A global database on coral recovery following marine heatwaves.

Coral reefs support the world's most diverse marine ecosystem and provide invaluable goods and services for millions of people worldwide. They are however experiencing frequent and intensive marine heatwaves that are causing coral bleaching and mortality. Coarse-grained climate models predict that few coral reefs will survive the 3 °C sea-surface temperature rise in the coming century. Yet, field studies show localized pockets of coral survival and recovery even under high-temperature conditions. Quantifying recovery from marine heatwaves is central to making accurate predictions of coral-reef trajectories into the near future. Here we introduce the world's most comprehensive database on coral recovery following marine heatwaves and other disturbances, called Heatwaves and Coral-Recovery Database (HeatCRD) encompassing 29,205 data records spanning 44 years from 12,266 sites, 83 countries, and 160 data sources. These data provide essential information to coral-reef scientists and managers to best guide coral-reef conservation efforts at both local and regional scales.

Environmental predictors for the restoration of a critically endangered coral, Acropora palmata, along the Florida reef tract.

The population decline and lack of natural recovery of multiple coral species along the Florida reef tract have instigated the expanding application of coral restoration and conservation efforts. Few studies, however, have determined the optimal locations for the survival of outplanted coral colonies from restoration nurseries. This study predicts the optimal locations for Acropora palmata colonies along the Florida reef tract using a boosted-regression-tree model to examine the relationships between the occurrence of wild A. palmata and ten environmental variables. Our model results predicted A. palmata was most likely to occur in shallow reef habitats with (i) generally low mean chlorophyll-a concentrations (< 1 mg m-3), (ii) moderate fetch (3 kJ m-2), (iii) salinities between 20 and 37.5 ppt, (iv) temperatures between 20 and 32°C, (vi) low mean concentrations of total nitrogen (0.16 ppm), and (iv) irradiance between 26.5 and 53.5 mol m-2 s-1. The most suitable habitats for A. palmata were disproportionately allocated to reefs in Biscayne Bay, the Upper Keys, the western-lower Florida Keys, the Marquesas, and the Dry Tortugas. The middle Florida Keys had unfavorable environmental conditions for A. palmata habitat. Results from this study inform where A. palmata, outplanted as part of restoration and conservation efforts, would have suitable environmental conditions to persist over time. This study also provides decision-making support for management focused on the conservation and restoration of the endangered species A. palmata along the Florida reef tract.

Past disturbances and local conditions influence the recovery rates of coral reefs.

Corals are being increasingly subjected to marine heatwaves. Theory suggests that increasing the intensity of disturbances reduces recovery rates, which inspired us to examine the recovery rates of coral cover following marine heatwaves, cyclones, and other disturbances at 1921 study sites, in 58 countries and three oceans, from 1977 to 2020. In the Atlantic Ocean, coral cover has decreased fourfold since the 1970s, and recovery rates following disturbances have been relatively slow, except in the Antilles. By contrast, reefs in the Pacific and Indian Oceans have maintained coral cover and recovery rates over time. There were positive relationships between rates of coral recovery and prior cyclone and heatwave frequency, and negative relationships between rates of coral recovery and macroalgae cover and distance to shore. A recent increase in the variance in recovery rates in some ecoregions of the Pacific and Indian Oceans suggests that some reefs in those ecoregions may be approaching a phase shift. While marine heatwaves are increasing in intensity and frequency, our results suggest that regional and local conditions influence coral recovery rates, and therefore, effective local management efforts can help reefs recover from disturbances.

Moderate chlorophyll-a environments reduce coral bleaching during thermal stress in Yap, Micronesia.

Thermal-stress events on coral reefs lead to coral bleaching, mortality, and changes in species composition. The coral reefs of Yap, in the Federated States of Micronesia, however, remained largely unaffected by major thermal-stress events until 2020, when temperatures were elevated for three months. Twenty-nine study sites were examined around Yap to determine geographical and taxonomic patterns of coral abundance, bleaching susceptibility, and environmental predictors of bleaching susceptibility. Island-wide, 21% (± 14%) of the coral cover was bleached in 2020. Although inner reefs had a greater proportion of thermally-tolerant Porites corals, the prevalence of bleaching was consistently lower on inner reefs (10%) than on outer reefs (31%) for all coral taxa. Corals on both inner and outer reefs along the southwestern coast exhibited the lowest prevalence of coral bleaching and had consistently elevated chlorophyll-a concentrations. More broadly, we revealed a negative relationship between bleaching prevalence and (moderate) chlorophyll-a concentrations that may have facilitated resistance to thermal stress by reducing irradiance and providing a heterotrophic energy source to benefit some corals exposed to autotrophic stress. Southwestern reefs also supported a high but declining fish biomass, making these bleaching-resistant and productive reefs a potential climate-change refuge and a prime target for conservation.

