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1 SUPPLEMENTARY INFORMATION DOI: /NCLIMATE1577 Decline of forereef corals in response to recent warming linked to history of thermal exposure By: Karl D. Castillo, Justin B. Ries, Jack M. Weiss, Fernando P. Lima Supplementary Figures Figure S1 Comparison of in situ seawater temperature and OI-SST records for inshore and offshore reefs. Average monthly in situ seawater temperature measurements for Hobo Water Temperature Pro Loggers installed at 4-to-5 m depth for (a) offshore (light grey lines) and (b) inshore (dark grey lines) reefs superimposed upon average monthly OI-SST (dashed lines) records retrieved from paired grids encompassing offshore (forereef, backreef) and inshore (nearshore) reef environments of the MBRS off southern Belize. Bottom panels show the difference between average monthly OI-SST records and in situ measurements for (c) offshore (light grey lines) and (d) inshore (dark grey lines). Data shown are for the interval 2002 through Missing in situ measurements are due to lost or stolen temperature loggers. NATURE CLIMATE CHANGE 1
2 a b In situ temperature range ( C) Daily Monthly Inshore Offshore Probability density c Daily Monthly Daily Monthly Year Difference in in situ ranges ( C), inshore offshore Figure S2 In situ seawater temperature variability for inshore and offshore reefs. (a) Daily and monthly seawater temperature ranges for inshore and offshore reefs based on in situ instrumental seawater temperature measurements for the interval 2002 through Gaps in the records are due to lost or stolen temperature loggers. (b) Kernel density estimates of the distributions of in situ seawater temperature range differences at daily (dark grey) and monthly (light grey) intervals. (c) Box plots show median (line inside the box), mean (asterisk), first and third quartiles (box edges), the minimum and maximum differences in in situ ranges, and any suspected outliers within the distribution. Positive range differences indicate greater in situ seawater temperature variability for the inshore relative to the offshore reefs, and negative range differences indicate greater temperature variability for the offshore reefs relative to the inshore reefs for that time interval (daily or monthly).
3 a 4 3 Nearshore b 2.5 Backreef forereef Nearshore backreef Nearshore forereef OI-SST monthly range ( C) Forereef Backreef Probability density c Nearshore forereef Nearshore backreef 1 Backreef forereef Year Difference in OI-SST monthly ranges ( C) Figure S3 Monthly SST variability amongst reef zones of the Mesoamerican Barrier Reef System. (a) Monthly temperature ranges acquired from daily OI-SST records for nearshore, forereef and backreef reef environments of the MBRS off southern Belize for the years 1982 through (b) Kernel density estimates of the distributions of OI-SST monthly pairwise range differences amongst forereef, backreef, and nearshore reef environments for the ranges shown in (a). (c) Box plots show median (line inside the box), mean (asterisk), first and third quartiles (box edges), the minimum and maximum differences in OI-SST ranges, and any suspected outliers for the distribution of pairwise range differences for the two reef zones compared. For differences between hypothetical reef zones A B, positive range differences indicate greater OI-SST variability for reef zone A relative to reef zone B and negative range differences indicate greater OI-SST variability for reef zone B relative to reef zone A.
4 a 6.0 Nearshore b 4 Backreef forereef Nearshore backreef Nearshore forereef OI-SST annual range ( C) Forereef Backreef c Probability density Nearshore forereef Nearshore backreef Backreef forereef Year Difference in OI-SST annual ranges ( C) Figure S4 Annual SST variability amongst reef zones of the Mesoamerican Barrier Reef System. (a) Annual temperature ranges acquired from daily OI-SST records for nearshore, forereef and backreef reef environments of the MBRS off southern Belize for the years 1982 through (b) Kernel density estimates of the distributions of OI-SST annual pairwise range differences amongst forereef, backreef, and nearshore reef environments for the ranges shown in (a). (c) Box plots show median (line inside the box), mean (asterisk), first and third quartiles (box edges), the minimum and maximum differences in OI-SST ranges, as well as the individual differences (displayed points) for the two reef zones compared. For differences between hypothetical reef zones A B, positive range differences indicate greater OI-SST variability for reef zone A relative to reef zone B and negative range differences indicate greater OI- SST variability for reef zone B relative to reef zone A.
5 Figure S5 Monthly and annual SST variability for north and south grids within the forereef environment. (a) Monthly and annual temperature ranges acquired from daily OI-SST records for north and south grids within the forereef environments of the MBRS off southern Belize for the years 1982 through (b) Kernel density estimates of the distributions of OI- SST monthly and annual pairwise range differences between the southern and the northern portions of forereef environments for the ranges shown in (a). (c) Box plots show median (line inside the box), mean (asterisk), first and third quartiles (box edges), the minimum and maximum differences in OI-SST ranges, as well as the individual differences (displayed points) for the two forereef grids that are compared. Positive range differences indicate greater OI-SST variability for the southern grid relative to the northern grid and negative range differences indicate greater OI-SST variability for the northern grid relative to the southern grid.
