Differences in carbonate chemistry up-regulation of long-lived reef-building corals

With climate projections questioning the future survival of stony corals and their dominance as tropical reef builders, it is critical to understand the adaptive capacity of corals to ongoing climate change. Biological mediation of the carbonate chemistry of the coral calcifying fluid is a fundamental component for assessing the response of corals to global threats. The Tara Pacific expedition (2016–2018) provided an opportunity to investigate calcification patterns in extant corals throughout the Pacific Ocean. Cores from colonies of the massive Porites and Diploastrea genera were collected from different environments to assess calcification parameters of long-lived reef-building corals. At the basin scale of the Pacific Ocean, we show that both genera systematically up-regulate their calcifying fluid pH and dissolved inorganic carbon to achieve efficient skeletal precipitation. However, while Porites corals increase the aragonite saturation state of the calcifying fluid (Ωcf) at higher temperatures to enhance their calcification capacity, Diploastrea show a steady homeostatic Ωcf across the Pacific temperature gradient. Thus, the extent to which Diploastrea responds to ocean warming and/or acidification is unclear, and it deserves further attention whether this is beneficial or detrimental to future survival of this coral genus.


Results and discussion
Coral samples were collected from 33 sites in the Pacific Ocean characterized by different environmental conditions. The mean SST values (integrated over the period 2010-2016) varied between 22.44 °C in Easter Island and 29.76 °C in Papua New Guinea (> 7 °C difference). Mean pH exhibited a relatively small difference between 8.01 in Kiribati and 8.09 in Heron Island (ΔpH = 0.08). Thus, the calculated seawater saturation states (Ω SW ) varied from 3.21 in Coiba to 3.95 in Moorea ("integrated seawater properties" in Table S2, Fig. S1). Boron-derived values of the cf carbonate chemistry revealed significant differences in [CO 3 2− ] cf and Ω cf (P < 0.05) between Porites and Diploastrea, with the latter showing lower values (Table S1). Cores of the two genera also showed significantly different linear extension and calcification rates (P < 0.05). The comparison between environmental data, growth parameters, and boron-derived cf estimates for Porites (Figs. 2, S2) indicates that average pH cf was not controlled by spatial differences in seawater pH or aragonite saturation state (P > 0.05). Instead, our data suggest that spatially average pH cf is linked to SST (R = − 0.63, P < 0.001) and DIC sw (R = 0.41, P = 0.017). While DIC sw showed a significant correlation with salinity (R = 0.98, P < 0.001), pH cf was also related to salinity but to a lesser degree (R = 0.35, P = 0.046). Similarly, DIC cf was related to SST (R = 0.71, P < 0.001). Thus, on spatial scales a strong negative correlation exists between pH cf and DIC cf (R = − 0.81, P < 0.001), consistent with other studies at a seasonal scale 20,30,31 . Our results suggest that seawater temperature explains most of the variance in pH cf and DIC cf in Porites colonies at a basin-scale (Fig. 2). Similarly, overall observations apply to Diploastrea samples, since B/Ca, δ 11 B, DIC cf , and pH cf were significantly correlated with seawater temperature (Fig. 3A-D). However, this contrasts with other studies that have shown that seawater pH is the main driver of pH cf on annual and longer time scales, while temperature only plays a secondary role 32,33 . This suggests that the magnitude of SST variations (seasonal vs. annual and temporal vs. spatial) is what effectively controls the relationship between temperature and cf carbonate chemistry. At large, as expected and previously observed in various Indo-Pacific regions 20,[30][31][32][33][34] , Porites calcification was positively correlated with SST (R = 0.37, P = 0.034) and displayed a positive correlation with DIC cf (R = 0.35, P = 0.044). www.nature.com/scientificreports/ In agreement with recent studies focused on Porites at a seasonal scale ( Fig. S3; 20,22 ), our bulk 6 yr-integrated results show a strong negative relationship between pH cf and SST as well as a positive correlation between DIC cf and SST for both coral genera (Fig. 3). These opposing relationships suggest that corals up-regulate their internal pH in response to temperature-related changes in metabolic DIC, as already posited in previous studies (e.g., by means of higher metabolic DIC availability from algal symbiont photosynthesis at warmer temperatures and/ or light) 23,32 .
