Thermal refugia against coral bleaching throughout the northern Red Sea

Tropical reefs have been impacted by thermal anomalies caused by global warming that induced coral bleaching and mortality events globally. However, there have only been very few recordings of bleaching within the Red Sea despite covering a latitudinal range of 15° and consequently it has been considered a region that is less sensitive to thermal anomalies. We therefore examined historical patterns of sea surface temperature (SST) and associated anomalies (1982–2012) and compared warming trends with a unique compilation of corresponding coral bleaching records from throughout the region. These data indicated that the northern Red Sea has not experienced mass bleaching despite intensive Degree Heating Weeks (DHW) of >15°C‐weeks. Severe bleaching was restricted to the central and southern Red Sea where DHWs have been more frequent, but far less intense (DHWs <4°C‐weeks). A similar pattern was observed during the 2015–2016 El Niño event during which time corals in the northern Red Sea did not bleach despite high thermal stress (i.e. DHWs >8°C‐weeks), and bleaching was restricted to the central and southern Red Sea despite the lower thermal stress (DHWs < 8°C‐weeks). Heat stress assays carried out in the northern (Hurghada) and central (Thuwal) Red Sea on four key reef‐building species confirmed different regional thermal susceptibility, and that central Red Sea corals are more sensitive to thermal anomalies as compared to those from the north. Together, our data demonstrate that corals in the northern Red Sea have a much higher heat tolerance than their prevailing temperature regime would suggest. In contrast, corals from the central Red Sea are close to their thermal limits, which closely match the maximum annual water temperatures. The northern Red Sea harbours reef‐building corals that live well below their bleaching thresholds and thus we propose that the region represents a thermal refuge of global importance.     

A coral reef refuge in the Red Sea

The stability and persistence of coral reefs in the decades to come is uncertain due to global warming and repeated bleaching events that will lead to reduced resilience of these ecological and socio‐economically important ecosystems. Identifying key refugia is potentially important for future conservation actions. We suggest that the Gulf of Aqaba (GoA) (Red Sea) may serve as a reef refugium due to a unique suite of environmental conditions. Our hypothesis is based on experimental detection of an exceptionally high bleaching threshold of northern Red Sea corals and on the potential dispersal of coral planulae larvae through a selective thermal barrier estimated using an ocean model. We propose that millennia of natural selection in the form of a thermal barrier at the southernmost end of the Red Sea have selected coral genotypes that are less susceptible to thermal stress in the northern Red Sea, delaying bleaching events in the GoA by at least a century.     

Large-amplitude internal waves benefit corals during thermal stress

Tropical scleractinian corals are particularly vulnerable to global warming as elevated sea surface temperatures (SSTs) disrupt the delicate balance between the coral host and their algal endosymbionts, leading to symbiont expulsion, mass bleaching and mortality. While satellite sensing of SST has proved a reliable predictor of coral bleaching at the regional scale, there are large deviations in bleaching severity and mortality on the local scale that are poorly understood. Here, we show that internal waves play a major role in explaining local coral bleaching and mortality patterns in the Andaman Sea. Despite a severe region-wide SST anomaly in May 2010, frequent upslope intrusions of cold sub-pycnocline waters due to breaking large-amplitude internal waves (LAIW) mitigated coral bleaching and mortality in shallow waters. In LAIW-sheltered waters, by contrast, bleaching-susceptible species suffered severe bleaching and total mortality. These findings suggest that LAIW benefit coral reefs during thermal stress and provide local refugia for bleaching-susceptible corals. LAIW are ubiquitous in tropical stratified waters and their swash zones may thus be important conservation areas for the maintenance of coral diversity in a warming climate. Taking LAIW into account can significantly improve coral bleaching predictions and provide a valuable tool for coral reef conservation and management.     

Incorporating adaptive responses into future projections of coral bleaching

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

Large-amplitude internal waves sustain coral health during thermal stress

Ocean warming is a major threat for coral reefs causing widespread coral bleaching and mortality. Potential refugia are thus crucial for coral survival. Exposure to large-amplitude internal waves (LAIW) mitigated heat stress and ensured coral survival and recovery during and after an extreme heat anomaly. The physiological status of two common corals, Porites lutea and Pocillopora meandrina, was monitored in host and symbiont traits, in response to LAIW-exposure throughout the unprecedented 2010 heat anomaly in the Andaman Sea. LAIW-exposed corals of both species survived and recovered, while LAIW-sheltered corals suffered partial and total mortality in P. lutea and P. meandrina, respectively. LAIW are ubiquitous in the tropics and potentially generate coral refuge areas. As thermal stress to corals is expected to increase in a warming ocean, the mechanisms linking coral bleaching to ocean dynamics will be crucial to predict coral survival on a warming planet.     

