Incorporating adaptive responses into future projections of coral bleaching

Climate warming threatens to increase mass coral bleaching events, and several studies have projected the demise of tropical coral reefs this century. However, recent evidence indicates corals may be able to respond to thermal stress though adaptive processes (e.g., genetic adaptation, acclimatization, and symbiont shuffling). How these mechanisms might influence warming‐induced bleaching remains largely unknown. This study compared how different adaptive processes could affect coral bleaching projections. We used the latest bias‐corrected global sea surface temperature (SST) output from the NOAA/GFDL Earth System Model 2 (ESM2M) for the preindustrial period through 2100 to project coral bleaching trajectories. Initial results showed that, in the absence of adaptive processes, application of a preindustrial climatology to the NOAA Coral Reef Watch bleaching prediction method overpredicts the present‐day bleaching frequency. This suggests that corals may have already responded adaptively to some warming over the industrial period. We then modified the prediction method so that the bleaching threshold either permanently increased in response to thermal history (e.g., simulating directional genetic selection) or temporarily increased for 2–10 years in response to a bleaching event (e.g., simulating symbiont shuffling). A bleaching threshold that changes relative to the preceding 60 years of thermal history reduced the frequency of mass bleaching events by 20–80% compared with the ‘no adaptive response’ prediction model by 2100, depending on the emissions scenario. When both types of adaptive responses were applied, up to 14% more reef cells avoided high‐frequency bleaching by 2100. However, temporary increases in bleaching thresholds alone only delayed the occurrence of high‐frequency bleaching by ca. 10 years in all but the lowest emissions scenario. Future research should test the rate and limit of different adaptive responses for coral species across latitudes and ocean basins to determine if and how much corals can respond to increasing thermal stress.     

Opposite latitudinal gradients in projected ocean acidification and bleaching impacts on coral reefs

Coral reefs and the services they provide are seriously threatened by ocean acidification and climate change impacts like coral bleaching. Here, we present updated global projections for these key threats to coral reefs based on ensembles of IPCC AR5 climate models using the new Representative Concentration Pathway (RCP) experiments. For all tropical reef locations, we project absolute and percentage changes in aragonite saturation state (Ωarag) for the period between 2006 and the onset of annual severe bleaching (thermal stress >8 degree heating weeks); a point at which it is difficult to believe reefs can persist as we know them. Severe annual bleaching is projected to start 10–15 years later at high‐latitude reefs than for reefs in low latitudes under RCP8.5. In these 10–15 years, Ωarag keeps declining and thus any benefits for high‐latitude reefs of later onset of annual bleaching may be negated by the effects of acidification. There are no long‐term refugia from the effects of both acidification and bleaching. Of all reef locations, 90% are projected to experience severe bleaching annually by 2055. Furthermore, 5% declines in calcification are projected for all reef locations by 2034 under RCP8.5, assuming a 15% decline in calcification per unit of Ωarag. Drastic emissions cuts, such as those represented by RCP6.0, result in an average year for the onset of annual severe bleaching that is ~20 years later (2062 vs. 2044). However, global emissions are tracking above the current worst‐case scenario devised by the scientific community, as has happened in previous generations of emission scenarios. The projections here for conditions on coral reefs are dire, but provide the most up‐to‐date assessment of what the changing climate and ocean acidification mean for the persistence of coral reefs.     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light‐dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching‐related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30–75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.     

Forecasted coral reef decline in marine biodiversity hotspots under climate change

Coral bleaching events threaten coral reef habitats globally and cause severe declines of local biodiversity and productivity. Related to high sea surface temperatures (SST), bleaching events are expected to increase as a consequence of future global warming. However, response to climate change is still uncertain as future low‐latitude climatic conditions have no present‐day analogue. Sea surface temperatures during the Eocene epoch were warmer than forecasted changes for the coming century, and distributions of corals during the Eocene may help to inform models forecasting the future of coral reefs. We coupled contemporary and Eocene coral occurrences with information on their respective climatic conditions to model the thermal niche of coral reefs and its potential response to projected climate change. We found that under the RCP8.5 climate change scenario, the global suitability for coral reefs may increase up to 16% by 2100, mostly due to improved suitability of higher latitudes. In contrast, in its current range, coral reef suitability may decrease up to 46% by 2100. Reduction in thermal suitability will be most severe in biodiversity hotspots, especially in the Indo‐Australian Archipelago. Our results suggest that many contemporary hotspots for coral reefs, including those that have been refugia in the past, spatially mismatch with future suitable areas for coral reefs posing challenges to conservation actions under climate change.     

