led to concerns that increases in marine temperatures may threaten entire coral reef regions. We report exponential increases in the geographical extent and intensity of coral bleaching in the Caribbean with increasing SST anomalies. A rise in regional SST of 0.1 C results in 35% and 42% increases in the geographic extent and intensity of coral bleaching, respectively. Maximum bleaching extent and intensity are predicted to occur at regional SST anomalies of less than 1 C, which coincides with the most conservative projections for warming in the Caribbean by the end of the 21st century. Coral bleaching is therefore likely to become a chronic source of stress for Caribbean reefs in the near future. Key words: Caribbean; climate change; coral bleaching; sea surface temperature; thermal stress. INTRODUCTION Coral bleaching, the whitening of corals due to loss of symbiotic algae and/or their pigments (see Plate 1), is a response that can be triggered by a variety of stressors acting at local scales. These stressors include solar radiation, salinity shock, sedimentation, disease, and temperature increases (Brown 1997). Much recent research has focused on the latter, in part because the frequency and geographic extent of coral bleaching events appears to have increased since the early 1980s (Goreau and Hayes 1994, Goreau et al. 2000), concomitant with a global rise in sea surface temperatures (SST; Strong 1989). This potential direct link between anomalously high temperatures and coral bleaching (Hoegh-Guldberg 1999, Hughes et al. 2003, West and Salm 2003; but see Atwood et al. 1992) raises concerns that rising sea temperatures, driven by global climate change, could cause an increase in the frequency and severity of coral bleaching events, compounding the effects of localized anthropogenic stressors that already affect coral reefs (Hoegh-Guldberg 1999, Reaser et al. 2000, Hughes et al. 2003). Laboratory studies have unequivocally demonstrated that elevated seawater temperatures can trigger coral bleaching (e.g., Hoegh-Guldberg and Smith 1989, Glynn and D Croz 1990), which suggests the existence of bleaching temperature thresholds. Subsequent field studies of the link between high SSTs and the onset of Manuscript received 1 November 2004; revised 4 February 2005; accepted 1 March Corresponding Editor: S. G. Morgan. 4 Corresponding author. i.cote@uea.ac.uk 2055 bleaching have confirmed that the two often coincide (e.g., Cook et al. 1990, Smith 2001). However, bleaching temperature thresholds, if they exist, appear to be highly variable. For example, Brown (1997) reported that bleaching in Thailand and Tahiti was observed only when SST exceeded the seasonal maximum. Goreau et al. (1993) found that at seven Caribbean sites, bleaching appeared to take place only when temperature was 1 C above the long-term average for the warmest month. Hoegh-Guldberg (1999) reported thermal thresholds for seven sites around the world, but these thresholds differed among sites ( C). Applications of the concept of thermal thresholds in predictive models of bleaching onset sometimes incorporate an element of time that reflects cumulative heat stress. For example, Gleeson and Strong (1995) developed degree heating weeks indices for Bermuda, Belize, Jamaica, and Tahiti based on cumulative positive temperature anomalies. Similarly, Berkelmans (2002) incorporated cumulative thermal stress in the development of predictive bleaching curves for several sites on the Great Barrier Reef. In addition, Winter et al. (1998) showed that three temperature-related threshold indices (maximum daily SST, number of days 29.5 C, and number of days 30 C) were equally well related to the onset of past bleaching events in Puerto Rico. While the threshold approach may be useful for predicting the localized onset of coral bleaching, there may be several drawbacks to its use. For example, thresholds may not be comparable between methods using different data sets (Mumby et al. 2001), or between
