GCRA
OVERVIEW
FAQ
NEWS
ARTICLES
PHOTOS
REEF ISSUES
RESTORATION
PAPERS
LINKS
|
|
|
|
Elevated Sea
Surface Temperatures Correlate Thomas J. Goreau, Raymond L. Hayes, Jennifer W. Clark, Daniel J. Basta, and Craig N. Robertson NOTE: This paper was the first to examine detailed long term satellite sea surface temperature records with regard to coral bleaching. It showed that coral bleaching at sites across the Caribbean region took place following temperatures which reached levels only around 1 degree C above average in the warmest months. This paper was published in A Global Warming Forum: Scientific, Economic, and Legal Overview, (R. A. Geyer, editor), 1992, CRC Press, Boca Raton, Florida USA, Chapter 9, pages 225-255. I.
INTRODUCTION In contrast to previous bleaching events, those of the late 1980s affected unprecedented numbers of individual colonies and species of coral. Bleaching was observed at the greatest depths to which symbiotic corals are found and appeared over large areas tree from any obvious stress other than elevated temperature (Williams et al. 1987). Bleached corals show altered pigment concentrations (Kleppel et al. 1989), disruption of function at the cellular and biochemical lexels (Glynn et al. 1985; Hayes 1988). reduced photosynthesis (Porter et al. 1989) and failure to grow a skeleton (Goreau and Macfarlane 1990a) or to deposit annual dense skeletal bands (Goreau and Dodge unpublished data). Corals which survive bleaching may take up to ten months to regain normal pigmentation and growth, but reduced symbiotic algae causes starvation which weakens their ability to complete with seaweed overgrowth (Goreau and Macfarlane 1990b). Numerous observers of recent mass coral reef bleaching events have suggested that elevated water temperatures were a likely environmental cause, however, there has remained a lack of adequately documented seawater temperatures from coral reef sites. In this paper, biweekly National Oceanic and Atmospheric Administration (NOAA) satellite-derived Ocean Features Analysis (OFA) is examined for seven sites in the Caribbean Coral Reef Province where bleaching was reported. These analyses show that bleaching events have invariably accompanied the highest extremes of water temperature in the late 1980s. Ii. Methods: Processing And Calibration Of Satellite Temperature Data The seven locations which were selected as our data set are indicated geographically in Figure I. High resolution satellite data were used, with a pixel size of 4 km. Polar orbiting Tiros-N/NOAA (Kidwell 1986) weather satellites with Advanced Very High Resolution Radiometer sensors (AVHRR) provided these data. The AVHRR features a cross-track scanning system with three channels which record in the thermal IR spectral rance. The southern boundary of those data was 18 N, passing through central Jamaica and Puerto Rico. and covering most of the region's reefs where bleaching has been intensively observed (see Figure 2). This range did not include sites such as Belize, Curacao, Colombia. Barbados. and the Lesser Antilles, where bleaching has also been reported. FIGURE I. Map of the Greater Caribbean Coral Reef Province. showing the locations of the seven sites monitored and major regional surface current flows according to Sverdup et al., 1942. Satellite data provide global coverage of sea surface temperature (SST). The U.S. Department of Commerce's NOAA has satellites equipped with high resolution IR sensors. Polar-orbiting IR satellite imagery is the primary data source for generating the OFA. These IR sensors detect sea surface brightness which is analyzed to generate sea surface thermal structures of the OFA. The South Panel OFA (Figure 2) is generated twice a week. The bulk of SST values on the chart are from thermal IR satellite data, with a spatial resolution of 4 km. supplemented by much spatially sparser SST measurements from buoys, expendable bathythermographs (XBTs), and ships in areas where cloud cover prevents direct surface observations. Because the final data set contains numbers from a variety of sources, it is referred to as "blended''. Almost all readings published in the OFA have been made by the same oceanographer (J. W. Clark). Sea surface without cloud cover is selected for enumeration to avoid artificial reduction in SST. Presence of even small and thin clouds in the pixel would bias the data toward lower temperatures. However, this represents a minor problem in the Caribbean since well developed convection patterns in the lower atmosphere provide a fine scale mosaic of cloudy and cloud-free areas in regions of ascending and descending air, respectively. Cloud distributions are usually such that cloud-free areas can be found fairly close to any given site, except during relatively rare cases of large scale frontal cloud systems which typically occur in winter. To construct the SST at each site, the measured values nearest to each location were averaged. The data used could consist of a single measurement immediately offshore, or the average of up to four measurements within several hundred kilometers of the site, weighted by hand according to distance. This means that the values reported have in effect been averaged over a spatial scale of a few hundred kilometers, although on very cloudy days. or in the case of Puerto Rico, where data is relatively sparse compared to other sites, the average scale may be larger. Averaging done independently by different observers (T. J. Goreau and R. L. Hayes) produced monthly average values which are within 0.09 + 0.18°C (n = 14). Monthly mean values from the OFA as described above were calibrated for the north coast of Jamaica against in situ measurements made at 3 m depth on the fore reef at the Discovery Bay Marine Laboratory (Discovery Bay, Jamaica) from 1985 to 1990. showing that: Tsat = 1.998 + 0.920 x Tmeas R = 0.897 P = <0.001 n = 65 where R is the correlation coefficient, P is the probability that the variables are uncorrelated, and n is the number of measurements. Satellite derived values were lower than measured water temperatures by 0.08 degrees at 26.00°C, and by 0.40 degrees at 30.00°C. Comparison of OFA data and monthly mean water temperatures measured on the west coast of Grand Cayman at 10 m depth from May to October 1990 showed that the two correlated strongly (R = 0.9634, P = 0.002, n = 6), but satellite