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BackgroundVenous malformation (VM) consists of a network of ectatic anomalous thin-walled venous channels. A role for an activating TIE2 mutation in the development of the dilated luminal vessels in VM, and its proposed involvement of embryonic stem cells (ESCs), led us to investigate the expression of ESC markers in subcutaneous VM (SCVM) and intramuscular VM (IMVM).MethodsFormalin-fixed paraffin-embedded sections of SCVM from seven patients and IMVM samples from seven patients were analyzed for the expression of Nanog, pSTAT3, OCT4, SOX2, SALL4, and CD44, using 3,3′-diaminobenzidine (DAB) immunohistochemical (IHC) staining. All these samples did not express lymphatic marker D2-40. NanoString mRNA analysis and RT-PCR were performed on snap-frozen samples of SCVM (n = 3) and IMVM (n = 3) from the respective original cohorts of patients included in DAB IHC staining. To confirm co-expression of two proteins, immunofluorescent (IF) IHC staining on two representative samples of IMVM and SCVM samples from the original cohorts of patients included for DAB IHC staining was performed.ResultsDAB IHC staining demonstrated expression of all of the above ESC markers in both SCVM and IMVM samples. IF IHC staining showed that these markers were localized to the endothelium within these lesions and that Nanog, pSTAT3, SOX2, and CD44 were also expressed by cells outside of the endothelium. NanoString mRNA analysis confirmed transcription activation of pSTAT3, OCT4, and CD44. RT-qPCR confirmed transcription activation of Nanog, SOX2, and SALL4.ConclusionOur findings support the presence of two ESC-like subpopulations, one within and one outside of the endothelium, of both SCVM and IMVM. Given that the endothelial ESC-like subpopulation expresses the more primitive marker, OCT4, it is exciting to speculate that they give rise to the non-endothelial subpopulation.

Abstract Coral bleaching, a consequence of stressed symbiotic relationships between corals and algae, has escalated due to intensified heat stress events driven by climate change. Despite global efforts, current early warning systems lack local precision. Our study, spanning 2015–2017 in the Mesoamerican Reef, revealed prevalent intermediate bleaching, peaking in 2017. By scrutinizing 23 stress exposure and sensitivity metrics, we accurately predicted 75% of bleaching severity variation. Notably, distinct thermal patterns—particularly the climatological seasonal warming rate and various heat stress metrics—emerged as better predictors compared to conventional indices (such as Degree Heating Weeks). Surprisingly, deeper reefs with diverse coral communities showed heightened vulnerability. This study presents a framework for coral reef bleaching vulnerability assessment, leveraging accessible data (including historical and real-time sea surface temperature, habitat variables, and species composition). Its operational potential lies in seamless integration with existing monitoring systems, offering crucial insights for conservation and management.

Abstract The biodiversity in coral reef ecosystems is distributed heterogeneously across spatial and temporal scales, being commonly influenced by biogeographic factors, habitat area and disturbance frequency. A potential association between gradients of usable energy and biodiversity patterns has received little empirical support in these ecosystems. Here, we analyzed the productivity and biodiversity variation over depth gradients in symbiotic coral communities, whose members rely on the energy translocated by photosynthetic algal symbionts (zooxanthellae). Using a mechanistic model we explored the association between the depth-dependent variation in photosynthetic usable energy to corals and gradients of species diversity, comparing reefs with contrasting water clarity and biodiversity patterns across global hotspots of marine biodiversity. The productivity-biodiversity model explained between 64 and 95% of the depth-related variation in coral species richness, indicating that much of the variation in species richness with depth is driven by changes in the fractional contribution of photosynthetically fixed energy by the zooxanthellae. These results suggest a fundamental role of solar energy availability and photosynthetic production in explaining global-scale patterns of coral biodiversity and community structure along depth gradients. Accordingly, the maintenance of water optical quality in coral reefs is fundamental to protect coral biodiversity and prevent reef degradation.

A combination of experimental and literature analyses indicate that heat stress is a greater threat for coral calcification than ocean acidification, stressing the need for further investigation on key regulatory processes.

