珊瑚礁白化的因素有哪些

FUNDING: None Coral reefs are diverse and productive but sensitive ecosystems. Due to the impact of climate change, these organisms are in danger of dying out, mainly through the process of coral bleaching, which is the process by which zooxanthellae (algal endosymbionts) are expelled from their respective coral hosts, causing the coral to lose colour and become white. Coral bleaching has been linked to increases in sea surface temperatures as well as an increase in light intensity. We reviewed the different zooxanthellae taxa and their ecological traits, as well as the information available on the protective mechanisms present in zooxanthellae cells when they experience environmental stress conditions, such as temperature fluctuations, specifically concentrating on heat shock proteins and their response to antioxidant stress. The eight clades (A–H) previously recognised were reorganised into seven existing genera. Different zooxanthellae taxa exhibit different ecological traits such as their photosynthetic stress responses to light and temperature. Zooxanthellae have the ability to regulate the number and type of heat shock proteins (Hsps) they produce during a heat response. They can also regulate the host’s respective Hsps. Antioxidant responses that can prevent coral hosts from expelling the zooxanthellae, can be found both within exposed coral tissue and the zooxanthellae cells. Despite the lower likelihood of bleaching in South African coral reefs, genetic engineering presents a useful tool to understand and adapt traits within zooxanthellae genotypes to help mitigate coral bleaching in the future.

… the degeneration of zooxanthellae in situ, release of zooxanthellae from mesenterial … ) in zooxanthellae are likely to play an important role in limiting the bleaching response which is …

Impairment of the photosynthetic machinery of the algal endosymbiont ("zooxanthellae") is the proximal driver of the thermal breakdown of the coral-algae symbiosis ("coral bleaching"). Yet, the initial site of damage, and early dynamics of the impairment are still not well resolved. In this perspective essay, I consider further a recent hypothesis which proposes an energetic disruption to the carbon-concentrating mechanisms (CCMs) of the coral host, and the resultant onset of CO 2 -limitation within the photosynthetic "dark reactions" as a unifying cellular mechanism. The hypothesis identifies the enhanced retention of photosynthetic carbon for zooxanthellae (re)growth following an initial irradiance-driven expulsion event as a strong contributing cause of the energetic disruption. If true, then it implies that the onset of the bleaching syndrome and setting of upper thermal bleaching limits are emergent attributes of the coral symbiosis that are ultimately underpinned by the characteristic growth profile of the intracellular zooxanthellae; which is known to depend not just on temperature, but also external (seawater) nutrient availability and zooxanthellae genotype. Here, I review this proposed bleaching linkage at a variety of observational scales, and find it to be parsimonious with the available evidence. Future experiments are suggested that can more formally test the linkage. If correct, the new cellular model delivers a valuable new perspective to consider the future prospects of the coral symbiosis in an era of rapid environmental change, including: (i) the underpinning mechanics (and biological significance) of observed changes in resident zooxanthellae genotypes, and (ii) the now crucial importance of reef water quality in co-determining thermal bleaching resistance.

… in hospite zooxanthellae upon return to the … bleaching corals (ie, when zooxanthella densities are below approximately 2 × 10 6 cells/cm 2 ; Fig. 2), irrespective of whether the bleaching …

… of corals to bleaching varies significantly and is dependent on environmental conditions. We documented a mass coral bleaching … and measurement of coral zooxanthellae density and …

… Coral bleaching is a generic term … coral zooxanthellae and result in bleaching of the coral. Hypotheses are proposed for mechanisms involved in pigment bleaching in the zooxanthellae …

… no substantial bleaching mortality is recorded from corals on … We compared the coral–zooxanthellae associations and coral … In relation to coral bleaching, both the terms ‘adaptation’ and …

… corals to temperatures observed in coral bleaching events. We suggest a new model for coral bleaching … impairment of dark metabolism of the zooxanthellae (sink limitation), ultimately …

… we use the term bleaching only to mean loss of zooxanthellae.) … bleached corals, regardless of the severity of the bleaching or whether there is a zooxanthella type with which the coral …

… Coral bleaching is normally characterized by expulsion of the endosymbiotic zooxanthellae (the unicellular … Coral bleaching events, defined here as concomitant with very low …

… changes in zooxanthellae in bleached corals, we observed zooxanthellae in colonies of … During the last two decades there has been an increasing incidence of coral bleaching. …

… but patchy coral bleaching (expulsion of zooxanthellae by the coral host and/or … zooxanthella type harbored by the coral colonies and the extent of damage suffered from the bleaching …

… of zooxanthellae and/or photosynthetic pigments is known as coral bleaching and may cause coral … Incidences of mass coral bleaching have increased since the 1980s and was for the …

… leaching in organisms such as hard and soft corals, giant clams, and sea anemones is the loss of pigment associated with their symbiotic algae (zooxanthellae). Bleaching can be the …

The ability of coral reefs to survive the projected increases in temperature due to global warming will depend largely on the ability of corals to adapt or acclimatize to increased temperature extremes over the next few decades. Many coral species are highly sensitive to temperature stress and the number of stress (bleaching) episodes has increased in recent decades. We investigated the acclimatization potential of Acropora millepora , a common and widespread Indo-Pacific hard coral species, through transplantation and experimental manipulation. We show that adult corals, at least in some circumstances, are capable of acquiring increased thermal tolerance and that the increased tolerance is a direct result of a change in the symbiont type dominating their tissues from Symbiodinium type C to D. Our data suggest that the change in symbiont type in our experiment was due to a shuffling of existing types already present in coral tissues, not through exogenous uptake from the environment. The level of increased tolerance gained by the corals changing their dominant symbiont type to D (the most thermally resistant type known) is around 1–1.5 °C. This is the first study to show that thermal acclimatization is causally related to symbiont type and provides new insight into the ecological advantage of corals harbouring mixed algal populations. While this increase is of huge ecological significance for many coral species, in the absence of other mechanisms of thermal acclimatization/adaptation, it may not be sufficient to survive climate change under predicted sea surface temperature scenarios over the next 100 years. However, it may be enough to ‘buy time’ while greenhouse reduction measures are put in place.

Mass coral bleaching has emerged in the 21st century as the greatest threat to the health of the world's reefs. A sophisticated process understanding of bleaching at the polyp scale has now been achieved through laboratory and field studies, but this knowledge is yet to be applied in mechanistic models of shelf-scale reef systems. In this study we develop a mechanistic model of the coral-symbiont relationship that considers temperature-mediated build-up of reactive oxygen species due to excess light, leading to zooxanthellae expulsion. The model explicitly represents the coral host biomass, as well as zooxanthellae biomass, intracellular pigment concentration, nutrient status, and the state of reaction centres and the xanthophyll cycle. Photophysiological processes represented include photoadaptation, xanthophyll cycle dynamics, and reaction centre state transitions. The mechanistic model of the coral-symbiont relationship is incorporated into a ∼1 km resolution coupled hydrodynamic – biogeochemical model that encompasses the entire ∼2000 km length of the Great Barrier Reef. A simulation of the 2016 bleaching event shows the model is able to capture the broadscale features of the observed bleaching, but fails to capture bleaching on offshore reefs due to the model's grid being unable to resolve the bathymetry of shallow platforms surrounded by deep water. To further analyse the model behaviour, a ∼200 m resolution nested simulation of Davies Reef (18°49′ S, 147°38′ E) is undertaken. We use this nested model to demonstrate the depth gradient in zooxanthellae response to thermal stress. Finally, we discuss the uncertainties in the bleaching model, which lie primarily in quantifying the link between reactive oxygen build-up and the expulsion process. Through the mechanistic representation of environmental forcing, this model of coral bleaching applied in realistic environmental conditions has the potential to generate more detailed predictions than the presently-available satellite-based coral bleaching metrics, and can be used to evaluate proposed management strategies.

Caribbean corals of the Montastraea annularis species complex associate with four taxa of symbiotic dinoflagellates (zooxanthellae; genus Symbiodinium) in ecologically predictable patterns. To investigate the resilience of these host-zooxanthella associations, we conducted field experiments in which we experimentally reduced the numbers of zooxanthellae (by transplanting to shallow water or by shading) and then allowed treated corals to recover. When depletion was not extreme, recovering corals generally contained the same types of zooxanthellae as they did prior to treatment. After severe depletion, however, recovering corals were always repopulated by zooxanthellae atypical for their habitat (and in some cases atypical for the coral species). These unusual zooxanthellar associations were often (but not always) established in experimentally bleached tissues even when adjacent tissues were untreated. Atypical zooxanthellae were also observed in bleached tissues of unmanipulated Montastraea with yellow-blotch disease. In colonies where unusual associations were established, the original taxa of zooxanthellae were not detected even 9 months after the end of treatment. These observations suggest that zooxanthellae in Montastraea range from fugitive opportunists and stress-tolerant generalists (Symbiodinium A and E) to narrowly adapted specialists (Symbiodinium B and C), and may undergo succession.

