Corals that survive repeated thermal stress show signs of selection and acclimatization.

Climate change is transforming coral reefs by increasing the frequency and intensity of marine heatwaves, often leading to coral bleaching and mortality. Coral communities have demonstrated modest increases in thermal tolerance following repeated exposure to moderate heat stress, but it is unclear whether these shifts represent acclimatization of individual colonies or mortality of thermally susceptible individuals. For corals that survive repeated bleaching events, it is important to understand how past bleaching responses impact future growth potential. Here, we track the bleaching responses of 1,832 corals in leeward Maui through multiple marine heatwaves and document patterns of coral growth and survivorship over a seven-year period. While we find limited evidence of acclimatization at population scales, we document reduced bleaching over time in specific individuals that is indicative of acclimatization, primarily in the stress-tolerant taxa Porites lobata. For corals that survived both bleaching events, we find no relationship between bleaching response and coral growth in three of four taxa studied. This decoupling suggests that coral survivorship is a better indicator of future growth than is a coral's bleaching history. Based on these results, we recommend restoration practitioners in Hawai'i focus on colonies of Porites and Montipora with a proven track-record of growth and survivorship, rather than devote resources toward identifying and cultivating bleaching-resistant phenotypes in the lab. Survivorship followed a latitudinal thermal stress gradient, but because this gradient was small, it is likely that local environmental factors also drove differences in coral performance between sites. Efforts to reduce human impacts at low performing sites would likely improve coral survivorship in the future.

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

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

Connectivity modelling identifies sources and sinks of coral recruitment within reef clusters.

Connectivity aids the recovery of populations following disturbances, such as coral bleaching and tropical cyclones. Coral larval connectivity is a function of physical connectivity and larval behaviour. In this study, we used OceanParcels, a particle tracking simulator, with 2D and 3D velocity outputs from a high resolution hydrodynamic-biogeochemical marine model (RECOM) to simulate the dispersal and settlement of larvae from broadcast spawning Acropora corals in the Moore Reef cluster, northern Great Barrier Reef, following the annual spawning events in 2015, 2016 and 2017. 3D velocity simulations showed 19.40-68.80% more links and sinks than those of 2D simulations. Although the patterns of connectivity among sites vary over days and years, coral larvae consistently dispersed from east to west in the cluster domain, with some sites consistently acting as sources or sinks for local larval recruitment. Results can inform coral reef intervention plans for climate change, such as the design of marine protected areas and the deployment of proposed interventions within reef clusters. For example, the wider benefits of interventions (e.g., deployment of heat adapted corals) may be optimised when deployed at locations that are a source of larvae to others within comparable habitats across the reef cluster.

Should I stay or should I go? Coral bleaching from the symbionts' perspective.

Coral bleaching, the stress-induced breakdown of coral-algal symbiosis, threatens reefs globally. Paradoxically, despite adverse fitness effects, corals bleach annually, even outside of abnormal temperatures. This generally occurs shortly after the once-per-year mass coral spawning. Here, we propose a hypothesis linking annual coral bleaching and the transmission of symbionts to the next generation of coral hosts. We developed a dynamic model with two symbiont growth strategies, and found that high sexual recruitment and low adult coral survivorship and growth favour bleaching susceptibility, while the reverse promotes bleaching resilience. Otherwise, unexplained trends in the Indo-Pacific align with our hypothesis, where reefs and coral taxa exhibiting higher recruitment are more bleaching susceptible. The results from our model caution against interpreting potential shifts towards more bleaching-resistant symbionts as evidence of climate adaptation-we predict such a shift could also occur in declining systems experiencing low recruitment rates, a common scenario on today's reefs.

Mitigation of Vibrio coralliilyticus-induced coral bleaching through bacterial dysbiosis prevention by Ruegeria profundi.

