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Once one of the predominant reef-building corals in the region, Acropora cervicornis is now a focal species of coral restoration efforts in Florida and the western Caribbean. Scientists and restoration practitioners have been independently collecting phenotypic data on genets of A. cervicornis grown in restoration nurseries. While these data are important for understanding the intraspecific response to varying environmental conditions, and thus the potential genetic contribution to phenotypic variation, in isolation these observations are of limited use for large-scale, multi- institution restoration efforts that are becoming increasingly necessary. Here, we present the Acropora cervicornis Data Coordination Hub, a web-accessible relational database to align disparate datasets to compare genet-specific performance. In this data descriptor, we release data for 248 genets evaluated across 38 separate traits. We present a framework to align datasets with the ultimate goal of facilitating informed, data-driven restoration throughout the Caribbean.

Difference-in-differences analysis with staggered treatment timing is frequently used to assess the impact of policy changes on corporate outcomes in academic research. However, recent advances in econometric theory show that such designs are likely to be biased in the presence of treatment effect heterogeneity. Given the pronounced use of staggered treatment designs in applied corporate finance and accounting research, this finding potentially impacts a large swath of prior findings in these fields. We survey the nascent literature and document how and when such bias arises from treatment effect heterogeneity. We apply recently proposed methods to a set of prior published results, and find that correcting for the bias induced by the staggered nature of policy adoption frequently impacts the estimated effect from standard difference-in-difference studies. In many cases, the reported effects in prior research become indistinguishable from zero.

Stony coral tissue loss disease (SCTLD) has been causing significant whole colony mortality on reefs in Florida and the Caribbean. The cause of SCTLD remains unknown, with the limited concurrence of SCTLD-associated bacteria among studies. We conducted a meta-analysis of 16S ribosomal RNA gene datasets generated by 16 field and laboratory SCTLD studies to find consistent bacteria associated with SCTLD across disease zones (vulnerable, endemic, and epidemic), coral species, coral compartments (mucus, tissue, and skeleton), and colony health states (apparently healthy colony tissue (AH), and unaffected (DU) and lesion (DL) tissue from diseased colonies). We also evaluated bacteria in seawater and sediment, which may be sources of SCTLD transmission. Although AH colonies in endemic and epidemic zones harbor bacteria associated with SCTLD lesions, and aquaria and field samples had distinct microbial compositions, there were still clear differences in the microbial composition among AH, DU, and DL in the combined dataset. Alpha-diversity between AH and DL was not different; however, DU showed increased alpha-diversity compared to AH, indicating that, prior to lesion formation, corals may undergo a disturbance to the microbiome. This disturbance may be driven by Flavobacteriales, which were especially enriched in DU. In DL, Rhodobacterales and Peptostreptococcales–Tissierellales were prominent in structuring microbial interactions. We also predict an enrichment of an alpha-toxin in DL samples which is typically found in Clostridia. We provide a consensus of SCTLD-associated bacteria prior to and during lesion formation and identify how these taxa vary across studies, coral species, coral compartments, seawater, and sediment.

Climate change is radically altering coral reef ecosystems, mainly through increasingly frequent and severe bleaching events. Yet, some reefs have exhibited higher thermal tolerance after bleaching severely the first time. To understand changes in thermal tolerance in the eastern tropical Pacific (ETP), we compiled four decades of temperature, coral cover, coral bleaching, and mortality data, including three mass bleaching events during the 1982 to 1983, 1997 to 1998 and 2015 to 2016 El Niño heatwaves. Higher heat resistance in later bleaching events was detected in the dominant framework-building genus, Pocillopora, while other coral taxa exhibited similar susceptibility across events. Genetic analyses of Pocillopora spp . colonies and their algal symbionts (2014 to 2016) revealed that one of two Pocillopora lineages present in the region ( Pocillopora “ type 1”) increased its association with thermotolerant algal symbionts ( Durusdinium glynnii ) during the 2015 to 2016 heat stress event. This lineage experienced lower bleaching and mortality compared with Pocillopora “type 3”, which did not acquire D. glynnii . Under projected thermal stress, ETP reefs may be able to preserve high coral cover through the 2060s or later, mainly composed of Pocillopora colonies that associate with D. glynnii . However, although the low-diversity, high-cover reefs of the ETP could illustrate a potential functional state for some future reefs, this state may only be temporary unless global greenhouse gas emissions and resultant global warming are curtailed.

Although coexisting mangrove-coral (CMC) habitats have been identified and categorized globally, they are still underreported and understudied. Visual surveys revealed the presence of five species of corals in two out of four potential CMC habitats around Biscayne Bay, Miami, Florida, a highly urbanized subtropical lagoon. These corals were dominated by algal symbionts in the genus Breviolum, suggesting these low-light but thermally variable environments may be buffered from photoinhibition stress that characterizes nearby hardbottom environments. Further surveys and monitoring of CMCs, particularly in urban environments, may inform coastal community ecology and advance conservation and restoration efforts.