The dynamics of architectural complexity on coral reefs under climate change

One striking feature of coral reef ecosystems is the complex benthic architecture which supports diverse and abundant fauna, particularly of reef fish. Reef‐building corals are in decline worldwide, with a corresponding loss of live coral cover resulting in a loss of architectural complexity. Understanding the dynamics of the reef architecture is therefore important to envision the ability of corals to maintain functional habitats in an era of climate change. Here, we develop a mechanistic model of reef topographical complexity for contemporary Caribbean reefs. The model describes the dynamics of corals and other benthic taxa under climate‐driven disturbances (hurricanes and coral bleaching). Corals have a simplified shape with explicit diameter and height, allowing species‐specific calculation of their colony surface and volume. Growth and the mechanical (hurricanes) and biological erosion (parrotfish) of carbonate skeletons are important in driving the pace of extension/reduction in the upper reef surface, the net outcome being quantified by a simple surface roughness index (reef rugosity). The model accurately simulated the decadal changes of coral cover observed in Cozumel (Mexico) between 1984 and 2008, and provided a realistic hindcast of coral colony‐scale (1–10 m) changing rugosity over the same period. We then projected future changes of Caribbean reef rugosity in response to global warming. Under severe and frequent thermal stress, the model predicted a dramatic loss of rugosity over the next two or three decades. Critically, reefs with managed parrotfish populations were able to delay the general loss of architectural complexity, as the benefits of grazing in maintaining living coral outweighed the bioerosion of dead coral skeletons. Overall, this model provides the first explicit projections of reef rugosity in a warming climate, and highlights the need of combining local (protecting and restoring high grazing) to global (mitigation of greenhouse gas emissions) interventions for the persistence of functional reef habitats.     

Climate‐change refugia: shading reef corals by turbidity

Coral reefs have recently experienced an unprecedented decline as the world's oceans continue to warm. Yet global climate models reveal a heterogeneously warming ocean, which has initiated a search for refuges, where corals may survive in the near future. We hypothesized that some turbid nearshore environments may act as climate‐change refuges, shading corals from the harmful interaction between high sea‐surface temperatures and high irradiance. We took a hierarchical Bayesian approach to determine the expected distribution of 12 coral species in the Indian and Pacific Oceans, between the latitudes 37°N and 37°S, under representative concentration pathway 8.5 (W m^?2) by 2100. The turbid nearshore refuges identified in this study were located between latitudes 20–30°N and 15–25°S, where there was a strong coupling between turbidity and tidal fluctuations. Our model predicts that turbidity will mitigate high temperature bleaching for 9% of shallow reef habitat (to 30 m depth) – habitat that was previously considered inhospitable under ocean warming. Our model also predicted that turbidity will protect some coral species more than others from climate‐change‐associated thermal stress. We also identified locations where consistently high turbidity will likely reduce irradiance to <250 μmol m^?2 s^?1, and predict that 16% of reef‐coral habitat ≤30 m will preclude coral growth and reef development. Thus, protecting the turbid nearshore refuges identified in this study, particularly in the northwestern Hawaiian Islands, the northern Philippines, the Ryukyu Islands (Japan), eastern Vietnam, western and eastern Australia, New Caledonia, the northern Red Sea, and the Arabian Gulf, should become part of a judicious global strategy for reef‐coral persistence under climate change.     

Coral reef resilience to thermal stress in the Eastern Tropical Pacific

Coral reefs worldwide are threatened by thermal stress caused by climate change. Especially devastating periods of coral loss frequently occur during El Niño‐Southern Oscillation (ENSO) events originating in the Eastern Tropical Pacific (ETP). El Niño‐induced thermal stress is considered the primary threat to ETP coral reefs. An increase in the frequency and intensity of ENSO events predicted in the coming decades threatens a pan‐tropical collapse of coral reefs. During the 1982–1983 El Niño, most reefs in the Galapagos Islands collapsed, and many more in the region were decimated by massive coral bleaching and mortality. However, after repeated thermal stress disturbances, such as those caused by the 1997–1998 El Niño, ETP corals reefs have demonstrated regional persistence and resiliency. Using a 44 year dataset (1970–2014) of live coral cover from the ETP, we assess whether ETP reefs exhibit the same decline as seen globally for other reefs. Also, we compare the ETP live coral cover rate of change with data from the maximum Degree Heating Weeks experienced by these reefs to assess the role of thermal stress on coral reef survival. We find that during the period 1970–2014, ETP coral cover exhibited temporary reductions following major ENSO events, but no overall decline. Further, we find that ETP reef recovery patterns allow coral to persist under these El Niño‐stressed conditions, often recovering from these events in 10–15 years. Accumulative heat stress explains 31% of the overall annual rate of change of living coral cover in the ETP. This suggests that ETP coral reefs have adapted to thermal extremes to date, and may have the ability to adapt to near‐term future climate‐change thermal anomalies. These findings for ETP reef resilience may provide general insights for the future of coral reef survival and recovery elsewhere under intensifying El Niño scenarios.     

