A biological condition gradient for Caribbean coral reefs: Part II. Numeric rules using sessile benthic organisms.

The Biological Condition Gradient (BCG) is a conceptual model used to describe incremental changes in biological condition along a gradient of increasing anthropogenic stress. As coral reefs collapse globally, scientists and managers are focused on how to sustain the crucial structure and functions, and the benefits that healthy coral reef ecosystems provide for many economies and societies. We developed a numeric (quantitative) BGC model for the coral reefs of Puerto Rico and the US Virgin Islands to transparently facilitate ecologically meaningful management decisions regarding these fragile resources. Here, reef conditions range from natural, undisturbed conditions to severely altered or degraded conditions. Numeric decision rules were developed by an expert panel for scleractinian corals and other benthic assemblages using multiple attributes to apply in shallow-water tropical fore reefs with depths <30 m. The numeric model employed decision rules based on metrics (e.g., % live coral cover, coral species richness, pollution-sensitive coral species, unproductive and sediment substrates, % cover by Orbicella spp.) used to assess coral reef condition. Model confirmation showed the numeric BCG model predicted the panel's median site ratings for 84% of the sites used to calibrate the model and 89% of independent validation sites. The numeric BCG model is suitable for adaptive management applications and supports bioassessment and criteria development. It is a robust assessment tool that could be used to establish ecosystem condition that would aid resource managers in evaluating and communicating current or changing conditions, protect water and habitat quality in areas of high biological integrity, or develop restoration goals with stakeholders and other public beneficiaries.

A biological condition gradient for coral reefs in the US Caribbean Territories: Part I. Coral narrative rules.

As coral reef condition and sustainability continue to decline worldwide, losses of critical habitat and their ecosystem services have generated an urgency to understand and communicate reef response to management actions, environmental contamination, and natural disasters. Increasingly, coral reef protection and restoration programs emphasize the need for robust assessment tools for protecting high-quality waters and establishing conservation goals. Of equal importance is the need to communicate assessment results to stakeholders, beneficiaries, and the public so that environmental consequences of decisions are understood. The Biological Condition (BCG) model provides a structure to evaluate the condition of a coral reef in increments of change along a gradient of human disturbance. Communication of incremental change, regardless of direction, is important for decision makers and the public to better understand what is gained or lost depending on what actions are taken. We developed a narrative (qualitative) Biological Condition Gradient (BCG) from the consensus of a diverse expert panel to provide a framework for coral reefs in US Caribbean Territories. The model uses narrative descriptions of biological attributes for benthic organisms to evaluate reefs relative to undisturbed or minimally disturbed conditions. Using expert elicitation, narrative decision rules were proposed and deliberated to discriminate among six levels of change along a gradient of increasing anthropogenic stress. Narrative rules for each of the BCG levels are presented to facilitate the evaluation of benthic communities in coral reefs and provide specific narrative features to detect changes in coral reef condition and biological integrity. The BCG model can be used in the absence of numeric, or quantitative metrics, to evaluate actions that may encroach on coral reef ecosystems, manage endangered species habitat, and develop and implement management plans for marine protected areas, watersheds, and coastal zones. The narrative BCG model is a defensible model and communication tool that translates scientific results so the nontechnical person can understand and support both regulatory and non-regulatory water quality and natural resource programs.

Warming and pollutants interact to modulate octocoral immunity and shape disease outcomes.