2 2056 JOHN P. MCWILLIAMS ET AL. Ecology, Vol. 86, No. 8 characteristics and temperature is unknown. Uncovering such a relationship could allow predictions of the extent and intensity of bleaching events on a regional scale. It may also allow the rigorous and quantitative definition of terms such as mild or mass bleaching which are often used qualitatively in regional assessments (Glynn 1993, Westmacott et al. 2000). Given the concerns that rising sea temperatures threaten entire reef regions (e.g., Hoegh-Guldberg 1999, Reaser et al. 2000), it is important to assess coral bleaching quantitatively and at larger spatial scales than individual reefs or countries. In this paper, we therefore examine the relationships between yearly temperature anomalies and the geographic extent and intensity of coral bleaching on a Caribbean-wide scale over two decades. Although nonclimatic sources of stress (e.g., disease, overfishing, and pollution) have been relatively more important than coral bleaching in causing the recent decline of live coral cover on Caribbean reefs (Gardner et al. 2003, Bellwood et al. 2004), increases in sea surface temperatures are widely perceived as a serious future threat for reefs (Hoegh- Guldberg 1999, Reaser et al. 2000, Gardner et al. 2003). Our results suggest that episodic bleaching events could become a chronic source of stress for Caribbean reefs in the near future. PLATE 1. Bleached Montastrea cavernosa on the bank reef of Barbados. Photo credit: Karen L. Cheney. sites with different coral species compositions if responses vary between species (Hoegh-Guldberg and Salvat 1995, Baird and Marshall 2002). Thermal thresholds also do not take into account other climatic variables that may influence bleaching (e.g., cloud influence on radiative stress) (Mumby et al. 2001). Invariably, the thresholds reported are specific to individual countries or reefs within countries. Furthermore, thresholds may predict the onset of bleaching, but not its intensity or geographic extent. To our knowledge, no regional-scale empirical studies exist of the relationship between temperature and the spatial extent and intensity of bleaching (defined here as the proportion of coral colonies bleached at a given location) in the field beyond any bleaching threshold. The existence of thermal thresholds might imply a step function in coral bleaching, but the relationship between bleaching extent or intensity and temperature might be expected to be more gradual. It is known, for example, that the geographic extent of bleaching within a region can vary greatly among bleaching events (Reaser et al. 2000, Hughes et al. 2003). The intensity of bleaching can also vary among sites within the same year (CARICOMP 1997) and among years at the same site (Winter et al. 1998, Mumby et al. 2001). This variability is not consistent with the idea of a simple step function, but the exact nature of the relationship between variation in bleaching event METHODS We collated reports of bleaching occurring on Caribbean coral reefs between 1983 and 2000 from published literature, correspondence and internet sources. We noted the time (month, year) and location of bleaching and, if quantified, bleaching intensity. Years that were referred to in the literature as mass bleaching or severe bleaching events for the region were also recorded. The most commonly quantified measure of bleaching intensity was the proportion of coral colonies in an area that was affected by bleaching; hence, we use this parameter as our quantitative measure of bleaching intensity. The main bleaching period in the Caribbean occurs during the summer (Strong et al. 1997, Goreau et al. 2000), specifically from August to October (Fig. 1). We therefore focused exclusively on these months; any reports suggesting bleaching from causes unrelated to temperature were excluded (e.g., bleaching at Snake Keys, Belize, in 1997 was probably caused by low salinity stress; Wilkinson 2000). In an attempt to reduce temporal and spatial biases generated by intensively studied sites, we divided the Caribbean basin into 1 latitude/longitude cells containing coral reefs (92 cells in total). Bleaching reports were allocated to a cell depending on their location. Each cell was allowed a maximum of one value per year. We used two estimates of regional bleaching severity: (1) bleaching extent and (2) bleaching intensity. Regional bleaching extent was obtained for every year by counting the number of cells reporting bleaching
