Coral Disease: Direct and Indirect Agents, Mechanisms of Disease, and Innovations for Increasing Resistance and Resilience.

As climate change drives health declines of tropical reef species, diseases are further eroding ecosystem function and habitat resilience. Coral disease impacts many areas around the world, removing some foundation species to recorded low levels and thwarting worldwide efforts to restore reefs. What we know about coral disease processes remains insufficient to overcome many current challenges in reef conservation, yet cumulative research and management practices are revealing new disease agents (including bacteria, viruses, and eukaryotes), genetic host disease resistance factors, and innovative methods to prevent and mitigate epizootic events (probiotics, antibiotics, and disease resistance breeding programs). The recent outbreak of stony coral tissue loss disease across the Caribbean has reenergized and mobilized the research community to think bigger and do more. This review therefore focuses largely on novel emerging insights into the causes and mechanisms of coral disease and their applications to coral restoration and conservation.

Microbiomes of three coral species in the Mexican Caribbean and their shifts associated with the Stony Coral Tissue Loss Disease.

Stony Coral Tissue Loss Disease (SCTLD) has caused widespread coral mortality in the Caribbean Region. However, how the disease presence alters the microbiome community, their structure, composition, and metabolic functionality is still poorly understood. In this study, we characterized the microbial communities of the tissues of apparently healthy and diseased SCTLD colonies of the species Siderastrea siderea, Orbicella faveolata, and Montastraea cavernosa to explore putative changes related to the presence of SCTLD. Gammaproteobacteria, Alphaproteobacteria, and Bacteroidia were the best represented classes in the healthy tissues of all coral species, and alpha diversity did not show significant differences among the species. The microbial community structure between coral species was significantly different (PERMANOVA: F = 3.46, p = 0.001), and enriched genera were detected for each species: Vibrio and Photobacterium in S. siderea, Spirochaeta2 and Marivivens in O. faveolata and SAR202_clade and Nitrospira in M. cavernosa. Evidence of SCTLD in the microbial communities was more substantial in S. siderea, where differences in alpha diversity, beta diversity, and functional profiles were observed. In O. faveolata, differences were detected only in the community structure, while M. cavernosa samples showed no significant difference. Several microbial groups were found to have enriched abundances in tissue from SCTLD lesions from S. siderea and O. faveolata, but no dominant bacterial group was detected. Our results contribute to understanding microbial diversity associated with three scleractinian coral species and the shifts in their microbiomes associated with SCTLD in the Mexican Caribbean.

Similar functional composition of fish assemblages despite contrasting levels of habitat degradation on shallow Caribbean coral reefs.

Functional trait-based approaches provide an opportunity to assess how changes in habitat affect the structure of associated communities. Global analyses have found a similarity in the composition of reef fish functional traits despite differences in species richness, environmental regimes, and habitat components. These large-scale patterns raised the question of whether this same stability can be observed at smaller spatial scales. Here, we compared the fish trait composition and their functional diversity in two Caribbean shallow coral reefs with contrasting levels of habitat degradation: Limones (>30% cover), constituted mainly by colonies of Acropora palmata and Bonanza, a reef with extensive areas of dead Acropora structures, dominated by algae. To characterize the functional structure of fishes on each reef, we calculated the community-weighted mean trait values (CWM), functional richness, functional evenness, functional dispersion, and functional originality. Despite the differences in habitat quality, reefs exhibited a similar proportion and common structure on fish functional traits. Functional richness and functional evenness differed significantly, but functional dispersion and functional originality did not show differences between reefs. The greater niche complexity driven by the high availability of microhabitats provided by A. palmata may explain the higher functional richness in Limones, whereas the reef degradation in Bonanza may contribute to a higher functional evenness because of a similar distribution of abundance per fish trait combinations. Our results suggest that widespread degradation on Caribbean reefs has limited the type, variety, and range of traits, which could lead to a functional homogenization of fish communities even at local scales.

