A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity.

Stony corals are colonial cnidarians that sustain the most biodiverse marine ecosystems on Earth: coral reefs. Despite their ecological importance, little is known about the cell types and molecular pathways that underpin the biology of reef-building corals. Using single-cell RNA sequencing, we define over 40 cell types across the life cycle of Stylophora pistillata. We discover specialized immune cells, and we uncover the developmental gene expression dynamics of calcium-carbonate skeleton formation. By simultaneously measuring the transcriptomes of coral cells and the algae within them, we characterize the metabolic programs involved in symbiosis in both partners. We also trace the evolution of these coral cell specializations by phylogenetic integration of multiple cnidarian cell type atlases. Overall, this study reveals the molecular and cellular basis of stony coral biology.

Unlocking the Complex Cell Biology of Coral-Dinoflagellate Symbiosis: A Model Systems Approach.

Symbiotic interactions occur in all domains of life, providing organisms with resources to adapt to new habitats. A prime example is the endosymbiosis between corals and photosynthetic dinoflagellates. Eukaryotic dinoflagellate symbionts reside inside coral cells and transfer essential nutrients to their hosts, driving the productivity of the most biodiverse marine ecosystem. Recent advances in molecular and genomic characterization have revealed symbiosis-specific genes and mechanisms shared among symbiotic cnidarians. In this review, we focus on the cellular and molecular processes that underpin the interaction between symbiont and host. We discuss symbiont acquisition via phagocytosis, modulation of host innate immunity, symbiont integration into host cell metabolism, and nutrient exchange as a fundamental aspect of stable symbiotic associations. We emphasize the importance of using model systems to dissect the cellular complexity of endosymbiosis, which ultimately serves as the basis for understanding its ecology and capacity to adapt in the face of climate change.

Distinguishing the molecular diversity, nutrient content, and energetic potential of exometabolomes produced by macroalgae and reef-building corals.

Metabolites exuded by primary producers comprise a significant fraction of marine dissolved organic matter, a poorly characterized, heterogenous mixture that dictates microbial metabolism and biogeochemical cycling. We present a foundational untargeted molecular analysis of exudates released by coral reef primary producers using liquid chromatography-tandem mass spectrometry to examine compounds produced by two coral species and three types of algae (macroalgae, turfing microalgae, and crustose coralline algae [CCA]) from Mo'orea, French Polynesia. Of 10,568 distinct ion features recovered from reef and mesocosm waters, 1,667 were exuded by producers; the majority (86%) were organism specific, reflecting a clear divide between coral and algal exometabolomes. These data allowed us to examine two tenets of coral reef ecology at the molecular level. First, stoichiometric analyses show a significantly reduced nominal carbon oxidation state of algal exometabolites than coral exometabolites, illustrating one ecological mechanism by which algal phase shifts engender fundamental changes in the biogeochemistry of reef biomes. Second, coral and algal exometabolomes were differentially enriched in organic macronutrients, revealing a mechanism for reef nutrient-recycling. Coral exometabolomes were enriched in diverse sources of nitrogen and phosphorus, including tyrosine derivatives, oleoyl-taurines, and acyl carnitines. Exometabolites of CCA and turf algae were significantly enriched in nitrogen with distinct signals from polyketide macrolactams and alkaloids, respectively. Macroalgal exometabolomes were dominated by nonnitrogenous compounds, including diverse prenol lipids and steroids. This study provides molecular-level insights into biogeochemical cycling on coral reefs and illustrates how changing benthic cover on reefs influences reef water chemistry with implications for microbial metabolism.

Alternating regimes of shallow and deep-sea diversification explain a species-richness paradox in marine fishes.

The deep sea contains a surprising diversity of life, including iconic fish groups such as anglerfishes and lanternfishes. Still, >65% of marine teleost fish species are restricted to the photic zone <200 m, which comprises less than 10% of the ocean's total volume. From a macroevolutionary perspective, this paradox may be explained by three hypotheses: 1) shallow water lineages have had more time to diversify than deep-sea lineages, 2) shallow water lineages have faster rates of speciation than deep-sea lineages, or 3) shallow-to-deep sea transition rates limit deep-sea richness. Here we use phylogenetic comparative methods to test among these three non-mutually exclusive hypotheses. While we found support for all hypotheses, the disparity in species richness is better described as the uneven outcome of alternating phases that favored shallow or deep diversification over the past 200 million y. Shallow marine teleosts became incredibly diverse 100 million y ago during a period of warm temperatures and high sea level, suggesting the importance of reefs and epicontinental settings. Conversely, deep-sea colonization and speciation was favored during brief episodes when cooling temperatures increased the efficiency of the ocean's carbon pump. Finally, time-variable ecological filters limited shallow-to-deep colonization for much of teleost history, which helped maintain higher shallow richness. A pelagic lifestyle and large jaws were associated with early deep-sea colonists, while a demersal lifestyle and a tapered body plan were typical of later colonists. Therefore, we also suggest that some hallmark characteristics of deep-sea fishes evolved prior to colonizing the deep sea.