Oceanic differences in coral-bleaching responses to marine heatwaves.

Anomalously high ocean temperatures have increased in frequency, intensity, and duration over the last several decades because of greenhouse gas emissions that cause global warming and marine heatwaves. Reef-building corals are sensitive to such temperature anomalies that commonly lead to coral bleaching, mortality, and changes in community structure. Yet, despite these overarching effects, there are geographical differences in thermal regimes, evolutionary histories, and past disturbances that may lead to different bleaching responses of corals within and among oceans. Here we examined the overall bleaching responses of corals in the Atlantic, Indian, and Pacific Oceans, using both a spatially explicit Bayesian mixed-effects model and a deep-learning neural-network model. We used a 40-year global dataset encompassing 23,288 coral-reef surveys at 11,058 sites in 88 countries, from 1980 to 2020. Focusing on ocean-wide differences we assessed the relationships between the percentage of bleached corals and different temperature-related metrics alongside a suite of environmental variables. We found that while high sea-surface temperatures were consistently, and strongly, related to coral bleaching within all oceans, there were clear geographical differences in the relationships between coral bleaching and most environmental variables. For instance, there was an increase in coral bleaching with depth in the Atlantic Ocean whereas the opposite was observed in the Indian Ocean, and no clear trend could be seen in the Pacific Ocean. The standard deviation of thermal-stress anomalies was negatively related to coral bleaching in the Atlantic and Pacific Oceans, but not in the Indian Ocean. Globally, coral bleaching has progressively occurred at higher temperatures over the last four decades within the Atlantic, Indian, and Pacific Oceans, although, again, there were differences among the three oceans. Together, such patterns highlight that historical circumstances and geographical differences in oceanographic conditions play a central role in contemporary coral-bleaching responses.

Unified methods in collecting, preserving, and archiving coral bleaching and restoration specimens to increase sample utility and interdisciplinary collaboration.

Coral reefs are declining worldwide primarily because of bleaching and subsequent mortality resulting from thermal stress. Currently, extensive efforts to engage in more holistic research and restoration endeavors have considerably expanded the techniques applied to examine coral samples. Despite such advances, coral bleaching and restoration studies are often conducted within a specific disciplinary focus, where specimens are collected, preserved, and archived in ways that are not always conducive to further downstream analyses by specialists in other disciplines. This approach may prevent the full utilization of unexpended specimens, leading to siloed research, duplicative efforts, unnecessary loss of additional corals to research endeavors, and overall increased costs. A recent US National Science Foundation-sponsored workshop set out to consolidate our collective knowledge across the disciplines of Omics, Physiology, and Microscopy and Imaging regarding the methods used for coral sample collection, preservation, and archiving. Here, we highlight knowledge gaps and propose some simple steps for collecting, preserving, and archiving coral-bleaching specimens that can increase the impact of individual coral bleaching and restoration studies, as well as foster additional analyses and future discoveries through collaboration. Rapid freezing of samples in liquid nitrogen or placing at -80 °C to -20 °C is optimal for most Omics and Physiology studies with a few exceptions; however, freezing samples removes the potential for many Microscopy and Imaging-based analyses due to the alteration of tissue integrity during freezing. For Microscopy and Imaging, samples are best stored in aldehydes. The use of sterile gloves and receptacles during collection supports the downstream analysis of host-associated bacterial and viral communities which are particularly germane to disease and restoration efforts. Across all disciplines, the use of aseptic techniques during collection, preservation, and archiving maximizes the research potential of coral specimens and allows for the greatest number of possible downstream analyses.

Coral-bleaching responses to climate change across biological scales.

The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral-bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for example hierarchical models to estimate major coral-reef processes, will not only rapidly advance coral-reef science but will also provide necessary information to guide decision-making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km2 ) that transcend national boundaries. Such networks of protected reefs will provide reef connectivity, through larval dispersal that transverse thermal environments, and genotypic repositories that may become essential units of selection for environmentally diverse locations. Together, multinational networks may be the best chance corals have to persist through climate change, while humanity struggles to reduce emissions of greenhouse gases to net zero.

Present and future bright and dark spots for coral reefs through climate change.