Sclerochronological characteristics of Orbicella faveolata in Cayo Arenas, a remote coral reef from the Gulf of Mexico.

During coral calcification in massive scleractinian corals, a double annual banding of different densities (high- and low-density) is formed in their skeletons, which can provide a retrospective record of growth and the influence of environmental conditions on the coral's lifespan. Evidence indicates that during the last decades, the reduction in coral calcification rate is attributed to the combination of global stress factors such as Sea Surface Temperature (SST) and local anthropic stressors. Yet, coral growth trajectories can vary between regions and coral species, where remote locations of coral reefs can act as natural laboratories, as they are far from the harmful effects of direct anthropogenic stressors. The present study reports historical chronology over a 24-year period (1992-2016) of coral extension rate (cm yr-1), skeletal density (g cm-3), and calcification rate (g cm-2 yr-1) of the reef-building coral Orbicella faveolata at the remote reef Cayo Arenas, Campeche Bank, in the south-eastern Gulf of Mexico. The relationships between the three sclerochronological features show that O. faveolata uses its calcification resources to build denser skeletons. Chronological trends indicate that coral extension increased, skeletal density and calcification rate decreased (33% calcification rate) over time. The results reveal that despite the remoteness of the locality the maximum SST has been increased, and the coral calcification rate decreased over time. If the temperature continues to rise, there is a conceivable risk of experiencing a decline in reef-building coral species. This scenario, in turn, could pose a significant threat, endangering not only the framework of coral reefs but also their ecological functionality, even within remote Atlantic reef ecosystems.

Newly deceased Caribbean reef-building corals experience rapid carbonate loss and colonization by endolithic organisms.

Coral mortality triggers the loss of carbonates fixed within coral skeletons, compromising the reef matrix. Here, we estimate rates of carbonate loss in newly deceased colonies of four Caribbean reef-building corals. We use samples from living and recently deceased colonies following a stony coral tissue loss disease (SCTLD) outbreak. Optical densitometry and porosity analyses reveal a loss of up to 40% of the calcium carbonate (CaCO3) content in dead colonies. The metabolic activity of the endolithic organisms colonizing the dead skeletons is likely partially responsible for the observed dissolution. To test for the consequences of mass mortality events over larger spatial scales, we integrate our estimates of carbonate loss with field data of the composition and size structure of coral communities. The dissolution rate depends on the relative abundance of coral species and the structural properties of their skeletons, yet we estimate an average reduction of 1.33 kg CaCO3 m-2, nearly 7% of the total amount of CaCO3 sequestered in the entire system. Our findings highlight the importance of including biological and chemical processes of CaCO3 dissolution in reef carbonate budgets, particularly as the impacts of global warming, ocean acidification, and disease likely enhance dissolution processes.

Morphometric responses of two zooxanthellate octocorals along a water quality gradient in the Cuban northwestern coast.

Octocoral abundance is increasing on Caribbean reefs, and one of the possible causes is their vertical morphological plasticity that allows them to grow above the substrate to reduce the effect of processes that occur in it (e.g., scour by sediments) as well as adapt to environmental gradients. The aim of this study was to determine the morphometric response of two octocorals species (Eunicea flexuosa and Plexaura kükenthali) with different life strategies in a water quality gradient. The research was carried out between 2008 and 2016 on eight forereefs of northwest Cuba. Different morphometric indicators were measured in the colonies of both species found within a belt transect (100 x 2 m) randomly located at each site. The lowest means in height, diameter, number of terminal branches/colony, cover index, and least arborescent colonies of E. flexuosa were detected at the sites with the greatest anthropogenic pollution. The water quality gradient did not explain the variability of the five morphometric indicators of P. kükenthali. However, hydrodynamic stress was the factor that most negatively affected the morphometry of this species. The chronic effect of poor water quality over time resulted in more small sized colonies of E. flexuosa at the polluted site, probably due to higher mortality. The size distribution of P. kükenthali also showed the same trend but at the sites with greater hydrodynamic stress. These results show that the morphometric response of octocorals along a water quality gradient is species-specific. This study suggests that poor water quality decreases the size and thus availability of habitat provided by octocorals sensitive to that factor (e.g., E. flexuosa) while other tolerant species (e.g., P. kükenthali) could provide the habitat of several organisms in a scenario of increasing anthropogenic pollution.

