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Coral bleaching has a profound impact on the health and function of reef ecosystems, but the metabolomic effects of coral bleaching are largely uncharacterized. Here, untargeted metabolomics was used to analyse pairs of adjacent Montipora capitata corals that had contrasting bleaching phenotypes during a severe bleaching event in 2015. When these same corals were sampled four years later while visually healthy, there was a strong metabolomic signature of bleaching history. This was primarily driven by betaine lipids from the symbiont, where corals that did not bleach were enriched in saturated lyso-betaine lipids. Immune modulator molecules were also altered by bleaching history in both the coral host and the algal symbiont, suggesting a shared role in partner choice and bleaching response. Metabolomics from a separate set of validation corals was able to predict the bleaching phenotype with 100% accuracy. Experimental temperature stress induced phenotype-specific responses, which magnified differences between historical bleaching phenotypes. These findings indicate that natural bleaching susceptibility is manifested in the biochemistry of both the coral animal and its algal symbiont. This metabolome difference is stable through time and results in different physiological responses to temperature stress. This work provides insight into the biochemical mechanisms of coral bleaching and presents a valuable new tool for resilience-based reef restoration.

Mesophotic reefs (30‐150 m) have been proposed as potential refugia that facilitate the recovery of degraded shallow reefs following acute disturbances such as coral bleaching and disease. However, because of the technical difficulty of collecting samples, the connectivity of adjacent mesophotic reefs is relatively unknown compared with shallower counterparts. We used genotyping by sequencing to assess fine‐scale genetic structure of Montastraea cavernosa at two sites at Pulley Ridge, a mesophotic coral reef ecosystem in the Gulf of Mexico, and downstream sites along the Florida Reef Tract. We found differentiation between reefs at Pulley Ridge (~68 m) and corals at downstream upper mesophotic depths in the Dry Tortugas (28–36 m) and shallow reefs in the northern Florida Keys (Key Biscayne, ~5 m). The spatial endpoints of our study were distinct, with the Dry Tortugas as a genetic intermediate. Most striking were differences in population structure among northern and southern sites at Pulley Ridge that were separated by just 12km. Unique patterns of clonality and outlier loci allele frequency support these sites as different populations and suggest that the long‐distance horizontal connectivity typical of shallow‐water corals may not be typical for mesophotic systems in Florida and the Gulf of Mexico. We hypothesize that this may be due to the spawning of buoyant gametes, which commits propagules to the surface, resulting in greater dispersal and lower connectivity than typically found between nearby shallow sites. Differences in population structure over small spatial scales suggest that demographic constraints and/or environmental disturbances may be more variable in space and time on mesophotic reefs compared with their shallow‐water counterparts.

Coral reefs are under extreme threat due to a number of stressors, but temperature increases due to changing climate are the most severe. Rising ocean temperatures coupled with local extremes lead to extensive bleaching, where the coral-algal symbiosis breaks down and corals may die, compromising the structure and function of reefs. Although the symbiotic nature of the coral colony has historically been a focus of research on coral resilience, the host itself is a foundational component in the response to thermal stress. Fixed effects in the coral host set trait baselines through evolutionary processes, acting on many loci of small effect to create mosaics of thermal tolerance across latitudes and individual coral reefs. These genomic differences can be strongly heritable, producing wide variation among clones of different genotypes or families of a specific larval cross. Phenotypic plasticity is overlaid on these baselines and a growing body of knowledge demonstrates the potential for acclimatization of reef-building corals through a variety of mechanisms that promote resilience and stress tolerance. The long-term persistence of coral reefs will require many of these mechanisms to adjust to warmer temperatures within a generation, bridging the gap to reproductive events that allow recombination of standing diversity and adaptive change. Business-as-usual climate scenarios will probably lead to the loss of some coral populations or species in the future, so the interaction between intragenerational effects and evolutionary pressure is critical for the survival of reefs.