Abstract In this study, we explore how the Caribbean coral Orbicella faveolata recovers after bleaching, using fragments from 13 coral colonies exposed to heat stress (32 °C) for ten days. Biological parameters and coral optical properties were monitored during and after the stress. Increases in both, the excitation pressure over photosystem II (Qm) and pigment specific absorption (a*Chla ) were observed in the stressed corals, associated with reductions in light absorption at the chlorophyll a red peak (D e675 ) and symbiont population density. All coral fragments exposed to heat stress bleached but a fraction of the stressed corals recovered after removing the stress, as indicated by the reductions in Q m and increases in D e675 and the symbiont population observed. This subsample of the experimentally bleached corals also showed blooms of the endolithic algae Ostreobium spp. underneath the tissue. Using a numerical model, we quantified the amount of incident light reflected by the coral, and absorbed by the different pigmented components: symbionts, host-tissue and Ostreobium spp. Our study supports the key contribution of Ostreobium spp. blooms near the skeletal surface, to coral recovery after bleaching by reducing skeleton reflectance. Endolithic blooms can thus significantly alleviate the high light stress that affects the remaining symbionts during the stress or when the coral has achieved the bleached phenotype.

The upregulation of animal chromoproteins (CPs) during thermal stress produces “colorful” bleached corals that facilitate coral recovery after bleaching. In situ measurements indicate that animal CPs present in coral tissues reduce the elevated internal light environment of the remaining symbionts in bleached or low-pigmented stressed corals. However, there is still a lack of understanding regarding the extent to which animal CPs contribute to modifying the internal light environment of the symbionts in hospite. In this study, we evaluate the effect of three animal CPs on the optical properties of the coral tissue and their internal light environment using a numerical model. The model allows estimations of the absorbance spectra of corals as a function of changes in symbiont and animal pigmentation, as well as descriptions of the light environment in hospite of the symbionts. These descriptions were derived from the quantification of the contribution of each pigment component to light absorption, together with the contribution of the coral skeleton’s reflectance. Simulations indicate that animal CPs upregulation modifies the spectral distribution and the intensity of the internal light field. Animal CPs can reduce up to 11% of the light intensity in hospite when present individually, and up to 24% when present in combination. Such reduction may play a critical role in preventing the full development of the bleached phenotype when irradiance rises to excessive levels at low coral pigmentation, facilitating coral recovery and symbiont tissue re-colonization after bleaching. Accordingly, coral’s CPs components need to also be considered when selecting coral species for future restoration efforts.

As corals struggle to survive under climate change, it is crucial to know whether they can withstand increasing seawater temperatures. Using a controlled thermal stress experiment across three divergent coral holobionts, this study examines metatranscriptomic responses to heat stress corresponding to the coral host, photosymbionts and associated microbiota.

Mass coral bleaching compromises the long-term persistence of coral reefs, yet our current understanding of the different cellular mechanisms leading to the development of a bleached coral is still limited. In this perspective, we mapped the cascade of cellular events and physiological responses of symbiotic corals triggered by thermal stress. Based on existing knowledge, we created an integrated model that describes phenotypic changes induced by sensing mechanisms. Cellular responses are mapped in the context of reactive oxygen species (ROS) production in the algal symbiont chloroplast, followed by signaling to the nucleus and subsequent “leak” to the coral host cell. The starting point is set by ROS production and signaling, which is a day-to-day mechanism by which symbiotic corals maintain homeostasis and acclimate to environmental variation. As stress and acclimation are intimately linked, our model maps coral responses from the initial stimulus in the chloroplast to the complex cascade of events leading to seasonal phenotypic changes (i.e., seasonal acclimation), and if stress progresses, to the downstream coral bleached phenotype (i.e., when the coral’s capacity to acclimate is overwhelmed by heat stress). Placing acclimation, heat stress and bleaching responses in a common ground is a critical step to reduce the source of uncertainty in understanding the coral response to climate change, fundamental for the development of predictive climate models.

The distinction between shallow coral reefs and mesophotic coral ecosystems (MCEs) has not been fully clarified yet. The original definition of MCEs, by depths of 30–150 m, fixes their bathymetrical limits and fails to accommodate environmental and biological variation. Recent studies have indicated that water transparency and light availability may explain why MCEs do not occur at fixed depths but vary among localities. This study aimed to evaluate the presence and distribution of MCEs, along the central coast of Oaxaca, through optical depths and the associated benthic community. Using MODIS-Aqua satellite data (Kd490), we estimated the mesophotic optical depths monthly (z10%, z1%, z0.1%), over the last four years. In addition, to characterize benthic community structure, we conducted underwater photo quadrat surveys at two locations on the southern Mexican Pacific coast from 10 to 55 m depth. Significant differences between depths and locations were found in benthic communities. Furthermore, the lower distribution of photosynthetic taxa was different between the two locations but indicative to the z10% and z1% in both cases. Those differences were associated with the upwelling season, which reduces, drastically and differentially, the light availability for benthic communities between the two locations and limits the development of MCEs on the central coast of Oaxaca.