Shifting paradigms in restoration of the world's coral reefs

Many ecosystems around the world are rapidly deteriorating due to both local and global pressures, and perhaps none so precipitously as coral reefs. Management of coral reefs through maintenance (e.g., marine‐protected areas, catchment management to improve water quality), restoration, as well as global and national governmental agreements to reduce greenhouse gas emissions (e.g., the 2015 Paris Agreement) is critical for the persistence of coral reefs. Despite these initiatives, the health and abundance of corals reefs are rapidly declining and other solutions will soon be required. We have recently discussed options for using assisted evolution (i.e., selective breeding, assisted gene flow, conditioning or epigenetic programming, and the manipulation of the coral microbiome) as a means to enhance environmental stress tolerance of corals and the success of coral reef restoration efforts. The 2014–2016 global coral bleaching event has sharpened the focus on such interventionist approaches. We highlight the necessity for consideration of alternative (e.g., hybrid) ecosystem states, discuss traits of resilient corals and coral reef ecosystems, and propose a decision tree for incorporating assisted evolution into restoration initiatives to enhance climate resilience of coral reefs.     

Coping with Commitment: Projected Thermal Stress on Coral Reefs under Different Future Scenarios

Background

Periods of anomalously warm ocean temperatures can lead to mass coral bleaching. Past studies have concluded that anthropogenic climate change may rapidly increase the frequency of these thermal stress events, leading to declines in coral cover, shifts in the composition of corals and other reef-dwelling organisms, and stress on the human populations who depend on coral reef ecosystems for food, income and shoreline protection. The ability of greenhouse gas mitigation to alter the near-term forecast for coral reefs is limited by the time lag between greenhouse gas emissions and the physical climate response.

Methodology/Principal Findings

This study uses observed sea surface temperatures and the results of global climate model forced with five different future emissions scenarios to evaluate the “committed warming” for coral reefs worldwide. The results show that the physical warming commitment from current accumulation of greenhouse gases in the atmosphere could cause over half of the world''s coral reefs to experience harmfully frequent (p≥0.2 year⁻¹) thermal stress by 2080. An additional “societal” warming commitment, caused by the time required to shift from a business-as-usual emissions trajectory to a 550 ppm CO₂ stabilization trajectory, may cause over 80% of the world''s coral reefs to experience harmfully frequent events by 2030. Thermal adaptation of 1.5°C would delay the thermal stress forecast by 50–80 years.

Conclusions/Significance

The results suggest that adaptation – via biological mechanisms, coral community shifts and/or management interventions – could provide time to change the trajectory of greenhouse gas emissions and possibly avoid the recurrence of harmfully frequent events at the majority (97%) of the world''s coral reefs this century. Without any thermal adaptation, atmospheric CO₂ concentrations may need to be stabilized below current levels to avoid the degradation of coral reef ecosystems from frequent thermal stress events.     

Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments

Studying the mechanisms that enable coral populations to inhabit spatially varying thermal environments can help evaluate how they will respond in time to the effects of global climate change and elucidate the evolutionary forces that enable or constrain adaptation. Inshore reefs in the Florida Keys experience higher temperatures than offshore reefs for prolonged periods during the summer. We conducted a common garden experiment with heat stress as our selective agent to test for local thermal adaptation in corals from inshore and offshore reefs. We show that inshore corals are more tolerant of a 6‐week temperature stress than offshore corals. Compared with inshore corals, offshore corals in the 31 °C treatment showed significantly elevated bleaching levels concomitant with a tendency towards reduced growth. In addition, dinoflagellate symbionts (Symbiodinium sp.) of offshore corals exhibited reduced photosynthetic efficiency. We did not detect differences in the frequencies of major (>5%) haplotypes comprising Symbiodinium communities hosted by inshore and offshore corals, nor did we observe frequency shifts (‘shuffling’) in response to thermal stress. Instead, coral host populations showed significant genetic divergence between inshore and offshore reefs, suggesting that in Porites astreoides, the coral host might play a prominent role in holobiont thermotolerance. Our results demonstrate that coral populations inhabiting reefs <10‐km apart can exhibit substantial differences in their physiological response to thermal stress, which could impact their population dynamics under climate change.     

