Seawater surface pH (total scale), Ωarag and temperature (SST) showed a strong gradient at the entrance into the bay (Figs. 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)20. 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 Ωarag, (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 reefs21. This contradicts with most CO2 vents where the seawater pH is highly variable temporally14,15,16. Average chlorophyll-a (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, Figs. 2c, d, Table S2) and 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 days11), mean net calcification and net primary production (Pn) rates within the bay were calculated to be 22.7 mmol CaCO3 m− 2 d− 1 and − 6.9 C mmol m− 2 d− 1. This value was lower than the net calcification rate found at most reefs22, however the positive net calcification at seawater Ωarag of 2.44 within the bay contradicts with previous studies suggesting that coral reef formation is restricted to seawater Ωarag higher than ca. 2.8 (pCO2 lower than 560 µatm)23, and also with CO2 seep studies indicating that reef development ceases where pH is lower than 7.7 (Ωarag 2.1) in Papua New Guinea14, and lower than 7.9 in the Mariana Islands16.
To evaluate the correlation among seawater carbonate chemistry and benthic community structure, six sites (N2-N7) along with the Ωarag 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 Ωarag 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 Ωarag (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 site15. Turf algae coverage increased with Ωarag (GLM, p = 0.04), contradicting with previous observations at a CO2 vent in the Mariana Islands16 (Table S5, Fig. S1). In Nikko Bay, the coral community was found to differentiate along with the Ωarag gradient observed from the outer reef to the inner reef area19. 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 Ωarag, 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 Ωarag (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 Ωarag (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 Ωarag (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 Ωarag (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 Ωarag) 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) which had different seawater temperature 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 pCO224, 25 or high pCO2 and high temperature conditions26. Additionally, in contrast to massive Porites, P. cylindrica was found to have less capacity of up-regulating the calicoblastic calcifying fluid pH, suggesting a high sensitivity to increases of seawater pCO227. Additionally, the skeleton density of P. cylindrica did not show significant differences among sites (Fig. S2), again contradicting previous studies that showed lower skeleton density of corals at a CO2 vent28 and naturally acidified sites29. 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 concentration 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 lagoon30. 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 sedimentation30. 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 availability31,32. 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 rate 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 bay33.
P. cylindrica from N5 was also found to host two types of Cladocopium subclade C134 (former Symbiodinium ‘Clade C’), as well as Durusdinm34 (former Symbiodinium ‘Clade D’), which are known to be tolerant to high temperatures35, 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. However, for further understand, molecular studies evaluating the potential genetic differentiation of those host coral within the bay are essentially needed before evaluation for the local adaptation possibility.
From the present study, the 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 can maintain their fitness in the warmed and acidified conditions found within the bay. However, interpretation of these results to future climate change should be taken carefully, as several other environmental factors including Chl-a, DO, inorganic nutrient concentration and light intensity also varied among sites. Additionally, corals within this bay have been suggested to have been continuously exposed to the unique environment found within Nikko Bay for more than 5,000 years11, while climate change will occur within a few hundred years. Nevertheless, these results give important insights about the potential acclimatization and adaptation capacity of corals to different environmental conditions, even at small spatial scales, on coral reefs.