Cumulative risk of future bleaching for the world's coral reefs.

Spatial and temporal patterns of future coral bleaching are uncertain, hampering global conservation efforts to protect coral reefs against climate change. Our analysis of daily projections of ocean warming establishes the severity, annual duration, and onset of severe bleaching risk for global coral reefs this century, pinpointing vital climatic refugia. We show that low-latitude coral regions are most vulnerable to thermal stress and will experience little reprieve from climate mitigation. By 2080, coral bleaching is likely to start on most reefs in spring, rather than late summer, with year-round bleaching risk anticipated to be high for some low-latitude reefs regardless of global efforts to mitigate harmful greenhouse gasses. By identifying Earth's reef regions that are at lowest risk of accelerated bleaching, our results will prioritize efforts to limit future loss of coral reef biodiversity.

Multi-Factor Coral Disease Risk: A new product for early warning and management.

Ecological forecasts are becoming increasingly valuable tools for conservation and management. However, there are few examples of near-real-time forecasting systems that account for the wide range of ecological complexities. We developed a new coral disease ecological forecasting system that explores a suite of ecological relationships and their uncertainty and investigates how forecast skill changes with shorter lead times. The Multi-Factor Coral Disease Risk product introduced here uses a combination of ecological and marine environmental conditions to predict the risk of white syndromes and growth anomalies across reefs in the central and western Pacific and along the east coast of Australia and is available through the US National Oceanic and Atmospheric Administration Coral Reef Watch program. This product produces weekly forecasts for a moving window of 6 months at a resolution of ~5 km based on quantile regression forests. The forecasts show superior skill at predicting disease risk on withheld survey data from 2012 to 2020 compared with predecessor forecast systems, with the biggest improvements shown for predicting disease risk at mid- to high-disease levels. Most of the prediction uncertainty arises from model uncertainty, so prediction accuracy and precision do not improve substantially with shorter lead times. This result arises because many predictor variables cannot be accurately forecasted, which is a common challenge across ecosystems. Weekly forecasts and scenarios can be explored through an online decision support tool and data explorer, co-developed with end-user groups to improve use and understanding of ecological forecasts. The models provide near-real-time disease risk assessments and allow users to refine predictions and assess intervention scenarios. This work advances the field of ecological forecasting with real-world complexities and, in doing so, better supports near-term decision making for coral reef ecosystem managers and stakeholders. Secondarily, we identify clear needs and provide recommendations to further enhance our ability to forecast coral disease risk.

The vulnerability of World Heritage seagrass habitats to climate change.

Seagrass is an important natural attribute of 28 World Heritage (WH) properties. These WH seagrass habitats provide a wide range of services to adjacent ecosystems and human communities, and are one of the largest natural carbon sinks on the planet. Climate change is considered the greatest and fastest-growing threat to natural WH properties and evidence of climate-related impacts on seagrass habitats has been growing. The main objective of this study was to assess the vulnerability of WH seagrass habitats to location-specific key climate stressors. Quantitative surveys of seagrass experts and site managers were used to assess exposure, sensitivity and adaptive capacity of WH seagrass habitats to climate stressors, following the Climate Vulnerability Index approach. Over half of WH seagrass habitats have high vulnerability to climate change, mainly from the long-term increase in sea-surface temperature and short-term marine heatwaves. Potential impacts from climate change and certainty scores associated with them were higher than reported by a similar survey-based study from 10 years prior, indicating a shift in stakeholder perspectives during the past decade. Additionally, seagrass experts' opinions on the cumulative impacts of climate and direct-anthropogenic stressors revealed that high temperature in combination with high suspended sediments, eutrophication and hypoxia is likely to provoke a synergistic cumulative (negative) impact (p < .05). A key component contributing to the high vulnerability assessments was the low adaptive capacity; however, discrepancies between adaptive capacity scores and qualitative responses suggest that managers of WH seagrass habitats might not be adequately equipped to respond to climate change impacts. This thematic assessment provides valuable information to help prioritize conservation actions, monitoring activities and research in WH seagrass habitats. It also demonstrates the utility of a systematic framework to evaluate the vulnerability of thematic groups of protected areas that share a specific attribute.

