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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.

Many reef invertebrates reproduce through simultaneous broadcast spawning, with an apparent advantage of overwhelming potential predators and maximizing propagule survival. Although reef fish have been observed to consume coral gamete bundles during spawning events, there are no published records of such predation by benthic invertebrates. Here, we document several instances of the ruby brittle star, Ophioderma rubicundum, capturing and consuming egg-sperm bundles of the mountainous star coral, Orbicella faveolata, and the symmetrical brain coral, Pseudodiploria strigosa, during spawning events in the Cayman Islands in 2012 and the Florida Keys in 2022. These observations are widely separated in space and time (>600 km, 10 years), suggesting that this behavior may be ubiquitous on western Atlantic reefs. Since O. rubicundum spawns on the same or subsequent nights as these coral species, we hypothesize that this opportunistic feeding behavior takes advantage of the coral’s lipid-rich bundles to recover energy reserves expended by the brittle star during gametogenesis. The consumption of coral gametes by adult brittle stars suggests a novel trophic link between reef invertebrates, and also provides evidence that ophiuroid-coral symbioses may oscillate between commensalism and parasitism depending on the ontogeny and reproductive status of both animals. Our observations provide insights into the nuanced, dynamic associations between coral reef invertebrates and may have implications for coral fecundity and resilience.

Many reef invertebrates reproduce through simultaneous broadcast spawning, with an apparent advantage of overwhelming potential predators and maximizing propagule survival. Although reef fish have been observed to consume coral gamete bundles during spawning events, there are no published records of such predation by benthic invertebrates. Here, we document several instances of the ruby brittle star, Ophioderma rubicundum, capturing and consuming egg-sperm bundles of the mountainous star coral, Orbicella faveolata, and the symmetrical brain coral, Pseudodiploria strigosa, during spawning events in the Cayman Islands in 2012 and the Florida Keys in 2022. These observations are widely separated in space and time (>600 km, 10 years), suggesting that this behavior may be ubiquitous on western Atlantic reefs. Since O. rubicundum spawns on the same or subsequent nights as these coral species, we hypothesize that this opportunistic feeding behavior takes advantage of the coral’s lipid-rich bundles to recover energy reserves expended by the brittle star during gametogenesis. The consumption of coral gametes by adult brittle stars suggests a novel trophic link between reef invertebrates, and also provides evidence that ophiuroid-coral symbioses may oscillate between commensalism and parasitism depending on the ontogeny and reproductive status of both animals. Our observations provide insights into the nuanced, dynamic associations between coral reef invertebrates and may have implications for coral fecundity and resilience.

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.

Algal symbiont shuffling in favour of more thermotolerant species has been shown to enhance coral resistance to heat-stress. Yet, the mechanistic underpinnings and long-term implications of these changes are poorly understood. This work studied the modifications in coral DNA methylation, an epigenetic mechanism involved in coral acclimatization, in response to symbiont manipulation and subsequent heat stress exposure. Symbiont composition was manipulated in the great star coral Montastraea cavernosa through controlled thermal bleaching and recovery, producing paired ramets of three genets dominated by either their native symbionts (genus Cladocopium) or the thermotolerant species (Durusdinium trenchi). Single-base genome-wide analyses showed significant modifications in DNA methylation concentrated in intergenic regions, introns and transposable elements. Remarkably, DNA methylation changes in response to heat stress were dependent on the dominant symbiont, with twice as many differentially methylated regions found in heat-stressed corals hosting different symbionts (Cladocopium vs. D. trenchii) compared to all other comparisons. Interestingly, while differential gene body methylation was not correlated with gene expression, an enrichment in differentially methylated regions was evident in repetitive genome regions. Overall, these results suggest that changes in algal symbionts favouring heat tolerant associations are accompanied by changes in DNA methylation in the coral host. The implications of these results for coral adaptation, along with future avenues of research based on current knowledge gaps, are discussed in the present work.