values were higher than in situ values by a statistically insignificant (P = 0.060) amount, 0.177 + 0.502 C. Differences between satellite and in situ data at higher temperatures in Jamaica could be caused by increased surface evaporation and atmospheric water vapor as well as sea surface layer effects. Cloud contamination, which is more likely near Jamaica than near Cayman due to topographically induced convection, could bias satellite SST estimates to lower values when ocean temperatures are high. Although differences between satellite and in situ records are small, additional data from the OFA data set should be examined to see if it may offer clues for evaluating greenhouse feedbacks caused by water vapor. Local heating of coastal waters where bleaching occurs is a function of the extent of shallow coastal banks and of circulation between shelf waters and open ocean. Shallow banks are nonexistent at Jamaica, Cayman, and Puerto Rico sites, small at Cozumel and Bermuda, but extensive at Florida and Bahamas sites. Exchange between shelf waters and ocean waters is a rapidly changing function of fluctuating winds and currents, so corrections for inshore-offshore differences would be both site specific and temporally variable. Jamaica is unique among Caribbean islands in being a high, wet, limestone island, with numerous near shore groundwater springs with water temperatures as low as 25.7°C. which tend to cool Jamaican near shore waters. As water temperature records were only available to us from Jamaica and Cayman, corrections were not applied and could not be verified at other sites. Only detailed year-round measurements at each site would allow accurate estimation of local correction factors. In their absence, uncorrected open-ocean satellite values have been used in our analyses, even though they may be slightly different than the temperatures to which reef corals are actually exposed. Temperatures for the whole Caribbean are also available as maps at 4 to 6 degrees (about 400 to 600 km) spatial mean resolution (Reynolds, personal communication) published in NOAA's Oceanographic Monthly Summaries (OMS). These low resolution data were examined by Atwood and co-workers, to conclude that there were no unusual sea temperature anomalies in the Caribbean during the 1987 bleaching event (Atwood et al. 1988). Other researchers, using satellite SST data, reported that positive temperature anomalies were associated with coral bleaching in the Caribbean in 1987 (McCormack and Strong 1990; Strong and McCormack 1991). The low resolution OMS data were not used in our study because details of monthly SST anomalies did not correspond closely with in situ seawater temperature measurements, whereas the OFA data correlated highly with observed water temperatures. Table I shows regressions of OMS temperature anomalies against anomalies determined from the OFA data set. These results show that the OMS data considerably underestimate large positive temperature anomalies recorded by OFA data and in in situ measurements. A possible explanation is cloud contamination in the much larger pixels of the Iow resolution OMS data. TABLE I Regression of OMS vs. OFA Data Sets
Location A(°C) B R P Puerto Rico -0.03159 0.29528 0.423 0.052 Jamaica -0.08399 0.27908 0.602 0.003 Cayman -0.06039 0.29421 0.561 0.007 Cozumel +0.02282 0.33613 0.516 0.014 Florida -0.11022 0.35211 0.510 0.015 Nassau + 0.09246 0.04585 0.069 0.760 Bermuda +0.41257 0.58513 0.708 <0.001 Note: Temperature deviations from long-term averages were taken from NOAA's OMS and regressed against values taken from the OFA data set from January 1989 to October 1990 at each site (n = 22). A is the y intercept in degrees Celsius, B is the slope of the regression, R is the correlation coefficient, and P is the probability that the two data sets are unrelated. If both data sets agreed perfectly A would be 0, B would be 1, R would be 1, and P would be 0. All regressions have slopes < I. indicating that the low resolution OMS data set underestimates positive temperature anomalies compared to the high resolution OFA data. III. SITE LOCATIONS AND HYDROGRAPHIC FEATURES Water entering the Caribbean is predominantly supplied by the westward Guyana current, driven by trade winds through passages between the Lesser Antilles (Figure 1). A small amount of water enters via the Mona Passage between Puerto Rico and the Dominican Republic and via the Windward Passage between Haiti and Cuba. Surface water is transported westward through most of the Caribbean, veering northwestward and then northward towards the only exit, the Yucatan Channel. There the outflow is squeezed into a powerful northward jet flow into the Eastern Gulf of Mexico, which curves around 180 degrees to form the Loop Current. The rate of water flow out of the Caribbean determines the strength of the current, its northern extent, and amount of mixing with water from the Gulf of Mexico. The current then flows eastward between Florida and Cuba, before turning north between Florida and the Bahamas to form the Florida Current. The flow follows the edge of the continental shelf to Cape Hatteras, where it turns northeastward as the Gulf Stream. The Gulf Stream is subsequently influenced by admixture with North American coastal shelf waters and the Sargasso Sea as it passes north of Bermuda towards northwestern Europe. The weather of eastern North America and Europe is influenced by the position and strength of the Gulf Stream. Eddies form in geographically protected embankments on the fringes of the Caribbean: (1) in the southwestern Caribbean between Colombia, Panama, Costa Rica, and Nicaragua; (2) in the western Caribbean between Honduras and Belize: (3) in the shelf waters of Southern Cuba; (4) in the Gulf of Mexico: and (5) also in the central Caribbean between Haiti, Jamaica, Cayman, and Cuba. Surface waters in eddies have a prolonged local residence time, and may gain additional heat from solar radiation. This is counteracted by localized sporadic upwelling along leeward shores, heavy rainfall along the Colombian. Panamanian, Costa Rican, Honduran, and Belizean coasts, and seasonally strong winter cooling along the northern fringes of the Gulf of Mexico. Fringing reef growth in mainland coastal waters is often poor, with reefs found offshore (e.g.. the Belize Barrier Reef, the Bay Islands, San