Ernesto Weil

Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005

Background The rising temperature of the worlds oceans has become a major threat to coral reefs globally as the severity and frequency of mass coral bleaching and mortality events increase. In 2005, high ocean temperatures in the tropical Atlantic and Caribbean resulted in the most severe bleaching event ever recorded in the basin. Methodology/Principal Findings Satellite-based tools provided warnings for coral reef managers and scientists, guiding both the timing and location of researchers field observations as anomalously warm conditions developed and spread across the greater Caribbean region from June to October 2005. Field surveys of bleaching and mortality exceeded prior efforts in detail and extent, and provided a new standard for documenting the effects of bleaching and for testing nowcast and forecast products. Collaborators from 22 countries undertook the most comprehensive documentation of basin-scale bleaching to date and found that over 80% of corals bleached and over 40% died at many sites. The most severe bleaching coincided with waters nearest a western Atlantic warm pool that was centered off the northern end of the Lesser Antilles. Conclusions/Significance Thermal stress during the 2005 event exceeded any observed from the Caribbean in the prior 20 years, and regionally-averaged temperatures were the warmest in over 150 years. Comparison of satellite data against field surveys demonstrated a significant predictive relationship between accumulated heat stress (measured using NOAA Coral Reef Watchs Degree Heating Weeks) and bleaching intensity. This severe, widespread bleaching and mortality will undoubtedly have long-term consequences for reef ecosystems and suggests a troubled future for tropical marine ecosystems under a warming climate.

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.

Geomorphology and benthic cover of mesophotic coral ecosystems of the upper insular slope of southwest Puerto Rico

The upper insular slope of southwest Puerto Rico is defined as extending from the shelf break at ~20xa0m water depth down to a depth of ~160xa0m where there is a pronounced change in geomorphic character and the basal slope begins. The upper slope is divided into two geomorphic zones separated by a pronounced break in slope gradient at ~90xa0m water depth. Descending from the shelf break, these are Zone I (20–90xa0m) and Zone II (90–160xa0m). As orientation of the shelf margin changes, geomorphology of Zone I shows systematic variations consistent with changes in exposure to prevailing waves. Within Zone I, exposed southeast-facing slopes have a gentler gradient and lower relief than more sheltered southwest-facing slopes, which are steep and irregular. Mesophotic coral ecosystems (MCEs) are largely restricted to Zone I and concentrated on topographic highs removed from the influence of active downslope sediment transport. Accordingly, MCEs are more abundant, extensive and diverse on southwest-facing slopes where irregular topography funnels downslope sediment transport into steep narrow grooves. MCEs are more sporadic and widely spaced on southeast-facing slopes where topographic highs are more widely spaced and downslope sediment transport is spread over open, low-relief slopes inhibiting coral recruitment and growth. Relict features formed during preexisting sea levels lower than present include deep buttresses at ~45–65xa0m water depth and a prominent terrace at ~80xa0m. Based on correlations with existing reef accretion and sea-level records, it is proposed that the 80-m terrace formed during the last deglaciation ~14–15xa0ka and subsequently drowned during a period of rapid sea-level rise associated with meltwater pulse 1A at ~14xa0ka and deep buttresses at ~45–65xa0m formed between ~11.5 and 13.5xa0ka and then drowned during a period of rapid sea-level rise associated with meltwater pulse 1B at ~11.3xa0ka.

RNA-Seq of the Caribbean reef-building coral Orbicella faveolata (Scleractinia-Merulinidae) under bleaching and disease stress expands models of coral innate immunity.

Climate change-driven coral disease outbreaks have led to widespread declines in coral populations. Early work on coral genomics established that corals have a complex innate immune system, and whole-transcriptome gene expression studies have revealed mechanisms by which the coral immune system responds to stress and disease. The present investigation expands bioinformatic data available to study coral molecular physiology through the assembly and annotation of a reference transcriptome of the Caribbean reef-building coral, Orbicella faveolata. Samples were collected during a warm water thermal anomaly, coral bleaching event and Caribbean yellow band disease outbreak in 2010 in Puerto Rico. Multiplex sequencing of RNA on the Illumina GAIIx platform and de novo transcriptome assembly by Trinity produced 70,745,177 raw short-sequence reads and 32,463 O. faveolata transcripts, respectively. The reference transcriptome was annotated with gene ontologies, mapped to KEGG pathways, and a predicted proteome of 20,488 sequences was generated. Protein families and signaling pathways that are essential in the regulation of innate immunity across Phyla were investigated in-depth. Results were used to develop models of evolutionarily conserved Wnt, Notch, Rig-like receptor, Nod-like receptor, and Dicer signaling. O. faveolata is a coral species that has been studied widely under climate-driven stress and disease, and the present investigation provides new data on the genes that putatively regulate its immune system.

Caribbean-wide, long-term study of seagrass beds reveals local variations, shifts in community structure and occasional collapse.

The CARICOMP monitoring network gathered standardized data from 52 seagrass sampling stations at 22 sites (mostly Thalassia testudinum-dominated beds in reef systems) across the Wider Caribbean twice a year over the period 1993 to 2007 (and in some cases up to 2012). Wide variations in community total biomass (285 to >2000 g dry m−2) and annual foliar productivity of the dominant seagrass T. testudinum (<200 and >2000 g dry m−2) were found among sites. Solar-cycle related intra-annual variations in T. testudinum leaf productivity were detected at latitudes > 16°N. Hurricanes had little to no long-term effects on these well-developed seagrass communities, except for 1 station, where the vegetation was lost by burial below ∼1 m sand. At two sites (5 stations), the seagrass beds collapsed due to excessive grazing by turtles or sea-urchins (the latter in combination with human impact and storms). The low-cost methods of this regional-scale monitoring program were sufficient to detect long-term shifts in the communities, and fifteen (43%) out of 35 long-term monitoring stations (at 17 sites) showed trends in seagrass communities consistent with expected changes under environmental deterioration.

