Performance of Orbicella faveolata larval cohorts does not align with previously observed thermal tolerance of adult source populations.

Orbicella faveolata, commonly known as the mountainous star coral, is a dominant reef-building species in the Caribbean, but populations have suffered sharp declines since the 1980s due to repeated bleaching and disease-driven mortality. Prior research has shown that inshore adult O. faveolata populations in the Florida Keys are able to maintain high coral cover and recover from bleaching faster than their offshore counterparts. However, whether this origin-specific variation in thermal resistance is heritable remains unclear. To address this knowledge gap, we produced purebred and hybrid larval crosses from O. faveolata gametes collected at two distinct reefs in the Upper Florida Keys, a nearshore site (Cheeca Rocks, CR) and an offshore site (Horseshoe Reef, HR), in two different years (2019, 2021). We then subjected these aposymbiotic larvae to severe (36°C) and moderate (32°C) heat challenges to quantify their thermal tolerance. Contrary to our expectation based on patterns of adult thermal tolerance, HR purebred larvae survived better and exhibited gene expression profiles that were less driven by stress response under elevated temperature compared to purebred CR and hybrid larvae. One potential explanation could be the compromised reproductive output of CR adult colonies due to repeated summer bleaching events in 2018 and 2019, as gametes originating from CR in 2019 contained less storage lipids than those from HR. These findings provide an important counter-example to the current selective breeding paradigm, that more tolerant parents will yield more tolerant offspring, and highlight the importance of adopting a holistic approach when evaluating larval quality for conservation and restoration purposes.

Different disease inoculations cause common responses of the host immune system and prokaryotic component of the microbiome in Acropora palmata.

Reef-building corals contain a complex consortium of organisms, a holobiont, which responds dynamically to disease, making pathogen identification difficult. While coral transcriptomics and microbiome communities have previously been characterized, similarities and differences in their responses to different pathogenic sources has not yet been assessed. In this study, we inoculated four genets of the Caribbean branching coral Acropora palmata with a known coral pathogen (Serratia marcescens) and white band disease. We then characterized the coral's transcriptomic and prokaryotic microbiomes' (prokaryiome) responses to the disease inoculations, as well as how these responses were affected by a short-term heat stress prior to disease inoculation. We found strong commonality in both the transcriptomic and prokaryiomes responses, regardless of disease inoculation. Differences, however, were observed between inoculated corals that either remained healthy or developed active disease signs. Transcriptomic co-expression analysis identified that corals inoculated with disease increased gene expression of immune, wound healing, and fatty acid metabolic processes. Co-abundance analysis of the prokaryiome identified sets of both healthy-and-disease-state bacteria, while co-expression analysis of the prokaryiomes' inferred metagenomic function revealed infected corals' prokaryiomes shifted from free-living to biofilm states, as well as increasing metabolic processes. The short-term heat stress did not increase disease susceptibility for any of the four genets with any of the disease inoculations, and there was only a weak effect captured in the coral hosts' transcriptomic and prokaryiomes response. Genet identity, however, was a major driver of the transcriptomic variance, primarily due to differences in baseline immune gene expression. Despite genotypic differences in baseline gene expression, we have identified a common response for components of the coral holobiont to different disease inoculations. This work has identified genes and prokaryiome members that can be focused on for future coral disease work, specifically, putative disease diagnostic tools.

Coral persistence despite marginal conditions in the Port of Miami.

Coral cover has declined worldwide due to anthropogenic stressors that manifest on both global and local scales. Coral communities that exist in extreme conditions can provide information on how these stressors influence ecosystem structure, with implications for their persistence under future conditions. The Port of Miami is located within an urbanized environment, with active coastal development, as well as commercial shipping and recreational boating activity. Monitoring of sites throughout the Port since 2018 has revealed periodic extremes in temperature, seawater pH, and salinity, far in excess of what have been measured in most coral reef environments. Despite conditions that would kill many reef species, we have documented diverse coral communities growing on artificial substrates at these sites-reflecting remarkable tolerance to environmental stressors. Furthermore, many of the more prevalent species within these communities are now conspicuously absent or in low abundance on nearby reefs, owing to their susceptibility and exposure to stony coral tissue loss disease. Natural reef frameworks, however, are largely absent at the urban sites and while diverse fish communities are documented, it is unlikely that these communities provide the same goods and services as natural reef habitats. Regardless, the existence of these communities indicates unlikely persistence and highlights the potential for coexistence of threatened species in anthropogenic environments, provided that suitable stewardship strategies are in place.

Restoration and coral adaptation delay, but do not prevent, climate-driven reef framework erosion of an inshore site in the Florida Keys.

