Shifts in coral reef biogeochemistry and resultingacidification linked to offshore productivityKiley L. Yeakela, Andreas J. Anderssona,b,1, Nicholas R. Batesb,c, Timothy J. Noyesb, Andrew Collinsb, and Rebecca Garleyb

aScripps Institution of Oceanography, University of California, San Diego, La Jolla CA 92093-0244; bBermuda Institute of Ocean Sciences, St. George’s GE01,Bermuda; and cDepartment of Ocean and Earth Sciences, National Oceanography Center, University of Southampton, Southampton SO14 3ZH, United Kingdom

Edited by Paul G. Falkowski, Rutgers, The State University of New Jersey, New Brunswick, NJ, and approved October 1, 2015 (received for review April 9, 2015)

Oceanic uptake of anthropogenic carbon dioxide (CO2) has acidi-fied open-ocean surface waters by 0.1 pH units since preindustrialtimes. Despite unequivocal evidence of ocean acidification (OA) viaopen-ocean measurements for the past several decades, it has yet tobe documented in near-shore and coral reef environments. A lack oflong-term measurements from these environments restricts our un-derstanding of the natural variability and controls of seawaterCO2-carbonate chemistry and biogeochemistry, which is essential tomake accurate predictions on the effects of future OA on coral reefs.Here, in a 5-y study of the Bermuda coral reef, we show evidencethat variations in reef biogeochemical processes drive interannualchanges in seawater pH and Ωaragonite that are partly controlled byoffshore processes. Rapid acidification events driven by shifts to-ward increasing net calcification and net heterotrophy were ob-served during the summers of 2010 and 2011, with the frequencyand extent of such events corresponding to increased offshore pro-ductivity. These events also coincided with a negative winter NorthAtlantic Oscillation (NAO) index, which historically has been associ-ated with extensive offshore mixing and greater primary productiv-ity at the Bermuda Atlantic Time-series Study (BATS) site. Our resultsreveal that coral reefs undergo natural interannual events of rapidacidification due to shifts in reef biogeochemical processes that maybe linked to offshore productivity and ultimately controlled bylarger-scale climatic and oceanographic processes.

coral reef | ocean acidification | biogeochemistry | NAO | calcification

Ocean acidification (OA) resulting from rising atmosphericCO2 (1–3) and the associated declines in surface seawater

pH and saturation state with respect to CaCO3 minerals such asaragonite (Ωaragonite = [Ca2+][CO3

2-]/Ksp*, where Ksp* is the ionsolubility product) have raised concerns on the potential conse-quences to marine calcifiers and ecosystems (4, 5). Reductions inΩaragonite have been found to negatively affect organismal CaCO3production (6) while accelerating bioerosion and CaCO3 disso-lution (7, 8). Hence, it has been hypothesized that coral reefscould shift from a condition of net calcification to net dissolu-tion, with some model estimates predicting a transition forworldwide reefs at atmospheric CO2 levels of 560 ppm (5, 7).Despite growing concern about the vulnerability of coral reefs,

a lack of long-term measurements has prevented direct obser-vation of anthropogenic OA owing to increasing atmosphericCO2 in these environments. Additionally, short-term observa-tions have revealed large variability and modification of reefseawater CO2-carbonate chemistry on diurnal and seasonaltimescales as a result of coral reef biogeochemical processes suchas photosynthesis, respiration, calcification, and CaCO3 disso-lution (9, 10). It has been hypothesized that these natural pro-cesses, quantified as net ecosystem production (NEP = grossprimary production − autotrophic and heterotrophic respiration)and net ecosystem calcification (NEC = gross calcification −gross CaCO3 dissolution), could modulate local seawater chem-istry such that the rate of acidification on coral reefs is signifi-cantly different from the open ocean (11). Consequently,the anthropogenic OA signal could be either alleviated or ex-acerbated by reef biogeochemical processes (10–12). Centuries-long records of reef pH derived from 11B of coral cores reveal

