Tolerance to a highly variable environment does not infer resilience to future ocean warming and acidification in a branching coral

Abstract

Coral populations from reef habitats that experience extreme daily abiotic fluctuations have been suggested as candidates to survive and proliferate under future climate change. Few studies, however, have exposed corals from dynamic environments to the synergistic effects of ocean warming and acidification to investigate whether tolerance of present‐day environmental variability is maintained under future climate stress. This study assessed the impact of RCP2.6 (+0.8°C and +25 ppm) and RCP4.5 (+1.3°C and +66 ppm) ocean warming and acidification on the survivorship, primary calcification (i.e., extension), secondary calcification (i.e., densification), and protein densities of Isopora palifera originating from two distinct reef habitats (abiotically variable reef flat vs. stable reef slope) over 9 weeks. Temperature and pCO2 were offset from a reef slope baseline temperature of 26.0°C ± 0.6°C and pCO2 concentration of 559 ± 56 ppm, incorporating natural diurnal variability. A trade‐off was observed in I. palifera originating from the reef flat, which significantly increased tissue protein densities but reduced densification relative to corals from the reef slope. Survivorship nor extension rates differed between corals originating from the variable or stable reef habitats. Mortality increased under RCP4.5 as extension rates increased, indicating that energetic investment in skeletal expansion becomes unsustainable under future climate stress. Increasing temperature and CO2 reduced calcification rates irrespective of the corals originating reef habitat suggesting with future climate change, exposure to greater environmental variability may not benefit coral calcification. These results demonstrate that tolerance to present‐day abiotic variability does not necessarily infer resilience to moderate future ocean warming and acidification conditions.

Environmental memory gained from exposure to extreme pCO2variability promotes coral cellular acid–base homeostasis

“…storms, marine heatwaves). Furthermore, as ocean warming and acidification intensify, corals will be pushed to the edge of their physiological limits, with tolerance to present-day variability not necessarily conferring resilience to future ocean warming and acidification [ 9 , 11 ]. While more research is needed to determine how long it takes to acquire resistance to acidification stress, it is evident from this study that P. damicornis native to stable environments cannot acclimatize to extreme pCO 2 oscillations conditions over relatively short time scales.…”

“…This study focused on two distinct habitats, the reef flat (North Beach) and reef slope (North Bommie) ( figure 1 ). Semidiurnal tidal fluctuations on the reef flat result in higher variability in temperature and CO 2 compared to reef slope habitats, and exposes reef flat corals to extreme temperature and CO 2 conditions projected for future reefs [ 11 , 12 , 20 ] ( figure 1 ; electronic supplementary material, figure S1). In-field measurements (temperature, photosynthetically active radiation (PAR) and nutrients) were recorded concurrently with the manipulative experiment at the same locations where corals were collected (8 January to 18 March 2021), whereas pCO 2 was recorded over the same season, but in 2016 (8 January to 18 March 2016; electronic supplementary material, Methods).…”

“…R. Soc. B 289: 20220941 temperature and CO 2 conditions projected for future reefs [11,12,20] (figure 1; electronic supplementary material, figure S1). In-field measurements (temperature, photosynthetically active radiation (PAR) and nutrients) were recorded concurrently with the manipulative experiment at the same locations where corals were collected (8 January to 18 March 2021), whereas pCO 2 was recorded over the same season, but in 2016 (8 January to 18 March 2016; electronic supplementary material, Methods).…”

“…Naturally variable habitats provide a glimmer of hope that climate-resilient coral populations already exist on coral reefs worldwide. Variable habitats or extreme environments, such as tidally dominated back reefs and reef flats, expose organisms to short-term fluctuations in temperature and pH conditions similar to those projected for future reefs [6,[9][10][11][12]. There is evidence that exposure to high diel temperature variability can promote resilience to temperature stress via holobiont adaptation or non-genetic mechanisms such as acclimatization through 'environmental memory', stress-tolerant endosymbiont communities (Symbiodiniaceae) and/or changes in gene expression [13][14][15].…”

Fine-scale heterogeneity reveals disproportionate thermal stress and coral mortality in thermally variable reef habitats during a marine heatwave

“…Individual reef systems are made up of interconnected geomorphological zones that are characterized by distinct diel and seasonal fluctuations in multiple seawater physicochemical parameters (Phinn et al 2012;Brown et al 2018;Cyronak et al 2020). For example, reef flats and lagoons are subject to semidiurnal tidal oscillations, resulting in extreme short-term variability in temperature, pH, irradiance, and oxygen, whereas conditions on neighboring subtidal fore reefs and reef slopes are typically more stable (Oliver and Palumbi 2011;Schoepf et al 2020;Rathbone et al 2022). As such, the physicochemical conditions to which reef communities are exposed can vary dramatically across small spatial scales (Cyronak et al 2020;Reid et al 2020;Kekuewa et al 2021), often resulting in distinct benthic communities across habitats (Phinn et al 2012;Brown et al 2018;Roelfsema et al 2021).…”