Legacy effects of anthropogenic disturbances modulate dynamics in the world's coral reefs.

Rapidly changing conditions alter disturbance patterns, highlighting the need to better understand how the transition from pulse disturbances to more persistent stress will impact ecosystem dynamics. We conducted a global analysis of the impacts of 11 types of disturbances on reef integrity using the rate of change of coral cover as a measure of damage. Then, we evaluated how the magnitude of the damage due to thermal stress, cyclones, and diseases varied among tropical Atlantic and Indo-Pacific reefs and whether the cumulative impact of thermal stress and cyclones was able to modulate the responses of reefs to future events. We found that reef damage largely depends on the condition of a reef before a disturbance, disturbance intensity, and biogeographic region, regardless of the type of disturbance. Changes in coral cover after thermal stress events were largely influenced by the cumulative stress of past disturbances and did not depend on disturbance intensity or initial coral cover, which suggests that an ecological memory is present within coral communities. In contrast, the effect of cyclones (and likely other physical impacts) was primarily modulated by the initial reef condition and did not appear to be influenced by previous impacts. Our findings also underscore that coral reefs can recover if stressful conditions decrease, yet the lack of action to reduce anthropogenic impacts and greenhouse gas emissions continues to trigger reef degradation. We uphold that evidence-based strategies can guide managers to make better decisions to prepare for future disturbances.

Structure-from-motion photogrammetry demonstrates variability in coral growth within colonies and across habitats.

Coral growth is an important metric of coral health and underpins reef-scale functional attributes such as structural complexity and calcium carbonate production. There persists, however, a paucity of growth data for most reef-building regions, especially for coral species whose skeletal architecture prevents the use of traditional methods such as coring and Alizarin staining. We used structure-from-motion photogrammetry to quantify a range of colony-scale growth metrics for six coral species in the Mexican Caribbean and present a newly developed workflow to measure colony volume change over time. Our results provide the first growth metrics for two species that are now major space occupiers on Caribbean reefs, Agaricia agaricites and Agaricia tenuifolia. We also document higher linear extension, volume increase and calcification rates within back reef compared to fore reef environments for four other common species: Orbicella faveolata, Porites astreoides, Siderastrea siderea and Pseudodiploria strigosa. Linear extension rates in our study were lower than those obtained via computed tomography (CT) scans of coral cores from the same sites, as the photogrammetry method averages growth in all dimensions, while the CT method depicts growth only along the main growth axis (upwards). The comparison of direct volume change versus potential volume increase calculated from linear extension emphasizes the importance of assessing whole colony growth to improve calcification estimates. The method presented here provides an approach that can generate accurate calcification estimates alongside a range of other whole-colony growth metrics in a non-invasive way.

Stony coral tissue loss disease decimated Caribbean coral populations and reshaped reef functionality.

Diseases are major drivers of the deterioration of coral reefs and are linked to major declines in coral abundance, reef functionality, and reef-related ecosystems services. An outbreak of a new disease is currently rampaging through the populations of the remaining reef-building corals across the Caribbean region. The outbreak was first reported in Florida in 2014 and reached the northern Mesoamerican Reef by summer 2018, where it spread across the ~450-km reef system in only a few months. Rapid spread was generalized across all sites and mortality rates ranged from 94% to <10% among the 21 afflicted coral species. Most species of the family Meandrinadae (maze corals) and subfamily Faviinae (brain corals) sustained losses >50%. This single event further modified the coral communities across the region by increasing the relative dominance of weedy corals and reducing reef functionality, both in terms of functional diversity and calcium carbonate production. This emergent disease is likely to become the most lethal disturbance ever recorded in the Caribbean, and it will likely result in the onset of a new functional regime where key reef-building and complex branching acroporids, an apparently unaffected genus that underwent severe population declines decades ago and retained low population levels, will once again become conspicuous structural features in reef systems with yet even lower levels of physical functionality.

