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  REPORT Calcifying coral abundance near low-pH springs: implicationsfor future ocean acidification E. D. Crook • D. Potts • M. Rebolledo-Vieyra • L. Hernandez • A. Paytan Received: 11 July 2011/Accepted: 1 November 2011 Ó The Author(s) 2011. This article is published with open access at Abstract Rising atmospheric CO 2 and its equilibrationwith surface ocean seawater is lowering both the pH andcarbonate saturation state ( X ) of the oceans. Numerouscalcifying organisms, including reef-building corals, maybe severely impacted by declining aragonite and calcitesaturation, but the fate of coral reef ecosystems in responseto ocean acidification remains largely unexplored. Naturallylow saturation ( X * 0.5) low pH (6.70–7.30) groundwaterhas been discharging for millennia at localized submarinesprings (called ‘‘ojos’’) at Puerto Morelos, Me´xico near theMesoamerican Reef. This ecosystem provides insights intopotential long term responses of coral ecosystems to lowsaturation conditions. In-situ chemical and biological dataindicate that both coral species richness and coral colonysize decline with increasing proximity to low-saturation,low-pH waters at the ojo centers. Only three scleractiniancoral species ( Porites astreoides , Porites divaricata , and Siderastrea radians ) occur in undersaturated waters at allojos examined. Because these three species are rarely majorcontributors to Caribbean reef framework, these data mayindicate that today’s more complex frame-building speciesmay be replaced by smaller, possibly patchy, colonies of only a few species along the Mesoamerican Barrier Reef.The growth of these scleractinian coral species at under-saturated conditions illustrates that the response to oceanacidification is likely to vary across species and environ-ments; thus, our data emphasize the need to better under-stand the mechanisms of calcification to more accuratelypredict future impacts of ocean acidification. Keywords Ocean acidification Á Coral reefs Á Calcification Á Saturation state Á Omega Introduction AtmosphericCO 2 iscurrentlyontherise,anditsequilibrationwith surface seawater is expected to reduce the pH of thesurface oceans by approximately 0.4 pH units by year 2100(Caldeira and Wickett2005; Orr et al.2005; Doney et al. 2009). Numerous calcifying organisms, including reef-buildingcorals,maybeseverelyimpactedbythisreductioninpH,whichwilllowerthearagoniteandcalcitesaturationstate( X ) and make skeletal and shell formation for many organ-isms more difficult (Fine and Tchernov2007; Anthony et al.2008; Doney et al.2009). Recent field studies in the Medi- terranean and Papua New Guinea have demonstrated strongimpacts of low pH related to volcanic CO 2 vents on bothindividualorganisms andcommunitystructure (Hall-Spenceret al.2008; Cigliano et al.2010; Dias et al.2010; Rodolfo- Metalpa et al.2010; Fabricius et al.2011). However, additional field studies under different natural conditions arenecessary to ascertain a wider range of potential long-termimpactsofoceanacidificationoncommunitiesandecosystemprocesses (Doney et al.2009; Riebesell et al.2010). Communicated by Environment Editor Prof. Rob van Woesik  Electronic supplementary material The online version of thisarticle (doi:10.1007/s00338-011-0839-y) contains supplementarymaterial, which is available to authorized users.E. D. Crook  Á D. Potts Á A. Paytan ( & )Institute of Marine Science, University of California,1156 High Street, Santa Cruz, CA 95064, USAe-mail: apaytan@ucsc.eduM. Rebolledo-Vieyra Á L. HernandezUnidad de Ciencias del Agua (UCIA), Centro de Investigacio´nCientı´fica de Yucata´n, A.C., Calle 8 # 39, Lote 1, Manzana 29,S.M. 64, 77524 Cancu´n, Quintana Roo, Me´xico  123 Coral ReefsDOI 10.1007/s00338-011-0839-y  AlongtheeasterncoastoftheYucata´nPeninsula,Me´xico(Electronic Supplementary Material, ESM Fig. 1S), near-shore springs, referred to locally as ‘‘ojos,’’ discharge natu-rally low-pH, low carbonate saturation groundwater ( X = [Ca 2 ? ][CO 32 - ]/K’ sp ). These highly localized springs are anatural feature of the karst terrain, have been continuouslydischarging water for millennia (Beddows et al.2002), andhave been the focus of many studies since the early 1990s(van Tussenbroek 1995; Ruiz-Renteria et al.1998; Carru- thers et al.2005). Discharge from these ‘‘ojos’’ is markedlymore acidic (pH = 6.70–7.30 total scale) and less saturated( X arag = 0.30–0.97 at ojo centers) than the surroundingocean water ( X arag = 3.60), and they occur in close prox-imity toone of the Caribbean’s largest coral reef ecosystems(the Mesoamerican Barrier Reef). Thus, the ojos of the Yu-cata´n Peninsula provide a natural laboratory for examiningthe long-term impacts of low saturation waters on specificorganismsandthecoastalecosystem.Specifically,muchcanbe learned from this site about the response of calcifyingorganisms exposed to reduce saturation states over timescales much longer than the life span of individual organ-isms. The conditions creating low-pH seawater at the ojosdiffer from those of the ocean acidification scenario: spe-cifically, the discharging water at the ojos is derived fromhigh CO 2 concentrations associated with brackish water thathasinteractedwithsoilandlimestone.Itisthuscharacterizedby low pH, high Ca 2 ? (salinity normalized), high dissolvedinorganic carbon (DIC), and high total alkalinity (TA).However, the organisms residing at the ojos have beenexposed to low-pH and low aragonite saturation, as is pre-dicted for future ocean acidification (Table1), but theorganisms are also exposed to high nutrients, high dissolvedinorganiccarbon,and highalkalinitythat are notnecessarilypredicted in future oceans subjected to acidification. Table 1 Chemical measurements and calculations at centers of ojo dischargeDate and site DIC ± 3 l mol kg - 1 TA ± 2 l mol kg - 1 Salinity Temp ° C pH X cal X arag Control 2,099 2,403 35.5 31.6 8.03 5.35 3.60June 2009Ojo Gorgos 3,545 3,427 28.6 27.2 7.13 1.15 0.75Ojo Norte 3,122 3,113 28.7 27.0 7.23 1.28 0.84Ojo Laja 3,314 3,228 25.8 28.1 7.20 1.22 0.79Ojo Mini 4,246 3,771 25.9 27.2 6.74 0.50 0.32Ojo H-10 Fractura 2,773 2,740 30.5 29.2 7.24 1.30 0.86Ojo Fractura 3,996 3,864 26.7 30.4 7.10 1.45 0.96November 2009Ojo Gorgos (1) 3,340 3,279 26.2 28.3 7.25 1.41 0.91Ojo Gorgos (2) 3,466 3,264 25.4 25.8 7.01 0.81* 0.54*Ojo Laja 3,473 3,392 26.9 28.3 7.21 1.35 0.88Ojo Pargos (1) 3,156 3,095 24.7 24.9 7.29 1.32 0.87Ojo Pargos (2) 3,178 3,109 25.2 25.2 7.26 1.28 0.82Ojo Mini 5,233 4,691 25.3 25.6 6.79 0.65* 0.41*August 2010Ojo Gorgos (1) 3,194 3,097 29.6 27.2 7.14 1.38* 0.90*Ojo Gorgos (2) 3,326 2,996 29.6 27.2 6.77 0.75* 0.49*Ojo Norte 3,326 3,142 29.2 27.0 6.61 0.77 0.50Ojo Laja 3,187 3,027 28.7 27.5 7.02 0.91* 0.6*Ojo Pargos (1) 3,332 3,079 28.7 27.5 6.88 0.70* 0.46*Ojo H-10 Fractura 3,407 2,736 29.4 27.9 7.09 0.81* 0.54*Ojo de Agua 3,145 2,946 29.7 27.2 6.94 0.84* 0.55*Summary of chemical parameters measured over three sampling excursions (June 2009, November 2009, and September 2010) at the 10 ojos.Values reported are from the centers of discharge, and analytical measurement errors are indicated. Saturation values were calculated using theprogram CO 2 Sys, unless noted by (*), which indicates that measured calcium concentrations were higher than expected due to limestonedissolution. CO 2 dissociation constants in CO 2 Sys were calculated from Mehrbach et al. (1973), refit by Dickson and Millero (1987), and pH isreported on the total scale. In the case of (*), a more conservative estimate of  X is reported that accounts for these higher Ca 2 ? concentrations(see Fig. 3, Supplementary Material). Natural variability in water characteristics based on samples collected at different times during thesampling trips was approximately: TIC (7%), TA (6%), Salinity (6%), and Temperature (4%). Natural variability in calculated pH (total scale)and saturation levels using CO 2 Sys at sites sampled multiple times were pH (2%) and X (20%). Continuous pH data are published in Hoffmanet al. (2011), and nutrient concentrations are available upon request from the corresponding authorCoral Reefs  123  Yet, these environments provide an opportunity to study insitu community impacts on corals exposed to low carbonatesaturation conditions and often extreme drops in pH forextended time intervals.At least thirteen ojos lie approximately 500 m offshorewithin the National Maritime Park at Puerto Morelos, in ashallow lagoon approximately 5 m deep (ESM Fig. 1S).The ojos range from 10-m long ‘‘fractures’’ to small circulardepressions (seeps) only a few centimeters across (ESMFig, 2S). Based on monitoring over two and a half years(April 2008 to September 2010), discharge from the ojos iscontinuous with a combined discharge flux (estimatedusing excess 224 Ra measurements) reaching as high as * 800,000 m 3 h - 1 (Derse et al.2008). Discrete watersamples taken during three different sampling events (June2009, November 2009, and September 