Benzoyl Chloride Derivatization Advances the Quantification of Dissolved Polar Metabolites on Coral Reefs.

Extracellular chemical cues constitute much of the language of life among marine organisms, from microbes to mammals. Changes in this chemical pool serve as invisible signals of overall ecosystem health and disruption to this finely tuned equilibrium. In coral reefs, the scope and magnitude of the chemicals involved in maintaining reef equilibria are largely unknown. Processes involving small, polar molecules, which form the majority components of labile dissolved organic carbon, are often poorly captured using traditional techniques. We employed chemical derivatization with mass spectrometry-based targeted exometabolomics to quantify polar dissolved phase metabolites on five coral reefs in the U.S. Virgin Islands. We quantified 45 polar exometabolites, demonstrated their spatial variability, and contextualized these findings in terms of geographic and benthic cover differences. By comparing our results to previously published coral reef exometabolomes, we show the novel quantification of 23 metabolites, including central carbon metabolism compounds (e.g., glutamate) and novel metabolites such as homoserine betaine. We highlight the immense potential of chemical derivatization-based exometabolomics for quantifying labile chemical cues on coral reefs and measuring molecular level responses to environmental stressors. Overall, improving our understanding of the composition and dynamics of reef exometabolites is vital for effective ecosystem monitoring and management strategies.

Emergent Spatial Patterns Can Indicate Upcoming Regime Shifts in a Realistic Model of Coral Community.

AbstractIncreased stress on coastal ecosystems, such as coral reefs, seagrasses, kelp forests, and other habitats, can make them shift toward degraded, often algae-dominated or barren communities. This has already occurred in many places around the world, calling for new approaches to identify where such regime shifts may be triggered. Theoretical work predicts that the spatial structure of habitat-forming species should exhibit changes prior to regime shifts, such as an increase in spatial autocorrelation. However, extending this theory to marine systems requires theoretical models connecting field-supported ecological mechanisms to data and spatial patterns at relevant scales. To do so, we built a spatially explicit model of subtropical coral communities based on experiments and long-term datasets from Rapa Nui (Easter Island, Chile), to test whether spatial indicators could signal upcoming regime shifts in coral communities. Spatial indicators anticipated degradation of coral communities following increases in frequency of bleaching events or coral mortality. However, they were generally unable to signal shifts that followed herbivore loss, a widespread and well-researched source of degradation, likely because herbivory, despite being critical for the maintenance of corals, had comparatively little effect on their self-organization. Informative trends were found under both equilibrium and nonequilibrium conditions but were determined by the type of direct neighbor interactions between corals, which remain relatively poorly documented. These inconsistencies show that while this approach is promising, its application to marine systems will require detailed information about the type of stressor and filling current gaps in our knowledge of interactions at play in coral communities.

Thermal tolerance traits of individual corals are widely distributed across the Great Barrier Reef.

Adaptation of reef-building corals to global warming depends upon standing heritable variation in tolerance traits upon which selection can act. Yet limited knowledge exists on heat-tolerance variation among conspecific individuals separated by metres to hundreds of kilometres. Here, we performed standardized acute heat-stress assays to quantify the thermal tolerance traits of 709 colonies of Acropora spathulata from 13 reefs spanning 1060 km (9.5° latitude) of the Great Barrier Reef. Thermal thresholds for photochemical efficiency and chlorophyll retention varied considerably among individual colonies both among reefs (approximately 6°C) and within reefs (approximately 3°C). Although tolerance rankings of colonies varied between traits, the most heat-tolerant corals (i.e. top 25% of each trait) were found at virtually all reefs, indicating widespread phenotypic variation. Reef-scale environmental predictors explained 12-62% of trait variation. Corals exposed to high thermal averages and recent thermal stress exhibited the greatest photochemical performance, probably reflecting local adaptation and stress pre-acclimatization, and the lowest chlorophyll retention suggesting stress pre-sensitization. Importantly, heat tolerance relative to local summer temperatures was the greatest on higher latitude reefs suggestive of higher adaptive potential. These results can be used to identify naturally tolerant coral populations and individuals for conservation and restoration applications.