Twenty-year record of white pox disease in the Florida Keys: importance of environmental risk factors as drivers of coral health.

Declining coral populations worldwide place a special premium on identifying risks and drivers that precipitate these declines. Understanding the relationship between disease outbreaks and their drivers can help to anticipate when the risk of a disease pandemic is high. Populations of the iconic branching Caribbean elkhorn coral Acropora palmata have collapsed in recent decades, in part due to white pox disease (WPX). To assess the role that biotic and abiotic factors play in modulating coral disease, we present a predictive model for WPX in A. palmata using 20 yr of disease surveys from the Florida Keys plus environmental information collected simultaneously in situ and via satellite. We found that colony size was the most influential predictor for WPX occurrence, with larger colonies being at higher risk. Water quality parameters of dissolved oxygen saturation, total organic carbon, dissolved inorganic nitrogen, and salinity were implicated in WPX likelihood. Both low and high wind speeds were identified as important environmental drivers of WPX. While high temperature has been identified as an important cause of coral mortality in both bleaching and disease scenarios, our model indicates that the relative influence of HotSpot (positive summertime temperature anomaly) was low and actually inversely related to WPX risk. The predictive model developed here can contribute to enabling targeted strategic management actions and disease surveillance, enabling managers to treat the disease or mitigate disease drivers, thereby suppressing the disease and supporting the persistence of corals in an era of myriad threats.

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.

Experiment Degree Heating Week (eDHW) as a novel metric to reconcile and validate past and future global coral bleaching studies.

Coral bleaching has increasingly impacted reefs worldwide over the past four decades. Despite almost 40 years of research into the mechanistic, physiological, ecological, biophysical and climatic drivers of coral bleaching, metrics to allow comparison between ecological observations and experimental simulations still do not exist. Here we describe a novel metric - experimental Degree Heating Week (eDHW) - with which to standardise the persistently variable thermal conditions employed across experimental studies of coral bleaching by modify the widely used Degree Heating Week (DHW) metric used in ecological studies to standardise cumulative heat loading.

Emergent properties in the responses of tropical corals to recurrent climate extremes.

The frequency, intensity, and spatial scale of climate extremes are changing rapidly due to anthropogenic global warming.1,2 A growing research challenge is to understand how multiple climate-driven disturbances interact with each other over multi-decadal time frames, generating combined effects that cannot be predicted from single events alone.3-5 Here we examine the emergent dynamics of five coral bleaching events along the 2,300 km length of the Great Barrier Reef that affected >98% of the Reef between 1998 and 2020. We show that the bleaching responses of corals to a given level of heat exposure differed in each event and were strongly influenced by contingency and the spatial overlap and strength of interactions between events. Naive regions that escaped bleaching for a decade or longer were the most susceptible to bouts of heat exposure. Conversely, when pairs of successive bleaching episodes were close together (1-3 years apart), the thermal threshold for severe bleaching increased because the earlier event hardened regions of the Great Barrier Reef to further impacts. In the near future, the biological responses to recurrent bleaching events may become stronger as the cumulative geographic footprint expands further, potentially impairing the stock-recruitment relationships among lightly and severely bleached reefs with diverse recent histories. Understanding the emergent properties and collective dynamics of recurrent disturbances will be critical for predicting spatial refuges and cumulative ecological responses, and for managing the longer-term impacts of anthropogenic climate change on ecosystems.

Rebuilding relationships on coral reefs: Coral bleaching knowledge-sharing to aid adaptation planning for reef users: Bleaching emergence on reefs demonstrates the need to consider reef scale and accessibility when preparing for, and responding to, coral bleaching.

