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∼ Climate Sciences Sciences Dynamics Chemistry of the Past Solid Earth Techniques Geoscientific Methods and and Physics and treatments (410, 770, Atmospheric Atmospheric Atmospheric ected by food level but Data Systems Geoscientific may respond to ocean Earth System Earth System Measurement ff 2 Instrumentation Hydrology and Ocean Science Annales Biogeosciences The Cryosphere Natural Hazards Natural Hazards CO and Earth System and Earth 35–45 %. Higher p by the oceans that decreases ∼ Model Development Geophysicae impacts on 2 , and A. Paytan 2 1 B. elegans CO ects of three p ff 7762 7761

Open Access Open Access Open Access Open Access Open Access Open Access Open Access Open AccessBalanophyllia elegans Open Access Open Access Open Access Open Access Open Access , T. Lambert

2 ) of seawater, is projected to have severe conse- Ω Climate spring. Planulation rates were a Sciences Sciences ff Dynamics Chemistry of the Past Solid Earth Techniques Geoscientific Methods and and Physics and Advances in Atmospheric Atmospheric Atmospheric , D. C. Potts Data Systems Geoscientific Geosciences Earth System Earth System Measurement 2 Instrumentation Hydrology and Ocean Science Biogeosciences is a solitary, azooxanthellate scleractinian species common on The Cryosphere Natural Hazards Natural Hazards EGU Journal Logos (RGB) EGU Journal Logos and Earth System and Earth planulation (larval release) rates, and on the survival, growth, and saturation state ( . Net calcification was positive even at 1230 µatm ( ), although the increase from 410 to 1230 µatm reduced overall cal- Model Development 2 3 2 CO CO 25–45 %, and reduced skeletal density by p , H. Cooper p ∼ 1 , while juvenile survival was highest under 410 µatm and High Food condi- 2 than CO p ects azooxanthellate coral calcification, and how ff This discussion paper is/has been under review for the journal Biogeosciences (BG). Please refer to the corresponding final paper in BG if available. University of California, Santa Cruz, Department of Earth andUniversity Planetary of Sciences, California, Santa Cruz, Department of Ecology and Evolutionary Biology, atmospheric cification by altered aragonite crystal morphologya significantly. We discuss howacidification feeding in frequency coastal upwelling waters. anophyllia elegans calcification of their juvenile o not tions. Our results suggestelegans that feeding rate has a greater impact on calcification of calcification over the nextacidification century. The are responses less of wellsynthetic azooxanthellate understood, corals energy to and from ocean becausefects symbionts, they of they cannot acidification provide obtainBalanophyllia on a extra elegans the photo- system energy forthe available studying California for coast the calcification. where direct iting The thrives an ef- orange in 8 the month cup low study,and coral pH we 1230 µatm) waters addressed and of the two an e feeding upwelling frequencies regime. (High Dur- Food and Low Food) on adult Ocean acidification, the assimilation of atmosphericthe CO pH and CaCO quences for calcifying organisms. Strongcorals evidence containing suggests algal that symbionts tropical (zooxanthellae) reef-building will experience dramatic declines in Abstract Biogeosciences Discuss., 10, 7761–7783, 2013 www.biogeosciences-discuss.net/10/7761/2013/ doi:10.5194/bgd-10-7761-2013 © Author(s) 2013. CC Attribution 3.0 License. Food availability and planulation, juvenile survival, and calcification of the azooxanthellate scleractinian coral, E. D. Crook 1 1156 High Street,2 Santa Cruz, CA 95064, USA 1156 High Street, Santa Cruz, CA 95064, USA Received: 30 March 2013 – Accepted: 19Correspondence April to: 2013 E. – D. Published: Crook 7 ([email protected]) MayPublished 2013 by Copernicus Publications on behalf of the European Geosciences Union. 