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Biogeosciences, 11, 4321–4337, 2014 www.biogeosciences.net/11/4321/2014/ doi:10.5194/bg-11-4321-2014 © Author(s) 2014. CC Attribution 3.0 License. Diverse coral communities in mangrove habitats suggest a novel refuge from climate change K. K. Yates1, C. S. Rogers2, J. J. Herlan2,*, G. R. Brooks3, N. A. Smiley1, and R. A. Larson3 1US Geological Survey, Coastal and Marine Science Center, St Petersburg, Florida 33701, USA 2US Geological Survey, Southeast Ecological Science Center, St John, US Virgin Islands 00830, USA 3Eckerd College, Galbraith Marine Science Laboratory, St. Petersburg, Florida 33711, USA *now at: Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile Correspondence to: K. K. Yates (kyates@usgs.gov) Received: 20 February 2014 – Published in Biogeosciences Discuss.: 31 March 2014 Revised: 30 June 2014 – Accepted: 8 July 2014 – Published: 19 August 2014 Abstract. Risk analyses indicate that more than 90 % of the world’s reefs will be threatened by climate change and local anthropogenic impacts by the year 2030 under “business-as- usual” climate scenarios. Increasing temperatures and solar radiation cause coral bleaching that has resulted in extensive coral mortality. Increasing carbon dioxide reduces seawater pH, slows coral growth, and may cause loss of reef structure. Management strategies include establishment of marine pro- tected areas with environmental conditions that promote reef resiliency. However, few resilient reefs have been identified, and resiliency factors are poorly defined. Here we characterize the first natural, non-reef coral refuge from thermal stress and ocean acidification and iden- tify resiliency factors for mangrove–coral habitats. We mea- sured diurnal and seasonal variations in temperature, salin- ity, photosynthetically active radiation (PAR), and seawa- ter chemistry; characterized substrate parameters; and ex- amined water circulation patterns in mangrove communities where scleractinian corals are growing attached to and under mangrove prop roots in Hurricane Hole, St. John, US Vir- gin Islands. Additionally, we inventoried the coral species and quantified incidences of coral bleaching, mortality, and recovery for two major reef-building corals, Colpophyllia natans and Diploria labyrinthiformis, growing in mangrove- shaded and exposed (unshaded) areas. Over 30 species of scleractinian corals were growing in as- sociation with mangroves. Corals were thriving in low-light (more than 70 % attenuation of incident PAR) from man- grove shading and at higher temperatures than nearby reef tract corals. A higher percentage of C. natans colonies were living shaded by mangroves, and no shaded colonies were bleached. Fewer D. labyrinthiformis colonies were shaded by mangroves, however more unshaded colonies were bleached. A combination of substrate and habitat heterogeneity, prox- imity of different habitat types, hydrographic conditions, and biological influences on seawater chemistry generate chem- ical conditions that buffer against ocean acidification. This previously undocumented refuge for corals provides evi- dence for adaptation of coastal organisms and ecosystem transition due to recent climate change. Identifying and pro- tecting other natural, non-reef coral refuges is critical for sus- taining corals and other reef species into the future. 1 Introduction Evidence that repeated coral bleaching events (Baker et al., 2008; Eakin et al., 2009; Fitt et al., 2001; Hoegh-Guldberg et al., 2007; Hoegh-Guldberg, 2011; Lesser, 2011) and ocean acidification (Fabricius et al., 2011; Kleypas and Yates, 2009; Kroeker et al., 2013, Silverman et al., 2009) will severely impede coral growth within the next few decades (Burke et al., 2011; van Hooidonk et al., 2014) has prompted an ur- gent search for coral reef systems that provide natural refuges from climate threats and efforts to identify mechanisms that could help reef organisms acclimatize to the changing cli- mate. The complex interplay among climate, oceanographic, and biological factors that influences susceptibility and re- silience of reefs has made identification and characteriza- tion of refuges challenging. Research is needed on how these Published by Copernicus Publications on behalf of the European Geosciences Union. 4322 K. K. Yates et al.: Diverse coral communities in mangrove habitats factors interact and how they will affect the overall biodi- versity, function, and transition of these ecosystems. Focus has been placed on identifying reefs with low exposure to or potential for adaptation to climate threats, and reduced lo- cal anthropogenic impacts (Keller et al., 2009; McClanahan et al., 2011; Mumby and Steneck, 2008; Salm et al., 2006; West and Salm, 2003). Recent studies have identified only a few reef systems, for example, in the western Indian Ocean (McClanahan et al., 2011), on the Great Barrier Reef (Berkel- mans, 2002), and in shallow bays of Palau (van Woesik et al., 2012) that show resistance to elevated temperatures and less coral bleaching. Only one reef, in the Florida Keys, has been identified as a potential refuge from ocean acidifica- tion (Manzello et al., 2012). To our knowledge, no alterna- tive (non-reef) natural habitats have ever been identified as potential climate change refuges for corals. Mangrove communities, while often near coral reef ecosystems, are not thought of as having suitable conditions for coral recruitment and growth due to high sedimentation rates, lack of suitable substrate, and inadequate water qual- ity. Therefore, no prior focus has been placed on identify- ing mangrove–coral habitats, the scientific literature contains few references to scleractinian corals growing in mangrove habitats (e.g. Macintyre et al., 2000; Rutzler et al., 2000), and no comprehensive surveys or multidisciplinary studies of these habitats have been performed. In St. John, US Virgin Islands, over 30 species of sclerac- tinian corals are growing on and under mangrove prop roots in small bays located along the perimeter of a large bay, Hur- ricane Hole, within the Virgin Islands Coral Reef National Monument (Table 1). Many are reef-building corals that sur- vived a 2005 to 2006 bleaching and disease event that caused major losses of coral throughout the northeastern Caribbean (Miller et al., 2009). Qualitative surveys conducted in one bay in 1984 suggest that corals were present, but neither di- verse nor abundant (Beets et al., 1986). We considered that an increase in the diversity and abundance of corals in man- grove communities since that time (Rogers and Herlan, 2012) could be a response to climate change. Keppel et al. (2012) define refugia as “habitats that compo- nents of biodiversity retreat to, persist in and can potentially expand from under changing environmental conditions”. The presence of such a remarkable abundance and diversity of coral species in the mangroves of St. John, and their largely intact condition in contrast to severe declines of corals on nearby reefs following bleaching and a major disease out- break support the concept of this habitat as a refuge. This mangrove–coral habitat is characterized by heterogeneity in the physical environment that allows it to be out of equi- librium with open ocean conditions, resulting in differenti- ation of local physical, chemical, and biological attributes. This ecosystem serves as an example of how some man- grove habitats could provide alternative refuges for corals from climate threats, particularly increasing seawater tem- perature, high levels of solar radiation, and decreasing pH. Table 1. Species list of corals living in mangroves. Coral species Princess Otter Water Bay Creek Creek Stephanocoenia intersepta × × × Acropora palmata × Agaricia agaricites × × × Agaricia spp. × × Siderastrea siderea × × × Siderastrea radians × × × Porites astreoides × × × Porites porites × × × Porites furcata × × × Porites divaricata × Favia fragum × × × Diploria labyrinthiformis × × × Pseudodiploria clivosa × × Pseudodiploria strigosa × × × Manicina areolata × × × Colpophyllia natans × × × Colpophyllia amaranthus × Cladocora arbuscula × Orbicella annularis × × Orbicella faveolata × × × Orbicella franksi × × Montastraea cavernosa × × Solenastrea bournoni × Phyllangia americana × Oculina diffusa × × Meandrina meandrites × × Dichocoenia stokesi × Dendrogyra cylindrus × × Scolymia cubensis × × × Scolymia lacera × Mycetophyllia spp. × × Eusmilia fastigiata × × Tubastrea aurea × × Millepora spp. × × × Totals 19 30 26 We identified and quantified physical, chemical, and biolog- ical resiliency factors in mangrove communities with corals in Hurricane Hole, St. John, US Virgin Islands. We present a list of resiliency factors to help guide identification of other alternative refuges for reef-building corals. 