Coral disease has progressively become one of the most pressing issues affecting coral reef survival. In the last 50 years, several reefs throughout the Caribbean have been severely impacted by increased frequency and intensity of disease outbreaks leading to coral death. A recent example of this is stony coral tissue loss disease which has quickly spread throughout the Caribbean, devastating coral reef ecosystems. Emerging from these disease outbreaks has been a coordinated research response that often integrates ‘omics techniques to better understand the coral immune system. ‘Omics techniques encompass a wide range of technologies used to identify large scale gene, DNA, metabolite, and protein expression. In this review, we discuss what is known about coral immunity and coral disease from an ‘omics perspective. We reflect on the development of biomarkers and discuss ways in which coral disease experiments to test immunity can be improved. Lastly, we consider how existing data can be better leveraged to combat future coral disease outbreaks.

Coral cover is declining worldwide due to multiple interacting threats. We compared the effects of elevated nutrients and temperature on three Caribbean corals: Acropora cervicornis, Orbicella faveolata, and Siderastrea siderea. Colonies hosting different algal symbionts were exposed to either ambient nutrients (A), elevated NH4 (N), or elevated NH4 + PO4 (N + P) at control temperatures (26 °C) for > 2 months, followed by a 3-week thermal challenge (31.5 °C). A. cervicornis hosted Symbiodinium (S. fitti) and was highly susceptible to the combination of elevated nutrients and temperature. During heat stress, A. cervicornis pre-exposed to elevated nutrients experienced 84%–100% mortality and photochemical efficiency (Fv/Fm) declines of 41–50%. In comparison, no mortality and lower Fv/Fm declines (11–20%) occurred in A. cervicornis that were heat-stressed but not pre-exposed to nutrients. O. faveolata and S. siderea response to heat stress was determined by their algal symbiont community and was not affected by nutrients. O. faveolata predominantly hosted Durusdinium trenchii or Breviolum, but only corals hosting Breviolum were susceptible to heat, experiencing 100% mortality, regardless of nutrient treatment. S. siderea colonies predominantly hosted Cladocopium C1 (C. goreaui), Cladocopium C3, D. trenchii, or variable proportions of Cladocopium C1 and D. trenchii. This species was resilient to elevated nutrients and temperature, with no significant mortality in any of the treatments. However, during heat stress, S. siderea hosting Cladocopium C3 suffered higher reductions in Fv/Fm (41–56%) compared to S. siderea hosting Cladocopium C1 and D. trenchii (17–26% and 10–16%, respectively). These differences in holobiont susceptibility to elevated nutrients and heat may help explain historical declines in A. cervicornis starting decades earlier than other Caribbean corals. Our results suggest that tackling only warming temperatures may be insufficient to ensure the continued persistence of Caribbean corals, especially A. cervicornis. Reducing nutrient inputs to reefs may also be necessary for these iconic coral species to survive.

Intervention strategies to enhance coral resilience include manipulating the association between corals and their algal endosymbionts. While hosting thermotolerant Durusdinium trenchii can increase bleaching thresholds in adults, its effects remain largely unknown during the early life stages of Caribbean corals. Here, we tested if Orbicella faveolata recruits could establish symbiosis with D. trenchii supplied by nearby “donor” colonies and examined the resulting ecological trade-offs to evaluate early Symbiodiniaceae manipulation as a scalable tool for reef restoration. We exposed aposymbiotic recruits to 29°C or 31°C and to fragments of either Montastraea cavernosa (containing Cladocopium) or Siderastrea siderea (containing D. trenchii). After 60 days, recruits reared with D. trenchii donors hosted nearly three times more D. trenchii than those with Cladocopium donors, suggesting that recruits can acquire Symbiodiniaceae from nearby corals of different species. Temperature did not affect D. trenchii uptake. Next, donor colonies were removed and surviving recruits were maintained for three months at ambient temperatures, after which a subset was exposed to a 60-day heat stress trial. Recruits previously reared at 31°C survived twice as long at 34°C as those reared at 29°C, suggesting that pre-exposure to heat can prime recruits to withstand future thermal stress. In addition, recruits hosting primarily D. trenchii survived twice as long at 34°C as those hosting little or no D. trenchii. However, the proportion of D. trenchii hosted was negatively correlated with polyp size and symbiont density, indicating a trade-off between growth (of both host and symbiont) and heat tolerance. These findings suggest that, while donor colonies may be effective sources for seeding coral recruits with thermotolerant symbionts, practitioners will need to balance the likely benefits and costs of these approaches when designing restoration strategies.

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

Prospects for coral persistence through increasingly frequent and extended heatwaves seem bleak. Coral recovery from bleaching is only known to occur after temperatures return to normal, and mitigation of local stressors does not appear to augment coral survival. Capitalizing on a natural experiment in the equatorial Pacific, we track individual coral colonies at sites spanning a gradient of local anthropogenic disturbance through a tropical heatwave of unprecedented duration. Unexpectedly, some corals survived the event by recovering from bleaching while still at elevated temperatures. These corals initially had heat-sensitive algal symbiont communities, endured bleaching, and then recovered through proliferation of heat-tolerant symbionts. This pathway to survival only occurred in the absence of strong local stressors. In contrast, corals in highly disturbed areas were already dominated by heat-tolerant symbionts, and despite initially resisting bleaching, these corals had no survival advantage in one species and 3.3 times lower survival in the other. These unanticipated connections between disturbance, coral symbioses and heat stress resilience reveal multiple pathways to coral survival through future prolonged heatwaves., Climate change and local anthropogenic stressors threaten the persistence of coral reefs. Here the authors track coral bleaching over the course of a heatwave and find that some colonies recovered from bleaching while high temperatures persisted, but only at sites lacking in other strong anthropogenic stressors.