5 15 20 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | 1, and < Ω and shoaling of the carbonate sat- formation) decrease (Fine and Tch- 2 3 rich, low pH water from intermediate CO 2 p 7764 7763 manipulation experiments (Form and Riebesell, 2012; 2 is a solitary, azooxanthellate scleractinian coral common in man et al., 2012). ff , a measure of ease of CaCO concentrations continue to rise over the next century, pH of the 2 arag Ω dissolves readily (Form and Riebesell, 2012; McCulloch et al., 2012). Because 3 Responses of calcifying corals to ocean acidification depend on species-specific en- Balanophyllia elegans despite acidification. Some research indicates that zooxanthellate coral calcification saturation state inpumping the raises calcifying the fluid. saturationent state (Al In Horani in zooxanthellate et the al.,that tropical calcifying 2003; deep-water Cohen corals, fluid azooxanthellate and corals by this Holcomb, canet 2009), up proton create al., and to even 2012). recent steeper 5–10 Lower evidence gradients saturation suggests timesmore (McCulloch states ambi- energy in the to external remove seawatertially excess require at corals protons the to (Ries, expend costbudget 2011; of would McCulloch other enable et critical corals al.,tion to life 2012), states vary processes poten- the of (Wood energy et the expended al., calcifying to 2008). fluids, raise A and the flexible perhaps pH energy enable and them satura- to maintain calcification ergy allocations for calcification.calcifying Corals compartments, the expend extracellular energy mediumthe to between the remove skeleton coral’s protons basal below from layerConnaughey, (Al and their 2003). Horani Removing et protons al., facilitates calcification 2003; by Allemand increasing et pH al., and 2004; Cohen and Mc- et al., 2008; Hauricalcification et and on al., the 2009). interplayimportant Understanding between calcification the in and impacts upwelling nutritional of status regionslower is ocean where thresholds critically acidification many for on organisms pHularly may tolerance vulnerable already (Barton to be et ocean livingnegative al., consequences acidification. at 2012) of their Several and future recentthe ocean therefore studies CA acidification may coastal have events upwelling be zone for described (Gaylord partic- several2012; et likely key al., Timmins-Schi 2011; species Barton in et al., 2012; Hettinger et al., depths to the surface, andsaturated coastal waters organisms for may several be monthsWith exposed of to anticipated the low increases year and (Feely in even eturation surface under- al., horizon, ocean 2008; calcifying Hauri organisms et livingence al., in seasonal 2009). increases these in coastal the waters magnitude, duration, are and likely extent to of low experi- pH waters (Feely strong seasonal upwelling which brings CO et al., 2009; Hauri et al., 2009). The western North American coastline experiences tion at or belowCaCO the carbonate saturationazooxanthellate horizon, corals the lack depth symbionts and belowcan rely which be solely used on to heterotrophy shedcalcification. for light energy, on they the role of nutrition and energetic resourcesshallow in coastal controlling waters around Montereyupwelling Bay, waters. California, Ocean where acidification it isupwelling often predicted regions thrives to where in have low especially saturation cool, waters severe occur impacts naturally in (Feely et al., 2008; Fabry saturation state of seawaterrates decreases, and they may changes face in similar2008; geographical Fabry declines distributions et in al., (Turley et 2009; calcification Maier al.,a et 2007; al., range 2009). Andersson of Some et widespread sensitivities cold-water al., Maier in species et have CO al., 2011), and some deep-water species can maintain positive net calcifica- crease in pHet from al., 8.1 2008; to Doneycalcification 7.8 et rates al., (Orr of 2009). many et tropical Both coraluration al., laboratory species state and 2005; decrease ( as field Hoegh-Guldberg the investigations pHernov, et suggest and 2007; that al., aragonite Anthony sat- 2007; et al.,tropical Fabry corals 2008; have Jokiel algal et symbionts al.,to (zooxanthellae) whose 2008; the photosynthesis Krief contributes host’s etzooxanthellae al., nutrition and 2010). and their A responses increases majority to of calcification ocean rates. acidification are Most poorly cold-water known, but corals as lack the As aqueous CO surface oceans will declineWicket, 2003, in 2005; a Sabine et process al.,ganisms, known 2004). including Growing as reef-building evidence ocean suggests scleractinian that corals, acidification calcifying will or- (Caldeira be and heavily impacted by a de- 1 Introduction 5 5 25 15 20 10 25 15 20 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | 2 ects CO ered ff ff p 7.8), and = T 8.0), 770 µatm = T (3 levels) and feed- 2 300 m depth along the in the seawater di CO ∼ p 2 CO p levels were based on present day at- Verrill, 1964 is a solitary (single polyp) 2 8.0) and two IPCC emissions scenarios = CO T p 7766 7765 during an 8 month incubation experiment. The and food availability on planulation