Oxidative stress causes coral bleaching during exposure to elevated temperatures

 Elevated temperatures and solar ultraviolet (UV) radiation have been implicated as recent causes for the loss of symbiotic algae (i.e., bleaching) in corals and other invertebrates with photoautotrophic symbionts. One hypothesized mechanism of coral bleaching involves the production of reduced oxygen intermediates, or toxic oxygen, in the dinoflagellate symbionts and host tissues that subsequently causes cellular damage and expulsion of symbionts. Measurements of photosynthesis in the Caribbean coral Agaricia tenuifolia, taken during temperature-induced stress and exposure to full solar radiation, showed a decrease in photosynthetic performance followed by bleaching. Exposure of corals to exogenous antioxidants that scavenge reactive oxygen species during temperature-induced stress improves maximum photosynthetic capacity to rates indistinguishable from corals measured at the ambient temperature of their site of collection. Additionally, these antioxidants prevent the coral from “ bleaching ” and affect the mechanism of symbiont loss from the coral host. These observations confirm a role for oxidative stress, whether caused by elevated temperatures or exposure to UV radiation, in the bleaching phenomenon. Accepted: 18 October 1996     

Annual coral bleaching and the long-term recovery capacity of coral

Mass bleaching events are predicted to occur annually later this century. Nevertheless, it remains unknown whether corals will be able to recover between annual bleaching events. Using a combined tank and field experiment, we simulated annual bleaching by exposing three Caribbean coral species (Porites divaricata, Porites astreoides and Orbicella faveolata) to elevated temperatures for 2.5 weeks in 2 consecutive years. The impact of annual bleaching stress on chlorophyll a, energy reserves, calcification, and tissue C and N isotopes was assessed immediately after the second bleaching and after both short- and long-term recovery on the reef (1.5 and 11 months, respectively). While P. divaricata and O. faveolata were able to recover from repeat bleaching within 1 year, P. astreoides experienced cumulative damage that prevented full recovery within this time frame, suggesting that repeat bleaching had diminished its recovery capacity. Specifically, P. astreoides was not able to recover protein and carbohydrate concentrations. As energy reserves promote bleaching resistance, failure to recover from annual bleaching within 1 year will likely result in the future demise of heat-sensitive coral species.     

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.     

Climatological context for large-scale coral bleaching

Large-scale coral bleaching was first observed in 1979 and has occurred throughout virtually all of the tropics since that time. Severe bleaching may result in the loss of live coral and in a decline of the integrity of the impacted coral reef ecosystem. Despite the extensive scientific research and increased public awareness of coral bleaching, uncertainties remain about the past and future of large-scale coral bleaching. In order to reduce these uncertainties and place large-scale coral bleaching in the longer-term climatological context, specific criteria and methods for using historical sea surface temperature (SST) data to examine coral bleaching-related thermal conditions are proposed by analyzing three, 132 year SST reconstructions: ERSST, HadISST1, and GISST2.3b. These methodologies are applied to case studies at Discovery Bay, Jamaica (77.27°W, 18.45°N), Sombrero Reef, Florida, USA (81.11°W, 24.63°N), Academy Bay, Galápagos, Ecuador (90.31°W, 0.74°S), Pearl and Hermes Reef, Northwest Hawaiian Islands, USA (175.83°W, 27.83°N), Midway Island, Northwest Hawaiian Islands, USA (177.37°W, 28.25°N), Davies Reef, Australia (147.68°E, 18.83°S), and North Male Atoll, Maldives (73.35°E, 4.70°N). The results of this study show that (1) The historical SST data provide a useful long-term record of thermal conditions in reef ecosystems, giving important insight into the thermal history of coral reefs and (2) While coral bleaching and anomalously warm SSTs have occurred over much of the world in recent decades, case studies in the Caribbean, Northwest Hawaiian Islands, and parts of other regions such as the Great Barrier Reef exhibited SST conditions and cumulative thermal stress prior to 1979 that were comparable to those conditions observed during the strong, frequent coral bleaching events since 1979. This climatological context and knowledge of past environmental conditions in reef ecosystems may foster a better understanding of how coral reefs will respond in future, ocean warming scenarios.     