For over three decades, scientists have conducted heat-stress experiments to predict how coral will respond to ocean warming due to global climate change. However, there are often conflicting results in the literature that are difficult to resolve, which we hypothesize are a result of unintended biases, variation in experimental design, and underreporting of critical methodological information. Here, we reviewed 255 coral heat-stress experiments to (1) document where and when they were conducted and on which species, (2) assess variability in experimental design, and (3) quantify the diversity of response variables measured. First, we found that two-thirds of studies were conducted in only three countries, three coral species were more heavily studied than others, and only 4% of studies focused on earlier life stages. Second, slightly more than half of all heat-stress exposures were less than 8 d in duration, only 17% of experiments fed corals, and experimental conditions varied widely, including the level and rate of temperature increase, light intensity, number of genets used, and the length of acclimation period. In addition, 95%, 55%, and > 35% of studies did not report tank flow conditions, light–dark cycle used, or the date of the experiment, respectively. Finally, we found that 21% of experiments did not measure any bleaching phenotype traits, 77% did not identify the Symbiodiniaceae endosymbiont, and the contribution of the coral host in the physiological response to heat-stress was often not investigated. This review highlights geographic, taxonomic, and heat-stress duration biases in our understanding of coral bleaching, and large variability in the reporting and design of heat-stress experiments that could account for some of the discrepancies in the literature. Development of some best practice recommendations for coral bleaching experiments could improve cross-studies comparisons and increase the efficiency of coral bleaching research at a time when it is needed most.

The global coral bleaching event of 2014–2017 resulted from the latest in a series of heat stress events that have increased in intensity. We assessed global- and basin-scale variations in sea surface temperature-based heat stress products for 1985–2017 to provide the context for how heat stress during 2014–2017 compared with the past 3 decades. Previously, undefined “Heat Stress Year” periods (used to describe interannual variation in heat stress) were identified for the Northern and Southern Hemispheres, in which heat stress peaks during or shortly after the boreal and austral summers, respectively. The proportion of reef pixels experiencing bleaching-level heat stress increased through the record, accelerating during the last decade. This increase in accumulated heat stress at a bleaching level is a result of longer stress events rather than an increase in the peak stress intensity. Thresholds of heat stress extent for the three tropical ocean basins were established to designate “global” events, and a Global Bleaching Index was defined that relates heat stress extent to that observed in 1998. Notably, during the 2014–2017 global bleaching event, more than three times as many reefs were exposed to bleaching-level heat stress as in the 1998 global bleaching.

Coral bleaching is the breakdown of symbiosis between coral animal hosts and their dinoflagellate algae symbionts in response to environmental stress. On large spatial scales, heat stress is the most common factor causing bleaching, which is predicted to increase in frequency and severity as the climate warms. There is evidence that the temperature threshold at which bleaching occurs varies with local environmental conditions and background climate conditions. We investigated the influence of past temperature variability on coral susceptibility to bleaching, using the natural gradient in peak temperature variability in the Gilbert Islands, Republic of Kiribati. The spatial pattern in skeletal growth rates and partial mortality scars found in massive Porites sp. across the central and northern islands suggests that corals subject to larger year-to-year fluctuations in maximum ocean temperature were more resistant to a 2004 warm-water event. In addition, a subsequent 2009 warm event had a disproportionately larger impact on those corals from the island with lower historical heat stress, as indicated by lower concentrations of triacylglycerol, a lipid utilized for energy, as well as thinner tissue in those corals. This study indicates that coral reefs in locations with more frequent warm events may be more resilient to future warming, and protection measures may be more effective in these regions.

The National Oceanic and Atmospheric Administration (NOAA) Coral Reef Watch (CRW) program has been providing resource managers, scientific researchers, and other coral reef ecosystem stakeholders with coral bleaching heat stress products for more than 20 years. The development of the CoralTemp sea surface temperature (SST) dataset has allowed CRW to produce the Coral Bleaching Heat Stress product suite with climatologies and daily SST measurements from within the same SST dataset, significantly improving data quality. Previously, the Monthly Mean (MM) SST and Maximum Monthly Mean (MMM) SST climatologies were derived using a different dataset from the near real-time SST. Here we provide an up-to-date description of how each product within the Coral Reef Watch Coral Bleaching Heat Stress product suite version 3.1 is derived, including descriptions of the MM, MMM, SST Anomaly, Coral Bleaching HotSpot and Degree Heating Week (DHW) products.

Abstract The global loss and degradation of coral reefs, as a result of intensified frequency and severity of bleaching events, is a major concern. Evidence of heat stress affecting corals through loss of symbionts and consequent coral bleaching was first reported in the 1930s. However, it was not until the 1998 major global bleaching event that the urgency for heat stress studies became internationally recognized. Current efforts focus not only on examining the consequences of heat stress on corals but also on finding strategies to potentially improve thermal tolerance and aid coral reefs survival in future climate scenarios. Although initial studies were limited in comparison with modern technological tools, they provided the foundation for many of today's research methods and hypotheses. Technological advancements are providing new research prospects at a rapid pace. Understanding how coral heat stress studies have evolved is important for the critical assessment of their progress. This review summarizes the development of the field to date and assesses avenues for future research.

… stress plays a mechanistic role in the process of sea-surface temperature-related coral bleaching, we examined corals … by unusually high sea-surface temperatures. We observed strong …

Ocean warming threatens the functioning of coral reef ecosystems by inducing mass coral bleaching and mortality events. The link between temperature and coral bleaching is now well-established based on observations that mass bleaching events usually occur when seawater temperatures are anomalously high. However, times of high heat stress but without coral bleaching are equally important because they can inform an understanding of factors that regulate temperature-induced bleaching. Here, we investigate the absence of mass coral bleaching on the Great Barrier Reef (GBR) during austral summer 2004. Using four gridded sea surface temperature data products, validated with in situ temperature loggers, we demonstrate that the summer of 2004 was among the warmest summers of the satellite era (1982-2017) on the GBR. At least half of the GBR experienced temperatures that were high enough to initiate bleaching in other years, yet mass bleaching was not reported during 2004. The absence of bleaching is not fully explained by wind speed or cloud cover. Rather, 2004 is clearly differentiated from bleaching years by the slow speed of the East Australian Current (EAC) offshore of the GBR. An anomalously slow EAC during summer 2004 may have dampened the upwelling of nutrient-rich waters onto the GBR shelf, potentially mitigating bleaching due to the lower susceptibility of corals to heat stress in low-nutrient conditions. Although other factors such as irradiance or acclimatization may have played a role in the absence of mass bleaching, 2004 remains a key case study for demonstrating the dynamic nature of coral responses to marine heatwaves.

In the 1980s and early 1990s, coral reef bleaching events of unprecedented frequency and global extent were observed. Elevated water temperature is suspected as the primary causal stress of mass bleaching events from this period. The relationship between sea surface temperatures (SSTs) and coral bleaching events was investigated using National Oceanic and Atmospheric Administration (NOAA) Multi-Channel Sea Surface Temperature (MCSST) satellite imagery from 1982-1992. Nighttime MCSST weekly averages were compared with moored-buoy temperatures for sea-truthing the satellite. Average errors from 11 individual buoy comparisons throughout the tropics were found to be approximately 0.5bC. Confirmed satellite SST data were applied to bleaching events at Bermuda (1988, 1991), Tahiti (1984, 1987, 1991), and Jamaica (1987, 1989, 1990), with a non-bleached site off Belize selected as control. MCSST data showed elevated SSTs coincided with bleaching events both in onset and duration. Bleaching thresholds were developed. An MCSST Degree Heating Weeks (DHW) bleaching index was developed for the Belizean and Jamaican reef sites. A cumulative heating stress of 26 DHW is proposed as the threshold for mass reef bleaching at Belize and Jamaica.