Symbiodiniaceae diversity varies by host and environment across thermally distinct reefs.

Endosymbiotic dinoflagellates (Symbiodiniaceae) influence coral thermal tolerance at both local and regional scales. In isolation, the effects of host genetics, environment, and thermal disturbances on symbiont communities are well understood, yet their combined effects remain poorly resolved. Here, we investigate Symbiodiniaceae across 1300 km in Australia's Coral Sea Marine Park to disentangle these interactive effects. We identified Symbiodiniaceae to species-level resolution for three coral species (Acropora cf humilis, Pocillopora verrucosa, and Pocillopora meandrina) by sequencing two genetic markers of the symbiont (ITS2 and psbAncr), paired with genotype-by-sequencing of the coral host (DArT-seq). Our samples predominantly returned sequences from the genus Cladocopium, where Acropora cf humilis affiliated with C3k, Pocillopora verrucosa with C. pacificum, and Pocillopora meandrina with C. latusorum. Multivariate analyses revealed that Acropora symbionts were driven strongly by local environment and thermal disturbances. In contrast, Pocillopora symbiont communities were both partitioned 2.5-fold more by host genetic structure than by environmental structure. Among the two Pocillopora species, the effects of environment and host genetics explained four times more variation in symbionts for P. meandrina than P. verrucosa. The concurrent bleaching event in 2020 had variable impacts on symbiont communities, consistent with patterns in P. verrucosa and A. cf humilis, but not P. meandrina. Our findings demonstrate how symbiont macroscale community structure responses to environmental gradients depend on host species and their respective population structure. Integrating host, symbiont, and environmental data will help forecast the adaptive potential of corals and their symbionts amidst a rapidly changing environment.

Host diet drives gut microbiome convergence between coral reef fishes and mammals.

Animal gut microbiomes are critical to host physiology and fitness. The gut microbiomes of fishes-the most abundant and diverse vertebrate clade-have received little attention relative to other clades. Coral reef fishes, in particular, make up a wide range of evolutionary histories and feeding ecologies that are likely associated with gut microbiome diversity. The repeated evolution of herbivory in fishes and mammals also allows us to examine microbiome similarity in relationship to diet across the entire vertebrate tree of life. Here, we generate a large coral reef fish gut microbiome dataset (n = 499 samples, 19 species) and combine it with a diverse aggregation of public microbiome data (n = 447) to show that host diet drives significant convergence between coral reef fish and mammalian gut microbiomes. We demonstrate that this similarity is largely driven by carnivory and herbivory and that herbivorous and carnivorous hosts exhibit distinct microbial compositions across fish and mammals. We also show that fish and mammal gut microbiomes share prominent microbial taxa, including Ruminoccocus spp. and Akkermansia spp., and predicted metabolic pathways. Despite the major evolutionary and ecological differences between fishes and mammals, our results reveal that their gut microbiomes undergo similar dietary selective pressures. Thus, diet, in addition to phylosymbiosis must be considered even when comparing the gut microbiomes of distantly related hosts.

Severe hurricanes increase recruitment and gene flow in the clonal sponge Aplysina cauliformis.

Upright branching sponges, such as Aplysina cauliformis, provide critical three-dimensional habitat for other organisms and assist in stabilizing coral reef substrata, but are highly susceptible to breakage during storms. Breakage can increase sponge fragmentation, contributing to population clonality and inbreeding. Conversely, storms could provide opportunities for new genotypes to enter populations via larval recruitment, resulting in greater genetic diversity in locations with frequent storms. The unprecedented occurrence of two Category 5 hurricanes in close succession during 2017 in the U.S. Virgin Islands (USVI) provided a unique opportunity to evaluate whether recolonization of newly available substrata on coral reefs was due to local (e.g. re-growth of remnants, fragmentation, larval recruitment) or remote (e.g. larval transport and immigration) sponge genotypes. We sampled A. cauliformis adults and juveniles from four reefs around St. Thomas and two in St. Croix (USVI). Using a 2bRAD protocol, all samples were genotyped for single-nucleotide polymorphisms (SNPs). Results showed that these major storm events favoured sponge larval recruitment but did not increase the genetic diversity of A. cauliformis populations. Recolonization of substratum post-storms via clonality was lower (15%) than expected and instead was mainly due to sexual reproduction (85%) via local larval recruitment. Storms did enhance gene flow among and within reef sites located south of St. Thomas and north of St. Croix. Therefore, populations of clonal marine species with low pelagic dispersion, such as A. cauliformis, may benefit from increased frequency and magnitude of hurricanes for the maintenance of genetic diversity and to combat inbreeding, enhancing the resilience of Caribbean sponge communities to extreme storm events.

