Research articlesSpecies-specific calcification response of Caribbean corals after 2-year transplantation to a low aragonite saturation submarine spring
Abstract
Coral calcification is expected to decline as atmospheric carbon dioxide concentration increases. We assessed the potential of Porites astreoides, Siderastrea siderea and Porites porites to survive and calcify under acidified conditions in a 2-year field transplant experiment around low pH, low aragonite saturation (Ωarag) submarine springs. Slow-growing S. siderea had the highest post-transplantation survival and showed increases in concentrations of Symbiodiniaceae, chlorophyll a and protein at the low Ωarag site. Nubbins of P. astreoides had 20% lower survival and higher chlorophyll a concentration at the low Ωarag site. Only 33% of P. porites nubbins survived at low Ωarag and their linear extension and calcification rates were reduced. The density of skeletons deposited after transplantation at the low Ωarag spring was 15–30% lower for all species. These results suggest that corals with slow calcification rates and high Symbiodiniaceae, chlorophyll a and protein concentrations may be less susceptible to ocean acidification, albeit with reduced skeletal density. We postulate that corals in the springs are responding to greater energy demands for overcoming larger differences in carbonate chemistry between the calcifying medium and the external environment. The differential mortality, growth rates and physiological changes may impact future coral species assemblages and the reef framework robustness.
1. Introduction
Anthropogenic activities are increasing the amount of carbon dioxide (CO2) entering the atmosphere. A large fraction of this CO2 dissolves in the ocean and lowers ocean pH and carbonate ion concentrations [1]. Low carbonate ion concentrations decrease the aragonite saturation state (Ωarag) of seawater and the availability of carbonate ions needed for deposition of calcium carbonate skeletons [2]. A meta-analysis of experimental studies found a decrease of approximately 15% in coral calcification rates per unit decrease in Ωarag [3]. Data from laboratory experiments and modelling suggest that coral reef carbonate accretion diminishes at Ωarag lower than 3.3 [4], a level likely to be reached in much of the surface ocean by 2100 [1,5]. Many laboratory experiments have reported reduced coral growth under low Ωarag [6], but other experiments show little impact on calcification [7,8]. These conflicting results reflect the limitations of short-term single-organism manipulative experiments since, while laboratory experiments allow precise control of physico-chemical parameters, they do not fully reflect the complexity of the natural environment [9]. Moreover, such experiments are often too short for organisms to fully acclimate [10].
Scleractinian corals have been observed living in low pH waters near CO2 vents (pH < 7.7 [11]), low Ωarag submarine springs (Ωarag < 1 [12]), upwelling areas (Ωarag: 2.27–4.18 [13]) and mangrove lagoons (Ωarag: 1.47–2.02 [14]), although the taxonomic richness and calcification at some of these sites is lower than at nearby sites with ambient carbonate chemistry. At high CO2 vents in the Mediterranean, temperate corals were absent at Ωarag less than 2.5 [15], although two species that were transplanted to these low pH vents survived and grew at rates typical to the species used [16]. We investigated the survival, physiological response and calcification rate of three species of Caribbean corals in a two-year long, in situ transplantation experiment leveraging naturally occurring low pH, low Ωarag submarine springs.
Off the Yucatán peninsula, Mexico, submarine groundwater springs discharge low pH, low Ωarag water (Ωarag ∼ 0.5) into the back-reef lagoon of the Mesoamerican Barrier Reef. These springs, locally referred to as ‘ojos’, can be used for testing the potential of corals to acclimatize or adapt to low Ωarag conditions, although the ‘ojos’ are not perfect analogues for future ocean acidification. In this region, the groundwater mixes with seawater before discharging [17], and sensor and discrete sampling demonstrate that the discharged water has relatively high dissolved inorganic carbon (DIC), high alkalinity and slightly lower than ambient salinity, in addition to the low pH, resulting in low Ωarag [12,18–22]. Only three scleractinian coral species (Siderastrea siderea, Porites astreoides and Porites divaricata) grow within the areas continuously exposed to low Ωarag conditions, while taxonomic richness is higher outside the influence of discharge [12]. It has been shown that coral colonies living in the low Ωarag seawater are smaller than those exposed to ambient seawater [12] and have lower skeleton densities and calcification rates [19].