… Coral Bleaching Alert Area has two levels: Alert Level 1 (heat stress indicates significant coral bleaching) and Alert Level 2 (heat stress indicates widespread coral bleaching and …

… of the cause of stress [46]. For example, corals bleach in response to high temperature, high light or … Furthermore, it is not known whether FPs can provide relief from heat stress alone. …

… complex and interacting responses of temperature and geography for coral bleaching. … resistance to heat stress. Understanding past and emerging mechanisms of coral bleaching are, …

… complex and interacting responses of temperature and geography for coral bleaching. … resistance to heat stress. Understanding past and emerging mechanisms of coral bleaching are, …

… temperatures that are responsible for basin- to global-scale … in heat stress and patterns of coral bleaching. Furthermore, the latest advances in satellite-based sea surface temperature …

… the role of oxidative stress during high temperature-induced bleaching in corals. Previous … stress in the photoinhibition of cultured zooxanthellae exposed to elevated temperatures by …

Climate change and warming ocean temperatures are a threat to coral reef ecosystems. Since the 1980s, there has been an increase in mass coral bleaching and associated coral mortality due to more frequent and severe thermal stress. Although most research has focused on the role of temperature, coral bleaching is a product of the interacting effects of temperature and other environmental variables such as solar radiation. High light exacerbates the effects of thermal stress on corals, whereas reductions in light can reduce sensitivity to thermal stress. Here, we use an updated global dataset of coral bleaching observations (n = 35,769) from 1985 to 2017 and satellite‐derived datasets of SST and clouds to examine for the first time at a global scale the influence of cloudiness on the likelihood of bleaching from thermal stress. We find that among coral reefs exposed to severe bleaching‐level heat stress (Degree Heating Weeks >8°Cˑweek), bleaching severity is inversely correlated with the interaction of heat stress and cloud fraction anomalies (p < 0.05), such that higher cloudiness implies reduced bleaching response. A Random Forest model analysis employing different set of environmental variables shows that a model employing Degree Heating Weeks and the 30‐day cloud fraction anomaly most accurately predicts bleaching severity (Accuracy = 0.834; Cohen's Kappa = 0.769). Based on these results and global warm‐season cloudiness patterns, we develop a ‘cloudy refugia’ index which identifies the central equatorial Pacific and French Polynesia as regions where cloudiness is most likely to protect corals from bleaching. Our findings suggest that incorporating cloudiness into prediction models can help delineate bleaching responses and identify reefs which may be more resilient to climate change.

… Coral bleaching due to thermal and environmental stress threatens coral reefs and possibly people who rely on their resources. Here we explore patterns of coral bleaching and …

The National Oceanic and Atmospheric Administration’s Coral Reef Watch program developed and operates several global satellite products to monitor bleaching-level heat stress. While these products have a proven ability to predict the onset of most mass coral bleaching events, they occasionally miss events; inaccurately predict the severity of some mass coral bleaching events; or report false alarms. These products are based solely on temperature and yet coral bleaching is known to result from both temperature and light stress. This study presents a novel methodology (still under development), which combines temperature and light into a single measure of stress to predict the onset and severity of mass coral bleaching. We describe here the biological basis of the Light Stress Damage (LSD) algorithm under development. Then by using empirical relationships derived in separate experiments conducted in mesocosm facilities in the Mexican Caribbean we parameterize the LSD algorithm and demonstrate that it is able to describe three past bleaching events from the Great Barrier Reef (GBR). For this limited example, the LSD algorithm was able to better predict differences in the severity of the three past GBR bleaching events, quantifying the contribution of light to reduce or exacerbate the impact of heat stress. The new Light Stress Damage algorithm we present here is potentially a significant step forward in the evolution of satellite-based bleaching products.

The coral-dinoflagellate endosymbiosis is based on nutrient exchanges that impact holobiont energetics. Of particular concern is the breakdown or dysbiosis of this partnership that is seen in response to elevated temperatures, where loss of symbionts through coral bleaching can lead to starvation and mortality. Here we extend a dynamic bioenergetic model of coral symbioses to explore the mechanisms by which temperature impacts various processes in the symbiosis and to enable simulational analysis of thermal bleaching. Our model tests the effects of two distinct mechanisms for how increased temperature impacts the symbiosis: 1) accelerated metabolic rates due to thermodynamics and 2) damage to the photosynthetic machinery of the symbiont caused by heat stress. Model simulations show that the model can capture key biological responses to different levels of increased temperatures. Moderately increased temperatures increase metabolic rates and slightly decrease photosynthesis. The slightly decreased photosynthesis rates cause the host to receive less carbon and share more nitrogen with the symbiont. This results in temporarily increased symbiont growth and a higher symbiont/host ratio. In contrast, higher temperatures cause a breakdown of the symbiosis due to escalating feedback that involves further reduction in photosynthesis and insufficient energy supply for CO2\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\hbox {CO}_2$$\end{document} concentration by the host. This leads to the accumulation of excess light energy and the generation of reactive oxygen species, eventually triggering symbiont expulsion and coral bleaching. Importantly, bleaching does not result from accelerated metabolic rates alone; it only occurs as a result of the photodamage mechanism due to its effect on nutrient cycling. Both higher light intensities and higher levels of DIN render corals more susceptible to heat stress. Conversely, heterotrophic feeding can increase the maximal temperature that can be tolerated by the coral. Collectively these results show that a bioenergetics model can capture many observed patterns of heat stress in corals, such as higher metabolic rates and higher symbiont/host ratios at moderately increased temperatures and symbiont expulsion at strongly increased temperatures.

Coral bleaching is a significant contributor to the worldwide degradation of coral reefs and is indicative of the termination of symbiosis between the coral host and its symbiotic algae (dinoflagellate; Symbiodinium sp. complex), usually by expulsion or xenophagy (symbiophagy) of its dinoflagellates. Herein, we provide evidence that during the earliest stages of environmentally induced bleaching, heat stress and light stress generate distinctly different pathomorphological changes in the chloroplasts, while a combined heat- and light-stress exposure induces both pathomorphologies; suggesting that these stressors act on the dinoflagellate by different mechanisms. Within the first 48 hours of a heat stress (32°C) under low-light conditions, heat stress induced decomposition of thylakoid structures before observation of extensive oxidative damage; thus it is the disorganization of the thylakoids that creates the conditions allowing photo-oxidative-stress. Conversely, during the first 48 hours of a light stress (2007 µmoles m−2 s−1 PAR) at 25°C, condensation or fusion of multiple thylakoid lamellae occurred coincidently with levels of oxidative damage products, implying that photo-oxidative stress causes the structural membrane damage within the chloroplasts. Exposure to combined heat- and light-stresses induced both pathomorphologies, confirming that these stressors acted on the dinoflagellate via different mechanisms. Within 72 hours of exposure to heat and/or light stresses, homeostatic processes (e.g., heat-shock protein and anti-oxidant enzyme response) were evident in the remaining intact dinoflagellates, regardless of the initiating stressor. Understanding the sequence of events during bleaching when triggered by different environmental stressors is important for predicting both severity and consequences of coral bleaching.

… for coral thermal stress experiments … coral species, populations or genotypes, as heat stress assays vary widely in duration and temperature, ranging from chronic, lower-temperature …

Significance Corals are disappearing worldwide due to both local and global stressors. Yet, our understanding of the interaction among these two types of stressors is limited, hindering efforts to conserve coral reefs. With a large dataset at a seascape scale across Moorea, French Polynesia, we showed that coral bleaching was more severe as both heat stress and nitrogen pollution increased. We also found that corals bleached more severely at comparatively low heat stress if they lived where nitrogen pollution was high. Thus, given that nitrogen pollution worsens the severity of coral bleaching, even during mild heat stress events, there is a critical need to address both local and global threats to coral reefs. Climate change is increasing the frequency and magnitude of temperature anomalies that cause coral bleaching, leading to widespread mortality of stony corals that can fundamentally alter reef structure and function. However, bleaching often is spatially variable for a given heat stress event, and drivers of this heterogeneity are not well resolved. While small-scale experiments have shown that excess nitrogen can increase the susceptibility of a coral colony to bleaching, we lack evidence that heterogeneity in nitrogen pollution can shape spatial patterns of coral bleaching across a seascape. Using island-wide surveys of coral bleaching and nitrogen availability within a Bayesian hierarchical modeling framework, we tested the hypothesis that excess nitrogen interacts with temperature anomalies to alter coral bleaching for the two dominant genera of branching corals in Moorea, French Polynesia. For both coral genera, Pocillopora and Acropora, heat stress primarily drove bleaching prevalence (i.e., the proportion of colonies on a reef that bleached). In contrast, the severity of bleaching (i.e., the proportion of an individual colony that bleached) was positively associated with both heat stress and nitrogen availability for both genera. Importantly, nitrogen interacted with heat stress to increase bleaching severity up to twofold when nitrogen was high and heat stress was relatively low. Our finding that excess nitrogen can trigger severe bleaching even under relatively low heat stress implies that mitigating nutrient pollution may enhance the resilience of coral communities in the face of mounting stresses from global climate change.