Coral bleaching has impacted reefs worldwide and the predictions of near-annual bleaching from over two decades ago have now been realized. While technology currently provides the means to predict large-scale bleaching, predicting reef-scale and within-reef patterns in real-time for all reef users is limited. In 2020, heat stress across the Great Barrier Reef underpinned the region's third bleaching event in 5 years. Here we review the heterogeneous emergence of bleaching across Heron Island reef habitats and discuss the oceanographic drivers that underpinned variable bleaching emergence. We do so as a case study to highlight how reef end-user groups who engage with coral reefs in different ways require targeted guidance for how, and when, to alter their use of coral reefs in response to bleaching events. Our case study of coral bleaching emergence demonstrates how within-reef scale nowcasting of coral bleaching could aid the development of accessible and equitable bleaching response strategies on coral reefs. Also see the video abstract here: https://youtu.be/N9Tgb8N-vN0.

Correction: Quantifying Climatological Ranges and Anomalies for Pacific Coral Reef Ecosystems.

[This corrects the article DOI: 10.1371/journal.pone.0061974.].

Convergence of stakeholders' environmental threat perceptions following mass coral bleaching of the Great Barrier Reef.

Managing human use of ecosystems in an era of rapid environmental change requires an understanding of diverse stakeholders' behaviors and perceptions to enable effective prioritization of actions to mitigate multiple threats. Specifically, research examining how threat perceptions are shared or diverge among stakeholder groups and how these can evolve through time is increasingly important. We investigated environmental threat perceptions related to Australia's Great Barrier Reef and explored their associations before and after consecutive years of mass coral bleaching. We used data from surveys of commercial fishers, tourism operators, and coastal residents (n = 5254) conducted in 2013 and 2017. Threats perceived as most serious differed substantially among groups before bleaching but were strongly aligned after bleaching. Climate change became the most frequently reported threat by all stakeholder groups following the coral bleaching events, and perceptions of fishing and poor water quality as threats also ranked high. Within each of the 3 stakeholder groups, fishers, tourism operators, and coastal residents, the prioritization of these 3 threats tended to diverge in 2013, but convergence occurred after bleaching. These results indicate an emergence of areas of agreement both within and across stakeholder groups. Changes in perceptions were likely influenced by high-profile environmental-disturbance events and media representations of threats. Our results provide insights into the plasticity of environmental-threat perceptions and highlight how their convergence in response to major events may create new opportunities for strategic public engagement and increasing support for management.

Convergencia de la Percepción de las Amenazas Ambientales por los Actores Sociales después del Blanqueamiento Masivo del Coral de la Gran Barrera Arrecifal Resumen La administración del uso que las personas dan a los ecosistemas en una época de cambios ambientales rápidos requiere un entendimiento del comportamiento de diferentes actores sociales y sus percepciones para facilitar la priorización de las acciones que mitigan a las múltiples amenazas. Específicamente, las investigaciones que examinan cómo se comparten o difieren las percepciones de las amenazas entre los grupos de actores y cómo estas percepciones pueden evolucionar con el tiempo son cada vez más importantes. Investigamos las percepciones de las amenazas ambientales relacionadas con la Gran Barrera Arrecifal en Australia y exploramos sus asociaciones antes y después de varios años consecutivos de blanqueamiento masivo del coral. Usamos datos tomados de encuestas realizadas a pescadores comerciales, operadores turísticos y residentes de la costa (n = 5,254) en 2013 y 2017. Las amenazas percibidas como las más serias difirieron sustancialmente entre los tres grupos antes del blanqueamiento, pero se alinearon marcadamente después del blanqueamiento. El cambio climático se convirtió en la amenaza reportada con mayor frecuencia por todos los grupos de actores después de los eventos de blanqueamiento del coral. Las percepciones de la pesca y la baja calidad del agua como amenazas también tuvieron una clasificación alta. Dentro de cada uno de los tres grupos de actores (pescadores, operadores turísticos y residentes de la costa) la priorización de estas tres amenazas tendió a diferir en 2013 pero la convergencia ocurrió después del blanqueamiento. Estos resultados indican un surgimiento de áreas de acuerdo dentro y entre los grupos de actores. Los cambios en las percepciones probablemente estuvieron influenciados por eventos de perturbación ambiental de alto perfil y la representación mediática de las amenazas. Nuestros resultados proporcionaron conocimiento sobre la plasticidad de las percepciones de las amenazas ambientales y resalta cómo su convergencia en la respuesta a los eventos más importantes puede crear nuevas oportunidades para la participación estratégica del público e incrementar el apoyo para su manejo.