6 Figure S6 Sample X-radiographs of coral cores from each reef zone of the Mesoamerican Barrier Reef System in southern Belize. Core sections shown represent skeletal extension for approximately the last four decades (~1970 to 2008) for Siderastrea siderea from (a) forereef (core FR-12), (b) backreef (core BR-06), and (c) nearshore (core NS-14) reef zones. Numbers correspond to year of paired high-density (light band) and low-density (dark band) growth bands. Scale bars are 1 cm.
7 Figure S7 Impact of annual accumulated thermal stress on annual coral skeletal extension. Time series of Siderastrea siderea annual skeletal extension (measured and calculated trends) showing annual accumulated thermal stress (light blue vertical bars) within forereef (FR), backreef (BR), and nearshore (NS) reef environments. Dashed lines correspond to populationaverage models, which include estimates of the fixed effects only; solid lines correspond to subject-specific models, which include estimates of the fixed effects and best linear unbiased predictions of the random effects. Grey lines are line segments that connect the observed annual skeletal extension rates for adjacent years. Trend lines were estimated using a mixed effects model with random intercepts.
8 Supplementary Methods Seawater Temperature In situ Seawater Temperature In situ instrumental seawater temperature measurements were acquired for the interval 2002 through 2008 using Hobo Water Pro Temperature Loggers (Onset Computer Corporation, Pocasset Massachusetts) installed in the offshore (forereef, backreef) and inshore (nearshore) reefs of southern Belize. Each logger was installed by attaching a 1-m polypropylene rope to a stainless steel eyebolt affixed to the seafloor using Z-Spar underwater epoxy. A subsurface buoy was then attached to the rope to keep the logger suspended in the water column. Loggers were programmed to record subsurface temperatures at 10, 15, or 30 minute intervals. Some gaps exist in the in situ time series due to lost or stolen loggers. In situ monthly seawater temperature was calculated for each reef habitat from the logger data for comparison with NOAA s Optimum Interpolation Sea Surface Temperature (OI-SST; version 2) records (Fig. S1). Additionally, in situ temperature ranges were calculated for each reef environment to show diurnal and seasonal variability in seawater temperature amongst reef zones (Fig. S2; Table S4). Sea Surface Temperature and Annual Accumulated Thermal Stress Average annual summer sea surface temperature (SST) was calculated by averaging daily temperatures for August, September, and October (separately for each year and reef zone) and for the interval 1982 through 2008 from OI-SST records. Monthly and annual OI-SST ranges were calculated for each reef zone from daily OI-SST records (Figs. S3, S4; Table S4). In addition to average annual summer SST, annual accumulated thermal stress was calculated in degree-heating-months (DHM) from OI-SST records for each reef zone. DHM, measured in o C- months, is similar to NOAA s degree-heating-weeks (DHW) product, which is the accumulation of weekly SSTs over a 12 week interval that are 1 o C above the maximum monthly mean SST (MMM-SST) of the hottest month of the year. Both DHM and DHW are used for quantifying thermal stress and provide a reliable measure of the likelihood that thermal stress will induce coral bleaching. We calculated annual accumulated thermal stress as the annual sum of the average monthly SSTs that exceeded the long-term MMM-SST. The MMM-SST of the hottest month of the year for each grid cell was calculated using all data for the interval In addition, monthly and annual temperature ranges were calculated from daily OI-SST records for
9 north and south grids within the forereef zone from 1982 through 2008 to explore thermal variability with latitude (Fig. S5; Table S4). Coral Core Extraction Procedure Siderastrea siderea cores were extracted from thirteen different coral colonies in the forereef, backreef, and nearshore reef zones of the Mesoamerican Barrier Reef System in southern Belize. Cores were extracted by SCUBA divers using a 2-horsepower (CP-315; Chicago Pneumatic) pneumatic drill affixed with a hollow extension rod (5 cm in diameter, 90 cm in length) and a wet diamond core bit (5 cm in diameter, 30 cm length). Compressed air from SCUBA cylinders located on a boat powered the pneumatic drill. Extracting a coral core ~100 cm in length required 5 to 8 standard size SCUBA cylinders and ca. 45 min of drilling. Only coral colonies that appeared healthy were sampled (i.e., showed no obvious abnormalities, scarring, bleaching, or disease at time of core extraction). Coral cores were extracted at 4-to-5 m depth within all three reef zones. After core extraction, a concrete plug was inserted into the drilled holes and sealed with Z-spar underwater epoxy. See Castillo et al. (2011) 1 for a more detailed description of core extraction procedures. Sclerochronology Development Extracted coral cores were rinsed with 95% ethanol and air-dried. Six-mm thick slabs were sectioned vertically from the center of each core using a water-cooled trim saw. Core slabs were then X-rayed from a source-to-object distance of 100 cm at 6.0 ma s -1 and at 40 kv using a Fuji FCR radiography system to reveal annual cycles in skeletal density. Digital X-radiographs of each coral core were then inserted into Coral X-radiography Densitometry System (Coral XDS) for processing (Fig. S6). The half range delimiting function of Coral XDS was then used to identify annual cycles in coral skeletal growth. In the western Caribbean Sea, S. siderea deposits low-density growth bands from approximately December-through-May and high-density growth bands from approximately June-through-November. 