Thermal stress is a major contributor to loss of coral cover, significantly impacting reefs during the third global bleaching event between 2014 and 2017. The long-term persistence of coral reefs depends on acclimatization and adaptation to changing climate, which are influenced greatly by the interactions between bleaching and reproductive success. We observed a genotypically diverse population of Orbicella faveolata before, during, and after consecutive bleaching events in 2014 and 2015 in the Florida Keys. We documented less bleaching during the second event despite 40% more time above local bleaching thresholds and an association between bleaching severity and subsequent spawning. Approximately 75% of colonies experienced the same or less severe bleaching in the second event despite being metabolically compromised, with a substantial minority (~ 35%) faring better in the second event. The second bleaching event also resulted in smaller decreases in chlorophyll content per symbiont cell and symbiont-to-host cell ratio reef-wide, representing less damage to the coral–algal symbiosis. All colonies that recovered quickly (~ 1 month) or did not bleach in 2014 released gametes in 2015, while only 60% of colonies that recovered more slowly did. Bleaching also impacted the amount of gametes released, with more severe bleaching significantly associated with gamete release from

As coral reefs decline, cryptic sources of resistance and resilience to stress may be increasingly important for the persistence of these communities. Among these sources, inter‐ and intraspecific diversity remain understudied on coral reefs but extensively impact a variety of traits in other ecosystems. We use a combination of field and sequencing data at two sites in Florida and two in the Dominican Republic to examine clonal diversity and genetic differentiation of high‐ and low‐density aggregations of the threatened coral Acropora cervicornisin the Caribbean. We find that high‐density aggregations called thickets are composed of up to 30 genotypes at a single site, but 47% of genotypes are also found as isolated, discrete colonies outside these aggregations. Genet–ramet ratios are comparable for thickets (0.636) and isolated colonies after rarefaction (0.569), suggesting the composition of each aggregation is not substantially different and highlighting interactions between colonies as a potential influence on structure. There are no differences in growth rate, but a significant positive correlation between genotypic diversity and coral cover, which may be due to the influence of interactions between colonies on survivorship or fragment retention during asexual reproduction. Many polymorphisms distinguish isolated colonies from thickets despite the shared genotypes found here, including putative nonsynonymous mutations that change amino acid sequence in 25 loci. These results highlight intraspecific diversity as a density‐dependent factor that may impact traits important for the structure and function of coral reefs.

Significance Ocean warming has caused catastrophic losses of corals on reefs worldwide and is intensifying faster than the adaptive rate of most coral populations that remain. Human interventions, such as propagation of heat-resistant corals, may help maintain reef function and delay further devastation of these valuable ecosystems as society confronts the climate crisis. However, exposing adult corals to a complex suite of new environmental conditions could lead to tradeoffs that alter their heat stress responses, and empirical data are needed to test the utility of this approach. Here, we show that corals transplanted to novel reef conditions did not exhibit changes in their heat stress response or negative fitness tradeoffs, supporting the inclusion of this approach in our management arsenal., Urgent action is needed to prevent the demise of coral reefs as the climate crisis leads to an increasingly warmer and more acidic ocean. Propagating climate change–resistant corals to restore degraded reefs is one promising strategy; however, empirical evidence is needed to determine whether stress resistance is affected by transplantation beyond a coral’s native reef. Here, we assessed the performance of bleaching-resistant individuals of two coral species following reciprocal transplantation between reefs with distinct pH, salinity, dissolved oxygen, sedimentation, and flow dynamics to determine whether heat stress response is altered following coral exposure to novel physicochemical conditions in situ. Critically, transplantation had no influence on coral heat stress responses, indicating that this trait was relatively fixed. In contrast, growth was highly plastic, and native performance was not predictive of performance in the novel environment. Coral metabolic rates and overall fitness were higher at the reef with higher flow, salinity, sedimentation, and diel fluctuations of pH and dissolved oxygen, and did not differ between native and cross-transplanted corals, indicating acclimatization via plasticity within just 3 mo. Conversely, cross-transplants at the second reef had higher fitness than native corals, thus increasing the fitness potential of the recipient population. This experiment was conducted during a nonbleaching year, so the potential benefits to recipient population fitness are likely enhanced during bleaching years. In summary, this study demonstrates that outplanting bleaching-resistant corals is a promising tool for elevating the resistance of coral populations to ocean warming.