Turbid reefs moderate coral bleaching under climate‐related temperature stress

Thermal‐stress events that cause coral bleaching and mortality have recently increased in frequency and severity. Yet few studies have explored conditions that moderate coral bleaching. Given that high light and high ocean temperature together cause coral bleaching, we explore whether corals at turbid localities, with reduced light, are less likely to bleach during thermal‐stress events than corals at other localities. We analyzed coral bleaching, temperature, and turbidity data from 3,694 sites worldwide with a Bayesian model and found that K_d490, a measurement positively related to turbidity, between 0.080 and 0.127 reduced coral bleaching during thermal‐stress events. Approximately 12% of the world's reefs exist within this “moderating turbidity” range, and 30% of reefs that have moderating turbidity are in the Coral Triangle. We suggest that these turbid nearshore environments may provide some refuge through climate change, but these reefs will need high conservation status to sustain them close to dense human populations.     

Resilience in reef‐building corals: The ecological and evolutionary importance of the host response to thermal stress

Coral reefs are under extreme threat due to a number of stressors, but temperature increases due to changing climate are the most severe. Rising ocean temperatures coupled with local extremes lead to extensive bleaching, where the coral‐algal symbiosis breaks down and corals may die, compromising the structure and function of reefs. Although the symbiotic nature of the coral colony has historically been a focus of research on coral resilience, the host itself is a foundational component in the response to thermal stress. Fixed effects in the coral host set trait baselines through evolutionary processes, acting on many loci of small effect to create mosaics of thermal tolerance across latitudes and individual coral reefs. These genomic differences can be strongly heritable, producing wide variation among clones of different genotypes or families of a specific larval cross. Phenotypic plasticity is overlaid on these baselines and a growing body of knowledge demonstrates the potential for acclimatization of reef‐building corals through a variety of mechanisms that promote resilience and stress tolerance. The long‐term persistence of coral reefs will require many of these mechanisms to adjust to warmer temperatures within a generation, bridging the gap to reproductive events that allow recombination of standing diversity and adaptive change. Business‐as‐usual climate scenarios will probably lead to the loss of some coral populations or species in the future, so the interaction between intragenerational effects and evolutionary pressure is critical for the survival of reefs.     

Coral bleaching patterns are the outcome of complex biological and environmental networking

Continued declines in coral reef health over the past three decades have been punctuated by severe mass coral bleaching‐induced mortality events that have grown in intensity and frequency under climate change. Intensive global research efforts have therefore persistently focused on bleaching phenomena to understand where corals bleach, when and why—resulting in a large—yet still somewhat patchy—knowledge base. Particularly catastrophic bleaching‐induced coral mortality events in the past 5 years have catalyzed calls for a more diverse set of reef management tools, extending far beyond climate mitigation and reef protection, to also include more aggressive interventions. However, the effectiveness of these various tools now rests on rapidly assimilating our knowledge base of coral bleaching into more integrated frameworks. Here, we consider how the past three decades of intensive coral bleaching research has established the basis for complex biological and environmental networks, which together regulate outcomes of bleaching severity. We discuss how we now have enough scaffold for conceptual biological and environmental frameworks underpinning bleaching susceptibility, but that new tools are urgently required to translate this to an operational system informing—and testing—bleaching outcomes. Specifically, adopting network models that can fully describe and predict metabolic functioning of coral holobionts, and how this functioning is regulated by complex doses and interactions among environmental factors. Identifying knowledge gaps limiting operation of such models is the logical step to immediately guide and prioritize future experiments and observations. We are at a time‐critical point where we can implement new capacity to resolve how coral bleaching patterns emerge from complex biological–environmental networks, and so more effectively inform rapidly evolving ecological management and social adaptation frameworks aimed at securing the future of coral reefs.     