2 Methods Physical, chemical, and biological attributes were character- ized in three small, adjacent bays in Hurricane Hole includ- ing Water Creek, Otter Creek, and Princess Bay in Novem- ber 2010, July 2011, and July 2012 (Fig. 1). In each bay, we measured diurnal and seasonal variations in temperature, salinity, photosynthetically active radiation (PAR), and sea- water chemistry [total alkalinity (AT), dissolved inorganic Biogeosciences, 11, 4321–4337, 2014 www.biogeosciences.net/11/4321/2014/ K. K. Yates et al.: Diverse coral communities in mangrove habitats 4323 Figure 1. Study sites (STJ#) in Hurricane Hole. MC are mangroves with corals growing on and near mangrove prop roots and shaded by the mangrove canopy, MNC are mangroves with no corals growing in association with them, ROC are rock outcrops with live corals and no shading from mangroves. carbon (CT), pHT (pH on the total H+ scale), dissolved oxygen (DO), and nutrients]. We characterized substrate pa- rameters and examined water circulation patterns associated with inner-bay mangrove communities with no corals (MNC sites), nearby mid- to outer-bay mangrove communities with corals growing on and under prop roots (MC sites), and rock outcrops with unshaded corals (ROC sites) in all three bays. Corals at these sites were growing near the coastline in shal- low water ranging from 1.2 to 2.0 m water depth. Addition- ally, we inventoried coral species in all three bays, and quan- tified incidences of coral bleaching, mortality, and recovery for two major reef-building corals, Colpophyllia natans and Diploria labyrinthiformis, growing in mangrove-shaded and exposed (unshaded) areas in the bays with the highest coral diversity (Otter Creek and Water Creek). Logistics prevented concurrent collection of similar data from reefs around St. John. However, we previously collected limited data from four sites on a nearby reef in Long Bay (approximately 2 km from the nearest mangrove coral study site and 6.3 m water depth, Fig. 1) from 16 July to 22 August 2004. The reef sites were characterized by scattered coral colonies of Orbicella annularis complex, Montastraea cavernosa. Porites porites, Porites astreoides, Agaricia agaricites, Favia fragum, Diplo- ria labyrinthiformis, and the hydrocoral Millepora alcicor- nis growing among sea fans, other gorgonians, sponges, turf algae, macroalgae and coral rubble. All seawater chemistry data from Hurricane Hole and Long Bay reef sites were col- lected near the seafloor (less than 0.5 m from the bottom). Additionally, we collected vertical profile data of carbon- ate system parameters over a coral habitat at 6.5 m water depth near the mouth of Otter Creek (Fig. 1) at 07:00 AST on 19 July 2011. Profile data were collected at 1.5, 3.0, 4.6, and 6.0 m depth. 2.1 Seawater chemistry Seawater was collected for AT, CT, and pHT analyses from each site every 4 h (n = 7) throughout 24 h periods in November 2010, July 2011, and July 2012. Measurements were made every 4 h for 3 consecutive days (n = 19) in Otter Creek during July 2012. No DO data were collected in Wa- ter Creek during July 2012 due to DO sensor failure. Twenty percent of pH values (47 of 225) were calculated from AT and CT. A peristaltic pump was used to pump seawater from less than 0.5 m above the seafloor through a 0.45 µm filter into 500 ml borosilicate glass bottles. Samples for AT and CT were preserved by adding 100 µL saturated HgCL2 solution. Bottles were positive-pressure sealed with ground glass stop- pers coated with Apiezon grease. Seawater samples for pHT were collected from the same peristaltic pump and filtered into 30 mL glass optical cells, and were analyzed within 1 h of collection. Samples were analyzed for AT (±1 µmol kg−1) using spectrophotometric methods of Yao and Byrne (1998) with an Ocean Optics USB2000 spectrometer and bromocre- sol purple indicator dye, for CT (±3 µmol kg−1) using a UIC carbon coulometer model CM5014 and CM5130 acidifica- tion module using methods of Dickson et al. (2007) and for pHT (±0.005) via spectrophotometric methods of Zhang and Byrne with an Ocean Optics USB2000 spectrometer and thymol blue indicator dye. Dissolved oxygen (±0.1 mg l−1), temperature (±0.01 ◦C), and salinity (±0.01) were measured using a YSI multimeter calibrated daily. Certified reference materials (CRM) for AT and CT analyses were from the Ma- rine Physical Laboratory of Scripps Institution of Oceanogra- phy (A. Dickson). Duplicate or triplicate analyses were per- formed on at least 10 % of samples. Seawater from Long Bay reef was also collected and ana- lyzed for AT and CT using the same methods as in Hurricane Hole. pHT was calculated from AT and CT using the carbon- ate speciation program CO2sys (Pierrot et al., 2006). Dis- solved oxygen (±0.1 mg l−1), temperature (±0.01 ◦C), and salinity (±0.01) were measured using a flow-through analyt- ical system and methods of Yates and Halley (2003). These data were collected at 07:00 (n = 7) or 11:00 (n = 3). Vertical profile data were collected by attaching a weighted peristaltic sampling tube (marked with depth in- crements) to the YSI multimeter and lowering the collec- tion apparatus to depth along a guide line attached to a buoy at the surface and a weight at the seafloor. Samples and measurements for AT, CT, pHT, DO, salinity, and temper- ature were collected and analyzed using the same methods as described for Hurricane Hole analyses. Carbonate sys- tem parameters for all study sites including aragonite min- eral saturation state (A) and pCO2 were calculated from AT, pHT (or AT and CT for Long Bay reef samples), tem- perature, and salinity measurements using the carbonate spe- ciation program CO2sys (Pierrot et al., 2006) with dissoci- ation constants K1 and K2 from Merbach et al. (1973) refit by Dickson and Millero (1987), KSO4 from Dickson (1990), www.biogeosciences.net/11/4321/2014/ Biogeosciences, 11, 4321–4337, 2014 4324 K. K. Yates et al.: Diverse coral communities in mangrove habitats and using the total pH scale (pHT). Correlation analysis of salinity-normalized total alkalinity (nAT) and dissolved in- organic carbon (nCT) was performed on Hurricane Hole data using methods of Suzuki and Kawahata (2003) to examine heterogeneity of chemical and biological processes. Seawater samples were collected for the measurement of total nitrogen and phosphate in November 2010 and July 2011. In November 2010, nutrient samples (n = 58) were collected in transects spanning the innermost reaches to the mouth of all three bays. During July 2011, water sam- ples were collected every 4 h throughout 24 h time periods at every sample site in all three bays. Water samples (20 mL) were filtered through 0.22 µm pore size Millepore Sterivex filters rinsed with two volumes of sample water. Samples were stored in 20 mL acid-washed polypropylene scintilla- tion vials at 0 ◦C until time of analysis. Nutrient samples were analyzed at the NOAA Atlantic Oceanographic and Meteorological Laboratory in Miami, FL. 2.2 Sediment samples Bulk surface sediment samples (approximately 2 kg wet weight) were collected via grab-sampling from the seafloor (approximately 1.2 m water depth) at each study site in each bay (Fig. 1). Wet samples were dehydrated to remove water and salts within 6 h of collection by rinsing with 70 % iso- propyl alcohol, allowing samples to settle, decanting the al- cohol, and repeating this process two additional times. Sam- ples were then allowed to air dry prior to analysis for grain size and composition. Grain size was measured via settling- tube for sand-sized fractions (Gibbs, 1974), and pipette for mud-sized fractions (Folk, 1965). Calcium carbonate con- tent was determined by the acid leaching method (Milliman, 1974). Total organic matter (TOM) was measured by loss on ignition (LOI) at 550 ◦C for > 2.5 h (Dean, 1974). Miner- alogic composition was measured by XRD on a Bruker D-8 advanced system using cobalt radiation at the University of Georgia, Department of Geology. 2.3 Coral surveys A list of coral species growing in Princess Bay, Otter Creek, and Water Creek was compiled based on over 100 sur- veys conducted by snorkeling the perimeter of each bay and identifying all live coral colonies growing from the shore- line to a depth of approximately 6 m (Rogers and Herlan, 2012). Minor coral bleaching was observed in July 2010 with more severe bleaching in August through October 2010. From November 2010 to January 2011, a complete census of colonies of Diploria labyrinthiformis and Colpophyllia natans (the most abundant framework-building corals in Hur- ricane Hole) was conducted in Otter Creek and Water Creek. The census included colonies growing in the mangroves and on the nearby substrate that sloped to the sandy bottom in each of the bays. Coral depths ranged from near the surface Table 2. Location of HOBO temperature loggers in Hurricane Hole. Logger ID Location Latitude (DD) Longitude (DD) 1208639 Otter Creek mid-bay 18.34965 −64.69215 9712498 Princess Bay mid-bay 18.35562 −64.69455 9712499 Otter Creek mid-bay 18.35160 −64.69240 9712501 Water Creek mid-bay 18.34777 −64.69076 9712501 Water Creek mid-bay 18.34773 −64.69072 9712503 Water Creek inner-bay 18.34963 −64.68951 9712511 Otter Creek inner-bay 18.35119 −64.69111 9712522 Otter Creek outer-bay 18.34950 −64.69243 9712524 Otter Creek inner-bay 18.35008 −64.69069 9712525 Water Creek mid-bay 18.34850 −64.69146 9712534 Water Creek inner-bay 18.35066 −64.68871 9712537 Water Creek outer-bay 18.34596 −64.69165 9712538 Princess Bay outer-bay 18.35328 −64.69333 9712540 Otter Creek inner-bay 18.35107 −64.69013 9712541 Water Creek mid-bay 18.34890 −64.69048 9712545 Princess Bay inner-bay 18.35615 −64.69069 9712546 Water Creek mid-bay 18.34755 −64.68956 9712547 Otter Creek inner-bay 18.35198 −64.69169 to about 6 meters. Each coral was photographed and exam- ined for condition (e.g., bleached or unbleached) and expo- sure (shaded or unshaded). A coral was considered shaded if it grew directly under mangroves or within a few meters of them where it received shading for at least a portion of each day. Subsets of these colonies in Otter Creek were re- examined in May 2011 to document recovery and mortality. Fisher’s exact tests performed in SAS 9.2 were used to com- pare the response of shaded and unshaded coral colonies for each species. Additionally, we calculated the log-odds ratios and confidence intervals to determine the effect of shading on coral bleaching for both species combined. 