Tropical corals live close to their upper thermal limit making them vulnerable to unusually warm summer sea temperatures. The resulting thermal stress can lead to breakdown of the coral-algal symbiosis, essential for the functioning of reefs, and cause coral bleaching. Mass coral bleaching is a modern phenomenon associated with increases in reef temperatures due to recent global warming. Widespread bleaching has typically occurred during El Niño events. We examine the historical level of stress for 100 coral reef locations with robust bleaching histories. The level of thermal stress (based on a degree heating month index, DHMI) at these locations during the 2015–2016 El Niño was unprecedented over the period 1871–2017 and exceeded that of the strong 1997–1998 El Niño. The DHMI was also 5 times the level of thermal stress associated with the ‘pre-industrial’, 1877–1878, El Niño. Coral reefs have, therefore, already shown their vulnerability to the modest (~0.92 °C) global warming that has occurred to date. Estimates of future levels of thermal stress suggest that even the optimistic 1.5 °C Paris Agreement target is insufficient to prevent more frequent mass bleaching events for the world’s reefs. Effectively, reefs of the future will not be the same as those of the past.

Satellite monitoring of thermal stress on coral reefs has become an essential component of reef management practice around the world. A recent development by the U.S. National Oceanic and Atmospheric Administration’s Coral Reef Watch (NOAA CRW) program provides daily global monitoring at 5 km resolution—at or near the scale of most coral reefs. In this paper, we introduce two new monitoring products in the CRW Decision Support System for coral reef management: Regional Virtual Stations, a regional synthesis of thermal stress conditions, and Seven-day Sea Surface Temperature (SST) Trend, describing recent changes in temperature at each location. We describe how these products provided information in support of management activities prior to, during and after the 2014 thermal stress event in the Commonwealth of the Northern Mariana Islands (CNMI). Using in situ survey data from this event, we undertake the first quantitative comparison between 5 km satellite monitoring products and coral bleaching observations. Analysis of coral community characteristics, historical temperature conditions and thermal stress revealed a strong influence of coral biodiversity in the patterns of observed bleaching. This resulted in a model based on thermal stress and generic richness that explained 97% of the variance in observed bleaching. These findings illustrate the importance of using local benthic characteristics to interpret the level of impact from thermal stress exposure. In an era of continuing climate change, accurate monitoring of thermal stress and prediction of coral bleaching are essential for stakeholders to direct resources to the most effective management actions to conserve coral reefs.

Coral reefs are a globally threatened ecosystem due to a range of anthropogenic impacts. Increasing sea surface temperatures associated with global warming are a particular threat, as corals grow close to their upper thermal limit. When this limit is exceeded for a sufficient length of time during thermal stress events, corals lose their algal symbionts, resulting in coral bleaching and possible mortality. Coral reefs have experienced the most severe and extended global bleaching event to date from 2014 to 2017. The most recent global climate models predict that similar global bleaching events are likely to become an annual occurrence by the middle of the present century. Current understanding of coral reef recovery following disturbance events is based around decadal to sub-decadal impacts, making the adaptive capacity of corals as bleaching events approach an annual frequency unknown. However, there is considerable spatial heterogeneity in bleaching impacts across a range of scales, from global reef provinces to local reef areas and between coral species. Understanding of the mechanisms responsible for this observed coral resilience to thermal stress is increasing in a variety of disciplines, with particular recent advances at the sub-cellular level, facilitated partly by technological developments. This understanding suggests that some resilience factors have the potential to operate within the predicted annual frequency of thermal stress events, whilst others act over longer time-scales. The ability of coral reef management actions to successfully support coral resilience is a significant challenge and requires increased empirical evidence to support and refine actions. However, in addition to essential global actions to reduce carbon dioxide emissions, protective actions can be strengthened by a focus on identifying reef locations that have the potential to exhibit resilience to thermal stress events, either via resisting them or recovering quickly following impact. Here, we present a spatially explicit overview of the potential resilience factors and mechanisms that can be considered in such an approach.

The U.S. National Oceanic and Atmospheric Administration (NOAA) Coral Reef Watch (CRW) program has developed a daily global 5-km product suite based on satellite observations to monitor thermal stress on coral reefs. These products fulfill requests from coral reef managers and researchers for higher resolution products by taking advantage of new satellites, sensors and algorithms. Improvements of the 5-km products over CRW’s heritage global 50-km products are derived from: (1) the higher resolution and greater data density of NOAA’s next-generation operational daily global 5-km geo-polar blended sea surface temperature (SST) analysis; and (2) implementation of a new SST climatology derived from the Pathfinder SST climate data record. The new products increase near-shore coverage and now allow direct monitoring of 95% of coral reefs and significantly reduce data gaps caused by cloud cover. The 5-km product suite includes SST Anomaly, Coral Bleaching HotSpots, Degree Heating Weeks and Bleaching Alert Area, matching existing CRW products. When compared with the 50-km products and in situ bleaching observations for 2013–2014, the 5-km products identified known thermal stress events and matched bleaching observations. These near reef-scale products significantly advance the ability of coral reef researchers and managers to monitor coral thermal stress in near-real-time.

Background The rising temperature of the world's oceans has become a major threat to coral reefs globally as the severity and frequency of mass coral bleaching and mortality events increase. In 2005, high ocean temperatures in the tropical Atlantic and Caribbean resulted in the most severe bleaching event ever recorded in the basin. Methodology/Principal Findings Satellite-based tools provided warnings for coral reef managers and scientists, guiding both the timing and location of researchers' field observations as anomalously warm conditions developed and spread across the greater Caribbean region from June to October 2005. Field surveys of bleaching and mortality exceeded prior efforts in detail and extent, and provided a new standard for documenting the effects of bleaching and for testing nowcast and forecast products. Collaborators from 22 countries undertook the most comprehensive documentation of basin-scale bleaching to date and found that over 80% of corals bleached and over 40% died at many sites. The most severe bleaching coincided with waters nearest a western Atlantic warm pool that was centered off the northern end of the Lesser Antilles. Conclusions/Significance Thermal stress during the 2005 event exceeded any observed from the Caribbean in the prior 20 years, and regionally-averaged temperatures were the warmest in over 150 years. Comparison of satellite data against field surveys demonstrated a significant predictive relationship between accumulated heat stress (measured using NOAA Coral Reef Watch's Degree Heating Weeks) and bleaching intensity. This severe, widespread bleaching and mortality will undoubtedly have long-term consequences for reef ecosystems and suggests a troubled future for tropical marine ecosystems under a warming climate.

Coral reefs across the world’s oceans are in the midst of the longest bleaching event on record (from 2014 to at least 2016). As many of the world’s reefs are remote, there is limited information on how past thermal conditions have influenced reef composition and current stress responses. Using satellite temperature data for 1985–2012, the analysis we present is the first to quantify, for global reef locations, spatial variations in warming trends, thermal stress events and temperature variability at reef-scale (~4 km). Among over 60,000 reef pixels globally, 97% show positive SST trends during the study period with 60% warming significantly. Annual trends exceeded summertime trends at most locations. This indicates that the period of summer-like temperatures has become longer through the record, with a corresponding shortening of the ‘winter’ reprieve from warm temperatures. The frequency of bleaching-level thermal stress increased three-fold between 1985–91 and 2006–12 – a trend climate model projections suggest will continue. The thermal history data products developed enable needed studies relating thermal history to bleaching resistance and community composition. Such analyses can help identify reefs more resilient to thermal stress.

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.

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 Kd490, 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.

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.

… The onset and occurrence of this coral bleaching is primarily defined via the … that thermal stress responses occur in the coral host tissues in the days before the onset of coral bleaching. …

… Coral bleaching, as presently defined … coral±algal complex, including response to thermal stress. Three general types of high-temperature bleaching are defined: physiological bleaching…

The response of coral-reef ecosystems to contemporary thermal stress may be in part a consequence of recent or historical sea-surface temperature (SST) variability. To test this hypothesis, we examined whether: (i) there was a relationship between the historical frequency of SST variability and stress experienced during the most recent thermal-stress events (in 1998 and 2005–2006) and (ii) coral reefs that historically experienced frequent thermal anomalies were less likely to experience coral bleaching during these recent thermal-stress events. Examination of nine detrended coral δ 18 O and Sr/Ca anomaly records revealed a high- (5.7-year) and low-frequency (&gt;54-year) mode of SST variability. There was a positive relationship between the historical frequency of SST anomalies and recent thermal stress; sites historically dominated by the high-frequency mode experienced greater thermal stress than other sites during both events, and showed extensive coral bleaching in 1998. Nonetheless, in 2005–2006, corals at sites dominated by high-frequency variability showed reduced bleaching, despite experiencing high thermal stress. This bleaching resistance was most likely a consequence of rapid directional selection that followed the extreme thermal event of 1998. However, the benefits of regional resistance could come at the considerable cost of shifts in coral species composition.