For reef framework to persist, calcium carbonate production by corals and other calcifiers needs to outpace loss due to physical, chemical, and biological erosion. This balance is both delicate and dynamic and is currently threatened by the effects of ocean warming and acidification. Although the protection and recovery of ecosystem functions are at the center of most restoration and conservation programs, decision makers are limited by the lack of predictive tools to forecast habitat persistence under different emission scenarios. To address this, we developed a modelling approach, based on carbonate budgets, that ties species-specific responses to site-specific global change using the latest generation of climate models projections (CMIP6). We applied this model to Cheeca Rocks, an outlier in the Florida Keys in terms of high coral cover, and explored the outcomes of restoration targets scheduled in the coming 20 years at this site by the Mission: Iconic Reefs restoration initiative. Additionally, we examined the potential effects of coral thermal adaptation by increasing the bleaching threshold by 0.25, 0.5, 1 and 2˚C. Regardless of coral adaptative capacity or restoration, net carbonate production at Cheeca Rocks declines heavily once the threshold for the onset of annual severe bleaching is reached. The switch from net accretion to net erosion, however, is significantly delayed by mitigation and adaptation. The maintenance of framework accretion until 2100 and beyond is possible under a decreased emission scenario coupled with thermal adaptation above 0.5˚C. Although restoration initiatives increase reef accretion estimates, Cheeca Rocks will only be able to keep pace with future sea-level rise in a world where anthropogenic CO2 emissions are reduced. Present results, however, attest to the potential of restoration interventions combined with increases in coral thermal tolerance to delay the onset of mass bleaching mortalities, possibly in time for a low-carbon economy to be implemented and complementary mitigation measures to become effective.

The influences of diurnal variability and ocean acidification on the bioerosion rates of two reef-dwelling Caribbean sponges.

Ocean acidification (OA) is expected to modify the structure and function of coral reef ecosystems by reducing calcification, increasing bioerosion, and altering the physiology of many marine organisms. Much of our understanding of these relationships is based on experiments with static OA treatments, although evidence suggests that the magnitude of diurnal fluctuations in carbonate chemistry may modulate the calcification response to OA. These light-mediated swings in seawater pH are projected to become more extreme with OA, yet their impact on bioerosion remains unknown. We evaluated the influence of diurnal carbonate chemistry variability on the bioerosion rates of two Caribbean sponges: the zooxanthellate Cliona varians and azooxanthellate Cliothosa delitrix. Replicate fragments from multiple colonies of each species were exposed to four precisely controlled pH treatments: contemporary static (8.05 ± 0.00; mean pH ± diurnal pH oscillation), contemporary variable (8.05 ± 0.10), future OA static (7.80 ± 0.00), and future OA variable (7.80 ± 0.10). Significantly enhanced bioerosion rates, determined using buoyant weight measurements, were observed under more variable conditions in both the contemporary and future OA scenarios for C. varians, whereas the same effect was only apparent under contemporary pH conditions for C. delitrix. These results indicate that variable carbonate chemistry has a stimulating influence on sponge bioerosion, and we hypothesize that bioerosion rates evolve non-linearly as a function of pCO2 resulting in different magnitudes and directions of rate enhancement/reduction between day and night, even with an equal fluctuation around the mean. This response appeared to be intensified by photosymbionts, evident by the consistently higher percent increase in bioerosion rates for photosynthetic C. varians across all treatments. These findings further suggest that more variable natural ecosystems may presently experience elevated sponge bioerosion rates and that the heightened impact of OA enhanced bioerosion on reef habitat could occur sooner than prior predictions.

Role of host genetics and heat-tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming.

Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back-to-back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef-building coral Orbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRAD and profiled for algal symbiont abundance and type. O. faveolata at the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerant Durusdinium trenchii (formerly Symbiondinium trenchii) was the dominant endosymbiont type region-wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated by D. trenchii. 2bRAD host genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion of D. trenchii was attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably, D. trenchii was rarely dominant in O. faveolata from the Florida Keys in previous studies, even during bleaching. The region-wide high abundance of D. trenchii was likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys, O. faveolata was most abundant, had the highest bleaching resistance, and contained the most corals dominated by D. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.

Loss of coral reef growth capacity to track future increases in sea level.

Sea-level rise (SLR) is predicted to elevate water depths above coral reefs and to increase coastal wave exposure as ecological degradation limits vertical reef growth, but projections lack data on interactions between local rates of reef growth and sea level rise. Here we calculate the vertical growth potential of more than 200 tropical western Atlantic and Indian Ocean reefs, and compare these against recent and projected rates of SLR under different Representative Concentration Pathway (RCP) scenarios. Although many reefs retain accretion rates close to recent SLR trends, few will have the capacity to track SLR projections under RCP4.5 scenarios without sustained ecological recovery, and under RCP8.5 scenarios most reefs are predicted to experience mean water depth increases of more than 0.5 m by 2100. Coral cover strongly predicts reef capacity to track SLR, but threshold cover levels that will be necessary to prevent submergence are well above those observed on most reefs. Urgent action is thus needed to mitigate climate, sea-level and future ecological changes in order to limit the magnitude of future reef submergence.