3 August 2005 REGIONAL SEVERITY OF CORAL BLEACHING 2057 FIG. 1. Distribution of bleaching reports (n 182) in the Caribbean between 1983 and 2000 in relation to month of onset of bleaching. were derived from the ReefBase database (available online at ). from August to October comprise 75% of the total. and calculating the area over which bleached cells were distributed using minimum convex polygons (Arc- View, ESRI, Redlands, California, USA; Covex Hulls, Jenness Enterprises, Flagstaff, Arizona, USA). A minimum of three bleached cells was required to generate a polygon. Regional bleaching intensity was calculated by averaging multiple values (percentage of colonies bleached), first within individual cells, and then using cells across the region to produce one intensity value per year. We obtained sea surface temperature anomalies from the MOHSST6 (UK Met Office Historical Sea Surface Temperature; Parker et al. 1995) data set, which provides in situ monthly SST anomalies globally for 5 latitude/longitude cells from 1856 to the present. These anomalies are relative to monthly means for the period of 1961 to SST anomalies were taken from 15 cells covering the Caribbean for the months of August, September, and October, and averaged to provide a single Caribbean summer mean SST anomaly for each year. MOHSST6 data have been previously used elsewhere to demonstrate that high temperatures coincide with coral bleaching (Brown 1997, Spencer et al. 2000). Data for the number of cells bleached and the mean percentage of colonies bleached were log 10 transformed to generate linear relationships with temperature. All bleaching reports used in this study are summarized in Appendices A and B. anomalies (Fig. 2). Thus, a 0.1 C rise in regional SST produced a 35% increase in the number of cells reporting bleaching. Those years that were reported in the literature as mass bleaching events occurred at regional SST anomalies of 0.2 C and above. The area encompassing bleaching reports increased linearly with summer SST anomalies (Fig. 3). Those years that were reported in the literature as mass bleaching events encompassed an area from km 2 in 1990 to km 2 in 1998, which covered the entire area studied in this paper. Data on bleaching intensity were only available for eight years, demonstrating the paucity of quantitative records. Despite the small sample size, a strong logarithmic relationship was evident between the mean percentage of coral colonies affected by bleaching and regional SST anomalies (Fig. 4). This relationship indicates that a 0.1 C rise in SST anomaly produces a 42% increase in the mean percentage of coral colonies bleached. The number of cells in which bleaching was recorded and mean percent bleaching intensity (both log 10 transformed) were strongly positively correlated (r 0.89, n 8, P 0.003). The number of cells in which bleaching was recorded, and the (log 10 -transformed) area over which bleaching reports were distributed, were also strongly positively correlated (r 0.93, n 11, P 0.001). DISCUSSION Both the spatial extent and the intensity of coral bleaching on Caribbean reefs correlate strongly and positively with sea surface temperature anomalies at the regional scale. A 0.1 C increase in regional SST produces a 35% increase in the number of coral reef cells reporting bleaching and a 42% increase in the RESULTS Increasing SST anomalies are used here to refer to increasingly positive temperature anomalies. Summer (August October) SST anomalies increased from 1983 to 2000 (r , n 18, P 0.012) with the maximum anomaly occurring in 1998 ( 0.72 C) and the minimum in 1984 ( 0.51 C), relative to the base period. The number of 1 cells in which bleaching was recorded each year increased logarithmically with SST FIG. 2. The relationship between regional SST anomalies and the percentage of 1 cells from which at least one coral bleaching occurrence was recorded during August October in the Caribbean between 1983 and Each data point represents one year. Solid circles represent years described in the literature as mass bleaching events, open circles represent other years. The solid line represents the regression line (log[cells] 1.34[SST] 0.71; r , n 18, P 0.001). The dashed line shows the SST at which maximum bleaching extent should occur based on extrapolation of the regression line.
