Impact of seawater acidification on pH at the tissue-skeleton interface and calcification in reef corals

Abstract

Insight into the response of reef corals and other major marine calcifiers to ocean acidification is limited by a lack of knowledge about how seawater pH and carbonate chemistry impact the physiological processes that drive biomineralization. Ocean acidification is proposed to reduce calcification rates in corals by causing declines in internal pH at the calcifying tissue-skeleton interface where biomineralization takes place. Here, we performed an in vivo study on how partial-pressure CO(2)-driven seawater acidification impacts intracellular pH in coral calcifying cells and extracellular pH in the fluid at the tissue-skeleton interface [subcalicoblastic medium (SCM)] in the coral Stylophora pistillata. We also measured calcification in corals grown under the same conditions of seawater acidification by measuring lateral growth of colonies and growth of aragonite crystals under the calcifying tissue. Our findings confirm that seawater acidification decreases pH of the SCM, but this decrease is gradual relative to the surrounding seawater, leading to an increasing pH gradient between the SCM and seawater. Reductions in calcification rate, both at the level of crystals and whole colonies, were only observed in our lowest pH treatment when pH was significantly depressed in the calcifying cells in addition to the SCM. Overall, our findings suggest that reef corals may mitigate the effects of seawater acidification by regulating pH in the SCM, but they also highlight the role of calcifying cell pH homeostasis in determining the response of reef corals to changes in external seawater pH and carbonate chemistry.

Fig. 1.

The impact of CO₂-driven seawater acidification on pH at the tissue–skeleton interface in S. pistillata in samples exposed to experimental treatments in Table 1 for >1 y. (A) pH in the subcalicoblastic medium (pH_SCM, solid line) and pH of the treatment seawater (SWpH, dashed line). (B) Intracellular pH in the calicoblastic epithelium (pH_CE, solid line) and pH of the treatment seawater (SWpH, dashed line). Plotted values represent pH (mean ± SE, for pH_SCM n = 5 colonies, for pH_CE n = 4 colonies) determined on the NBS scale. Asterisk (*) indicates pH values significantly different to treatment 4, pH 8.0.

Fig. 2.

(A) Merged confocal and transmitted light image of an aragonite crystal under the calicoblastic epithelium marked with calcein (green) at time 0 and allowed to grow for 4 h in treatment 4, pH 8.0 (treatment details given in Table 1). (B) The same image as A with the original cross-sectional area of crystal highlighted in yellow (t = 0) and new growth measured at t = 4 h highlighted in blue. Green line gives position of calcein band. (C) Percentage increase in a cross-sectional area of crystals in coral colonies in the four pH treatments (mean ± SE, n = 5 colonies). (D) Increase in surface area of whole coral colonies grown on glass slides for 2 mo in the four pH treatments (mean ± SE, n = 9 colonies). Asterisk (*) indicates mean values significantly different to treatment 4, pH 8.

Fig. 3.

Rates of proton removal and calcification in two models that explored mechanisms leading to changes in pH_SCM. (A) Model 1 assumes a fixed rate of proton removal from the subcalicoblastic medium and predicts a steady decline in calcification. (B) Model 2 is set with our observed relative rates of crystal growth (Fig. 2C) and predicts a decline in proton removal rate in treatment 1 (pH 7.2). Both models were set with our pH_SCM data. See Discussion for details.