Andres, and Providencia). or in locally protected coastal sites. The region between Cayman, Cuba, Jamaica, and Haiti lies in the lee of the mountains of Hispaniola, and warms more than central Caribbean waters when winds are calm, especially in the Bay of Gonave between the Massif de la Hotte and the Massif du Nord of westem Haiti and in the Gulf of Batabano off southern Cuba. The three northernmost sites lie outside the trade-wind belt during winter, when they are exposed to continentally derived cyclonic air masses, but the strength of their major ocean currents is primarily influenced by volume and strength of Caribbean heat loss. Most of the rest of the region is subjected to uniform trade winds from the east year-round, but during winter, cold continental air masses from North America cause occasional frontal systems to penetrate the region. Distinctive hydrographic features of each site are 1. Northern Puerto Rico—There is no coastal shelf and the bottom drops steeply into the Puerto Rico Trench, the deepest waters in the North Atlantic. Currents are predominantly westward, and representative of entering water pushed into the Caribbean Sea by the Trade Winds. Reef development in Puerto Rico is best in the southwest, but is poor and declining due to high sediment loads from erosion (Acevedo et al. 1989). 2. North-Central Jamaica—There is no coastal shelf and the bottom drops steeply into the Cayman Trench, the deepest waters in the Caribbean. Currents are predominantly westward. Because Northern Jamaica is mostly limestone, there is little surface drainage or erosion, and extremely well-developed fringing reefs extend all along the North Coast. 3. Grand Cayman—The Cayman Islands lie atop a narrow ridge, with the Cayman Trench to the south and a deep basin to the north. There is virtually no terrestrial runoff from these flat and dry islands. Currents and winds are very similar to the north coast of Jamaica. Cayman lies directly in the path of Caribbean surface waters flowing towards the Yucatan Channel. 4. Eastern Cozumel—Cozumel lies on the western side of the Yucatan Channel, and offshore currents are predominantly northward. Cozumel waters are an admixture of central Caribbean outflow with entrained waters which have been trapped in the gyre between Yucatan, Belize, and Honduras, and in the southwestern Caribbean eddy. 5. Mid-Florida Keys—Florida reefs lie on an extensive submarine bank, and reefs are bathed by the edge of the Florida Current. When the Loop Current is strong. the flow axis tends to lie further offshore, exposing reefs to water moving between the Keys from Florida Bay. Water circulates poorly on the shallow West Florida Shelf and in the Northern Gulf of Mexico. Calm conditions intensify local heating in summer, and cold fronts cause intense winter cooling. Reef conditions have deteriorated recently due to climatic extremes, boat damage, and eutrophication from septic tanks (LaPointe et al., 1990) and coral cover is declining (Porter, personal communication). 6. New Providence (Nassau), Bahamas—Water masses are influenced by the Florida Current to the west, and by the westward flowing Antillean current driven by trade winds and the Sargasso Sea to the east. Very shallow and extensive banks limit water exchange and cause seasonal extremes of cooling and heating during calm weather. Reefs are limited to narrow fringes at bank edges. Temperatures were evaluated for an area about 12 km south of Nassau, near the boundary of the Bahamas banks and the deep water Tongue of the Ocean passage, at a site where bleaching has been recorded (Hayes, personal communication). 7. Bermuda—The extreme northern limit of coral reef growth, Bermuda is a largely submerged seamount atoll. A small shallow shelf causes some local heating. Waters do not get as warm here as at the other sites, since solar radiation is less intense and the dominant influence is interior waters of the North Atlantic Sargasso Sea Gyre. Conditions are near the lower tolerance limit of corals (ca. 18°C) during passage of North American winter air masses. Most sites monitored represent coastal waters of islands that have active private or governmental marine laboratories that are conducting coral reef research. The University of Puerto Rico at Mayaguez, Department of Marine Sciences, maintains a marine laboratory off La Parguera in the southwestern portion of the island. For over 30 years, research activities have been conducted at that facility. The University of the West Indies has operated the Discovery Bay Marine Laboratory and the Port Royal Marine Laboratory since the early 1950s. These laboratories were the sites for the pioneering reef studies using SCUBA initiated by the late Professor T. F. Goreau and colleagues (Goreau 1959; Goreau and Goreau 1973; Goreau et al. 1979). In the Cayman Islands, the governmental Natural Resources Unit has conducted coral reef research and monitoring of the Marine Park system for several years. Active sport diving enterprises on Grand Cayman Island, Nassau, and Cozumel have been developed during the past 20 years. The Florida Department of Natural Resources, the Looe Key National Marine Sanctuary, and the Key Largo National Marine Sanctuary have monitored reef conditions during the past 20 years. The Bermuda Biological Laboratory is one of the oldest research facilities in the western North Atlantic, and has been the site of offshore oceanographic expeditions and shore-based reef studies since the 1960s (Logan, 1988). There are no marine laboratories at Cozumel or Nassau. IV. RESULTS AND DISCUSSION: SPATIO-TEMPORAL PATTERNS OF TEMPERATURE AND BLEACHING Figure 3a shows mean monthly SST at the seven sites from May 1980 to October 1990. These data were obtained by computing monthly means of over 1000 measurements at each site from the charts, typically around 8 or 9 biweekly measurements per month. Tabular display of these numerical data are given in Table 2. All existing chart observations were used. Figure 3b shows the monthly temperature variability. Table 3 shows the mean water temperature at each site during the 1980 baseline period (May 1980 to Apal 1990). Annual temperature variability at different sites, measured by the standard deviation (S.D.) of monthly average temperature, decreases with rising mean temperature (MT): S.D. = 11.880 - 0.383 x MT R = 0.946 P = <0.001 