Resistance to thermal stress in corals without changes in symbiont composition

Discovering how corals can adjust their thermal sensitivity in the context of global climate change is important in understanding the long-term persistence of coral reefs. In this study, we showed that short-term preconditioning to higher temperatures, 3°C below the experimentally determined bleaching threshold, for a period of 10 days provides thermal tolerance for the symbiosis stability between the scleractinian coral, Acropora millepora and Symbiodinium. Based on genotypic analysis, our results indicate that the acclimatization of this coral species to thermal stress does not come down to simple changes in Symbiodinium and/or the bacterial communities that associate with reef-building corals. This suggests that the physiological plasticity of the host and/or symbiotic components appears to play an important role in responding to ocean warming. The further study of host and symbiont physiology, both of Symbiodinium and prokaryotes, is of paramount importance in the context of global climate change, as mechanisms for rapid holobiont acclimatization will become increasingly important to the long-standing persistence of coral reefs.     

Boring sponges,an increasing threat for coral reefs affected by bleaching events

Coral bleaching is a stress response of corals induced by a variety of factors, but these events have become more frequent and intense in response to recent climate‐change‐related temperature anomalies. We tested the hypothesis that coral reefs affected by bleaching events are currently heavily infested by boring sponges, which are playing a significant role in the destruction of their physical structure. Seventeen reefs that cover the entire distributional range of corals along the Mexican Pacific coast were studied between 2005/2006, and later between 2009/2010. Most of these coral reefs were previously impacted by bleaching events, which resulted in coral mortalities. Sponge abundance and species richness was used as an indicator of bioerosion, and coral cover was used to describe the present condition of coral reefs. Coral reefs are currently highly invaded (46% of the samples examined) by a very high diversity of boring sponges (20 species); being the coral reef framework the substrate most invaded (56%) followed by the rubbles (45%), and the living colonies (36%). The results also indicated that boring sponges are promoting the dislodgment of live colonies and large fragments from the framework. In summary, the eastern coral reefs affected by bleaching phenomena, mainly provoked by El Niño, present a high diversity and abundance of boring sponges, which are weakening the union of the colony with the reef framework and promoting their dislodgment. These phenomena will probably become even more intense and severe, as temperatures are projected to continue to rise under the scenarios for future climate change, which could place many eastern coral reefs beyond their survival threshold.     

海洋酸化对珊瑚礁生态系统的影响研究进展

目前,大气CO2浓度的升高已导致海水pH值比工业革命前下降了约0.1,海水碳酸盐平衡体系随之变化,进而影响珊瑚礁生态系统的健康。近年来的研究表明海洋酸化导致造礁石珊瑚幼体补充和群落恢复更加困难,造礁石珊瑚和其它造礁生物(Reef-building organisms)钙化率降低甚至溶解,乃至影响珊瑚礁鱼类的生命活动。虽然海洋酸化对造礁石珊瑚光合作用的影响不显著,但珊瑚-虫黄藻共生体系会受到一定影响。建议选择典型海区进行长期系统监测,结合室内与原位模拟试验,从个体、种群、群落到系统不同层面,运用生理学和分子生物学技术,结合生态学研究手段,综合研究珊瑚的相应响应,以期深入认识海洋酸化对珊瑚礁生态系统健康(例如珊瑚白化)的影响及其效应。     

New insights into global patterns of ocean temperature anomalies: implications for coral reef health and management

Aim Coral reefs are widely considered to be particularly vulnerable to changes in ocean temperatures, yet we understand little about the broad‐scale spatio‐temporal patterns that may cause coral mortality from bleaching and disease. Our study aimed to characterize these ocean temperature patterns at biologically relevant scales. Location Global, with a focus on coral reefs. Methods We created a 4‐km resolution, 21‐year global ocean temperature anomaly (deviations from long‐term means) database to quantify the spatial and temporal characteristics of temperature anomalies related to both coral bleaching and disease. Then we tested how patterns varied in several key metrics of disturbance severity, including anomaly frequency, magnitude, duration and size. Results Our analyses found both global variation in temperature anomalies and fine‐grained spatial variability in the frequency, duration and magnitude of temperature anomalies. However, we discovered that even during major climatic events with strong spatial signatures, like the El Niño–Southern Oscillation, areas that had high numbers of anomalies varied between years. In addition, we found that 48% of bleaching‐related anomalies and 44% of disease‐related anomalies were less than 50 km², much smaller than the resolution of most models used to forecast climate changes. Main conclusions The fine‐scale variability in temperature anomalies has several key implications for understanding spatial patterns in coral bleaching‐ and disease‐related anomalies as well as for designing protected areas to conserve coral reefs in a changing climate. Spatial heterogeneity in temperature anomalies suggests that certain reefs could be targeted for protection because they exhibit differences in thermal stress. However, temporal variability in anomalies could complicate efforts to protect reefs, because high anomalies in one year are not necessarily predictive of future patterns of stress. Together, our results suggest that temperature anomalies related to coral bleaching and disease are likely to be highly heterogeneous and could produce more localized impacts of climate change.     