Vibrio species are prevalent in ocean ecosystems, particularly Vibrio coralliilyticus, and pose a threat to corals and other marine organisms under global warming conditions. While microbiota manipulation is considered for coral disease management, understanding the role of commensal bacteria in stress resilience remains limited. Here, a single bacterial species (Ruegeria profundi) rather than a consortium of native was used to combat pathogenic V. coralliilyticus and protect corals from bleaching. R. profundi showed therapeutic activity in vivo, preventing a significant reduction in bacterial diversity in bleached corals. Notably, the structure of the bacterial community differed significantly among all the groups. In addition, compared with the bleached corals caused by V. coralliilyticus, the network analysis revealed that complex interactions and positive correlations in the bacterial community of the R. profundi protected non-bleached corals, indicating R. profundi's role in fostering synergistic associations. Many genera of bacteria significantly increased in abundance during V. coralliilyticus infection, including Vibrio, Alteromonas, Amphritea, and Nautella, contributing to the pathogenicity of the bacterial community. However, R. profundi effectively countered the proliferation of these genera, promoting potential probiotic Endozoicomonas and other taxa, while reducing the abundance of betaine lipids and the type VI section system of the bacterial community. These changes ultimately influenced the interactive relationships among symbionts and demonstrated that probiotic R. profundi intervention can modulate coral-associated bacterial community, alleviate pathogenic-induced dysbiosis, and preserve coral health. These findings elucidated the relationship between the behavior of the coral-associated bacterial community and the occurrence of pathological coral bleaching.IMPORTANCEChanges in the global climate and marine environment can influence coral host and pathogen repartition which refers to an increased likelihood of pathogen infection in hosts. The risk of Vibrio coralliilyticus-induced coral disease is significantly heightened, primarily due to its thermos-dependent expression of virulent and populations. This study investigates how coral-associated bacterial communities respond to bleaching induced by V. coralliilyticus. Our findings demonstrate that Ruegeria profundi exhibits clear evidence of defense against pathogenic bacterial infection, contributing to the maintenance of host health and symbiont homeostasis. This observation suggests that bacterial pathogens could cause dysbiosis in coral holobionts. Probiotic bacteria display an essential capability in restructuring and manipulating coral-associated bacterial communities. This restructuring effectively reduces bacterial community virulence and enhances the pathogenic resistance of holobionts. The study provides valuable insights into the correlation between the health status of corals and how coral-associated bacterial communities may respond to both pathogens and probiotics.

Algal symbiont diversity in Acropora muricata from the extreme reef of Bouraké associated with resistance to coral bleaching.

Widespread coral bleaching has generally been linked to high water temperatures at larger geographic scales. However, the bleaching response can be highly variable among individual of the same species, between different species, and across localities; what causes this variability remains unresolved. Here, we tracked bleached and non-bleached colonies of Acropora muricata to see if they recovered or died following a stress event inside the semi-enclosed lagoon of Bouraké (New Caledonia), where corals are long-term acclimatized to extreme conditions of temperature, pH and dissolved oxygen, and at a nearby control reef where conditions are more benign. We describe Symbiodiniaceae community changes based on next-generation sequencing of the ITS2 marker, metabolic responses, and energetic reserve measures (12 physiological traits evaluated) during the La Niña warm and rainy summer in 2021. Widespread coral bleaching (score 1 and 2 on the coral colour health chart) was observed only in Bouraké, likely due to the combination of the high temperatures (up to 32°C) and heavy rain. All colonies (i.e., Bouraké and reference site) associated predominantly with Symbiodinaceae from the genera Cladocopium. Unbleached colonies in Bouraké had a specific ITS2-type profile (proxies for Symbiodiniaceae genotypes), while the bleached colonies in Bouraké had the same ITS2-type profile of the reef control colonies during the stress event. After four months, the few bleached colonies that survived in Bouraké (B2) acquired the same ITS2 type profiles of the unbleached colonies in Bouraké. In terms of physiological performances, all bleached corals showed metabolic depression (e.g., Pgross and Rdark). In contrast, unbleached colonies in Bouraké maintained higher metabolic rates and energetic reserves compared to control corals. Our study suggests that Acropora muricata enhanced their resistance to bleaching thanks to specific Symbiodiniaceae associations, while energetic reserves may increase their resilience after stress.

Microbiome ecological memory and responses to repeated marine heatwaves clarify variation in coral bleaching and mortality.