The long-term persistence of coral reefs under climate change requires heritable drivers of thermal tolerance which support adaptation. The genomic basis of thermal tolerance has been evaluated across strong spatial and environmental gradients, but this variation also exists within populations due to neutral evolutionary processes. Small scale heterogeneity in coral bleaching is ubiquitous, so we used corals from a single reef to examine genomic signatures of bleaching performance, their biochemical correlates and the downstream consequences of selective breeding. In the absence of directional selection due to environmental differences, adult corals from a single population exhibit strong genomic patterns related to natural bleaching tolerance and symbiosis state, including functional differentiation in signaling pathways, protein and amino acid modification and metabolism. Conversely, growth, development and innate immune responses did not distinguish bleaching tolerance in adult corals. The genomic signatures of these gene ontologies influence biochemical patterns in healthy corals, primarily via cell-signaling pathway impacts on peptides and amino acids. Thermal tolerance in this population is highly heritable, with significantly higher survivorship under temperature stress in larvae and juveniles reared from thermally tolerant parents than those from sensitive parents. Using a select and re-sequence approach, certain gene ontologies were reproducibly impacted, while antioxidant activity and cell signaling ontologies were disproportionately selected in thermally tolerant corals, demonstrating the genomic drivers of successful selective breeding. These data show that intrapopulation variance in the absence of historical selection supports the adaptive capacity of coral reefs under climate change.

Reef-building corals rely on intracellular algal symbionts to meet energetic demands. Increasing extreme weather driven by climate change often leads to disruption of this symbiosis and to coral death. Corals can better withstand stress after previous exposure to sublethal conditions, but the mechanisms for this resilience remain unclear. Here, we show that a three-day thermal preconditioning increases tolerance of acute heat stress through modulations in cell death pathways in the stony coral Pocillopora acuta. In preconditioned corals, the ratio of pro-survival (pa-Bcl-2 and pa-BI-1) to pro-death (pa-BAK and pa-BAX) gene expression increased and the corals underwent significantly less bleaching. When treated with Bcl-2 inhibitor, corals lost the improved thermal tolerance, suggesting an important role of programmed cell death in coral bleaching and acclimatization. During heat stress, the activity of acid phosphatase increased but caspase-3 did not, suggesting the involvement of autophagy/symbiophagy rather than apoptosis in this process. A similar shift in gene expression also occurs in thermally stressed corals that have been exposed to naturally higher temperatures during summer thermal maxima in Kāne'ohe Bay, Hawai'i, suggesting that corals can increase their resilience to realistic warming events during high-risk periods through alterations in cell signalling. These data suggest that programmed cell death pathways underly coral acclimatization and resilience and may be important for coral reef conservation and management.

Urgent action is needed to prevent the demise of coral reefs as the climate crisis leads to an increasingly warmer and more acidic ocean. Propagating climate change resistant corals to restore degraded reefs is one promising strategy; however, empirical evidence is needed to determine if resistance is retained following transplantation within or beyond a coral’s natal reef. Here we assessed the performance of bleaching-resistant individuals of two coral species following reciprocal transplantation between environmentally distinct reefs (low vs high diel variability) to determine if stress resistance is retained following transplantation. Critically, transplantation to either environment had no influence on coral bleaching resistance, indicating that this trait was relatively fixed and is thus a useful metric for selecting corals for reef restoration within their native range. In contrast, growth was highly plastic, and native performance was not predictive of performance in the novel environment. Coral metabolism was also plastic, with cross transplants of both species matching the performance of native corals at both reefs within three months. Coral physiology (autotrophy, heterotrophy, and metabolism) and overall fitness (survival, growth, and reproduction) were higher at the reef with higher flow and fluctuations in diel pH and dissolved oxygen, and did not differ between native corals and cross-transplants. Conversely, cross-transplants at the low-variability reef had higher fitness than native corals, thus increasing overall fitness of the recipient population. This experiment was conducted during a non-bleaching year, which suggests that introduction of these bleaching-resistant individuals will provide even greater fitness benefits to recipient populations during bleaching years. In summary, this study demonstrates that propagating and transplanting bleaching-resistant corals can elevate the resistance of coral populations to ocean warming while simultaneously maintaining reef function as the climate crisis worsens.

