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Exposure to high-frequency temperature variability often but not always enhances coral heat tolerance, raising the question of whether this depends on the type of variability regime and past vs. current exposure. We collected corals from a macrotidal, highly fluctuating temperature environment and preconditioned them to either constant or variable daily temperatures for ∼ 1.5 yr. Corals were then exposed to three new temperature variability regimes for ∼ 1 month (constant control, symmetric variability, and tidal variability) to assess the effect of short-term environmental history, followed by a 12-d heat stress test. Measurements of visual coral health, photophysiology, photosynthesis, respiration, and calcification rates showed that preconditioning to constant vs. variable temperatures for 1.5 yr did not significantly impact coral physiology and heat tolerance. In contrast, environmental history experienced in the month prior to the heat stress test significantly influenced the physiological responses, with corals exposed to both types of variability having lower heat tolerance. Interestingly, corals in the tidal variability regime suffered greater health declines than in the symmetric variability regime although both treatments had the same cumulative heat exposure. Since heating rate and temperature amplitude were higher in the tidal variability regime (but time spent above the bleaching threshold was shorter), this suggests that short, extreme heat pulses may be more deleterious than longer but more moderate ones, though other factors likely also played a role. Overall, our findings demonstrate that daily temperature variability has significant potential to alter coral heat tolerance but only certain types of variability may enhance coral adaptive capacity.

Ocean acidification (OA) is a pressing threat to reef-building corals, but it remains poorly understood how coral calcification is inhibited by OA and whether corals could acclimatize and/or adapt to OA. Using a novel geochemical approach, we reconstructed the carbonate chemistry of the calcifying fluid in two coral species using both a pH and dissolved inorganic carbon (DIC) proxy (δ11B and B/Ca, respectively). To address the potential for adaptive responses, both species were collected from two sites spanning a natural gradient in seawater pH and temperature, and then subjected to three pHT levels (8.04, 7.88, 7.71) crossed by two temperatures (control, +1.5°C) for 14 weeks. Corals from the site with naturally lower seawater pH calcified faster and maintained growth better under simulated OA than corals from the higher-pH site. This ability was consistently linked to higher pH yet lower DIC values in the calcifying fluid, suggesting that these differences are the result of long-term acclimatization and/or local adaptation to naturally lower seawater pH. Nevertheless, all corals elevated both pH and DIC significantly over seawater values, even under OA. This implies that high pH upregulation combined with moderate levels of DIC upregulation promote resistance and adaptive responses of coral calcification to OA.

Naturally extreme temperature environments can provide important insights into the processes underlying coral thermal tolerance. We determined the bleaching resistance of Acropora aspera and Dipsastraea sp. from both intertidal and subtidal environments of the naturally extreme Kimberley region in northwest Australia. Here tides of up to 10 m can cause aerial exposure of corals and temperatures as high as 37 °C that fluctuate daily by up to 7 °C. Control corals were maintained at ambient nearshore temperatures which varied diurnally by 4-5 °C, while treatment corals were exposed to similar diurnal variations and heat stress corresponding to ~20 degree heating days. All corals hosted Symbiodinium clade C independent of treatment or origin. Detailed physiological measurements showed that these corals were nevertheless highly sensitive to daily average temperatures exceeding their maximum monthly mean of ~31 °C by 1 °C for only a few days. Generally, Acropora was much more susceptible to bleaching than Dipsastraea and experienced up to 75% mortality, whereas all Dipsastraea survived. Furthermore, subtidal corals, which originated from a more thermally stable environment compared to intertidal corals, were more susceptible to bleaching. This demonstrates that while highly fluctuating temperatures enhance coral resilience to thermal stress, they do not provide immunity to extreme heat stress events.

Coral bleaching occurs when stressful conditions result in the expulsion of the algal partner from the coral. Before anthropogenic climate warming, such events were relatively rare, allowing for recovery of the reef between events. Hughes et al. looked at 100 reefs globally and found that the average interval between bleaching events is now less than half what it was before. Such narrow recovery windows do not allow for full recovery. Furthermore, warming events such as El Niño are warmer than previously, as are general ocean conditions. Such changes are likely to make it more and more difficult for reefs to recover between stressful events. Science , this issue p. 80 Coral reefs in the present day have less time than in earlier periods to recover from bleaching events. Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished steadily since 1980 and is now only 6 years. As global warming has progressed, tropical sea surface temperatures are warmer now during current La Niña conditions than they were during El Niño events three decades ago. Consequently, as we transition to the Anthropocene, coral bleaching is occurring more frequently in all El Niño–Southern Oscillation phases, increasing the likelihood of annual bleaching in the coming decades.