Climate‐change refugia: shading reef corals by turbidity

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

Turbid reefs moderate coral bleaching under climate‐related temperature stress

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

Interpreting the sign of coral bleaching as friend vs. foe

Coral bleaching is a major concern to researchers, conservationists and the general public worldwide. To date, much of the high profile attention for bleaching has coincided with major environmental impacts and for many the term coral bleaching is synonymously associated with coral mortality (so‐called ‘lethal’ bleaching episodes). While this synonymous association has undoubtedly been key in raising public support, it carries unfair representation: nonlethal bleaching is, and always has been, a phenomenon that effectively occurs regularly in nature as corals acclimatize to regular periodic changes in growth environment (days, seasons etc). In addition, corals can exhibit sublethal bleaching during extreme environmental conditions whereby mortality does not occur and corals can potentially subsequently recover once ambient environmental conditions return. Perhaps not surprisingly it is the frequency and extent of these non and sublethal processes that yield key evidence as to how coral species and reef systems will likely withstand environmental and thus climatic change. Observations of non and sublethal bleaching (and subsequent recovery) are arguably not as readily reported as those of lethal bleaching since (1) the convenient tools used to quantify bleaching yield major ambiguity (and hence high potential for misidentification) as to the severity of bleaching; and (2) lethal bleaching events inevitably receive higher profile (media) attention and so are more readily reported. Under‐representation of non and sublethal bleaching signs may over‐classify the severity of bleaching, under‐estimate the potential resilience of reefs against environmental change, and thus ultimately limit (if not depreciate) the validity and effectiveness of reef management policies and practices. While bleaching induced coral mortality must remain our key concern it must be better placed within the context of bleaching signs that do not result in a long‐term loss of reef viability.     

Coral reef bleaching: ecological perspectives

Coral reef bleaching, the whitening of diverse invertebrate taxa, results from the loss of symbiotic zooxanthellae and/or a reduction in photosynthetic pigment concentrations in zooxanthellae residing within the gastrodermal tissues of host animals. Of particular concern are the consequences of bleaching of large numbers of reef-building scleractinian corals and hydrocorals. Published records of coral reef bleaching events from 1870 to the present suggest that the frequency (60 major events from 1979 to 1990), scale (co-occurrence in many coral reef regions and often over the bathymetric depth range of corals) and severity (>95% mortality in some areas) of recent bleaching disturbances are unprecedented in the scientific literature. The causes of small scale, isolated bleaching events can often be explained by particular stressors (e.g., temperature, salinity, light, sedimentation, aerial exposure and pollutants), but attempts to explain large scale bleaching events in terms of possible global change (e.g., greenhouse warming, increased UV radiation flux, deteriorating ecosystem health, or some combination of the above) have not been convincing. Attempts to relate the severity and extent of large scale coral reef bleaching events to particular causes have been hampered by a lack of (a) standardized methods to assess bleaching and (b) continuous, long-term data bases of environmental conditions over the periods of interest. An effort must be made to understand the impact of bleaching on the remainder of the reef community and the long-term effects on competition, predation, symbioses, bioerosion and substrate condition, all factors that can influence coral recruitment and reef recovery. If projected rates of sea warming are realized by mid to late AD 2000, i.e. a 2°C increase in high latitude coral seas, the upper thermal tolerance limits of many reef-building corals could be exceeded. Present evidence suggests that many corals would be unable to adapt physiologically or genetically to such marked and rapid temperature increases.     

