Mass Coral Bleaching in 2010 in the Southern Caribbean

Ocean temperatures are increasing globally and the Caribbean is no exception. An extreme ocean warming event in 2010 placed Tobago''s coral reefs under severe stress resulting in widespread coral bleaching and threatening the livelihoods that rely on them. The bleaching response of four reef building taxa was monitored over a six month period across three major reefs systems in Tobago. By identifying taxa resilient to bleaching we propose to assist local coral reef managers in the decision making process to cope with mass bleaching events. The bleaching signal (length of exposure to high ocean temperatures) varied widely between the Atlantic and Caribbean reefs, but regardless of this variation most taxa bleached. Colpophyllia natans, Montastraea faveolata and Siderastrea siderea were considered the most bleaching vulnerable taxa. Interestingly, reefs with the highest coral cover showed the greatest decline reef building taxa, and conversely, reefs with the lowest coral cover showed the most bleaching but lowest change in coral cover with little algal overgrowth post-bleaching.     

Cyanobacteria Associated with Coral Black Band Disease in Caribbean and Indo-Pacific Reefs

For 30 years it has been assumed that a single species of cyanobacteria, Phormidium corallyticum, is the volumetrically dominant component of all cases of black band disease (BBD) in coral. Cyanobacterium-specific 16S rRNA gene primers and terminal restriction fragment length polymorphism analyses were used to determine the phylogenetic diversity of these BBD cyanobacteria on coral reefs in the Caribbean and Indo-Pacific Seas. These analyses indicate that the cyanobacteria that inhabit BBD bacterial mats collected from the Caribbean and Indo-Pacific Seas belong to at least three different taxa, despite the fact that the corals in each case exhibit similar signs and patterns of BBD mat development.     

Disturbance Driven Colony Fragmentation as a Driver of a Coral Disease Outbreak

In September of 2010, Brewer''s Bay reef, located in St. Thomas (U.S. Virgin Islands), was simultaneously affected by abnormally high temperatures and the passage of a hurricane that resulted in the mass bleaching and fragmentation of its coral community. An outbreak of a rapid tissue loss disease among coral colonies was associated with these two disturbances. Gross lesion signs and lesion progression rates indicated that the disease was most similar to the Caribbean coral disease white plague type 1. Experiments indicated that the disease was transmissible through direct contact between colonies, and five-meter radial transects showed a clustered spatial distribution of disease, with diseased colonies being concentrated within the first meter of other diseased colonies. Disease prevalence and the extent to which colonies were bleached were both significantly higher on unattached colony fragments than on attached colonies, and disease occurred primarily on fragments found in direct contact with sediment. In contrast to other recent studies, disease presence was not related to the extent of bleaching on colonies. The results of this study suggest that colony fragmentation and contact with sediment played primary roles in the initial appearance of disease, but that the disease was capable of spreading among colonies, which suggests secondary transmission is possible through some other, unidentified mechanism.     

Identification of Candidate Coral Pathogens on White Band Disease-Infected Staghorn Coral

Bacterial diseases affecting scleractinian corals pose an enormous threat to the health of coral reefs, yet we still have a limited understanding of the bacteria associated with coral diseases. White band disease is a bacterial disease that affects the two Caribbean acroporid corals, the staghorn coral Acropora cervicornis and the elkhorn coral A. palmate. Species of Vibrio and Rickettsia have both been identified as putative WBD pathogens. Here we used Illumina 16S rRNA gene sequencing to profile the bacterial communities associated with healthy and diseased A. cervicornis collected from four field sites during two different years. We also exposed corals in tanks to diseased and healthy (control) homogenates to reduce some of the natural variation of field-collected coral bacterial communities. Using a combination of multivariate analyses, we identified community-level changes between diseased and healthy corals in both the field-collected and tank-exposed datasets. We then identified changes in the abundances of individual operational taxonomic units (OTUs) between diseased and healthy corals. By comparing the diseased and healthy-associated bacteria in field-collected and tank-exposed corals, we were able to identify 16 healthy-associated OTUs and 106 consistently disease-associated OTUs, which are good candidates for putative WBD pathogens. A large percentage of these disease-associated OTUs belonged to the order Flavobacteriales. In addition, two of the putative pathogens identified here belong to orders previously suggested as WBD pathogens: Vibronales and Rickettsiales.     