rates of adult ects of the same treatments on survival, growth, 7.6). High Food corals were fed newly hatched ff 2 = T CO p B. elegans Balanophyllia elegans ects of ff ) nauplii larvae every 3 d to represent a plentiful food supply, while 7.6) (Solomon et al., 2007). Actual = T Artemia -enriched air, an outlet for excess air and a sampling port (a stoppered 2 is an azooxanthellate species (lacking photosynthetic symbiotic algae) that . We also explored the e 7.8), and 1230 µatm (pH = T Each experimental unit was a 4 L glass jar with an airtight screw cap containing an Temperature was maintained close to ocean ambient by placing the jars in a water We assessed the e fluorescent bulbs) with 12 h of darkness was maintained throughout the experiment. rubber valve) for takingquick pH access readings and to water thelid. samples. An water oscillating The in paddle sampling inserted the portcontinuous through jars a provided water double-layered without rubber movement having membrane by provided treatment, to mechanical with break 16–17 stirring. the juvenile There airtightjuveniles corals per were seal assigned treatment. 2 of randomly replicate to the each jars jar, per for atable with total running of seawater. 33 A daily light regime that alternated 12 h of light (overhead slightly from these(pH atmospheric targets, andbrineshrimp ( were 410 µatmLow Food (pH corals were fed once every 3 weeks, corresponding to ainlet minimal for food supply. CO 2.2 Experimental design The experiment used a fulling factorial frequency design with (2 two levels).mospheric factors: The concentrations seawater (380 ppm,projected pH for the yeara 2100, high the emissions A1B scenario(1200 “business ppm, (A1F1) as pH approximately usual” 3 (750 ppm, times pH current atmospheric into juvenile corals, usually withinB. a elegans few centimeters ofdepends the on mother heterotrophic feeding (Gerrodette, on 1981). zooplanktonof or its dissolved organic energy molecules and for nutrients. all It grows slowly and can survive for months without feeding. (planulation) the larvae crawl down the mother’s column and settle and metamorphose ternal and zygotes are brooded foruntil an average they of develop 15 into months mature in the planula mother’s larvae coelenteron (Fadlallah and Pearse, 1982). On release 2 Materials and methods 2.1 Organisms The orange cup coral species living on rockywest substrates coast of from North the America, from(has low southern separate intertidal Alaska sexes) to to species Baja California. with It a is sex a ratio gonochoric of approximately 1 : 1. Fertilization is in- long-term exposure more accurately predicts responsesexperiments to (Form acidification than and short-term Riebesell,spond 2012). to We lower ocean address pH, how andin the azooxanthellate low role corals of saturation re- nutrition upwelling level regimes. on their calcification and survival available for calcification. Becausesynthetic azooxanthellate energy corals from cannot symbionts, obtain theyof extra provide acidification photo- and a energy system availability for on studying calcification. the direct e B. elegans and calcification of juvenile duration was basedet on al. recommendations (2010) of for long-term Doney manipulation et experiments. al. Recent evidence (2009) suggests and that Widdicombe stances (Cohen and Holcomb, 2009).excess It nutrients, has some also been species shown cannear that, maintain under-saturation when 100 conditions provided % (Langdon with of andRies their Atkinson, et calcification 2005; al., rates Holcomb 2009; despite etlating Cohen al., increased et 2010, photosynthesis al., by 2009). zooxanthellae, This which may gives be the due coral to more the energy nutrient surplus stimu- is energetically costly and that a coral’s energy budget is fixed under normal circum- 5 5 25 15 20 10 25 15 20 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | magni- × 15 months B. elegans sys (Pierrot at 380, 750, ∼ 2 2 ) via CO 0.1 mm) and the volume arag + and feeding treatment af- Ω 2 CO p ). T 7.9–8.0) seawater during the peak plan- ∼ 7768 7767 ered with 0.1 M NaOH. As the juvenile corals are 0.01 mg) was determined on an analytical balance ff + bu 2 C oven for 48 h. All tissue was removed from skeletons in filtered seawater. The brineshrimp remained in the jars ◦ O 2 gas mixture flowing continuously into the headspace. -air mixtures were obtained from PraxAir (CO 2 2 . The jars and lids were then scrubbed and rinsed, and new 2 CO p CO p 5cm ceramic tiles (approximately 5 