Warming environments can alter the outcome of host-parasite relationships with important consequences for biodiversity. Warming often increases disease risk, and interactions with other environmental factors can intensify impacts by modifying the underlying mechanisms, such as host immunity. In coastal ecosystems, metal pollution is a pervasive stressor that influences disease and immunity in many organisms. Despite the crisis facing coral reefs, which stems in part from warming-associated disease outbreaks, the impacts of metal pollutants on scleractinian and octocoral disease are largely unknown. We investigated how warming oceans and copper pollution affect host immunity and disease risk for two diseases of the abundant Caribbean octocoral, the sea fan Gorgonia ventalina. Field surveys across a sediment copper concentration gradient in Puerto Rico, USA revealed that cellular immunity of sea fans increased by 12.6% at higher sediment copper concentrations, while recovery from multifocal purple spots disease (MFPS) tended to decrease. MFPS severity in the field increased at warmer sites. In a controlled laboratory experiment, sea fans were inoculated with live cultures of a labyrinthulid parasite to test the interactive effects of temperature and copper on immune activation. As in the field, higher copper induced greater immunity, but the factorial design of the experiment revealed that copper and temperature interacted to modulate the immune response to the parasite: immune cell densities increased with elevated temperature at lower copper concentrations, but not with high copper concentrations. Tissue damage was also greater in treatments with higher copper and warmer temperatures. Field and lab evidence confirm that elevated copper hinders sea fan immune defenses against damaging parasites. Temperature and copper influenced host-pathogen interactions in octocorals by modulating immunity, disease severity, and disease recovery. This is the first evidence that metal pollution affects processes influencing disease in octocorals and highlights the importance of immune mechanisms in environmentally mediated disease outbreaks. Although coral conservation efforts must include a focus on global factors, such as rapid warming, reducing copper and other pollutants that compromise coral health on a local scale may help corals fight disease in a warming ocean.

Octocoral co-infection as a balance between host immunity and host environment.

Co-infection is the reality in natural populations, but few studies incorporate the players that matter in the wild. We integrate the environment, host demography, two parasites, and host immunity in a study of co-infection to determine the drivers of parasite interactions. Here, we use an ecologically important Caribbean sea fan octocoral, Gorgonia ventalina, that is co-infected by a copepod and a labyrinthulid protist. We first expanded upon laboratory studies by showing that immune suppression is associated with the labyrinthulid in a natural setting. Histological analyses revealed that immune cells (amoebocytes) were significantly suppressed in both labyrinthulid infections and co-infections relative to healthy sea fans, but remained unchanged in copepod infections. However, surveys of natural coral populations demonstrated a critical role for the environment and host demography in this co-infection: the prevalence of copepod infections increased with sea fan size while labyrinthulid prevalence increased with water depth. Although we predicted that immune suppression by the labyrinthulid would facilitate copepod infection, the two parasites did not co-occur in the sea fans more often than expected by chance. These results suggest that the distinct ecological drivers for each parasite overwhelm the role of host immune suppression in determining the distribution of parasites among hosts. This interplay of the environment and parasite-mediated immune suppression in sea fan co-infection provides insights into the factors underlying co-occurrence patterns in wild co-infections. Moving forward, simultaneous consideration of co-occurring parasites, host traits, and the environmental context will improve the understanding of host - parasite interactions and their consequences.

Life or death: disease-tolerant coral species activate autophagy following immune challenge.

Global climate change has increased the number and severity of stressors affecting species, yet not all species respond equally to these stressors. Organisms may employ cellular mechanisms such as apoptosis and autophagy in responding to stressful events. These two pathways are often mutually exclusive, dictating whether a cell adapts or dies. In order to examine differences in cellular response to stress, we compared the immune response of four coral species with a range of disease susceptibility. Using RNA-seq and novel pathway analysis, we were able to identify differences in response to immune stimulation between these species. Disease-susceptible species Orbicella faveolata activated pathways associated with apoptosis. By contrast, disease-tolerant species Porites porites and Porites astreoides activated autophagic pathways. Moderately susceptible species Pseudodiploria strigosa activated a mixture of these pathways. These findings were corroborated by apoptotic caspase protein assays, which indicated increased caspase activity following immune stimulation in susceptible species. Our results indicate that in response to immune stress, disease-tolerant species activate cellular adaptive mechanisms such as autophagy, while susceptible species turn on cell death pathways. Differences in these cellular maintenance pathways may therefore influence the organismal stress response. Further study of these pathways will increase understanding of differential stress response and species survival in the face of changing environments.

Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome.