How Microbial Community Composition Regulates Coral Disease Development

Reef coral cover is in rapid decline worldwide, in part due to bleaching (expulsion of photosynthetic symbionts) and outbreaks of infectious disease. One important factor associated with bleaching and in disease transmission is a shift in the composition of the microbial community in the mucus layer surrounding the coral: the resident microbial community—which is critical to the healthy functioning of the coral holobiont—is replaced by pathogenic microbes, often species of Vibrio. In this paper we develop computational models for microbial community dynamics in the mucus layer in order to understand how the surface microbial community responds to changes in environmental conditions, and under what circumstances it becomes vulnerable to overgrowth by pathogens. Some of our model''s assumptions and parameter values are based on Vibrio spp. as a model system for other established and emerging coral pathogens. We find that the pattern of interactions in the surface microbial community facilitates the existence of alternate stable states, one dominated by antibiotic-producing beneficial microbes and the other pathogen-dominated. A shift to pathogen dominance under transient stressful conditions, such as a brief warming spell, may persist long after environmental conditions have returned to normal. This prediction is consistent with experimental findings that antibiotic properties of Acropora palmata mucus did not return to normal long after temperatures had fallen. Long-term loss of antibiotic activity eliminates a critical component in coral defense against disease, giving pathogens an extended opportunity to infect and spread within the host, elevating the risk of coral bleaching, disease, and mortality.     

Genetic Susceptibility,Colony Size,and Water Temperature Drive White-Pox Disease on the Coral Acropora palmata

Outbreaks of coral diseases are one of the greatest threats to reef corals in the Caribbean, yet the mechanisms that lead to coral diseases are still largely unknown. Here we examined the spatial-temporal dynamics of white-pox disease on Acropora palmata coral colonies of known genotypes. We took a Bayesian approach, using Integrated Nested Laplace Approximation algorithms, to examine which covariates influenced the presence of white-pox disease over seven years. We showed that colony size, genetic susceptibility of the coral host, and high-water temperatures were the primary tested variables that were positively associated with the presence of white-pox disease on A. palmata colonies. Our study also showed that neither distance from previously diseased individuals, nor colony location, influenced the dynamics of white-pox disease. These results suggest that white-pox disease was most likely a consequence of anomalously high water temperatures that selectively compromised the oldest colonies and the most susceptible coral genotypes.     

Caribbean coral diseases: primary transmission or secondary infection?

Over the last 40 years, disease outbreaks have significantly reduced coral populations throughout the Caribbean. Most coral‐disease models assume that coral diseases are contagious and that pathogens are transmitted from infected to susceptible hosts. However, this assumption has not been rigorously tested. We used spatial epidemiology to examine disease clustering, at scales ranging from meters to tens of kilometers, to determine whether three of the most common Caribbean coral diseases, (i) yellow‐band disease, (ii) dark‐spot syndrome, and (iii) white‐plague disease, were spatially clustered. For all three diseases, we found no consistent evidence of disease clustering and, therefore, these diseases did not follow a contagious‐disease model. We suggest that the expression of some coral diseases is instead a two‐step process. First, environmental thresholds are exceeded. Second, these environmental conditions either weaken the corals, which are then more susceptible to infection, or the conditions increase the virulence or abundance of pathogens. Exceeding such environmental thresholds will most likely become increasingly common in rapidly warming oceans, leading to more frequent coral‐disease outbreaks.     