Case-control design identifies ecological drivers of endemic coral diseases.

Endemic disease transmission is an important ecological process that is challenging to study because of low occurrence rates. Here, we investigate the ecological drivers of two coral diseases-growth anomalies and tissue loss-affecting five coral species. We first show that a statistical framework called the case-control study design, commonly used in epidemiology but rarely applied to ecology, provided high predictive accuracy (67-82%) and disease detection rates (60-83%) compared with a traditional statistical approach that yielded high accuracy (98-100%) but low disease detection rates (0-17%). Using this framework, we found evidence that 1) larger corals have higher disease risk; 2) shallow reefs with low herbivorous fish abundance, limited water motion, and located adjacent to watersheds with high fertilizer and pesticide runoff promote low levels of growth anomalies, a chronic coral disease; and 3) wave exposure, stream exposure, depth, and low thermal stress are associated with tissue loss disease risk during interepidemic periods. Variation in risk factors across host-disease pairs suggests that either different pathogens cause the same gross lesions in different species or that the same disease may arise in different species under different ecological conditions.

The Rarity of Depth Refugia from Coral Bleaching Heat Stress in the Western and Central Pacific Islands.

Some researchers have suggested that corals living in deeper reefs may escape heat stress experienced by shallow corals. We evaluated the potential of deep coral reef refugia from bleaching stress by leveraging a long record of satellite-derived sea surface temperature data with a temporal, spatial, and depth precision of in situ temperature records. We calculated an in situ stress metric using a depth bias-adjusted threshold for 457 coral reef sites among 49 islands in the western and central Pacific Ocean over the period 2001-2017. Analysis of 1,453 heating events found no meaningful depth refuge from heat stress down to 38 m, and no significant association between depth and subsurface heat stress. Further, the surface metric underestimated subsurface stress by an average of 39.3%, across all depths. Combining satellite and in situ temperature data can provide bleaching-relevant heat stress results to avoid misrepresentation of heat stress exposure at shallow reefs.

Increases and decreases in marine disease reports in an era of global change.

Outbreaks of marine infectious diseases have caused widespread mass mortalities, but the lack of baseline data has precluded evaluating whether disease is increasing or decreasing in the ocean. We use an established literature proxy method from Ward and Lafferty (Ward and Lafferty 2004 PLoS Biology2, e120 (doi:10.1371/journal.pbio.0020120)) to analyse a 44-year global record of normalized disease reports from 1970 to 2013. Major marine hosts are combined into nine taxonomic groups, from seagrasses to marine mammals, to assess disease swings, defined as positive or negative multi-decadal shifts in disease reports across related hosts. Normalized disease reports increased significantly between 1970 and 2013 in corals and urchins, indicating positive disease swings in these environmentally sensitive ectotherms. Coral disease reports in the Caribbean correlated with increasing temperature anomalies, supporting the hypothesis that warming oceans drive infectious coral diseases. Meanwhile, disease risk may also decrease in a changing ocean. Disease reports decreased significantly in fishes and elasmobranchs, which have experienced steep human-induced population declines and diminishing population density that, while concerning, may reduce disease. The increases and decreases in disease reports across the 44-year record transcend short-term fluctuations and regional variation. Our results show that long-term changes in disease reports coincide with recent decades of widespread environmental change in the ocean.

Refugia under threat: Mass bleaching of coral assemblages in high-latitude eastern Australia.

