Potential local adaptation of corals at acidified and warmed Nikko Bay, Palau

Seawater surface pH (total scale), Ω_arag and temperatures (SST) showed a strong gradient at the entrance into the bay (Fig. 2a, b, e) and the seawater pH range (7.65–8.02) observed within the bay was equivalent to the ocean pH value from present to the value expected by the end of this century (IPCC 2013, RCP 8.5)²⁹. The mean daytime seawater temperature within the bay was significantly warmer (31.8 ± 0.6 °C, mean ± S.D.) and had lower pH (7.83 ± 0.06), lower Ω_arag, (2.44 ± 0.34) and higher pCO₂ (619 ± 104 μatm) compared to parameters outside the bay (30.4 ± 0.1 °C, 8.02 ± 0.02, 391 ± 31 μatm, 3.63 ± 0.14, Wilcoxon-test, p < 0.01, Tables S2), respectively. The seawater pH at Nikko Bay showed diurnal variation, ranging from 0.05 to 0.25, which was consistent with the range observed outside the bay (Fig. 1e, Table S2) and at other coral reefs³⁰. This contradicts with most conditions at CO₂ vents where the seawater pH is highly variable temporally^18,19,20. Average Chl-a and nutrient concentration values inside Nikko Bay were slightly but significantly higher than those outside the bay (Wilcoxon-test, p < 0.01, Fig. 2f–g, Table S1).

Daytime average total alkalinity (TA) and dissolved inorganic carbon (DIC) were significantly lower within the bay compared to outside the bay (Wilcoxon-test, p < 0.01, Fig. 2c, d, Table S2) and the TA-DIC diagram indicated that the low pH and high pCO₂ within Nikko Bay were mainly caused by low seawater TA due to calcification and by high DIC due to respiration (Fig. 3). By using the calculated mean water residence time within the bay (71 days¹²), mean net calcification (Gn) and net primary production (Pn) rates within the bay were calculated to be 22.7 mmol CaCO₃ m⁻² d⁻¹ and − 6.9 mmol C m⁻² d⁻¹. These values were lower than the net calcification rates found at most reefs³¹, however the positive net calcification at seawater Ω_arag of 2.44 within the bay contradicts with previous studies suggesting that coral reef formation is restricted to seawater Ω_arag higher than ca. 2.8 (pCO₂ lower than 560 μatm)³², and also with CO₂ seep studies indicating that reef development ceases where pH is lower than 7.7 (Ω_arag 2.1) in Papua New Guinea¹⁸, and lower than 7.9 in the Mariana Islands²⁰. When CO₂ gas exchange is considered, the heterotrophy of Nikko Bay becomes even higher. Although there are no wind speed data measured directly inside Nikko Bay, wind speed measured at PICRC station was 0.51 ± 0.80 m s⁻¹ (N = 4320) during this period, and wind can be expected to be weaker in Nikko Bay, which is surrounded by islands. Using the average pCO₂ of seawater in the bay (670 μatm, Table S2), atmospheric pCO₂ (390 μatm, calculated from mole fraction of CO₂ in dry air data collected at Guam), and gas exchange coefficient³³ utilized; gives the largest gas flux under this condition), the pCO₂ flux was calculated to be about 5.6 mmol m⁻² d⁻¹. Using this value, the Pn in Nikko Bay would be approximately -12.5 mmol m⁻² d⁻¹.

To evaluate the correlation among seawater carbonate chemistry and benthic community structure, six sites (N2-N7) along with the Ω_arag gradient (1.28–3.51) inside the bay and one site outside of Nikko Bay (N1) were selected for benthic community observation (Fig. 1, Table S3). Even though the seawater inside the bay was warmer and more acidified than the seawater outside the bay, hard coral coverage inside the bay (N2-N7) ranged from 34 to 82%, while the coverage at the N1 site outside the bay was 24% (Tables S4). There was no significant correlation between seawater Ω_arag and scleractinian hard coral cover (GLM, p = 0.97), CCA (GLM, p = 0.68), macroalgae, or seagrass coverage (GLM, p = 0.06, Fig. S1, Table S5). On the other hand, there was a significant increase in soft coral (= octocoral) coverage with an observed decrease of Ω_arag (GLM, p = 0.01), which follows previous results at a CO₂ vent at Iwotorishima in southern Japan showing high coverage of soft coral at a high pCO₂ site¹⁹. Turf algae coverage increased with Ω_arag (GLM, p = 0.04), contradicting previous observations at a CO₂ vent in the Mariana Islands²⁰ (Table S5, Fig. S1). In Nikko Bay, the coral community was found to differentiate along with the Ω_arag gradient observed from the outer reef to the inner reef area²³. Here we found that although coral coverage was not affected, the hard coral community structure showed differentiation among sites within the inner reef bay area, and this structure was mainly predicted by seawater Ω_arag, dissolved oxygen (DO), Chl-a, nitrate plus nitrite (NO₃⁻  + NO₂⁻) concentration, pCO₂ and temperature (Fig. 4, Table S6). Site N1 (outside of the bay) was characterized by high Ω_arag (3.51), low pCO₂ (395 μatm), low temperature (29. 3 °C), low Chl-a (0.55 μg/L), high DO (6.09 mg/L), and was dominated by Acropora spp. (coverage 16.5 ± 4.1%), while site N5 was characterized by low Ω_arag (1.28), high pCO₂ (1,305 μatm), high temperature (30.5 °C), high Chl-a (1.68 μg/L), low DO (4.52 mg/L), and was dominated by Merulinidae spp. (15.6 ± 5.2%, Fig. 4, Tables S3–S5). Both Acropora spp. and massive Porites showed a slight but positive correlation with seawater Ω_arag (GLM, p = 0.04, Fig. S1, Table S5), suggesting that species belonging to these genera are sensitive to OA, though other environmental factors may also have interactively affected the coverage of those species. Branching Porites (mainly consisting of Porites cylindrica) showed the highest coverage, accounting for 22 to 79% of hard coral cover inside the bay (Fig. 4g, Table S4), and there was no significant correlation with branching Porites spp. and Ω_arag (GLM, p = 0.16, Table S5. These results suggest that the high coral cover observed within Nikko Bay is related to the potential acclimatization or adaptation capacity of corals such as P. cylindrica to high pCO₂ (low Ω_arag) seawater.