n = 7 FIGURE 3a and b. (a) Mean annual water temperatures at each site during the 1980s: (b) monthly temperature standard deviations (S.D) at each site show minimum variability in summer. January is month 1 and December is month 12.TABLE 2 Caribbean Monthly Average SST (May 1980 to October 1990) Month Puerto Rico Jamaica Cayman Cozumel Florida Nassau Bermuda TABLE 3 Mean Decadal Temperatures (May 1980 to April 1990) Location MT S.D. Minbl Tmin Tmax Puerto Rico 27.17 1.17 29.1 24.91 29.32 Jamaica 27.84 1.17 29.6 25.57 30.30 Cayman 27.75 1.24 29.6 25.30 30.51 Cozumel 27.71 1.18 29.6 25.50 30.00 Florida 26.67 1.99 29.6 22.44 30.08 Nassau 26.42 1.99 29.3 22.94 29.99 Bermuda 23.05 2.95 27.6 18.18 28.06 Note. Mean temperatures (MT) and standard deviations (S.D.) are computed from monthly average values from May 1980 to April 1990. Minbl is the highest monthly average temperature at which bleaching was not observed, and is an estimate of the minimum bleaching temperature, Tmin and Tmax are the lowest and highest, respectively, monthly average temperatures during the baseline period. Increasing seasonal variability at colder sites is largely due to lower minimum temperatures: the highest and lowest monthly mean values during the baseline period are both proportional to mean temperature, but the lowest values increase over three times faster with increasing mean temperature as do the highest values: Tmax = 17.743 + 0.451 x MT R = 0.976 P = <0.001 n = 7 Tmin = - 18.049 + 1.561 x MT R = 0.976 P = <0.001 n = 7 where Tmax and Tmin are the highest and lowest monthly average temperatures during the baseline period, respectively. Patterns of absolute temperature maxima and of bleaching coverage in both space and time: 1. Puerto Rico (Figure 4a) had widespread mass bleaching only in 1987 (Williams and Bunkley-Williams 1990; Williams et al. 1987) and 1990 (Goenaga 1991), the warmest years of the decade. Isolated local bleaching was reported in other years (Avecedo and Goenaga 1986; Goenaga and Canals 1979) but these were largely in shallow reefs downstream from river mouths, after hurricane rains caused heavy runoff and erosion. 2. Jamaica (Figure 4b) had mass bleaching in 1987 (Gates 1990; Goreau 1990a,b: Goreau and Macfarlane, 1990), 1989 (Goreau 1990a,b), and 1990, the three warmest years in the satellite SST record. The 1987 maximum temperatures were only slightly above previous maxima, but were unique in being unusually prolonged. Most previous maxima lasted only a month, but that of 1987 was prolonged for 4 months. Reef-water temperatures reached 30°C in July, and remained at those levels until December (Gates 1990). Mass bleaching began in mid-July and reached a maximum in December. Corals then gradually recovered pigmentation, with around 5% being still visibly pale in May 1988 (Goreau and Macfarlane 1990a). Temperatures in 1988 never reached above 29.5°C. The water cooled immediately following Hurricane Gilbert, the strongest hurricane measured in the Caribbean, whose eye passed over Jamaica, Cayman, and Cozumel on September 13 to 15, prior to the historical October maximum. In 1989, reef water temperatures reached 30°C by early August (Goreau 1990a,b). Bleaching was first observed in early October, and around 80% of all corals along the north coast bleached. In 1990, temperatures were even higher, and bleaching was more intense. Only minor bleaching was found on the south coast of the island, where water was observed to be noticeably cooler than the north coast. Most of Jamaica's population, almost all industry and manufacturing, and the bulk of its pollution is on the south coast, reducing the possibility of local pollution as a cause of bleaching. Such widespread mass bleaching events had never been seen in Jamaica since coral reef research began in 1951. Isolated local bleaching occurred in Jamaica in 1963 (Goreau, 1964) and 1988 (Goreau, 1990a,b) but only in shallow reefs directly affected by muddy freshwater plumes of rivers exceptionally swollen by Hurricanes Flora and Gilbert, respectively. 3. Cayman (Figure 4c) had mass bleaching in 1987, 1989, and 1990 (Hayes 1988; Hayes and Bush 1989 and 1990; Hayes, personal communication). The exceptionally warm patterns in these years are almost identical to Jamaica, with 1987 being most prolonged and 1990 hottest. Bleaching was most intense in 1990 and more intense in 1987 than in 1989, in contrast to Jamaica. 4. Cozumel (Figure 4d) bleaching was reported only in 1987 (Williams and Bunkley Williams 1990) and 1990 (R. Sammon, personal communication). The water temperature patterns was very different from Jamaica or Cayman: 1989 was not unusually warm, and high temperatures also occurred in the early 1980s. The temperature difference with Cayman implies that central Caribbean waters are significantly mixed with waters from the Belize-Honduras and Colombia-Nicaragua embankments at Cozumel, and that either those waters were warm in the early 1980s but cooled at the end of the decade, or that Cozumel has been exposed to a greater proportion of water which has rapidly traversed the entire Caribbean. The difference may lie either in changes of cloudiness, sunshine, and rainfall in the southwestern Caribbean, or changes in ocean current flows reducing water residence time. These alternative possibilities are not distinguishable from the data available in this study, but might be tested by more detailed ocean current measurements, or by satellite altimetry. Water temperatures in 1981 were nearly as warm as in 1987, so it is possible that bleaching could have occurred then. No known reports from that period are available. Observations of bleaching at that time could strongly the hypothesis that bleaching is caused by elevated temperatures, but its absence would imply that corals have become more sensitive to temperature. FIGURE 4a to g. Mean monthly SST at each site from May 1980 to October 1990 from the NOAA satellite borne AVHRR. They have not been corrected for near shore effects. Observed mass coral-bleaching events are marked X. 5. Florida (Figure 4e) mass bleaching was most severe in 1987 (Causey 1988) 1989 and 1990 (B. Causey, personal communication). the three hottest years in the record. The 1987 bleaching was more intense than the 1989 event, which was brief because an early cold front rapidly cooled down the water. Bleaching in 1990 caused severe coral mortality. Localized bleaching was reported in 1918 (Mayor 1918), 1979 (Jaap 1979), and 1983 (Jaap 1985). The first was confined to a shallow lagoon on the Dry Tonugas, heated during calm, cloudless. sunny weather, and the second was very local in extent. The 1983 event was also local in extent. Although that year did not have an exceptional maximum monthly mean value, it included a short hot spell with one of the highest single daily water temperature value measured in shallow Florida Bay, just to the north. Fluctuations of the Florida Current could have caused highly local warming patterns around flow channels between the Keys (Jaap 1979, 1985). 