Resilience in carbonate production despite three coral bleaching events in 5 years on an inshore patch reef in the Florida Keys.

The persistence of coral reef frameworks requires that calcium carbonate (CaCO3) production by corals and other calcifiers outpaces CaCO3 loss via physical, chemical, and biological erosion. Coral bleaching causes declines in CaCO3 production, but this varies with bleaching severity and the species impacted. We conducted census-based CaCO3 budget surveys using the established ReefBudget approach at Cheeca Rocks, an inshore patch reef in the Florida Keys, annually from 2012 to 2016. This site experienced warm-water bleaching in 2011, 2014, and 2015. In 2017, we obtained cores of the dominant calcifying coral at this site, Orbicella faveolata, to understand how calcification rates were impacted by bleaching and how they affected the reef-wide CaCO3 budget. Bleaching depressed O. faveolata growth and the decline of this one species led to an overestimation of mean (± std. error) reef-wide CaCO3 production by + 0.68 (± 0.167) to + 1.11 (± 0.236) kg m-2 year-1 when using the static ReefBudget coral growth inputs. During non-bleaching years, the ReefBudget inputs slightly underestimated gross production by - 0.10 (± 0.022) to - 0.43 (± 0.100) kg m-2 year-1. Carbonate production declined after the first year of back-to-back bleaching in 2014, but then increased after 2015 to values greater than the initial surveys in 2012. Cheeca Rocks is an outlier in the Caribbean and Florida Keys in terms of coral cover, carbonate production, and abundance of O. faveolata, which is threatened under the Endangered Species Act. Given the resilience of this site to repeated bleaching events, it may deserve special management attention.

Enhanced macroboring and depressed calcification drive net dissolution at high-CO2 coral reefs.

Ocean acidification (OA) impacts the physiology of diverse marine taxa; among them corals that create complex reef framework structures. Biological processes operating on coral reef frameworks remain largely unknown from naturally high-carbon-dioxide (CO2) ecosystems. For the first time, we independently quantified the response of multiple functional groups instrumental in the construction and erosion of these frameworks (accretion, macroboring, microboring, and grazing) along natural OA gradients. We deployed blocks of dead coral skeleton for roughly 2 years at two reefs in Papua New Guinea, each experiencing volcanically enriched CO2, and employed high-resolution micro-computed tomography (micro-CT) to create three-dimensional models of changing skeletal structure. OA conditions were correlated with decreased calcification and increased macroboring, primarily by annelids, representing a group of bioeroders not previously known to respond to OA. Incubation of these blocks, using the alkalinity anomaly methodology, revealed a switch from net calcification to net dissolution at a pH of roughly 7.8, within Intergovernmental Panel on Climate Change's (IPCC) predictions for global ocean waters by the end of the century. Together these data represent the first comprehensive experimental study of bioerosion and calcification from a naturally high-CO2 reef ecosystem, where the processes of accelerated erosion and depressed calcification have combined to alter the permanence of this essential framework habitat.

Elevated Colonization of Microborers at a Volcanically Acidified Coral Reef.

Experiments have demonstrated that ocean acidification (OA) conditions projected to occur by the end of the century will slow the calcification of numerous coral species and accelerate the biological erosion of reef habitats (bioerosion). Microborers, which bore holes less than 100 µm diameter, are one of the most pervasive agents of bioerosion and are present throughout all calcium carbonate substrates within the reef environment. The response of diverse reef functional groups to OA is known from real-world ecosystems, but to date our understanding of the relationship between ocean pH and carbonate dissolution by microborers is limited to controlled laboratory experiments. Here we examine the settlement of microborers to pure mineral calcium carbonate substrates (calcite) along a natural pH gradient at a volcanically acidified reef at Maug, Commonwealth of the Northern Mariana Islands (CNMI). Colonization of pioneer microborers was higher in the lower pH waters near the vent field. Depth of microborer penetration was highly variable both among and within sites (4.2-195.5 µm) over the short duration of the study (3 mo.) and no clear relationship to increasing CO2 was observed. Calculated rates of biogenic dissolution, however, were highest at the two sites closer to the vent and were not significantly different from each other. These data represent the first evidence of OA-enhancement of microboring flora colonization in newly available substrates and provide further evidence that microborers, especially bioeroding chlorophytes, respond positively to low pH. The accelerated breakdown and dissolution of reef framework structures with OA will likely lead to declines in structural complexity and integrity, as well as possible loss of essential habitat.