Ocean warming and acidification threaten the future growth of coral reefs. This is because the calcifying coral reef taxa that construct the calcium carbonate frameworks and cement the reef together are highly sensitive to ocean warming and acidification. However, the global-scale effects of ocean warming and acidification on rates of coral reef net carbonate production remain poorly constrained despite a wealth of studies assessing their effects on the calcification of individual organisms. Here, we present global estimates of projected future changes in coral reef net carbonate production under ocean warming and acidification. We apply a meta-analysis of responses of coral reef taxa calcification and bioerosion rates to predicted changes in coral cover driven by climate change to estimate the net carbonate production rates of 183 reefs worldwide by 2050 and 2100. We forecast mean global reef net carbonate production under representative concentration pathways (RCP) 2.6, 4.5, and 8.5 will decline by 76, 149, and 156%, respectively, by 2100. While 63% of reefs are projected to continue to accrete by 2100 under RCP2.6, 94% will be eroding by 2050 under RCP8.5, and no reefs will continue to accrete at rates matching projected sea level rise under RCP4.5 or 8.5 by 2100. Projected reduced coral cover due to bleaching events predominately drives these declines rather than the direct physiological impacts of ocean warming and acidification on calcification or bioerosion. Presently degraded reefs were also more sensitive in our analysis. These findings highlight the low likelihood that the world’s coral reefs will maintain their functional roles without near-term stabilization of atmospheric CO₂ emissions.

In 2015/16, a marine heatwave associated with a record El Niño led to the third global mass bleaching event documented to date. This event impacted coral reefs around the world, including in Western Australia (WA), although WA reefs had largely escaped bleaching during previous strong El Niño years. Coral health surveys were conducted during the austral summer of 2016 in four bioregions along the WA coast (~17 degrees of latitude), ranging from tropical to temperate locations. Here we report the first El Niño-related regional-scale mass bleaching event in WA. The heatwave primarily affected the macrotidal Kimberley region in northwest WA (~16°S), where 4.5–9.3 degree heating weeks (DHW) resulted in 56.6–80.6% bleaching, demonstrating that even heat-tolerant corals from naturally extreme, thermally variable reef environments are threatened by heatwaves. Some heat stress (2.4 DHW) and bleaching (<30%) also occurred at Rottnest Island (32°01’S), whereas coral communities at Ningaloo Reef (23°9’S) and Bremer Bay (34°25’S) were not impacted. The only other major mass bleaching in WA occurred during a strong La Niña event in 2010/11 and primarily affected reefs along the central-to-southern coast. This suggests that WA reefs are now at risk of severe bleaching during both El Niño and La Niña years.

Naturally heat-resistant coral populations hold significant potential for facilitating coral reef survival under rapid climate change. However, it remains poorly understood whether they can acclimatize to ocean warming when superimposed on their already thermally-extreme habitats. Furthermore, it is unknown whether they can maintain their heat tolerance upon larval dispersal or translocation to cooler reefs. We test this in a long-term mesocosm experiment using stress-resistant corals from thermally-extreme reefs in NW Australia. We show that these corals have a remarkable ability to maintain their heat tolerance and health despite acclimation to 3–6 °C cooler, more stable temperatures over 9 months. However, they are unable to increase their bleaching thresholds after 6-months acclimation to + 1 °C warming. This apparent rigidity in the thermal thresholds of even stress-resistant corals highlights the increasing vulnerability of corals to ocean warming, but provides a rationale for human-assisted migration to restore cooler, degraded reefs with corals from thermally-extreme reefs. Coral populations from thermally extreme conditions may help restore reefs degraded by bleaching. Here, the authors show that these corals can maintain their heat tolerance despite acclimation to colder temperatures but have a limited capacity to acclimatize to ocean warming.

