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.

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.

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.

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.

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.

No barrier to emergence of bathyal king crabs on the Antarctic shelf.

Cold-water conditions have excluded durophagous (skeleton-breaking) predators from the Antarctic seafloor for millions of years. Rapidly warming seas off the western Antarctic Peninsula could now facilitate their return to the continental shelf, with profound consequences for the endemic fauna. Among the likely first arrivals are king crabs (Lithodidae), which were discovered recently on the adjacent continental slope. During the austral summer of 2010 ‒ 2011, we used underwater imagery to survey a slope-dwelling population of the lithodid Paralomis birsteini off Marguerite Bay, western Antarctic Peninsula for environmental or trophic impediments to shoreward expansion. The population density averaged ∼ 4.5 individuals × 1,000 m(-2) within a depth range of 1,100 ‒ 1,500 m (overall observed depth range 841-2,266 m). Images of juveniles, discarded molts, and precopulatory behavior, as well as gravid females in a trapping study, suggested a reproductively viable population on the slope. At the time of the survey, there was no thermal barrier to prevent the lithodids from expanding upward and emerging on the outer shelf (400- to 550-m depth); however, near-surface temperatures remained too cold for them to survive in inner-shelf and coastal environments (<200 m). Ambient salinity, composition of the substrate, and the depth distribution of potential predators likewise indicated no barriers to expansion of lithodids onto the outer shelf. Primary food resources for lithodids--echinoderms and mollusks--were abundant on the upper slope (550-800 m) and outer shelf. As sea temperatures continue to rise, lithodids will likely play an increasingly important role in the trophic structure of subtidal communities closer to shore.

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.

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.

Reef-coral refugia in a rapidly changing ocean.

This study sought to identify climate-change thermal-stress refugia for reef corals in the Indian and Pacific Oceans. A species distribution modeling approach was used to identify refugia for 12 coral species that differed considerably in their local response to thermal stress. We hypothesized that the local response of coral species to thermal stress might be similarly reflected as a regional response to climate change. We assessed the contemporary geographic range of each species and determined their temperature and irradiance preferences using a k-fold algorithm to randomly select training and evaluation sites. That information was applied to downscaled outputs of global climate models to predict where each species is likely to exist by the year 2100. Our model was run with and without a 1°C capacity to adapt to the rising ocean temperature. The results show a positive exponential relationship between the current area of habitat that coral species occupy and the predicted area of habitat that they will occupy by 2100. There was considerable decoupling between scales of response, however, and with further ocean warming some 'winners' at local scales will likely become 'losers' at regional scales. We predicted that nine of the 12 species examined will lose 24-50% of their current habitat. Most reductions are predicted to occur between the latitudes 5-15°, in both hemispheres. Yet when we modeled a 1°C capacity to adapt, two ubiquitous species, Acropora hyacinthus and Acropora digitifera, were predicted to retain much of their current habitat. By contrast, the thermally tolerant Porites lobata is expected to increase its current distribution by 14%, particularly southward along the east and west coasts of Australia. Five areas were identified as Indian Ocean refugia, and seven areas were identified as Pacific Ocean refugia for reef corals under climate change. All 12 of these reef-coral refugia deserve high-conservation status.

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.

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.

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.

Hosts of the Plio-Pleistocene past reflect modern-day coral vulnerability.

The risk of global extinction of reef-building coral species is increasing. We evaluated extinction risk using a biological trait-based resiliency index that was compared with Caribbean extinction during the Plio-Pleistocene, and with extinction risk determined by the International Union for Conservation of Nature (IUCN). Through the Plio-Pleistocene, the Caribbean supported more diverse coral assemblages than today and shared considerable overlap with contemporary Indo-Pacific reefs. A clear association was found between extant Plio-Pleistocene coral genera and our positive resilience scores. Regional extinction in the past and vulnerability in the present suggests that Pocillopora, Stylophora and foliose Pavona are among the most susceptible taxa to local and regional isolation. These same taxa were among the most abundant corals in the Caribbean Pliocene. Therefore, a widespread distribution did not equate with immunity to regional extinction. The strong relationship between past and present vulnerability suggests that regional extinction events are trait-based and not merely random episodes. We found several inconsistencies between our data and the IUCN scores, which suggest a need to critically re-examine what constitutes coral vulnerability.

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.

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.

Sampling state and process variables on coral reefs.

Contemporary coral reefs are forced to survive through and recover from disturbances at a variety of spatial and temporal scales. Understanding disturbances in the context of ecological processes may lead to accurate predictive models of population trajectories. Most coral-reef studies and monitoring programs examine state variables, which include the percentage coverage of major benthic organisms, but few studies examine the key ecological processes that drive the state variables. Here we outline a sampling strategy that captures both state and process variables, at a spatial scale of tens of kilometers. Specifically, we are interested in (1) examining spatial and temporal patterns in coral population size-frequency distributions, (2) determining major population processes, including rates of recruitment and mortality, and (3) examining relationships between processes and state variables. Our effective sampling units are randomly selected 75 × 25 m stations, spaced approximately 250-500 m apart, representing a 10(3) m spatial scale. Stations are nested within sites, spaced approximately 2 km apart, representing a 10(4) m spatial scale. Three randomly selected 16 m(2) quadrats placed in each station and marked for relocation are used to assess processes across time, while random belt-transects, re-randomized at each sampling event, are used to sample state variables. Both quadrats and belt-transects are effectively sub-samples from which we will derive estimates of means for each station at each sampling event. This nested sampling strategy allows us to determine critical stages in populations, examine population performance, and compare processes through disturbance events and across regions.

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.