Regional-scale disturbances drive long-term decline of inshore coral reef fish assemblages in the Great Barrier Reef Marine Park.

Anthropogenic pressure is increasing the variety and frequency of environmental disturbance events, limiting recovery and leading to long-term declines in wild plant and animal populations. Coral reefs and associated fish assemblages are inherently dynamic due to their susceptibility to a host of disturbances, but regional-scale nuances in the drivers of long-term change frequently remain poorly resolved. Here, we examine the effects of multiple potential drivers of change in coral reef fish assemblages across 4 inshore regions of the Great Barrier Reef Marine Park (GBRMP), Australia, over 12-14 years (2007-2021). Each region had a unique disturbance history, in conjunction with long-term changes in physical and habitat variables. Phases of recovery were apparent in the years between disturbance events at all locations, but these were not long enough to prevent substantial declines in reef fish density (by 33%-72%) and species richness (by 41%-75%) throughout the study period. The main drivers of change in fish assemblages varied among regions; however, the most rapid changes followed cyclone and flood events. Limited recovery periods resulted in temporal shifts in fish species composition from typically coral-associated to algae-associated. Most trophic groups declined in density except farmers, grazers, omnivores and parrotfish. No-take marine reserves (NTMRs) had small and inconsistent effects on total fish assemblages, but delivered benefits for fishery-targeted piscivores. Our findings suggest that coral reef responses to local stressors and cumulative escalating climate change impacts are highly variable at regional scales, and that small NTMRs are unlikely to mitigate the impacts of increasingly frequent climatic disturbances. Nearshore coral reefs worldwide are high-value habitats that are either already degraded or vulnerable to degradation and the loss of important fish groups. Global efforts to reduce greenhouse gas emissions must be coupled with effective local management that can support the functioning and adaptive capacity of coral reefs.

Coral reef protection is fundamental to human rights.

The intensifying loss of coral reefs from global climate change and local stressors has seen international commitments targeted at conservation and repair, for example the Kunming-Montreal Global Biodiversity Framework. Fulfilling these targets requires decisions to be made on where, when, and how to act, ultimately dictating where limited resources will be deployed. Every choice on action or inaction toward our ocean has direct and indivisible consequences not only for the health of marine ecosystems but also for the health of humans, particularly those who directly depend on marine habitats, both culturally and economically. The well-being of the environment, humans, and animals is interlinked, co-dependent, and even co-produced, as has already been acknowledged by One Health approaches, which endorse a cross- and trans-disciplinary view to health. Coral reefs epitomie how tightly intertwined ecosystem health and the fate of the human and nonhuman communities that depend on them are. A field that thus far remains poorly considered is a human rights-based approach to coral reef protection. A human rights-based approach implements human rights obligations, including the recently affirmed right to a clean, healthy, and sustainable environment, while embedding principles of accountability, nondiscrimination, participation, and empowerment for local and Indigenous communities that ensure effectiveness and meaningful stakeholder engagement. Tying the protection of coral reef ecosystems to human rights emphasises the importance of healthy ecosystems to human well-being and thus the inevitable connection between nonhuman and human life. The general failure to consider coral reef protection through a human rights-based approach is a missed opportunity to expedite reef protection while simultaneously advancing climate justice for both humans and nonhumans.

Impacts of marine heatwaves in coastal ecosystems depend on local environmental conditions.