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.

Stony coral tissue loss disease (SCTLD) has devastated coral populations along Florida’s Coral Reef and beyond. Although widespread infection and mortality of adult colonies have been documented, no studies have yet investigated the susceptibility of recruits to this disease. Here, we subjected eight-month-old Diploria labyrinthiformis recruits and four-month-old Colpophyllia natans recruits to two sequential exposures to SCTLD in the laboratory to track infection and assess potential resilience. Both species began to develop lesions as early as 48 h after exposure began. During the first exposure, 59.6% of C. natans recruits lost all tissue (died) within two to eight days of developing lesions, whereas D. labyrinthiformis recruits experienced slower tissue loss and minimal eventual mortality. In C. natans, larger recruits and those fused into groups of multiple genets (chimeras) exhibited the highest survivorship. In contrast, smaller and/or single (ungrouped) recruits had the lowest survivorship (9.9 - 24.8%). After 20 days, a second SCTLD exposure was delivered to further test resistance in remaining recruits, and all recruits of both species succumbed within six days. Although no recruits showed absolute resistance to SCTLD following repeated exposures, our results provide evidence that interactions between size and chimerism can impact relative resistance in C. natans. This study represents the first report of SCTLD in Caribbean coral recruits and carries implications for natural species recovery and reef restoration efforts. Additional research on the susceptibility of coral juveniles to SCTLD is urgently needed, to include different species, locations, parents, and algal symbionts, with the goals of assessing relative susceptibility and identifying potential sources of resilience for this critical life history stage.

Stony coral tissue loss disease (SCTLD) has devastated coral populations along Florida’s Coral Reef and beyond. Although widespread infection and mortality of adult colonies have been documented, no studies have yet investigated the susceptibility of recruits to this disease. Here, we exposed eight-month-old Diploria labyrinthiformis recruits and four-month-old Colpophyllia natans recruits to two sequential doses of SCTLD in the laboratory to track infection and assess potential resilience. Both species began to develop lesions as early as 48 h after exposure began. During the first dose, 59.0% of C. natans recruits lost all tissue (died) within two to eight days of developing lesions, whereas D. labyrinthiformis recruits experienced significantly slower rates of tissue loss and minimal eventual mortality. In C. natans, larger recruits and those fused into groups of multiple genets (chimeras) exhibited the highest survivorship. In contrast, smaller and/or single (ungrouped) recruits had the lowest survivorship (9.9 - 26.5%). After 20 days, a second SCTLD dose was delivered to further test resistance in remaining recruits, and all recruits of both species succumbed within 6 days. Although no recruits showed absolute resistance to SCTLD following repeated exposures, our results provide evidence that interactions between species, size, and chimerism can impact relative resistance. This study represents the first report of SCTLD in Caribbean coral recruits and carries implications for natural species recovery and reef restoration efforts. Additional research on the susceptibility of coral juveniles to SCTLD is urgently needed, to include different species, locations, parents, and algal symbionts, with the goal of assessing relative susceptibility and identifying potential sources of resilience for this critical life history stage.

The rapid loss of reef-building corals owing to ocean warming is driving the development of interventions such as coral propagation and restoration, selective breeding and assisted gene flow. Many of these interventions target naturally heat-tolerant individuals to boost climate resilience, but the challenges of quickly and reliably quantifying heat tolerance and identifying thermotolerant individuals have hampered implementation. Here, we used coral bleaching automated stress systems to perform rapid, standardized heat tolerance assays on 229 colonies of Acropora cervicornis across six coral nurseries spanning Florida's Coral Reef, USA. Analysis of heat stress dose–response curves for each colony revealed a broad range in thermal tolerance among individuals (approx. 2.5°C range in F v /F m ED50), with highly reproducible rankings across independent tests ( r = 0.76). Most phenotypic variation occurred within nurseries rather than between them, pointing to a potentially dominant role of fixed genetic effects in setting thermal tolerance and widespread distribution of tolerant individuals throughout the population. The identification of tolerant individuals provides immediately actionable information to optimize nursery and restoration programmes for Florida's threatened staghorn corals. This work further provides a blueprint for future efforts to identify and source thermally tolerant corals for conservation interventions worldwide.