Coral diseases are characterized by microbial community shifts in coral mucus and tissue, but causes and consequences of these changes are vaguely understood due to the complexity and dynamics of coral-associated bacteria. We used 16S rRNA gene microarrays to assay differences in bacterial assemblages of healthy and diseased colonies displaying White Plague Disease (WPD) signs from two closely related Caribbean coral species, Orbicella faveolata and Orbicella franksi. Analysis of differentially abundant operational taxonomic units (OTUs) revealed strong differences between healthy and diseased specimens, but not between coral species. A subsequent comparison to data from two Indo-Pacific coral species (Pavona duerdeni and Porites lutea) revealed distinct microbial community patterns associated with ocean basin, coral species and health state. Coral species were clearly separated by site, but also, the relatedness of the underlying bacterial community structures resembled the phylogenetic relationship of the coral hosts. In diseased samples, bacterial richness increased and putatively opportunistic bacteria were consistently more abundant highlighting the role of opportunistic conditions in structuring microbial community patterns during disease. Our comparative analysis shows that it is possible to derive conserved bacterial footprints of diseased coral holobionts that might help in identifying key bacterial species related to the underlying etiopathology. Furthermore, our data demonstrate that similar-appearing disease phenotypes produce microbial community patterns that are consistent over coral species and oceans, irrespective of the putative underlying pathogen. Consequently, profiling coral diseases by microbial community structure over multiple coral species might allow the development of a comparative disease framework that can inform on cause and relatedness of coral diseases.

Shadows over Caribbean reefs: Identification of a new invasive soft coral species, Xenia umbellata, in southwest Puerto Rico.

In October 2023, several colonies of an alien soft coral species were reported on shallow reefs in southwest Puerto Rico. The soft coral was identified as a xeniid octocoral (species undetermined), resembling the octocoral Unomia stolonifera, which has invaded and overgrown reefs in Venezuela in recent years. To conclusively characterize the species of the invading xeniid, we employed multilocus barcoding targeting four genes (ND2, mtMutS, COI, and 28S) of three separate colonies across three locations in southwest Puerto Rico. Sequence comparisons with xeniid sequences from GenBank, including those from the genera Xenia and Unomia, indicated a 100% sequence identity (>3,000 bp combined) with the species Xenia umbellata (Octocorallia : Malacalcyonacea : Xeniidae). Xenia umbellata is native to the Red Sea and to our knowledge, this represents the first confirmed case of this species as an invader on Caribbean reefs. Similar to U. stolonifera, X. umbellata is well known for its ability to rapidly overgrow substrate as well as tolerate environmental extremes. In addition, X. umbellata has recently been proposed as a model system for tissue regeneration having the ability to regenerate completely from a single tentacle. These characteristics greatly amplify X. umbellata's potential to adversely affect any reef it invades. Our findings necessitate continued collaborative action between local management agencies and stakeholders in Puerto Rico, as well as neighboring islands, to monitor and control this invasion prior to significant ecological perturbation.

The Montastraea faveolata microbiome: ecological and temporal influences on a Caribbean reef-building coral in decline.

Coral-associated microbial communities, including protists, bacteria, archaea and viruses, are important components of the coral holobiont that influence the health of corals and coral reef ecosystems. Evidence suggests that the composition of these microbial communities is affected by numerous parameters; however, little is known about the confluence of these ecological and temporal effects. In this study, we used ribosomal RNA gene sequencing to identify the zooxanthellae, bacteria and archaea associated with healthy and yellow band diseased (YBD) colonies in the Media Luna reef of La Parguera, Puerto Rico, in order to examine the influence of YBD on the Montastraea faveolata microbiome. In addition, we evaluated the influence of season on the differences between healthy and YBD M. faveolata microbiomes by sampling from the same tagged colonies in both March and September of 2007. To the best of our knowledge, this is the first coral microbiome study to examine sequences from the zooxanthellar, bacterial and archaeal communities simultaneously from individual coral samples. Our results confirm differences in the M. faveolata zooxanthellar, bacterial and archaeal communities between healthy and YBD colonies in March; however, the September communities do not exhibit the same differences. Moreover, we provide evidence that the differences in the M. faveolata microbiomes between March and September are more significant than those observed between healthy and YBD. This data suggest that the entire coral microbiome, not just the bacterial community, is a dynamic environment where both disease and season play important roles.

Connectivity of Caribbean coral populations: complementary insights from empirical and modelled gene flow.