per tile), and immediately exposed × Artemia nauplii of 410 and 1230 µatm, excluding 770 µatm) were imaged with 10k 2 and stabilize pH before siphoning into the experimental jars. Jars were sealed CO 2 p , and then dried in a 50 × pH was measured daily in each jar with an Oakton WD-35613 hand-held meter, and Our first experiment aimed to determine whether Juveniles used in the second experiment came from a stock of adult Corals were fed through the sampling port in the jar lid using a 50 mL syringe with CO MACS facility at NASA/Ames. Thefor same measurements. region of The each length skeleton (the and septa) width was of used individual crystals were measured using in a 1 : 1roughly solution elliptic of cylinders 30 % inthe H shape, major linear and measurements minor of axes)of were height each taken and coral with diameter calculated. vernier Weight (both and calipers ( overall ( density of therandomly entire selected skeleton calculated skeletons by from dividingwith each weight of by volume. four Five treatmentsfication (High on a Food Hitachi and TM1000 Tabletop Low SEM scanning Food electron microscope at the UCSC et al., 2006). pH is reported in total2.4 scale (pH Skeletal growth At the end of40 the experiment, each living coral was imaged under a microscope at with the appropriate 40 mL water samples were taken(DIC) from each and jar total every 3 alkalinity dCarbon (TA) for analysis. dissolved Coulometer inorganic DIC (UIC, carbon andprocedure, Inc.) TA respectively. were and Certified measured an using ReferenceDickson automated, a Materials lab open-cell CM5011 (batch at potentiometric 118) UCwere titration used from San to the Diego calculate Andrew were aragonite saturation used state to and calibrate pH each ( instrument. DIC and TA Certified cylinders of CO and 1200 ppmV). Seawater wasbubbled with filtered the to appropriate 0.2 µmp gas and mixture collected in each in carboy 20 L for carboys, at and least 4 d to equilibrate 2.3 Seawater carbonate chemistry Survival was monitored by recording deaths as they occurred. placed in glass dishes in apolypropylene separate plastic tank sheets with pre-conditioned flowing with seawater, and aalgae allowed living (Fig. to biofilm 1). settle and After on crustose settlement, small coralline and pieces glued of to plastic, 5 each holding oneto larva, their were randomly cut assigned experimentalbegin treatments. for Since at skeletal least formation 2 doesto not weeks experimental conditions. after All settlement, juvenile thereand corals was started volumes, and no with initial calcification approximately skeletal equal before weightsment weights exposure of began in 0 g late (i.e. November no 2011 calcium and carbonate). ran for This approximately experi- 8 months until July 2012. experimental jars. maintained for severalplaced generations in in a the tankulation with laboratory. season flowing (October Approximately ambient to 85 adults December (pH 2011). were Emerging larvae were collected weekly, filtered, equilibrated seawater was siphoned into the jars to preventfected air planulation exchange. rates. Ten adult coralseach of treatment equal size (i.e. (sex 5 unknown)2011 were adults to assigned per January to jar) 2012). The forUCSC 60 the marine adults first had laboratory 3 previously for months been two held(Fadlallah of years in and, and the the because Pearse, experiment same they 1982), brood (October tank larvae atlarvae. all for the Every females 3 should d we have counted been numbers equally of likely larvae produced to and produce removed them from the concentrated for several hours to ensure thecleaned corals once had eaten every their 3 fill. dimately Every (after jar, 30 feeding lid, min and was and paddle finished). placed were their Corals in experimental were small removed glass for approx- dishes with filtered seawater equilibrated to 5 5 25 15 20 10 25 15 20 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | er ff 0.04) 0.37) 45 %) 0.06), = = ∼ = ects and p p 20 µatm), ff p 7.6). Tem- 0.29), but, ± erence was T = ff p 0.04, Fig. 3c), 0.01, and feeding fre- = = 2 p p 0.001) than the Low 0.04 (pH CO 0.01 (410 p ± ± 0.06). p < 0.62, Fig. 2a). = p = p 10 µatm). The saturation state ects on volume ( ± ff 0.001). In the High Food regime, 0.35, = 7.6 treatments ( 7.8), and 0.9 = p T T p 0.001) and Low Food ( = 0.005 (1230 0.1 (pH 7770 7769 p ± ± 7.6 corals ( T 8.0 corals weighed significantly more (by 0.008) and pH T 0.03, 0.34). ) of each treatment was 8.02 erence in density between the