Microbiomes are essential features of holobionts, providing their hosts with key metabolic and functional traits like resistance to environmental disturbances and diseases. In scleractinian corals, questions remain about the microbiome's role in resistance and resilience to factors contributing to the ongoing global coral decline and whether microbes serve as a form of holobiont ecological memory. To test if and how coral microbiomes affect host health outcomes during repeated disturbances, we conducted a large-scale (32 exclosures, 200 colonies, and 3 coral species sampled) and long-term (28 months, 2018-2020) manipulative experiment on the forereef of Mo'orea, French Polynesia. In 2019 and 2020, this reef experienced the two most severe marine heatwaves on record for the site. Our experiment and these events afforded us the opportunity to test microbiome dynamics and roles in the context of coral bleaching and mortality resulting from these successive and severe heatwaves. We report unique microbiome responses to repeated heatwaves in Acropora retusa, Porites lobata, and Pocillopora spp., which included: microbiome acclimatization in A. retusa, and both microbiome resilience to the first marine heatwave and microbiome resistance to the second marine heatwave in Pocillopora spp. Moreover, observed microbiome dynamics significantly correlated with coral species-specific phenotypes. For example, bleaching and mortality in A. retusa both significantly increased with greater microbiome beta dispersion and greater Shannon Diversity, while P. lobata colonies had different microbiomes across mortality prevalence. Compositional microbiome changes, such as changes to proportions of differentially abundant putatively beneficial to putatively detrimental taxa to coral health outcomes during repeated heat stress, also correlated with host mortality, with higher proportions of detrimental taxa yielding higher mortality in A. retusa. This study reveals evidence for coral species-specific microbial responses to repeated heatwaves and, importantly, suggests that host-dependent microbiome dynamics may provide a form of holobiont ecological memory to repeated heat stress.

Relationship between anthropogenic impacts and bleaching-associated tissue mortality of corals in Curaçao (Netherlands Antilles) / Relación entre los impactos antropogénicos y la mortalidad tisular asociada al blanqueamiento de corales en Curaçao (Antillas Holandesas)

Chronic anthropogenic impacts can have a negative effect on coral health and on coral energy budgets needed for regeneration of lesions. I therefore hypothesise that during massive bleaching events, the degree of corals showing bleaching-related tissue mortality is higher in areas subject to chronic anthropogenic impacts than in relatively pristine areas. In the present study, the degree of bleaching and bleaching-related tissue mortality was estimated for eight abundant coral species in Curaçao, at the onset of a massive Caribbean bleaching event in 1995, and three months afterwards. To study the possible effects of anthropogenic disturbances, the study was done at four unpolluted control sites, two polluted sites (sedimentation, sewage), and four sites at the mouth of lagoons with outflow of nutrient-rich, warm and turbid seawater. No pattern of an overall difference in bleaching between impacted and control sites was found for the degree of bleaching. However, the percentage of corals showing bleaching-related tissue mortality was higher at the impacted sites than at the control sites for the total number of corals and for corals with < 50% of their surface area bleached. Highest and most significant values of tissue mortality were found at a reef site experiencing chronic pollution by raw sewage. The data thus suggest that unfavourable conditions caused by anthropogenic influences, such as increased sedimentation, eutrophication and seawater temperature, have an additional negative effect on the tissue survival of coral colonies during bleaching episodes. Rev. Biol. Trop. 54 (Suppl. 3): 31-43. Epub 2007 Jan. 15.

Los impactos antropogénicos crónicos pueden tener efectos negativos en la salud y en las cantidades de energía necesarias para la regeneración de lesiones en los corales. Mi hipótesis fue que durante los casos de blanqueamiento masivo, el grado en que los corales muestren mortalidades de tejido relacionadas con el blanqueamiento, será mayor en áreas sujetas a impactos antropogénicos crónicos que en áreas relativamente prístinas. Estimé los grados de blanqueamiento y mortalidad tisular en ocho especies de coral abundantes en Curaçao, durante el comienzo de un de blanqueamiento masivo en el Caribe en 1995 y tres meses después. El estudio se realizó en cuatro sitios control no contaminados, dos sitios contaminados (sedimentación, aguas residuales), y cuatro sitios en la boca de lagunas con aguas tibias, ricas en nutrientes y turbias. En general, no se encontró ningún patrónx de diferencias en el grado de blanqueamiento entre sitios. Sin embargo, el porcentaje de corales que mostraron mortalidad tisular relacionada con el blanqueamiento fue mayor en los sitios impactados que en los controles, tanto en el número total de corales como en corales con <50% de su superficie blanquedada. Los valores más altos y más significativos de mortalidad tisular se encontraron en un arrecife que experimentaba contaminación crónica por aguas residuales crudas. La información sugiere que las condiciones desfavorables causadas por la influencia antropogénica, como el incremento en la sedimentación, eutrofización y la temperatura del agua, tienen un efecto negativo adicional en la supervivencia del tejido de las colonias de coral, durante el blanqueamiento.