2.4 Temperature and PAR measurements Temperature measurements were collected every 2 h during 2010 and 2011 using HOBO Pendant data loggers at 18 lo- cations in Hurricane Hole (Table 2). Loggers were placed near mangrove and coral habitats at inner-, mid-, and outer- bay locations. Daily averages were generated from all log- gers. Temperature data from long-term monitoring transects were collected every 2 h from loggers at reef depth on the fore-reef slope area of six reefs around St. John during 2005 and 2010 by the National Park Service (Miller et al., 2009; National Park Service 2012). These data were used to cal- culate daily means at each site and averaged among sites to generate daily averages for the long-term reef transects. Photosynthetically active radiation (PAR) was measured ev- ery 15 min (15-minute averages) at study sites in Otter Creek and Water Creek approximately 20 cm above the seafloor us- ing LI-COR 4π sensors and approximately 3 m above sea level and above the mangrove canopy using LI-COR 2π sen- sors coupled with LiCor 1000 or LI-COR 1400 data loggers. PAR sensors were placed on the seafloor under the mangrove canopy and outside of the mangrove canopy at MNC and MC Biogeosciences, 11, 4321–4337, 2014 www.biogeosciences.net/11/4321/2014/ K. K. Yates et al.: Diverse coral communities in mangrove habitats 4325 Table 3. Grain size of surface sediments. Sample % Gravel % Sand % Silt % Clay % Mud Mean 81 % Carbonate % TOM2 % Insoluble location residue STJ5 71.0 20.7 4.7 3.5 8.2 −0.4 93.9 2.2 3.9 STJ7 14.9 80.6 3.7 0.8 4.5 1.0 73.8 0.3 25.9 STJ8 58.2 25.8 11.6 4.4 16.0 0.4 69.7 7.1 23.2 STJ10 15.0 27.7 44.2 13.1 57.3 3.5 54.6 11.9 33.5 STJ11 2.7 81.7 13.6 2.0 15.6 1.9 20.0 1.0 79.0 STJ12 9.2 88.2 1.0 1.6 2.6 1.3 96.8 0.1 3.1 STJ13 24.2 52.4 17.6 5.9 23.5 2.0 82.8 1.4 15.8 STJ14 38.0 31.2 27.0 3.7 30.8 1.6 74.9 6.2 18.9 STJ15 0.5 35.0 61.8 2.6 64.5 4.3 11.7 2.9 85.4 1 −log2 of the grain diameter in mm, 2 total organic matter from loss on ignition. See Fig. 1 for sample locations. Figure 2. Corals growing under a mangrove canopy and attached to mangrove prop roots including a colony of Colpophyllia natans (center of photo). sites, on the seafloor at unshaded ROC sites, and above the mangrove canopy at MC and MNC sites. 3 Results and discussion 3.1 Heterogeneity of the physical environment Heterogeneity in the physical environment provides for semi- isolation of coastal water masses from open ocean water en- abling local differentiation of physical, chemical, and bio- logical attributes of coastal ecosystems. The potential for a refuge to sustain characteristics that promote climate change resiliency is, in part, dependent upon the ability of the sys- tem to remain out of equilibrium with open ocean chemical conditions. The bays in Hurricane Hole range in area from 0.06 to 0.11 km2, have small watersheds ranging in size from 0.11 to 0.43 km2, are surrounded by steeply sloped, rocky hill- sides, and have a narrow (up to approximately 10 m) fringe of red mangroves (Rhizophora mangle). Bedrock is exposed as cliffs and outcrops along the coast and consists of ig- neous and metamorphic rocks including Cretaceous basalt, andesite, and keratophyre (Rankin, 1998). Carbonate sedi- ments on St. John are in situ marine biogenic carbonates. There is no permanent source of freshwater inflow to any of the bays, nutrient concentrations are low, water clarity is generally high, and tidal range is low (< 0.25 m). The inner areas of the bays are very shallow, less than 2 m, and well protected from high winds and seas. The mangrove fringe is thickest in the inner bays. Prop roots support abundant com- munities of reef and mangrove organisms including crustose coralline algae, and are surrounded by communities of inter- mediate density seagrass (Thalassia testudinum) and calcare- ous algae including Halimeda spp. and Penicillus spp. Very few corals are growing near inner-bay mangroves. Grain size analyses showed that sediments in the inner bays are primar- ily fine-grained ranging from 16 to 65 % mud-sized fractions (Table 3). Mid- to outer-bay areas are characterized by narrower mangrove fringes and shallow (< 1 m) water depths immedi- ately adjacent to the shoreline that slopes steeply to 5 to 10 m just beyond the mangrove canopy. The mangrove prop roots support sponges, crustose coralline algae, numerous sclerac- tinian corals and other organisms (Fig. 2). The outer bays are infrequently exposed to storm waves that remove fine- grained sediments, and sediments consist primarily of 69 to 96 % sand and gravel with occasional occurrences of large boulders (Table 3). Corals are growing attached directly to prop roots and to hard substrates under roots. Near the en- trance to the bays, there are rock outcrops with few or no mangroves nearby. These sites have primarily hard bottom substrate with small pockets of coarse-grained sediments, corals growing directly on the hard bottom, very sparse oc- currences of calcareous algae, and little seagrass growing nearby. www.biogeosciences.net/11/4321/2014/ Biogeosciences, 11, 4321–4337, 2014 4326 K. K. Yates et al.: Diverse coral communities in mangrove habitats Figure 3. Chemical and physical parameters. Median and range for chemical and physical parameters in Hurricane Hole bays during Novem- ber 2010, July 2011, and July 2012 and for Long Bay reef during July and August 2004 (n = 10). Measurements were made every 4 h throughout a diurnal cycle (n = 7) at each study site during November 2010 and July 2011, and July 2012, and for 3 consecutive days (n = 19) in Otter Creek during July 2012. Measurements at Long Bay reef were made at 07:00 and 11:00 (n = 7 and 3, respectively). No DO data were collected in Water Creek during July 2012 due to DO sensor failure. Red shaded areas (3g and 3h) show reported ranges for pCO2 and A thresholds for carbonate calcification and dissolution. Data and latitude/longitude of study sites are available at http://doi.pangaea.de/10.1594/PANGAEA.825752. 3.2 Chemical heterogeneity Heterogeneity in the physical environment and benthic community structure creates chemical micro-climates that can affect adjacent habitats. Variations in chemical trends were observed at the sub-kilometer scale in each bay and in association with specific habitat types (Fig. 3). MNC sites showed the lowest DO, pHT, and A (with the ex- ception of Otter Creek in November 2010) and highest pCO2, AT, and CT. Salinity and AT showed the high- est range in Water Creek and Princess Bay during Trop- ical Storm Tomás in November 2010. These bays have larger watersheds than Otter Creek and are more heav- ily influenced by terrestrial runoff during rain events. MC and ROC sites showed higher DO, pHT, and A, and lower pCO2, AT, and CT than MNC sites. Diurnal vari- ability was also observed at each study site. Lowest A, pHT, temperature and DO, and highest CT, pCO2, and TA generally occurred in early morning and were reflected in our 07:00 measurements (see http://doi.pangaea.de/10. 1594/PANGAEA.825752). Vertical profile data showed wa- ter column heterogeneity with considerable differences in A (1 0.34), pH (1 0.04), pCO2 (1 40 µatm), TA (1 45.3 µmol kg−1), and CT (1 20.9 µmol kg−1) between sur- face and bottom water (Fig. 4, Table 4), indicating that sur- Biogeosciences, 11, 4321–4337, 2014 www.biogeosciences.net/11/4321/2014/ K. K. Yates et al.: Diverse coral communities in mangrove habitats 4327 face water measurements do not reflect bottom water condi- tions. Average total nitrate and phosphate values (data at http: //doi.pangaea.de/10.1594/PANGAEA.825752) were near the limits of resolution for AT measurements and, therefore, were not included in calculation of carbonate system param- eters from AT and pHT measurements. Calcification/dissolution thresholds are the levels of A below which (and pCO2 levels above which) net dissolution of carbonate sediments exceeds calcification rates as deter- mined by in situ, mesocosm, and modeling studies of coral reef ecosystems. Aragonite saturation states fell considerably lower than threshold ranges of 3.0 to 3.2 and/or pCO2 ex- ceeded thresholds of 504 to 584 µatm (Langdon et al., 2003; Silverman et al., 2009; Yamamoto et al., 2012; Yates and Hal- ley, 2006) at all MNC study sites in Princess Bay and Wa- ter Creek during November 2010 and July 2011 and 2012. Thresholds at the Otter Creek MNC site were exceeded only during July 2011. Aragonite saturation states at all MC and ROC sites remained above threshold levels except in Water Creek and Princess Bay during the November 2010 tropical storm; pCO2 values were considerably lower at all MC and ROC sites than at MNC sites (Fig. 3g and h). Long Bay reef data were collected only at 07:00 and 11:00 AST (Fig. 3, Table 5). Therefore, only minimum A, pH, temperature and DO, and maximum TA, CT, and pCO2 values are