large variability in pH over decadal timescales (13), possibly in-dicative of the dynamic nature of reef biogeochemical processes.However, these records of pH alone (which are nonethelessinferred rather than directly measured) cannot explicitly revealthe drivers behind the observed variations in seawater pH. Long-term measurements of reef (and offshore) biogeochemistry aretherefore necessary to understand the natural variation andcontrols (whether they be biological, physical oceanographic, orclimatic) on reef CO2-carbonate chemistry, and how this willchange under future OA and climate change scenarios.We have measured and characterized the seawater CO2-car-

bonate chemistry across the Bermuda coral reef platform monthlybetween June 2007 and May 2012 to investigate temporal andspatial variability in seawater pCO2, pH, and Ωaragonite. Theseparameters were calculated based on surface seawater measure-ments of temperature, salinity, total dissolved inorganic carbon(DIC =[CO2]+[HCO3

−]+[CO32-]), and total alkalinity [TA =

excess of bases over acids relative to a reference state (14)] at fourdiscrete locations on a transect traversing the coral reef platform(Fig. S1). Given the large variability in reef CO2 system param-eters on seasonal timescales, a 5-y record is too short to detect thesecular trend of anthropogenic OA. However, contemporaneousmonthly measurements from the nearby Bermuda Atlantic Time-series Study (BATS) station, located ∼80 km southeast of Ber-muda in the open ocean of the North Atlantic subtropical gyre(Fig. S1), allow us to decipher variations in the offshore sourcewater chemistry from changes occurring on the coral reef owingto local biogeochemical processes.Relative changes in DIC and TA reflect the biogeochemical

partitioning of carbon between the inorganic and organic carboncycles on the reef (15, 16) and the balance of NEP, NEC, andair–sea CO2 gas exchange. NEC changes DIC and TA in a ratio

Significance

Ocean acidification is hypothesized to have a negative impact oncoral reef ecosystems, but to understand future potential im-pacts it is necessary to understand the natural variability andcontrols of coral reef biogeochemistry. Here we present a 5-ystudy from the Bermuda coral reef platform that demonstrateshow rapid interannual acidification events on the local reef scaleare driven by shifts in reef biogeochemical processes towardincreasing net calcification and net respiration. These bio-geochemical shifts are possibly linked to offshore productivitythat ultimately may be controlled by large-scale climatologicaland oceanographic processes.

Author contributions: A.J.A. and N.R.B. designed research; K.L.Y., A.J.A., T.J.N., A.C.,and R.G. performed research; K.L.Y. and A.J.A. analyzed data; and K.L.Y., A.J.A., andN.R.B. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

Data deposition: The inshore reef data reported in this paper have been deposited in theBiological and Chemical Oceanography Data Management Office (BCO-DMO) under projectBEACON, www.bco-dmo.org/project/2190.1To whom correspondence should be addressed. Email: aandersson@ucsd.edu.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1507021112/-/DCSupplemental.

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of 1:2, with net calcification (NEC > 0) acting to draw down DICand TA, causing a decrease in seawater pH and Ωaragonite. NEPmainly alters DIC, with net organic carbon production (NEP >0) reducing DIC concentrations as CO2 is used and increasingpH and Ωaragonite. Air–sea CO2 gas exchange affects DIC only,but typically exerts minor influence on DIC relative to NEC andNEP in reef environments with residence times of a few days,such as Bermuda (17, 18). Consequently, comparison of salinitynormalized changes in seawater DIC and TA (nDIC and nTA)between the reef and offshore can be used to evaluate the rel-ative contribution and variability in reef NEC and NEP over timeand space. Deviations between reef and BATS nTA concentra-tions reveal the relative extent of reef NEC, whereas deviationsin nDIC corrected for the influences of NEC and air–sea CO2gas exchange reveal the relative extent of reef NEP. In thepresent study, we used these relationships to evaluate the influ-ence of biogeochemical processes on reef seawater carbonatechemistry and the relative attribution of NEC and NEP tochanges in reef pH and Ωaragonite (see Materials and Methods forfurther details).