Metatranscriptome analysis of the reef-building coral Orbicella faveolata indicates holobiont response to coral disease

White Plague Disease (WPD) is implicated in coral reef decline in the Caribbean and is characterized by microbial community shifts in coral mucus and tissue. Studies thus far have focused on assessing microbial communities or the identification of specific pathogens, yet few have addressed holobiont response across metaorganism compartments in coral disease. Here, we report on the first metatranscriptomic assessment of the coral host, algal symbiont, and microbial compartment in order to survey holobiont structure and function in healthy and diseased samples from Orbicella faveolata collected at reef sites off Puerto Rico. Our data indicate metaorganism-wide as well as compartment-specific responses to WPD. Gene expression changes in the diseased coral host involved proteins playing a role in innate immunity, cytoskeletal integrity, cell adhesion, oxidative stress, chemical defense, and retroelements. In contrast, the algal symbiont showed comparatively few expression changes, but of large magnitude, of genes related to stress, photosynthesis, and metal transport. Concordant with the coral host response, the bacterial compartment showed increased abundance of heat shock proteins, genes related to oxidative stress, DNA repair, and potential retroelement activity. Importantly, analysis of the expressed bacterial gene functions establishes the participation of multiple bacterial families in WPD pathogenesis and also suggests a possible involvement of viruses and/or phages in structuring the bacterial assemblage. In this study, we implement an experimental approach to partition the coral holobiont and resolve compartment- and taxa-specific responses in order to understand metaorganism function in coral disease.

Hyperspectral Sensing of Disease Stress in the Caribbean Reef-Building Coral, Orbicella faveolata - Perspectives for the Field of Coral Disease Monitoring

The effectiveness of management plans developed for responding to coral disease outbreaks is limited due to the lack of rapid methods of disease diagnosis. In order to fulfill current management guidelines for responding to coral disease outbreaks, alternative methods that significantly reduce response time must be developed. Hyperspectral sensing has been used by various groups to characterize the spectral signatures unique to asymptomatic and bleached corals. The 2010 combined bleaching and Caribbean yellow band disease outbreak in Puerto Rico provided a unique opportunity to investigate the spectral signatures associated with bleached and Caribbean yellow band-diseased colonies of Orbicella faveolata for the first time. Using derivative and cluster analyses of hyperspectral reflectance data, the present study demonstrates the proof of concept that spectral signatures can be used to differentiate between coral disease states. This method enhanced predominant visual methods of diagnosis by distinguishing between different asymptomatic conditions that are identical in field observations and photographic records. The ability to identify disease-affected tissue before lesions become visible could greatly reduce response times to coral disease outbreaks in monitoring efforts. Finally, spectral signatures associated with the poorly understood Caribbean yellow band disease are presented to guide future research on the role of pigments in the etiology.

Associations between transcriptional changes and protein phenotypes provide insights into immune regulation in corals

Disease outbreaks in marine ecosystems have driven worldwide declines of numerous taxa, including corals. Some corals, such as Orbicella faveolata, are particularly susceptible to disease. To explore the mechanisms contributing to susceptibility, colonies of O.xa0faveolata were exposed to immune challenge with lipopolysaccharides. RNA sequencing and protein activity assays were used to characterize the response of corals to immune challenge. Differential expression analyses identified 17 immune-related transcripts that varied in expression post-immune challenge. Network analyses revealed several groups of transcripts correlated to immune protein activity. Several transcripts, which were annotated as positive regulators of immunity were included in these groups, and some were downregulated following immune challenge. Correlations between expression of these transcripts and protein activity results further supported the role of these transcripts in positive regulation of immunity. The observed pattern of gene expression and protein activity may elucidate the processes contributing to the disease susceptibility of species like O.xa0faveolata.

Morphological and genetic evaluation of the hydrocoral Millepora species complex in the Caribbean

BackgroundThe hydrocoral Millepora is an important framework builder that dominates shallow turbulent environments in the Indo-Pacific and the Atlantic-Caribbean. The Caribbean representatives of the genus are classified in four species - Millepora alcicornis, Millepora complanata, Millepora striata, and Millepora squarrosa - but their taxonomic boundaries are not clearly defined. We used mitochondrial gene sequences to delineate the four Millepora species and evaluated whether morphological traits and mitochondrial sequence divergence were correlated for two most common species M. alcicornis and M. complanata.ResultsSamples were collected from Puerto Rico, Guadeloupe, Curaçao, Grand Cayman, and Panama during 2006 to 2007. Diameter of dactylopores distinguished the branching and encrusting morphotypes of M. alcicornis and M. complanata, and gastropore diameter discriminated between M. alcicornis and M. complanata. High levels of haplotypic diversity (Hdu2009=u20090.94) were observed, with the most common haplotypes shared by M. alcicornis and M. complanata. Sequence divergence ranged from 0% to 3% among M. alcicornis, M. complanata, and M. striata to 25% between these three species and M. squarrosa. Bayesian analysis of cytochrome oxidase subunit I (COI) gene indicated the presence of three Caribbean taxa: M. squarrosa, M. striata, and the species complex’ encompassing the morphologies displayed by M. complanata and M. alcicornis.ConclusionsThe branched M. alcicornis and encrusted M. alcicornis and M. complanata can be differentiated morphologically but not genetically. Phylogenetic analysis suggests that the Caribbean milleporids include three species - M. squarrosa, M. striata, and the species complex of M. alcicornis-M. complanata. Millepora striata is closely related to the M. alcicornis-M. complanata species complex.

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.