The seagrass Thalassia testudinum is the dominant habitat-builder in coastal reef lagoons of the Caribbean, and provides vital ecosystem services including coastal protection and carbon storage. We used a remote sensing methodology to map T. testudinum canopies over 400 km of coastline of the eastern Yucatán Peninsula, comparing the depth distribution of canopy density, in terms of leaf area index (LAI), to a previously established ecological model of depth and LAI for this species in oligotrophic conditions. The full archive of Sentinel-2 imagery from 2016 to 2020 was applied in an automated model inversion method to simultaneously estimate depth and LAI, covering ∼900 km2 of lagoon with approximately 800 images. Data redundancy allowed for statistical tests of change detection. Achieved accuracy was sufficient for the objectives: LAI estimates compared to field data had mean absolute error of 0.59, systematic error of 0.04 and r2 > 0.67 over a range of 0–5. Bathymetry compared to 46,000 ICESat-2 data points had a mean absolute error of 1 m, systematic error less than 0.5 m, and r2 > 0.88 over a range of 0–15 m. The estimated total area of seagrass canopy was consistent with previously published estimates of ∼580 km2, but dense canopies (LAI > 3), which are the primary contributors to below-ground carbon storage, comprise only ∼40 km2. Within the year-to-year variation there was no change in overall seagrass abundance 2017–2020, but localised statistically significant (p < 0.01) patches of canopy extension and retraction occurred. 2018 and 2019 were affected by beaching of pelagic Sargassum and dispersion as organic matter into the lagoon. The multi-year analysis enabled excluding this influence and provided an estimate of its extent along the coast. Finally, the distribution of LAI with depth was consistent with the ecological model and showed a gradient from north to south which mirrored a well-established gradient in anthropogenic pressure due to touristic development. Denser canopies were more abundant in developed areas, the expected growth response to nutrient enrichment. This increase in canopy density may be a useful early bio-indicator of environmental eutrophication, detectable by remote sensing before habitat deterioration is observed.

Abstract The potential effects of seasonal acclimatization on coral sensitivity to heat-stress, has received limited attention despite differing bleaching thresholds for summer and winter. In this study, we examined the response of two contrasting phenotypes, termed winter and summer, of four Caribbean reef corals to similar light and heat-stress levels. The four species investigated were categorized into two groups: species with the ability to harbour large number of symbionts, Orbicella annularis and O. faveolata, and species with reduced symbiont density (Montastraea cavernosa and Pseudodiploria strigosa). The first group showed higher capacity to enhance photosynthetic rates per area (Pmax), while Pmax enhancement in the second group was more dependent on Symbiodinium performance (Psym). In summer all four species presented higher productivity, but also higher sensitivity to lose coral photosynthesis under heat-stress. In contrast, corals in winter exhibit symbionts with higher capacity to photoacclimate to the increased levels of light-stress elicited by heat-stress. Overall, our study supports the importance of the acclimatory coral condition in addition to the previous thermal history, to determine the severity of the impact of heat-stress on coral physiology, but also the dependence of this response on the particular structural and functional traits of the species.