Results and DiscussionLong-Term OA Signal Offshore. Observations since 1983 at BATSand Hydrostation S (another long-term time series near Ber-muda) reveal a rise in surface seawater nDIC by ∼1.20 ±0.09 μmol kg−1·y−1 (2), driven by the oceanic uptake of anthropo-genic CO2 (Fig. 1). Consequently, surface seawater offshore Ber-muda has become less alkaline, with temperature- and salinity-normalized pH and Ωaragonite dropping by −0.05 and −0.25 units,respectively, since 1983 (2). (Note that temperature- and salinity-normalized data are referred to throughout this discussion.) In-creasing nDIC has driven most of these changes whereas nTA hasremained relatively constant. Superimposed on the steady rise innDIC over time, a seasonal oscillation driving large-amplitudeswings in pH and Ωaragonite is apparent. This reveals the influenceof physical, biological, and climatic processes on surface oceancarbon dynamics, with the predominant driver being seasonalphytoplankton blooms as observed in the average annual cycle (i.e.,climatology, Fig. 2).

Near-Shore Biogeochemical Processes Dictate Reef Acidification.Over the 5-y study period between 2007 and 2012, no apparenttrends in seawater CO2-carbonate chemistry parameters result-ing from rising atmospheric CO2 are observed on the coral reefplatform (Fig. 2). However, large depletions in nTA and nDIC,relative to BATS, are observed each year with the extent of thedrawdown variable on the interannual timescale. Offshore vari-ability of seawater carbonate chemistry at BATS is representa-tive of conditions in the subtropical gyre of the North AtlanticOcean surrounding Bermuda and provides a direct comparison

with onshore variability on the Bermuda reef. Despite thesedepletions in reef nTA and nDIC, reef pH and Ωaragonite remaincomparatively constant while offshore a predictable seasonalpattern of acidification persists throughout the 5-y study (Fig. 2).Occasionally, rapid acidification events are observed on the

reef platform, particularly in August 2010, when the largest dif-ference in pH between the reef and BATS (ΔpHREEF−BATS =−0.14, Fig. 3) was observed. The climatology of the reef pH andΩaragonite shows that the range of variability is greater and av-erage values are slightly lower during the summer compared withthe rest of the year, coinciding with the drawdown and maximumvariability in nTA and nDIC (Fig. 2 E–H).The observed drawdown in reef nTA is mainly caused by reef

NEC, with modifications in nDIC driven both by reef NEC and

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Fig. 2. Reef and BATS seawater carbonate chemistry observations, 2007–2012. (A–D) Time series of seawater nTA, nDIC, pH, and Ωaragonite observedat BATS (blue) and across the reef platform (orange) from 2007 to 2012.Reef data are shown as individual markers per site with average of foursites shown as a line with ±1SD shaded; (E–H) Climatology of same sea-water CO2 parameters with ±1SD shaded. Rapid acidification events areevident in the short-term observations on the reef (A–D), particularly inthe summer of 2010. The climatology reveals summertime drawdown inreef nTA and nDIC, whereas reef pH and Ωaragonite remain relatively con-stant year-round. pH and Ωaragonite have been temperature- and salinity-normalized to values of 23.1 °C and 36.6 g kg−1, respectively, for bothBATS and reef data.

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NEP (the influences of air–sea gas exchange of CO2 are minimal,Fig. 3). Consequently, seasonal changes in NEC and NEP areultimately driving the observed pH and Ωaragonite variability onthe reef, with increasing NEC causing acidification and in-creasing NEP having the opposite effect. Summertime increasesin NEC produce a reoccurring reduction in seawater pH, withthe strength of NEC corresponding to the extent of pH reduction(Fig. 3). In contrast, NEP fluctuates with no discernible seasonalcycle. When increases in NEC correspond with decreases inNEP, as they did during the summer of 2010, we observe themost extensive reduction in reef seawater pH and Ωaragonite(Fig. 3).