4 2058 JOHN P. MCWILLIAMS ET AL. Ecology, Vol. 86, No. 8 FIG. 3. The relationship between regional SST anomalies and the area encompassing all cells reporting bleaching from 1983 to Solid circles represent years described in the literature as mass bleaching events; open circles represent other years. The solid line represents the regression line (area 3784[SST] 909; r , n 11, P 0.001). mean percentage of coral colonies affected by bleaching. The clear regional link between temperature and bleaching offers a tool to help define quantitatively episodes of mass bleaching, as well as predict the severity of future bleaching events. Future assessments would also need to take account of whether coral was lost completely from any of the cells, although given their size this seems unlikely in the near future. It is important to remember that the associations reported here between coral bleaching and SST anomalies do not represent direct physiological relationships because the SST data were averaged over the entire Caribbean region. These regional temperatures therefore do not reflect the actual temperatures that were experienced at localities where corals bleached. Instead, small increments in regional SST anomalies may simply indicate an increasing number of local temperature hotspots across the region. For example, an increase in regional anomaly of 0.1 C may represent local increases of 1 C in approximately 32 1 cells, i.e., about 10% of ocean cells in the Caribbean. Our results indicate that as regional sea temperatures increase in the Caribbean, coral bleaching is reported in more cells (Fig. 2) and over a larger area (Fig. 3). The highest data point in Fig. 3, which relates to 1998, is probably close to the maximum area over which bleaching can occur because bleaching in that year was reported along all edges of the Caribbean basin. This near-maximum area was achieved with 44 cells reporting bleaching, i.e., only 48% of the total number of cells containing coral reefs in the Caribbean. Thus, SSTs higher than those experienced in 1998 are not likely to increase significantly the overall area affected by bleaching, although the number of affected cells is likely to rise until all Caribbean cells have reported bleaching in a year. However, the latter scenario is unlikely because local factors (e.g., cloud cover) can act to reduce the stress caused by high temperatures, thus causing patchiness in bleaching (Mumby et al. 2001). We also found a higher proportion of bleached coral colonies in years of higher temperature anomalies (Fig. 4). Although the intensity of bleaching does not directly reflect coral mortality, particularly in the Caribbean (e.g., Glynn 1983, Goreau et al. 2000, Aronson et al. 2002), it may be a useful indicator of stress because several sublethal effects are associated with bleaching. These effects range from reduced coral growth (Goreau and Macfarlane 1990) and reproduction (Szmant and Gassman 1990) to increased susceptibility to disease (Mitchelmore et al. 2002), all of which can add to other sources of stress to increase rates of coral decline (Hoegh-Guldberg 1999, Gardner et al. 2005). Reported intensities of bleaching may have been affected by the timing of surveys since the percentage of colonies affected by bleaching will differ between the onset, peak and recovery periods (CARICOMP 1997). However, it is not clear to us that the timing of reporting should be biased in relation to sea surface temperature. Despite the growing amount of work conducted on coral bleaching, there is still no standard quantitative measure of bleaching severity (Glynn 1993, Westmacott et al. 2000). Mass bleaching typically refers to a geographically widespread bleaching event, a term that has been applied to individual countries (e.g., Mumby et al. 2001) and to reef regions (e.g., Wilkinson 1998). For the Caribbean basin, four years (1987, 1990, 1995, and 1998) have been described in the literature as being mass, severe, or widespread bleaching events (e.g., Williams et al. 1987, Holden 1995, Wilkinson 1998, Goreau et al. 2000). Our results suggest that these qualitative descriptions correspond empirically to bleaching of widespread regional extent (i.e., 10 cells reporting bleaching, Fig. 2) and high intensity (i.e., 20% colonies bleached, Fig. 4). However, qualitative assessments of bleaching have failed to identify 1999 as a year of mass bleaching, despite the fact that FIG. 4. The relationship between the percentage of coral colonies (mean SE) affected by bleaching and regional SST anomalies in the Caribbean. Each data point represents one year. Solid circles represent years described in the literature as mass bleaching events. The solid line represents the regression line (log[percentage of colonies bleached] 1.47[SST] 0.77; r , n 8, P 0.012). The dashed line shows the SST at which maximum bleaching intensity (100% of colonies) should occur based on extrapolation of the regression line.