Marine heatwaves can cause coral bleaching and reduce coral cover on reefs, yet few studies have identified "bright spots," where corals have recently shown a capacity to survive such pressures. We analyzed 7714 worldwide surveys from 1997 to 2018 along with 14 environmental and temperature metrics in a hierarchical Bayesian model to identify conditions that contribute to present-day coral cover. We also identified locations with significantly higher (i.e., "bright spots") and lower coral cover (i.e., "dark spots") than regionally expected. In addition, using 4-km downscaled data of Representative Concentration Pathways (RCPs) 4.5 and 8.5, we projected coral cover on reefs for the years 2050 and 2100. Coral cover on modern reefs was positively associated with historically high maximum sea-surface temperatures (SSTs), and negatively associated with high contemporary SSTs, tropical-cyclone frequencies, and human-population densities. By 2100, under RCP8.5, we projected relative decreases in coral cover of >40% on most reefs globally but projected less decline on reefs in Indonesia, Malaysia, the central Philippines, New Caledonia, Fiji, and French Polynesia, which should be focal localities for multinational networks of protected areas.

A global coral-bleaching database, 1980-2020.

Coral reefs are the world's most diverse marine ecosystems that provide resources and services that benefit millions of people globally. Yet, coral reefs have recently experienced an increase in the frequency and intensity of thermal-stress events that are causing coral bleaching. Coral bleaching is a result of the breakdown of the symbiosis between corals and their symbiotic microalgae, causing the loss of pigments and symbionts, giving corals a pale, bleached appearance. Bleaching can be temporary or fatal for corals, depending on the species, the geographic location, historical conditions, and on local and regional influences. Indeed, marine heat waves are the greatest threat to corals worldwide. Here we compile a Global Coral-Bleaching Database (GCBD) that encompasses 34,846 coral bleaching records from 14,405 sites in 93 countries, from 1980-2020. The GCBD provides vital information on the presence or absence of coral bleaching along with site exposure, distance to land, mean turbidity, cyclone frequency, and a suite of sea-surface temperature metrics at the times of survey.

Local conditions magnify coral loss after marine heatwaves.

Climate change threatens coral reefs by causing heat stress events that lead to widespread coral bleaching and mortality. Given the global nature of these mass coral mortality events, recent studies argue that mitigating climate change is the only path to conserve coral reefs. Using a global analysis of 223 sites, we show that local stressors act synergistically with climate change to kill corals. Local factors such as high abundance of macroalgae or urchins magnified coral loss in the year after bleaching. Notably, the combined effects of increasing heat stress and macroalgae intensified coral loss. Our results offer an optimistic premise that effective local management, alongside global efforts to mitigate climate change, can help coral reefs survive the Anthropocene.

Thermal stress jeopardizes carbonate production of coral reefs across the western and central Pacific Ocean.

Coral reefs protect islands, coastal areas, and their inhabitants from storm waves and provide essential goods and services to millions of people worldwide. Yet contemporary rates of ocean warming and local disturbances are jeopardizing the reef-building capacity of coral reefs to keep up with rapid rates of sea-level rise. This study compared the reef-building capacity of shallow-water habitats at 142 sites across a potential thermal-stress gradient in the tropical Pacific Ocean. We sought to determine the extent to which habitat differences and environmental variables potentially affect rates of net carbonate production. In general, outer-exposed reefs and lagoonal-patch reefs had higher rates of net carbonate production than nearshore reefs. The study found that thermal anomalies, particularly the intensity of thermal-stress events, play a significant role in reducing net carbonate production-evident as a diminishing trend of net carbonate production from the western to the central tropical Pacific Ocean. The results also showed a latent spatial effect along the same gradient, not explained by thermal stress, suggesting that reefs in the western tropical Pacific Ocean are potentially enhanced by the proximity of reefs in the Coral Triangle-an effect that diminishes with increasing distance and isolation.

Different population trajectories of two reef-building corals with similar life-history traits.

Increases in the frequency and intensity of acute and chronic disturbances are causing declines of coral reefs world-wide. Although quantifying the responses of corals to acute disturbances is well documented, detecting subtle responses of coral populations to chronic disturbances is less common, but can also result in altered population and community structures. We investigated the population dynamics of two key reef-building Merulinid coral species, Dipsastraea favus and Platygyra lamellina, with similar life-history traits, in the Gulf of Eilat and Aqaba, Red Sea from 2015 to 2018, to assess potential differences in their population trajectories. Demographic processes, which included rates of survival, growth, reproduction and recruitment were used to parametrize integral projection models and estimate population growth rates and the likely population trajectories of both coral species. The survival and reproduction rates of both D. favus and P. lamellina were positively related to coral colony size, and elasticity analyses showed that large colonies most influenced population dynamics. Although both species have similar life-history traits and growth morphologies and are generally regarded as 'stress-tolerant', the populations showed contrasting trajectories-D. favus appears to be increasing whereas P. lamellina appears to be decreasing. As many corals have long-life expectancies, the process of local and regional decline might be subtle and slow. Ecological assessments based on total living coral coverage, morphological groups or functional traits might overlook subtle, species-specific trends. However, demographic approaches capable of detecting subtle species-specific population changes can augment ecological studies and provide valuable early warning signs of decline before major coral loss becomes evident.