Reef Biogeochemistry Responds to Offshore Forcing. Our resultsreveal that seasonal and interannual changes in NEC and NEPare responsible for the observed changes in temperature- andsalinity-normalized pH and Ωaragonite, but what is the driver ofthese changes? Pronounced acidification events, such as duringthe summer of 2010, occurred during periods of anomalouslyhigh NEC and low NEP, indicating shifts in reef biogeochemicalprocesses toward increased calcification and heterotrophy.Generally, calcification is thought of as an autotrophy-enhancedprocess with photosynthetic drawdown of seawater CO2 con-centrations elevating Ωaragonite and providing conditions favor-able for organismal CaCO3 deposition (19). In contrast, respirationreleases CO2, reduces Ωaragonite, and therefore is thought todecrease calcification. Thus, our finding of enhanced calcifica-tion during periods of increased heterotrophy runs counterto some modeling and field-based studies (10, 19). However,numerous experiments have shown that if corals, the dominantreef calcifiers, are well fed (such as by zooplankton) or have

nutritionally replete diets, they will have greater rates of bothtissue and skeletal growth (20–24). Some results have evendemonstrated that corals may be able to counteract reducedrates of calcification resulting from OA by increasing feedingrates (23). Furthermore, increased heterotrophy and elevatedtissue growth in corals have been found to cause overall res-piration rates to increase (21). Therefore, we speculate thatexternal pulses of nutrition to the reef could have enabled boththe anomalously high summertime calcification and shifts toincreasing heterotrophy responsible for the observed acidifi-cation events.Measurements at BATS indicate that phytoplankton blooms

were enhanced during our study period, particularly in thewinter and spring of 2010 and to a lesser degree 2011 (Fig. 3).Whereas the Sargasso Sea surrounding Bermuda is typicallyoligotrophic, enhanced spring phytoplankton blooms havepreviously been documented and are hypothesized to belinked to the North Atlantic Oscillation (NAO) (25, 26),a climate mode describing differences in pressure betweenthe atmospheric subtropical high-pressure system near theAzores and the subpolar low-pressure system near Iceland(27). A negative winter NAO state infers a southern shift inthe Gulf Stream and winter storm track, causing deepermixed layers in the Sargasso Sea due to enhanced winds (25,27). With deeper mixed layers come lower sea surface tem-peratures and greater entrainment of nutrients, resulting inproductivity blooms and increased mesozooplankton abun-dance (25, 26, 28–30).Since measurements began at BATS, the winter NAO state has

been primarily positive, with sporadic neutral to slightly negativeevents causing documented increases in offshore productivity

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Fig. 3. Influence of NAO and offshore primaryproductivity on reef carbonate chemistry dynamics.Time series of (A) NAO [monthly in gray and winter(December–March), mean in black]; (B) wind speed(green) and mixed-layer depth (MLD) (black); (C)primary production (PP); nTA (D) and nDIC (E) atBATS (squares) and across the reef platform (circles);(F) NEC (blue), NEP (red), and air–sea CO2 gas ex-change (green); and (G) the contributions of NEC,NEP, and air–sea gas exchange to pH differencesbetween BATS and the reef (ΔpHREEF– BATS). Nega-tive NAO winter events enhance storm activity insubtropical waters surrounding Bermuda, deepeningtheMLD, which brings colder, relatively nutrient-richwaters to the surface and results in increased PP.During 2010 and 2011, deep winter MLD coincidedwith intensified spring blooms and enhanced latesummer/fall NEC, causing greater drawdown of nTAacross the reef and consequently driving acidifica-tion. In contrast, a positive winter (December–March)NAO state and consequently weaker PP signal in 2008resulted in a subdued reef NEC signal the followingsummer.