6. Nassau (Figure 4f) had mass bleaching reported in 1987 (Lang), 1989 (Hayes and personal communication), and 1990—the three hottest years in the record. 1989 was cooler, and bleaching less severe than 1987 and 199O, consistent with water temperatures. 7. Bermuda (Figure 4g) shows a different temperature pattern, with exceptional warmth occurring only in 1988. This was the first year in which mass bleaching was reported (Cook et al. 1990). Bleaching in Bermuda did not coincide with bleaching at Caribbean sites in 1987. The spatial and temporal pattern of mass bleaching correlates very closely with the hottest water temperatures during the satellite record. Maximal temperatures and bleaching intensities in 1990 were the highest in the record at most sites. Obvious abnormalities in SST or bleaching were not seen during the strongest El Nino recorded in 1982 to 1983, or the weaker one in 1986 to 1987, and warm conditions were found in the Caribbean in 1989 despite cold water temperatures in the eastern Pacific. No correction was made for the effects of El Chichon, the Mexican volcano which put large amounts of sulfur aerosols into the atmosphere in 1982, reducing satellite-derived SST with a contribution from stratosphere aerosols (Strong 1984). The Caribbean lies directly upwind of the Mexican Cordillera, and would have been less affected than the Eastern Pacific, where SST measured from satellite records are known to be, low (Strong 1984, 1989; Robock 1989; Reynolds et al. 1989). The lowest maximum-monthly temperature coincident with bleaching (see Table 3) was estimated by taking the warmest monthly maximum water temperature from the satellite record for which bleaching was known not to occur, Minbl. Because bleaching is likely to be sensitive to magnitude, duration, and rate of change of temperature (Hoegh-Guldberg and Smith 1989; Glynn and D'Croz 1990) higher values over shorter intervals could result in bleaching. Minimum monthly average temperatures required for bleaching are strongly correlated with mean water temperatures: Minbl = 18.118 + 0.41591 x MT R = 0.953 P = <0.001 n = 7 Bleaching in Bermuda, the coldest site, took place at a temperature 1.5°C lower than at Jamaica, Cayman, Cozumel, and Florida. This implies that corals and/or their symbiotic algae physiologically or genetically adapt to local temperatures, so there is no single critical threshold temperature for bleaching across the entire geographical range of each species. However, all sites exceeded their local thresholds in the 1987 to 1990 period to an unprecedented amount. Our temperature data suggest that coral reef bleaching is a response to exceptionally warm water temperatures. These data can also be examined to determine whether mean water temperatures rose over the period. Trends should be most readily detectable at sites with the smallest annual range. particularly Jamaica and Cayman. Figure 5a to g shows the linear regressions to monthly temperature values from May 1980 through October 1990 at each site, using May 1980 to April 1990 as a baseline period. Table 4 shows the statistical parameters of each trend. Linear regression fits to changes in SST deviations from mean values are presented. A is the y intercept in degree Celsius; B is the slope of the regression, the mean rate of change of temperature over time, in degrees Celsius per month; the next column converts these values into average warming rates in degrees Celsius per decade over the 1980s; P is the probability that this regression could result from chance; and the final column shows the uncorrected F ratios. These values should be divided by a factor to correct for a reduced number of degrees of freedom caused by 'memory" lags in SST (Sciremammano 1979). This was estimated to be about 2 months or less from transient relaxation time scales. This correction did not change the significance of the temperature trends. Out of the seven sites examined, five showed significant increasing temperature trends during the 1980s. The trends in Puerto Rico and Cozumel are small and not statistically significant, but the increases at the five other sites are highly significant (P <0.001). Figure 6a to 6g shows the standard deviation (S.D.) of the temperature variance each month over the entire period. There is no statistically significant change in the monthly temperature variability at Bermuda or Puerto Rico. a barely significant rise at Nassau, and strongly significant decreases in monthly variability at Jamaica, Cayman, Cozumel, and Florida. These data suggest that the trend in increasing mean temperature is not a statistical artifact of increasing variability (Table 5), since variability has decreased at most sites. Figure 7 shows the temperature trends month-by-month at each site. Positive values indicate that temperatures in that month have risen over the period. At all sites the increase in temperature is greater in winter than in summer. This implies that seasonal temperature variability is decreasing because minimum temperatures are rising faster than maximum temperatures. Although maximum temperatures are correlated with bleaching, rising minimum temperatures are reducing the length of the recovery period between bleaching events. Puerto Rico and Cozumel show a summer cooling trend. FIGURE 5a to g. Linear regression of temperature records, whose parameters are given in Table 4. TABLE 4 Linear Regressions to Temperature Trends (1980 to 1990) Location A(°C) B(°C/mo) (°C/drec) P F ratio Puerto Rico 0.00229 -0.00005 - 0 006 0.967 0.00168 Jamaica -0.28097 0.00519 0.623 <0.001 21.21659 Cayman -0.23071 0.00410 0.492 <0.001 12.91092 Cozumel -0.05107 0.00116 0.139 0.352 0.87426 Flonda -0.34227 0.00614 0.737 <0.001 17.36845 Nassau -0.45303 0.00798 0.958 <0.001 33.93642 Bermuda -0.45386 0.00701 0.841 <0.001 22.76517 Note: Regression analysis of the temperature data, derived by subtracting the baseline-period mean monthly temperatures from the measured values. A is the y intercept in degrees Celsius, B is the slope of the temporal trend, in units of degrees Celsius per month and then in units of degrees Celsius per decade. P is the probability that there is no change with time, and F is the uncorrected F ratio. F values and numbers of degrees of freedom were divided by two to account for serial dependence (' memory effects"), and compared to critical F values for the reduced number of degrees of freedom using an F table. Significance of trends were unchanged. Values are from May 1980 to October 1990, using May 1980 to April 1990 as a baseline period. FIGURE 6a to g. Within-month temperature variance at each site The value plotted is the standard deviation (S.D.) of all measurements made each month—a measure of the day-to-day temperature variability. TABLE 5 Linear Regressions to Within-Month Temperature Variability (June 1980 to October 1990) Location A(°C) B(°C/mo) P Puerto Rico 0.67785 - 0.00090 0.080 Jamaica 0.69986 -0.00146 0.002 Cayman 0.69692 -0.00134 0.008 Cozumel 0.88792 - 0.00344 <0.001 Florida 0.93297 -0.00208 0.010 Nassau 0.75967 +0.00075 0.046 Bermuda 0.83446 - 0.00049 0.595
Note: The standard deviation of within-month temperature variability for each month was regressed against time. A is the y intercept in degrees Celsius, B is the rate of change of within-month temperature variability in degrees Celsius per month, and P is the probability that there is no change in monthly temperature variability. FIGURE 7. Monthly trends in temperature change at each site The temperature rate of change for each month at each site is shown At all sites the increase in temperature is greater in winter than in summer. January is month1and December is month 12. V. CONCLUSIONS
The exact spatial and temporal synchronies seen between bleaching and elevated water temperature provide strong support for the view that high water temperatures have been correlating recently with mass bleaching. No diseases or pathogenic organisms have been found (Hayes 1988; Glynn et al. 1985) and other factors known to induce localized bleaching are absent. An alternative hypothesis (that pollution is lowering the resistance of corals) is contradicted by intense bleaching in sites far from obvious sources of pollution. For a pollutant to cause this pattern, it would have to be ubiquitous and uniformly distributed in tropical waters, and have a strongly temperature dependent biological effect. The fact that the high water temperatures of the late 1980s and mass coral bleaching have not been seen before in the Greater Caribbean during nearly 40 years of continuous study of coral reef ecosystems implies that temperatures have only recently exceeded tolerance limits of the corals. Reports of increased bleaching in the Indo-Pacific region in the 1980s may suggest that these are global and not regional events. Temperature data reported from Hawaii (Jokiel and Coles 1990) show that the maximum monthly average temperatures have risen by 0.764°C per decade between 1978 and 1989 (P = 0.021), a similar trend to that seen in the Caribbean. The temperature data which we present in this paper cover a limited period. If bleaching events are part of a natural long-term cycle they must have a longer recurrence period than the observational record. Detailed studies of coral banding from 1918 to 1983 in eastern Florida corals reveal precise year-to-year correlations of growth rates with hydrological changes in the Everglades (Goreau et al. 1988). Cessation of growth during bleaching would cause missing years in the banding pattern. Exact temporal matches between coral banding and hydrological chronologies imply that there are no missing years between 1918 and 1983 and, hence, that massive bleaching did not occur in Florida during that period. Our data indicate that since 1985, tropical SST has exceeded 30 C for extended periods. Heat transfer and evaporative cooling by release of excess heat to the atmosphere (Ellsaesser 1990) or cloud formation (Ramanathan and Collins 1991) have not prevented SST from reaching 31 to 32°C on occasion. Despite suggestions that the rate of warming would not be expected to exceed 1°C/20 days, (Ellsaesser 1984, 1990), we have observed changes of 1°C within 7 to 10 days. Local SST is affected by changes in current and wind patterns, changes in vertical mixing profiles, changes in cloudiness or rainfall, and changes in sea surface height, as well as global warming. Further data are needed to separate each of these as contributing factors to the changes we report. The two coldest years, 1984, and 1986, fall in the middle of the record, and so do not bias the decadal trend. This pattern may explain why Spencer and Christie found no significant trend in their satellite microwave sounding unit (MSU) data from the 1980s (Spencer and Christy, 1990), the warmest decade on record (Jones and Wigley 1990, Hansen and Lebedeff 1987). MSU data are primarily sensitive to temperatures in the middle troposphere (channel 2) and lower stratosphere (channel 4). Since the tropical atmosphere is generally heated from below by the ocean, changes at the lower troposphere should precede changes in the upper troposphere or stratosphere. Only 10 years of observations from a small part of the Earth’s surface cannot confirm long term global trends, and only time will tell if they are short term or continuing. Mass regional bleaching in the 1980s may be accentuated in tropical surface waters by evaporative increases in total humidity, which amplify warming by a local greenhouse effect (Flohn and Kapala 1989; Ramanathan et al. 1989a,b). Organisms in tropical habitats live at temperatures much closer to their upper tolerance limits than those elsewhere, and are negatively affected by much smaller absolute temperature increases than those in cooler habitats. Corals are highly sensitive to extreme maxima in water temperature, which become more statistically frequent as mean temperature rises (Hansen and Lebedeff 1987). The increased level of mortality seen in 1990 implies that if bleaching continues many Caribbean