We assessed the potential of three coral species to survive and calcify under low Ωarag conditions by conducting an in situ transplant experiment with genetically identical coral fragments (nubbins). We monitored the corals for 2 years and collected surviving nubbins for analyses of skeletal characteristics (density, linear extension, calcification rate), and physiological characteristics (coral tissue protein content, and cell densities and chlorophyll a concentration of photosymbiotic algae Symbiodiniaceae). We then explored responses that may allow coral populations to survive and calcify at very low Ωarag conditions by comparing coral responses between transplantation sites (reflecting putative environmental control) and among sites of origin (reflecting putative genotypic influence).
2. Material and methods
(a) Study area
The Yucatán peninsula, Mexico, is a karstic region where rainfall flows through a complex aquifer system that discharges low pH, low Ωarag water at submarine springs (ojos) in the lagoon approximately 500 m offshore [23]. The conditions creating low pH seawater at the ojos differ from those of the ocean acidification scenario, as the high CO2 in the discharging water is derived from brackish water that has interacted with soil and limestone. The spring water is characterized by lower pH, higher DIC and higher total alkalinity compared to the ambient conditions. Nutrient concentrations vary between ojos but, at the transplant site, the spring waters only have higher silicate (not N or P). The corals at these ojos are constantly exposed to the discharging water, as discussed in detail in [12,19,20] and they represent settings with persistent low Ωarag. We note that Ωarag is the main parameter that affects calcification, and when calculating Ωarag in our study, all relevant environmental parameters were considered (e.g.: higher alkalinity and DIC in addition to the low pH). Ojos occur along the entire Yucatan karst platform and have been discharging water since the rise in sea level associated with the retreating ice sheets after the last glacial maximum [24]. The specific transplantation site at ojo Laja, Puerto Morelos (20.8°N, 86.8°W) was selected to minimize as much as possible the differences between the spring water and the surrounding seawater so that the main difference is in carbonate chemistry parameters.
(b) Coral species and transplant experiment design
We collected two genetically identical fragments (i.e. two nubbins collected from the same colony) from 10 P. astreoides colonies and 10 S. siderea colonies from areas impacted by the ojo discharge, and from 10 P. astreoides colonies and 9 S. siderea colonies from adjacent control sites away from the influence of discharge (a total of 39 colonies) (see electronic supplementary material, table S1 for collection details). Both species are found throughout the lagoon, including within low Ωarag ojo discharge plumes [12]. We also collected two nubbins each from 10 Porites porites colonies, a species not found in the lagoon, and from 10 additional S. siderea colonies from the main barrier reef structure. From each colony, one nubbin was transplanted to a low Ωarag site (ojo) and the second was transplanted to an ambient Ωarag site (control) in the lagoon, approximately 5 m away from the discharge site. A total of 59 colonies and 118 nubbins were transplanted (see electronic supplementary material, table S2 for transplantation details and figure 1 for transplant experiment design). One nubbin of P. porites transplanted to low Ωarag ojo was lost in the process and was not included in further analyses.
Figure 1. Transplant experiment design. Numbers are numbers of nubbins from each origin.
Nubbins of approximately 2–3 cm in length of massive P. astreoides and S. siderea were extracted by coring the upper horizontal surface with a submersible pneumatic drill. P. porites nubbins (small upright branches approx. 3–5 cm long) were broken off each colony with pliers. Each nubbin was mounted on a 5 × 5 cm square of stainless-steel mesh with epoxy putty that also covered all exposed skeletal surfaces to prevent bioerosion. Each nubbin was individually labelled with a tag tied to the mesh. The nubbins were placed in shallow trays with seawater and alizarin red S dye for 6–8 h to stain the surface and mark the beginning of new skeleton growth. After staining, each nubbin was photographed, and then randomly assigned to one of the transplantation sites (low Ωarag or ambient Ωarag). Within transplant sites, nubbins were randomly assigned to positions on stainless-steel grids and attached to the grids with cable ties (electronic supplementary material, figure S1). The grids were secured at the location of maximum discharge and approximately 5 m away from the influence of the discharging water.
Divers monitored the nubbins weekly for the first two months and then 14 times over the following 22 months. At the end of the transplant experiment, all surviving nubbins were collected and preserved in liquid nitrogen.