Coral reefs function as submerged breakwaters providing wave mitigation and flood-reduction benefits for coastal communities. Although the wave-reducing capacity of reefs has been associated with wave breaking and friction, studies quantifying the relative contribution by corals are lacking. To fill this gap, a series of experiments was conducted on a trapezoidal artificial reef model with and without fragments of staghorn coral skeletons attached. The experiments were performed at the University of Miami’s Surge-Structure-Atmosphere-Interaction (SUSTAIN) Facility, a large-scale wind/wave tank, where the influence of coral skeletons on wave reduction under different wave and depth conditions was quantified through water level and wave measurements before and after the reef model. Coral skeletons reduce wave transmission and increase wave-energy dissipation, with the amount depending on the hydrodynamic conditions and relative geometrical characteristics of the reef. The trapezoidal artificial coral reef model was found to reduce up to 98% of the wave energy with the coral contribution estimated to be up to 56% of the total wave-energy dissipation. Depending on the conditions, coral skeletons can thus enhance significantly, through friction, the wave-reducing capability of a reef.

Host species often support a genetically diverse guild of symbionts, the identity and performance of which can determine holobiont fitness under particular environmental conditions. These symbiont communities are structured by a complex set of potential interactions, both positive and negative, between the host and symbionts and among symbionts. In reef‐building corals, stable associations with specific symbiont species are common, and we hypothesize that this is partly due to ecological mechanisms, such as succession and competition, which drive patterns of symbiont winnowing in the initial colonization of new generations of coral recruits. We tested this hypothesis using the experimental framework of the de Wit replacement series and found that competitive interactions occurred among symbionts which were characterized by unique ecological strategies. Aposymbiotic octocoral recruits within high‐ and low‐light environments were inoculated with one of three Symbiodiniaceae species as monocultures or with cross‐paired mixtures, and we tracked symbiont uptake using quantitative genetic assays. Priority effects, in which early colonizers excluded competitive dominants, were evidenced under low light, but these early opportunistic species were later succeeded by competitive dominants. Under high light, a more consistent competitive hierarchy was established in which competitive dominants outgrew and limited the abundance of others. These findings provide insight into mechanisms of microbial community organization and symbiosis breakdown and recovery. Furthermore, transitions in competitive outcomes across spatial and temporal environmental variation may improve lifetime host fitness., Reef‐building corals rely on a genetically diverse group of dinoflagellate symbionts to meet their nutritional needs. The ecological mechanisms that regulate symbiont communities are not well understood. Here, we show that competition and succession among symbiont species are important in the early stages of the symbiosis.

To survive the pelagic stage, reef fish larvae need to find a settlement habitat and determine its suitability using a combination of environmental cues. Previous studies have shown that fish larvae are attracted by different components of their settlement habitat, such as conspecifics, algae, coral rubble, or living corals. However, it is not known whether larval fish use coral diversity as a settlement cue. Here, we tested the ability of presettlement reef fish larvae to discriminate coral diversity in laboratory experiments. We constructed coral assemblages of equal surface area, but with different coral species richness using live coral colonies of five species [Acropora cervicornis (Lamarck, 1816), Dichocoenia stokesii Milne-Edwards and Haime, 1848, Montastrea cavernosa (Linnaeus, 1767), Siderastrea siderea (Ellis and Solander, 1786), and Stephanocoenia intersepta (Lamarck, 1836)] and recorded the settlement choice of individual reef fish larvae. We found that reef fish larvae seem to prefer to settle on assemblages with higher coral diversity, regardless of the species used. We then used a two-choice tank to test the potential of reef fish larvae to visually perceive different coral species diversity and found that higher diversity attracts more settlement stage reef fish larvae, potentially changing the distribution of settlers at local scales. If preference for higher coral diversity stems from attraction to olfactory or other long-range cues—in addition to visual preference—coral diversity may play a role in connectivity among fish populations. This mechanism may further explain why degraded coral reefs do not maintain abundant fish populations.

The late twentieth-century American South hosted a thriving lakefront development industry. The arrival of the invasive aquatic plant hydrilla in reservoirs across the region during the 197...

Coral research is being ushered into the genomic era. To fully capitalize on the potential discoveries from this genomic revolution, the rapidly increasing number of high-quality genomes requires effective pairing with rigorous taxonomic characterizations of specimens and the contextualization of their ecological relevance. However, to date there is no formal framework that genomicists, taxonomists, and coral scientists can collectively use to systematically acquire and link these data. Spurred by the recently announced “Coral symbiosis sensitivity to environmental change hub” under the “Aquatic Symbiosis Genomics Project” - a collaboration between the Wellcome Sanger Institute and the Gordon and Betty Moore Foundation to generate gold-standard genome sequences for coral animal hosts and their associated Symbiodiniaceae microalgae (among the sequencing of many other symbiotic aquatic species) - we outline consensus guidelines to reconcile different types of data. The metaorganism nature of the coral holobiont provides a particular challenge in this context and is a key factor to consider for developing a framework to consolidate genomic, taxonomic, and ecological (meta)data. Ideally, genomic data should be accompanied by taxonomic references, i.e., skeletal vouchers as formal morphological references for corals and strain specimens in the case of microalgal and bacterial symbionts (cultured isolates). However, exhaustive taxonomic characterization of all coral holobiont member species is currently not feasible simply because we do not have a comprehensive understanding of all the organisms that constitute the coral holobiont. Nevertheless, guidelines on minimal, recommended, and ideal-case descriptions for the major coral holobiont constituents (coral animal, Symbiodiniaceae microalgae, and prokaryotes) will undoubtedly help in future referencing and will facilitate comparative studies. We hope that the guidelines outlined here, which we will adhere to as part of the Aquatic Symbiosis Genomics Project sub-hub focused on coral symbioses, will be useful to a broader community and their implementation will facilitate cross- and meta-data comparisons and analyses. CV acknowledges funding from the German Research Foundation (DFG), grants 433042944 and 458901010. Open Access publication fees are covered by an institutional agreement of the University of Konstanz.