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(25, 26). However, the winter 2010 event (and to a lesser de-gree 2011) was anomalously negative (Fig. 3), and coincidentwith an abnormally large spring bloom. At the onset of the2010 event, a strongly negative shift in reef NEP (i.e., netrespiration) coincided with a deep mixed-layer depth (MLD)and consequent upwelling of nutrients [as indicated by anom-alously low sea-surface temperature (SST) and high nDICwaters at BATS, Figs. S2–S4] (25). Reef nTA values that wereelevated above those at BATS indicate that the shift in NEPcoincided with platform-wide net CaCO3 dissolution (Fig. 3).Whereas increased offshore primary productivity occurred inthe winter to spring season of 2010 and 2011, the followinglate summer and fall, relative measurements of reef NEC, asinferred by alkalinity anomalies, reached their highest valuesover the 5-y measurement period, signifying intensified com-munity calcification (max. NEC 2007: 39.8 μmol kg−1; 2008:30.9 μmol kg−1; 2009: 42.2 μmol kg−1; 2010: 50.5 μmol kg−1; 2011:50.0 μmol kg−1, Fig. 3), and coincided with negative NEP values.Noticeably, the following winters in 2011 and 2012 also had NECrates higher compared with previous years (Fig. 3). Cross-corre-lation analysis revealed the potential time dependence betweenoffshore and reef processes, with maximum correlation betweenoffshore primary productivity and MLD observed when pro-ductivity lagged MLD by 0 to 1 mo (r > 0.8, Fig. 4). In contrast,reef biogeochemical processes lagged offshore productivity byseveral months. Reef NEC showed the strongest correlation withoffshore productivity at a lag of 4 mo (r = 0.77), whereas negativeNEP (i.e., heterotrophy) was most strongly correlated at a lag of6 mo (r = −0.45, Fig. 4). These correlations were statistically sig-nificant at the 99.5% confidence level.Given the experimental evidence linking increased hetero-

trophy to higher calcification rates in corals (20–24) and thestatistical significance of our cross-correlation analysis, we hy-pothesize that lateral advection of offshore blooms as well asnutrient upwelling, both of which were exacerbated during thewinters of 2010 and 2011, possibly due to the NAO state, pro-vided external pulses of nutrition to the reef. These pulses ofnutrition enabled short-term shifts in reef NEC and NEP towardincreasing calcification and heterotrophy, respectively, and it wasthese biogeochemical shifts that ultimately caused the observed

changes in seawater pH and Ωaragonite (Fig. 5). Additional evi-dence in support of this hypothesis is provided by coral coresfrom Bermuda that exhibit thicker layers of CaCO3 deposition,and therefore greater rates of calcification, corresponding toyears of negative SST anomalies (indicative of deeper MLD) (31,32), negative winter NAO events (33), and presumably higheroffshore productivity (25, 26).However, without direct measurements of phytoplankton

and zooplankton quantities on the reef, nor biogeochemicalmeasurements extending directly off the platform, our hy-pothesis linking reef biogeochemistry to offshore productivityrelies on the assumption that BATS is representative of watersadvecting onto the reef and that reef water residence timeremained relatively unchanged (17). Additionally, discrep-ancies within our time series indicate that year-to-year subtletiesin climatic and oceanographic processes may have cascadingeffects, with slight changes in offshore upwelling and phyto-plankton blooms having subsequently large effects on reef bio-geochemical processes and carbonate chemistry. For instance,unlike the 2010 event, the 2011 bloom in offshore primaryproduction and summertime increase in NEC correspondedwith a much smaller shift to heterotrophy; although summeracidification once again occurred, it was not as pronounced anevent as 2010 (Fig. 3). It remains unclear why such differencesin reef biogeochemistry were observed during years of relativelysimilar offshore productivity blooms, although it is possiblethey relate to variations in the timing, magnitude, and taxo-nomic composition (34) of the bloom (26), which are related tothe strength of stratification, mixing, and the nutrient reservoirwithin the North Atlantic subtropical mode water (35). Forinstance, the 2010 spring bloom was noted for a shift from cya-nobacteria in the preceding years to pico/nanoeukaryotic algae(34), having potentially cascading effects on higher trophic levelssuch as zooplankton (30), and ultimately affecting reef biogeo-chemical processes.Similar to our observations from the Bermuda coral reef