feeding treatments at T = = = ff and feeding frequency. Coral volumes and weights were 8.0), 1.3 ects. Where statistical significance is indicated, Tukey’s p p p ff 2 T below 8.0, skeletal density declined by approximately 35– T 0.04, Fig. 1b). In both the Low Food and High Food groups, CO 7.8 ( p = T 0.001) and heavier weights (4–5 times; 0.001) and pH p standard error of the mean (s.e.m.). ect on numbers of larvae released ( 12 µatm), and 7.59 0.05 (pH ff p < ± p < ± ± 7.8 ( 0.11). At pH T and feeding frequency as fixed factors. For planulation, an additive model planulae were collected as they emerged from adults and the total number = 25 %) and not statistically significant ( 1.5) over the duration of the experiment. For a full data report, including had no e 2 p ± ∼ 2 0.006 (770 CO ) of each group, calculated from measurements of DIC and TA from discrete water C( CO p 0.01, Fig. 2b); mortality in the pH 7.8 treatment was intermediate, but did not di ◦ ± 8.0 ( 8.0 corals also weighed more than the lower pH treatments, but the di p T T = arag The Low Food corals were approximately 35–40 % more dense than the High Food Approximately 5–15 % more juvenile corals survived in the High Food than in the p Ω 45 % in both thetreatments. High Food ( for the Low Foodthan regime, the the pH pH pH smaller ( corals for both thebut there pH was nopH significant di 3.3 Impacts on growth calcification, density,Juvenile and crystal coral structure skeletons fromumes the (6–7 High times; Food treatmentsFood had treatments (Fig. significantly 3a, greater b). vol- pH had no significant e per treatment were counted and compared.more Adult planulae in corals the released High approximately 120 Foodbut % treatments than in the Low Food treatments ( Low Food treatment ( 10–15 % more juveniles( died in thesignificantly pH from the 7.6 control ( treatment than in the control treatment a summary of water chemistry, see Supplement. 3.2 Planulation and juvenile survival B. elegans 13.6 perature in the jars varied with the temperature of the external seawater, but averaged 3 Results 3.1 Water chemistry The average pH (total scale,7.78 pH ( samples, was 2.1 HSD tests were used togistic regression compare against treatments. the Juvenile two survivalquency. categorical was The predictor assessed variables, interaction by term aand was lo- was not significant therefore (Tukey’spressed excluded test as for from mean additivity; the logistic regression model. All results are ex- volume, weight, density andwith crystal structure werewas analyzed applied using because interaction 2-factor termstreatment. ANOVAs All could other not ANOVAs be used athe assessed interaction full with between model a to single investigatelog-transformed count both the per to main satisfy e normalityindividual assumptions. corals For from crystal whichnested structure within crystals analyses, the were the two sampled main e were treated as random factors from the SEM images. 2.5 Statistics The software R was used for all statistical analyses (R Core Team 2013). Planulation, Imaging Processing and Analysis in Java (Image J, US National Institute of Health) 5 5 20 25 15 10 20 15 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | 2 7.6 T erent B. el- ff 0.93) or . In this 1 = − had no ef- p 2 CO . Because p level (1230 µatm, 1 level, the trend to − ects on final length 2 2 ected by increased 8.0 than at pH ff ff yr T 2 CO CO − are small compared to er with pH ( p p ff treatments, their skeletal 2 2 CO p CO increases beyond the projected p 2 18 %) at pH level. Although corals within a food ∼ CO 2 p , either the shapes of skeletal elements had no significant e 2 CO 2 p 15 % longer in the High Food than the Low suggests that the structural integrity of the CO 2 ∼ CO p 7772 7771 p ; CO p negatively impacts such processes as gametogenesis, ects of stressors experienced during larval stages can 2 ff B. elegans treatments (410 and 770 µatm). Within the 1230 µatm CO ect numbers of planulae released, subsequent survival of CO 2 ff p 7.6, crystals were CO T p erences in bulk density due to high 0.41, Fig. 4b). ff = did not a p 2 0.001, Fig. 4a). Crystal width did not significantly di CO p is a solitary species, its radial expansion must be considered in the calculation p < 7.6) where average survival was about 10 % lower (across both food levels) , a trend that is consistent with more energy being available for, allocation to and skele- well-fed corals had heavier skeletons within each . This suggests that with increasing 2 2 2 