Coral cover is declining worldwide due to multiple interacting threats. We compared the effects of elevated nutrients and temperature on three Caribbean corals: Acropora cervicornis, Orbicella faveolata, and Siderastrea siderea. Colonies hosting different algal types were exposed to either ambient nutrients (A), elevated NH4 (N), or elevated NH4 + PO4 (N+P) at control temperatures (26 °C) for > 2 months, followed by a 3-week thermal challenge (31.5 °C). A. cervicornis hosted Symbiodinium (S. fitti) and was highly susceptible to the combination of elevated nutrients and temperature. During heat stress, A. cervicornis pre-exposed to elevated nutrients experienced 84%-100% mortality and photochemical efficiency (Fv/Fm) declines of 41-50%. In comparison, no mortality and lower Fv/Fm declines (11-20%) occurred in A. cervicornis that were heat-stressed but not pre-exposed to nutrients. O. faveolata and S. siderea response to heat stress was determined by their algal symbiont community and was not affected by nutrients. O. faveolata predominantly hosted Durusdinium trenchii or Breviolum, but only corals hosting Breviolum were susceptible to heat, experiencing 100% mortality, regardless of nutrient treatment. S. siderea colonies predominantly hosted Cladocopium C1 (C. goreaui), Cladocopium C3, D. trenchii, or variable proportions of Cladocopium C1 and D. trenchii. This species was resilient to elevated nutrients and temperature, with no significant mortality in any of the treatments. However, during heat stress, S. siderea hosting Cladocopium C3 suffered higher reductions in Fv/Fm (41-56%) compared to S. siderea hosting Cladocopium C1 and D. trenchii (17-26% and 10-16%, respectively). These differences in holobiont susceptibility to elevated nutrients and heat may help explain historical declines in A. cervicornis starting decades earlier than other Caribbean corals. Our results suggest that tackling only warming temperatures may be insufficient to ensure the continued persistence of Caribbean corals, especially A. cervicornis. Reducing nutrient inputs to reefs may also be necessary for these iconic coral species to survive.

For millennia, coastal and marine ecosystems have adapted and flourished in the Red Sea’s unique environment. Surrounded by deserts on all sides, the Red Sea is subjected to high dust inputs and receives very little freshwater input, and so harbors a high salinity. Coral reefs, seagrass meadows, and mangroves flourish in this environment and provide socio-economic and environmental benefits to the bordering coastlines and countries. Interestingly, while coral reef ecosystems are currently experiencing rapid decline on a global scale, those in the Red Sea appear to be in relatively better shape. That said, they are certainly not immune to the stressors that cause degradation, such as increasing ocean temperature, acidification and pollution. In many regions, ecosystems are already severely deteriorating and are further threatened by increasing population pressure and large coastal development projects. Degradation of these marine habitats will lead to environmental costs, as well as significant economic losses. Therefore, it will result in a missed opportunity for the bordering countries to develop a sustainable blue economy and integrate innovative nature-based solutions. Recognizing that securing the Red Sea ecosystems’ future must occur in synergy with continued social and economic growth, we developed an action plan for the conservation, restoration, and growth of marine environments of the Red Sea. We then investigated the level of resources for financial and economic investment that may incentivize these activities. This study presents a set of commercially viable financial investment strategies, ecological innovations, and sustainable development opportunities, which can, if implemented strategically, help ensure long-term economic benefits while promoting environmental conservation. We make a case for investing in blue natural capital and propose a strategic development model that relies on maintaining the health of natural ecosystems to safeguard the Red Sea’s sustainable development.

International audience; Maintaining coral reef ecosystems is a social imperative, because so many people depend on coral reefs for food production, shoreline protection, and livelihoods. The survival of reefs this century, however, is threatened by the mounting effects of climate change. Climate mitigation is the foremost and essential action to prevent coral reef ecosystem collapse. Without it, reefs will become extremely diminished within the next 20-30 years. Even with strong climate mitigation, however, existing conservation measures such as marine protected areas and fisheries management are no longer sufficient to sustain the ecosystem and many additional and innovative actions to increase reef resilience must also be taken. In this paper we assess the suite of protections and actions in terms of their potential be effective according to a set of criteria that include effectiveness, readiness, co-benefits and disbenefits. Even with the best scientific innovation, saving coral reefs will require a well-funded, welldesigned, and rapidly executed strategy with political and social commitments at the level of other grand challenges.