Seawater temperature and sublethal coral bleaching in Jamaica

Permanent study sites were established at 6 m, 12 m and 18 m on the West Fore Reef at Discovery Bay, Jamaica. Colonies of Montastrea annularis, Porites astreoides, Porites porites and Agaricia spp. were assessed for presence and extent of bleached tissue at two month intervals between October 1986 and September 1987. In 98% of all corals exhibiting a bleaching response, less than 25% of the colony appeared pale. In the remaining 2%, more than 25% of the tissue appeared pale. M. annularis, P. astreoides and Agaricia spp. showed a significant positive correlation between the percent of colonies exhibiting a partial bleaching response and seawater temperature. There was no significant difference in the percentage of colonies bleached between the three depths. M. annularis and Agaricia spp. exhibited a significantly higher percentage of colonies bleached than P. astreoides and P. porites. For M. annularis 15% of coral colonies studied showed 1–2 cm² randomly seattered patches of pale tissue which remained constant throughout the study. The partial bleaching patterns observed in this study were never lethal and are considered, in part, to be a response to seasonal variations in seawater temperature. Study location: Discovery Bay Marine Laboratory, P.O. Box 35, Discovery Bay, Jamaica, W. Indies     

Relationships among thermal stress, bleaching and oxidative damage in the hermatypic coral, Pocillopora capitata

To examine the response to exposure to a thermal gradient in coral, we assessed the effect of a gradual 10 degrees C temperature increase (22 to 32 degrees C over 10 h) on normal (N), partially bleached (P) and control (C) samples collected from different branches of the same coral (Pocillopora capitata). We examined markers of oxidative stress, including lipid peroxidation (MDA) and superoxide dismutase (SOD) activity, indicators of bleaching, including chlorophyll a (Chl a) and carotenoid pigment (PC) levels, as well as zooxanthellae density. Our results revealed that N, P and C coral samples all contained higher levels of PC versus Chl a. The levels of both pigments increased as the temperature increased from 22 to 28 degrees C only in N and C samples, whereas P samples showed less cellular damage than N and C samples at temperatures between 26 and 28 degrees C, and had greater antioxidant activities at temperatures between 26 and 30 degrees C. The rate of zooxanthellar expulsion consistently increased with temperature in all three coral types across the entire temperature range. Collectively, these results indicate that temperature has a direct effect on the antagonistic relationship between temperature-induced damage and protective antioxidant mechanisms in this type of coral.     

Quantifying the quality of coral bleaching predictions

Techniques that utilize sea surface temperature (SST) observations to predict coral reef bleaching are in common use and form the foundation for predicted global coral reef ecosystem demise within this century. Yet, quality assessments of these methods are typically qualitative or anecdotal. Quality is the correspondence of forecasts with observations and has standard quantitative measures. Here a forecast verification method, commonly used in meteorology, is presented and used to measure the quality of the degree heating weeks (DHW) technique as an exploration of insights that can be gleaned from this methodology. DHW values were calculated from NOAA Optimum Interpolation SST version 2 data and compared to a database of bleaching observations from 1990–2007. Quality is expressed with an objective measure, the Peirce Skill Score (PSS). The quality at varying DHW thresholds above which bleaching was projected to occur is calculated. By selecting the thresholds that maximize quality, the predictive technique is objectively optimized. This results in optimal threshold maps, showing reefs more prone and more resistant to bleaching. Optimization increases the quality of DHW as a predictor of bleaching from PSS = 0.55 to PSS = 0.83, in global average, but the optimal PSS and corresponding DHW values vary significantly from location to location. The coral reef research and management community are urged to adopt the simple, but rigorous tools of forecast verification routinely used in other disciplines so that bleaching forecasts can be quantitatively compared and their quality improved.     