2010) indicate thatthe pH(and other waterchemicalcharacteristics) ateach ojocenter varied on tidal time scales. However, the water dis-charged at the ojo center remained undersaturated during allsampling events (Table1). Continuous pH monitoring over2 months using a SeapHOx sensor supports this conclusion(Hofmann et al.2011). The relationship between waterchemistry and benthic biota (identity, density, and size) wasinvestigated at 10 ojos dominated by rocky substrates andcharacterized by similar temperature, salinity, light, and pHconditions over the three different sampling events. Wereport the calculated saturation states (Pierrot et al.2006)based onmeasured DIC, TA,and nutrientconcentrations foreachdiscretesampleusingCO 2 Sys.Forsampleswithhigherthan expected Ca 2 ? concentrations, conservative aragonitesaturation values were calculated based on measured Ca 2 ? concentrations (Table1). Materials and methods The area of influence of the low-pH waters was determinedby direct measurement of physiochemical parameterseither in situ (temperature, salinity, and pH) or from dis-crete water samples (DIC, TA, salinity, and nutrients).In the case of circular seeps (see Fig.1e), water sampleswere collected at 0.25-m intervals along transects placed atright angles and intersecting over the center of each ojo:transects were at least 4 m from the ojo center in alldirections. In the case of fractures (see Fig.1a, d), sampleswere taken along one long transect (up to 10 m) followingthe fracture line, and samples were also collected at 5 ormore cross-transect lines perpendicular to the main frac-ture. Divers collected the water in syringes that wereimmediately transported to a waiting boat for filtration,poisoning (for DIC and TA), and storage using standardoperating procedures outlined by Dickson et al. (2007). Fig. 1 Saturation state distribution along select transects in thevicinity of three different ojos with pictures of corals situated aroundthe ojo centers. The saturation state ( X arag ) is shown as a contourimage (plotted in Surfer Ò ), and the colors represent the range of saturation levels from blue (low saturation) to red  (supersaturation).The contour image gives a visual representation of what the saturationstate may look like along a sample transect line. The saturation ( X arag )values were determined based upon discreet water samples taken at0.25-m intervals (up to 36 samples per transect). Distance along the transect line is noted in the contour image in meters (  X axis ), and the Y axis represents 0.25 cm. The coral images give examples of wherethe corals were found along these transect lines. a (Ojo Laja) and d (Ojo Fractura) are examples of large ‘‘fractures,’’ while e (Ojo deAgua) is a large circular ‘‘seep’’. Calcifying coral species including Siderastrea radians ( b ) and Porites astreoides ( c , f  ) were found inundersaturated and low saturation water at all 10 ojos sampled. Sixadditional species including Agaricia (alongside Porites ) g lived insupersaturated waters where X arag [ 2.5Coral Reefs  123  Ecological surveys commenced after the water wassampled to reduce the risk of contamination or mechanicalmixing by divers. Data from benthic biota (identity, den-sity, and size) around each ojo were scored in contiguous0.25 9 0.25 m quadrats along the transect lines as descri-bed above (ESM Fig. 5S). Particular care was taken torecord coral size and position within each transect.DIC samples were analyzed in triplicates on a model5011 CO 2 Coulometer (UIC, Inc), and care was taken toensure that the samples were not exposed to the atmosphereprior to analysis (measurement error of  ± 3 l M). The TAsamples were run using an automated, open-cell, potenti-ometric titration procedure (measurement error ± 2 l M).Certified CO 2 reference material (Batch 90) from theAndrew Dickson lab at UC San Diego was used to ascer-tain the quality of results obtained. Nutrient (NO 3 - , NO 2 - ,NH 4 ? , Si, and PO 4 - 3 ) analyses were run on a flow injectionautoanalyzer (FIA, Lachat Instruments Model QuickChem8000) using standard procedures. Ca 2 ? concentrations weredetermined via ICP-OES (Perkin Elmer Optima 4300)using standard dilution and internal spikes. The carbonatesystem (carbonate saturation) was calculated from themeasured parameters (DIC, TA, pH, temperature, salinity,Ca, and nutrients) using the program CO 2 Sys (see Table1).Total coral area was calculated based on observedmeasurements from the field and reported as area coverageper 