Understanding patterns of connectivity among populations of marine organisms is essential for the development of realistic, spatially explicit models of population dynamics. Two approaches, empirical genetic patterns and oceanographic dispersal modelling, have been used to estimate levels of evolutionary connectivity among marine populations but rarely have their potentially complementary insights been combined. Here, a spatially realistic Lagrangian model of larval dispersal and a theoretical genetic model are integrated with the most extensive study of gene flow in a Caribbean marine organism. The 871 genets collected from 26 sites spread over the wider Caribbean subsampled 45.8% of the 1900 potential unique genets in the model. At a coarse scale, significant consensus between modelled estimates of genetic structure and empirical genetic data for populations of the reef-building coral Montastraea annularis is observed. However, modelled and empirical data differ in their estimates of connectivity among northern Mesoamerican reefs indicating that processes other than dispersal may dominate here. Further, the geographic location and porosity of the previously described east-west barrier to gene flow in the Caribbean is refined. A multi-prong approach, integrating genetic data and spatially realistic models of larval dispersal and genetic projection, provides complementary insights into the processes underpinning population connectivity in marine invertebrates on evolutionary timescales.

Friend or foe: the association of Labyrinthulomycetes with the Caribbean sea fan Gorgonia ventalina.

A new syndrome in sea fans Gorgonia ventalina consisting of multifocal purple spots (MFPS) has been observed in the Caribbean Sea. Surveys of MFPS on sea fans were conducted from 2006 to 2010 at a shallow and deep site in La Parguera, Puerto Rico (PR). At the shallow site, MFPS increased between 2006 and 2010 (site average ranged from 8 to 23%), with differences found at depths over time using an analysis of covariance (ANCOVA, p < 0.0001). As a potential causative agent we examined a Labyrinthulomycota-like ovoid parasite that was observed to be abundant in MFPS lesions in light micrographs. Labyrinhylomycetes were successfully isolated, cultured and characterized in sea fans from Florida and PR. Sequence information obtained from the small subunit (SSU) rRNA gene indicated that Labyrinthulomycetes in most sea fans (healthy and MFPS sea fans from Florida; MFPS from PR) and the cultured microorganism are in the genus Aplanochytrium, although some healthy sea fans from PR contained members of the genus Thraustochytrium. Both genera fall within the family Thraustochytriidae. Histology confirmed observations of thraustochytrids within apparently healthy and MFPS sea fans from PR, and specific staining indicated a host melanization response only in colonies containing Labyrinthulomycetes or fungal infections. Growth trials indicate that the temperature-growth optima for the cultured microorganism is ~30°C. In inoculation experiments, the cultured Aplanochytrium did not induce purple spots, and histology revealed that many of the apparently healthy recipients contained Labyrinthulomycetes prior to inoculation. Taken together, these results indicate that the Labyrinthulomycetes associated with sea fans is likely an opportunistic pathogen. Further studies are needed to understand the pathogenesis of this microorganism in sea fans and its relationship with MFPS.

Global coral disease prevalence associated with sea temperature anomalies and local factors.

Coral diseases are taking an increasing toll on coral reef structure and biodiversity and are important indicators of declining health in the oceans. We implemented standardized coral disease surveys to pinpoint hotspots of coral disease, reveal vulnerable coral families and test hypotheses about climate drivers from 39 locations worldwide. We analyzed a 3 yr study of coral disease prevalence to identify links between disease and a range of covariates, including thermal anomalies (from satellite data), location and coral cover, using a Generalized Linear Mixed Model. Prevalence of unhealthy corals, i.e. those with signs of known diseases or with other signs of compromised health, exceeded 10% on many reefs and ranged to over 50% on some. Disease prevalence exceeded 10% on 20% of Caribbean reefs and 2.7% of Pacific reefs surveyed. Within the same coral families across oceans, prevalence of unhealthy colonies was higher and some diseases were more common at sites in the Caribbean than those in the Pacific. The effects of high disease prevalence are potentially extensive given that the most affected coral families, the acroporids, faviids and siderastreids, are among the major reef-builders at these sites. The poritids and agaricids stood out in the Caribbean as being the most resistant to disease, even though these families were abundant in our surveys. Regional warm temperature anomalies were strongly correlated with high disease prevalence. The levels of disease reported here will provide a much-needed local reference point against which to compare future change.