SUMMARYThe mutualistic relationship between corals and their unicellular dinoflagellate symbionts (Symbiodinium sp.) is a fundamental component within the ecology of coral reefs. Thermal stress causes the breakdown of the relationship between corals and their symbionts (bleaching). As with other organisms, this symbiosis may acclimate to changes in the environment, thereby potentially modifying the environmental threshold at which they bleach. While a few studies have examined the acclimation capacity of reef-building corals, our understanding of the underlying mechanism is still in its infancy. The present study focused on the role of recent thermal history in influencing the response of both corals and symbionts to thermal stress, using the reef-building coral Acropora aspera. The symbionts of corals that were exposed to 31°C for 48 h (pre-stress treatment) 1 or 2 weeks prior to a 6-day simulated bleaching event (when corals were exposed to 34°C) were found to have more effective photoprotective mechanisms. These mechanisms included changes in non-photochemical quenching and xanthophyll cycling. These differences in photoprotection were correlated with decreased loss of symbionts, with those corals that were not prestressed performing significantly worse, losing over 40% of their symbionts and having a greater reduction in photosynthetic efficiency. These results are important in that they show that thermal history, in addition to light history, can influence the response of reef-building corals to thermal stress and therefore have implications for the modeling of bleaching events. However, whether acclimation is capable of modifying the thermal threshold of corals sufficiently to cope as sea temperatures increase in response to global warming has not been fully explored. Clearly increases in sea temperatures that extend beyond 1–2°C will exhaust the extent to which acclimation can modify the thermal threshold of corals.

… understanding of coral bleaching. Although high seawater temperature is widely accepted as the primary trigger of coral bleaching, irradiance is also known to trigger coral bleaching (…

… irradiances increase Q m and when exposed to thermal stress result in an increase in ROS and coral bleaching, but under low irradiances … leading to coral bleaching. This suggests that …

… responsible for coral bleaching in colonies … UV light levels possible at 24 m. On the basis of the attenuation coefficients for the clearest oceanic waters", and the highest UV irradiances …

… This irradiance was the same maximum daily irradiance measured at the collection site. Four treatments were tested in each of the two temperatures. The treatments were dim with UV (…

The photoacclimation of endolithic algae (of the genus Ostreobium ) inhabiting the skeleton of the Mediterranean coral Oculina patagonica during a bleaching event was examined. Pulse amplitude modulated (PAM) chlorophyll fluorescence techniques in situ were used to assess the photosynthetic efficiency of endolithic algae in the coral skeleton and the symbiotic dinoflagellates (zooxanthellae) in the coral tissue. Relative photosynthetic electron transport rates (ETRs) of the endolithic algae under bleached areas of the colony were significantly higher than those of endolithic algae from a healthy section of the colony and those of zooxanthellae isolated from the same section. Endolithic algae under healthy parts of the colony demonstrated an ETRmax of 16.5% that of zooxanthellae from tissue in the same section whereas endolithic algae under bleached sections showed ETRmax values that were 39% of those found for healthy zooxanthellae. The study demonstrates that endolithic algae undergo photoacclimation with increased irradiance reaching the skeleton. As PAM fluorometry has become a major tool for assessing levels of stress and bleaching in corals, the importance of considering the contribution of the endolithic algae to the overall chlorophyll fluorescence measured is highlighted.

… cause bleaching in tropical corals, we therefore test the underlying premize that warm water … excess irradiance alone can cause the dissociation of the coral-algal symbiosis (bleaching). …

… large-scale coral reef bleaching are elevated sea temperatures and high solar irradiance (especially ultraviolet … Finally, experimentally reduced light levels also cause coral bleaching. …

… through the interactive effects of high temperature and exposure to high irradiances of solar radiation on the zooxanthellae of corals. Subsequently, a multifactorial experiment showed …

… Coral bleaching events are often associated with higher levels of coral mortality but when … Underwater light levels decreased from peak irradiances approaching ∼650 μmol quanta m 2 …

Abstract Marine heatwaves occurring against the backdrop of rising global sea surface temperatures have triggered mass coral bleaching and mortality. Irradiance is critical to coral growth but is also an implicating factor in photodamage, leading to the expulsion of symbiotic algae under increased temperatures. Numerical modelling is a valuable tool that can provide insight into the state of the symbiont photochemistry during coral bleaching events. However, very few numerical physiological models combine the influence of light and temperature for simulating coral bleaching. The coral bleaching model used was derived from the coral bleaching representation in the eReefs configuration of the CSIRO Environmental Modelling Suite, with the most significant change being the equation for the rate of detoxification of reactive oxygen species. Simulated physiological bleaching outcomes from the model were compared to photochemical bleaching proxies measured during an ex situ moderate degree-heating week (up to 4.4) experiment. The bleaching response of Acropora divaricata was assessed in an unshaded and 30% shade treatment. The model-simulated timing for the onset of bleaching under elevated temperatures closely corresponded with an initial photochemical decline as observed in the experiment. Increased bleaching severity under elevated temperature and unshaded light was also simulated by the model, an outcome confirmed in the experiment. This is the first experimental validation of a temperature-mediated, light-driven model of coral bleaching from the perspective of the symbiont. When forced by realistic environmental conditions, process-based mechanistic modelling could improve accuracy in predicting heterogeneous bleaching outcomes during contemporary marine heatwave events and future climate change scenarios. Mechanistic modelling will be invaluable in evaluating management interventions for deployment in coral reef environments.

… of coral bleaching is … solar irradiance, reduced water quality, and mortality risks are unclear. Here, we analyze the effects of high temperature, irradiance, and sediment loading on coral …

Warm-water growth and survival of corals are constrained by a set of environmental conditions such as temperature, light, nutrient levels and salinity. Water temperatures of 1 to 2°C above the usual summer maximum can trigger a phenomenon known as coral bleaching, whereby disruption of the symbiosis between coral and dinoflagellate micro-algae, living within the coral tissue, reveals the white skeleton of coral. Anomalously cold water can also lead to coral bleaching but has been the subject of limited research. Although cold-water bleaching events are less common, they can produce similar impacts on coral reefs as warm-water events. In this study, we explored the effect of temperature and light on the likelihood of cold-water coral bleaching from 1998-2017 using available bleaching observations from the Eastern Tropical Pacific and the Florida Keys. Using satellite-derived sea surface temperature, photosynthetically available radiation and light attenuation data, cold temperature and light exposure metrics were developed and then tested against the bleaching observations using logistic regression. The results show that cold-water bleaching can be best predicted with an accumulated cold-temperature metric, i.e. ‘degree cooling weeks’, analogous to the heat stress metric ‘degree heating weeks’, with high accuracy (90%) and fewer Type I and Type II errors in comparison with other models. Although light, when also considered, improved prediction accuracy, we found that the most reliable framework for cold-water bleaching prediction may be based solely on cold-temperature exposure.

… stresses, such as sustained high temperatures, may destabilize the symbiosis. Coral bleaching is linked to oxidative stress of the coral … or synergistically to elevate oxidative stress. The …

Ocean warming is resulting in increased occurrence of mass coral bleaching; a response in which the intracellular algal endosymbionts (Symbiodinium sp.) are expelled from the coral host due to physiological stress. This detrimental process is often attributed to overproduction of reactive oxygen species (ROS) that leak out of the endosymbionts and causes damage to the host cell, though direct evidence validating this link is limited. Here, for the first time, we used confocal microscopy and fluorescent dyes to investigate if endosymbiont ROS production significantly and predictably affects physiological parameters in its host cell. Heat treatment resulted in a 60% reduction in coral symbiont density, a ~70% increase in median endosymbiont ROS and a small reduction in photosystem efficiency (FV/FM, 11%), indicating absence of severe light stress. Notably, no other physiological parameters were affected in either endosymbionts or host cells, including reduced glutathione and ROS-induced lipid peroxidation. Taken together, the increase in endosymbiont ROS could not be linked to physiological damage in either partner, suggesting that oxidative stress is unlikely to have been the driver for symbiont expulsion in this study.

… of the same coral (Pocillopora capitata). We examined markers of oxidative stress, including lipid peroxidation (MDA) and superoxide dismutase (SOD) activity, indicators of bleaching, …

This review discusses the evidence for the involvement of superoxide radical, hydrogen peroxide and singlet oxygen (reactive oxygen species, ROS) as triggers for coral bleaching. …

The intracellular coral–dinoflagellate symbiosis is the engine that underpins the success of coral reefs, one of the most diverse ecosystems on the planet. However, the breakdown of the symbiosis and the loss of the microalgal symbiont (i.e. coral bleaching) due to environmental changes are resulting in the rapid degradation of coral reefs globally. There is an urgent need to understand the cellular physiology of coral bleaching at the mechanistic level to help develop solutions to mitigate the coral reef crisis. Here, at an unprecedented scope, we present novel models that integrate putative mechanisms of coral bleaching within a common framework according to the triggers (initiators of bleaching, e.g. heat, cold, light stress, hypoxia, hyposalinity), cascades (cellular pathways, e.g. photoinhibition, unfolded protein response, nitric oxide), and endpoints (mechanisms of symbiont loss, e.g. apoptosis, necrosis, exocytosis/vomocytosis). The models are supported by direct evidence from cnidarian systems, and indirectly through comparative evolutionary analyses from non‐cnidarian systems. With this approach, new putative mechanisms have been established within and between cascades initiated by different bleaching triggers. In particular, the models provide new insights into the poorly understood connections between bleaching cascades and endpoints and highlight the role of a new mechanism of symbiont loss, i.e. ‘symbiolysosomal digestion’, which is different from symbiophagy. This review also increases the approachability of bleaching physiology for specialists and non‐specialists by mapping the vast landscape of bleaching mechanisms in an atlas of comprehensible and detailed mechanistic models. We then discuss major knowledge gaps and how future research may improve the understanding of the connections between the diverse cascade of cellular pathways and the mechanisms of symbiont loss (endpoints).