(c) Water chemistry
Water samples were collected weekly for the first two months of the experiment and then seven times during the following 22 months. Water samples were collected by divers, during the day time (9:00–13:00) into HDPE bottles, filtered (0.2 µm) into glass bottles and preserved with saturated mercuric chloride solution following Dickson, Sabine [25]. Temperature was measured with a handheld probe (YSI model 63). DIC was measured with a CM5011 Carbon Coulometer (UIC, Inc.). Alkalinity was measured with an automated open-cell, potentiometric titrator (Orion model 950). Salinity was measured with a salinometer (Portasal Model 8410, Guild Line). Certified CO2 seawater standards (UC San Diego # 108 and 135) were used as reference material. Ωarag was calculated using the CO2Sys program [26] with constants from Mehrbach et al. [27] refit by Dickson & Millero [28]. In addition, SeapHOx sensors were deployed for the duration of the experiment at the transplant sites (electronic supplementary material, figure S1) and collected temperature, conductivity, pressure, oxygen and pH every hour.
(d) Tissue extraction and skeletal analysis
Coral tissues were extracted with an airbrush using artificial seawater. Aliquots of the homogenized tissue were used for protein, symbiont cells and chlorophyll a measurements following the procedures of Krief et al. [29]. Coral skeletons were then submerged in 10% sodium hypochlorite overnight to remove residual tissue. Each nubbin was sliced vertically through the primary growth axis. Linear extension above the alizarin red mark was measured under a microscope. A piece (surface area: approx. 2 cm2) of the coral skeleton was cut from the top of the alizarin red mark to the top of the coral, and its volume was calculated following the procedure of Smith et al. [30] to determine the bulk density using the buoyant weight method [31]. The annual calcification rate (g cm−2 year−1) was calculated as the product of linear extension (cm year−1) and density (g cm−3).
(e) Tissue analysis
Symbiodiniaceae concentrations were determined in triplicate with a hemocytometer and symbiont counts were normalized to skeleton surface area (Symbiodiniaceae cells cm−2). Chlorophyll a was extracted in 90% acetone and concentration was measured with a spectrophotometer (Genesys 10s UV–VIS, ThermoScientific), calculated with equations in Jeffrey & Humphrey [32], and the chlorophyll a concentrations were then divided by Symbiodiniaceae cell concentrations (μg cell−1). Protein concentration was determined with a Nanodrop 2000 spectrophotometer and then divided by skeleton surface area (mg cm−2).
(f) Statistical analysis
Statistical analyses were performed with R v. 3.4.3 [33] and plots were made with the ‘ggplot2’ package in R [34]. The ‘survival’ package [35] was used to plot Kaplan–Meier survival curves and Mantel–Cox log-rank tests were used for statistical comparisons among survival curves. Mann–Whitney U non-parametric tests were used when comparing two groups (i.e. transplantation sites) and Kruskal–Wallis non-parametric tests for comparing three groups (i.e. coral origins) followed by pairwise Mann–Whitney Upost hoc tests. Non-parametric tests were used after visual assessment of normality with histograms and Q–Q plots.
3. Results
(a) Water chemistry
Total alkalinity and DIC were higher at the ojo than at the control site (total alkalinity: Mann–Whitney U, W = 244, p < 0.001; DIC: W = 252, p < 0.001) (table 1). Average total alkalinity was 2759 µmol kg−1 at the ojo site and 2365 µmol kg−1 at the control site and average DIC was 2621 µmol kg−1 at the ojo and 2019 µmol kg−1 at the control site. Salinity and calculated Ωarag and pH were lower at the ojo than at the control site (salinity: W = 6, p < 0.001; Ωarag: W = 32, p < 0.01; pH: W = 50, p < 0.01). The average salinity, Ωarag and pH were 33.3, 2.10 and 7.70, respectively, at the ojo site and 35.6, 3.53 and 8.17 at the control site. Temperature fluctuated throughout the experiment but did not differ among transplantation sites (approx. 27°C ± 0.3 s.e.; W = 122, p = 0.676). The temperature, pH and conductivity data recorded by the SeapHOx sensors were within the range of values measured in our discreet samples. These data were used to confirm that our spot analyses are representative, but were not used to calculate Ωarag since total alkalinity and DIC data were not available.