Microbial functional structure of Montastraea faveolata, an important Caribbean reef-building coral, differs between healthy and yellow-band diseased colonies.

A functional gene array (FGA), GeoChip 2.0, was used to assess the biogeochemical cycling potential of microbial communities associated with healthy and Caribbean yellow band diseased (YBD) Montastraea faveolata. Over 6700 genes were detected, providing evidence that the coral microbiome contains a diverse community of archaea, bacteria and fungi capable of fulfilling numerous functional niches. These included carbon, nitrogen and sulfur cycling, metal homeostasis and resistance, and xenobiotic contaminant degradation. A significant difference in functional structure was found between healthy and YBD M. faveolata colonies and those differences were specific to the physical niche examined. In the surface mucopolysaccharide layer (SML), only two of 31 functional categories investigated, cellulose degradation and nitrification, revealed significant differences, implying a very specific change in microbial functional potential. Coral tissue slurry, on the other hand, revealed significant changes in 10 of the 31 categories, suggesting a more generalized shift in functional potential involving various aspects of nutrient cycling, metal transformations and contaminant degradation. This study is the first broad screening of functional genes in coral-associated microbial communities and provides insights regarding their biogeochemical cycling capacity in healthy and diseased states.

Antimicrobial resistance of the coral pathogen Vibrio coralliilyticus and Caribbean sister phylotypes isolated from a diseased octocoral.

Vibrio coralliilyticus is a global marine pathogen that has been found to cause disease in several marine organisms, including corals. This study is the first report of the isolation of V. coralliilyticus from a diseased Caribbean octocoral, Pseudopterogorgia americana. Five sister phylotypes were positively identified using 16S rRNA gene sequencing, recA probes specific for V. coralliilyticus, and rep-PCR fingerprinting. The antimicrobial resistance was compared between pathogenic strains of V. coralliilyticus and the Caribbean strains. First, the antimicrobial resistance of V. coralliilyticus-type strain ATCC BAA-450 was determined using an agar-overlay antimicrobial bioassay at 24 degrees C and 27 degrees C, temperatures which are relevant to its known temperature-dependent virulence. From 108 distinct bacteria isolated from P. americana, 12 inhibited the V. coralliilyticus-type strain at 24 degrees C and five at 27 degrees C. Next, the phenotypic comparison of two Caribbean phylotypes and three V. coralliilyticus reference strains against a subset of 30 bacteria demonstrated a similar resistance trend. At both temperatures, the reference strains were inhibited by three bacteria isolates, while the Caribbean strains were inhibited by four to nine bacteria. Additionally, V. coralliilyticus-type strain ATCC BAA-450 and one of the Caribbean strains were inhibited by a higher number of bacteria at 24 degrees C compared with 27 degrees C. Together, these results highlight that V. coralliilyticus strains have antimicrobial resistance to the majority of coral-associated bacteria tested, which may be temperature-dependent in some strains. Furthermore, all V. coralliilyticus strains tested showed multi-drug resistance to a range of 11-16 (out of 26) commercial antibiotics. This study establishes V. coralliilyticus in association with a Caribbean octocoral and demonstrates its resistance to the antimicrobial activity of coral-associated bacteria and to commercial antibiotics.

Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan Octocorals.