0.001), and at pH = T However, the di Calcification rates in reef-building corals are commonly measured as the annual lin- In the juvenile incubation experiment, food availability was the major factor controlling While Aragonite crystals were significantly longer (by CO CO CO p < the High Food corals. While the Low Food corals did not grow as quickly or weigh study, higher food ledp to both greater extensiontal and formation. greater Although calcification the withinp linear every dimensions ofless corals dense were skeletons una with increasing skeleton may decline and leave thedislodgement coral (Hoegh-Guldberg more et vulnerable to al., predation, 2007). bioerosion, and those between the feeding levels, with the Low Food corals actually being denser than ear extension multiplied byegans the density, and expressedof in calcification gcm rates. Therefore,tal we skeletal expressed weight calcification measured as over the known change intervals in and the normalized to- to gyr or volume. At the end ofvolumes the than experiment, the the High Low Food Foodlevel corals corals had had up at similar to every sizes 7weights, times (length greater and and hence volume) across bulkp densities, all declined significantly fromchanged, 410 or µatm there to was 1230mechanism µatm less secondary is thickening that of energyskeletal the extension, available initial at for the skeleton. cost calcification One of possible is a less allocated heavily first calcified skeleton. to ensuring full ment. This pattern suggests that,750 if ppm atmospheric over the next century,decline, the even numbers if of food corals is surviving plentiful. to the adult stage might the growth (and final size) of treatments, survival was up to 15 % higher in the High Food than the Low Food treat- pH than in the other two longed exposure to high fertilization, cleavage or early larvalisms development (Kurihara, that 2008; Kroeker have et beenthat al., seen prolonged 2010, in exposure 2013; to other low Nakamura organ- pH ettion, may al., divert but 2011). energetic this It resources experiment away is from provideslow possible reproduc- pH no or information low about food possible on impacts adult of nutrition or prolonged reproduction. the juvenile corals was substantially reduced at the highest released by 50–200 %.feeding This conditions suggests are optimal, that either females formany completing may months maturation delay of earlier, the or release larvae forfect of conceived sustaining on larvae either the until the larvae timing afterbefore or release release. means numbers High that of this larvae experiment released, provides but no the information 15 about months whether of pro- brooding 4 Discussion Responses of calcifying organismsstages to of ocean acidification their are lifejuvenile) likely cycles, stages to and of vary several many at studies marineacidification di provide (Kroeker taxa evidence et in that al., upwelling early 2010,also regions 2013; (larval are showed Hettinger and particularly that et sensitive al., adverse“carry-over” to 2012). to e the Hettinger next et life al. stageIn and (2012) be the compounded present by study, the high time food adulthood levels is increased reached. the numbers of brooded planula larvae ( Food ( feeding group ( 5 5 25 20 10 15 25 15 20 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | 2 17 CO ∼ ), the p 2 CO are able to p cient grazers ffi . At 1230 µatm, High 2 . This is consistent with cf CO and other e Ω p and other calcifying organisms Balanophyllia elegans deposited will decline even as ex- cient to maintain positive growth at 0.89) (1) 3 ffi ± B. elegans may be able to compensate for the extra B. elegans 0.20 ( + 7774 7773 ) in a coral’s calcifying compartment (Cohen and cf Ω B. elegans significantly reduced crystal length, with crystals being 2 conditions to calcify at rates similar to those of corals at CO indicate that these corals may not be able to expel enough 2 cf p > Ω CO , the total amount of CaCO 2 crystal aspect ratio p × CO p was lower than in corals grown at ambient , even when provided with plentiful high energy food. cf 2 0.06) may be negatively impacted due to lower food concentrations. However, Ω ± , albeit very slowly. We suggest that removing protons to increase the pH 21 and 20 for High and Low Food 410 µatm corals, respectively, and CO 2 ∼ p CO 0.93 ( p was = Our observation that heterotrophic feeding rate has a greater impact on calcifica- Combined, these lines of evidence suggest that The aspect ratio (length