Scleractinian corals are the principal builders of coral reefs. These megadiverse ecosystems are declining due to coral mortality from a variety of stressors, including disease. Corals are dependent upon symbiotic dinoflagellates in the family Symbiodiniaceae for phototrophic contributions to their energy budgets. However, suppression of host immunity may be necessary to maintain these intracellular symbioses. To explore the consequences of symbiosis on host immunity, we manipulated symbiont density by increasing nitrogen availability. Replicate cores from four colonies of the Caribbean coral, Orbicella faveolata, were reared in seawater treated with ammonium for one month to increase symbiont density. Corals were then immune-stimulated using lipopolysaccharide and poly I:C. Gene expression was analyzed using RNAseq and symbiont density was quantified (as symbiont:host cell ratio) using quantitative PCR (qPCR). Ammonium treatment had limited positive effects on host immunity. In contrast, increases in symbiont density had large negative effects on host expression of immune-related transcripts. These results suggest links between nutrient enrichment and coral disease may be the result of the effect of increased symbiont density on host immunity, rather than the direct effect of the nutrients. Further study of the trade-offs between symbiont density and immunity may help understand how decreasing water quality and increasing disease will shape future reef communities.

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.

Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations to boost the abundance of these symbionts in corals may increase resilience in warming oceans. However, the thermotolerant symbiont Durusdinium trenchii may reduce growth and fecundity in Caribbean corals, and these tradeoffs need to be better understood as this symbiont spreads through the region. We sought to understand how D. trenchii modulates coral gene expression by manipulating symbiont communities in Montastraea cavernosa to produce replicate ramets containing D. trenchii together with paired ramets of these same genets (n = 3) containing Cladocopium C3 symbionts. We then examined differences in global gene expression between corals hosting Durusdinium and Cladocopium under control temperatures, and in response to short-term heat stress. We identified numerous transcriptional differences associated with symbiont identity, which explained 2%-14% of the transcriptional variance. Corals with D. trenchii upregulated genes related to translation, ribosomal structure and biogenesis, and downregulated genes related to extracellular structures, and carbohydrate and lipid transport and metabolism, relative to corals with Cladocopium. Unexpectedly, these changes were similar to those observed in Cladocopium-dominated corals in response to heat stress, suggesting that thermotolerant D. trenchii may cause corals to increase expression of heat stress-responsive genes, explaining both the increased heat tolerance and the associated energetic tradeoffs in corals containing D. trenchii. These findings provide insight into the ecological changes occurring on contemporary coral reefs in response to climate change, and the diverse ways in which different symbionts modulate emergent phenotypes of their hosts.

Comparative analysis of the expanding genomic resources for scleractinian corals may provide insights into the evolution of these organisms, with implications for their continued persistence under global climate change. Here, we sequenced and annotated the genome of Pocillopora damicornis, one of the most abundant and widespread corals in the world. We compared this genome, based on protein-coding gene orthology, with other publicly available coral genomes (Cnidaria, Anthozoa, Scleractinia), as well as genomes from other anthozoan groups (Actiniaria, Corallimorpharia), and two basal metazoan outgroup phlya (Porifera, Ctenophora). We found that 46.6% of P. damicornis genes had orthologs in all other scleractinians, defining a coral ‘core’ genome enriched in basic housekeeping functions. Of these core genes, 3.7% were unique to scleractinians and were enriched in immune functionality, suggesting an important role of the immune system in coral evolution. Genes occurring only in P. damicornis were enriched in cellular signaling and stress response pathways, and we found similar immune-related gene family expansions in each coral species, indicating that immune system diversification may be a prominent feature of scleractinian coral evolution at multiple taxonomic levels. Diversification of the immune gene repertoire may underlie scleractinian adaptations to symbiosis, pathogen interactions, and environmental stress.

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., Mesophotic reefs (30‐150 m) have been proposed as potential refugia that facilitate the recovery of degraded shallow reefs following acute disturbances at shallower depths, such as coral bleaching and disease. We find extensive population structure among mesophotic Montastraea cavernosa, even between nearby 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 shallow‐water counterparts.

As coral reefs continue to decline due to climate change and other stressors, scientists have proposed adopting genomic tools, such as biomarkers, to aid in the conservation and restoration of these threatened ecosystems. Biomarkers are easily measured indicators of biological processes that can be used to predict or diagnose health, resilience, and other key performance metrics. The ultimate goal of developing biomarkers is to determine the conservation value and utility of a given coral colony, including the host animal, its algal symbionts, and their microbial partners. However, this goal remains distant because most efforts have not yet moved beyond the initial discovery phase. We review recent progress in the development of coral molecular biomarkers from a practical standpoint and consider the many challenges that remain as roadblocks to large‐scale implementation. We caution practitioners that, while biomarkers are a promising technology, they are unlikely to be available for field application in the near future barring a rapid shift in research focus from discovery to subsequent validation and field trials. To facilitate such a shift, we propose a stepwise framework to guide additional study in this area, with the aim of accelerating practical molecular biomarker development to enhance coral restoration practice.