The interplay among environment, demography, and host-parasite interactions is a challenging frontier. In the ocean, fundamental changes are occurring due to anthropogenic pressures, including increased disease outbreaks on coral reefs. These outbreaks include multiple parasites, calling into question how host immunity functions in this complex milieu. Our work investigates the interplay of factors influencing co-infection in the Caribbean sea fan octocoral, Gorgonia ventalina, using metrics of the innate immune response: cellular immunity and expression of candidate immune genes. We used existing copepod infections and live pathogen inoculation with the Aspergillus sydowii fungus, detecting increased expression of the immune recognition gene Tachylectin 5A (T5A) in response to both parasites. Cellular immunity increased by 8.16% in copepod infections compared to controls and single Aspergillus infections. We also detected activation of cellular immunity in reef populations, with a 13.6% increase during copepod infections. Cellular immunity was similar in the field and in the lab, increasing with copepod infections and not the fungus. Amoebocyte density and the expression of T5A and a matrix metalloproteinase (MMP) gene were also positively correlated across all treatments and colonies, irrespective of parasitic infection. We then assessed the scaling of immune metrics to population-level disease patterns and found random co-occurrence of copepods and fungus across 15 reefs in Puerto Rico. The results suggest immune activation by parasites may not alter parasite co-occurrence if factors other than immunity prevail in structuring parasite infection. We assessed non-immune factors in the field and found that sea fan colony size predicted infection by the copepod parasite. Moreover, the effect of infection on immunity was small relative to that of site differences and live coral cover, and similar to the effect of reproductive status. While additional immune data would shed light on the extent of this pattern, ecological factors may play a larger role than immunity in controlling parasite patterns in the wild. Parsing the effects of immunity and ecological factors in octocoral co-infection shows how disease depends on more than one host and one parasite and explores the application of co-infection research to a colonial marine organism.

Lack of recovery of the long-spined sea urchin Diadema antillarum Philippi in Puerto Rico 33 years after the Caribbean-wide mass mortality.

Caribbean populations of the long-spined black sea urchin Diadema antillarum Philippi were decimated by a disease-induced mass mortality in the early 1980's. The present study provides an updated status of the D. antillarum recovery and population characteristics in La Parguera Natural Reserve, Puerto Rico. The last detailed study to assess population recovery in 2001, indicated a slow, and modest recovery, albeit densities remained far below pre-mass mortality levels. Population densities were assessed along three depth intervals in six reef localities and one depth in three lagoonal sea-grass mounds using ten 20 m2 (10 × 2 m) belt-transects at each depth interval. Most of these were previously surveyed in 2001. All individuals encountered along the belt transects were sized in situ with calipers and rulers to characterize the size (age) structure of each population and get insight into the urchin's population dynamics and differences across localities in the area. Habitat complexity (rugosity) was assessed in all depth intervals. No significant differences in population densities between reef zones (inner shelf and mid-shelf) were observed, but significantly higher densities were found on shallow habitats (<5 m depth; 2.56 ± 1.6 ind/m2) compared to intermediate (7-12 m; 0.47 ± 0.8 ind/m2) and deep (>12 m; 0.04 ± 0.08 ind/m2) reef habitats in almost all sites surveyed. Habitat complexity had the greatest effect on population densities at all levels (site, zone and depth) with more rugose environments containing significantly higher densities and wider size structures. Comparison between survey years revealed that D. antillarum populations have not increased since 2001, and urchins seem to prefer shallower, more complex and productive areas of the reef. Populations were dominated by medium to large (5-9 cm in test diameter) individuals and size-frequency distributions indicated that smaller juveniles were virtually absent compared to 2001, which could reflect a recruitment-limited population and explain in part, the lack of increase in population densities. The limited temporal scale of this study, high horizontal movement of individuals along the complex, shallower reef and inshore habitats could also explain the general decline in mean densities. Other extrinsic factors affecting reproductive output and/or succesful recruitment and survival of juveniles likely contribute to the high variablility in population densities observed over time.

Growth dynamics in Acropora cervicornis and A. prolifera in southwest Puerto Rico.