| transplant site | N | alkalinity (μmol kg−1) | DIC (μmol kg−1) | pHa | Ωaraga | Temperature (°C) | Salinity |
|---|---|---|---|---|---|---|---|
| control | 15 | 2365 ± 32 | 2019 ± 12 | 8.17 ± 0.07 | 3.53 ± 0.43 | 26.9 ± 0.3 | 35.6 ± 0.1 |
| ojo | 17 | 2759 ± 104 | 2621 ± 93 | 7.70 ± 0.14 | 2.10 ± 0.35 | 27.1 ± 0.2 | 33.2 ± 0.5 |
(b) Survival
Two years after transplantation, the survival of P. astreoides nubbins transplanted to the ojo was lower (60%) than those transplanted to the control site (90%) (log-rank test: χ2 = 4.1, d.f. = 1, p = 0.042; figure 2; electronic supplementary material, table S3). The survival of P. astreoides nubbins originating from ojos was qualitatively lower (65%) than those originated from control sites (85%), although the survival curves did not differ significantly (χ2 = 2.2, d.f. = 1, p = 0.141). S. siderea survival was similar among transplantation sites (control: 96%; ojo: 86.2%; log-rank test: χ2 = 2, d.f. = 1, p = 0.16), but survival of nubbins originating from the reef was marginally lower (80%) than those originating from ojos (100%) and controls (94%) (χ2 = 5.6, d.f. = 2, p = 0.062). All P. porites nubbins originated from the reef, and their survival at the ojo transplantation site was significantly lower (33%) than those at the control site (80%), but their survival curves were not different (χ2 = 2.9, d.f. = 1, p = 0.087).
Figure 2. Survival curves of nubbins over 24 months after transplanting into (a) ambient Ωarag control site and (b) low Ωarag ojo: Porites astreoides (n = 40), Siderastrea siderea (n = 58) and Porites porites (n = 19). Solid and dashed lines indicate collection origins of the corals.
(c) Density
The skeletal density of corals transplanted to the ojo was lower than that of corals transplanted to the control site for all three species (figure 3a; electronic supplementary material, table S3). The median density of coral skeletons transplanted to ojo and control sites, respectively, was 1.10 g cm−3 ± 0.03 s.e. and 1.58 g cm−3 ± 0.02 s.e. for P. astreoides, (Mann–Whitney U: W = 150, p < 0.001); 1.38 g cm−3 ± 0.03 s.e. and 1.63 g cm−3 ± 0.02 s.e. for S. siderea (W = 250, p < 0.001); and 1.29 g cm−3 ± 0.07 s.e. and 1.72 g cm−3 ± 0.05 s.e. for P. porites (W = 20, p = 0.033). Skeletal density of P. astreoides originating from ojos and control sites was similar (W = 85, p = 0.728). Skeletal density of S. siderea differed based on nubbin origin (Kruskal–Wallis: H = 7.783, d.f. = 2, p = 0.020). Density of S. siderea nubbins originating from ojos was lower than that of nubbins originating from the reef (p = 0.017) but was not different than nubbins originating from control sites (p = 0.163). Density of S. siderea nubbins originating from control sites and from the reef did not differ (p = 0.508).
Figure 3. (a) Bulk density, (b) linear extension and (c) calcification rates of skeletons deposited during the two years after transplantation. Symbols indicate collection origins. Note the different ranges on y-axes. Data are mean ± s.e. Letters indicate overall comparisons of origin (O) and transplantation (T). Asterisks indicate statistical significance at *p < 0.05, **p < 0.01 and ***p < 0.001.
(d) Linear extension
Linear extension of P. astreoides did not vary among transplantation sites (Mann–Whitney U: W = 59.5, p = 0.079) or origins (W = 77, p = 0.245; figure 3b; electronic supplementary material, table S3). S. siderea linear extension did not vary among transplantation sites (W = 257, p = 0.302) but varied based on nubbin origin (Kruskal–Wallis: H = 16.679, d.f. = 2, p < 0.001). Linear extension of S. siderea nubbins originating from the reef was higher (0.31 cm year−1 ± 0.02 s.e.) than nubbins originating either from control (0.19 cm year−1 ± 0.02 s.e., p = 0.004) or ojo sites (0.16 cm year−1 ± 0.01 s.e., p < 0.001). Linear extension of P. porites nubbins transplanted to the ojo was half that of nubbins transplanted to the control site (W = 21, p = 0.017).
(e) Calcification
P. astreoides calcification did not differ among sites (Mann–Whitney U: W = 72, p = 0.815) or origins (W = 46, p = 0.143; figure 3c; electronic supplementary material, table S3). Calcification rates of S. siderea also did not vary with transplantation site (W = 144, p = 0.762), but they did differ with nubbin origin (Kruskal–Wallis: H = 15.113, d.f. = 2, p < 0.001). Calcification of S. siderea nubbins originated from the reef was almost double those from ojo sites (p < 0.001), and approximately 35% more than nubbins originated from control sites (p = 0.058). The calcification rate of P. porites was approximately 66% lower at the ojo than at the control site (W = 21, p = 0.017).
