pH variability at volcanic CO₂ seeps regulates coral calcifying fluid chemistry

Abstract

Coral reefs are iconic ecosystems having immense ecological, economic and cultural value, but globally their carbonate-based skeletal construction is threatened by ocean acidification. Identifying coral species that have specialised mechanisms to maintain high rates of calcification in the face of declining seawater pH is of paramount importance to predicting future species composition, and growth of coral reefs. Here, we studied multiple coral species from two distinct volcanic CO2 seeps in Papua New Guinea to assess their capacity to control their calcifying fluid chemistry. Several coral species living under conditions of low mean seawater pH but with either low or high variability in seawater pH were examined and compared with those living under 'normal' (non-seep) ambient seawater pH. We show that when mean seawater pH is low but highly variable, corals have a greater ability to maintain constant pHcf in their calcifying fluid, but this characteristic was not linked with changes in abundance.Under less variable low seawater pH, corals with limited reductions in pHcf at the seep sites compared to controls tended to be more abundant at the seeps site than at the control site. However, this finding was strongly influenced by a single species (Montipora foliosa), able to maintain complete pHcf homeostasis. Overall, while our findings indicate that there might be an association between ecological success and greater pHcf homeostasis, further research with more species and at more sites with differing seawater pH regimes is required to solidify inferences regarding coral ecological success under future ocean acidification.

Corals adapted to extreme and fluctuating seawater pH increase calcification rates and have unique symbiont communities

“…Brown et al (2022) incubated coralPocillopora damicornis from both a flat and a sloping reef, where seawater pH variability differed, in aquaria with stable and variable pH. As in our study, they found higher rates of calcification for corals from a more variable environment, probably because they maintained less intracellular pH acidosis, as previously found for other corals (Comeau et al, 2022;Cornwall et al, 2018;Gibbin & Davy, 2014). Clearly, this compensatory mechanism might have a cost.…”

“…By assessing the holobiont physiological responses and the Symbiodiniaceae profiles of three coral species from both Bouraké and a Reference reef to a large range in pH, we found that corals from Bouraké constantly exhibited higher growth rates and had a specific and more consistent ITS2 majority sequence than corals from the Reference reef under low and variable pH conditions. It seems likely that such patterns were linked to the strong life-long environmental fluctuations, which might have promoted coral resilience as previously suggested (e.g., Brown et al, 2022;Comeau et al, 2022;Enochs et al, 2020;Rivest et al, 2017;Schoepf et al, 2020). We are aware that this study explored only a few of the compensatory mechanisms that might be at the origin of the resilience observed for corals from Bouraké.…”

“…These stressors are expected to exceed optimal levels for the good functioning of coral reefs as early as 2050 (Hoegh-Guldberg et al, 2017;IPCC Report, 2021), when most coral reefs are expected to dramatically decline. However, species-specific responses in the reefs' environment (Altieri et al, 2021;Comeau et al, 2022;Jury & Toonen, 2019;Rodolfo-Metalpa et al, 2011), and in vitro experiments (Comeau et al, 2019;Cornwall et al, 2018) have shown that some corals seem to be resilient to one stressor or to the combination of more stressors.…”

“…Among the most likely hypotheses to explain coral resilience to OA, is the phenomenon that corals chronically exposed to major environmental changes are more resilient to future changes (Comeau et al, 2022;Enochs et al, 2020;Schoepf et al, 2020). Possible mechanisms that could support resilience include physiological plasticity, epigenetics, and/or host microbiome shifts (Camp et al, 2017(Camp et al, , 2020Putnam et al, 2016;Ros et al, 2021;Voolstra & Ziegler, 2020), although coral response remains equivocal (Camp et al, 2016;Cornwall et al, 2018;Enochs et al, 2020;Rathbone et al, 2021;Rivest et al, 2017).…”

Proton gradients across the coral calcifying cell layer: Effects of light, ocean acidification and carbonate chemistry

“…Understanding how calicoblastic cells regulate pH in the context of their apical and basal microenvironments within the organism has profound implications for our understanding of how and why coral calcification responds to environmental variation. It is well known that ocean acidification (decreases in seawater pH due to oceanic uptake of man-made CO 2 ) drives down pH in the ECM of many coral species (Wall et al, 2016;Comeau et al, 2019;Venn et al, 2019;Comeau et al, 2022), but a clear physiological understanding of how and why pH ECM and intracellular pH (pH i ) of the calicoblastic epithelium responds to ocean acidification is lacking. Other changes in seawater carbonate chemistry also modulate pH ECM including variation in seawater dissolved inorganic carbon concentration [DIC] (Comeau et al, 2017;McCulloch et al, 2017) but the links between seawater carbonate chemistry and pH ECM are not fully understood.…”