5 August 2005 REGIONAL SEVERITY OF CORAL BLEACHING 2059 the extent of bleaching in 1999 was greater than all other years, except for 1998 (Figs. 2 and 3). Note, however, that the average proportion of coral colonies bleached in 1999 was lower than expected given the SST anomaly and lower than for other mass-bleaching years (Fig. 4). It is possible that this widespread, but low-intensity event went largely unnoticed because of the attention focused on the globally unprecedented bleaching events of the previous year (Wilkinson 1998, 2000). This oversight reinforces the need for an objective means for assessing the severity of coral bleaching events. The Caribbean Basin is expected to experience continued warming in the future, but the magnitude of this temperature increase is uncertain (Wigley and Santer 1993). For example, with a doubling of CO 2, SSTs may rise by 1 2 C by 2100 (Intergovernmental Panel on Climate Change [IPCC] 1998, McClean and Tysban 2001). Alternative estimates forecast a rise of 1 3 C between the early 1990s and (Wigley and Santer 1993). Our regression models predict maximum bleaching extent (i.e., 100% of coral-bearing cells) and maximum bleaching intensity (100% of coral colonies) when regional SST anomalies reach C and C, respectively. These estimates of 100% bleaching extent and intensity are slightly below the most conservative forecasted temperature increases, suggesting that coral bleaching could become a chronic source of stress throughout the entire Caribbean by the end of the 21st century. Although coral species may adapt to a warmer climate (Baker et al. 2004, Rowan 2004), the rate of adaptation may be outpaced by the rate of environmental change (Hughes et al. 2003). The increasing frequency of coral bleaching events, both in the Caribbean and elsewhere in the world, suggests that this may already be the case. ACKNOWLEDGMENTS This research was funded by the Tyndall Centre for Climate Change Research and the Joint Nature Conservation Committee (UK). LITERATURE CITED Aronson, R. B., W. F. Precht, M. A. Toscano, and K. H. Koltes The 1998 bleaching event and its aftermath on a coral reef in Belize. Marine Biology 141: Atwood, D. K., J. C. Hendee, and A. Mendez An assessment of global warming stress on Caribbean coral reef ecosystems. Bulletin of Marine Science 51: Baird, A. H., and P. A. Marshall Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Marine Ecology Progress Series 237: Baker, A. C., C. J. Starger, T. R. McClanahan, and P. W. Glynn Corals adaptive response to climate change. Nature 430:741. Bellwood, D. R., T. P. Hughes, C. Folke, and M. Nyström Confronting the coral reef crisis. Nature 429: Berkelmans, R Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef. Marine Ecology Progress Series 229: Brown, B. E Coral bleaching: causes and consequences. Coral Reefs 16:S129 S138. CARICOMP Studies on Caribbean coral bleaching, Pages in H. A. Lessios and I. G. Macintyre, editors. Proceedings of the Eighth International Coral Reef Symposium (Panama, June 1996). Smithsonian Tropical Research Institute, Balboa, Republic of Panama. Cook, C. B., A. Logan, J. Ward, B. Luckhurst, and C. J. Berg Jr Elevated temperatures and bleaching on a high latitude coral reef: the 1998 Bermuda event. Coral Reefs 9: Gardner, T. A., I. M. Côté, J. A. Gill, A. Grant, and A. R. Watkinson Long-term region-wide declines in Caribbean corals. Science 301: Gardner, T. A., I. M. Côté, J. A. Gill, A. Grant, and A. R. Watkinson Hurricanes and Caribbean coral reefs: impacts, recovery patterns, and role in long-term decline. Ecology 86: Gleeson, M. W., and A. E. Strong Applying MCSST to coral reef bleaching. Advances in Space Research 16: Glynn, P. W Extensive bleaching and death of reef corals on the Pacific Coast of Panama. Environmental Conservation 10: Glynn, P. W Coral reef bleaching ecological perspectives. Coral Reefs 12:1 17. Glynn, P. W., and L. D Croz Experimental evidence for high temperature stress as the cause of El Niño coincident coral mortality. Coral Reefs 8: Goreau, T., and R. L. Hayes Coral bleaching and ocean hot spots. Ambio 23: Goreau, T. J., R. L. Hayes, J. W. Clark, D. J. Basla, and C. N. Robertson Elevated sea surface temperatures correlate with Caribbean coral reef bleaching. Pages in R. A. Geyer, editor. A global warming forum: scientific, economic and legal overview. CRC Press, Boca Raton, Florida, USA. Goreau, T. J., R. L. Hayes, and T. McClanahan Conservation of coral reefs after the 1998 global bleaching event. Conservation Biology 14:5 15. Goreau, T. J., and A. H. Macfarlane Reduced growth of Montastrea annularis following the coralbleaching event. Coral Reefs 8: Hoegh-Guldberg, O Climate change, coral bleaching and the future of the world s coral reefs. Marine and Freshwater Research 50: Hoegh-Guldberg, O., and B. Salvat Periodic massbleaching and elevated sea temperatures bleaching of outer reef slope communities in Moorea, French Polynesia. Marine Ecology Progress Series 121: Hoegh-Guldberg, O., and G. J. Smith The effect of sudden changes in temperature, irradiance and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata (Esper 1797) and Seriatopora hystrix (Dana 1846). Journal of Experimental Marine Biology and Ecology 129: Holden, C Reef bleaching spreads in Caribbean. Science 270:919. Hughes, T. P., et al Climate change, human impacts and the resilience of coral reefs. Science 301: Intergovernmental Panel on Climate Change (IPCC) The regional impacts of climate change: an assessment of vulnerability. A Special Report of IPCC Working Group 2. Cambridge University Press, Cambridge, UK. McClean, R. F., and A. Tysban Coastal Zones and Marine Ecosystems. Pages in J. J. McCarthy, O. F. Canziani, N. A. Leary, D. J. Dokken, and K. S. White, editors. Climate change 2001: impacts, adaptation, and vulnerability. Cambridge University Press, Cambridge, UK.