25 cm 2 . Due to differences in the area influenced by theojo waters between sites (e.g., discharge flux was differentat each ojo as was the area impacted by the dischargingwater), statistical analyses were conducted for data groupedbased on the calculated saturation state. Samples weregrouped by ‘‘supersaturation’’ ( X [ 2.5), ‘‘low saturation’’(1 \ X \ 2.5), and ‘‘undersaturation’’ ( X \ 1) at each site. Results At all 10 ojos sampled, the center of each discharge point(Fig.1) was undersaturated with respect to aragonite (i.e., X arag \ 1), and low saturation conditions (i.e., X arag \ 2.5)were seen close to the discharge area. Saturation valuesincreased rapidly with distance from the ojo center (Fig.1).While waters generally reached saturation ( X arag = 1)within 0.5 m of the center of discharge, saturation valuesbelow 2.5 were observed up to 2 m from the ojo (ambient X in the lagoon was 3.60; see Fig.1). Salinities at the ojocenter were always lower than ambient due to the brackishdischarge, but not lower than 25. Despite these low salin-ities, Ca 2 ? concentrations were generally somewhat higherthan expected from simple dilution of seawater to themeasured salinities, because Ca 2 ? was added to thegroundwater from the dissolution of limestone (ESMFig. 3S). DIC and TA concentrations were highest at the Fig. 2 a Number of species as a function of saturation state.No ‘‘other hard corals’’ (  Diploria , Montipora , Montastrea , Agaricia , Porites , and Favia sp .) were found in low saturation or undersaturated( X \ 2.5) waters. Species richness increased significantly( P \ 0.001) with increasing saturation state. b Coral size as afunction of saturation state for the different species. Average valuesfor each group are reported, and error bars indicate standard error.Corals were grouped into 3 classes based on the saturation of thewater in which they were observed: X \ 1 ( n = 31); 1 \ X \ 2.5( n = 72); or X [ 2.5 ( n = 172). No significant differences in sizewere observed in colonies of  Siderastrea radians ; however, coloniesof  Porites astreoides were significantly larger in supersaturated( X [ 2.5) water when compared to Porites astreoides colonies in lowsaturation and undersaturated water ( P = 0.05). Porites divericata colonies were omitted due to the rarity of their occurrence in bothundersaturated and supersaturated water. Although comparing coralcolony size for assemblages composed of different species iscomplicated by species-related morphology and growth rates, wealso report the average size of all species found in supersaturatedwaters to provide qualitative information regarding coral growthoutside of the springs. We note that the average size of all speciesfound in supersaturated waters was significantly larger ( P \ 0.03)than the average size of corals found where X \ 2.5. c Number of coral colonies per unit area as a function of saturation state. Resultsare normalized to per unit area (0.25 m 2 ) to account for differences inarea sampled between groups. The total (i.e., all species combined)number of coral colonies per unit area increased significantly withsaturation state ( P \ 0.0001, N  = 275)Coral Reefs  123  center of discharge and decreased with distance from thedischarge site. TA and DIC were correlated (  R 2 = 0.86)(ESM Fig. 4S). Dissolved nutrient (nitrate, ammonium,phosphate, and silica) concentrations ranged fromapproximately 2–10 times ambient (Derse et al.2008).Calcifying organisms such as corals, coralline algae, andcalcifying macroalgae were often present in undersaturatedor low saturation waters close to the ojos. Here, we focus oncalcifying corals, which were present where X arag \ 2.5 atall 10 ojos sampled. Only three scleractinian species( Porites astreoides , Porites divaricata , and Siderastrearadians ) and one hydrozoan ‘‘fire coral’’ (  Millepora alci-cornis ) were observed where X arag \ 2.5. All of thesespecies have aragonitic skeletons. Another six scleractiniancoral species (  Diploria , Montipora , Montastraea , Agaricia , Porites , and Favia ) were present near the ojos, but onlywhere the water saturation was above 2.5 ( X arag [ 2.5).These distributions may be evidence that certain calcifyingcoral species are more tolerant of low saturation waters thanother species, with potential implications for differentialsurvival under future CO 2 projections. A goodness-of-fitanalysis indicates that the number of species (i.e., speciesrichness) increased significantly as saturation valuesincreased