Marine heatwaves (MHWs), increasing in duration and intensity because of climate change, are now a major threat to marine life and can have lasting effects on the structure and function of ecosystems. However, the responses of marine taxa and ecosystems to MHWs can be highly variable, making predicting and interpreting biological outcomes a challenge. Here, we review how biological responses to MHWs, from individuals to ecosystems, are mediated by fine-scale spatial variability in the coastal marine environment (hereafter, local gradients). Viewing observed responses through a lens of ecological theory, we present a simple framework of three 'resilience processes' (RPs) by which local gradients can influence the responses of marine taxa to MHWs. Local gradients (1) influence the amount of stress directly experienced by individuals, (2) facilitate local adaptation and acclimatization of individuals and populations, and (3) shape community composition which then influences responses to MHWs. We then synthesize known examples of fine-scale gradients that have affected responses of benthic foundation species to MHWs, including kelp forests, coral reefs, and seagrass meadows and link these varying responses to the RPs. We present a series of case studies from various marine ecosystems to illustrate the differential impacts of MHWs mediated by gradients in both temperature and other co-occurring drivers. In many cases, these gradients had large effect sizes with several examples of local gradients causing a 10-fold difference in impacts or more (e.g., survival, coverage). This review highlights the need for high-resolution environmental data to accurately predict and manage the consequences of MHWs in the context of ongoing climate change. While current tools may capture some of these gradients already, we advocate for enhanced monitoring and finer scale integration of local environmental heterogeneity into climate models. This will be essential for developing effective conservation strategies and mitigating future marine biodiversity loss.

Changing disturbance regimes, material legacies, and stabilizing feedbacks: Dead coral skeletons impair key recovery processes following coral bleaching.

Ecosystem responses to disturbance depend on the nature of the perturbation and the ecological legacies left behind, making it critical to understand how climate-driven changes in disturbance regimes modify resilience properties of ecosystems. For coral reefs, recent increases in severe marine heat waves now co-occur with powerful storms, the historic agent of disturbance. While storms kill coral and remove their skeletons, heat waves bleach and kill corals but leave their skeletons intact. Here, we explored how the material legacy of dead coral skeletons modifies two key ecological processes that underpin coral reef resilience: the ability of herbivores to control macroalgae (spatial competitors of corals), and the replenishment of new coral colonies. Our findings, grounded by a major bleaching event at our long-term study locale, revealed that the presence of structurally complex dead skeletons reduced grazing on turf algae by ~80%. For macroalgae, browsing was reduced by >40% on less preferred (unpalatable) taxa, but only by ~10% on more preferred taxa. This enabled unpalatable macroalgae to reach ~45% cover in 2 years. By contrast, herbivores prevented macroalgae from becoming established on adjacent reefs that lacked skeletons. Manipulation of unpalatable macroalgae revealed that the cover reached after 1 year (~20%) reduced recruitment of corals by 50%. The effect of skeletons on juvenile coral growth was contingent on the timing of settlement relative to the disturbance. If corals settled directly after bleaching (before macroalgae colonized), dead skeletons enhanced colony growth by 34%, but this benefit was lost if corals colonized dead skeletons a year after the disturbance once macroalgae had proliferated. These findings underscore how a material legacy from a changing disturbance regime can alter ecosystem resilience properties by disrupting key trophic and competitive interactions that shape post-disturbance community dynamics.

Patterns of spawning and settlement of reef fishes as strategic responses to post-settlement competition.

Settlement is a critical transition in the life history of reef fish, and the timing of this event can have a strong effect on fitness. Key factors that influence settlement timing are predictable lunar cyclic variation in tidal currents, moonlight, and nocturnal predation risk as larvae transition from pelagic to benthic environments. However, populations typically display wide variation in the arrival of settlers over the lunar cycle. This variation is often hypothesized to result from unpredictable conditions in the pelagic environment and bet-hedging by spawning adults. Here, we consider the hypothesis that the timing of spawning and settlement is a strategic response to post-settlement competition. We use a game theoretic model to predict spawning and settlement distributions when fish face a tradeoff between minimizing density-independent predation risk while crossing the reef crest vs. avoiding high competitor density on settlement habitat. In general, we expect competition to spread spawning over time such that settlement is distributed around the lunar phase with the lowest predation risk, similar to an ideal free distribution in which competition spreads competitors across space. We examine the effects of overcompensating density dependence, age-dependent competition, and competition among daily settler cohorts. Our model predicts that even in the absence of stochastic variation in the larval environment, competition can result in qualitative divergence between spawning and settlement distributions. Furthermore, we show that if competitive strength increases with settler age, competition results in covariation between settler age and settlement date, with older larvae settling when predation risk is minimal. We predict that competition between daily cohorts delays peak settlement, with priority effects potentially selecting for a multimodal settlement distribution.