platform, coral coring studies from other locations have revealedthat reef pH varies greatly on annual to decadal timescales, al-though the oceanographic and climatic mechanisms driving suchvariations may be site-specific (13). Using 11B as a proxy forseawater pH, coral cores from Flinder’s Reef in the Great Bar-rier Reef revealed large interdecadal variations in reef pH of upto 0.3 units over the past few centuries, which ref. 13 postulatedwere driven by changes in reef residence time and ultimately theInterdecadal Pacific Oscillation. However, those authors did notaddress whether the observed changes in pH could result fromchanges in reef biogeochemical processes. In the present study,contemporaneous measurements of residence time on the Ber-muda coral reef platform (17) lead to the conclusion thatchanges in residence time or other physical oceanographic pa-rameters on the reef platform were likely small or nonexistent,and could not explain the observed variations in seawater car-bonate chemistry. In contrast with the study by ref. 13, directmeasurement of seawater carbonate chemistry rather than in-ference through paleoproxies allows for quantification of reefbiogeochemical processes, and their contribution to acidifica-tion. Whereas coral cores provide us with a longer perspective onOA, as well as natural subdecadal cycles of acidification, a recordof pH alone does not provide a mechanistic explanation of whyor how such fluctuations occur.As anthropogenic OA continues unabated, and the scientific

community tries to elucidate the impacts on coral reefs, it isbecoming increasingly apparent that this problem must beviewed in the context of natural climatic and oceanographicdrivers as well as the ability of reefs to partly modify the sur-rounding seawater chemistry (11). Similar to the offshore envi-ronment where anthropogenic CO2 trends are only discernibleafter decades of observations (2, 3), confounding local biologicalprocesses easily mask the OA signal on coral reefs. Addingcomplexity to the system is the proposed connection to offshoreprocesses and climatic phenomena such as the NAO, which

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Fig. 4. Time-dependent correlations between offshore and reef processes.MLD at BATS shows maximum positive correlation with offshore primaryproductivity (PP) when it precedes PP by 1 mo (r = 0.83). In contrast, reef NECand negative NEP (i.e., heterotrophy) show maximum correlation with PPwhen they lag PP by 4 (r = 0.77) and 6 mo (r = −0.45), respectively. Thecorrelations were significant at the 99.5% confidence level, indicated by theblack dashed lines.

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exerts demonstrable control on biogeochemical processes (26, 30)and seawater CO2 dynamics (36), but has yet to be extensivelyexamined as a driver of coral reef, or more generally, coastalbiogeochemistry (37). Continued and expanded observationswill allow the scientific community to address these links innear-shore environments, as well as discern the effect of an-thropogenic CO2.

Materials and MethodsSampling DIC and TA. Surface seawater samples from the Bermuda coral reefplatform were collected once a month at 0.5–1-m depth using a 5-L Niskinbottle. TA and DIC samples were collected according to standard protocols(14) using 250-mL Kimax brand glass sample bottles. Samples were im-mediately poisoned with 100 μL saturated solution of HgCl2. Temperaturewas measured in the Niskin bottle while samples for salinity were collectedin glass bottles and later analyzed using an autosalinometer (GuildlineInstruments). DIC was analyzed coulometrically using a UIC CM5011 CO2