Dataset of coral reefs monitoring, Puerto Morelos, Mexico, 2019.

Noticeable within the Mexican Caribbean is the Arrecife de Puerto Morelos National Park (APMNP), a marine protected area established as an essential component for managing and protecting coral reefs. In June 2019, we conducted a survey in eight shallow reef sites of the APMNP with the purpose of applying a coral reef assessment method, based on biological indicators of the condition of both benthos and fish communities. In this paper we present tables with data of biological and ecological variables such as: benthos coverage, species composition and abundance of corals, abundance of urchins and coral recruits, bleaching, coral diseases and coral mortality percent, reef relief, and composition and abundance of key commercial and herbivorous fish species. The research article related to these databases was published in the journal Diversity with the title: Puerto Morelos coral reefs, current state and their classification by a scoring system.

Geomorphically controlled coral distribution in degraded shallow reefs of the Western Caribbean.

The development of coral reefs results from the interaction between ecological and geological processes in space and time. Their difference in scale, however, makes it difficult to detect the impact of ecological changes on geological reef development. The decline of coral cover over the last 50 years, for example, has dramatically impaired the function of ecological processes on reefs. Yet given the limited-resolution of their Holocene record, it is uncertain how this will impact accretion and structural integrity over longer timescales. In addition, reports of this ecological decline have focused on intrinsic parameters such as coral cover and colony size at the expense of extrinsic ones such as geomorphic and environmental variables. Despite these problems, several attempts have been made to predict the long-term accretion status of reefs based entirely on the contemporary health status of benthic communities. Here we explore how this ecological decline is represented within the reef geomorphic structure, which represents the long-term expression of reef development. Using a detailed geomorphic zonation scheme, we analyze the distribution and biodiversity of reef-building corals in fringing-reef systems of the Mesoamerican Reef tract. We find a depth-related pattern in community structure which shows that the relative species distribution between geomorphic zones is statistically different. Despite these differences, contemporary coral assemblages in all zones are dominated by the same group of pioneer generalist species. These findings imply that first, coral species distribution is still controlled by extrinsic processes that generate the geomorphic zonation; second, that coral biodiversity still reflects species zonation patterns reported by early studies; and third that dominance of pioneer species implies that modern coral assemblages are in a prolonged post-disturbance adjustment stage. In conclusion, any accurate assessment of the future viability of reefs requires a consideration of the geomorphic context or risks miscalculating the impact of ecological changes on long-term reef development.

Recovery disparity between coral cover and the physical functionality of reefs with impaired coral assemblages.

The ecology and structure of many tropical coral reefs have been markedly altered over the past few decades. Although long-term recovery has been observed in terms of coral cover, it is not clear how novel species configurations shape reef functionality in impaired reefs. The identities and life-history strategies of the corals species that recover are essential for understanding reef functional dynamics. We used a species identity approach to quantify the physical functionality outcomes over a 13 year period across 56 sites in the Mexican Caribbean. This region was affected by multiple stressors that converged and drastically damaged reefs in the early 2000s. Since then, the reefs have shown evidence of a modest recovery of coral cover. We used Bayesian linear models and annual rates of change to estimate temporal changes in physical functionality and coral cover. Moreover, a functional diversity framework was used to explore changes in coral composition and the traits of those assemblages. Between 2005 and 2018, physical functionality increased at a markedly lower rate compared to that of coral cover. The disparity between recovery rates depended on the identity of the species that increased (mainly non-framework and foliose-digitate corals). No changes in species dominance or functional trait composition were observed, whereas non-framework building corals consistently dominated most reefs. Although the observed recovery of coral cover and functional potential may provide some ecological benefits, the long-term effects on reef frameworks remain unclear, as changes in the cover of key reef-building species were not observed. Our findings are likely to be representative of many reefs across the wider Caribbean basin, as declines in coral cover and rapid increases in the relative abundance of weedy corals have been reported regionally. A coral identity approach to assess species turnover is needed to understand and quantify changes in the functionality of coral reefs.