The capability for mapping two species of seagrass, Thalassia testudinium and Syringodium filiforme, by remote sensing using a physics based model inversion method was investigated. The model was based on a three-dimensional canopy model combined with a model for the overlying water column. The model included uncertainty propagation based on variation in leaf reflectances, canopy structure, water column properties, and the air-water interface. The uncertainty propagation enabled both a-priori predictive sensitivity analysis of potential capability and the generation of per-pixel error bars when applied to imagery. A primary aim of the work was to compare the sensitivity analysis to results achieved in a practical application using airborne hyperspectral data, to gain insight on the validity of sensitivity analyses in general. Results showed that while the sensitivity analysis predicted a weak but positive discrimination capability for species, in a practical application the relevant spectral differences were extremely small compared to discrepancies in the radiometric alignment of the model with the imagery—even though this alignment was very good. Complex interactions between spectral matching and uncertainty propagation also introduced biases. Ability to discriminate LAI was good, and comparable to previously published methods using different approaches. The main limitation in this respect was spatial alignment with the imagery with in situ data, which was heterogeneous on scales of a few meters. The results provide insight on the limitations of physics based inversion methods and seagrass mapping in general. Complex models can degrade unpredictably when radiometric alignment of the model and imagery is not perfect and incorporating uncertainties can have non-intuitive impacts on method performance. Sensitivity analyses are upper bounds to practical capability, incorporating a term for potential systematic errors in radiometric alignment may be advisable. While T. testudinium and S. filiforme were too spectrally similar to be discriminated purely on spectral grounds, mapping of these, and other species may be achievable by exploiting co-incident factors based on ecological zonation.

Red coralline algae are a cosmopolitan group with the ability to precipitate CaCO3 within the walls of their vegetative cells. The resultant carbonate structure is key for explaining their ecological success, as it provides protection against herbivores and resistance to water motion. However, its potential contribution to enhance thallus light absorption efficiency through multiple light scattering on algal skeleton, similar to the effect documented for scleractinian corals, has not been yet investigated. Here, we initiate this analysis, characterizing thallus optical properties of three coralline species, which differed in pigment content and thallus mass area (TMA, gDW m−2). The three species, the rhodolith Neogoniolithon sp., the crustose coralline alga (CCA), Lithothamnion sp., and the articulated alga Amphiroa tribulus, represent the more distinctive coralline growth-forms and are able to colonize contrasting light environments in Caribbean coral reefs. The thicker thalli of the rhodoliths were the most efficient light collectors, as evidenced by their higher pigment absorption efficiency (a*Chla; m2 mgChla−1) and photosynthetic rates per unit area. This could explain rhodolith success in oligotrophic, highly illuminated reef environments. In contrast, the thinner thalli of the CCA, a low-light specialist, showed the highest metabolic rates normalized to mass and the highest light absorption efficiencies per unit mass (a*M; m2 gdw−1). Therefore, the ecological success of the CCA in cryptic habitats within the reef cannot be explained only by its low-light physiology, but also by its capacity to reduce the structural costs of their thalli, and thus of its new growth. Lastly, the ecological success of Amphiroa tribulus, which displayed intermediate values for the efficiency of light absorption, metabolic rates and TMA, was explained by its ability to construct the largest light collectors (algal canopies) thanks to the presence of flexible, non-calcified segments (genicula). This ability enables enhanced photosynthetic and carbonate production at the organism/canopy level. The resulting fragile canopy survives best within the protection provided by colonies of the lettuce coral Agaricia agaricites. In conclusion, our study demonstrates the utility of optical traits as powerful tools to investigate differences in the competitive abilities, abundances and niche distribution among algal species and/or growth-forms.

In order to understand the contribution of pigmented coral tissues to the extraordinary optical properties of the coral-symbiont-skeleton unit, we analyzed the associations between structural and optical traits for four coral species, which broadly differ in skeleton morphology, tissue thickness and in the variation of coral pigmentation, symbiont content, Symbiodinium dominant type and Symbiodinium cell pigmentation (Ci). Significant differences among species were found for the maximum capacity of light absorption (Amax) and for the minimum pigmentation required to reach that maximum. The meandroid morphotype represented by Pseudodiploria strigosa showed a slightly lower Amax than the other three chalice-type species, while the thickest species, Montastraea cavernosa, required 2–3.5 times higher pigmentation to reach Amax. In contrast, Orbicella faveolata and Orbicella annularis, which were able to harbor high number of symbionts and achieve the highest photosynthetic rates per area, showed the largest abilities for light collection at decreasing symbiont densities, leading to a more fragile photophysiological condition under light and heat-stress. Holobiont photosynthesis was more dependent on Symbiodinium performance in the less populated organisms. At reduced pigmentation, we observed a similar non-linear increase in holobiont light absorption efficiency (a*Chla), which was differentially modulated by reductions in the number of symbionts and Symbiodinium Ci. For similar pigmentation, larger symbiont losses relative to Ci declines resulted in smaller increases in a*Chla. Two additional optical traits were used to characterize light absorption efficiency of Symbiodinium (a*sym) and coral host (a*M). Optimization of a*sym was well represented by P. strigosa, whereas a*M was better optimized by O. annularis. The species with the largest symbiont content, O. faveolata, and with the thickest tissues, M. cavernosa, represented, respectively, less efficient solutions for both coral traits. Our comparison demonstrates the utility of optical traits to characterize inter-specific differences in coral acclimatization and performance. Furthermore, holobiont light absorption efficiency (a*Chla) appeared as a better proxy for the “bleached phenotype” than simple reductions in coral color. The analysis of a putative coordinated variation in the number of symbionts and in Symbiodinium cell pigmentation deserves special attention to understand holobiont optimization of energy collection (a*Chla) and photosynthetic performance.