Multi-Factor Coral Disease Risk: A new product for early warning and management.

Ecological forecasts are becoming increasingly valuable tools for conservation and management. However, there are few examples of near-real-time forecasting systems that account for the wide range of ecological complexities. We developed a new coral disease ecological forecasting system that explores a suite of ecological relationships and their uncertainty and investigates how forecast skill changes with shorter lead times. The Multi-Factor Coral Disease Risk product introduced here uses a combination of ecological and marine environmental conditions to predict the risk of white syndromes and growth anomalies across reefs in the central and western Pacific and along the east coast of Australia and is available through the US National Oceanic and Atmospheric Administration Coral Reef Watch program. This product produces weekly forecasts for a moving window of 6 months at a resolution of ~5 km based on quantile regression forests. The forecasts show superior skill at predicting disease risk on withheld survey data from 2012 to 2020 compared with predecessor forecast systems, with the biggest improvements shown for predicting disease risk at mid- to high-disease levels. Most of the prediction uncertainty arises from model uncertainty, so prediction accuracy and precision do not improve substantially with shorter lead times. This result arises because many predictor variables cannot be accurately forecasted, which is a common challenge across ecosystems. Weekly forecasts and scenarios can be explored through an online decision support tool and data explorer, co-developed with end-user groups to improve use and understanding of ecological forecasts. The models provide near-real-time disease risk assessments and allow users to refine predictions and assess intervention scenarios. This work advances the field of ecological forecasting with real-world complexities and, in doing so, better supports near-term decision making for coral reef ecosystem managers and stakeholders. Secondarily, we identify clear needs and provide recommendations to further enhance our ability to forecast coral disease risk.

The Abrolhos Nominally Herbivorous Coral Reef Fish Acanthurus chirurgus, Kyphosus sp., Scarus trispinosus, and Sparisoma axillare Have Similarities in Feeding But Species-Specific Microbiomes.

Coral reefs rely heavily on reef fish for their health, yet overfishing has resulted in their decline, leading to an increase in fast-growing algae and changes in reef ecosystems, a phenomenon described as the phase-shift. A clearer understanding of the intricate interplay between herbivorous, their food, and their gut microbiomes could enhance reef health. This study examines the gut microbiome and isotopic markers (δ13C and δ15N) of four key nominally herbivorous reef fish species (Acanthurus chirurgus, Kyphosus sp., Scarus trispinosus, and Sparisoma axillare) in the Southwestern Atlantic's Abrolhos Reef systems. Approximately 16.8 million 16S rRNA sequences were produced for the four fish species, with an average of 317,047 ± 57,007 per species. Bacteria such as Proteobacteria, Firmicutes, and Cyanobacteria were prevalent in their microbiomes. These fish show unique microbiomes that result from co-diversification, diet, and restricted movement. Coral-associated bacteria (Endozoicomonas, Rhizobia, and Ruegeria) were found in abundance in the gut contents of the parrotfish species Sc. trispinosus and Sp. axillare. These parrotfishes could aid coral health by disseminating such beneficial bacteria across the reef. Meanwhile, Kyphosus sp. predominantly had Pirellulaceae and Rhodobacteraceae. Four fish species had a diet composed of turf components (filamentous Cyanobacteria) and brown algae (Dictyopteris). They also had similar isotopic niches, suggesting they shared food sources. A significant difference was observed between the isotopic signature of fish muscular gut tissue and gut contents, pointing to the role that host genetics and gut microbes play in differentiating fish tissues.

Diversification of refugia types needed to secure the future of coral reefs subject to climate change.

Identifying locations of refugia from the thermal stresses of climate change for coral reefs and better managing them is one of the key recommendations for climate change adaptation. We review and summarize approximately 30 years of applied research focused on identifying climate refugia to prioritize the conservation actions for coral reefs under rapid climate change. We found that currently proposed climate refugia and the locations predicted to avoid future coral losses are highly reliant on  excess heat metrics, such as degree heating weeks. However, many existing alternative environmental, ecological, and life-history variables could be used to identify other types of refugia that lead to the desired diversified portfolio for coral reef conservation. To improve conservation priorities for coral reefs, there is a need to evaluate and validate the predictions of climate refugia with long-term field data on coral abundance, diversity, and functioning. There is also the need to identify and safeguard locations displaying resistance toprolonged exposure to heat waves and the ability to recover quickly after thermal exposure. We recommend using more metrics to identify a portfolio of potential refugia sites for coral reefs that can avoid, resist, and recover from exposure to high ocean temperatures and the consequences of climate change, thereby shifting past efforts focused on avoidance to a diversified risk-spreading portfolio that can be used to improve strategic coral reef conservation in a rapidly warming climate.