Caribbean mesophotic coral ecosystems are unlikely climate change refugia

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

Forecasted coral reef decline in marine biodiversity hotspots under climate change

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

The dynamics of architectural complexity on coral reefs under climate change

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

Differential thermal tolerance between algae and corals may trigger the proliferation of algae in coral reefs

Marine heatwaves can lead to rapid changes in entire communities, including in the case of shallow coral reefs the potential overgrowth of algae. Here we tested experimentally the differential thermal tolerance between algae and coral species from the Red Sea through the measurement of thermal performance curves and the assessment of thermal limits. Differences across functional groups (algae vs. corals) were apparent for two key thermal performance metrics. First, two reef‐associated algae species (Halimeda tuna and Turbinaria ornata) had higher lethal thermal limits than two coral species (Pocillopora verrucosa and Stylophora pistillata) conferring those species of algae with a clear advantage during heatwaves by surpassing the thermal threshold of coral survival. Second, the coral species had generally greater deactivation energies for net and gross primary production rates compared to the algae species, indicating greater thermal sensitivity in corals once the optimum temperature is exceeded. Our field surveys in the Red Sea reefs before and after the marine heatwave of 2015 show a change in benthic cover mainly in the southern reefs, where there was a decrease in coral cover and a concomitant increase in algae abundance, mainly turf algae. Our laboratory and field observations indicate that a proliferation of algae might be expected on Red Sea coral reefs with future ocean warming.     

Standardized short‐term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites

Coral bleaching is one of the main drivers of reef degradation. Most corals bleach and suffer mortality at just 1–2°C above their maximum monthly mean temperatures, but some species and genotypes resist or recover better than others. Here, we conducted a series of 18‐hr short‐term acute heat stress assays side‐by‐side with a 21‐day long‐term heat stress experiment to assess the ability of both approaches to resolve coral thermotolerance differences reflective of in situ reef temperature thresholds. Using a suite of physiological parameters (photosynthetic efficiency, coral whitening, chlorophyll a, host protein, algal symbiont counts, and algal type association), we assessed bleaching susceptibility of Stylophora pistillata colonies from the windward/exposed and leeward/protected sites of a nearshore coral reef in the central Red Sea, which had previously shown differential mortality during a natural bleaching event. Photosynthetic efficiency was most indicative of the expected higher thermal tolerance in corals from the protected reef site, denoted by an increased retention of dark‐adapted maximum quantum yields at higher temperatures. These differences were resolved using both experimental setups, as corroborated by a positive linear relationship, not observed for the other parameters. Notably, short‐term acute heat stress assays resolved per‐colony (genotype) differences that may have been masked by acclimation effects in the long‐term experiment. Using our newly developed portable experimental system termed the Coral Bleaching Automated Stress System (CBASS), we thus highlight the potential of mobile, standardized short‐term acute heat stress assays to resolve fine‐scale differences in coral thermotolerance. Accordingly, such a system may be suitable for large‐scale determination and complement existing approaches to identify resilient genotypes/reefs for downstream experimental examination and prioritization of reef sites for conservation/restoration. Development of such a framework is consistent with the recommendations of the National Academy of Sciences and the Reef Restoration and Adaptation Program committees for new intervention and restoration strategies.     

Coral bleaching is linked to the capacity of the animal host to supply essential metals to the symbionts

Massive coral bleaching events result in extensive coral loss throughout the world. These events are mainly caused by seawater warming, but are exacerbated by the subsequent decrease in nutrient availability in surface waters. It has therefore been shown that nitrogen, phosphorus or iron limitation contribute to the underlying conditions by which thermal stress induces coral bleaching. Generally, information on the trophic ecology of trace elements (micronutrients) in corals, and on how they modulate the coral response to thermal stress is lacking. Here, we demonstrate for the first time that heterotrophic feeding (i.e. the capture of zooplankton prey by the coral host) and thermal stress induce significant changes in micro element concentrations and isotopic signatures of the scleractinian coral Stylophora pistillata. The results obtained first reveal that coral symbionts are the major sink for the heterotrophically acquired micronutrients and accumulate manganese, magnesium and iron from the food. These metals are involved in photosynthesis and antioxidant protection. In addition, we show that fed corals can maintain high micronutrient concentrations in the host tissue during thermal stress and do not bleach, whereas unfed corals experience a significant decrease in copper, zinc, boron, calcium and magnesium in the host tissue and bleach. In addition, the significant increase in δ⁶⁵Cu and δ⁶⁶Zn signature of symbionts and host tissue at high temperature suggests that these isotopic compositions are good proxy for stress in corals. Overall, present findings highlight a new way in which coral heterotrophy and micronutrient availability contribute to coral resistance to global warming and bleaching.     