As sea surface temperatures increase worldwide due to climate change, coral bleaching events are becoming more frequent and severe, resulting in reef degradation. Leveraging the inherent ability of reef-building corals to acclimatize to thermal stress via pre-exposure to protective temperature treatments may become an important tool in improving the resilience of coral reefs to rapid environmental change. We investigated whether historical bleaching phenotype, coral host genotype, and exposure to protective temperature treatments would affect the response of the Hawaiian coral Montipora capitata to natural thermal stress. Fragments were collected from colonies that demonstrated different bleaching responses during the 2014-2015 event in Kāne’ohe Bay (O’ahu, Hawai’i) and exposed to four different artificial temperature pre-treatments (and a control at ambient temperature). After recovery, fragments experienced a natural thermal stress event either in laboratory conditions or their native reef environment. Response to thermal stress was quantified by measuring changes in the algal symbionts’ photochemical efficiency, community composition, and relative density. Historical bleaching phenotype was reflected in stable differences in symbiont community composition, with historically bleached corals containing only Cladocopium symbionts and historically non-bleached corals having mixed symbiont communities dominated by Durusdinium. Mixed-community corals lost more Cladocopium than Cladocopium-only corals during the natural thermal stress event, and preferentially recovered with Durusdinium. Laboratory pre-treatments exposed corals to more thermal stress than anticipated, causing photochemical damage that varied significantly by genotype. While none of the treatments had a protective effect, temperature variation during treatments had a significant detrimental effect on photochemical efficiency during the thermal stress event. These results show that acclimatization potential is affected by fine-scale differences in temperature regime, host genotype, and relatively stable differences in symbiont community composition that underpin historical bleaching phenotypes in M. capitata.

Coral bleaching, a process where corals expel their photosynthetic symbionts, has a profound impact on the health and function of coral reefs. As global ocean temperatures continue to rise, bleaching poses the greatest threat to coral reef ecosystems. Here, untargeted metabolomics was used to analyze the biochemicals in pairs of adjacent corals from a patch reef in Kāne‘ohe Bay, Hawai‘i, where one colony in the pair bleached (in 2015) and recovered while the other did not bleach. There was a strong metabolomic signature of prior bleaching history four years after recovery found in both the host and its algal symbionts. Machine learning analysis determined that the strongest metabolite drivers of the difference in bleaching phenotype were a group of betaine lipids. Those with saturated fatty acids were significantly enriched in thermally tolerant corals and those with longer, unsaturated and diacyl forms were enriched in historically bleached corals. Host immune response molecules, Lyso-PAF and PAF, were also altered by bleaching history and were strongly correlated with symbiont community and algal-derived metabolites suggesting a role of coral immune modulation in symbiont choice and bleaching response. To validate these findings, we tested a separatein situset of corals and were able to predict the bleaching phenotype with 100% accuracy. Furthermore, corals subjected to an experimental temperature stress had strong phenotype-specific responses in all components of the holobiont, which served to further increase the differences between historical bleaching phenotypes. Thus, we show that natural bleaching susceptibility is simultaneously manifested in the biochemistry of the coral animal and the algal symbiont and that this bleaching history results in different physiological responses to temperature stress. This work provides insight into the biochemical mechanisms involved in coral bleaching and presents a valuable new tool for resilience-based reef restoration.