coulometer combined with a versatile instrument for the determination oftotal inorganic carbon and titration alkalinity (VINDTA) 3C (Marianda Inc)or single-operator multiparameter metabolic analyzer (SOMMA) system, al-ternatively based on infrared absorption using an automated infrared in-organic carbon analyzer (AIRICA) (Marianda, Inc) and a Li-Cor 7000 as thedetector. TA was analyzed based on potentiometric acid titrations (∼0.1 NHCl) using a VINDTA3S (Marianda Inc). Performance and precision of the in-struments were regularly verified using certified reference material (CRM)prepared by A. Dickson at Scripps Institution of Oceanography (SIO). The ac-curacy and precision of replicate CRMs on any given day of analyses weretypically in the range of ±2–4 μmol kg−1 for both TA and DIC.

Since 1983, the surface seawater at the Hydrostation S (32°10′N, 66°30′W)and BATS (31°50′ N, 64°10′W) sites has been sampled approximatelymonthly for T, S, DIC, and TA, as well as other biogeochemical parameters.The sampling frequency of the time series has not been exactly uniform,ranging from 9 to 12 sampling cruises per year during the first few decadesof collection to 14–15 sampling cruises per year more recently. Between1983 and 1989, C. D. Keeling at SIO managed sample collection and analysis.

Since 1989 samples were collected using 500-mL Pyrex bottles (replaced by250-mL Kimax bottles in the early 2000s), which were quickly poisoned withHgCl2 and sealed until analysis at Bermuda Institute of Ocean Sciences (BIOS).Analysis occurred typically within a few months of collection (2). Similar to thereef platform samples, DIC samples were analyzed using coulometric methodswith an SOMMA system. TA was analyzed using a manual alkalinity titratoruntil the 2000s, when it was then replaced by a VINDTA 2S system. Precision ofthe instruments was verified on a daily basis using CRMs, with an accuracy andprecision of typically <0.2% for replicate analyses (2).

For both reef and BATS measurements, seawater CO2 chemical parameterswere calculated using CO2SYS (cdiac.ornl.gov/ftp/co2sys/) with measured TAand DIC at in situ temperature and salinity conditions, and stoichiometricconstants defined by ref. 38. The mean of the four reef sites at each time pointwas used to represent “reef” measurements. Temperature and salinity nor-malized seawater CO2 chemical parameters for BATS and reef sites were cal-culated using nDIC, nTA, and the average salinity and temperature observedacross the reef platform (36.63 g kg−1 and 23.1 °C, respectively). To account forthe nonuniform sampling intervals, which occurred primarily in the BATSdataset, samples occurring in the same month were averaged (2). Short-termdata at BATS and on the reef flat were clipped to exactly 5 y to prevent anyseasonal weighting. The climatology was calculated by averaging the seasonalcycle of a given parameter (Fig. S4), with the anomalies determined by sub-tracting the climatology from the time series of each parameter (2).

Computing Reef Biogeochemical Processes and Contribution to Acidification.The contributions of nDIC and nTA to the temperature and salinity nor-malized pH and Ωaragonite at BATS and on the reef platform were calcu-lated by using the temporal changes in nDIC and nTA. The starting pH andΩaragonite were determined based on the initial nDIC and nTA, with thefinal values for nDIC and nTA at each time point sequentially steppedthrough and the pH and Ωarag calculated for each step. To calculate reefNEC, NEP, and air–sea CO2 gas exchange, offshore BATS and reef datawere interpolated onto evenly sampled datasets, with BATS assumed to berepresentative of waters flowing onto the reef platform. Relative NEC(μmol kg−1) was calculated based on depletions in alkalinity from BATS to