6 2060 JOHN P. MCWILLIAMS ET AL. Ecology, Vol. 86, No. 8 Mitchelmore, C. L., J. A. Schwarz, and V. M. Weis Development of symbiosis-specific genes as biomarkers for the early detection of cnidarian algal symbiosis breakdown. Marine Environmental Research 54: Mumby, P. J., J. R. M. Chisolm, A. J. Edwards, S. Andrefouet, and J. Jaubert Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event. Marine Ecology Progress Series 222: Parker, D. E., C. K. Folland, and M. Jackson Marine surface temperature: observed variations and data requirements. Climatic Change 31: Reaser, J. K., R. Pomerance, and P. O. Thomas Coral bleaching and global climate change: scientific findings and policy recommendations. Conservation Biology 14: Rowan, R Thermal adaptation in reef coral symbionts. Nature 430:742. Smith, N. P Weather and hydrographic conditions associated with coral bleaching: Lee Stocking Island, Bahamas. Coral Reefs 20: Spencer, T., K. A. Teleki, C. Bradshaw, and M. D. Spalding Coral bleaching in the Southern Seychelles during the Indian Ocean warm event. Marine Pollution Bulletin 40: Strong, A. E Greater global warming revealed by satellite-derived sea-surface-temperature trends. Nature 338: Strong, A. E., C. B. Barrientos, C. Duda, and J. Sapper Improved satellite techniques for monitoring coral reef bleaching. Pages in H. Lessios and I. G. Macintyre, editors. Proceedings of the Eighth International Coral Reef Symposium. Volume 2. Smithsonian Tropical Research Institute, Balboa, Republic of Panama. Szmant, A. M., and N. J. Gassman The effects of prolonged bleaching on the tissue biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8: West, J. M., and R. V. Salm Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conservation Biology 17: Westmacott, S., K. A. Teleki, S. Wells, and J. West Management of bleached and severely damaged coral reefs. IUCN, Gland, Switzerland, and Cambridge, UK. Wigley, T. M. L., and B. D. Santer Future climate of the Gulf/Caribbean Basin from atmospheric general circulation models. Pages in G. A. Maul, editor. Climatic change in the Intra-Americas Sea. Chapman and Hall, New York, New York, USA. Wilkinson, C The mass bleaching event around the world. Australian Institute of Marine Science, Townsville, Australia. Wilkinson, C. R., editor Status of coral reefs of the world Australian Institute of Marine Science, Townsville, Australia. Williams, E. H., C. Goenaga, and V. Vicente Mass bleachings on Atlantic coral reefs. Science 238: Winter, A., R. S. Appeldorn, A. Bruckner, E. H. Williams, and C. Goenaga Sea surface temperatures and coral reef bleaching off La Parguera, Puerto Rico (northeastern Caribbean Sea). Coral Reefs 17: APPENDIX A Bleaching reports used to asses the geographical extent of coral bleaching in the Caribbean are available in ESA s Electronic Data Archive: Ecological Archives E A1. APPENDIX B Bleaching reports used to calculate the intensity (percentage of colonies affected) of coral bleaching in the Caribbean are available in ESA s Electronic Data Archive: Ecological Archives E A2.
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