Elevated seawater temperatures associated with climate change lead to coral bleaching. While the ultimate causes of bleaching are well understood, the proximate physiological mechanisms underlying the bleaching response are not as well defined. Here we measured nitric oxide synthase activity, oxidative stress, and cell death in algal symbionts (Symbiodinaceae) freshly isolated from the reef-building coral Pocillopora acuta collected in the field under natural non-bleaching conditions and from corals experimentally exposed to elevated temperatures. Nitric oxide synthase activity in the algal symbionts was >3 orders of magnitude higher than that of the host and increased dramatically with increasing temperature and time of exposure (up to 72 h), consistent with the onset of bleaching for these corals. Oxidative stress and cell death among the algal symbionts were highest in coral holobionts exposed to intermediate as opposed to maximal temperatures, suggesting that these mechanisms are not proximal triggers for bleaching in this species. Our results point to nitric oxide production by the algal symbionts, rather than symbiont dysfunction, as a more important driver of coral bleaching under acute thermal stress in this coral.

To survive in nutrient-poor waters corals rely on a symbiotic association with intracellular microalgae. However, increased sea temperatures cause algal loss—known as coral bleaching—often followed by coral death. Some of the most compelling evidence in support of the ‘oxidative stress theory of coral bleaching’ comes from studies that exposed corals, cultures of their algal endosymbionts, or the coral model Exaiptasia diaphana to exogenous antioxidants during thermal stress. Here, we replicate these experiments using E. diaphana with the addition of the antioxidants ascorbate + catalase, catechin, or mannitol under ambient and elevated temperatures along with an antioxidant-free control. In the absence of exogenous antioxidants, E. diaphana exposed to elevated temperatures bleached with no change in reactive oxygen species (ROS) levels associated with their microalgal cells. Ascorbate + catalase and mannitol treatments rescued the anemones from bleaching, although microalgal ROS levels increased in these antioxidant treatments under elevated temperature conditions. While bleaching was not associated with changes in net ROS for the intracellular algal symbionts, it is evident from our findings that excess ROS is connected to the bleaching phenotype as exogenous antioxidants were successful in mitigating the effects of thermal stress in cnidarians. This understanding may assist applied research that aims to reduce the impact of climate change on coral reefs.

Abstract The third global-scale coral bleaching event, triggered by the 2015–2016 El Nino, presented unprecedented levels of thermal stress and bleaching occurrence. Identification of potential cellular biomarkers in key reef species can greatly improve coral reef resource manager’s ability to make ecological forecasts and develop efficient mitigation strategies. In this context, the present study evaluated ecologically relevant biochemical parameters involved in thermal-stress response in two important reef building species of southwestern Atlantic Reefs – the scleractinian coral Mussismilia harttii and the hydrocoral Millepora alcicornis – aiming to assess their potential to forecast bleaching occurrence in corals/hydrocorals. Bleaching frequency, lipid peroxidation (LPO) and total antioxidant capacity (TAC), as well as thermal stress parameters (Degree Heating Weeks, DHW), were monitored during a six-month period in a reef area under influence of the 2015–2016 El Nino event. LPO is suggested as an informative, cost-effective and logical complement to reef monitoring programs; and TAC basal level as a potential measurement for predicting corals/hydrocorals susceptibility to bleaching. Further, results indicate M. alcicornis as a promising bioindicator in South Atlantic reefs. Findings presented here are expected to improve South Atlantic coral reef monitoring programs, as well as to contribute with potential biomarker-monitoring techniques to be used as additional tools in traditional reef monitoring programs worldwide. Further, observations on oxidative stress responses of a hydrocoral undergoing thermal stress conditions in the field are reported here for the first time.

SUMMARYCnidarian bleaching is a breakdown in the mutualistic symbiosis between host Cnidarians, such as reef building corals, and their unicellular photosynthetic dinoflagellate symbionts. Bleaching is caused by a variety of environmental stressors, most notably elevated temperatures associated with global climate change in conjunction with high solar radiation, and it is a major contributor to coral death and reef degradation. This review examines the underlying cellular events that lead to symbiosis dysfunction and cause bleaching, emphasizing that, to date, we have only some pieces of a complex cellular jigsaw puzzle. Reactive oxygen species (ROS), generated by damage to both photosynthetic and mitochondrial membranes, is shown to play a central role in both injury to the partners and to inter-partner communication of a stress response. Evidence is presented that suggests that bleaching is a host innate immune response to a compromised symbiont, much like innate immune responses in other host–microbe interactions. Finally, the elimination or exit of the symbiont from host tissues is described through a variety of mechanisms including exocytosis, host cell detachment and host cell apoptosis.

… as oxidative stress, in most cases bleaching is driven primarily by direct impacts on one partner or the other. There is evidence of oxidative stress taking place within the coral holobiont …

Chavanich, S., Viyakarn, V., Loyjiw, T., Pattaratamrong, P., and Chankong, A. 2009. Mass bleaching of soft coral, Sarcophyton spp. in Thailand and the role of temperature and salinity stress. – ICES Journal of Marine Science, 66: 1515–1519. From June to October 2006 and 2007, mass bleaching of the soft coral, Sarcophyton spp., occurred for the first time in the upper Gulf of Thailand. Approximately 90% of the populations experienced extensive bleaching, and almost 95% of colonies were affected. Field observations also revealed that fragmentation of Sarcophyton spp. set in 1 month after the onset of bleaching. Some colonies started to recover to some extent by the end of July, with 95% of the population of Sarcophyton spp. recovering by October. Both acute and chronic trials were conducted to determine whether temperature and/or salinity triggered bleaching. In the acute tests, Sarcophyton spp. at 40°C and salinity 20 psu were completely bleached, and death occurred after 57 and 204 h, respectively. However, the colonies at 40 psu could survive through the experimental trial. In the chronic tests, Sarcophyton spp. died when exposed to 34°C, whereas complete bleaching and mortality of Sarcophyton spp. occurred at salinities of 10 and 49 psu. We conclude that elevated temperatures had a greater effect on the bleaching of Sarcophyton spp. than did salinity.

… , and coral bleaching occurred up to … stresses, expecially temperature.8489 However, little information is available on the effects of sublethal salinity stress on reef corals or other coral …

… of the coral-algal symbiosis (coral bleaching) occurred during exposure to reduced-salinity … when considering that corals may experience salinity stress in combination with other factors …

ABSTRACT The endosymbiosis between dinoflagellate algae of the genus Symbiodinium and stony corals provides the foundation of coral reef ecosystems. Coral bleaching, the expulsion of endosymbionts from the coral host tissue as a consequence of heat or light stress, poses a threat to reef ecosystem functioning on a global scale. Hence, a better understanding of the factors contributing to heat stress susceptibility and tolerance is needed. In this regard, some of the most thermotolerant corals live in particularly saline habitats, but possible effects of high salinity on thermotolerance in corals are anecdotal. Here we test the hypothesis that high salinity may lead to increased thermotolerance. We conducted a heat stress experiment at low, intermediate, and high salinities using a set of host-endosymbiont combinations of the coral model Aiptasia. As expected, all host-endosymbiont combinations showed reduced photosynthetic efficiency and endosymbiont loss during heat stress, but the severity of bleaching was significantly reduced with increasing salinities for one of the host-endosymbiont combinations. Our results show that higher salinities can convey increased thermotolerance in Aiptasia, although this effect seems to be dependent on the particular host strain and/or associated symbiont type. This finding may help explain the extraordinarily high thermotolerance of corals in high salinity environments, such as the Red Sea and the Persian/Arabian Gulf, and provides novel insight regarding factors that contribute to thermotolerance. Since our results are based on a salinity effect in symbiotic sea anemones, it remains to be determined whether this salinity effect can also be observed in stony corals. Summary: High salinity can be a factor contributing to increased cnidarian thermal tolerance, as indicated by reduced algal endosymbiont loss and reduced photosynthetic impairment in the sea anemone Aiptasia. This article has an associated First Person interview with the first author of the paper as part of the supplementary information.