comparable to Hurricane Hole data. Median data for reef parameters may be biased toward lower or higher values because they do not reflect full diurnal cycle condi- tions; comparison of reef data to Hurricane Hole excludes November 2010 data that reflect tropical storm conditions. Minimum reef A (2.93) was considerably lower than any other coral site in Hurricane Hole and lower than the re- ported range of dissolution thresholds. The lowest A (3.18) at Hurricane Hole coral sites occurred in Otter Creek dur- ing July 2011, and it was the only coral site that showed an A within the carbonate dissolution threshold range. All me- dian and maximum values from Hurricane Hole coral sites in July 2011 and July 2012 were above threshold ranges, and maximum values reached 4.2. Minimum pH at the reef was 7.894, and was lower than the lowest pH (7.950, also in Otter Creek during July 2011) recorded for any coral site in Hurri- cane Hole. Maximum pCO2 values at the reef (626 µatm) were higher than any coral site in Hurricane Hole (maxi- mum = 550 µatm in Water Creek, July 2011) and were above the reported dissolution threshold range. Our data indicate that A was not consistently elevated at mangrove coral sites relative to the reef. However, minimum A at mangrove coral sites was not as low as reef values, and, in most lo- cations, remained above thresholds for carbonate dissolution unlike reef values. X-ray diffraction analyses of sediments in Hurricane Hole indicated all MNC sites have the lowest percentages of car- bonate sediments (12 to 55 %) and no high-magnesium cal- cite (high-Mg calcite, the most soluble phase of calcium car- bonate) in two of the three bays (Princess Bay and Water Creek) despite the presence of crustose coralline algae that produce high-Mg calcite (Tables 3 and 6). Percent total or- ganic matter (TOM) was less than 12 % throughout the bays, but higher at inner- and mid-bay sites than outer-bay sites (Table 3). Low pHT and high pCO2 conditions generated by respiration and oxidation of organic matter at MNC sites cre- ate a chemical environment that is conducive to dissolution of fine-grained sediments produced by calcareous green al- gae and coralline algae associated with these mangrove com- munities. Highest percentages of carbonate sediments (70 to 97 %) and high-Mg calcite was found at all MC and ROC sites. The only MNC site with high-Mg calcite was in Ot- ter Creek. Our results suggest that dissolution of fine-grained carbonate sediments occurs in MNC areas with frequent ex- posure to pHT below 7.93 to 7.95, and coral growth is limited to areas with minimum pHT above 7.93 (Fig. 3d). 3.3 Process heterogeneity Process heterogeneity resulting from spatial variations in community structure and hydrographic conditions is a key factor in maintaining disequilibrium between coastal and open ocean water masses. Correlation of nAT and nCT can be used to indicate the potential influence of calcification, carbonate sediment dissolution, photosynthesis, and respira- tion on seawater carbonate chemistry (Suzuki and Kawahata, 2003). A linear regression slope approaching 2 indicates cal- cification and dissolution are dominant processes, and the slope can be used to calculate the ratio of net ecosystem cal- cification (NEC) to net community production (NCP). MNC sites generally showed a greater range of nAT and nCT and a greater influence from respiration and carbonate dissolu- tion than MC and ROC sites (Fig. 5). This result is consistent with low pHT, high pCO2, low mineral saturation state, and lower percentages of carbonate sediments characteristic of MNC sites. Eighteen of twenty-seven sites showed a correla- tion between nAT and nCT with r2 greater than 0.5 (Table 7). NEC : NCP for these sites showed a wide range between 0.14 and 12.1 (Table 7) reflecting the strong effect of variation in community structure on these processes. Lagrangian drifter studies conducted during August 2011 indicated that surface currents within the bays move primar- ily from the inner to outer bay due to prevailing easterly winds (McKenzie, 2012). Estimated water mass residence times are long (days) (McKenzie, 2012), which, combined with shallow water depths, increases the impact of NEC and NCP on seawater chemistry (Anthony et al., 2011). Carbon- ate sediment dissolution (a process that consumes CO2 and generates HCO− 3 and Ca2+) at upstream, inner-bay MNC sites may provide a source of alkalinity to downstream coral sites that helps maintain mineral saturation states and sup- ports coral calcification. This combined effect of hetero- geneity in community structure, hydrography, and biologi- cally driven changes in seawater chemistry has been demon- strated as an effective means to buffer decreases in mineral www.biogeosciences.net/11/4321/2014/ Biogeosciences, 11, 4321–4337, 2014 4328 K. K. Yates et al.: Diverse coral communities in mangrove habitats 10.0! 15.0! 20.0! 25.0! 30.0! 35.0! 40.0! Temperature (Co) ! Depth! ! 1.5 m! ! 3.0 m! ! 4.6 m! ! 6.0 m! 35.0! 35.5! 36.0! 36.5! 37.0! Salinity! Depth! ! 1.5 m! ! 3.0m! ! 4.6 m! ! 6.0 m! 5.6! 5.7! 5.8! 5.9! 6.0! 6.1! Dissolved oxygen (mg L-1) ! Depth! ! 1.5 m! ! 3.0 m! ! 4.6 m! ! 6.0 m! 7.98! 8.00! 8.02! 8.04! 8.06! pH! Depth! ! 1.5 m! ! 3.0 m! ! 4.6 m! ! 6.0 m! 2280! 2300! 2320! 2340! 2360! 2380! Total Alkalinity (µmol kg-1)! Depth! ! 1.5 m! ! 3.0 m! ! 4.6 m! ! 6.0 m! 1980! 1990! 2000! 2010! 2020! Total Carbon (µmol kg-1)! Depth! ! 1.5 m! ! 3.0 m! ! 4.6 m! ! 6.0 m! 380! 400! 420! 440! 460! pCO2 (µatm)! Depth! ! 1.5 m! ! 3.0 m! ! 4.6 m! ! 6.0 m! 3.4! 3.5! 3.6! 3.7! 3.8! 3.9! 4! 4.1! !A! Depth! ! 1.5 m! ! 3.0 m! ! 4.6 m! ! 6.0 m! Figure 4. Vertical profile data of seawater chemical parameters collected at 07:00 on 19 July 2011 over coral habitat at 6.5 m water depth. Vertical axis is depth below sea surface. Also refer to Table 4. Biogeosciences, 11, 4321–4337, 2014 www.biogeosciences.net/11/4321/2014/ K. K. Yates et al.: Diverse coral communities in mangrove habitats 4329 Table 4. Vertical profile data. Depth Temp. Sal. DO pHT TA CT pCO2 A (m) (◦C) (psu) (mg L−1) (µmol kg−1) (µmol kg−1) (µatm) 1.5 28.9 36.1 5.97 8.043 2368 2018 404 3.98 3.0 28.9 36.1 5.96 8.025 2336 2001 419 3.80 4.6 28.9 36.1 5.95 8.012 2322 1997 433 3.69 6.0 28.9 36.1 5.92 8.004 2323 2003 443 3.64 Vertical profile data were collected between 07:00 and 07:07 on 19 July 2011 near the mouth of Otter Creek at study site number STJ17 (Fig. 1). Also refer to Fig. 4. Table 5. Long bay reef data. Site Date Time Temp. Sal. DO pHT TA CT pCO2 A (AST) (◦C) (psu) (mg L−1) (µmol kg−1) (µmol kg−1) (µatm) 1 16 Jul 2004 11:00 28.7 35.7 6.9 7.996 2267 1962 443 3.47 1 18 Aug 2004 07:00 28.9 35.4 5.2 7.925 2283 2019 548 3.09 1 19 Aug 2004 07:00 29.2 35.2 5.0 7.955 2309 2023 509 3.33 2 16 Jul 2004 11:00 29.3 35.7 ND 8.031 2288 1954 404 3.80 2 17 Jul 2004 07:00 28.3 35.7 4.6 7.943 2286 2014 520 3.14 2 18 Aug 2004 07:00 28.6 35.4 5.3 7.937 2279 2010 528 3.12 2 19 Aug 2004 07:00 29.1 35.2 4.5 7.894 2282 2033 595 2.93 3 20 Jul 2004 11:00 28.8 35.7 7.2 8.006 2269 1956 431 3.55 3 22 Aug 2004 07:00 29.0 34.9 4.7 7.950 2275 2000 510 3.22 4 22 Aug 2004 07:00 29.0 34.9 4.9 7.936 2269 2002 529 3.13 Long Bay reef data were collected from four locations at 07:00 or 11:00 AST. between 16 July and 22 August 2004. ND = no data. Latitude and longitude for reefs sites are as follows: site 1 = 18.337972, −64.675944; 2 = 18.337944, 64.676028; 3 = 18.337833, −64.675861; 4 = 18.337806, 64.675917 (refer to Fig. 1 for reef location and to Fig. 3). saturation state and increase calcification in downstream communities in experimental coral/macroalgal assemblages (Anthony et al., 2011) and in seagrass/coralline algae and coral/seagrass assemblages on coral reefs in Tanzania and Moorea (Kleypas et al., 2011; Semesi et al., 2009a, b). This same combination of spatial and temporal variations in com- munity structure and processes in mangrove/coral habitats may help buffer against ocean acidification. 3.4 Biological responses The presence of decades-old coral colonies in these mangrove-lined bays suggests adaptation to higher water temperatures and more resistance to and rapid recovery from bleaching events such as the one that was followed by se- vere mortality from disease in 2005 on the island’s coral reefs. Coral surveys indicate at least 33 species of sclerac- tinian corals are growing in Hurricane Hole Bays (Table 1). Many coral colonies are growing directly on or close to man- grove prop roots, and others grow on rocks or hard substrate close to shore to a depth of approximately 6 m. Bleaching was observed on St. John’s coral reefs (NPS, 2012) and in Hurricane Hole in 2010. Initial surveys of bleached and un- bleached corals from November 2010 to January 2011 indi- cate that only 5 and 2 % of C. natans colonies were bleached in Otter Creek and Water Creek, respectively, while 58.9 and 17.4 % of D. labyrinthiformis colonies were bleached in Ot- ter and Water creeks, respectively. We chose these two coral species as the focus of our observations because they were the most abundant major reef-building species in Hurricane Hole, they are thriving there despite a decline in relative and absolute abundance of both species on St. John reefs dur- ing the 2005/2006 bleaching and disease event (Whelan et al. 2007, Miller et al. 2009), and both species typically occur in exposed as opposed to shaded locations. Re-examination