Two decades of carbonate budget change on shifted coral reef assemblages: are these reefs being locked into low net budget states?

The ecology of coral reefs is rapidly shifting from historical baselines. One key-question is whether under these new, less favourable ecological conditions, coral reefs will be able to sustain key geo-ecological processes such as the capacity to accumulate carbonate structure. Here, we use data from 34 Caribbean reef sites to examine how the carbonate production, net erosion and net carbonate budgets, as well as the organisms underlying these processes, have changed over the past 15 years in the absence of further severe acute disturbances. We find that despite fundamental benthic ecological changes, these ecologically shifted coral assemblages have exhibited a modest but significant increase in their net carbonate budgets over the past 15 years. However, contrary to expectations this trend was driven by a decrease in erosion pressure, largely resulting from changes in the abundance and size-frequency distribution of parrotfishes, and not by an increase in rates of coral carbonate production. Although in the short term, the carbonate budgets seem to have benefitted marginally from reduced parrotfish erosion, the absence of these key substrate grazers, particularly of larger individuals, is unlikely to be conducive to reef recovery and will thus probably lock these reefs into low budget states.

The role of geomorphic zonation in long-term changes in coral-community structure on a Caribbean fringing reef.

Ecological processes on coral reefs commonly have limited spatial and temporal scales and may not be recorded in their long-term geological history. The widespread degradation of Caribbean coral reefs over the last 40 years therefore provides an opportunity to assess the impact of more significant ecological changes on the geological and geomorphic structure of reefs. Here, we document the changing ecology of communities in a coral reef seascape within the context of its geomorphic zonation. By comparing basic ecological indices between historical and modern data we show that in 35 years the reef-front zone was transformed from a complex coral assemblage with a three-dimensional structure, to a size-homogenized and flattened one that is quasi indistinguishable from the adjacent non-accretional coral-ground zone. Today coral assemblages at Punta Maroma are characterized by the dominance of opportunistic species which are either tolerant to adverse environmental conditions, including sedimentation, or are known to be the first scleractinian species to recruit on disturbed reefs, implying they reflect a post-hurricane stage of adjustment. Despite an increase in similarity in ecological indices, the reef-front and coral-ground geomorphic zones still retain significant differences in coral assemblages and benthic habitat and are not homogeneous. The partial convergence of coral assemblages certainly has important consequences for the ecology and geological viability of the reef and its role in coastal protection, but environmental physical drivers continue to exert a fundamental role in the character and zonation of benthic communities of this reef seascape.

A meta-analysis to assess long-term spatiotemporal changes of benthic coral and macroalgae cover in the Mexican Caribbean.

Coral reefs in the wider Caribbean declined in hard coral cover by ~80% since the 1970s, but spatiotemporal analyses for sub-regions are lacking. Here, we explored benthic change patterns in the Mexican Caribbean reefs through meta-analysis between 1978 and 2016 including 125 coral reef sites. Findings revealed that hard coral cover decreased from ~26% in the 1970s to 16% in 2016, whereas macroalgae cover increased to ~30% in 2016. Both groups showed high spatiotemporal variability. Hard coral cover declined in total by 12% from 1978 to 2004 but increased again by 5% between 2005 and 2016 indicating some coral recovery after the 2005 mass bleaching event and hurricane impacts. In 2016, more than 80% of studied reefs were dominated by macroalgae, while only 15% were dominated by hard corals. This stands in contrast to 1978 when all reef sites surveyed were dominated by hard corals. This study is among the first within the Caribbean region that reports local recovery in coral cover in the Caribbean, while other Caribbean reefs have failed to recover. Most Mexican Caribbean coral reefs are now no longer dominated by hard corals. In order to prevent further reef degradation, viable and reliable conservation alternatives are required.