Natural population recovery of Acropora palmata, A. cervicornis and their hybrid, Acropora prolifera, have fluctuated significantly after their Caribbean-wide, disease-induced mass mortality in the early 1980s. Even though significant recovery has been observed in a few localities, recurrent disease outbreaks, bleaching, storm damage, local environmental deterioration, algae smothering, predation, low sexual recruitment and low survivorship have affected the expected, quick recovery of these weedy species. In this study, the status of three recovering populations of A. cervicornis and two of A. prolifera were assessed over one year using coral growth and mortality metrics, and changes in their associated algae and fish/invertebrate communities in three localities in the La Parguera Natural Reserve (LPNR), southwest coast of Puerto Rico. Five branches were tagged in each of 29, medium size (1-2 m in diameter) A. cervicornis and 18 A. prolifera colonies in the Media Luna, Mario and San Cristobal reefs off LPNR. Branches were measured monthly, together with observations to evaluate associated disease(s), algae accumulation and predation. A. cervicornis grew faster [3.1 ± 0.44 cm/month (= 37.2 cm/y)] compared to A. prolifera [2.6 ± 0.41 cm/month (= 31.2 cm/y)], and growth was significantly higher during Winter-Spring compared to Summer-Fall for both taxa (3.5 ± 0.58 vs. 0.53 ± 0.15 cm/month in A. cervicornis, and 2.43 ± 0.71 vs. 0.27 ± 0.20 cm/month in A. prolifera, respectively). Algal accumulation was only observed in A. cervicornis, and was higher during Spring-Summer compared to Fall-Winter (6.1 ± 0.91 cm/month and 3.8 ± 0.29 cm/month, respectively, (PERMANOVA, df = 2, MS = 10.2, p = 0.37)). Mortality associated with white band disease, algae smothering and fish/invertebrate predation was also higher in A. cervicornis and varied among colonies within sites, across sites and across season. The balance between tissue grow and mortality determines if colonies survive. This balance seems to be pushed to the high mortality side often by increasing frequency of high thermal anomalies, inducing bleaching and disease outbreaks and other factors, which have historically impacted the natural recovery of these taxa in the La Parguera Natural Reserve in Puerto Rico and possibly other areas in the region. Overall, results indicate variability in both growth and mortality rates in both taxa across localities and seasons, with A. cervicornis showing overall higher mortalities compared to A. prolifera.

Changes in Caribbean coral disease prevalence after the 2005 bleaching event.

Bleaching events and disease epizootics have increased during the past decades, suggesting a positive link between these 2 causes in producing coral mortality. However, studies to test this hypothesis, integrating a broad range of hierarchical spatial scales from habitats to distant localities, have not been conducted in the Caribbean. In this study, we examined links between bleaching intensity and disease prevalence collected from 6 countries, 2 reef sites for each country, and 3 habitats within each reef site (N = 6 x 2 x 3 = 36 site-habitat combinations) during the peak of bleaching in 2005 and a year after, in 2006. Patterns of disease prevalence and bleaching were significantly correlated (Rho = 0.58, p = 0.04). Higher variability in disease prevalence after bleaching occurred among habitats at each particular reef site, with a significant increase in prevalence recorded in 4 of the 10 site-habitats where bleaching was intense and a non-significant increase in disease prevalence in 18 out of the 26 site-habitats where bleaching was low to moderate. A significant linear correlation was found (r = 0.89, p = 0.008) between bleaching and the prevalence of 2 virulent diseases (yellow band disease and white plague) affecting the Montastraea species complex. Results of this study suggest that if bleaching events become more intense and frequent, disease-related mortality of Caribbean coral reef builders could increase, with uncertain effects on coral reef resilience.

Spatial variability in distribution and prevalence of Caribbean scleractinian coral and octocoral diseases. I. Community-level analysis.

Geographic assessments of coral diseases are needed to understand their local and geographic spatial-temporal variability. Coral and octocoral diseases and their prevalence were assessed along 4 permanent 10 x 2 m band-transects in each of 3 depth habitats (<4, 5-12 and >15 m) in each of 2 reefs in each of 6 countries across the wider Caribbean during the summer and fall of 2005. A permutational multivariate analysis of variance was used to test variability of major diseases and community level disease prevalence in corals and octocorals among habitats, reefs and countries. The most common and damaging diseases reported for the region were found in most reefs surveyed, but prevalence at the community level was generally low (ca. 2%) increasing from northern to southern latitudes. A significant interaction between sites (nested within country) and depth habitats was found (F = 2.1, df = 12, p = 0.02), with higher prevalence of coral diseases in deep habitats of Culebrita, Puerto Rico (14.8 +/- SE 6.5%) and in shallow habitats of Roldán, Panama (10.2 +/- SE 3.5%). The relative importance of each particular disease was dependent on site and habitat (depth intervals) (F = 1.7, df = 12, p = 0.001), with black band disease more prevalent in shallow habitats of Rita's, Bermuda (1.7 +/- SE 0.4%) and yellow band disease (YBD) more prevalent in deeper habitats of Chub Cut, Bermuda (3.7 +/- SE 0.5%). There was a significant interaction of total octocoral diseases with country and habitat (F = 2.8, df = 10, p = 0.04) with higher prevalence in deeper habitats of Curaçao (25.9 +/- SE 4.2%). Our results indicate that patterns of prevalence of coral and octocoral diseases were not consistent across the different spatial scales, showing differences produced by particular diseases and community composition present. There were no widespread epizootics, but local white plague-II and YBD epizootics were observed in Puerto Rico and other localities.