reef corals will not survive. Reduced coral growth could eventually cause serious economic losses in terms of fisheries reductions, species losses, lack of water clarity and limestone sand production in tourist beach resorts, and loss of shoreline protection from hurricane waves and rising sea level (Williams and Bunkley-Williams 1990, Goreau 1990a,b Williams et al. 1987). Coral's exquisite biological sensitivity may make it a more reliable natural indicator of rising temperature than our best available technology. Coral reef bleaching may be providing an early visible signal of global warming. Caribbean water temperatures during 1990 reached the highest levels yet measured, according to both field measurements and the AVHRR satellite data (Hayes 1991). Coral reefs are the most species-rich oceanic ecosystem, and are major sites of ocean limestone burial. Their productivity will be severely affected if bleaching continues to inhibit coral growth. Because tropical surface waters represent a major heat storage in the Earth's climate system, and a major driving force of winds and currents which affect global weather and climate, priority should be placed on increasing the network of systematic direct water temperature measurements in the tropics. Such a program could be most economically carried out by funding the required equipment and personnel in marine laboratories near coral reefs, and increased use of the information which the high resolution OFA data contains. NOTE ADDED IN PROOF Update since this chapter was submitted: (1) 1991—Water temperatures reached near maximum levels and strong mass bleaching occurred at all seven sites and most of the Caribbean. Elevated coral mortality was seen. (2) 1992—Through August press time of this book, temperatures were lower, close to long-term averages, and only very minor coral bleaching was reported. ACKNOWLEDGMENTS We thank Cy Macfarlane, Ruth Gates, and lan Sandeman for providing some of the thermometer records of sea temperatures from Jamaica, and Phillippe Bush for the data from Cayman. We thank Audrey Allen, Marshall Hayes, Steve Orzack, Nora Goreau, Richard Reynolds, Kevin McCarthy, Mark Waters, Catherine Woody, Jim Lynch, Alan Strong, and Kilho Park for assistance with data, discussions, and review of the manuscript. Special thanks go to Peter Goreau for preparing Figure 1. Statistics were calculated using Statworks 1.2 software on a Macintosh computer. Partial support for this investigation was provided by a HURD grant from Howard University to RLH. REFERENCES Acevedo, R and Goenaga, C., 1986, Note on a coral bleaching aher a chronic flooding in southwestern Puerto Rico, Carib J. Sci., 22, 225. Acevedo, R., Morelock, J., and Olivieri, R., 1989, Modification of coral reef zonation by terrigenous sedtment stress, Palaios, 4, 92-100. Atwood, D. K., Sylvester, J. C., Corredor, J. E., Morell, J. M., Mendez, A., Nodal, W. J., Huss, B. E, and Foltz C., 1988, Sea surface temperature anomalies for the Caribbean, Gulf of Mexico, Florida reef track, and Bahamas considered in light of the 1987 regional coral bleaching event, Proc. Assoc. Mar. Labs Caribbean, Brown, B. and Suharsono. 1990, Damage and recovery of coral reefs affected by El Nino related sea water warming in the Thousand Islands, Indonesia, Coral Reefs, 8, 163-170. Causey, B., 1988, Observations of environmental conditions preceding the coral bleaching event of 1987, Proc. Assoc. Island Mar. Labs. Caribbean, 21, 48. Causey, B., unpublished data Cook, C., Logan, A., Ward, J., Luckhurst, B., and Berg, C., 1990, Elevated temperatures and bleaching on a high latitude coral reef: the 1988 Bermuda event, Coral Reefs, 9, 45-49. Dustan, P., 1982, Depth dependent photo adaptation by zooxanthellae of the reef coral Montastrea annularis. Mar. Biol., 68, 253-264. Ellsaesser, H. W., 1984, The climatic effect of CO2: a different view, Atmosph. Envir., 18, 431-34. Ellsaesser, H. W., 1990. Oceanic role in terrestrial climate: a commentary, in The Ocean in Human Affairs, pp. I 17-134, S. F. Singer, Ed. Paragon House, New York.
Fankboner, P. V. and Reid, R. G. B., 1981. Mass expulsion of zooxanthellae by heat stressed reef corals: a source of food for giant clams, Experientia 37, 251-252. Fisk, D. A. and Done, T. J., 1985. Taxonomic and bathymetric patterns of bleaching, Myrmidon Reef, Proc. 5th Intern Coral Reef Symp 6. 149 - 154. Flohn, H. and Kapala, A., 1989. Changes of tropical sea-air interaction processes over a 30-year period, Nature 338, 244-246. Gates, R., 1990. Seawater temperature and sub lethal coral bleaching in Jamaica, Coral Reefs 8, 192-197. Glynn, P., 1983. Extensive ''bleaching'' and death of reef corals on the Pacific coast of Panama, Environ. Conserv. 10, 149-154. Glynn, P., 1984. Widespread coral mortality and the 1982/1983 El Nino warming event, Environ Conserv. 11, 133-146. Glynn, P and D'Croz, L., 1990. Experimental evidence for high temperature stress as the cause of El Nino coincident mortality, Coral Reefs 8, 181-191 Glynn, P W., Peters, E. C., and Muscatine, L., 1985. Coral tissue microstructure and necrosis: relation to catastrophic coral mortality in Panama, Dis. Aquat. Org., 1, 29-37. Goenaga, C. and Canals, M., 1990. Island-wide coral bleaching in Pueno Rico. 1990, Carib. J. Sci. 26, 171 Goenaga, C. and Canals, M., 1979. Relacion de mortandad masiva de Millepora complanata (Cnidaria. Anthozoa) con alta pluviosidad y escorrentia del Rio Fajardo en Cayo Ahogado, Fajardo, Symp. Nat. Res. San Juan, Puerto Rico 6, 84-95. Goreau, T. F., 1959. The ecology of Jamaican reefs. 1. Species composition and zonation. Ecology 40, 67-90. Goreau, T. F., 1964. Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane Flora Science 145, 383-386. Goreau, T. F and Goreau, N. I., 1959. The physiology of skeleton formation in corals. 11. Calcium deposition by hermatypic corals under various conditions in the reef, Biol. Bull. 117, 239-250. Goreau, T. F. and Goreau, N. I., 1960. Distribution of labeled carbon in reef building corals with and without zooxanthellae, Science 131, 668-669. Goreau, T. F. and Goreau, N. I., 1973. The ecology of Jamaican reefs. 