2 Coral core chronologies were established by identifying the most recent high-density growth band for 2008 and counting high-density growth bands backwards in time. Cores were visually cross-dated by identifying signature years of particularly narrow growth to prevent dating errors associated with poorly resolved banding a procedure commonly used in dendrochronology. 3
10 Statistical Analyses The data in the present study are an example of hierarchical data. The hierarchical structure arises because the individual sampling units are coral cores, but the observational units used in the statistical analyses are the multiple annual coral growth bands that are estimated from the individual cores. Since it is the coral cores that were sampled rather than the individual annual coral growth bands derived from those cores, the sampling of annual growth is not random. Instead, the sampling is analogous to one-stage cluster sampling. Annual coral growth bands obtained from the same core are likely correlated, while the annual growth bands obtained from different cores should be closer to being truly independent. The situation is further complicated by the fact that the individual annual growth bands obtained from the same core have a natural temporal order. This order superimposes an additional structure on observations coming from the same core, with any correlation likely decreasing with time. Random intercept models with residual correlation structures were employed to model the relationship between coral skeletal extension and SST and between coral skeletal extension and thermal stress. This approach distinguishes observational units from sampling units, recognizes that sampling variation exists both within and between core time series and addresses the temporal autocorrelation structure that is inherent in such data. Models were fit using the nlme package 4 of R Coral Skeletal Extension and Sea Surface Temperature Two-year running averages of mean summer OI-SST were obtained by averaging the temperature of the current year with that of the previous year. These were then matched to the corresponding coral growth data: the average summer SST in 1982 and 1983 was matched with coral growth in 1983; the average summer SST in 1983 and 1984 was matched with coral growth in 1984, and so on. This yielded 26 observations for each core except for one forereef core (FR- 05) that had 23 observations and one backreef core (BR-08) that had 19 observations. To establish the relationship between coral skeletal extension and summer OI-SST we used a random intercept model that regressed growth against smoothed average summertime temperature (two-year running averages; Table S1 and S2). We tested various random intercept models with a population average component in which intercepts and slopes were allowed to vary both separately and together by reef zone. A random intercept model in which each reef
11 zone has its own slope and intercept ranked best using Akaike Information Criterion (AIC). Since coral skeletal extension and OI-SST were collected over time, there is the potential for the model residuals to be serially correlated. We tested the autocorrelation function of the residuals using a Bonferoni adjustment of the Type I error to account for multiple testing, but found no evidence of significant residual autocorrelation. Coral Skeletal Extension and Thermal Stress A random intercept model with a population average component in which intercepts and slopes varied by reef zone was employed to establish the relationship between coral skeletal extension and annual accumulated thermal stress (Fig. S7; Table S3). To account for the significant temporal autocorrelation in the residuals that existed, year was added to the model as a predictor and the year effect was allowed to vary by reef zone. This effectively removed the residual temporal autocorrelation and yielded a model that ranked best using AIC. Quantifying Thermal Variability across Reef Zones and within the Forereef Zone Quantification of thermal variability was accomplished by statistical tests comparing daily, monthly, or annual variability in seawater temperature between reef locations (inshore and offshore), amongst reef zones (forereef, backreef, nearshore), and within forereef environment (north and south grids) of the Mesoamerican Barrier Reef System. Statistical analyses were made either using generalized least squares (GLS) with an autoregressive [AR (2)] correlation model for the residuals or with a paired t-test when there was no significant residual correlation.