(f) Symbiodiniaceae concentration
Symbiodiniaceae concentration per surface area of S. siderea was higher at the ojo (median: 1.26 × 107 cell cm−2 ± 3.6 × 106 s.e.) than at the control site (2.50 × 106 cell cm−2 ± 1.8 × 106 s.e., Mann–Whitney U: W = 75, p < 0.001; figure 4a; electronic supplementary material, table S4). Concentrations at the ojo were higher for P. astreoides and P. porites but the difference between transplantation sites for either P. astreoides (W = 52, p = 0.183) or P. porites (W = 4, p = 0.857) was not statistically significant. No coral species differed in Symbiodiniaceae concentration based on collection origin (P. astreoides: W = 73, p = 0.81; S. siderea: Kruskal–Wallis, H = 2.469, d.f. = 2, p = 0.291).
Figure 4. (a) Symbiodiniaceae, (b) chlorophyll a and (c) protein concentrations of surviving coral nubbins two years after transplantation at ambient Ωarag control and low Ωarag ojo sites. Data are mean ± s.e. Letters and significance values are denoted as in figure 3.
(g) Chlorophyll a concentration
Chlorophyll a concentrations per Symbiodiniaceae (μg per Symbiodiniaceae cell) of both P. astreoides and S. siderea were higher at the ojo than at the control site (P. astreoides: Mann–Whitney U, W = 15, p < 0.001; S. siderea: W = 58, p < 0.001; figure 4b; electronic supplementary material, table S4). Chlorophyll a concentration per Symbiodiniaceae of P. astreoides and S. siderea did not differ based on origins (P. astreoides: W = 98, p = 0.719; S. siderea: Kruskal–Wallis, H = 4.135, d.f. = 2, p = 0.126). Chlorophyll a concentration per Symbiodiniaceae of P. porites was higher at the ojo but the difference was not statistically significant among transplantation sites (W = 4, p = 0.262).
(h) Protein concentration
The protein concentration (mg cm−2) of S. siderea nubbins transplanted to the ojo was twice that of nubbins transplanted to the control (Mann–Whitney U: W = 119, p = 0.006; figure 4c; electronic supplementary material, table S4), but differences were not statistically significant among transplantation sites for either P. astreoides (W = 75, p = 0.936) or P. porites (W = 7, p = 0.571). Protein concentration did not differ among nubbin origins for P. astreoides (W = 98, p = 0.267) or S. siderea (Kruskal–Wallis, H = 4.807, d.f. = 2, p = 0.090).
4. Discussion
This study demonstrated that after 2 years of in situ transplantation, three Caribbean coral species (Porites astreoides, Siderastrea siderea and Porites porites) were able to survive and calcify at very low Ωarag; however, their skeletal density decreased while net linear extension and calcification rates were maintained. S. siderea nubbins had the highest survival and responded to low Ωarag by increasing the concentration of Symbiodiniaceae, chlorophyll a and protein.
(a) Survival of slow-growing corals was higher than fast-growing corals transplanted to low Ωarag
The survival of slow-growing massive P. astreoides and S. siderea was higher at low Ωarag than faster-growing branching P. porites (figure 2), indicating a species-specific tolerance to low Ωarag water discharging at the ojo. This is consistent with the coral assemblages naturally found at our study site: massive colonies of P. astreoides and S siderea are abundant at low Ωarag ojos, the only branching species found at the ojos is P. divaricata and it is present in very low numbers, and branching P. porites is absent [12]. Similarly, massive Porites corals were twice as abundant, while the abundance of structurally complex (e.g. branching) corals was a third lower at high pCO2 volcanic seeps than at ambient Ωarag sites in Papua New Guinea [11], and massive Pavonid corals were least sensitive to acidification in Panama [36]. While these results suggest massive corals have an advantage over branching corals at low Ωarag sites, this may be attributed to differential growth rates rather than morphologies, since morphology was found to be unrelated to calcification of corals experimentally incubated at high pCO2 [37,38]. Fast-growing corals may be more affected by low Ωarag because their rapid calcification makes them more sensitive to low carbonate ion availability [8] and requires them to remove protons from the calcification site fast enough to maintain an adequate inner pH [37], with a concomitant increased energy demand.