with distance from the ojo centers ( P \ 0.0001;Fig.2).To determine whether saturation state affected the sizesof coral colonies living near the ojos, we compared colonysizes (measured as the plane area) of the three scleractinianspecies in undersaturated ( X arag \ 1) plus low saturation(1 \ X arag \ 2.5) waters with sizes of the same species atcontrol sites in supersaturated waters where X arag [ 2.5(close to, but outside the influence of discharge). The sizeof  Siderastrea radians colonies did not differ significantlybetween the saturation levels; however, Porites astreoides colonies in undersaturated and low saturation waters nearojos were significantly smaller than Porites astreoides colonies in supersaturated water (ANOVA, P = 0.05;Fig.2). We then compared the sizes of all colonies presentwhere X \ 2.5 to the sizes of all coral species found insupersaturated waters and found that the colonies in lesssaturated waters were also significantly smaller (ANOVA, P = 0.03; Fig.2). We note that this last comparison pro-vides only a qualitative analysis, as the comparison isacross species with different morphologies. Combined, ourdata suggest that as saturation levels approached maximumambient values, both the number of species present and theaverage size of individual colonies of  Porites astreoides increased significantly and that in general the coral colo-nies tend to be larger away from the ojo.When abundances (number of colonies) of  Poritesastreoides and Siderastrea radians in low saturation( X arag \ 2.5) and supersaturated ( X arag [ 2.5) waters werecompared, the densities (number of colonies per 0.25 cm 2 )of these individual species did not vary with saturationstate. However, for all species combined, the densities weresignificantly greater away from the ojos (goodness-of-fit; P \ 0.001; Fig.2). This is attributed to the increase inspecies number as supersaturation was reached. Discussion Ecological surveys at the ojo sites indicate that certainscleractinian coral species can grow in undersaturatedconditions. Thus, these species may be more tolerant of low-pH and low aragonite saturation conditions, and hencemore resistant than other species when exposed to chang-ing oceanic pH and carbonate saturation. However, thenumber of species that can survive at these low saturationconditions is limited compared with the species richness of the surrounding area. These findings are generally consis-tent with those of Fabricius et al. (2011) from CO 2 vents inPapua New Guinea, where the diversity and abundance of structurally complex corals was reduced threefold at lowpH, yet Porites corals were still found at pH below 7.7 andaragonite saturation of 2.9. At Puerto Morelos, the condi-tions are more extreme as the water is often undersaturatedor has much lower saturation values than 2.9, yet Poritesastreoides and Siderastrea radians corals are still abun-dant. Therefore, the Puerto Morelos site demonstrates thatcertain coral species may tolerate extreme acidificationevents and still maintain their ability to calcify. While wedid not measure calcification rates during this study, wenote that the ojos are part of a complex and elaborateunderground conduit system that has developed over mil-lennia in this karstic terrain. The seepage at these sites hastherefore been continuous for an extended period of timecompared with the average age of coral colonies. Thus, thecorals settled, calcified, and the colonies grew within theplume of low-pH groundwater discharge. This is differentthan the more ephemeral volcanic vent sites, and thereforethe ojos represent areas where the ecosystem had ampletime to adapt and evolve exposed to low-pH conditions.Although the coral species found at the ojo sites( S. radians , P. astreoides , and P. divaricata ) all occur onreef structures, they are rarely major contributors to theframework of the Meso-American Barrier Reef: thus, whiletheir presence is encouraging when considering the futureof these specific scleractinian species, there are severeimplications for the future of reef ecosystems and the manyorganisms that rely on structurally complex corals to buildthe reef framework. Specifically, our data suggest that asseawater saturation nears 2.5, today’s larger, dominant,framework-building corals of the Meso-American Reef (e.g., Acropora and Montastraea ), may be replaced bysmaller, patchily distributed colonies of only a few species. Coral Reefs  123
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