of a subset of Otter Creek colonies in spring 2011 showed general recovery from bleaching but some mortality. Fisher’s exact test results indicated that different proportions of C. natans (72.5 % shaded, 27.5 % unshaded) and D. labyrinthiformis (18.2 % shaded, 81.8 % unshaded) were found in shaded versus unshaded condi- tions (p < 0.0001) and had different levels of initial bleach- ing (p < 0.0001, C. natans: no shaded colonies bleached, 10.5 % of unshaded colonies bleached; D. labyrinthiformis: 34.2 % of shaded colonies bleached, 66.1 % of unshaded colonies bleached). Different mortality outcomes were also observed combining partial and total mortality (p = 0.0327) (Fig. 6a and b, Table 8). There was no mortality of shaded C. natans colonies and 10.5 % mortality in unshaded colonies. D. labyrinthiformis showed 10.5 % mortality in shaded and www.biogeosciences.net/11/4321/2014/ Biogeosciences, 11, 4321–4337, 2014 4330 K. K. Yates et al.: Diverse coral communities in mangrove habitats Table 6. Carbonate mineralogical composition of surface sedi- ments. Sample Carbonate mineralogy location % Aragonite % Mg-calcite % Calcite STJ5 53.3 8.8 37.9 STJ7 75.4 8.0 16.7 STJ8 60.2 21.1 18.8 STJ10 70.7 16.3 13.1 STJ11 65.8 0.0 34.2 STJ12 82.3 16.5 1.2 STJ13 58.9 34.6 6.4 STJ14 74.6 11.3 14.1 STJ15 78.9 0.0 21.1 12.3 % mortality in unshaded colonies, respectively. More C. natans colonies grew in the shade than D. labyrinthiformis colonies. The fact that C. natans occurred statistically more often in the shade and that few of these colonies bleached supports the role of shading in providing refuge condi- tions. Although more unshaded D. labyrinthiformis colonies bleached and bleaching of these was more severe, shaded colonies were not more likely to recover normal pigmen- tation. For this species, shading affected the proportion of colonies that initially bleached (p < 0.0001), but not the out- come (p = 0.7582). Although more unshaded colonies of D. labyrinthiformis bleached, the mortality outcome for shaded and unshaded colonies was similar (p = 0.7508). Overall, re- covery from bleaching was high, with little mortality. Only two C. natans colonies bleached. Both had partial mortal- ity and none of the initially unbleached corals showed any mortality (p < 0.0001). Data in Table 8 were combined for both coral species into four categories and used to calcu- late log-odds ratios: (1) shaded, bleached; (2) shaded, un- bleached; (3) unshaded, bleached; and (4) unshaded, un- bleached (Table 8). Results indicate that the probability of unshaded corals bleaching relative to shaded corals is 8.84 at a 95 % confidence interval. All major Caribbean reef-building species, with the ex- ception of the acroporids, were observed in Hurricane Hole. Over 40 species of scleractinian corals and 3 species of Millepora occur in the US Virgin Islands (Rogers et al., 2008), and 33 have been seen in the mangroves. A rigorous quantitative comparison of the relative and absolute abun- dance of all the species of corals in the mangroves versus on the reefs around St. John is not possible primarily because so many of the corals are inaccessible growing in shallow water in the prop roots, and standard monitoring methods cannot be used. However, one can estimate the relative abundance of some of the coral species in the mangroves and on the reefs qualitatively based on direct observations and photographs. Data from the National Park Service (Atkinson and Miller, 2014) show species in the genus Orbicella consistently have had the highest cover on St. John’s reefs. This Orbicella Table 7. NEC : NEP ratios for study sites with nAT vs. nCT r2 > 0.5. Date Location Site NEC : NEP LRE r2 Nov 2010 Otter Creek MC NA 0.17570x + 2063 0.12 MNC 0.96 0.9795x + 376.87 0.86 ROC 12.11 2.1779x −2098.5 0.50 Water Creek MC NA −0.2660x + 3000.5 0.27 MNC 0.33 0.5031x + 1354.2 0.83 ROC NA −0.1158x + 2684.9 0.02 Princess Bay MC 0.32 0.4936x + 1343.3 0.57 MNC 3.35 1.5414x −823.71 0.93 ROC 0.75 0.8602x + 600.04 0.91 Jul 2011 Otter Creek MC 1.63 1.2413x −181.92 0.87 MNC NA 0.3334x + 1616.5 0.17 ROC 1.27 1.1153x + 66.438 0.70 Water Creek MC 0.44 0.6069x + 1075.7 0.68 MNC 0.80 0.8863x + 516.13 0.84 ROC 1.22 1.0582x + 192.54 0.58 Princess Bay MC 0.18 0.3060x + 1661.5 0.94 MNC 0.44 0.6141x + 1069.5 0.72 ROC NA 0.0369x + 2179.8 0.01 Jul 2012 Otter Creek MC 0.28 0.4376x + 1435.1 0.55 MNC NA 0.2189 + 1865.6 0.32 ROC NA 0.2080x + 1889.5 0.41 Water Creek MC NA 0.1773x + 1950.7 0.45 MNC 0.18 0.2965x + 1707.6 0.84 ROC NA 0.2915x + 1723.4 0.38 Princess Bay MC 0.25 0.4042x + 1507.2 0.89 MNC 0.14 0.2513x + 1810.3 0.95 ROC 0.31 0.4740x + 1366.3 0.85 Ratios of net ecosystem calcification to net community production (NEC : NCP) were calculated from the slopes of best-fit linear regression lines for 18 of 27 site measurements showing a correlation between nAT and nCT with r2 > 0.5. NEC : NCP was calculated using the expression 1/[(2/m) −1], where m is the slope from the corresponding linear regression equation (LRE). MC is mangrove–coral site, MNC is mangrove no coral site, and ROC is rock outcrop coral site. group is not as abundant in the mangroves as the two ma- jor reef-building species that we focused on in our research. The most common species in the mangroves are Colpophyl- lia natans, Diploria labyrinthiformis, Orbicella spp., Porites spp., and Agaricia spp. Colpophyllia natans and Diploria labyrinthiformis, the subject of the observations on bleach- ing and recovery reported here, have a higher relative and absolute abundance in some portions of Hurricane Hole than on the island’s coral reefs based on data on coral cover. Fur- thermore, these two species declined in relative and absolute abundance on the reefs as a result of bleaching and disease in 2005/2006. Many other species in the mangroves have an in- termediate abundance. Two coral species (Mycetophyllia and Scolymia), represented by only a few individuals in the man- groves, are more often found in deeper water (greater than 10 m) and are presumably able to survive because of shading by the mangroves. PAR measurements made above the sea surface and at the seafloor at MC sites and ROC sites of similar depth during November 2010, July 2011, and July 2012 indicate that PAR was attenuated during peak daylight hours of 10:00 to 14:00 by 88.6 ± 5.3 %, 70.7 ± 4.8 %, and 72.0 ± 1.7 % (Fig. 7), respectively, where corals grow shaded by the mangroves at MC sites. In addition to shading by mangrove trees, colored dissolved organic matter (CDOM) in the water near man- groves, especially where there is frequent freshwater input, could also attenuate harmful visible and ultraviolet radiation Biogeosciences, 11, 4321–4337, 2014 www.biogeosciences.net/11/4321/2014/ K. K. Yates et al.: Diverse coral communities in mangrove habitats 4331 2390! 2410! 2430! 2450! 2470! 2030! 2050! 2070! 2090! 2110! 2130! nAT (µmol kg-1)! Otter Creek! G! D! P! R! CU! CR! November 4 - 5, 2010! November 2010! 2100! 2150! 2200! 2250! 2300! 2350! 2400! 2450! 2500! 1900! 1950! 2000! 2050! 2100! 2150! 2200! Princess Bay! G! D! P! R! CU! CR! November 11 - 12, 2010! 2360! 2380! 2400! 2420! 2440! 2460! 2480! 2000! 2050! 2100! 2150! 2200! 2250! Water Creek! G! D! P! R! CU! CR! November 8 - 9, 2010! 2230! 2250! 2270! 2290! 2310! 2330! 1920! 1940! 1960! 1980! 2000! 2020! 2040! 2060! nAT (µmol kg-1)! G! D! P! R! CU! CR! July 15 - 16, 2011! July 2011! 2250! 2270! 2290! 2310! 2330! 2350! 1940! 1960! 1980! 2000! 2020! 2040! 2060! 2080! G! D! P! R! CU! CR! July 13 - 14, 2011! 2220! 2240! 2260! 2280! 2300! 2320! 2340! 1880!1900!1920!1940!1960!1980!2000!2020!2040! G! D! P! R! CU! CR! July 20 - 21, 2011! 2285! 2295! 2305! 2315! 1940! 1960! 1980! 2000! 2020! nAT (mmol kg-1)! nCT (µmol kg-1)! G! D! P! R! CU! CR! July 24 - 27, 2012! July 2012! 2280! 2290! 2300! 2310! 2320! 1940! 1960! 1980! 2000! 2020! 2040! 2060! nCT (µmol kg-1)! G! D! P! R! CU! CR! July 28 - 29, 2012! 2290! 2295! 2300! 2305! 2310! 2315! 2320! 2325! 2330! 1940! 1960! 1980! 2000! 2020! 2040! 