12 Supplementary Tables Table S1 Parameter estimates for the AIC-best fit model evaluating the association between summertime SST and annual coral skeletal extension for forereef and nearshore corals relative to backreef colonies. Parameter Estimate Standard Error t-statistic p-value Intercept Temperature Reef zone FR Reef zone NS Temperature Reef zone FR <0.001 Temperature Reef zone NS Parameter estimates for a regression of skeletal extension vs. summer SST for Siderastrea siderea colonies from the forereef ( FR ; n = 7) and nearshore ( NS ; n = 3), relative to backreef (n = 3) colonies, for the interval The estimates are for a random intercept model in which the slopes and intercepts of the population average model varied by reef zone. Reef zone FR and NS represent estimates of individual effects for forereef and nearshore relative to backreef (reference group). Temperature x Reef zone FR and NS represent effects of temperature and reef zone interaction for the specified reef zone relative to backreef.
13 Table S2 Model-derived estimates of the association between summertime SST and annual coral skeletal extension over approximately the last three decades for each reef zone. Parameter Estimate Standard Error t-statistic p-value Intercept Backreef Forereef <0.001 Nearshore Slope Backreef Forereef <0.001 Nearshore Results of a random intercept model for the association between summertime SST and annual skeletal extension for Siderastrea siderea colonies from the forereef (n = 7), backreef (n = 3), and nearshore (n = 3) reef zones for the interval
14 Table S3 Parameter estimates for the AIC-best fit model evaluating the association between annual accumulated thermal stress and annual coral skeletal extension over the last 27 years for each reef zone. Parameter Estimate Standard Error t-statistic p-value Intercept x (1967) <0.001 Thermal Stress: reef zone = BR Thermal Stress: reef zone = FR Thermal Stress: reef zone = NS Year: reef zone = BR Year: reef zone = FR Year: reef zone = NS Results of a random intercept model for the association between annual accumulated thermal stress and annual coral skeletal extension for Siderastrea siderea colonies from the forereef (n = 7), backreef (n = 3), and nearshore (n = 3) reef zones for the interval 1982 to The variable year was centered using a centering constant of This estimates the mean annual coral skeletal extension in year 1967 (rather than in year zero of an uncentered model). Thermal Stress: reef zone represents estimates of the effects of thermal stress on coral skeletal extension for the specified reef zone. Year: reef zone represents estimates of the change in coral skeletal extension over time for the specified reef zone.
15 Table S4 Statistical tests for difference in thermal variability between reef locations and amongst reef zones of the Mesoamerican Barrier Reef System in the western Caribbean Sea. Figure Comparison Difference Mean 95% CI t- statistic df p-value Analysis used S2 Inshore Offshore In situ daily range (0.127, 0.170) <0.001 GLS S2 Inshore Offshore In situ monthly range (0.218, 0.478) <0.001 paired t-test S3 Nearshore Forereef Monthly range (0.068, 0.133) <0.001 paired t-test S3 Backreef Forereef Monthly range (0.028, 0.064) <0.001 paired t-test S3 Nearshore Backreef Monthly range (0.038, 0.073) <0.001 paired t-test S4 Nearshore Forereef Annual range (0.188, 0.481) <0.001 paired t-test S4 Backreef Forereef Annual range (0.081, 0.232) <0.001 paired t-test S4 Nearshore Backreef Annual range (0.096, 0.259) <0.001 paired t-test S5 S5 South North South North Monthly range Annual range (0.064, 0.120) (0.100, 0.318) <0.001 <0.001 paired t-test paired t-test Results of statistical tests comparing daily, monthly, or annual variability in seawater temperature between reef locations (inshore and offshore), amongst reef zones (forereef, backreef, nearshore), and within forereef environment (north and south grids) of the Mesoamerican Barrier Reef System. Statistical analyses were made either using generalized least squares (GLS) with an autoregressive [AR (2)] correlation model for the residuals or with a paired t-test when there was no significant residual correlation.
16 Supplementary References 1 Castillo, K., Ries, J. & Weiss, J. Declining coral skeletal extension for forereef colonies of Siderastrea siderea on the Mesoamerican Barrier Reef System, southern Belize. PLoS ONE 6, e14615 (2011). 2 Guzmán, H. M. & Tudhope, A. Seasonal variation in skeletal extension rate and stable isotopic ( 13 C/ 12 C) and 18 O/ 16 O) composition in response to several environmental variables in the Caribbean reef coral Sideastrea siderea. Marine Ecology Progress Series 166, (1998). 3 Yamaguchi, D. A simple method for cross dating increments cores from living trees Canadian Journal of Forest Research 21, (1991). 4 Pinheiro, J., Bates, D., Saikat, D., Sarkar, D. & R Development Core Team. in nlme: Linear and Nonlinear Mixed Effects Models. R package version (2011). 5 R Development Core Team. R: A language and environment for statistical computing., < project.org> (2010).
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