In this study, for Porites we determined a DIC cf increase of 128 ± 23 μmol kg −1 per °C, while pH cf decreased by 0.015 ± 0.004 per °C (Fig. 3, Table S4), resulting in an increase in [CO 3 2 ] cf of 29 ± 5 μmol kg −1 per °C and higher Ω cf values (~ 21 vs. ~ 16, Fig. 3). The decrease in pH cf with temperature observed at a spatial scale is around three times lower than previous estimates observed at a seasonal scale 32 , and therefore steadier (homeostatic). Besides the notion that temperature influences pH cf up-regulation, our study demonstrates the pH cf up-regulation capacity of Porites across stable and warm regions as well as in regions with a large seasonal temperature amplitude and low mean annual temperatures (or mean annual light) (i.e., sub-equatorial vs. equatorial regions). Thus, pH cf up-regulation overcomes the decrease in DIC cf due to colder SSTs (Fig. 3) in sub-equatorial areas to enable coral calcification. Seasonally-resolved Porites records of δ 11 B and B/Ca have shown that DIC cf is lower during winter months (i.e., colder temperatures) due to lower metabolic supply of DIC within the calcifying fluid 20 . The supply of this metabolically derived carbon is driven by light and temperature through the respiration of algal symbiont photosynthates 35 , as colder temperatures reduce zooxanthellae activity and reduce the concentration of metabolic DIC in the calcifying fluid. However, higher nutrient availability at higher latitudes may contribute to partially offsetting the detrimental effects caused by the lower metabolic supply of DIC cf . The negative correlation between pH cf and DIC cf at a spatial scale in our study is consistent with intracolonial seasonal variations reported in previous studies 20, 33 .
The up-regulation of pH cf is one way for corals to compensate for the reduced metabolic carbon input from the algal symbiont and to maintain supersaturated conditions in a biologically controlled compartment with respect We used monthly global reconstructed surface ocean pCO 2 , airsea fluxes of CO 2 and pH to calculate seawater pH and associated uncertainties on a 1° × 1° regular grid 28 . These maps were obtained from an ensemble-based forward feed neural network approach mapping in situ data for surface ocean fugacity (SOCAT data base 29 , https:// www. socat. info/) and sea surface salinity, temperature, sea surface height, chlorophyll a, mixed layer depth, and atmospheric CO 2 mole fraction. www.nature.com/scientificreports/ to aragonite (Ω cf ~ 5 × Ω SW ) 20 . This explains why Porites corals living in equatorial and sub-equatorial regions display similar Ω cf values, despite their different internal pH cf , driven by temperature-dependent DIC cf regulation.
Since the photosynthetic activity of the coral associated algal symbiont is presumably reduced at higher latitudes (~ 27° N/S in this study) due to lower light availability compared to equatorial latitudes 36 , corals may use their energy to regulate their cf chemistry, in particular their pH cf , to maintain active growth and skeletal accretion. The results of our study, based on a multi-year sampling strategy of coral core-tops across the Pacific Ocean, are consistent with the calcification model proposed by Ross et al. 30,31 (Fig. S4), based on a seasonal timescale. The primary mechanism for the up-regulation of pH cf involves the Ca 2+ -ATPase pump, which exchanges one calcium ion for two protons across the cell membrane [37][38][39][40] . The removal of H + from the cf increases the diffusion of metabolic CO 2 38 , which is either protonated to bicarbonate (HCO 3 − ) by carbonic anhydrase (CA) and/ or transported in the form of HCO 3 − by bicarbonate anion transporters (BATs, i.e., through active transport) 41 . Up-regulation of pH cf shifts the DIC equilibrium in favor of CO 3 2− , thereby increasing the internal aragonite saturation state to promote skeletal formation 20,38,42,43 .