The Possible Role of Cyanobacterial Filaments in Coral Black Band Disease Pathology

Black band disease (BBD), characterized by a black mat or line that migrates across a coral colony leaving behind it a bare skeleton, is a persistent disease affecting massive corals worldwide. Previous microscopic and molecular examination of this disease in faviid corals from the Gulf of Eilat revealed a number of possible pathogens with the most prominent being a cyanobacterium identified as Pseudoscillatoria coralii. We examined diseased coral colonies using histopathological and molecular methods in order to further assess the possible role of this cyanobacterium, its mode of entry, and pathological effects on the coral host tissues. Affected areas of colonies with BBD were sampled for examination using both light and transmission electron microscopies. Results showed that this dominant cyanobacterium was found on the coral surface, at the coral–skeletal interface, and invading the polyp tissues and gastrovascular cavity. Although tissues surrounding the invasive cyanobacterial filaments did not show gross morphological alterations, microscopic examination revealed that the coral cells surrounding the lesion were dissociated, necrotic, and highly vacuolated. No amoebocytes were evident in the mesoglea of affected tissues suggesting a possible repression of the coral immune response. Morphological and molecular similarity of the previously isolated BBD-associated cyanobacterium P. coralii to the current samples strengthens the premise that this species is involved in the disease in this coral. These results indicate that the cyanobacteria may play a pivotal role in this disease and that the mode of entry may be via ingestion, penetrating the coral via the gastrodermis, as well as through the skeletal–tissue interface.     

Disease outbreaks, bleaching and a cyclone drive changes in coral assemblages on an inshore reef of the Great Barrier Reef

Coral disease is a major threat to the resilience of coral reefs; thus, understanding linkages between disease outbreaks and disturbances predicted to increase with climate change is becoming increasingly important. Coral disease surveys conducted twice yearly between 2008 and 2011 at a turbid inshore reef in the central Great Barrier Reef spanned two disturbance events, a coral bleaching event in 2009 and a severe cyclone (cyclone ‘Yasi’) in 2011. Surveys of coral cover, community structure and disease prevalence throughout this 4-yr study provide a unique opportunity to explore cumulative impacts of disturbance events and disease for inshore coral assemblages. The principal coral disease at the study site was atramentous necrosis (AtN), and it primarily affected the key inshore, reef-building coral Montipora aequituberculata. Other diseases detected were growth anomalies, white syndrome and brown band syndrome. Diseases affected eight coral genera, although Montipora was, by far, the genus mostly affected. The prevalence of AtN followed a clear seasonal pattern, with disease outbreaks occurring only in wet seasons. Mean prevalence of AtN on Montipora spp. (63.8 % ± 3.03) was three- to tenfold greater in the wet season of 2009, which coincided with the 2009 bleaching event, than in other years. Persistent wet season outbreaks of AtN combined with the impacts of bleaching and cyclone events resulted in a 50–80 % proportional decline in total coral cover. The greatest losses of branching and tabular acroporids occurred following the low-salinity-induced bleaching event of 2009, and the greatest losses of laminar montiporids occurred following AtN outbreaks in 2009 and in 2011 following cyclone Yasi. The shift to a less diverse coral assemblage and the concomitant loss of structural complexity are likely to have long-term consequences for associated vertebrate and invertebrate communities on Magnetic Island reefs.     

Partitioning of Bacterial Communities between Seawater and Healthy, Black Band Diseased, and Dead Coral Surfaces

Distinct partitioning has been observed in the composition and diversity of bacterial communities inhabiting the surface and overlying seawater of three coral species infected with black band disease (BBD) on the southern Caribbean island of Curaçao, Netherlands Antilles. PCR amplification and sequencing of bacterial 16S rRNA genes (rDNA) with universally conserved primers have identified over 524 unique bacterial sequences affiliated with 12 bacterial divisions. The molecular sequences exhibited less than 5% similarity in bacterial community composition between seawater and the healthy, black band diseased, and dead coral surfaces. The BBD bacterial mat rapidly migrates across and kills the coral tissue. Clone libraries constructed from the BBD mat were comprised of eight bacterial divisions and 13% unknowns. Several sequences representing bacteria previously found in other marine and terrestrial organisms (including humans) were isolated from the infected coral surfaces, including Clostridium spp., Arcobacter spp., Campylobacter spp., Cytophaga fermentans, Cytophaga columnaris, and Trichodesmium tenue.     