11. Geomorphology, zonation, and sedimentary phases, Bull. Mar. Sci. 23, 399-464. Goreau, T. F., Goreau, N. I., and Goreau, T. J., 1979. Corals and Coral Reefs, Sci. Amer. 241, 124-136. Goreau, T. J., 1990a. Coral bleaching in Jamaica, Nature 343, 417. Goreau, T. J., 1990b. Coral bleaching, New Scientist, (Jan. 13, 1990b) p. 76. Goreau, T J. and Dodge, R. E, unpublished data. Goreau. T. J, Dodge, R. E., Goreau, P, and Dunham, J., 1988. Coral fluorescence records Everglades hydrology 1918-1983, Proc Assoc. Island Mar Labs. Caribbean 21, 43. Goreau, T. J. and Macfarlane, A. H., 1990a Reduced growth rate of Montastrea annularis following the 1987-1988 bleaching event, Coral Reefs 8, 211-216. Goreau, T. J. and Macfarlane, A. H., 1990b. Mass bleaching, temperature, and Hurricane Gilbert: effects on Jamaican coral growth, 1987-1990, Proc. Assoc. Mar Labs. Caribbean 23, 141. Hansen, J. and Lebedeff, S. J., 1987. Global trends of measured surface temperature, Geophys. Res. 92, 13,345-13,372. Harriot, V. J., 1985. Mortality rates of scleractinian corals before and during a mass bleaching event, Mar. Ecol. Prog. Ser. 21, 81-88. Hayes, R. L., 1988. Histological and histochemical comparisons of bleached and normal tissues from Agaricia lamarckii, Proc. Assoc. Island Mar. Labs. Caribbean 21, 12 Hayes, R. L., 1991. Testimony presented to the U.S. House of Representatives, Committee on Health and the Environment, February, 1991. Hayes, R., unpublished data. Hayes, R, and Bush. P., 1990. Microscopic observations of recovery in the reef-building scleractinian coral Montastrea annularis, after bleaching on a Cayman reef, Coral Reefs 8, 203-209. Hoogh-Guldberg, O., McCloskey, L. R., and Muscatine, L., 1987. Expulsion of zoaxanthellae by symbiotic cnidarians from the Red Sea, Coral Reefs 5, 201-204. Hoegh-Guldberg, O. and Smith. G. J., 1989. Light, salinity, and temperature and the population density, metabolism, and export of zooxanthellae from Stylophora pistillata and Seriatopora hystrix, J. Exper. Mar. Biol. Ecol. 129, 279-303. Jaap, W., 1979. Observation on zoaxanthellae expulsion at Middle Sambo Reef, Flonda Keys, Bull Mar. Sci. 29, 414-422. Jaap, W., 1985. An epidemic zooxanthellae expulsion during 1983 in the lower Florida Keys coral reefs: hyperthermic etiology, Proc. 5th Intern. Coral Reef Symp. 6, 143-148. Jokiel, P. L. and Coles, S. L., 1990. Response of Hawaiian and other Indo-Pacific corals to elevated temperatures Coral Reefs 8, 155-162. Jones, P. and Wigley, T. M. L., 1990. Global warming trends, Scientific American 263, 84-91. Kidwell, K. B., 1986. NOAA Polar Orbital Data Users Guide Kleppel, G. S., Dodge, R. E., and Reese, C. J., 1989. Changes in pigmentation associated with the bleaching of stony corals, Limnol. Oceanogr. 34, 1331-1335. Lang, J., Wicklund, R., and Dill, R., in press. Unusual depth-related bleaching of reef corals near Lee Stocking Island, Bahamas, Proc. 6th Intern. Coral Reef Symp. LaPointe, B., O'Connell, J., and Garren, G., 1990. Nutrient couplings between on-site sewage disposal systems, groundwaters, and nearshore surface waters of the Flonda Keys, Biogeochemistry 10, 289-307. Lasker, H., Peters, E., and Coffroth, M. A., 1984. Bleaching of reef coelenterates in the San Blas Islands, Panama, Coral Reefs 3, 183-190. Logan, A., 1988. Holocene Reefs of Bermuda, Sedimenta X, 62pp. Mayor, A. G., 1918. Toxic effects due to high temperature, Carnegie Inst. Wash. Pap. Mar. Biol 12, 175-178 McCormack, R C. and Strong, A. E., 1990. Correlation between sea surface temperature trends and Caribbean coral bleaching events, Eos 71, 104. Nishihira, M., 1987. Natural and human interference with the coral reef and coastal communities in Okinawa. Galaxea 6, 311-324. Oliver, J., 1985. Recurrent seasonal bleaching and monality of corals on the Great Barrier Reef, Proc 5th Intern. Coral Reef Symp. 4, 201-206. Porter, J, Fitt, W., Spero, H., Rogers, C., and White, M., 1989. Bleaching in reef corals: physiological and stable isotopic responses, Proc. Nar. Acad. Sci. 86: 9342-9346. Porter, J., personal communication; unpublished data. Ramanathan, V., Barkstrom, B. R., and Harrison, E. F., 1989. Climate and the Earth's radiation budget, Physics Today 42, 22-32. Ramanathan, V., Cess, R. D., Harrison, E. F., Minnis, P., Barkstrom, B. R., Ahmad, E., and Hanmann, D., 1989 Cloud-radiative forcing and climate: results from the Earth Radiation Budget Experiment, Science 342, 57 63 Ramanathan, V. and Collins, W., 1991. Thermodynamic regulation of ocean warming by cirrus clouds deduced from observations of the 1987 El Nino, Nature 351, 27-32. Reimer, A., 1971 Observations on the relationship between several species of tropical zoanthids (Zoanthideea. Coelenterata) and their zoaxanthellae, J. Exper. Mar. Biol. Ecol. 7, 207-217. Reynolds, R W., Folland, C. K., and Parker, D. E., 1989. Biases in satellite-denved sea-surface-temperature data, Nature 341. 728-731. Reynolds, R W., personal communication. Robock, A, 1989 Satellite data contamination, Nature 341, 695. Sammon. R., personal communication, 1990. Sciremammano, F., 1979. A suggestion for the presentation of correlations and their significance levels, J. Phys. Oceanogr. 9, 1273-1276. Spencer. R and Christy, J., 1990. Precise monitonng of global temperature trends from satellites, Science 247, 1 558- 1 562. Steen, R. G. and Muscatine, L., 1987. How temperature evokes rapid exocytosis of symbiotic algae by a sea anemone. Biol Bull. 172, 245-263. Strong, A. E., 1984. Monitoring El Chichon aerosol distribution using NOAA-7 satellite AVHRR sea surface temperature observations, Geofisica Int. 23, 129-141. Strong, A. E., 1989. Greater global warming revealed by satellite-derived sea-surface-temperature trends, Nature 338, 642-645 Strong, A. E., 1989. Satellite data contamination, Nature 341, 695. Strong, A. E. and McCormack, R. C., 1991. Coral bleaching and sea surface temperatures, Proc. Oceanography. Soc. Conf, St. Petersburg, FL. Sverdup, H, Johnson, M., and Fleming, R., 1942. The Oceans: their Physics, Chemistry, and General Biology, Prentice-Hall, Englewood Cliffs, N.J. Trench, R., 1986. Dinoflagellates in non-parasitic symbioses, in Biology of Dinoflagellates, F. R. Williams, E. and Bunkley-Williams, L., 1990. The world-wide coral reef bleaching cycle and related sources of coral mortality, Atoll Res. Bull. 335, 1-71. Williams, E, Goenaga, C., and Vicente, V., 1987. Mass bleaching on Atlantic coral reefs, Science 238, 877878. Yonge, C. M. and Nicholls, A G., 1931. Studies on the physiology of corals, 5, Great Barrier Reef Expedition Scientific Papers 1, 135-176; 177-211.
|
|