珊瑚礁白化研究进展

珊瑚礁白化是由于珊瑚失去体内共生的虫黄藻和（或）共生的虫黄藻失去体内色素而导致五彩缤纷的珊瑚礁变白的生态现象。近年来,频繁发生的珊瑚礁白化导致了珊瑚礁生态系统严重退化,并已经影响到全球珊瑚礁生态系统的平衡,受到了人们的高度重视。研究认为：（1）大范围珊瑚礁白化主要是全球环境变化引起的,尤其是全球变暖和紫外辐射增强;（2）导致珊瑚礁白化的机制主要在于细胞机制和光抑制机制;（3）珊瑚礁白化后的恢复与白化程度有关,大范围白化的珊瑚礁完全恢复需要几年到几十年;（4）珊瑚礁白化的后果在于降低珊瑚繁殖能力、减缓珊瑚礁生长、改变礁栖生物的群落结构,导致大面积珊瑚死亡和改变珊瑚礁生态类型,如变为海藻型等;（5）与珊瑚共生的D系群虫黄藻更适应高温环境,珊瑚礁有可能通过D系群逐渐取代C系群的方式适应全球环境变化。     

Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching

Caribbean reef corals have declined precipitously since the 1980s due to regional episodes of bleaching, disease and algal overgrowth, but the extent of earlier degradation due to localised historical disturbances such as land clearing and overfishing remains unresolved. We analysed coral and molluscan fossil assemblages from reefs near Bocas del Toro, Panama to construct a timeline of ecological change from the 19th century-present. We report large changes before 1960 in coastal lagoons coincident with extensive deforestation, and after 1960 on offshore reefs. Striking changes include the demise of previously dominant staghorn coral Acropora cervicornis and oyster Dendrostrea frons that lives attached to gorgonians and staghorn corals. Reductions in bivalve size and simplification of gastropod trophic structure further implicate increasing environmental stress on reefs. Our paleoecological data strongly support the hypothesis, from extensive qualitative data, that Caribbean reef degradation predates coral bleaching and disease outbreaks linked to anthropogenic climate change.     

Species traits as indicators of coral bleaching

Coral Reefs - Coral bleaching as a response to increased sea surface temperature is regularly surveyed, but our understanding of species-specific differences in response is limited. We compiled...     

Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress

Background

Coral bleaching events vary in severity, however, to date, the hierarchy of susceptibility to bleaching among coral taxa has been consistent over a broad geographic range and among bleaching episodes. Here we examine the extent of spatial and temporal variation in thermal tolerance among scleractinian coral taxa and between locations during the 2010 thermally induced, large-scale bleaching event in South East Asia.

Methodology/Principal Findings

Surveys to estimate the bleaching and mortality indices of coral genera were carried out at three locations with contrasting thermal and bleaching histories. Despite the magnitude of thermal stress being similar among locations in 2010, there was a remarkable contrast in the patterns of bleaching susceptibility. Comparisons of bleaching susceptibility within coral taxa and among locations revealed no significant differences between locations with similar thermal histories, but significant differences between locations with contrasting thermal histories (Friedman = 34.97; p<0.001). Bleaching was much less severe at locations that bleached during 1998, that had greater historical temperature variability and lower rates of warming. Remarkably, Acropora and Pocillopora, taxa that are typically highly susceptible, although among the most susceptible in Pulau Weh (Sumatra, Indonesia) where respectively, 94% and 87% of colonies died, were among the least susceptible in Singapore, where only 5% and 12% of colonies died.

Conclusions/Significance

The pattern of susceptibility among coral genera documented here is unprecedented. A parsimonious explanation for these results is that coral populations that bleached during the last major warming event in 1998 have adapted and/or acclimatised to thermal stress. These data also lend support to the hypothesis that corals in regions subject to more variable temperature regimes are more resistant to thermal stress than those in less variable environments.     

Species-specific interactions between algal endosymbionts and coral hosts define their bleaching response to heat and light stress

The impacts of warming seas on the frequency and severity of bleaching events are well documented, but the potential for different Symbiodinium types to enhance the physiological tolerance of reef corals is not well understood. Here we compare the functionality and physiological properties of juvenile corals when experimentally infected with one of two homologous Symbiodinium types and exposed to combined heat and light stress. A suite of physiological indicators including chlorophyll a fluorescence, oxygen production and respiration, as well as pigment concentration consistently demonstrated lower metabolic costs and enhanced physiological tolerance of Acropora tenuis juveniles when hosting Symbiodinium type C1 compared with type D. In other studies, the same D-type has been shown to confer higher thermal tolerance than both C2 in adults and C1 in juveniles of the closely related species Acropora millepora. Our results challenge speculations that associations with type D are universally most robust to thermal stress. Although the heat tolerance of corals may be contingent on the Symbiodinium strain in hospite, our results highlight the complexity of interactions between symbiotic partners and a potential role for host factors in determining the physiological performance of reef corals.     