To determine this possibility, colonies of P. cylindrica were reciprocally transplanted between two inner reef bays; a reference site at Malakal Bay (site M1) and a site in Nikko Bay (site N5, Fig. 1) that had different seawater temperatures and pCO₂ conditions (Table S7). As a result, it was found that while the calcification rate of P. cylindrica originating from M1 significantly decreased when transplanted to N5, the calcification rate of corals from N5 did not show significant differences when transplanted to either M1 and N5 (Fig. 5a, Table S8). Most previous tank experiments have reported a decrease of calcification rates of P. cylindrica at high pCO₂^34,35 or under high pCO₂ and high temperature conditions³⁶. Additionally, in contrast to massive Porites, P. cylindrica was found to have less capacity of up-regulating calicoblastic calcifying fluid pH, suggesting a high sensitivity to increases of seawater pCO₂³⁷. Additionally, the skeleton density of P. cylindrica did not show significant differences among sites (Fig. S2), again contradicting previous studies that showed lower skeleton densities of corals at a CO₂ vent³⁸ and naturally acidified sites³⁹. The net photosynthesis (Pn) rate of P. cylindrica transplanted to site N5 had a significantly higher value (p = 0.04) regardless of their origin (Fig. 5b, Table S8), which may be related to the slightly higher nutrient concentrations at N5 site (Table S7). Respiration (R) rates showed interactive effects among transplanted site and origin site, and the R rate of both M1 and N5 corals was significantly lower when transplanted to their origin site (Fig. 5c, Table S8). As a result, there were also interactive effects among the transplanted site and origin site with regards to gross photosynthesis (Pg):R, with higher values when transplanted to their original site (Fig. 5d, Table S8), indicating higher energy acquirement of corals at their own origin site. Interestingly, the corals Acropora pulchra, Porites lutea and Coelastrea aspera in a semi-enclosed lagoon of New Caledonia with low pH, high temperature, low oxygen conditions but high coral coverage, were found to exhibit lower calcification, higher respiration (R) and lower Pg:R compared to corals outside of the lagoon²⁵. Acclimatization of corals at the New Caledonia lagoon was suggested to be caused by high respiration through potentially high heterotrophy of corals within the lagoon, which has high organic carbon sedimentation²⁵. A comparatively high heterotrophy of the corals in Nikko Bay is also suggested as zooplankton abundance (particularly copepod abundance) was observed to be higher at site N5 compared to reference site M1 (Fig. 6), and this may partially alleviate the effects of high temperature and high CO₂ by enhancing their energy availability^40,41. However, taking into account that only the calcification rate of P. cylindrica at site M1 decreased when transplanted to site N5, potential epigenetic or genetic adaptation to the environmental conditions found within the bay appears to have occurred for Nikko Bay corals. This is also indicated by other findings that showed Pocillopora acuta within Nikko Bay had higher calcification rates when transplanted to their original site than out of the bay, while P. acuta from out of the bay were not able to survive when transplanted within the bay⁴².

P. cylindrica from N5 was also found to host two types of Cladocopium subclade C1⁴³ (former Symbiodinium ‘Clade C’), as well as Durusdinium⁴³ (former Symbiodinium ‘Clade D’), which are known to be tolerant to high temperatures⁴⁴, while P. cylindrica from the other sites only hosted Cladocopium subclade C1 (Fig. S3). These differences in Symbiodiniaceae, particularly at the most sheltered Nikko Bay site, may be another adaptation mechanism of corals to the environment found within Nikko Bay. However, molecular studies evaluating the potential genetic differentiation of those host corals within the bay are first needed before implying the occurrence of local adaptation. Thus, for further understanding, molecular studies evaluating the potential genetic differentiation of these host corals within the bay are essential in evaluating of the possibility of local adaptation.

From the present study, coral community structure was found to change according to the seawater environmental conditions within the bay, and corals living within the bay such as P. cylindrica could maintain their fitness in the warmed and acidified conditions found within the bay. However, interpretation of these results as related to future climate change should be taken carefully, as several other environmental factors including Chl-a, DO, inorganic nutrient concentrations, and light intensities also varied among sites. Additionally, corals within this bay have been suggested to have been continuously exposed to the unique environment within Nikko Bay for at least the past 150–500 years¹², while climate change is predicted to continue for the next few decades to centuries. Nevertheless, these results give important insights about the potential acclimatization and adaptation capacities of corals to different environmental conditions, even at small spatial scales, on coral reefs.

Source: Ecology - nature.com