Our study provides evidence that to maintain growth Porites corals up-regulate their pH cf and increase their DIC cf concentration in response to changes in SST across the Pacific Ocean. This physiological mechanism has already been observed for Porites on a seasonal timescale in the Great Barrier Reef 20 (Fig. S3) and Galapagos 22 , as well as during the 1998 bleaching event and associated thermal stress 19 . Here, for the first time we demonstrate that this mechanism applies across a wide range of latitudes and longitudes. The ability of corals to modulate their calcifying fluid chemistry explains their sustained calcification rates, which are primarily driven by temperature and DIC cf . Porites corals in warmer environments display lower pH cf but higher DIC cf and [CO 3 2− ] cf (Fig. 3), leading to significantly higher Ω cf compared to the surrounding seawater ( Fig. 3) and increasing calcification rates. In contrast to Porites, branching corals 31,32 exhibit higher calcification rates at lower temperatures and higher pH cf and [CO 3 2− ] cf . It is now recognized that the internal modulation of coral calcifying fluid is genus-specific (if not species-specific) 21,31,44 . Our study demonstrates that Porites colonies living across a wide range of environments across the Pacific Ocean can modulate their cf chemistry in response to prevalent regional temperature regimes to maintain calcification rates, as previously suggested 20,22 . www.nature.com/scientificreports/ Conversely to Porites, the capacity of the long-lived massive coral Diploastrea to regulate its internal pH cf had not been studied yet. While Diploastrea and Porites showed similar decreases in B/Ca ratios with increasing temperature, Diploastrea consistently exhibited lower δ 11 B values (and therefore pH cf ) at the same temperature ( Fig. 3), indicating taxa-specific differences with regard to internal pH cf regulation (Fig. 4). In both coral genera, pH cf and DIC cf were positively correlated with the Pacific Ocean temperature. However, at higher temperatures, Diploastrea showed a reduced pH cf up-regulation due to a pH cf decrease of − 0.036 ± 0.006 per °C (n = 6), resulting in lower [CO 3 2− ] cf and Ω cf values (Table S1). This newly discovered finding suggests different mechanisms of calcification control in Porites and Diploastrea. Our interpretation is that either the Diploastrea Ca 2+ -ATPase pump is less effective than that of Porites in removing H + from the calcifying cell, or that Diploastrea has a mechanism for conserving energy by maintaining stable levels of [CO 3 2− ] cf and Ω cf (~ 16-18), particularly in regions of higher temperatures (Fig. 3, Table S1).
Response differences of corals to fluctuating temperature (e.g., based on a regional gradient, seasonality, thermal stress) in relation to their calcifying mechanisms have already been documented. It is worth noting that the observed pH cf decrease with SST for Diploastrea (− 0.036 per °C, Table S4) is comparable to the mean drop (− 0.03 per °C) recorded for seven symbiotic coral species (4 genera) studied on a seasonal scale in Western Australia over a wide range of latitudes (~ 11°) 31 . However, although the magnitude of change is equivalent, the underlying mechanisms are different. In particular, since DIC cf up-regulation was lower in the Australian corals, the resulting Ω cf values were lower (~ 10-12), and the Ω cf change with temperature varied among species. A notable difference has also been observed between aquaria-reared colonies of Pocillopora damicornis and Stylophora pistillata grown under various temperature and pCO 2 conditions 44 that indicate that only Pocillopora damicornis lose its compensatory ability under thermal stress (31 °C vs. 28 °C) with Ω cf values clearly below 10 for different pH sw conditions. Further, during a local thermal stress and bleaching event 45 , the branching coral Acropora aspera continued to up-regulate pH cf at high temperatures, while DIC cf up-regulation was significantly impaired, which is in contrast to the response of massive corals examined here. A species-specific response of pH cf and DIC cf up-regulation relative to seawater carbonate chemistry variation and ocean acidification has already been described at a seasonal timescale, showing marked differences in calcification control between massive corals such as Porites, Acropora, Psammocora, and Pocillopora 46,47 .