As marine heatwaves increasingly threaten coral reefs worldwide, some extreme reef environments naturally expose corals to high-temperature fluctuations and can therefore provide important insights into the mechanisms underlying coral heat tolerance. Coral reefs in the Kimberley region in northwest Australia experience the world’s largest tropical tides and are therefore exposed to highly fluctuating temperatures in the intertidal. In contrast, the subtidal remains mostly submerged, resulting in moderate daily temperature fluctuations. A marine heatwave in 2016 triggered wide-spread bleaching in the Kimberley. Intertidal corals bleached less and recovered faster than adjacent subtidal corals; however, the mechanisms underlying this differential bleaching and recovery response remain poorly understood. Here we assessed both host- and symbiont-based indicators of bleaching resilience in the coral Acropora aspera. We tagged visibly healthy and bleached colonies from both environments in April 2016 and measured symbiont community composition, cell density, chlorophyll a, total biomass and host tissue energy reserves (lipids, protein and carbohydrates) during bleaching in April and in November 2016. Bleaching severity was higher in the subtidal than in intertidal, and while Cladocopium dominated all corals, symbiont community compositions differed significantly between environments and between bleached and healthy subtidal corals. Interestingly, bleaching resilience seemed decoupled from energy reserves, even though high levels of energy reserves and/or sufficient consumption during bleaching are widely thought to increase resistance to and recovery from bleaching. Although all bleached/recovered corals showed a general pattern of catabolizing protein reserves, distinct environment-specific trends were observed: subtidal corals that suffered extensive mortality also catabolized energy-poor carbohydrate reserves. In contrast, intertidal corals recovered rapidly after bleaching and maintained energy reserves. Total biomass remained unchanged between bleached and healthy corals in both environments. Overall, the findings of this study demonstrate that the consumption of energy reserves during bleaching is not always a reliable indicator of bleaching resilience.

Coral reefs are increasingly threatened by climate change, mass bleaching events and ocean acidification (OA). Coral calcification, a process that is critical to build and maintain the structure of tropical coral reefs, is highly sensitive to both warming and acidifying oceans. However, in contrast to the impacts of OA on coral calcification, significant knowledge gaps remain regarding how coral biomineralization mechanisms are impacted by heat stress and bleaching. Using a combined physiological and geochemical approach, we investigated how a marine heatwave impacted coral symbiotic status (chlorophyll a, algal symbiont density), the carbonate chemistry of the coral calcifying fluid (via δ11B and B/Ca) and skeletal trace element composition in the branching coral Acropora aspera. Importantly, we recorded in situ temperature throughout the bleaching event and recovery as well as coral symbiotic status during peak bleaching and after 7 months of recovery. We show that heat-stressed Acropora corals continued to upregulate the pH of their calcifying fluid (cf); however, dissolved inorganic carbon upregulation inside the cf was significantly disrupted by heat stress. Similarly, we observed suppression of the typical seasonality in the trace element (TE) temperature proxies Sr/Ca, Mg/Ca, Li/Ca and Li/Mg, indicating disruption of important calcification mechanisms, Rayleigh fractionation and reduced growth rates. Anomalies in TE/Ca ratios were still observed 7 months after peak bleaching, even though algal symbiont densities and chlorophyll a concentrations were fully restored at this point. Interestingly, the biomineralization response to heat stress did not differ between thermally distinct reef habitats harbouring coral populations with different heat tolerance, nor between heat-stressed colonies with different severity of bleaching. Our findings suggest that coral biomineralization mechanisms in Acropora are highly sensitive to heat stress, showing similar patterns of biogeochemical stress response as other coral taxa.

Coral reefs provide ecosystem benefits to millions of people but are threatened by rapid environmental change and ever-increasing human pressures. Restoration is becoming a priority strategy for coral reef conservation, yet implementation remains challenging and it is becoming increasingly apparent that indirect conservation and restoration approaches will not ensure the long-term sustainability of coral reefs. The important role of environmental conditions in restoration practice are currently undervalued, carrying substantial implications for restoration success. Giving paramount importance to environmental conditions, particularly during the pre-restoration planning phase, has the potential to bring about considerable improvements in coral reef restoration and innovation. This Essay argues that restoration risk may be reduced by adopting an environmentally aware perspective that gives historical, contemporary, and future context to restoration decisions. Such an approach will open up new restoration opportunities with improved sustainability that have the capacity to dynamically respond to environmental trajectories.