(b) Skeletal density was lower at the low Ωarag transplantation site
While calcification rates were not consistently lower at the ojo transplantation site, the skeletal density for all species was 15–30% lower. This suggests these corals maintained their linear extension at the expense of density (figure 3). Linear extension is inversely correlated with density because a faster extension rate results in less time for skeleton thickening [39]. Phenotypically plastic skeletons have been described in many corals under a variety of environmental factors, with high-density skeletons associated with high Ωarag [40], high temperature [41], low cloud coverage and rainfall [42], low turbidity and sediment load [43] and high hydraulic energy [30]. In field studies, several environmental variables often covary and isolating the effect of a single environmental factor is challenging. In our experiment, most parameters except carbonate chemistry were similar at both transplantation sites, which emphasizes the role of low Ωarag in reducing density. Similar density and porosity differences occur naturally in P. astreoides sampled at ojos and control sites as measured with computerized tomography [19], suggesting that the differences in our study were not artefacts of the transplantation process, and that corals experiencing low Ωarag conditions for their entire lives do not achieve the skeletal densities of their counterparts in ambient Ωarag water. Field and laboratory studies collectively indicate that coral growth at low Ωarag waters usually results in precipitation of lower density skeletons [19,40,44,45]. Our data show that when moved to a more favourable environment, the corals can acclimatize and increase their skeletal density.
Decoupling extension and density, and the processes that control each, will increase our understanding of coral calcification and potential acclimatization in low Ωarag waters. Neither calcification rate nor skeletal growth alone fully reflects the effects of low Ωarag on the coral skeleton; it is necessary to consider density, linear extension and calcification rate together [44,45] to avoid conflicting results on the effects of ocean acidification on calcification.
Although all the S. siderea nubbins originating from the ojos survived the 2-year transplantation experiment, their skeletal density, linear extension and calcification rates were lower than that of nubbins originating from the reef site. It is possible that the early life history of corals is affected by low pH (e.g. post settlement growth) [46], impacting the ability of S. siderea originating from the ojos to respond to changing conditions later in life, potentially reflecting poor overall health state for corals that were obtained from sites that have less than optimal growth conditions, impairing their ability to overcome further stress. It is also possible that the populations have been physically isolated for an extended time allowing some genetic divergence. Indeed, a recent study [47] reported intra-specific variability of calcification rates of Acropora digitifera originating from two distinct locations after exposure to high CO2 in a laboratory experiment, suggesting different populations of the same coral species have different susceptibility to ocean acidification.
(c) Concentrations of symbiodiniaceae, chlorophyll a and proteins were higher at the low Ωarag ojo transplantation site
The higher concentrations of Symbiodiniaceae, chlorophyll a and tissue protein of S. siderea transplanted to the ojo (figure 4) may be responsible for its ability to survive and calcify at low Ωarag. Calcification requires transport of carbonate and calcium ions and proton removal from the extracellular calcifying medium to maintain a high Ωarag at the calcification site [48]. If the external seawater has a lower Ωarag, the coral may have to expend more energy for raising the internal Ωarag to promote calcification [49]. Tropical corals obtain the energy required to move these ions through heterotrophy and symbiotic algal photosynthesis. Although feeding rates were not measured in this study, corals can modify their heterotrophic feeding to increase their energy budget under low Ωarag conditions [49]; nevertheless, changes in heterotrophy are species-specific [50]. It is possible that nubbins transplanted to the low Ωarag ojo enhanced symbiont concentrations that provided more energy resources needed to cope with the greater difference between the external and internal carbonate chemistry. Indeed, the higher symbiont concentrations may have allowed S. siderea nubbins transplanted to the ojo to maintain calcification rates similar to those of nubbins transplanted to the control site, as observed in laboratory experiments [7,29,45]. It is also possible that photosynthates derived from endolithic algae may promote calcification under low Ωarag as they could also provide similar photosynthates to corals at low Ωarag. Collectively, our data and data from previous research suggest that the energy provided by the symbionts can be used to overcome the larger gradient of proton and carbonate ion between the environment and the calcification solution in order to maintain net growth at least in some coral species.