Diversificación de los tipos de refugio necesarios para asegurar el futuro de los arrecifes de coral sujetos al cambio climático Resumen Una de las principales recomendaciones para la adaptación al cambio climático es identificar los refugios de los arrecifes de coral frente al estrés térmico del cambio climático y mejorar su gestión. Revisamos y resumimos ∼30 años de investigación aplicada centrada en la identificación de refugios climáticos para priorizar las acciones de conservación de los arrecifes de coral bajo un rápido cambio climático. Descubrimos que los refugios climáticos propuestos actualmente y las ubicaciones que pueden evitarlos dependen en gran medida de métricas de exceso de calor, como las semanas de calentamiento en grados (SCG). Sin embargo, existen muchas variables alternativas de historia vital, ambientales y ecológicas que podrían utilizarse para identificar otros tipos de refugios que resulten en el acervo diversificado que se desea para la conservación de los arrecifes de coral. Para mejorar las prioridades de conservación de los arrecifes de coral, es necesario evaluar y validar las predicciones sobre refugios climáticos con datos de campo a largo plazo sobre abundancia, diversidad y funcionamiento de los corales. También es necesario identificar y salvaguardar lugares que muestren resistencia a la exposición climática prolongada a olas de calor y la capacidad de recuperarse rápidamente tras la exposición térmica. Recomendamos utilizar más métricas para identificar un acervo de posibles lugares de refugio para los arrecifes de coral que puedan evitar, resistir y recuperarse de la exposición a las altas temperaturas oceánicas y las consecuencias del cambio climático, para así desplazar los esfuerzos pasados centrados en la evitación hacia un acervo diversificado de riesgos que pueda utilizarse para mejorar la conservación estratégica de los arrecifes de coral en un clima que se calienta rápidamente.

Sunscreens Part 2: Regulation and Safety.

The second part of this CME article discusses sunscreen regulation and safety considerations for humans and the environment. First, we provide an overview of the history of the United States Food and Drug Administration's regulation of sunscreen. Recent Food and Drug Administration studies clearly demonstrate that organic ultraviolet filters are systemically absorbed during routine sunscreen use, but to date there is no evidence of associated negative health effects. We also review the current evidence of sunscreen's association with vitamin D levels and frontal fibrosing alopecia, and recent concerns regarding benzene contamination. Finally, we review the possible environmental effects of ultraviolet filters, particularly coral bleaching. While climate change has been shown to be the primary driver of coral bleaching, laboratory-based studies suggest that organic ultraviolet filters represent an additional contributing factor, which led several localities to ban certain organic filters.

Assessing spatiotemporal change in coral reef social-ecological systems.

Coral reef resilience is eroding at multiple spatial scales globally, with broad implications for coastal communities, and is thus a critical challenge for managing marine social-ecological systems (SESs). Many researchers believe that external stressors will cause key coral reefs to die by the end of the 21st century, virtually eliminating essential ecological and societal benefits. Here, we propose the use of resilience-based approaches to understand the dynamics of coral reef SESs and subsequent drivers of coral reef decline. Previous research has demonstrated the effectiveness of these methods, not only for tracking environmental change, but also for providing warning in advance of transitions, possibly allowing time for management interventions. The flexibility and utility of these methods make them ideal for assessing complex systems; however, they have not been used to study aquatic ecosystem dynamics at the global scale. Here, we evaluate these methods for examining spatiotemporal change in coral reef SESs across the global seascape and assess the subsequent impacts on coral reef resilience. We found that while univariate indicators failed to provide clear signals, multivariate resilience-based approaches effectively captured coral reef SES dynamics, unveiling distinctive patterns of variation throughout the global coral reef seascape. Additionally, our findings highlight global spatiotemporal variation, indicating patterns of degraded resilience. This degradation was reflected regionally, particularly in the Pacific Ocean and Indian Ocean SESs. These results underscore the utility of resilience-based approaches in assessing environmental change in SESs, detecting spatiotemporal variation at the global and regional scales, and facilitating more effective monitoring and management of coral reef SESs.