Predicting coral bleaching hotspots: the role of regional variability in thermal stress and potential adaptation rates

Sea surface temperature fields (1870–2100) forced by CO₂-induced climate change under the IPCC SRES A1B CO₂ scenario, from three World Climate Research Programme Coupled Model Intercomparison Project Phase 3 (WCRP CMIP3) models (CCSM3, CSIRO MK 3.5, and GFDL CM 2.1), were used to examine how coral sensitivity to thermal stress and rates of adaption affect global projections of coral-reef bleaching. The focus of this study was two-fold, to: (1) assess how the impact of Degree-Heating-Month (DHM) thermal stress threshold choice affects potential bleaching predictions and (2) examine the effect of hypothetical adaptation rates of corals to rising temperature. DHM values were estimated using a conventional threshold of 1°C and a variability-based threshold of 2σ above the climatological maximum Coral adaptation rates were simulated as a function of historical 100-year exposure to maximum annual SSTs with a dynamic rather than static climatological maximum based on the previous 100 years, for a given reef cell. Within CCSM3 simulations, the 1°C threshold predicted later onset of mild bleaching every 5 years for the fraction of reef grid cells where 1°C > 2σ of the climatology time series of annual SST maxima (1961–1990). Alternatively, DHM values using both thresholds, with CSIRO MK 3.5 and GFDL CM 2.1 SSTs, did not produce drastically different onset timing for bleaching every 5 years. Across models, DHMs based on 1°C thermal stress threshold show the most threatened reefs by 2100 could be in the Central and Western Equatorial Pacific, whereas use of the variability-based threshold for DHMs yields the Coral Triangle and parts of Micronesia and Melanesia as bleaching hotspots. Simulations that allow corals to adapt to increases in maximum SST drastically reduce the rates of bleaching. These findings highlight the importance of considering the thermal stress threshold in DHM estimates as well as potential adaptation models in future coral bleaching projections.     

Chronic parrotfish grazing impedes coral recovery after bleaching

Coral bleaching, in which corals become visibly pale and typically lose their endosymbiotic zooxanthellae (Symbiodinium spp.), increasingly threatens coral reefs worldwide. While the proximal environmental triggers of bleaching are reasonably well understood, considerably less is known concerning physiological and ecological factors that might exacerbate coral bleaching or delay recovery. We report a bleaching event in Belize during September 2004 in which Montastraea spp. corals that had been previously grazed by corallivorous parrotfishes showed a persistent reduction in symbiont density compared to intact colonies. Additionally, grazed corals exhibited greater diversity in the genetic composition of their symbiont communities, changing from uniform ITS2 type C7 Symbiodinium prior to bleaching to mixed assemblages of Symbiodinium types post-bleaching. These results suggest that chronic predation may exacerbate the influence of environmental stressors and, by altering the coral-zooxanthellae symbiosis, such abiotic-biotic interactions may contribute to spatial variation in bleaching processes.     

Chaos in the Pacific's coral reef bleaching cycle

There is no simple explanation for the unusual increase in coral reef bleaching events that have been occurring on a global scale over the last 2 decades. Recent studies focusing on this problem reveal that mass bleaching events have a strong periodic component, arising every 3-4 yr in step with the El Ni?o climatic phenomenon. To explore this possibility further, we examine a simple oceanographic-ecological model designed to simulate the warm and cool phases of the Pacific Ocean cycle and gauge its effect on local coral reefs. This allows us to identify causes for localized 'hot spots' in the ocean, whose high sea surface temperatures have disastrous consequences for corals. The underlying wave dynamics of the model lead to chaotic oscillations (every 3-4 yr), which help explain the coexistence of both order and irregularity in the dynamics of mass bleaching. The model makes use of a temperature threshold mechanism-a bleaching event is triggered whenever temperature anomalies exceed a critical level. In a variable environment, the threshold mechanism is sensitive to background fluctuations, and their effects are studied by making use of a 'stochastic resonance' formulation. Global climate change and other trends in external background environmental conditions are all shown to strongly influence the distribution of mass coral bleaching events.