Active coral restoration typically involves two interventions: crossing gametes to facilitate sexual larval propagation; and fragmenting, growing, and outplanting adult colonies to enhance asexual propagation. From an evolutionary perspective, the goal of these efforts is to establish self‐sustaining, sexually reproducing coral populations that have sufficient genetic and phenotypic variation to adapt to changing environments. Here, we provide concrete guidelines to help restoration practitioners meet this goal for most Caribbean species of interest. To enable the persistence of coral populations exposed to severe selection pressure from many stressors, a mixed provenance strategy is suggested: genetically unique colonies (genets) should be sourced both locally as well as from more distant, environmentally distinct sites. Sourcing three to four genets per reef along environmental gradients should be sufficient to capture a majority of intraspecies genetic diversity. It is best for practitioners to propagate genets with one or more phenotypic traits that are predicted to be valuable in the future, such as low partial mortality, high wound healing rate, high skeletal growth rate, bleaching resilience, infectious disease resilience, and high sexual reproductive output. Some effort should also be reserved for underperforming genets because colonies that grow poorly in nurseries sometimes thrive once returned to the reef and may harbor genetic variants with as yet unrecognized value. Outplants should be clustered in groups of four to six genets to enable successful fertilization upon maturation. Current evidence indicates that translocating genets among distant reefs is unlikely to be problematic from a population genetic perspective but will likely provide substantial adaptive benefits. Similarly, inbreeding depression is not a concern given that current practices only raise first‐generation offspring. Thus, proceeding with the proposed management strategies even in the absence of a detailed population genetic analysis of the focal species at sites targeted for restoration is the best course of action. These basic guidelines should help maximize the adaptive potential of reef‐building corals facing a rapidly changing environment.

The local environment shapes coral physiology through acclimatization and also selects for genotypes best suited to a particular site. Both acclimatization and selection likely affect the response of corals to future climate change. The local environment is therefore an important factor to consider for restoration ecology. In this study, we exposed Orbicella faveolata from two different locations in Florida (Emerald Reef, near Key Biscayne in the upper Florida Keys, and Truman Harbor near Key West in the lower Florida Keys) that were common-gardened for one month prior to experimentation to four temperature, CO 2 , and food availability treatments (26°C/390 ppm, 26°C/1000 ppm, 31°C/390 ppm, and 31°C/1000 ppm where each of these treatments had fed and unfed components). The goal was to determine how the same species of coral from different locations would respond to projected climate change scenarios. We found that growth (measured as changes in buoyant weight) was highly correlated to source location (i.e., whether the corals came from Emerald Reef or Truman Harbor) and not to parent colony, and growth, symbiont density, chlorophyll a content, and lipid content were highly correlated to feeding regime. These findings show that within a single reef tract, (i.e. the Florida Reef Tract), source location and food availability matter for the physiological outcome of a coral’s stress response, and suggest that an explicit consideration of these effects may be important for management activities such as coral restoration, transplantation, and MPA placement.

Gene expression biomarkers (GEBs) are emerging as powerful diagnostic tools for identifying and characterizing coral stress. Their capacity to detect sublethal stress prior to the onset of signs at the organismal level that might already indicate significant damage makes them more precise and proactive compared to traditional monitoring techniques. A high number of candidate GEBs, including certain heat shock protein genes, metabolic genes, oxidative stress genes, immune response genes, ion transport genes, and structural genes have been investigated, and some genes, including hsp16, Cacna1, MnSOD, SLC26, and Nf-kB, are already showing excellent potential as reliable indicators of thermal stress in corals. In this mini-review, we synthesize the current state of knowledge of scleractinian coral GEBs and highlight gaps in our understanding that identify directions for future work. We also address the underlying sources of variation that have sometimes led to contrasting results between studies, such as differences in experimental set-up and approach, intrinsic variation in the expression profiles of different experimental organisms (such as between different colonies or their algal symbionts), diel cycles, varying thermal history, and different expression thresholds. Despite advances in our understanding there is still no universally accepted biomarker of thermal stress, the molecular response of corals to heat stress is still unclear, and biomarker research in Symbiodinium still lags behind that of the host. These gaps should be addressed in future work.

Anthropogenic climate change compromises reef growth as a result of increasing temperatures and ocean acidification. Scleractinian corals vary in their sensitivity to these variables, suggesting species composition will influence how reef communities respond to future climate change. Because data are lacking for many species, most studies that model future reef growth rely on uniform scleractinian calcification sensitivities to temperature and ocean acidification. In order to address this knowledge gap, calcification of twelve common and understudied Caribbean coral species was measured for two months under crossed temperatures (27°C, 30.3°C) and CO2 partial pressures (pCO2) (400, 900, 1300 μatm). Mixed effects models of calcification for each species were then used to project community-level scleractinian calcification using Florida Keys reef composition data and IPCC AR5 ensemble climate model data. Three of the four most abundant species, Orbicella faveolata, Montastraea cavernosa, and Porites astreoides, had negative calcification responses to both elevated temperature and pCO2. In the business-as-usual CO2 emissions scenario, reefs with high abundances of these species had projected end-of-century declines in scleractinian calcification of >50% relative to present-day rates. Siderastrea siderea, the other most-common species, was insensitive to both temperature and pCO2 within the levels tested here. Reefs dominated by this species had the most stable end-of-century growth. Under more optimistic scenarios of reduced CO2 emissions, calcification rates throughout the Florida Keys declined