Functional consequences of the long-term decline of reef-building corals in the Caribbean: evidence of across-reef functional convergence.

Functional integrity on coral reefs is strongly dependent upon coral cover and coral carbonate production rate being sufficient to maintain three-dimensional reef structures. Increasing environmental and anthropogenic pressures in recent decades have reduced the cover of key reef-building species, producing a shift towards the relative dominance of more stress-tolerant taxa and leading to a reduction in the physical functional integrity. Understanding how changes in coral community composition influence the potential of reefs to maintain their physical reef functioning is a priority for their conservation and management. Here, we evaluate how coral communities have changed in the northern sector of the Mexican Caribbean between 1985 and 2016, and the implications for the maintenance of physical reef functions in the back- and fore-reef zones. We used the cover of coral species to explore changes in four morpho-functional groups, coral community composition, coral community calcification, the reef functional index and the reef carbonate budget. Over a period of 31 years, ecological homogenization occurred between the two reef zones mostly due to a reduction in the cover of framework-building branching (Acropora spp.) and foliose-digitiform (Porites porites and Agaricia tenuifolia) coral species in the back-reef, and a relative increase in non-framework species in the fore-reef (Agaricia agaricites and Porites astreoides). This resulted in a significant decrease in the physical functionality of the back-reef zone. At present, both reef zones have negative carbonate budgets, and thus limited capacity to sustain reef accretion, compromising the existing reef structure and its future capacity to provide habitat and environmental services.

A rapid spread of the stony coral tissue loss disease outbreak in the Mexican Caribbean.

Caribbean reef corals have experienced unprecedented declines from climate change, anthropogenic stressors and infectious diseases in recent decades. Since 2014, a highly lethal, new disease, called stony coral tissue loss disease, has impacted many reef-coral species in Florida. During the summer of 2018, we noticed an anomalously high disease prevalence affecting different coral species in the northern portion of the Mexican Caribbean. We assessed the severity of this outbreak in 2018/2019 using the AGRRA coral protocol to survey 82 reef sites across the Mexican Caribbean. Then, using a subset of 14 sites, we detailed information from before the outbreak (2016/2017) to explore the consequences of the disease on the condition and composition of coral communities. Our findings show that the disease outbreak has already spread across the entire region by affecting similar species (with similar disease patterns) to those previously described for Florida. However, we observed a great variability in prevalence and tissue mortality that was not attributable to any geographical gradient. Using long-term data, we determined that there is no evidence of such high coral disease prevalence anywhere in the region before 2018, which suggests that the entire Mexican Caribbean was afflicted by the disease within a few months. The analysis of sites that contained pre-outbreak information showed that this event considerably increased coral mortality and severely changed the structure of coral communities in the region. Given the high prevalence and lethality of this disease, and the high number of susceptible species, we encourage reef researchers, managers and stakeholders across the Western Atlantic to accord it the highest priority for the near future.

Coral reef systems of the Mexican Caribbean: Status, recent trends and conservation.

Over the last four decades the Mexican Caribbean has experienced intensive coastal development, and change on the reef system condition has already been observed. This paper describes the reef system characteristics, at local and seascape scales, and discusses the current status and trends, considering the main research efforts from academia and Non-Governmental Organizations. To date, the coral cover of most reefs in the region is between 15 and 20%, following a slight recovery on mean coral cover over the last decade. During this same period, fleshy macroalgae and herbivorous fish biomass appear to have increased. At seascape scales, an increase of macroalgae and the loss of seagrass habitat have been observed. Considering that anthropogenic and environmental disturbances will most likely increase, the establishment of newly protected areas in the Mexican Caribbean is appropriate, but sufficient accompanying funding is required.

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.