A summary of the taxon-specific responses of cf carbonate chemistry to temperature for the massive corals here studied as Δ (i.e., Porites values-Diploastrea values) is provided in Fig. 4B,D,F,H. It is apparent that  www.nature.com/scientificreports/ an increase in temperature leads to a substantial increase in Δ, especially for the key parameters [CO 3 2− ] cf and Ω cf that are directly linked to coral calcification. Thus, despite the elevation of DIC cf at high temperatures, the capacity of Diploastrea to increase Ω cf under warmer conditions is clearly different from Porites. However, based on our data, Diploastrea maintain their capacity to regulate Ω cf and exhibit homeostatic control of the aragonite saturation state independently of geographic location or temperature. This indicates that the pronounced drop of pH cf up-regulation with temperature (− 0.036 ± 0.006 per °C, n = 6) is sufficiently compensated by the buffering capacity and DIC cf increase (129 ± 30 per °C, n = 6). Therefore, the calcification ability of Diploastrea is less sensitive to ocean temperature changes compared to Porites when we consider the key parameters [CO 3 2− ] cf and Ω cf . This may suggest that calcification rate for Diploastrea is potentially less variable in space and time (seasonal amplitudes) compared to Porites. The mechanism observed in Diploastrea appears to resemble the one described by Georgiou et al. (2015) 46 , which demonstrated the capacity to maintain calcification irrespective of environmental differences (i.e., homeostasis), suggesting a similar mechanism in Diploastrea. By stabilizing its chemical composition, even at high temperatures, Diploastrea can achieve optimal calcification. Further studies are required to evaluate such a hypothesis but also better understand the potential impact of the lower Ca 2+ -ATPase pump efficiency and pH cf up-regulation posited for Diploastrea at higher temperatures on calcification, especially in the context of climate change. It should also be noted that Ω cf values (~ 16-18) were calculated assuming Ca 2+ concentrations in the calcifying fluid similar to that of the seawater. However, this assumption requires further investigation for Diploastrea and Porites, as recent studies have shown substantial variations in Ca 2+ concentration of the calcifying fluid 15 .
Our study across the Pacific Ocean confirms the ability of the massive reef-building Porites genus to modulate the composition of its calcifying fluid in response to seawater temperature and carbonate chemistry, as observed  www.nature.com/scientificreports/ for other scleractinian corals at different locations or exposed to disparate environmental conditions. For Porites, an upward shift in pH cf and DIC cf (relative to seawater) driven by temperature changes is the presumed mechanism for Porites to compensate for the impact of future thermal stress events or ocean warming on calcification in the Pacific Ocean. Further, our study demonstrates that SST rather than pH sw or Ω sw , is the key parameter controlling Porites calcifying fluid properties, through the activity of the zooxanthellae. Thus, Porites is able to adapt its metabolism to increases in seawater temperature, heralding the adaptive potential of Porites to maintain or reinforce a high aragonite saturation state Ω cf and calcification capacity in the face of climate change. Importantly, however, our results do not rule out that ocean acidification 12,33,[46][47][48][49][50] or other environmental factors, including changes in light conditions 23 , may affect coral calcification locally in the near future. Our study also demonstrates biological control of the calcification process is taxon-specific. We show that Diploastrea displays a different strategy than Porites at high temperatures (28-30 °C), in that it maintains consistent calcification rates irrespective of the prevailing environment. Species-specific differences need to be thus considered when forecasting coral future survival 51 . Further investigations of the response of Diploastrea corals at annual and seasonal timescales will reduce uncertainties and better constrain the range of their homeostatic ability to calcify at warming water temperatures. A part of these future research works will be conducted in the new program COR-Resilience (2023-2028) recently funded by the French National Research Agency.

Methods
Coral core sampling. Thirty-nine coral cores (40-150 cm long) were collected from living Porites and Diploastrea colonies during the Tara Pacific expedition 52 between 2016 and 2018 using a hydraulic drill (Stanley®) with a 7 cm diameter corer. After drilling, a cement plug was placed in the opening to facilitate the recovery of the colonies. Details of sampling locations, depth, date and hydrological conditions are reported in Table S1. Cores from both genera were collected at six locations (New Caledonia, three in Papua New Guinea, Palau, and Taiwan; black dots in Fig. 1), allowing comparison of results and evaluating genus effects in 6 different hydrological environments.