The chlorophyll a concentration per Symbiodiniaceae cell of P. astreoides and S. siderea was higher after 2 years of transplantation at low Ωarag (figure 4b), which suggests an increased capacity for the photosynthetic activity that could provide additional energy to the corals. The increase in primary production may mean that more photosynthates are produced and assimilated by the host in such a manner that the coral can keep calcification rates under low Ωarag. Nevertheless, further research is needed to elucidate the effects of low pH on chlorophyll a concentrations and assess the effect of chlorophyll a concentrations on calcification, since several authors have reported mixed results in laboratory experiments with Stylophora pistillata [7,29,45]. It is possible that the increase in chlorophyll a concentration is due to an increase in cyanobacteria rather than Symbiodiniaceae; the cyanobacteria may promote photosynthesis through nitrogen fixation [51] and ultimately, provide the needed energetic resources to facilitate calcification under low Ωarag.
The protein content per surface area was higher in S. siderea nubbins transplanted to the ojo than those at the control site (figure 4c), suggesting that these corals may be thickening their organic matrix protein content to promote calcification under low Ωarag seawater [45]. Several experimental studies have also reported an increase in host tissue and organic matrix protein concentrations under reduced pH in several species [29,45]. While we did not measure tissue thickness, thicker tissue has been observed in low Ωarag corals at this field site [19] and has been proposed to confer an advantage against coral bleaching [52] and low pH [16], since it serves as a protective barrier against hot or corrosive seawater.
(d) Shifting species assemblages in an acidified ocean
The differential sensitivity across populations and species to low Ωarag suggest that, as ocean acidification progresses, the relative abundances of different coral species and populations in reef ecosystems may change towards the dominance of slow-growing species, and hence changes in coral communities and reef structure are also likely, with potential cascading effects. This finding is particularly critical for reefs currently dominated by fast-growing, branching species, such as Acropora and Stylophora pistillata in Indo-Pacific shallow reefs [53]. As sea level is expected to rise by 26 to 55 cm by 2100 (scenario RCP2.6 of IPCC), it is possible that coral reefs dominated by slow-growing species may not be able to grow fast enough to avoid drowning [54]. In addition, reduced skeletal density has been linked to increased bioerosion and boring [4,19,55] and low Ωarag waters also weaken cementation of reef structures, which further promotes coral erosion [56] and leads to less cohesive reef frameworks that are more susceptible to storms. Differences in fecundity and recruitment among species can also shape the reef's species assemblage. All three species used in this study brood larvae able to settle soon after release [57] which increases the likelihood that larvae may settle in parental habitats and which would be advantageous if selection among adults has favoured adaptations for low pH. In particular, P. astreoides has additional advantages: it is hermaphroditic with potentially high rates of self-fertilization [58] and also appears capable of producing parthenogenic or asexual larvae [59], all of which are mechanisms for propagating maternal genotypes. Furthermore, P. astreoides appears capable of adaptation to thermal stress [60] further enhancing its potential for greater abundance in a warmer and more acidified future.
In summary, while corals can calcify and grow under ocean acidification conditions, the possible synergistic effects of sea-level rise on slow-growing corals; high temperature on Symbiodiniaceae concentrations; high nutrient concentrations on skeletal bioerosion; or increased storm intensity on less dense coral skeletons predict a challenging future for coral survival and growth. On the other hand, the differences in survival and calcification among coral species may be useful for studies of human-assisted evolution projects [61] and implementation of restoration programmes as a strategy to augment the capacity of reef organisms to tolerate stress and to facilitate recovery after disturbances.
Data accessibility
Data are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.3pm80bp [62].
Authors' contributions
A.P. and D.C.P. jointly conceived and led this project and designed the experimental set-up. A.M., L.H., M.R.-V., A.P. and D.C.P. participated in the fieldwork and A.M. conducted the laboratory and data analyses. All authors contributed to the interpretation of the data. A.M. wrote the paper with contribution from all authors.
Competing interests
The authors declare they have no competing interests.
Funding
This research was funded by The National Geographic Explorer grant no. 9915-16 to A.P. and Lawson hydrology award, International Association of Geochemistry student research grant and Wells Fargo Coastal Sustainability fellowship to A.M. Corals were collected under the permit DGOPA.00153.170111.-0051 of Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA) and exported under the Convention on International Trade in Endangered Species (CITES) Permit MX52912.
Acknowledgements
The water sampling and coral health assessment by members of Centro de Investigación Científica de Yucatán and the laboratory work assistance of Eva Jason and Natascha Varona made this study possible. We thank Yuichiro Takeshita for fieldwork assistance and sensor deployment, and workers of Puerto Morelos National Marine Park and Rob Franks for technical assistance.
Footnotes
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