… In Seriatopora caliendrum the Hsp60 modulation reflects the severity and length of the salinity stress. … In an extreme hyposalinity condition corals showed necrotic tissues and bleaching. …

… that corals exposed to hypo-saline conditions can undergo extensive bleaching and … As with other types of environmental stresses, exposure to hypo-saline conditions may have …

… Under several extraordinary or “stress” conditions, corals rapidly lose their … with coral bleaching. Two of these studies attributed localized coral bleaching to reduced seawater salinities …

Large-scale coral bleaching events have become increasingly frequent in recent years. This process occurs when corals are exposed to high temperatures and intense light stress, leading to an overproduction of reactive oxygen species (ROS) by their endosymbiotic dinoflagellates. The ROS buildup prompts corals to expel these symbiotic microalgae, resulting in the corals’ discoloration. Reducing ROS production and enhancing detoxification processes in these microalgae are crucial to prevent the collapse of coral reef ecosystems. However, research into the cell physiology and genetics of coral symbiotic dinoflagellates has been hindered by challenges associated with cloning these microalgae. A procedure for cloning coral symbiotic dinoflagellates was developed in this study. Several species of coral symbionts were successfully cloned, with two of them further characterized. Experiments with the two species isolated from Turbinaria sp. showed that damage from light intensity at 340 μmol photons/m2/s was more severe than from high temperature at 36 °C. Additionally, preincubation in high salinity conditions activated their endogenous tolerance to bleaching stress. Pretreatment at 50 ppt salinity reduced the percentage of cells stained for ROS by 59% and 64% in the two species under bleaching stress compared to those incubated at 30 ppt. Furthermore, their Fv’/Fm’ during the recovery period showed a significant improvement compared to the controls. These findings suggest that intense light plays a more important role than high temperatures in coral bleaching by enhancing ROS generation in the symbiotic dinoflagellates. The findings also suggest the genomes of coral symbiotic dinoflagellates have undergone evolutionary processes to develop mechanisms, regulated by gene expression, to mitigate damages caused by high temperature and high light stress. Understanding this gene expression regulation could contribute to strengthening corals’ resilience against the impact of global climate change.

Coral reefs can experience salinity fluctuations due to rainfall and runoff; these events can have major impacts on the corals and lead to bleaching and mortality. On the Great Barrier Reef (GBR), low salinity events, which occur during summer seasons and can involve salinity dropping ~ 10 PSU correlate with declines in coral cover, and these events are predicted to increase in frequency and severity under future climate change scenarios. In other marine invertebrates, exposure to low salinity causes increased expression of genes involved in proteolysis, responses to oxidative stress, and membrane transport, but the effects that changes in salinity have on corals have so far received only limited attention. To better understand the coral response to hypo-osmotic stress, here we investigated the transcriptomic response of the coral Acropora millepora in both adult and juvenile life stages to acute (1 h) and more prolonged (24 h) exposure to low salinity. Differential gene expression analysis revealed the involvement of both common and specific response mechanisms in Acropora. The general response to environmental stressors included up-regulation of genes involved in the mitigation of macromolecular and oxidative damage, while up-regulation of genes involved in amino acid metabolism and transport represent specific responses to salinity stress. This study is the first comprehensive transcriptomic analysis of the coral response to low salinity stress and provides important insights into the likely consequences of heavy rainfall and runoff events on coral reefs.

… heat stress. This study provides the first detailed map of metabolic pathways transition in corals in response to different environmental stresses, … and mitigate against coral bleaching. …

Coral cover has been declining in recent decades due to increased temperatures and environmental stressors. However, the extent to which different stressors contribute both individually and in concert to bleaching and mortality is still very uncertain. We develop and use a novel regression approach, using non-linear parametric models that control for unobserved time invariant effects to estimate the effects on coral bleaching and mortality due to temperature, solar radiation, depth, hurricanes and anthropogenic stressors using historical data from a large bleaching event in 2005 across the Caribbean. Two separate models are created, one to predict coral bleaching, and the other to predict near-term mortality. A large ensemble of supporting data is assembled to control for omitted variable bias and improve fit, and a significant improvement in fit is observed from univariate linear regression based on temperature alone. The results suggest that climate stressors (temperature and radiation) far outweighed direct anthropogenic stressors (using distance from shore and nearby human population density as a proxy for such stressors) in driving coral health outcomes during the 2005 event. Indeed, temperature was found to play a role ~4 times greater in both the bleaching and mortality response than population density across their observed ranges. The empirical models tested in this study have large advantages over ordinary-least squares–they offer unbiased estimates for censored data, correct for spatial correlation, and are capable of handling more complex relationships between dependent and independent variables. The models offer a framework for preparing for future warming events and climate change; guiding monitoring and attribution of other bleaching and mortality events regionally and around the globe; and informing adaptive management and conservation efforts.

Abstract Global warming is leading to both increases in frequency and intensity of tropical storms, with consequent salinity decrease at shallow reef areas, but also to mass bleaching events and mortality of reef-building corals around the world. Tropical storms can help reef-building corals to reproduce through fragmentation, allowing their expansion throughout the reefs. The combination of high temperature and low salinity may aggravate the effects of coral bleaching. Investigation of alterations at the cellular level will be useful since this is the first detectable response of organisms to changes in environmental conditions. In this study, the long-term oxidative stress induced by elevated temperature (30 °C), low salinity (20 psu), and their combination was studied on fragments of reef-forming corals, and compared to control conditions (26 °C, 33 psu). Determination of oxidative stress biomarkers: lipid peroxidation (LPO); superoxide dismutase (SOD), catalase (CAT) and glutathione S-transferase (GST) activities in a long-term experiment (60 days), using nine Indo-Pacific reef-forming coral species, provided useful information that was interpreted in combination with the observed general condition of these organisms (appearance: normal, pale, bleached, dead). High temperature affected the general condition of the species tested to a lower degree than did low salinity. Only two species died at high temperature, while low salinity resulted in the death of all species with the exception of two (P. contigua and G. fascicularis). Oxidative damage was detected in some species, as were antioxidant responses, at high temperature. Coral general condition was severely affected in all species in the low salinity treatment. Galaxea fascicularis and Psammocora contigua were the most resistant to salinity stress, having survived the experimental treatment. Oxidative damage was not detected in these species, but there was an antioxidant response. The high temperature + low salinity (HT + LS) treatment had synergistic effects in the condition of all species. Galaxea fascicularis was the only survivor in the HT + LS treatment. Mortality was high (60%) for this species, oxidative damage was not detected, but an increase in SOD activity revealed an antioxidant response.

… corals Acropora sp. and Stylophora pistillata. Physiological parameters and biochemical markers related to corals' … impacts of elevated salinity on the fitness of coral species. Associated …

… enough, can result in bleaching. Increased temperature and … of bleaching, but other factors like salinity can also stress the … salinity has been increasing in shallow waters where corals …

Sea temperatures in many tropical regions have increased by almost 1°C over the past 100 years, and are currently increasing at ~1–2°C per century. Coral bleaching occurs when the thermal tolerance of corals and their photosynthetic symbionts (zooxanthellae) is exceeded. Mass coral bleaching has occurred in association with episodes of elevated sea temperatures over the past 20 years and involves the loss of the zooxanthellae following chronic photoinhibition. Mass bleaching has resulted in significant losses of live coral in many parts of the world. This paper considers the biochemical, physiological and ecological perspectives of coral bleaching. It also uses the outputs of four runs from three models of global climate change which simulate changes in sea temperature and hence how the frequency and intensity of bleaching events will change over the next 100 years. The results suggest that the thermal tolerances of reef-building corals are likely to be exceeded every year within the next few decades. Events as severe as the 1998 event, the worst on record, are likely to become commonplace within 20 years. Most information suggests that the capacity for acclimation by corals has already been exceeded, and that adaptation will be too slow to avert a decline in the quality of the world’s reefs. The rapidity of the changes that are predicted indicates a major problem for tropical marine ecosystems and suggests that unrestrained warming cannot occur without the loss and degradation of coral reefs on a global scale.

The interaction between local, anthropogenic stressors, and larger scale regional/global stressors, is often used to explain the current poor condition of many corals reefs. This form of cumulative pressure is clearly manifested by situations where dredging projects happen to coincide with marine heatwaves that have caused coral bleaching. A key pressure associated with dredging is elevated sedimentation. In this study, 3 coral species (Acropora millepora, Porites spp. and Turbinaria reniformis), representing three common morphologies (branching, massive and foliose respectively), were experimentally induced to bleach by exposure to a temperature of 31 °C for 21 d. The corals were then subjected to a range of sedimentation rates (0, 11, 22 and 40 mg cm−2 d−1), and their sediment-rejection ability quantified after 1 and 7 successive sediment deposition events. Bleached corals were less capable of removing sediments from their surfaces, and sediment accumulated 3 to 4-fold more than on normally-pigmented corals. Repeated deposition resulted in a ~3-fold increase in the amount of sediment remaining on the corals, regardless of bleaching status. These results suggest that adaptive management practices need to be developed to reduce the impacts of future dredging projects that follow or coincide with elevated sea surface temperatures and coral bleaching events.