Revisiting the Cassandra syndrome; the changing climate of coral reef research

Climate change will be with us for decades, even with significant reductions in emissions. Therefore, predictions made with respect to climate change impacts on coral reefs need to be highly defensible to ensure credibility over the timeframes this issue demands. If not, a Cassandra syndrome could be created whereby future more well-supported predictions of the fate of reefs are neither heard nor acted upon. Herein, popularising predictions based on essentially untested assumptions regarding reefs and their capacity to cope with future climate change is questioned. Some of these assumptions include that: all corals live close to their thermal limits, corals cannot adapt/acclimatize to rapid rates of change, physiological trade-offs resulting from ocean acidification will lead to reduced fecundity, and that climate-induced coral loss leads to widespread fisheries collapse. We argue that, while there is a place for popularising worst-case scenarios, the coral reef crisis has been effectively communicated and, though this communication should be sustained, efforts should now focus on addressing critical knowledge gaps. Communicated by Environment Editor Prof. Rob van Woesik     

Paradise lost: End‐of‐century warming and acidification under business‐as‐usual emissions have severe consequences for symbiotic corals

Despite recent efforts to curtail greenhouse gas emissions, current global emission trajectories are still following the business‐as‐usual representative concentration pathway (RCP) 8.5 emission pathway. The resulting ocean warming and acidification have transformative impacts on coral reef ecosystems, detrimentally affecting coral physiology and health, and these impacts are predicted to worsen in the near future. In this study, we kept fragments of the symbiotic corals Acropora intermedia (thermally sensitive) and Porites lobata (thermally tolerant) for 7 weeks under an orthogonal design of predicted end‐of‐century RCP8.5 conditions for temperature and pCO₂ (3.5°C and 570 ppm above present‐day, respectively) to unravel how temperature and acidification, individually or interactively, influence metabolic and physiological performance. Our results pinpoint thermal stress as the dominant driver of deteriorating health in both species because of its propensity to destabilize coral–dinoflagellate symbiosis (bleaching). Acidification had no influence on metabolism but had a significant negative effect on skeleton growth, particularly when photosynthesis was absent such as in bleached corals or under dark conditions. Total loss of photosynthesis after bleaching caused an exhaustion of protein and lipid stores and collapse of calcification that ultimately led to A. intermedia mortality. Despite complete loss of symbionts from its tissue, P. lobata maintained small amounts of photosynthesis and experienced a weaker decline in lipid and protein reserves that presumably contributed to higher survival of this species. Our results indicate that ocean warming and acidification under business‐as‐usual CO₂ emission scenarios will likely extirpate thermally sensitive coral species before the end of the century, while slowing the recovery of more thermally tolerant species from increasingly severe mass coral bleaching and mortality. This could ultimately lead to the gradual disappearance of tropical coral reefs globally, and a shift on surviving reefs to only the most resilient coral species.     

Reserve design for uncertain responses of coral reefs to climate change

Rising sea temperatures cause mass coral bleaching and threaten reefs worldwide. We show how maps of variations in thermal stress can be used to help manage reefs for climate change. We map proxies of chronic and acute thermal stress and develop evidence-based hypotheses for the future response of corals to each stress regime. We then incorporate spatially realistic predictions of larval connectivity among reefs of the Bahamas and apply novel reserve design algorithms to create reserve networks for a changing climate. We show that scales of larval dispersal are large enough to connect reefs from desirable thermal stress regimes into a reserve network. Critically, we find that reserve designs differ according to the anticipated scope for phenotypic and genetic adaptation in corals, which remains uncertain. Attempts to provide a complete reserve design that hedged against different evolutionary outcomes achieved limited success, which emphasises the importance of considering the scope for adaptation explicitly. Nonetheless, 15% of reserve locations were selected under all evolutionary scenarios, making them a high priority for early designation. Our approach allows new insights into coral holobiont adaptation to be integrated directly into an adaptive approach to management.