divided by width) of aragonite crystals in coral skeletons has cf cf Chavez, 2000). This nutrient surpluston) drives production, phytoplankton and (and is subsequentcorals. therefore zooplank- likely In to fact, increase zooplanktontimes the concentrations the amount during concentration of upwelling during foodplanulation months non-upwelling available to occurs months, can the and (Marinovic be often et upis peak al., to at in 2002). its 10 the Thus, lowest, fall along foodfeed when the availability at is California higher at coast rates. its This when highestB. may pH and suggest elegans that the if corals acidification mayif is naturally food decoupled be availability from able upwelling, to remains high, tion than pH mayendemic explain to the upwelling success coastalthe waters, of pH despite is low atIndeed, saturation. its nutrient During lowest, concentrations upwelling, nutrient during when the andnutrient upwelling plankton concentration months concentrations during can are non-upwelling be periods up also to in at 20 Monterey their times Bay highest. the (Pennington and high and saturation state of theas calcifying compartment energetic may demands be energetically forwith costly maintaining and increasing that the saturationtension state rates are of maintained. the Thiswas calcifying decrease observed fluid in regardless calcification rise of at feedingnot moderate amount, entirely to overcome suggesting high the that stress even of well-fed acidification. corals can maintain moderate rates of calcificationvided even they during have extreme an acidification adequatethat events, nutritional do pro- supply. not dependincrease their on energy zooxanthellae reserves may (providedeven prey be feeding is once able available). every As to seen three increase in weeks our was their experiment, still feeding su rates to protons under high ambient Ω and 16 for High1230 and µatm, Low Food 1230Food µatm significantly increased corals crystal (Fig. length by 4c).resulting about in Even 15 % a in over slight those well-fed increase inthe corals in Low both Food calcification at corals crystal results aspect and ratiocounteract and may some of indicate the that negative impactslength excess of and food low saturation calculated enables state. corals The changes to in partially crystal Ω In our experiment, high approximately 18 % longer in thewidth 410 µatm did than the not 1230 µatm varycrystal corals. aspect between While the ratio any crystal was of higher the for the treatments ambient (feeding corals. frequency Using Eq. or (1) we calculate that ing compartment (Cohen andcrystals Holcomb, are 2009; associated Holcomb with etindicative high al., of saturation low 2009). states saturation Longer, states while thinner comb (Cohen shorter, (2009) and broader used McConnaughey, abiogenic 2003). crystals aragonites Cohen are precipitatedstates and in to Hol- seawater derive with a known saturation formularation in state which of crystal the aspect calcifyingHolcomb, 2009): ratio fluid linearly ( approximates the satu- be analogous todominates that when of conditions are certainformed favorable, while during reef-building slower less corals growing, favorable conditions denser in (Highsmith, skeletons 1979). which are rapidbeen linear used extension as an indirect proxy for saturation state of the seawater in a coral’s calcify- as much as the High Food corals, their bulk density was higher. This response may 5 5 25 15 20 10 25 15 20 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | , , exposure 2 B. elegans Galaxea fascicularis , Mar. Biol., 71, 223–231, ects, Limnol. Oceanogr., 57, 698–710, ` eque, F., Puverel, S., Reynaud, S., Tam- , 2009. ff Balanophyllia elegans 7776 7775 , Glob. Change Biol., 18, 843–853, 2012. . . 2 , 2012. 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P.: Seasonal fluctuations of temperature, salinity, nitrate, 5 25 20 15 10 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | and feeding T after 8 months s.e.m displayed. ± by pH B (b) Low Food High Food A High Food Low Food B. elegans B C A 380 High Food 380 Low Food 750 High Food 750 Low Food 1200 High Food 1200 Low Food 380 Low Food 750 Low Food 380 High Food 750 High Food 1200 High Food 1200 Low Food 380 High Food 380 Low Food 750 High Food 750 Low Food 1200 High Food 1200 Low Food 8.1 8.1 8.1 8.0 8.0 8 of juvenile 8 8 (c) 7.9 7.9 7.9 pH 7.8 7.8 7.8 pH pH 7.8 7.8 7782 7781 pH pH 7.7 and percent juvenile survival 7.7 7.7 (a) 7.6 , and bulk density 7.6 7.6 7.6 7.6 (b) 7.5 7.5 7.5 0 0