Coral growth parameters. Skeletal density (g cm −3 ) was measured at DOSEO Platform (CEA) in Paris-
Saclay using a Discovery CT750 high-definition Computed Tomography X-ray system operated at 120 kV 53,54 .
The spatial × resolution of the scans along the maximum growth axis of the colonies was 0.625 mm, while y (width) and z (height) resolutions ranged from about 0.59-0.79 mm. For each coral core, a mean density was calculated by averaging density measurements along 3 parallel transects corresponding to the growth period 2010-2016 (Fig. S5). Analytical precision of the CT density values was estimated to 4% (2σ) based on repeated measurements (n = 10) of 3 coral standards and uncertainties of the calibration curve 53,54 . CT scans were also used to quantify the linear extension rate (mm yr −1 ) based on the density banding pattern. Mean linear extension rates (upward linear growth) were determined for each coral core by measuring the distance between successive low-density bands over the last 6 years of growth (2010-2016), excluding the tissue layer (Fig. S5). The uncertainty of the linear extension rates was calculated from two sets of measurements (Table S3) performed with CT-scans and was 4% (2σ). Finally, coral calcification rate (g cm −2 yr −1 ) was calculated as the product of the annual linear extension rate (cm yr −1 ) and the skeletal density (g cm −3 ) with an overall uncertainty of 6% (2σ).
Coral powder sampling. Core-top samples for geochemical analyses (~ 1000 mg) were collected using a dental drill (Dremel®) with a 0.17 mm thick diamond-encrusted blade along transects (Fig. S5A) parallel to the maximum growth axis corresponding to the last 6 years of growth (2010-2016), excluding the tissue layer, and according to the density banding pattern observed on CT-scans (Fig. S5B). Each aragonite piece corresponding to the period 2010-2016 was finely crushed and thoroughly homogenized in an agate mortar. Prior to elemental (B/Ca) and isotopic (δ 11 B) analysis, 100 mg of powder was sub-sampled and cleaned from organic contaminations following an oxidative cleaning protocol 55 . Finally, they were dissolved in 3 mL of 4 wt% HNO3 for B/Ca and δ 11 B analysis. We opted here for a bulk sampling strategy (i.e. a single large sampling integrating 6 years of growth including all skeletal structures, 2-5 cm in length; 1-2 cm in width/thickness, Fig. S5) to avoid potential geochemical biases associated with the coral mesostructures/microstructures 56 and strong seasonal δ 11 B and B/ Ca variability 57 . The integration of several years into a single sample analysis, was intended to ensure a constant mixing ratio of coral micro-and mesostructures (COCs, aragonite fibers, thecal wall, and columella) with minor effects on boron geochemistry (see below δ 11 B section), especially for Diploastrea 58 . Among the 39 samples analysed in the present study, the uncertainty due to the possible inclusion of skeleton from other years in the coral samples was estimated for carbonate chemistry and SST and was considered negligible 59 . For example, uncertainties in SST due to our multiple-year sampling strategy would be less than 0.  (δ 11 B). Boron was purified using a batch protocol 61 www.nature.com/scientificreports/ boron solutions were introduced into the mass spectrometer through a PFA-50 μL min −1 nebulizer and a microcyclonic chamber. Instrumental mass fractionation and long-term drift of the 11 B/ 10 B ratio were systematically corrected by applying a standard-sample-standard bracketing protocol, and using a M1P-p solution with a typical measured δ 11 B value of 25.20 ± 0.25‰ (2σ, n = 50). Further details in Wu et al. 63 . Under this condition, the mean δ 11 B value obtained for Porites JCp-1 is 24.28 ± 0.36‰ (2σ, n = 15), which agrees well with the robust mean reported in Gutjahr et al. 64 (24.25 ± 0.22‰). Each sample was measured three times from the same solution and the precision (2σ) was in general better than 0.3‰. In addition, to evaluate possible effects of our sub-sampling strategy of each core-top powder and its heterogeneity, we also analysed eleven 100 mg-sub-samples of a Diploastrea homogenised powder from the core I28S3-D from Taiwan (sample I28S3D-OM) and six of Porites from the core I23S2-P from Papua New Guinea (sample I23S2P-38). The reproducibility obtained