2060! nCT (µmol kg-1)! G! D! P! R! CU! CR! July 22 - 23, 2012! Rock Outcrop Coral Mangrove Coral Mangrove No Coral Average nAT and nCT Figure 5. Salinity-normalized total alkalinity (nAT) and total carbon (nCT) plots with best-fit linear regressions (see Table 7 for equations and r2 values) for November 2010, July 2011, and July 2012 in Otter Creek, Water Creek, and Princess Bay. Average nAT and nCT for each time period was calculated from all data collected from each site within each bay. Gray lines represent the theoretical impact of calcification (G), carbonate sediment dissolution (D), photosynthesis (P), respiration (R), CO2 uptake (CU), and CO2 release (CR) on AT and CT. and reduce the photo-oxidative stress on corals (Fitt and Warner, 1995, Shick et al., 1996, Zepp et al., 2008, Ayoub et al., 2012). It is unlikely that CDOM is providing much additional shading in Hurricane Hole, but it could be a con- tributing factor. The water clarity is generally very high, par- ticularly in shallow water near the mangrove prop roots at our study sites. PAR data in Fig. 7 shows that PAR at the rock outcrops which are very close to the mangroves is not considerably attenuated relative to PAR measured in-air in- dicating that CDOM is likely not contributing much to the attenuation of solar radiation. Comparison of temperature records in the shallow waters of Hurricane Hole to coral reefs around St. John (Miller et al., 2009; National Park Service, 2012) indicate that corals grow- ing in Hurricane Hole are exposed to higher (0.5 ± 0.5 ◦C on average) and more variable temperatures than coral reefs around the island (Fig. 8). Low bleaching and mortality have been observed for corals growing on nearshore reefs of Palau that have constant exposure to high temperatures, more variable temperatures, and high vertical attenuation of light caused by suspended particulate matter (van Woesik et al., 2012). Experiments with corals from a shallow la- goon in American Samoa suggested that thermal tolerance www.biogeosciences.net/11/4321/2014/ Biogeosciences, 11, 4321–4337, 2014 4332 K. K. Yates et al.: Diverse coral communities in mangrove habitats Table 8. Condition of colonies of Diploria labyrinthiformis and Colpophyllia natans during 2010–2011. Colony condition D. labyrinthiformis D. labyrinthiformis C. natans C. natans shaded unshaded shaded unshaded Total number of colonies 38 171 50 19 Bleached to dead 1 5 0 0 Bleached to partial mortality 1 10 0 2 Bleached to unbleached 11 98 0 0 Unbleached to dead 1 2 0 0 Unbleached to partial mortality 1 4 0 0 Unbleached to unbleached 23 52 50 17 Summary Shaded Unshaded Bleached 13 115 Unbleached 75 75 Bleached-shaded and -unshaded, and unbleached-shaded and -unshaded data were combined for both species and used for log-odds ratio statistics. a. b. 0%! 10%! 20%! 30%! 40%! 50%! 60%! 70%! 80%! 90%! 100%! Shaded! Unshaded! Percent of colonies! 0! 20! 40! 60! 80! 100! Bleached corals that died entirely Bleached corals with partial mortality Bleached corals that recovered normal pigmentation Unbleached corals that died entirely Unbleached corals with partial mortality Unbleached corals that remained unbleached 0%! 10%! 20%! 30%! 40%! 50%! 60%! 70%! 80%! 90%! 100%! Shaded! Unshaded! Percent of colonies! 0! 20! 40! 60! 80! 100! Figure 6. Recovery results for shaded vs. unshaded (a) Diplo- ria labyrinthiformis (n = 38 and n = 171 for shaded and unshaded colonies, respectively) and (b) Colpophyllia natans (n = 50 and n = 19 for shaded and unshaded colonies, respectively) from 2010 to 2011. Also refer to Table 8. increased with previous exposure to highly variable tempera- tures (Oliver and Palumbi, 2011). Similarly, the resilience of mangrove corals following elevated temperatures likely re- sults from relief from solar radiation stress provided by shad- ing of corals by mangroves. 4 Alternative refuges and resiliency factors As reefs decline worldwide and sea level continues to rise, alternative shallow-water refuges like mangrove–coral habi- tats may be critical for insuring the survival of coral species. Few refuges have been identified to date. Potential refuges from thermal and irradiance stress have been suggested based on modeling (e.g., Karnauskas and Cohen, 2012; Fine et al., 2013) and field research (van Woesik et al., 2012). In Palau, corals exhibited less bleaching and mortality in bays where the highest temperatures were recorded, because of attenuation of light (shading) by suspended particulate mat- ter (van Woesik et al., 2012). Cloud cover substantially re- duced bleaching in the Society Islands in 1998, showing the role of increased solar irradiance in producing thermal stress in corals (Mumby et al., 2001). Based on modeling, Fine et al. (2013) suggest that the Gulf of Aqaba (Red Sea), where corals have very high bleaching thresholds, functions as a refuge because of its particular geographic configura- tion, with a thermal barrier at its southernmost end selecting more resistant coral genotypes. Glynn (1996) proposed that reefs near cool, upwelled waters might serve as refuges. Kar- nauskas and Cohen (2012) used models to show that warm- ing around a limited number of Pacific island reefs might be ameliorated by enhanced topographic upwelling accompany- ing a strengthening of the equatorial undercurrent. Riegl and Piller (2003) found some evidence of the role of upwelling in mitigating thermal stress in the Bahamas and South Africa. However, Chollett et al. (2010) showed that upwelling does not ensure that nearby reefs will act as refuges. Glynn (1996) also suggested that reefs far from detrimen- tal human activities might serve as refuges. However, sev- eral remote reefs that Riegl and Piller (2003) examined in the Caribbean had sustained significant loss of coral from bleaching and disease. The potential for deep reefs (often defined as 30 m and deeper) to serve as refuges for corals Biogeosciences, 11, 4321–4337, 2014 www.biogeosciences.net/11/4321/2014/ K. K. Yates et al.: Diverse coral communities in mangrove habitats 4333 Figure 7. Photosynthetically active radiation (PAR) measurements at study sites in Otter Creek (a, b, and c) and Water Creek (d and e). Measurements represent 15 min averages. STJ numerals indicate PAR sensor locations as referenced in Fig. 1. Data available at http: //doi.pangaea.de/10.1594/PANGAEA.825752. www.biogeosciences.net/11/4321/2014/ Biogeosciences, 11, 4321–4337, 2014 4334 K. K. Yates et al.: Diverse coral communities in mangrove habitats 24.0! 25.0! 26.0! 27.0! 28.0! 29.0! 30.0! 31.0! 32.0! J! F! M! A! M! J! J! A! S! O! N! D! Temperature (Co)! Month! Hurricane Hole mangrove-coral habitats, 2010 Hurricane Hole mangrove-coral habitats, 2011 Reef tract transects, 2005 Reef tract transects, 2010 Figure 8. Temperature trends from mangrove–coral and reef tract habitats. Hurricane Hole temperature data were averaged from 18 data loggers distributed throughout Hurricane Hole bays (Table 2). Temperature measurements were recorded every 2 h and daily av- erages were generated from all sites in Hurricane Hole and from 6 reef sites around St. John. Data are available at http://doi.pangaea. de/10.1594/PANGAEA.825752. and sources of replenishing larvae for shallower reef zones may be limited (Bongaerts et al., 2010). Deep (and moder- ately deep) reefs are not immune to major stressors includ- ing bleaching, disease (e.g. Riegl and Piller, 2003; Menza et al., 2007; Smith et al., 2010), and ocean acidification. Many coral species do not grow over an entire depth gradient, many do not broadcast (spawn) larvae, and deep corals may not, therefore, provide larvae that can settle and survive in shal- low waters. Recent studies indicate that some corals living on reefs downstream from seagrass beds and macroalgal com- munities where photosynthesis elevates A may be protected from ocean acidification (Manzello et al., 2012; Kleypas et al., 2011; Semesi et al., 2009a and b). However, many of those reefs may not be protected from thermal stress. Identi- fication and protection of natural, alternative, shallow-water refuges is essential as one of the few viable management strategies for sustaining coral and other reef species, and it provides one of the only direct actions that can be taken lo- cally to manage climate change impacts (Salm et al., 2006). The unlikely association of corals with mangroves in many coastal ecosystems due to unsuitable growth conditions has dissuaded previous consideration of these habitats as poten- tial coral refuges. Many mainland mangrove habitats espe- cially those with large watersheds and high rates of fresh- water runoff are not likely candidates for coral refuges. De- spite the fact that St. John is exposed to episodic storm events with high rainfall that can briefly lower salinity (for example as shown in our November 2010 data), corals are thriving in the bays of Hurricane Hole and have been for decades, partially because the island has no perennial streams. Study sites in Princess Bay showed lower coral diversity and abun- dance than in Otter and Water creeks perhaps because it re- ceives more freshwater runoff due to a larger watershed size. However, data are too few to quantify physical constraints on topographic boundaries that limit refuge potential for these coastal habitats. Numerous small tropical islands worldwide have physical characteristics similar to the US Virgin Islands (for example where freshwater input is limited due to small watersheds and no permanent sources of freshwater inflow) and the potential for suitable mangrove–coral refuge condi- tions. Our findings identify the first naturally existing, alter- native refuge from climate change for reef-building corals and provide baseline resiliency factors to assist in identify- ing and characterizing mangrove–coral habitats and other al- ternative refuges around the world. Mangrove–coral habitats provide evidence of ecosystem transition that may be a re- sponse to pressures from unprecedented rates of recent cli- mate change. Evidence of onshore migrations of coral in re- sponse to past changes in sea level rise is well documented in the geologic record (e.g. Hopley et al., 1983; Neumann and Macintyre, 1985). However, evidence for co-location of live corals and mangroves is not. These habitats may serve as an example of a novel coastal ecosystem (Graham et al., 2014) resulting from differential species responses, and pro- vide insights into future evolution of tropical coastal ecosys- tems with increasing sea level rise, thermal stress, and ocean acidification. We consider the St. John mangrove habitat as a refuge for corals because it provides relief from thermal and photo- oxidative stress through shading by mangroves and variabil- ity of seawater temperatures, and because biological and