60 50 40 30 20 10 90 80 70

100

) Volume (mm 0.001

3 0.0016 0.0012 0.0006 0.0002 0.0014 0.0008 0.0004

) Density (g/mm

2.00E-02 1.00E-02 3 6.00E-02 5.00E-02 4.00E-02 3.00E-02

0.00E+00

5 0

0.0 Dry Weight (g) 30 25 20 15 10

Number of larvae issued by adults 90.0 80.0 70.0 60.0 50.0 40.0 30.0 20.0 10.0

100.0 Percent juvenile survival , dry weight (a) Planulation rates of adults Volume exposure to experimental conditions (33every 3 juveniles/treatment). days High while Food Low corals Food corals were were fed fed once once every three weeks. Mean Fig. 3. frequency. Planulation rates werein determined experimental by conditions placing for 10cent three adults/treatment juvenile months, survival (60 and was total determined larvaecorals). adults) by were counting counted deaths as as they they emerged. occurred (198 Per- initial juvenile Fig. 2. Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | s.d.). ± , obtained from scan- (b) ) using Eq. (1) (mean cf Ω B C A 380_High Food 1200_High Food 1200_Low Food 380_Low Food 1200_High Food 1200_High Food 380_High Food 380_Low Food 1200_Low Food 380_High Food 380_Low Food 1200_Low Food 25 8.1 8.1 8 8 20 7.9 7.9 15 pH 7.8 7783 pH 7.8 calcifying fluid Ω 10 7.7 7.7 5 , and aragonite crystal width 7.6 7.6 (a) 7.5 0 7.5 2 3 5 0

35 30 25 20 15 10

2.6 2.2 3.2 2.8 2.4

0.13 0.12 0.15 0.14 Crystal Aspect Rao

Aragonite Crystal Length (µm) 0.145 0.135 0.125 0.155 Aragonite Crystal Width (µm) , the crystal aspect ratio (aragonite crystal length divided by the width) (c) s.e.m.). In Aragonite crystal length ± was used to calculate the saturation state in the calcifying fluid ( Fig. 4. ning electron microscope(mean (SEM) images taken from a subset of 20 juvenile coral samples