for δ 11 B measurements was ± 0.36‰ (2σ, n = 11) for Diploastrea and ± 0.18‰ (2σ, n = 6) for Porites, respectively. Even though the value for Diploastrea is twice that of Porites, possibly due to the effects of genus-specific micro-and mesostructures 58 , the uncertainties remain indistinguishable from the analytical uncertainties determined for the Porites standards (± 0.3‰), and significantly smaller than the difference observed between the two genera for each site, which ranges from 0.4 to 2‰. We also tested possible effects of genus-specific micro-and mesostructures (i.e. septa or columella) on the Diploastrea skeleton by taking 2 samples from the same core-top portion of the I21S2c17 colony (over the period 2010-2016; e.g. Fig. S5). The results show no major effect on δ 11 B and B/Ca composition, with the 2 samples having the same values within error (i.e. 24.00 ± 0.30‰ and 24.49 ± 0.30%, respectively; the difference in B/Ca was less than 2%). These results suggest that our sampling strategy that integrates multiple years into a single sample for each site avoids potential geochemical biases related to coral microstructures and different mixing ratios.

Boron isotopes analysis
Calcifying fluid carbonate chemistry. The pH of the calcifying fluid (pH cf ) was calculated from the boron isotopic composition of the coral skeleton (δ 11 B coral) according to the following Eq. 65,66 : where δ 11 B sw is the boron isotopic composition of seawater (39.61‰; Foster et al. 67 ) and α B is the isotopic fractionation factor (1.0272) 68 . The dissociation constant of boric acid (pK B ) in seawater 69 was calculated from the temperature (i.e. mean OiSST), salinity (i.e. mean EN4) and depth (pressure) for each sampling location. The carbonate ion concentration in the calcifying fluid was calculated using B/Ca according to the following equation 19 : where [B(OH) 4 ] cf is the concentration of borate ion in the calcifying fluid derived from δ 11 B-pH cf and corrected for SST, salinity, and depth. K D B/Ca is the distribution coefficient for boron between aragonite and seawater 70 that has been refit as a function of [H + ] 57 , and (B/Ca) CaCO 3 is the elemental ratio of boron to calcium measured in the coral skeleton. To estimate B(OH) − 4 cf , we assume that the concentration of total boron in the calcifying fluid is only salinity dependent and is equal to that of the surrounding seawater. Dissolved inorganic carbon (DIC cf ) and aragonite saturation state (Ω cf ) in the calcifying fluid were estimated from pH cf and [CO 3 2− ] cf , using CO2SYS.m Matlab script 71,72 , with carbonate species dissociation from Dickson and Millero 73 and Mehrbach et al. 74 , borate and sulfate dissociation from Dickson 69,75 and aragonite solubility from Mucci et al. 76 .
For Ω cf calculations, it was assumed that [Ca 2+ ] values in calcifying fluids (~ 13 mM) are higher than seawater values (~ 10.5 mM), based on the results reported in Sevilgen et al. 77 . These authors measured Ca 2+ concentration in the cf of the growing edge of Stylophora pistillata through direct in vivo measurements (microsensors) and found that this coral elevated [Ca 2+ ] by about 2 ± 2 mM compared to seawater values for both light and dark conditions. They also observed substantial Ca 2+ variations in cf, indicating temporal and spatial variation in Ω cf . Elevated Ca 2+ concentration (+ 25%) in cf was also inferred by DeCarlo et al 78 for Pocillopora damicornis using indirect methods (Raman spectroscopy and boron isotopes). However, as previously tested by Thompson et al. 79 , this [Ca 2+ ] upregulation compared to seawater only affects the absolute magnitude of the aragonite saturation state in the cf, not the relative differences between colonies, sites, or time periods. Therefore, we consider that our main findings and conclusions on the aragonite saturation state are here independent of the Ca 2+ concentration and that further studies would be useful to better quantify the calcium concentration in the calcifying fluids of massive corals. The Ω cf values displayed in Table S1 and discussed in this study were calculated by considering no difference in [Ca 2+ ] between calcifying fluid and seawater. These values in massive corals would increase of ~ 4 unit if we consider that Ca 2+ is around 25% more concentrated in fluids.