Predicting coral-reef futures from El Niño and Pacific Decadal Oscillation events.

El Niño Southern Oscillation (ENSO) events modulate oceanographic processes that control temperature and productivity in tropical waters, yet potential interactions with low frequency climate variability, such as the Pacific Decadal Oscillation (PDO), are poorly understood. We show that ENSO and PDO together predicted (i) maximum sea-surface temperatures (SST), which were associated with coral bleaching and declines in coral cover, and (ii) maximum chlorophyll-a concentrations, which were associated with high densities of coral-predatory Acanthaster starfish, across the tropical north Pacific Ocean since 1980. Asynchrony between the positive PDO and negative ENSO (i.e., La Niña) was associated with peaks in annual SST. By contrast, synchrony between the positive PDO and positive ENSO (i.e., El Niño) was associated with peaks in chlorophyll-a. Both conditions led to ecological disturbances and significant loss of coral cover, however, spatial models revealed where impacts to reefs were expected under varying climate scenarios.  The 2015/17 ENSO event was coupled with a positive PDO and resulted in high SST and Acanthaster abundances in eastern Micronesia, while positive coral growth occurred in western Micronesia.  Our novel approach for forecasting coral growth into the future may be applicable to other oceanic regions with differing oceanographic modulators.

Niche space of corals along the Florida reef tract.

Over the last three decades corals have declined precipitously in the Florida Keys. Their population decline has prompted restoration effort. Yet, little effort has been invested in understanding the contemporary niche spaces of coral species, which could assist in prioritizing conservation habitats. We sought to predict the probability of occurrence of 23 coral species, including the critically endangered Acropora cervicornis, using observations at 985 sites from 2011-2015. We ran boosted regression trees to evaluate the relationship between the presence of these corals and eight potential environmental predictors: (i) bathymetry (m), (ii) mean of daily sea surface temperature (SST) (°C), (iii) variance of SST (°C), (iv) range of SST (°C), (v) chlorophyll-a concentration (mg m3), (vi) turbidity (m-1), (vii) wave energy (kJ m-2), and (viii) distance from coast (km). The Marquesas and the lower and upper Florida Keys were predicted to support the most suitable habitats for the 23 coral species examined. A. cervicornis had one of the smallest areas of suitable habitat, which was limited to the lower and upper Florida Keys, the Dry Tortugas, and nearshore Broward-Miami reefs. The best environmental predictors of site occupancy of A. cervicornis were SST range (4-5°C) and turbidity (K490 between 0.15-0.25 m-1). Historically A. cervicornis was reported in clear oligotrophic waters, although the present results find the coral species surviving in nearshore turbid conditions. Nearshore, turbid reefs may shade corals during high-temperature events, and therefore nearshore reefs in south Florida may become important refuges for corals as the ocean temperatures continue to increase.

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 Kd 490, 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.

Ocean acidification changes the vertical movement of stone crab larvae.

Anthropogenic activities are increasing ocean temperature and decreasing ocean pH. Some coastal habitats are experiencing increases in organic runoff, which when coupled with a loss of vegetated coastline can accelerate reductions in seawater pH. Marine larvae that hatch in coastal habitats may not have the ability to respond to elevated temperature and changes in seawater pH. This study examined the response of Florida stone crab (Menippe mercenaria) larvae to elevated temperature (30°C control and 32°C treatment) and CO2-induced reductions in pH (8.05 pH control and 7.80 pH treatment). We determined whether those singular and simultaneous stressors affect larval vertical movement at two developmental stages. Geotactic responses varied between larval stages. The direction and rate of the vertical displacement of larvae were dependent on pH rather than temperature. Stage III larvae swam upwards under ambient pH conditions, but swam downwards at a faster rate under reduced pH. There was no observable change in the directional movement of Stage V larvae. The reversal in orientation by Stage III larvae may limit larval transport in habitats that experience reduced pH and could pose challenges for the northward dispersal of stone crabs as coastal temperatures warm.

Carbonate production of Micronesian reefs suppressed by thermal anomalies and Acanthaster as sea-level rises.