Relationship between Phylogeny and Immunity Suggests Older Caribbean Coral Lineages Are More Resistant to Disease

Diseases affect coral species fitness and contribute significantly to the deterioration of coral reefs. The increase in frequency and severity of disease outbreaks has made evaluating and determining coral resistance a priority. Phylogenetic patterns in immunity and disease can provide important insight to how corals may respond to current and future environmental and/or biologically induced diseases. The purpose of this study was to determine if immunity, number of diseases and disease prevalence show a phylogenetic signal among Caribbean corals. We characterized the constitutive levels of six distinct innate immune traits in 14 Caribbean coral species and tested for the presence of a phylogenetic signal on each trait. Results indicate that constitutive levels of some individual immune related processes (i.e. melanin concentration, peroxidase and inhibition of bacterial growth), as well as their combination show a phylogenetic signal. Additionally, both the number of diseases affecting each species and disease prevalence (as measures of disease burden) show a significant phylogenetic signal. The phylogenetic signal of immune related processes, combined with estimates of species divergence times, indicates that among the studied species, those belonging to older lineages tend to resist/fight infections better than more recently diverged coral lineages. This result, combined with the increasing stressful conditions on corals in the Caribbean, suggest that future reefs in the region will likely be dominated by older lineages while modern species may face local population declines and/or geographic extinction.     

Relationship of Vibrio Species Infection and Elevated Temperatures to Yellow Blotch/Band Disease in Caribbean Corals

The bacterial and temperature factors leading to yellow blotch/band disease (YBD), which affects the major reef-building Caribbean corals Montastrea spp., have been investigated. Groups of bacteria isolated from affected corals and inoculated onto healthy corals caused disease signs similar to those of YBD. The 16S rRNA genes from these bacteria were sequenced and found to correspond to four Vibrio spp. Elevating the water temperature notably increased the rate of spread of YBD on inoculated corals and induced greater coral mortality. YBD-infected corals held at elevated water temperatures had 50% lower zooxanthella densities, 80% lower division rates, and a 75% decrease in chlorophyll a and c₂ pigments compared with controls. Histological sections indicated that the algal pyrenoid was fragmented into separate segments, along with a reconfiguration and swelling of the zooxanthellae, as well as vacuolization. YBD does not appear to produce the same physiological response formerly observed in corals undergoing temperature-related bleaching. Evidence indicates that YBD affects primarily the symbiotic algae rather than coral tissue.     

Macroalgae Has No Effect on the Severity and Dynamics of Caribbean Yellow Band Disease

By removing herbivores and promoting increases in macroalgae, overfishing is thought to indirectly cause coral disease and mortality. We performed three field manipulations to test the general hypothesis that overfishing and the subsequent alteration of coral reef trophic dynamics are a cause of coral epizootics. Specifically, we asked whether the presence of macroalgae can influence within- and among-colony spread rates of Caribbean Yellow Band Disease in Montastraea faveolata. Macroalgae were placed next to infected and healthy, adult and small coral colonies to measure effects on disease spread rate, coral growth and coral survival. Surprisingly, the addition of macroalgae did not affect disease severity or coral fitness. Our results indicate that macroalgae have no effect on the severity and dynamics of Caribbean Yellow Band Disease and that fisheries management alone will not mitigate the effects of this important epizootic.     

Nutrient enrichment can increase the severity of coral diseases

The prevalence and severity of marine diseases have increased over the last 20 years, significantly impacting a variety of foundation and keystone species. One explanation is that changes in the environment caused by human activities have impaired host resistance and/or have increased pathogen virulence. Here, we report evidence from field experiments that nutrient enrichment can significantly increase the severity of two important Caribbean coral epizootics: aspergillosis of the common gorgonian sea fan Gorgonia ventalina and yellow band disease of the reef‐building corals Montastraea annularis and M. franksii. Experimentally increasing nutrient concentrations by 2–5× nearly doubled host tissue loss caused by yellow band disease. In a separate experiment, nutrient enrichment significantly increased two measures of sea fan aspergillosis severity. Our results may help explain the conspicuous patchiness of coral disease severity, besides suggesting that minimizing nutrient pollution could be an important management tool for controlling coral epizootics.     