Sexual reproduction in scleractinian corals is a critical component of species recovery, fostering population connectivity and enhancing genetic diveristy. The relative contribution of sexual reproduction to both connectivity and diversity in Acropora cervicornis may be variable due to this species’ capacity to reproduce effectively by fragmentation. Using a biophysical model and genomic data in this threatened species, we construct potential connectivity pathways on the Florida Reef Tract (FRT) and compare them to inferred migration rates derived from next-generation sequencing, using a link and node-based approach. Larval connectivity on the FRT can be divided into two zones: the northern region, where most transport is unidirectional to the north with the Florida Current, and the southern region that is more dynamic and exhibits complex spatial patterns. These biophysical linkages are poorly correlated with genetic connectivity patterns, which resolve many reciprocal connections and suggest a less sparse network. These results are difficult to reconcile with genetic data which indicate that individual reefs are diverse, suggesting important contributions of sexual reproduction and recruitment. Larval connectivity models highlight potential resources for recovery, such as areas with high larval export like the Lower Keys, or areas that are well connected to most other regions on the FRT, such as the Dry Tortugas.

The abundance of corals has declined significantly over past decades, to the point where several reef-building species in the Caribbean are now listed as threatened. Active reef restoration has expanded exponentially to help recover degraded coral populations and the ecological services associated with healthy and complex reefs. While restoration practitioners now grow hundreds of coral genotypes from several species within coral nurseries and thousands of corals are outplanted onto degraded reefs annually, the cost of these activities continues to be a limiting factor. We describe a citizen science program, Rescue a Reef (RAR), which trains participants in reef restoration and provides unique, experiential learning opportunities to recover degraded coral reefs by propagating and transplanting threatened coral species. Between 2015–2017, 230 participants outplanted >1300 staghorn corals, showing that citizen scientists significantly contribute to reef restoration. Most importantly, corals outplanted by RAR participants showed the same survivorship as those outplanted by scientific experts. The direct benefits of using citizen scientists for restoration are enhanced when the educational opportunities offered by these expeditions are considered. Results from our survey showed significant improvements in coral reef ecology and restoration knowledge for RAR participants. Thus, the growing field of reef restoration based on the coral gardening method offers a unique opportunity for participatory public engagement. By participating in these programs, citizen scientists can go beyond data collection to active restoration of degraded resources.

Climate-driven reef decline has prompted the development of next-generation coral conservation strategies, many of which hinge on the movement of adaptive variation across genetic and environmental gradients. This process is limited by our understanding of how genetic and genotypic drivers of coral bleaching will manifest in different environmental conditions. We reciprocally transplanted 10 genotypes ofAcropora cervicornisacross eight sites along a 60 km span of the Florida Reef Tract and documented significant genotype × environment interactions in bleaching response during the severe 2015 bleaching event. Performance relative to site mean was significantly different between genotypes and can be mostly explained by ensemble models of correlations with genetic markers. The high explanatory power was driven by significant enrichment of loci associated DNA repair, cell signalling and apoptosis. No genotypes performed above (or below) bleaching average at all sites, so genomic predictors can provide practitioners with ‘confidence intervals' about the chance of success in novel habitats. These data have important implications for assisted gene flow and managed relocation, and their integration with traditional active restoration.

Green macroalgal blooms are becoming a common problem in coastal waters and estuaries. This study describes the first occurrence of a persistent macroalgal bloom of the genus Anadyomene J.V. Lamouroux (Cladophorales, Anadyomenaceae) in the world and particularly in Biscayne Bay, FL, USA. The morphological-based identification of species was verified by a molecular analysis that sequenced the variable C1D2 region of the large subunit (LSU) nrDNA. Results indicate that the bloom is composed of two species: Anadyomene stellata, reported previously for Florida, and a diminutive perforate undetermined species, Anadyomene sp., potentially representing an introduction in the area. General surveys in Biscayne Bay based on a stratified random design, to visually estimate the percent cover of submerged aquatic vegetation, date from 1999; using the same methods recent intensive surveys of the detected bloom were conducted once a year from 2010 to 2012. Results show that the Anadyomene bloom densities have persisted since 2005 through 2012 covering an area of approximately 60 km2 of seagrass habitats. The spatial distribution of the bloom is restricted to the central inshore section of the Bay, an area affected by canals and groundwater discharges. The persistent 75% cover reported for several sites, has caused significant negative impacts to seagrass beds. This bloom occurring adjacent to metropolitan Miami, adds to the world trend of increasing green macroalgal blooms occurring at enriched coastal waters.