Spatial variability in distribution and prevalence of Caribbean scleractinian coral and octocoral diseases. II. Genera-level analysis.

Geographic assessments of coral/octocoral diseases affecting major reef-building genera and abundant reef species are important to understand their local and geographic spatial-temporal variability and their impact. The status and spatial variability of major Caribbean coral/octocoral diseases affecting important reef-building coral (Montastraea, Diploria, Siderastrea, Stephanocoenia, Porites, and Agaricia) and common, widespread octocoral genera (Gorgonia and Pseudopterogorgia) was assessed along 4 permanent 10 x 2 m band-transects in each of 3 depth habitats (<4, 5-12 and >15 m) on 2 reefs in 6 countries across the wider Caribbean during the summer and fall of 2005. A permutational multivariate analysis of variance was used to test the spatial variability (countries, reef sites and depth habitats) in prevalence of major diseases in these genera. We found a significant interaction of disease prevalence in the different coral and octocoral genera between reef sites and habitats (depth intervals). Montastraea was primarily affected by both white plague (WP-II) and yellow band disease in deep (16.9 +/- SE 16% and 16.9 +/- SE 2.3%) and intermediate (8.1 +/- SE 1.6% and 15.5 +/- SE 2.3%) depth habitats of Culebrita (Puerto Rico) and Chub Cut (Bermuda), respectively. Prevalence of multiple diseases simultaneously and other compromised-health problems affecting Montastraea colonies varied between 0.2 to 2% and 0.2 to 1.8%, respectively. Agaricia and Diploria were mostly affected by WP-II (0.5 to 16%), black band disease (0.4 to 5%) and Caribbean ciliate infections (0.2 to 12%). Siderastrea and Stephanocoenia were mainly affected by dark spots disease in Curaçao, with higher prevalence in intermediate (40.5 +/- SE 6.2%) and deep (26.6 +/- SE 4.2%) habitats. Aspergillosis and other compromised-health conditions affected Gorgonia ventalina (0.2 to 8%) and other common and widespread octocoral genera (1 to 14%), respectively.

Yellow band disease compromises the reproductive output of the Caribbean reef-building coral Montastraea faveolata (Anthozoa, Scleractinia).

Sexual reproduction is critical to coral population dynamics and the long-term regeneration of coral reefs. Bleaching, disease, and/or anthropogenic-induced tissue/colony loss reduce reproductive output. This is the first attempt to explore the effect of a biotic disease on the reproduction of scleractinian corals. The study aimed to assess the effect of yellow band disease (YBD) on the reproduction of the important Caribbean reef-builder Montastraea faveolata. Tissue samples were collected from diseased, transition, and healthy-looking areas in each of 5 infected colonies and from 5 healthy controls in southwest Puerto Rico. The effect of disease-induced mortality was assessed by collecting samples from the edge and center of surviving small and large, healthy-looking tissue patches from large, previously infected tagged colonies. Fecundity was significantly lower in disease lesions compared to transition and healthy-looking tissues and the controls (99% fewer eggs). Fecundity in transition areas was significantly lower (50%) than in healthy-looking tissues in diseased colonies, which had 23% lower fecundity than control tissues. Although this fecundity drop was not statistically significant, it could indicate a systemic effect of YBD across the colony. Large and small patches had 64 and 84% fewer eggs than controls, respectively, and edge polyps had 97% fewer eggs than those in central control areas. Field observations of the spawning behavior of each tissue area corroborated the histological results. Our results indicate that YBD significantly compromises the reproductive output of M. faveolata, potentially reducing the fitness and consequently, the recovery of this important reef-building species on Caribbean coral reefs.