Fragmentation of the gastrodermis and detachment of zooxanthellae in symbiotic cnidarians: a role for hydrogen peroxide and Ca2+ in coral bleaching and algal density control / Fragmentación de la gastrodermis y desprendimiento de zooxantelas en cnidarios simbióticos: papel del peróxido de hidrógeno y el Ca2+ en el blanqueamiento de corales y el control de la densidad de algas

Coral bleaching involves the detachment of zooxanthellae and the simultaneous fragmentation of the gastrodermis. Results obtained with a cell permeant fluorescent probe for calcium ions (Ca2+) indicates that "thermal" bleaching is the result of a temperature related breakdown of the Ca2+ exclusion system. "Solar" bleaching, which takes place at lower temperatures and is driven by light, is the result of a build-up of photo-synthetically produced hydrogen peroxide in the tissues. Gastrodermal tissue with its symbionts, scraped from between septa of corals, was observed under controlled conditions of high light and temperature. Pieces of gastrodermis round off, zooxanthellae move to the surface, protrude from the surface and after a delay, detach, surrounded by a thin layer of host cytoplasm, inclusions and plasma membrane. The higher the temperature and light level the shorter the delay and higher the rate of algal detachment. Fragmentation by the ballooning-out and detachment of small spheres of cytoplasm (bleb formation) takes place simultaneously. This is likely to be due to oxidation, by hydrogen peroxide (H2O2), of -SH groups on the cytoskeleton and its attachment to the plasma membrane. Ground, polished and stained thin acrylic resin sections reveal similar processes taking place in artificially bleached corals. Isolated zooxanthellae and whole corals are shown to release H2O2 in the light. This process of algal detachment and fragmentation that takes place at normal sea temperatures may underlie the mechanism limiting algal populations in the gastrodermis and may be localized to areas with a concentration of algae near the membrane. At above-normal temperatures under the synergistic effect of light and temperature, the rate of production of H2O2 exceeds the rate at which can it be lost by diffusion or destroyed and H2O2 accumulates. This results in damage to the calcium exclusion system, detachment of zooxanthellae into the coelenteron and fragmentation of the gastrodermis. Rev. Biol. Trop. 54 (Suppl. 3): 79-96. Epub 2007 Jan. 15.

El blanqueamiento de los corales implica el desprendimiento de zooxantelas y la simultánea fragmentación de la gastrodermis. Resultados obtenidos con una sonda florescente de iones Calcio (Ca2+) para células permeables, indican que el blanqueamiento "térmico" es el resultado de una interrupción del sistema de exclusión de Ca2+, provocada por la temperatura. El blanqueamiento "solar", que tiene lugar a temperaturas más bajas y está determinado por la luz, es el resultado de una acumulación de peróxido de hidrógeno producido fotosintéticamente en los tejidos. Para ver el proceso, se raspó tejido gastrodermal, junto con sus simbiontes, de entre los septos de los corales y se observó en condiciones controladas de luz y temperatura. Primero, los trozos de gastrodermis se dan vuelta, luego las zooxantelas se mueven hacia la superficie, sobresalen desde ella y tras un tiempo, se desprenden, rodeadas de una delgada capa de citoplasma del hospedero, inclusiones y membrana plasmática. Mientras mayor sea la temperatura y el nivel de luz, menor es el tiempo que tardan las zooxantelas en desprenderse y mayor es la tasa de desprendimiento algal. La fragmentación producida por el inflamación y el desprendimiento de pequeñas esferas de citoplasma (formación de ampollas), tiene lugar simultáneamente. Probablemente, esto es causado por oxidación en el citoesqueleto de grupos -SSH por el peróxido de hidrógeno (H2O2), y por su acoplamiento a la membrana plasmática. Secciones de resina acrílica delgada molida, pulida y teñida revelan que en corales blanqueados artificialmente se llevan a cabo procesos similares. Se ha demostrado que tanto las zooxantelas aisladas como los corales enteros, liberan H2O2 en la luz. Debajo este proceso de desprendimiento algal y fragmentación que tiene lugar a temperaturas normales en el mar, puede encontrarse el mecanismo que limita las poblaciones algales en la gastrodermis, el cual podría estar localizado en áreas con concentraciones de alga cerca de la membrana. A temperaturas más altas de lo normal, bajo el efecto sinérgico de la luz y la temperatura, la tasa de producción de H2O2 excede la tasa a la cual éste puede destruirse o perderse por difusión y, por ende,se acumula. Esto resulta en daño al sistema de exclusión de calcio, desprendimiento de zooxantelas hacia el celenterón y fragmentación de la gastrodermis.