Climate change-amplified heatwaves are known to drive extensive mortality in marine foundation species. However, a paucity of longitudinal genomic datasets has impeded understanding of how these rapid selection events alter species’ genetic structure. Impacts of these events may be exacerbated in species with obligate symbioses, where the genetics of multiple co-evolving species may be affected. Here, we tracked the symbiotic associations and fate of reef-building corals for six years through a prolonged heatwave. Coral genetics strongly predicted survival of the common coralPoritesthrough the event, with strong differential survival (15 to 64%) apparent across morphologically identical -but genetically distinct- lineages. The event also disrupted strong associations between coral lineages and their symbiotic partners, homogenizing symbiotic assemblages across lineages and reducing the specificity of coral-algal symbioses. These results highlight that marine heatwaves threaten cryptic genetic diversity of foundation species and have the potential to decouple tight relationships between co-evolving host-symbiont pairs.

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.

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 limited concurrence of SCTLD-associated bacteria among studies. We conducted a meta-analysis of SSU 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 disease 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. While Rhodobacterales and Peptostreptococcales-Tissierellales were prominent in structuring microbial interactions in DL. Peptostreptococcales-Tissierellales specifically may contribute to lesion progression through an alpha-toxin. We provide a consensus of SCTLD-associated bacteria both prior to and during lesion progression and identify how these taxa vary across studies, coral species, coral compartments, seawater, and sediment.

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.

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.

SummaryThe staghorn coral, Acropora cervicornis, was once abundant in the Caribbean, but now is listed as critically endangered. To recover A. cervicornis populations, restoration efforts have focused on preserving genetic diversity and increasing coral cover. However, identifying stress-resistant corals can help to increase restoration success, by allocating genotypes to reefs where they are more likely to survive. We assessed the performance (growth, survivorship, and photochemical efficiency) and characterized the microbiome (prokaryotes) of six A. cervicornis genotypes that were maintained at control temperatures (~26 °C) and either ambient nutrients or elevated nutrients (elevated NH4, and elevated NH4 + PO4) for > 2 months. We then compared how these parameters changed when the corals were exposed to heat-stress (3-weeks at ~31.5 °C). We found that exposure to elevated nutrients reduced A. cervicornis performance under control temperatures and heat stress. However, there was a wide range of variation among genotypes, with three genotypes maintaining relatively higher survivorship and growth rates when exposed to nutrients alone, and nutrients followed by heat stress. Heat stress alone changed the microbial composition among genotypes more than elevated nutrients alone, but heat stress also interacted with nutrient pre-exposure to affect microbial communities. The relative abundance of Midichloriaceae and Spirochaetaceae varied by coral genotype and a high abundance of these bacterial taxa was a positive predictor of coral survivorship rate, suggesting a microbial signature that could aid in identifying resistant A. cervicornis genotypes. Our findings suggest there is significant variation among genotypes in the response of A. cervicornis to elevated nutrients and temperatures. Resistant genotypes may be identifiable via their microbiomes and prioritized for outplanting at sites characterized by high levels of nutrient pollution. Large-scale microbiome screening may help expedite targeted outplanting and could be tested and extended to facilitate the identification of genotypes with other resistance characteristics.

Anthropogenic climate change is the biggest threat to coral reefs, but reef restoration efforts are buying time for these ecosystems. Lesion recovery, which can be a determinant of colony survival, is particularly important for restored species. Here, we evaluate lesion recovery of 18 genets of Acropora cervicornis from Florida reefs with different thermal regimes in a temperature challenge experiment. Genets demonstrated significant variability in healing, which greatly slowed under heat stress. Only 35% of fragments healed at 31.5 °C compared to 99% at 28 °C. Donor reef thermal regime significantly influenced lesion recovery under heat stress with corals from warmer reefs demonstrating greater healing than corals from cooler reefs, but did not influence recovery under ambient conditions. These findings should encourage practitioners to utilize rapidly healing genets, avoid fragmentation in high temperatures, and incorporate assisted relocation by moving corals from warmer to cooler reefs, where they might succeed under future climate conditions.

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 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.