Copper enrichment reduces thermal tolerance of the highly resistant Red Sea coral Stylophora pistillata

Coral Reefs - Corals in the Gulf of Aqaba (GoA) in the northern Red Sea show high thermal tolerance. The GoA has therefore been suggested as a coral reef refuge from climate change. However, as a...     

Impact of marine heatwaves for sea turtle nest temperatures

There are major concerns about the ecological impact of extreme weather events. In the oceans, marine heatwaves (MHWs) are an increasing threat causing, for example, recent devastation to coral reefs around the world. We show that these impacts extend to adjacent terrestrial systems and could negatively affect the breeding of endangered species. We demonstrate that during an MHW that resulted in major coral bleaching and mortality in a large, remote marine protected area, anomalously warm temperatures also occurred on sea turtle nesting beaches. Granger causality testing showed that variations in sea surface temperature strongly influenced sand temperatures on beaches. We estimate that the warm conditions on both coral reefs and sandy beaches during the MHW were unprecedented in the last 70 years. Model predictions suggest that the most extreme female-biased hatchling sex ratio and the lowest hatchling survival in nests in the last 70 years both occurred during the heatwave. Our work shows that predicted increases in the frequency and intensity of MHWs will likely have growing impacts on sea turtle nesting beaches as well as other terrestrial coastal environments.     

Century‐scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold

Coral bleaching, during which corals lose their symbiotic dinoflagellates, appears to be increasing in frequency and geographic extent, and is typically associated with abnormally high water temperatures and solar irradiance. A key question in coral reef ecology is whether local stressors reduce the coral thermal tolerance threshold, leading to increased bleaching incidence. Using tree‐ring techniques, we produced master chronologies of growth rates in the dominant reef builder, massive Montastraea faveolata corals, over the past 75–150 years from the Mesoamerican Reef. Our records indicate that the 1998 mass bleaching event was unprecedented in the past century, despite evidence that water temperatures and solar irradiance in the region were as high or higher mid‐century than in more recent decades. We tested the influence on coral extension rate from the interactive effects of human populations and thermal stress, calculated here with degree‐heating‐months (DHM). We find that when the effects of chronic local stressors, represented by human population, are taken into account, recent reductions in extension rate are better explained than when DHM is used as the sole predictor. Therefore, the occurrence of mass bleaching on the Mesoamerican reef in 1998 appears to stem from reduced thermal tolerance due to the synergistic impacts of chronic local stressors.     

Different responses of scleractinian coral Acropora pruinosa from Weizhou Island during extreme high temperature events

Ecological surveys observe coral “winners” and “losers” in global coral bleaching events. However, the key contributors to holobiont tolerance and interactions between symbionts remain unclear. Herein, we compared bleaching and unbleaching Acropora pruinosa corals from Weizhou Island, during an extreme high-temperature event in the northern South China Sea in 2020. We found the dominant Symbiodiniaceae subclade in the bleaching and unbleaching corals to be C1; however, the density of Symbiodiniaceae in the latter was significantly higher than that in the former. Additionally, the symbiotic bacteria α diversity in the unbleaching coral was significantly higher than that in the bleaching coral, with a reorganized bacterial community structure. Core microbiome analyses revealed 55 bacterial core operational taxonomic units (OTUs), of which 10 were significantly differentially enriched between the two coral groups. The significantly enriched bacterial core OTUs in the unbleaching coral were primarily nitrogen cycling related, while those enriched in the bleaching coral were associated with antimicrobial activity. RNA-Seq analyses revealed that significantly upregulated genes in the bleaching coral were primarily associated with diseases and autophagy, while those in the unbleaching coral were associated with immune defense and maintenance of the symbiotic relationship between corals and symbionts. We propose that the differences in tolerance of A. pruinosa result from the cooperation between coral host, Symbiodiniaceae, and symbiotic bacteria. In extreme high-temperature events, unbleaching corals may maintain stable symbiotic relationships by increasing the diversity of symbiotic bacteria, regulating the structure of the symbiotic bacteria community, improving the interaction between coral host and symbiont and enhancing host immunity, thus avoiding coral bleaching. This study illuminates the relationship between the coral symbiont and tolerance differences of coral holobionts, providing new insights for further exploration into the adaptability of scleractinian corals in the context of global warming.