Environmental anomalies that trigger adverse physiological responses and mortality are occurring with increasing frequency due to climate change. At species' range peripheries, environmental anomalies are particularly concerning because species often exist at their environmental tolerance limits and may not be able to migrate to escape unfavourable conditions. Here, we investigated the bleaching response and mortality of 14 coral genera across high-latitude eastern Australia during a global heat stress event in 2016. We evaluated whether the severity of assemblage-scale and genus-level bleaching responses was associated with cumulative heat stress and/or local environmental history, including long-term mean temperatures during the hottest month of each year (SSTLTMAX ), and annual fluctuations in water temperature (SSTVAR ) and solar irradiance (PARZVAR ). The most severely-bleached genera included species that were either endemic to the region (Pocillopora aliciae) or rare in the tropics (e.g. Porites heronensis). Pocillopora spp., in particular, showed high rates of immediate mortality. Bleaching severity of Pocillopora was high where SSTLTMAX was low or PARZVAR was high, whereas bleaching severity of Porites was directly associated with cumulative heat stress. While many tropical Acropora species are extremely vulnerable to bleaching, the Acropora species common at high latitudes, such as A. glauca and A. solitaryensis, showed little incidence of bleaching and immediate mortality. Two other regionally-abundant genera, Goniastrea and Turbinaria, were also largely unaffected by the thermal anomaly. The severity of assemblage-scale bleaching responses was poorly explained by the environmental parameters we examined. Instead, the severity of assemblage-scale bleaching was associated with local differences in species abundance and taxon-specific bleaching responses. The marked taxonomic disparity in bleaching severity, coupled with high mortality of high-latitude endemics, point to climate-driven simplification of assemblage structures and progressive homogenisation of reef functions at these high-latitude locations.

Rapid Coral Decay Is Associated with Marine Heatwave Mortality Events on Reefs.

Severe marine heatwaves have recently become a common feature of global ocean conditions due to a rapidly changing climate [1, 2]. These increasingly severe thermal conditions are causing an unprecedented increase in the frequency and severity of mortality events in marine ecosystems, including on coral reefs [3]. The degradation of coral reefs will result in the collapse of ecosystem services that sustain over half a billion people globally [4, 5]. Here, we show that marine heatwave events on coral reefs are biologically distinct to how coral bleaching has been understood to date, in that heatwave conditions result in an immediate heat-induced mortality of the coral colony, rapid coral skeletal dissolution, and the loss of the three-dimensional reef structure. During heatwave-induced mortality, the coral skeletons exposed by tissue loss are, within days, encased by a complex biofilm of phototrophic microbes, whose metabolic activity accelerates calcium carbonate dissolution to rates exceeding accretion by healthy corals and far greater than has been documented on reefs under normal seawater conditions. This dissolution reduces the skeletal density and hardness and increases porosity. These results demonstrate that severe-heatwave-induced mortality events should be considered as a distinct biological phenomenon from bleaching events on coral reefs. We also suggest that such heatwave mortality events, and rapid reef decay, will become more frequent as the intensity of marine heatwaves increases and provides further compelling evidence for the need to mitigate climate change and instigate actions to reduce marine heatwaves.

Seeking Resistance in Coral Reef Ecosystems: The Interplay of Biophysical Factors and Bleaching Resistance under a Changing Climate: The Interplay of a Reef's Biophysical Factors Can Mitigate the Coral Bleaching Response.

If we are to ensure the persistence of species in an increasingly warm world, of interest is the identification of drivers that affect the ability of an organism to resist thermal stress. Underpinning any organism's capacity for resistance is a complex interplay between biological and physical factors occurring over multiple scales. Tropical coral reefs are a unique system, in that their function is dependent upon the maintenance of a coral-algal symbiosis that is directly disrupted by increases in water temperature. A number of physical factors have been identified as affecting the biological responses of the coral organism under broadscale thermal anomalies. One such factor is water flow, which is capable of modulating both organismal metabolic functioning and thermal environments. Understanding the physiological and hydrodynamic drivers of organism response to thermal stress improves predictive capabilities and informs targeted management responses, thereby increasing the resilience of reefs into the future.

High-resolution characterization of the abiotic environment and disturbance regimes on the Great Barrier Reef, 1985-2017.