Coral reefs worldwide are affected by increasing dissolved inorganic carbon (DIC) and organic carbon (DOC) concentrations due to ocean acidification (OA) and coastal eutrophication. These two stressors can occur simultaneously, particularly in near-shore reef environments with increasing anthropogenic pressure. However, experimental studies on how elevated DIC and DOC interact are scarce and fundamental to understanding potential synergistic effects and foreseeing future changes in coral reef function. Using an open mesocosm experiment, the present study investigated the impact of elevated DIC (pHNBS: 8.2 and 7.8; pCO2: 377 and 1076 μatm) and DOC (added as 833 μmol L-1 of glucose) on calcification and photosynthesis rates of two common calcifying green algae, Halimeda incrassata and Udotea flabellum, in a shallow reef environment. Our results revealed that under elevated DIC, algal photosynthesis decreased similarly for both species, but calcification was more affected in H. incrassata, which also showed carbonate dissolution rates. Elevated DOC reduced photosynthesis and calcification rates in H. incrassata, while in U. flabellum photosynthesis was unaffected and thalus calcification was severely impaired. The combined treatment showed an antagonistic effect of elevated DIC and DOC on the photosynthesis and calcification rates of H. incrassata, and an additive effect in U. flabellum. We conclude that the dominant sand dweller H. incrassata is more negatively affected by both DIC and DOC enrichments, but that their impact could be mitigated when they occur simultaneously. In contrast, U. flabellum can be less affected in coastal eutrophic waters by elevated DIC, but its contribution to reef carbonate sediment production could be further reduced. Accordingly, while the capacity of environmental eutrophication to exacerbate the impact of OA on algal-derived carbonate sand production seems to be species-specific, significant reductions can be expected under future OA scenarios, with important consequences for beach erosion and coastal sediment dynamics.

The National Oceanic and Atmospheric Administration’s Coral Reef Watch program developed and operates several global satellite products to monitor bleaching-level heat stress. While these products have a proven ability to predict the onset of most mass coral bleaching events, they occasionally miss events; inaccurately predict the severity of some mass coral bleaching events; or report false alarms. These products are based solely on temperature and yet coral bleaching is known to result from both temperature and light stress. This study presents a novel methodology (still under development), which combines temperature and light into a single measure of stress to predict the onset and severity of mass coral bleaching. We describe here the biological basis of the Light Stress Damage (LSD) algorithm under development. Then by using empirical relationships derived in separate experiments conducted in mesocosm facilities in the Mexican Caribbean we parameterize the LSD algorithm and demonstrate that it is able to describe three past bleaching events from the Great Barrier Reef (GBR). For this limited example, the LSD algorithm was able to better predict differences in the severity of the three past GBR bleaching events, quantifying the contribution of light to reduce or exacerbate the impact of heat stress. The new Light Stress Damage algorithm we present here is potentially a significant step forward in the evolution of satellite-based bleaching products.

Reef managers cannot fight global warming through mitigation at local scale, but they can use information on thermal patterns to plan for reserve networks that maximize the probability of persistence of their reef system. Here we assess previous methods for the design of reserves for climate change and present a new approach to prioritize areas for conservation that leverages the most desirable properties of previous approaches. The new method moves the science of reserve design for climate change a step forwards by: (1) recognizing the role of seasonal acclimation in increasing the limits of environmental tolerance of corals and ameliorating the bleaching response; (2) using the best proxy for acclimatization currently available; (3) including information from several bleaching events, which frequency is likely to increase in the future; (4) assessing relevant variability at country scales, where most management plans are carried out. We demonstrate the method in Honduras, where a reassessment of the marine spatial plan is in progress.