Potential role of viruses in white plague coral disease

White plague (WP)-like diseases of tropical corals are implicated in reef decline worldwide, although their etiological cause is generally unknown. Studies thus far have focused on bacterial or eukaryotic pathogens as the source of these diseases; no studies have examined the role of viruses. Using a combination of transmission electron microscopy (TEM) and 454 pyrosequencing, we compared 24 viral metagenomes generated from Montastraea annularis corals showing signs of WP-like disease and/or bleaching, control conspecific corals, and adjacent seawater. TEM was used for visual inspection of diseased coral tissue. No bacteria were visually identified within diseased coral tissues, but viral particles and sequence similarities to eukaryotic circular Rep-encoding single-stranded DNA viruses and their associated satellites (SCSDVs) were abundant in WP diseased tissues. In contrast, sequence similarities to SCSDVs were not found in any healthy coral tissues, suggesting SCSDVs might have a role in WP disease. Furthermore, Herpesviridae gene signatures dominated healthy tissues, corroborating reports that herpes-like viruses infect all corals. Nucleocytoplasmic large DNA virus (NCLDV) sequences, similar to those recently identified in cultures of Symbiodinium (the algal symbionts of corals), were most common in bleached corals. This finding further implicates that these NCLDV viruses may have a role in bleaching, as suggested in previous studies. This study determined that a specific group of viruses is associated with diseased Caribbean corals and highlights the potential for viral disease in regional coral reef decline.     

Microbial Community Compositional Shifts in Bleached Colonies of the Brazilian Reef-Building Coral Siderastrea stellata

The association of metazoan, protist, and microbial communities with Scleractinian corals forms the basis of the coral holobiont. Coral bleaching events have been occurring around the world, introducing changes in the delicate balance of the holobiont symbiotic interactions. In this study, Archaea, bacteria, and eukaryotic phototrophic plastids of bleached colonies of the Brazilian coral Siderastrea stellata were analyzed for the first time, using 16S rRNA gene libraries. Prokaryotic communities were slightly more diverse in healthy than in bleached corals. However, the eukaryotic phototrophic plastids community was more diverse in bleached corals. Archaea phylogenetic analyses revealed a high percentage of Crenarchaeota sequences, mainly related to Nitrosopumilus maritimus and Cenarchaeum symbiosum. Dramatic changes in bacterial community composition were observed in this bleaching episode. The dominant bacterial group was Alphaproteobacteria followed by Gammaproteobacteria in bleached and Betaproteobacteria in healthy samples. Plastid operational taxonomic units (OTUs) from both coral samples were mainly related to red algae chloroplasts (Florideophycea), but we also observed some OTUs related to green algae chloroplasts (Chlorophyta). There seems to be a strong relationship between the Bacillariophyta phylum and our bleached coral samples as clones related to members of the diatom genera Amphora and Nitzschia were detected. The present study reveals information from a poorly investigated coral species and improves the knowledge of coral microbial community shifts that could occur during bleaching episodes.     

Sediment and Turbidity Associated with Offshore Dredging Increase Coral Disease Prevalence on Nearby Reefs

In recent decades, coral reef ecosystems have declined to the extent that reefs are now threatened globally. While many water quality parameters have been proposed to contribute to reef declines, little evidence exists conclusively linking specific water quality parameters with increased disease prevalence in situ. Here we report evidence from in situ coral health surveys confirming that chronic exposure to dredging-associated sediment plumes significantly increase the prevalence of white syndromes, a devastating group of globally important coral diseases. Coral health surveys were conducted along a dredging-associated sediment plume gradient to assess the relationship between sedimentation, turbidity and coral health. Reefs exposed to the highest number of days under the sediment plume (296 to 347 days) had two-fold higher levels of disease, largely driven by a 2.5-fold increase in white syndromes, and a six-fold increase in other signs of compromised coral health relative to reefs with little or no plume exposure (0 to 9 days). Multivariate modeling and ordination incorporating sediment exposure level, coral community composition and cover, predation and multiple thermal stress indices provided further confirmation that sediment plume exposure level was the main driver of elevated disease and other compromised coral health indicators. This study provides the first evidence linking dredging-associated sedimentation and turbidity with elevated coral disease prevalence in situ. Our results may help to explain observed increases in global coral disease prevalence in recent decades and suggest that minimizing sedimentation and turbidity associated with coastal development will provide an important management tool for controlling coral disease epizootics.