This data compilation synthesizes 36 static environmental and spatial variables, and temporally explicit modeled estimates of three major disturbances to coral cover on the Great Barrier Reef (GBR): (1) coral bleaching, (2) tropical cyclones, and (3) outbreaks of the coral-eating crown-of-thorns starfish Acanthaster cf. solaris. Data are provided on a standardized grid (0.01° × 0.01° ~ 1 × 1 km) for reef locations along the GBR, containing 15,928 pixels and excluding the northernmost sections (<12° S) where empirical data were sparse. This compilation provides a consistent and high-resolution characterization of the abiotic environment and disturbance regimes for GBR reef locations at a fine spatial scale to be used in the development of complex ecosystem models. Static estimates of environmental variables (e.g., depth, bed shear stress, average temperature, temperature variation) originally developed by the Commonwealth of Australia's Environment Research Facility (CERF) Marine Biodiversity Hub were provided by Geoscience Australia. Annual (1985-2017) disturbance estimates were either interpolated from empirical data (A. cf. solaris), predicted from proxy indicators (e.g., degree heating weeks [DHW] as a proxy for bleaching severity), or explicitly modeled (e.g., wave height model for each cyclone). This data set synthesizes some of the most recent advances in remote sensing and modeling of environmental conditions on the GBR; yet it is not exhaustive and we highlight areas that should be expanded through future research. The characterization of abiotic and disturbance regimes presented here represent an essential tool for the development of complex regional scale models of the GBR; preventing redundancy between working groups and promoting collaboration, innovation, and consistency. When using the data set, we kindly request that you cite this article and/or the articles cited in the reference section, recognizing the work that went into compiling the data together and the original authors' willingness to make it publicly available.

The future of resilience-based management in coral reef ecosystems.

Resilience underpins the sustainability of both ecological and social systems. Extensive loss of reef corals following recent mass bleaching events have challenged the notion that support of system resilience is a viable reef management strategy. While resilience-based management (RBM) cannot prevent the damaging effects of major disturbances, such as mass bleaching events, it can support natural processes that promote resistance and recovery. Here, we review the potential of RBM to help sustain coral reefs in the 21st century. We explore the scope for supporting resilience through existing management approaches and emerging technologies and discuss their opportunities and limitations in a changing climate. We argue that for RBM to be effective in a changing world, reef management strategies need to involve both existing and new interventions that together reduce stress, support the fitness of populations and species, and help people and economies to adapt to a highly altered ecosystem.

Global warming transforms coral reef assemblages.

Global warming is rapidly emerging as a universal threat to ecological integrity and function, highlighting the urgent need for a better understanding of the impact of heat exposure on the resilience of ecosystems and the people who depend on them 1 . Here we show that in the aftermath of the record-breaking marine heatwave on the Great Barrier Reef in 2016 2 , corals began to die immediately on reefs where the accumulated heat exposure exceeded a critical threshold of degree heating weeks, which was 3-4 °C-weeks. After eight months, an exposure of 6 °C-weeks or more drove an unprecedented, regional-scale shift in the composition of coral assemblages, reflecting markedly divergent responses to heat stress by different taxa. Fast-growing staghorn and tabular corals suffered a catastrophic die-off, transforming the three-dimensionality and ecological functioning of 29% of the 3,863 reefs comprising the world's largest coral reef system. Our study bridges the gap between the theory and practice of assessing the risk of ecosystem collapse, under the emerging framework for the International Union for Conservation of Nature (IUCN) Red List of Ecosystems 3 , by rigorously defining both the initial and collapsed states, identifying the major driver of change, and establishing quantitative collapse thresholds. The increasing prevalence of post-bleaching mass mortality of corals represents a radical shift in the disturbance regimes of tropical reefs, both adding to and far exceeding the influence of recurrent cyclones and other local pulse events, presenting a fundamental challenge to the long-term future of these iconic ecosystems.

Spatial and temporal patterns of mass bleaching of corals in the Anthropocene.

Tropical reef systems are transitioning to a new era in which the interval between recurrent bouts of coral bleaching is too short for a full recovery of mature assemblages. We analyzed bleaching records at 100 globally distributed reef locations from 1980 to 2016. The median return time between pairs of severe bleaching events has diminished steadily since 1980 and is now only 6 years. As global warming has progressed, tropical sea surface temperatures are warmer now during current La Niña conditions than they were during El Niño events three decades ago. Consequently, as we transition to the Anthropocene, coral bleaching is occurring more frequently in all El Niño-Southern Oscillation phases, increasing the likelihood of annual bleaching in the coming decades.