Coral reefs are essential to millions of island inhabitants. Yet, coral reefs are threatened by thermal anomalies associated with climate change and by local disturbances that include land-use change, pollution, and the coral-eating sea star Acanthaster solaris. In combination, these disturbances cause coral mortality that reduce the capacity of reefs to produce enough carbonate to keep up with sea-level rise. This study compared the reef-building capacity of shallow-water inner, patch, and outer reefs in the two islands of Pohnpei and Kosrae, Federated States of Micronesia. We identified which reefs were likely to keep up with sea-level rise under different climate-change scenarios, and estimated whether there were differences across habitats in the threshold of percentage coral cover at which net carbonate production becomes negative. We also quantified the influence of A. solaris on carbonate production. Whereas the northwestern outer reefs of Pohnpei and Kosrae had the highest net rates of carbonate production (18.5 and 16.4 kg CaCO3 m-2 yr-1, respectively), the southeastern outer reefs had the lowest rates of carbonate production (1.2-1.3 and 0.7 kg CaCO3 m-2 yr-1, respectively). The patch reefs of Pohnpei had on average higher net carbonate production rates (9.5 kg CaCO3 m-2 yr-1) than the inner reefs of both Pohnpei and Kosrae (7.0 and 7.8 kg CaCO3 m-2 yr-1, respectively). A. solaris were common on Kosrae and caused an average reduction in carbonate production of 0.6 kg CaCO3 m-2 yr-1 on Kosraean reefs. Northern outer reefs are the most likely habitats to keep up with sea-level rise in both Pohnpei and Kosrae. Overall, the inner reefs of Pohnpei and Kosrae need ~ 5.5% more coral cover to generate the same amount of carbonate as outer reefs. Therefore, inner reefs need special protection from land-use change and local pollution to keep pace with sea-level rise under all climate-change scenarios.

Keeping up with sea-level rise: Carbonate production rates in Palau and Yap, western Pacific Ocean.

Coral reefs protect islands from tropical storm waves and provide goods and services for millions of islanders worldwide. Yet it is unknown how coral reefs in general, and carbonate production in particular, will respond to sea-level rise and thermal stress associated with climate change. This study compared the reef-building capacity of different shallow-water habitats at twenty-four sites on each of two islands, Palau and Yap, in the western Pacific Ocean. We were particularly interested in estimating the inverse problem of calculating the value of live coral cover at which net carbonate production becomes negative, and whether that value varied across habitats. Net carbonate production varied among habitats, averaging 10.2 kg CaCO3 m-2 y-1 for outer reefs, 12.7 kg CaCO3 m-2 y-1 for patch reefs, and 7.2 kg CaCO3 m-2 y-1 for inner reefs. The value of live coral cover at which net carbonate production became negative varied across habitats, with highest values on inner reefs. These results suggest that some inner reefs tend to produce less carbonate, and therefore need higher coral cover to produce enough carbonate to keep up with sea-level rise than outer and patch reefs. These results also suggest that inner reefs are more vulnerable to sea-level rise than other habitats, which stresses the need for effective land-use practices as the climate continues to change. Averaging across all reef habitats, the rate of carbonate production was 9.7 kg CaCO3 m-2 y-1, or approximately 7.9 mm y-1 of potential vertical accretion. Such rates of vertical accretion are higher than projected averages of sea-level rise for the representative concentration pathway (RCP) climate-change scenarios 2.6, 4.5, and 6, but lower than for the RCP scenario 8.5.

Human disturbance amplifies Amazonian El Niño-Southern Oscillation signal.

The long-term interaction between human activity and climate is subject to increasing scrutiny. Humans homogenize landscapes through deforestation, agriculture, and burning and thereby might reduce the capacity of landscapes to provide archives of climate change. Alternatively, land-use change might overwhelm natural buffering and amplify latent climate signals, rendering them detectable. Here we examine a sub-annually resolved sedimentary record from Lake Sauce in the western Amazonian lowlands that spans 6900 years. Finely-laminated sediments were deposited from ca. 5000 years ago until the present, and human activity in the watershed was revealed through the presence of charcoal and maize agriculture. The laminations, analyzed for color content and bandwidth, showed distinctive changes that were coupled to more frequent occurrence of fossil maize pollen. As agricultural activity intensified ca. 2200 cal. BP, the 2- to 8-year periodicity characteristic of El Niño-Southern Oscillation became evident in the record. These agricultural activities appeared to have amplified an existing, but subtle climatic signal that was previously absorbed by natural vegetation. When agricultural activity slowed, or land use around Lake Sauce changed at ca. 800 cal. BP, the signal of El Niño-Southern Oscillation (ENSO) activity became erratic.