Understanding pressure pathways and their cumulative impacts is critical for developing effective environmental policy. For coral reefs, wide spread bleaching resulting from global warming is occurring concurrently with local pressures, such as increases in suspended sediments through coastal development. Here we examine the relative importance of suspended sediment pressure pathways for dredging impacts on corals and evidence for synergistic or antagonistic cumulative effects between suspended sediments and thermal stress. We show that low to moderate reductions in available light associated with dredging may lead to weak antagonistic (less than expected independently) cumulative effects. However, when sediment loads are high any reductions in mortality associated with reduced bleaching are outweighed by increased mortality associated with severe low light periods and high levels of sediment deposition and impacts become synergistic (greater than what would occur independently). The findings suggest efforts to assess global cumulative impacts need to consider how pressures interact to impact ecosystems, and that the cumulative outcome may vary across the range of realised pressure fields. Multiple aspects of anthropogenic change threaten coral reefs. Here, the authors show that bleaching associated with thermal stress was low when local dredging released moderate amounts of suspended sediments, but high sediment loads coupled with high temperatures had synergistic negative effects on coral survival.

The federal channel at Port of Miami, Florida, USA, was dredged between late 2013 and early 2015 to widen and deepen the channel. Due to the limited spatial extent of impact-assessment monitoring associated with the project, the extent of the dredging impacts on surrounding coral reefs has not been well quantified. Previously published remote sensing analyses, as well as agency and anecdotal reports suggest the most severe and largest area of sedimentation occurred on a coral reef feature referred to as the Inner Reef, particularly in the sector north of the channel. A confounding regional warm-water mass bleaching event followed by a coral disease outbreak during this same time frame made the assessment of dredging-related impacts to coral reefs adjacent to the federal channel difficult but still feasible. The current study sought to better understand the sedimentation impacts that occurred in the coral reef environment surrounding Port of Miami, to distinguish those impacts from other regional events or disturbances, and provide supplemental information on impact assessment that will inform discussions on compensatory mitigation requirements. To this end, in-water field assessments conducted after the completion of dredging and a time series analysis of tagged corals photographed pre-, during, and post-dredging, are used to discern dredging-related sedimentation impacts for the Inner Reef north. Results indicate increased sediment accumulation, severe in certain times and places, and an associated biological response (e.g., higher prevalence of partial mortality of corals) extended up to 700 m from the channel, whereas project-associated monitoring was limited to 50 m from the channel. These results can contribute to more realistic prediction of areas of indirect effect from dredging projects needed to accurately evaluate proposed projects and design appropriate compliance monitoring. Dredging projects near valuable and sensitive habitats subject to local and global stressors require monitoring methods capable of discerning non-dredging related impacts and adaptive management to ensure predicted and unpredicted project-related impacts are quantified. Anticipated increasing frequency and intensity of seasonal warming stress also suggests that manageable- but- unavoidable local stressors such as dredging should be partitioned from such seasonal thermal stress events.

… of poor water quality in lowering the upper thermal bleaching limits of symbiotic reef corals. … loading and the upper thermal bleaching thresholds of the inshore reefs of the Great Barrier …

Climate change, pollution and increased runoff are some of the main drivers of coral reefs degradation worldwide. However, the occurrence of runoff and marine pollution, as well as its ecological effects in South Atlantic coral reefs are still poorly understood. The aim of the present work is to characterize the terrigenous influence and contamination impact on the environmental health of five reefs located along a gradient of distance from a river source, using geochemical, water quality, and ecological indicators. Stable isotopes and sterols were used as geochemical indicators of sewage and terrigenous organic matter. Dissolved metal concentrations (Cu, Zn, Cd, and Pb) were used as indicators of water quality. Population density, bleaching and chlorophyll α content of the symbiont-bearing foraminifer Amphistegina gibbosa, were used as indicators of ecological effects. Sampling was performed four times during the year to assess temporal variability. Sediment and water quality indicators showed that reefs close to the river discharge experience nutrient enrichment and sewage contamination, and metals concentrations above international environmental quality guidelines. Higher levels of contamination were strongly related to the higher frequency of bleaching and lower density in A. gibbosa populations. The integrated evaluation of stable isotopes, sterols and metals provided a consistent diagnostic about sewage influence on the studied reefs. Additionally, the observed bioindicator responses evidenced relevant ecological effects. The water quality, geochemical and ecological indicators employed in the present study were effective as biomonitoring tools to be applied in reefs worldwide.

… discuss case histories of sewage pollution in coral-reef systems. Next, the … coral-reef recovery from disturbance, our current understanding of sewage pollution in relation to coral reefs …

Effective environmental management requires monitoring programmes that provide specific links between changes in environmental conditions and ecosystem health. This article reviews the suitability of a range of bioindicators for use in monitoring programmes that link changes in water quality to changes in the condition of coral-reef ecosystems. From the literature, 21 candidate bioindicators were identified, whose responses to changes in water quality varied spatially and temporally; responses ranged from rapid (hours) changes within individual corals to long-term (years) changes in community composition. From this list, the most suitable bioindicators were identified by determining whether responses were (i) specific, (ii) monotonic, (iii) variable, (iv) practical and (v) ecologically relevant to management goals. For long-term monitoring programmes that aim to quantify the effects of chronic changes in water quality, 11 bioindicators were selected: symbiont photophysiology, colony brightness, tissue thickness and surface rugosity of massive corals, skeletal elemental and isotopic composition, abundance of macro-bioeroders, micro- and meiobenthic organisms such as foraminifera, coral recruitment, macroalgal cover, taxonomic richness of corals and the maximal depth of coral-reef development. For short-term monitoring programmes, or environmental impact assessments that aim to quantify the effects of acute changes in water quality, a subset of seven of these bioindicators were selected, including partial mortality. Their choice will depend on the specific objectives and the timeframe available for each monitoring programme. An assessment framework is presented to assist in the selection of bioindicators to quantify the effects of changing water quality on coral-reef ecosystems.

There is a need to identify effective coral bioindicators that provide quantifiable links between changes in water quality and the condition of coastal coral reefs. Temporal variation in a range of coral bioindicators including symbiont density, concentration of chlorophyll a, skeletal density and colony brightness of Pocillopora damicornis, as well as colony brightness and density of macro-bioeroders of massive Porites spp. was examined for 2 years on a coastal coral reef of the Great Barrier Reef. The specificity to changes in water quality varied among bioindicators. For example, a 2.5-fold variation in symbiont density of P. damicornis was related strongly to mean 14-day sea surface temperature and seasonal changes in water quality, suggesting medium specificity to changes in water quality. In contrast, the density of macro-bioeroders in Porites did not vary seasonally but there were consistently more macro-bioeroders at the coastal than mid-shelf reference locations, suggesting high specificity of spatial differences in water quality. In situ measurements of benthic irradiance and turbidity allowed the quantification of potential stress thresholds for coastal corals. Our data suggest long-term turbidity &amp;gt;3 NTU leads to sublethal stress, whereas long-term turbidity &amp;gt;5 NTU corresponds to severe stress effects on corals at shallow depths.

Abstract Ocean warming has severe impacts on coral reef ecosystems with frequent incidences of coral bleaching. In addition, eutrophication poses an increasing threat to coral reef environments and has been found to increase the vulnerability of corals to thermal bleaching. Eutrophication has accelerated in recent years with coastal nutrient loads expected to continue to increase under global change. However, the mechanisms by which nutrient pollution affects corals and coral reefs are still under debate, in particular with regard to nitrogen. The main objective of this paper is to review mechanisms by which nitrogen pollution affects coral health and corresponding strategies to reduce the impact of nitrogen pollution. Different coral species possess varying tolerance thresholds for nitrogen enrichment and corals show differential responses to enrichment with nitrate and ammonium. Nitrate assimilation increases oxidative stress in corals, promotes growth of the phototrophic symbionts in corals, and induces phosphate starvation in these symbionts, which further impairs the symbiosis. In contrast, a moderate supply of ammonium is mostly beneficial for coral development. In addition, combined nitrogen and phosphorous enrichment can indirectly compromise coral health by enhancing macroalgae growth and increasing the incidence of coral diseases caused by predation on corals. It must be realized that both levels of nutrient pollution and the stoichiometric ratios of C: N: P: Fe availabilities determine the ultimate effect of nutrients on coral health. We confirm the strategy to conserve coral reefs via coral-targeted water quality management, in particular by including a reduction of the nitrate influx and by proper management of fish stocks to facilitate healthy reef ecology.