Coral reef restoration methods such as coral gardening are becoming increasingly considered as viable options to mitigate reef degradation and enhance recovery of depleted coral populations. In this study, we describe several aspects of the coral gardening approach that dem- onstrate this methodology is an effective way of propa- gating the threatened Caribbean staghorn coral Acropora cervicornis: (1) the growth of colonies within the nursery exceeded the growth rates of wild staghorn colonies in the same region; (2) the collection of branch tips did not result in any further mortality to the donor colonies beyond the coral removed for transplantation; (3) decreases in linear extension of the donor branches were only temporary and donor branches grew faster than control branches after an initial recovery period of approximately 3-6 weeks; (4) fragmentation did not affect the growth rates of non-donor branches within the same colony; (5) small branch tips experienced initial mortality due to handling and trans- portation but surviving tips grew well over time; and (6) when the growth of the branch tips is added to the regrowth of the fragmented donor branches, the new coral produced was 1.4-1.8 times more than new growth in undisturbed colonies. Based on these results, the collection of small (2.5-3.5 cm) branch tips was an effective propagation method for this branching coral species resulting in increased biomass accumulation and limited damage to parental stocks.

The relationship between the coral genotype and the environment is an important area of research in degraded coral reef ecosystems. We used a reciprocal outplanting experiment with 930 corals representing ten genotypes on each of eight reefs to investigate the influence of genotype and the environment on growth and survivorship in the threatened Caribbean staghorn coral, Acropora cervicornis. Coral genotype and site were strong drivers of coral growth and individual genotypes exhibited flexible, non-conserved reaction norms, complemented by ten-fold differences in growth between specific G-E combinations. Growth plasticity may diminish the influence of local adaptation, where foreign corals grew faster than native corals at their home sites. Novel combinations of environment and genotype also significantly affected disturbance response during and after the 2015 bleaching event, where these factors acted synergistically to drive variation in bleaching and recovery. Importantly, small differences in temperature stress elicit variable patterns of survivorship based on genotype and illustrate the importance of novel combinations of coral genetics and small differences between sites representing habitat refugia. In this context, acclimatization and flexibility is especially important given the long lifespan of corals coping with complex environmental change. The combined influence of site and genotype creates short-term differences in growth and survivorship, contributing to the standing genetic variation needed for adaptation to occur over longer timescales and the recovery of degraded reefs through natural mechanisms.

BACKGROUND: The drastic decline in the abundance of Caribbean acroporid corals (Acropora cervicornis, A. palmata) has prompted the listing of this genus as threatened as well as the development of a regional propagation and restoration program. Using in situ underwater nurseries, we documented the influence of coral genotype and symbiont identity, colony size, and propagation method on the growth and branching patterns of staghorn corals in Florida and the Dominican Republic. METHODOLOGY/PRINCIPAL FINDINGS: Individual tracking of> 1700 nursery-grown staghorn fragments and colonies from 37 distinct genotypes (identified using microsatellites) in Florida and the Dominican Republic revealed a significant positive relationship between size and growth, but a decreasing rate of productivity with increasing size. Pruning vigor (enhanced growth after fragmentation) was documented even in colonies that lost 95% of their coral tissue/skeleton, indicating that high productivity can be maintained within nurseries by sequentially fragmenting corals. A significant effect of coral genotype was documented for corals grown in a common-garden setting, with fast-growing genotypes growing up to an order of magnitude faster than slow-growing genotypes. Algal-symbiont identity established using qPCR techniques showed that clade A (likely Symbiodinium A3) was the dominant symbiont type for all coral genotypes, except for one coral genotype in the DR and two in Florida that were dominated by clade C, with A- and C-dominated genotypes having similar growth rates. CONCLUSION/SIGNIFICANCE: The threatened Caribbean staghorn coral is capable of extremely fast growth, with annual productivity rates exceeding 5 cm of new coral produced for every cm of existing coral. This species benefits from high fragment survivorship coupled by the pruning vigor experienced by the parent colonies after fragmentation. These life-history characteristics make A. cervicornis a successful candidate nursery species and provide optimism for the potential role that active propagation can play in the recovery of this keystone species.