Uncertainties in pH cf and [CO 3 2− ] cf were obtained using the boron systematics package of DeCarlo et al. 78 and were less than 0.03 pH units and 74 μmol kg −1 respectively. The uncertainties of DIC cf and Ω cf , calculated using the error m script Matlab 80 , were less than 278 μmol kg −1 and 1.06, respectively.
Environmental data (SST, salinity, and seawater carbonate chemistry). Key environmental parameters, including SST, salinity, total alkalinity, and dissolved inorganic carbon, were acquired as discrete measurements at coral sites (few meters from the coral drilling sites) during the Tara Pacific expedition. Ambient seawater temperature and salinity were obtained using a CTD (± 0.1 °C and ± 0.01, respectively), whereas seawater samples for TA and DIC measurements were collected in 500 mL glass-bottles. The unfiltered seawater samples were poisoned with HgCl 2 and stored onboard at room temperature prior to TA and DIC analy- www.nature.com/scientificreports/ ses performed at the SNAPOCO2 facility at Sorbonne University in Paris, France 81 following the SNAPOCO2 protocol 82,83 . Raw results were recently described in (Lombard et al., 2023) 84 and are now available in the PAN-GEA data base 85  ] sw , DIC sw , and Ω sw ) was calculated using the CO2SYS.m Matlab script 72 . Similar, to SST and salinity, discrete in situ measurements represent only a snapshot of the carbonate chemistry variability of the coral reef, which is affected by diurnal and seasonal cycles mainly related to temperature-driven pCO 2 solubility and other local factors (e.g. residence time of waters in the reef, balance between production and respiration). To overcome this limitation, we used SST from the AVHRR-OISSTv2 dataset with a spatial resolution of 0.25° × 0.25°8 7,88 , salinity from the EN4 dataset at 1° × 1°8 9,90 , and pH sw values from the Operational Mercator Ocean biogeochemical global ocean analysis and forecast system at 0.25 × 0.25°, based on in situ DIC and TA measurements from the GLODAPv2 database 91 . Mean SST and salinity values for each site were calculated by averaging monthly data from January 2010 to December 2016 (the period covered by the coral portion collected for the geochemical analyses).
Annual mean TA values were derived from salinity based on the following linear equation: TA (μmol kg −1 ) = 2299 × (salinity/35) for tropical and subtropical regions 92 . Finally, seawater [CO 3 2− ] and Ω were calculated using CO2SYS.m Matlab script 72 with the values of SST, salinity, TA, and pH.
All the environmental data are reported in Table S2 and Fig. S1.
Statistical data treatment. Pearson correlation coefficients were used to assess the degree of correlation between discrete Tara seawater measurements and values derived from the different datasets. Outliers were identified using the ROUT test and excluded if present. Independent two-sample t-tests were used to detect significant differences in growth parameters between Porites and Diploastrea samples. The non-parametric Spearman's rank-order correlation was performed to determine the strength and direction of the association between two ranked variables illustrated in Figure S1 and S2. Rank correlations sort observations by rank and compute the level of similarity between the rank of the variables. R coefficients are always between − 1 and 1 with values close to the extremity indicating strong relationships. The correlation matrixes (Fig. S2) represent the pair correlation of all the variables (i.e. seawater temperature, salinity and carbonate chemistry, coral cf chemistry, and growth parameters). The significance level of statistical tests is expressed with p-values (P) with a threshold of significance defined at 0.05 (5%) or 0.001 (1‰). Statistical data treatment was performed using PRISM software.

Data availability
All data generated or analyzed during this study are included in the publication or in the supplementary information files. Data will be also publicly available on the PANGAEA data repository. www.nature.com/scientificreports/