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Fig. 5. Conceptual model of interannual variations in winter NAO state and resulting shifts in reef biogeochemistry (modified from ref. 23). (A) Duringperiods of positive or neutral winter NAO states, spring blooms are weakened. With less advection of external biomass onto the coral reef, the reef com-munity tends toward autotrophy and weaker calcification, resulting in enrichment of seawater Ωaragonite when moving offshore to inshore across the reefplatform (contour plot C). (B) When the winter NAO state is negative, spring blooms are enhanced with greater primary productivity and zooplanktonbiomass. Increased advection of offshore biomass shifts reef community metabolism toward greater heterotrophy and calcification, resulting in reduction ofseawater Ωaragonite and increased acidification. (C) Ωaragonite as a function of nTA and nDIC with data from a positive (2008, light gray circles) and negative(2010, dark gray squares) NAO winter index year. Type II linear regression lines are shown for the positive (n = 33; m = 0.869 ± 0.124 SD; b = 582.111 ± 254.920SD; r = 0.773) and negative years (n = 48; m = 1.029 ± 0.112 SD; b = 240.322 ± 230.700 SD; r = 0.798). Note the steeper slope (corresponding to greateracidification) during the negative NAO index year driven by a higher frequency of acidification events (shift to +δNEC and –δNEP, red arrows). Average BATSnDIC and nTA ±1 SD is shown by the black circle.

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the reef using the following equation assuming constant residence timeand average depth:

NEC=−12ðnTAreef −nTABATSÞ.

Air–sea gas exchange of CO2, which impacts only the DIC concentration, wascalculated using in situ reef pCO2 values (calculated from in situ DIC, TA, T,and S data) and the equations described by refs. 39, 40. Wind and barometricpressure for air–sea flux calculations were measured at the Bermuda in-ternational airport, and assumed to be representative of conditions on thereef platform. Ten-min sustained wind speed at 10 m and barometric pressuredata taken at 3-h intervals were obtained from the World MeteorologicalOrganization and Bermuda Weather Service, and subsequently binned intomonths, averaged, and interpolated to match our measurement intervals forthe BATS and reef biogeochemistry data. Accounting for the effects of air–sea gas exchange and NEC on DIC mass balances, relative NEP (μmol kg−1) wassubsequently calculated according to the following equation:

NEP=−NEC−CO2   gas  exchange− ðnDICreef−nDICBATSÞ.

The attributions of NEC, NEP, and air–sea CO2 gas exchange of reef to BATSdifferences in pH (ΔpHREEF – BATS, Fig. 5) were calculated as previously de-scribed for nDIC and nTA contributions, with the impacts of each bio-geochemical process on nDIC and nTA calculated and the resulting nDIC andnTA used to then calculate pH.

Climatological and Offshore Primary Productivity Data. Monthly mean NAOindex data were obtained from the NOAA Climate Prediction Office (www.cpc.ncep.noaa.gov/products/precip/CWlink/pna/nao.shtml) with the winterNAO state taken as the average of December to March. Depth-integratedprimary productivity data were calculated using a trapezoidal integration ofprimary productivity data from the upper 140 m at BATS. Primary pro-duction is calculated as the mean difference in 14C uptake between lightand dark bottle incubations of seawater samples. The MLD was computed asthe depth where temperature was less than 0.5 °C cooler than surfacetemperatures (29).

Cross-correlations between offshore primary productivity, MLD, and reefNEC and NEP processes were calculated using the MATLAB function xcorr,with correlation coefficients normalized such that autocorrelations at zerolag were exactly 1. Confidence intervals of 99.5% were calculated using theequation ± 2.58/√N, where n = 60.

ACKNOWLEDGMENTS. We are grateful to Rod Johnson, Bermuda Instituteof Ocean Sciences (BIOS), for providing the most recent BATS data; MarkGuishard, BIOS, for providing the wind speed and barometric pressure data;and Brice Semmens, Scripps Institution of Oceanography (SIO), for providingadvice on the statistical analysis. Comments by two anonymous reviewersalso significantly improved an earlier draft of this manuscript. The authorsgratefully acknowledge support from National Science Foundation GrantsOCE 09-28406 (to A.J.A. and N.R.B.), OCE 12-55042 (to A.J.A.), and OCE 14-16518 (to A.J.A.).

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