sed- imentological processes buffer declines of pH and carbonate mineral saturation states that can impede growth of calcify- ing organisms. Our study showed that two major reef builders exhibited different responses to elevated temperatures. High diversity and variable response of reef organisms to climate change increases the likelihood that at least some species will be able to persist in locations with particular environ- mental conditions in the face of changing climate (Rogers, 2013). Coral diversity within the mangroves could help make these systems more resilient to future stresses. Exposure to warmer and more variable conditions in the mangroves may also facilitate adaptation of these corals to higher tempera- tures and may enhance resiliency for future expansion under changing environmental conditions (van Woesik et al., 2012; Palumbi et al., 2014; Oliver and Palumbi, 2011). Carbon- ate mineral saturation states and pH on a nearby reef were lower than in the mangrove coral habitats. Furthermore, A and pCO2 on the reef surpassed critical carbonate dissolu- tion threshold ranges while those in mangrove coral habitats generally did not. We suggest that the ability of a refuge envi- ronment to consistently buffer declines in pH and carbonate saturation state (as opposed to periodically elevating them) to keep them from surpassing critical thresholds relative to reef environments is the most important factor for providing relief from ocean acidification. The physicochemical con- ditions and benthic heterogeneity in these mangrove–coral habitats showed the potential to buffer against ocean acid- ification like the seagrass/coralline algae/coral assemblages Biogeosciences, 11, 4321–4337, 2014 www.biogeosciences.net/11/4321/2014/ K. K. Yates et al.: Diverse coral communities in mangrove habitats 4335 Table 9. Resiliency factors for mangrove–coral refuges. Resiliency factor Local condition at mangrove–coral sites in St. John, US Virgin Islands Diversity and response of organisms · High diversity of coral species · More than 30 coral species identified · Variable response of organisms · Preferential growth of C. natans in shaded areas, more bleaching of exposed than shaded D. labyrinthiformis colonies Heterogeneity and habitat proximity · Community heterogeneity · Collocation of corals and mangroves, upstream to downstream tran- sition from mangrove/seagrass/algae to mangrove/coral habitat · Available substrate for coral settlement · Prop roots, hard bottom · Low NEC : NCP ratios at upstream or coral locations and proximity to coral growth sites · Average NEC : NEP of 0.5 to 0.9 at mangrove–coral (MC) sites and upstream mangrove, calcareous algae, seagrass communities (MNC), respectively Hydrographic and chemical conditions · Limited or no influence from permanent freshwater inflow · No permanent or frequent freshwater inflow · Long water mass residence times · Days (McKenzie, 2012) · Hydrographic conditions that maintain substrate appropriate for coral settlement and growth · Periodic influence from storm waves that prevents settlement of fine-grained sediments, low TOM (< 12 %), > 69 % sand and gravel · Seawater chemistry conducive to coral growth · Minimum pH 7.93, maximum pCO2 550 µatm, minimum A 2.82 Exposure · Consistent exposure of corals to higher, more variable tem- peratures · Average temperature 0.5 ± 0.5 ◦C higher than reef tract tempera- tures (2010) · Physical shading from solar radiation · Mangrove canopy attenuates > 70 % of incident photosynthetically active radiation (PAR) of Tanzania and Malaysia (Kleypas et al., 2011; Semesi et al., 2009a, b). Key resiliency factors for mangrove–coral habitats include (1) high diversity and variable response of coral species to climate change stressors, (2) heterogeneity of benthic community composition, processes, and proxim- ity of different habitat types, (3) hydrographic conditions that amplify biogeochemical effects on seawater chemistry and promote chemical characteristics that support coral growth, and (4) exposure to variable water temperatures and phys- ical shading of corals from solar radiation (Table 9). The appropriate combination of all of these factors for creating refuge conditions is not generally characteristic of most coral reef environments. Thus, only a few reef systems that pro- tect against increased temperatures, solar radiation, or ocean acidification have been identified, and none have been iden- tified that protect from all three stressors like the mangrove– coral habitats of St. John. Acknowledgements. We would like to thank Nasseer Idrisi and Sophia McKenzie for collection and analysis of hydrographic data. Our gratitude goes to Chelsea Bliss and Rich Young for total alkalinity and total carbon measurements. We would like to thank Hannah Yates for assisting with collection of seawater samples and chemical parameter measurements, and Casey Evans and Miranda Bona for assisting with coral surveys. Thanks to Andrea Atkinson with the National Park Service and John Lisle with the US Geological Survey for statistical analysis of the coral data. We would like to thank Robin Clair of Estate Zootenvaal for logistical support and Candace Oviatt for early comments on the manuscript. We appreciate insightful comments from two anonymous reviewers that greatly improved our manuscript. The research was funded by the Park-Oriented Biological Sup- port Program of the US Geological Survey and National Park Service, and by the Southeast Ecological Science Center and the Coastal and Marine Geology Program of the US Geological Survey. Edited by: W. Kiessling References Anthony, K. R. N., Kleypas, J. A., and Gattuso, J.-P.: Coral reefs modify their seawater carbon chemistry – implications for im- pacts of ocean acidification, Glob. Change Biol., 17, 3655-3666, 2011. Atkinson, A. and Miller, W. J.: Coral relative abundance at in- dex sites in Virgin Islands National Park, Generic Multimedia- 2211046, https://irma.nps.gov/App/Reference/Profile/2211046, 2014. Ayoub, L. M., Hallock, P., Coble, P. G., and Bell, S. S.: MAA-like absorbing substances in Florida Keys phytoplankton vary with distance from shore and CDOM: Implications for coral reefs, JEMBE, 420, 91–98, 2012. Baker, A. C., Glynn, P. W., and Riegl, B.: Climate change and coral reef bleaching: an ecological assessment of long-term impacts, recovery trends and future outlooks, Estuar. Coast. Shelf S., 40, 435–471, 2008. Beets, J., Lewand, L., and Zullo, E.: Marine community descrip- tions and maps of bays within the Virgin Islands National Park/Biosphere Reserve, Virgin Islands Resource Management www.biogeosciences.net/11/4321/2014/ Biogeosciences, 11, 4321–4337, 2014 4336 K. K. Yates et al.: Diverse coral communities in mangrove habitats Cooperative: Biosphere Research Report 2. US Department of the Interior, National Park Service, 117 pp., 1986. Berkelmans, R.: Time-integrated thermal bleaching thresholds of reefs and their variation on the Great Barrier Reef, Mar. Ecol. Prog. Ser., 229, 73–82, 2002. Bongaerts, P., Ridgway, T., Sampayo, E. M., and Hoegh-Guldberg, O.: Assessing the “deep reef refugia” hypothesis: focus on Caribbean reefs, Coral Reefs, 29, 309–327, 2010. Burke, L. M., Reytar, K., Spalding, M., and Perry, A.: Reefs at risk revisited, World Resources Institute, Washington, DC, 114 pp., 2011. Chollett, I., Mumby, P. J., and Cortes, J.: Upwelling areas do not guarantee refuge for coral reefs in a warming ocean, Mar. Ecol. Prog. Ser., 416, 47–56, 2010. Dean, W. E.: Determination of carbonate and organic matter in cal- careous sediments and sedimentary rocks by loss on ignition: comparison with other methods, J. Sed. Pet., 44, 242–248, 1974. Dickson, A. G.: Standard potential for the reaction: AgCl(s) + 1/2 H2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO− 4 in synthetic seawater from 273.15 to 318.15 K, J. Chem. Therm., 22, 113–127, 1990. Dickson, A. G. and Millero, J. J.: A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media, Deep-Sea Res., 34, 1733–1743, 1987. Dickson, A. G., Sabine, C. L., and Christian, J. R.: Guide to best practices for ocean CO2 measurements, in: PICES Special Pub- lication, 3, 191 pp., 2007. Eakin, C. M., Lough, J. M., and Heron, S. F.: Climate variability and change: monitoring data and evidence for increased coral bleach- ing stress, in: Coral Bleaching, Springer, Heidelberg, Germany, 41–67, 2009. Fabricius, K. E., Langdon, C., Uthicke, S., Humphrey, C., Noonan, S., De’ath, G., Okazaki R., Muehllehner, N., Glas, M. S., and Lough, J. M.: Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations, Nat. Clim. Change, 1, 165–169, 2011. Fine, M., Gildor, H., and Genin, A.: A coral reef refuge in the Red Sea, Glob. Change Biol., 19, 3640–3647, 2013. Fitt, W. K. and Warner, M. E.: Bleaching patterns of four species of Caribbean reef corals, Biol. Bull., 189, 298–307, 1995. Fitt, W. K., Brown, B. E., Warner, M. E., and Dunne, P.: Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals, Coral Reefs, 20, 51–65, 2001. Folk, R. L.: Petrology of Sedimentary Rocks, Hemphill Publishing Company, Austin, 37–38, 1965. Gibbs, R. J.: A settling tube for sand-sized analysis, J. Sed. Pet., 44, 583–588, 1974. Glynn, P. W.: Coral reef bleaching: facts, hypotheses and implica- tions, Global Change Biol., 2, 495–509, 1996. Graham, N. A. J., Cinner, J. E., Norstrom, A. V., and Nystrom, M.: Coral reefs as novel ecosystems: embracing new futures, Curr. Opin. Environ. Sustain., 7, 9–14, 2014. Hoegh-Guldberg, O.: Coral reef ecosystems and anthropogenic cli- mate change, Reg. Env. Change, 11, S215–227, 2011. Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., Knowlton, N., Eakin, C. M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R. H., Dubi, A., and Hatziolos, M. E.: Coral reefs under rapid climate change and ocean acidification, Science, 318, 1737–1742, 2007. van Hooidonk, R., Manyard, J. A., Manzello, D., and Planes, S.: Op- posite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs, Glob. Change Biol., 20, 103– 112, 2014. Hopley, D., Slocombe, A. M., Muir, F., and Grant, C.: Nearshore fringing reefs in North Queensland, Coral Reefs, 1, 151–160, 1983. Karnauskas, K. and Cohen, A.: Equatorial refuge amid tropical warming, Nat. Clim. Change, 2, 530–534, 2012. Keller, B. D., Gleason, D. F., McLeod, E., Woodley, C. M., Airame, S., Causey, B. D., Friedlander, A. M., Grober-Dunsmore, R., Johnson, J. E., Miller, S. L., and Steneck, R. S.: Climate change, coral reef ecosystems, and management options for marine pro- tected areas, Environ. Manage., 44, 1069–1088, 2009. Keppel, G., Van Niel, K. P., Wardell-Johnson, G. W., Yates, C. J., Byrne, M., Mucina, L., Schut, A. G. T., Hopper, S. D., and Franklin, S. E.: Refugia: identifying and understanding safe havens for biodiversity under climate change, Global Ecol. Bio- geogr., 21, 393–404, 2012. Kleypas, J. A. and Yates, K. K.: Coral reefs and ocean acidification, Oceanography, 22, 108–117, 2009. Kleypas, J. A., Anthony, K. R. N., and Gattuso, J-P.: Coral reefs modify their seawater carbon chemistry – study from a barrier reef (Moorea, French Polynesia), Glob. Change Biol., 17, 3667– 3678, 2011. Langdon, C., Broecker, W. S., Hammond, D. E., Glenn, E., Fitzsim- mons, K., Nelson, S. G., Peng, T.-H., Hajdas, I., and Bonani, G.: Effect of elevated CO2on the community metabolism of an ex- perimental coral reef, Global Biogeochem. Cy., 17, 11-1–11-14, 2003. Lesser, M. P.: Coral bleaching: causes and mechanisms, in: Coral Reefs: An Ecosystem in Transition, Springer, Dordrecht, 405– 419, 2011. Macintyre, I. G., Goodbody, I., Rutzler, K., Littler, D. S., and Littler, M. M.: A general biological and geological survey of the rims of ponds in the major mangrove islands of the Pelican Cays, Belize, Atoll Res. Bull., 467, 13–44, 2000. Manzello, D. P., Enochs, I. C., Melo, N., Gledhill, D. K., and Johns, E. M.: Ocean acidification refugia of the Florida Reef Tract, PLoS ONE, 7, e41715, doi:10.1371/journal.pone.0041715, 2012. McClanahan, T. R., Maina, J. M., and Muthiga, N. A: Associations between climate stress and coral reef diversity in the western In- dian Ocean, Glob. Change Biol., 17, 2023–2032, 2011. McKenzie, S.: Influence of oceanographic processes on the distri- bution of coral communities in Hurricane Hole, St. John, United States Virgin Islands, MS thesis, University of the Virgin Islands, US Virgin Islands, 51 pp., 2012. Menza, C., Kendall, M., Rogers, C., and Miller, J.: A deep reef in deep trouble, Continent. Shelf Res., 27, 2224–2230, 2007. Merbach, C., Culberson, C. H., Hawley, J. E., and Pytdowicz, R. M.: Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure, Limnol. Oceanogr., 18, 897–907, 1973. Miller, J., Muller, E., Rogers, C., Waara, R., Atkinson, A., Whelan, K. R. T., Patterson, M., and Witcher, B.: Coral disease following Biogeosciences, 11, 4321–4337, 2014 www.biogeosciences.net/11/4321/2014/ K. K. Yates et al.: Diverse coral communities in mangrove habitats 4337 massive bleaching in 2005 causes 60 % decline in coral cover on reefs in the US Virgin Islands, Coral Reefs, 28, 925–937, 2009. Milliman, J. D.: Marine Carbonates, Springer-Verlag, New York, 1974. Mumby, P. J. and Steneck, R. S.: Coral reef management and conservation in light of rapidly evolving ecological paradigms, Trends Ecol. Evol., 23, 555–563, 2008. Mumby, P. J., Chisholm, J. R. M., Edwards, A. J., Andrefouet, S., and Jaubert, J.: Cloudy weather may have saved Society Island reef corals during the 1998 ENSO event, Mar. Ecol. Prog. Ser., 222, 209–216, 2001. National Park Service South Florida/Caribbean Network: Annual administrative report (FY 2011) and work plan (FY 2012) for inventories and vital signs monitoring: South Florida/Caribbean Network, Natural Resource Report NPS/SFCN/NRR, National Park Service, Fort Collins, Colorado, 2012/488, 2012. Neumann, A. C. and Macintyre, I.: Reef response to sea level rise: keep-up, catch-up or give up, in: Proceedings of the Fifth Inter- national Coral Reef Congress, 3, Tahiti, 27 May – 1 June 1985, 105–110, 1985. Oliver, T. A. and Palumbi, S. R.: Do fluctuating temperature envi- ronments elevate coral thermal tolerance?, Coral Reefs, 30, 429– 440, 2011. Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N, and Bay, R. A.: Mechanisms of reef coral resistance to future climate change, Science, 344, 895–898, 2014. Pierrot, D. E., Lewis, E., and Wallace, D. W. R.: Ms Excel pro- gram developed for CO2 system calculations, ORNL/CDIAC- 105a, Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Ten- nessee, 2006. Rankin, D. W.: Geology of St. John, US Virgin Islands, US Dept. of Interior, 1631 pp., 2002. Riegl, B. and Piller, W. E.: Possible refugia for reefs in times of environmental stress, Int. J. Earth Sci., 92, 520–531, 2003. Rogers, C. S.: Coral reef resilience through biodiversity, ISRN Oceanography: Article ID 739034, 18 pp., 2013. Rogers, C. S. and Herlan, J. J.: Life on the edge: corals in man- groves and climate change, in: Proceedings of the 12th Interna- tional Coral Reef Symposium, Cairns, Australia, 5 pp., 2012. Rogers, C. S., Miller, J., Muller, E. M., Edmunds, P., Nemeth, R. S., Beets, J. P., Friedlander, A. M., Smith, T. B., Boulon, R., Jeffrey, C. F. G., Menza, C., Caldow, C., Idrisi, N., Kojis, B., Monaco, M. E., Spitzack, A., Gladfelter, E. H., Ogden, J. C., Hillis-Starr, Z., Lundgren, I., Schill, W. B., Kuffner, I. B., Richardson, L. L., Devine, B., Voss, J.: Ecology of Coral Reefs in the US Virgin Islands, Chapter 8, in: Riegl, B. and Dodge, R. E., Coral Reefs of the USA, Springer, 303–374, 2008. Rutzler, K., Diaz, M. C., Van Soest, R. W. M., Zea, S., Smith, K. P., Alvarez, B., and Wulff, J.: Diversity of sponge fauna in man- grove ponds, Pelican Cays, Belize, Atoll Res. Bull., 229, 466– 495, 2000. Salm, R. V., Done, T., and Mcleod, E.: Marine protected area plan- ning in a changing climate, in: Coral Reefs and Climate Change: Science and Management, American Geophysical Union, Wash- ington, DC, 207–221, 2006. Semesi, S., Beer, S., and Bjork, M.: Seagrass photosynthesis con- trols rates of calcification and photosynthesis of calcareous macroalgae in a tropical seagrass meadow, Mar. Ecol. Prog. Ser., 382, 41–47, 2009a. Semesi, S., Kangwe, J., and Bjork, M.: Alterations in pH and CO2 affect calcification and photosynthesis in the tropical coralline alga, Hydrolithon sp. (Rhodophyta), Estuar. Coastal Shelf S., 84, 337–341, 2009b. Silverman, J., Lazar, B., Cao, L., Caldeira, K., and Erez, J.: Coral reefs may start dissolving when atmospheric CO2 doubles, Geo- phys. Res. Lett., 36, L05606, doi:10.1029/2008GL036282, 2009. Smith, T. B., Blondeau, J., Nemeth, R. S., Pittman, S. J., Calnan, J. M., Kadison, E., and Gass, J.: Benthic structure and cryp- tic mortality in a Caribbean mesophotic coral reef bank system, the Hind Bank Marine Conservation District, US Virgin Islands, Coral Reefs, 29, 289–308, 2010. Suzuki, S. and Kawahata, H.: Carbon budget of coral reef systems: an overview of observations in fringing reefs, barrier reefs and atolls in the Indo-Pacific regions, Tellus 55B, 428–444, 2003. West, J. M. and Salm, R. V.: Resistance and resilience to coral bleaching: implications for coral reef conservation and manage- ment, Cons. Biol., 17, 956–967, 2003. Whelan, K. R. T., Miller, J., Sanchez, O., and Patterson, M.: Im- pact of the 2005 coral bleaching event on Porites porites and Colpophyllia natans at Tektite Reef, US Virgin Islands, Coral Reefs, 26, 689–693, 2007. van Woesik, R., Houk, P., Isechal, A. L., Idechong, J. W., Victor, S., and Golbuu, Y.: Climate change refugia in the sheltered bays of Palau: analogs of future reefs, Ecol. Evol, 2, 2472–2484, 2012. Yamamoto, S., Kayanne, H., Terai, M., Watanabe, A., Kato, K., Negishi, A., and Nozaki, K.: Threshold of carbonate saturation state determined by CO2 control experiment, Biogeosciences, 9, 1441–1450, doi:10.5194/bg-9-1441-2012, 2012. Yao, W. and Byrne, R. H. Simplified seawater alkalinity analy- sis: use of linear array spectrometers, Deep-Sea Res. Part 1, 45, 1383–1392, 1998. Yates, K. K. and Halley, R. B.: CO2− 3 concentration and pCO2 thresholds for calcification and dissolution on the Molokai reef flat, Hawaii, Biogeosciences, 3, 357–369, doi:10.5194/bg-3-357- 2006, 2006. Zepp, R. G., Shank, G. C., Stabenau, E., Patterson, K. W., Cyter- ski, M., Fisher, W., Bartels, E., and Anderson, S. L.: Spatial and temporal variability of solar ultraviolet exposure of coral assem- blages in the Florida Keys: importance of colored dissolved or- ganic matter, Limnol. Oceanogr., 53, 1909–1922, 2008. Zhang, H. and Byrne, R. H.: Spectrophotometric pH measurements of surface seawater at in-situ conditions: absorbance and proto- nation behavior of thymol blue, Mar. Chem., 52, 17–25, 1996. www.biogeosciences.net/11/4321/2014/ Biogeosciences, 11, 4321–4337, 2014