As coral reefs continue to decline due to climate change and other stressors, scientists have proposed adopting genomic tools, such as biomarkers, to aid in the conservation and restoration of these threatened ecosystems. Biomarkers are easily measured indicators of higher-order biological processes that can be used to predict or diagnose health, resilience, and other key performance metrics. The ultimate goal of developing biomarkers is to determine the conservation value and utility of a given coral colony, including the host animal, its algal symbionts, and their microbial partners. However, we remain far from achieving this goal because most efforts have not yet moved beyond the initial discovery phase. Here, we review recent progress in the development of coral molecular biomarkers from a practical standpoint and consider the many challenges that remain as roadblocks to large-scale implementation. We caution practitioners that, while biomarkers are a promising technology, they are unlikely to be available for field application in the near future barring a rapid shift in research focus from discovery to subsequent validation and field trials. To facilitate such a shift, we propose a stepwise framework to guide additional study in this area, with the aim of accelerating practical molecular biomarker development to enhance coral restoration practice.

Recent molecular studies of symbiotic dinoflagellates (genus Symbiodinium) from a wide array of invertebrate hosts have revealed exceptional fine-scale symbiont diversity whose distribution among hosts, regions and environments exhibits significant biogeographic, ecological and evolutionary patterns. Here, similar molecular approaches using the internal transcribed spacer-2 (ITS-2) region were applied to investigate cryptic diversity in Symbiodinium inhabiting soritid foraminifera. Approximately 1,000 soritid specimens were collected and examined during a 12-month period over a 40 m depth gradient from a single reef in Guam, Micronesia. Out of 61 ITS-2 types distinguished, 46 were novel. Most types found are specific for soritid hosts, except for three types (C1, C15 and C19) that are common in metazoan hosts. The distribution of these symbionts was compared with the phylotype of their foraminiferal hosts, based on soritid small subunit ribosomal DNA sequences, and three new phylotypes of soritid hosts were identified based on these sequences. Phylogenetic analyses of 645 host-symbiont pairings revealed that most Symbiodinium types associated specifically with a particular foraminiferal host genus or species, and that the genetic diversity of these symbiont types was positively correlated with the genetic diversity found within each of the three host genera. Compared to previous molecular studies of Symbiodinium from other locations worldwide, the diversity reported here is exceptional and suggests that Micronesian coral reefs are home to a remarkably large Symbiodinium assemblage.

Coral populations and structural coral reefs have undergone severe reductions and losses respectively over large parts of the Galapagos Islands during and following the 1982-83 El Nino event. Coral tissue loss amounted to 95% across the Archipelago. Also at that time, all coral reefs in the central and southern islands disappeared following severe degradation and eventual collapse due primarily to intense bioerosion and low recruitment. Six sites in the southern islands have demonstrated low to moderate coral community (scattered colonies, but no carbonate framework) recovery. The iconic pocilloporid reef at Devil's Crown (Floreana Island) experienced recovery to 2007, then severe mortality during a La Nina cooling event, and is again (as of 2017) undergoing rapid recovery. Notable recovery has occurred at the central (Marchena) and northern islands (Darwin and Wolf). Of the 17 structural reefs first observed in the mid-1970s, the single surviving reef (Wellington Reef) at Darwin Island remains in a positive growth mode. The remainder either degraded to a coral community or was lost. Retrospective analyses of the age structure of corals killed in 1983, and isotopic signatures of the skeletal growth record of massive corals suggest the occurrence of robust coral populations during at least a 500-year period before 1983. The greatest potential threats to the recovery and persistence of coral reefs include: ocean warming and acidification, bioerosion, coral diseases, human population growth (increasing numbers of residents and tourists), overfishing, invasive species, pollution, and habitat destruction. Such a diverse spectrum of disturbances, acting alone or in combination, are expected to continue to cause local and archipelago-wide mortality and degradation of the coral reef ecosystem.

Regulating partner abunclance may allow symmotic organisms to mediate interaction outcomes, facilitating adaptive responses to environmental change. To explore the capacity for-adaptive regulation in an ecologically important endosymbiosis, we studied the population dynamics of symbiotic algae in reef-building corals under different abiotic contexts. We found high natural variability in symbiont abundance in corals across reefs, but this variability converged to different symbiont-specific abundances when colonies were maintained under constant conditions. When conditions changed seasonally, symbiont abundance readjusted to new equilibria. We explain these patterns using an a priori model of symbiotic costs and benefits to the coral host, which shows that the observed changes in symbiont abundance are consistent with the maximization of interaction benefit under different environmental conditions. These results indicate that, while regulating symbiont abundance helps hosts sustain maximum benefit in a dynamic environment, spatiotemporal variation in abiotic factors creates a broad range of symbiont abundances (and interaction outcomes) among corals that may account for observed natural variability in performance (e.g., growth rate) and stress tolerance (e.g., bleaching susceptibility). This cost or benefit framework provides a new perspective on the dynamic regulation of reef coral symbioses and illustrates that the dependence of interaction outcomes on biotic and abiotic contexts may be important in understanding how diverse mutualisms respond to environmental change.