Severe hurricanes increase recruitment and gene flow in the clonal sponge Aplysina cauliformis.

Upright branching sponges, such as Aplysina cauliformis, provide critical three-dimensional habitat for other organisms and assist in stabilizing coral reef substrata, but are highly susceptible to breakage during storms. Breakage can increase sponge fragmentation, contributing to population clonality and inbreeding. Conversely, storms could provide opportunities for new genotypes to enter populations via larval recruitment, resulting in greater genetic diversity in locations with frequent storms. The unprecedented occurrence of two Category 5 hurricanes in close succession during 2017 in the U.S. Virgin Islands (USVI) provided a unique opportunity to evaluate whether recolonization of newly available substrata on coral reefs was due to local (e.g. re-growth of remnants, fragmentation, larval recruitment) or remote (e.g. larval transport and immigration) sponge genotypes. We sampled A. cauliformis adults and juveniles from four reefs around St. Thomas and two in St. Croix (USVI). Using a 2bRAD protocol, all samples were genotyped for single-nucleotide polymorphisms (SNPs). Results showed that these major storm events favoured sponge larval recruitment but did not increase the genetic diversity of A. cauliformis populations. Recolonization of substratum post-storms via clonality was lower (15%) than expected and instead was mainly due to sexual reproduction (85%) via local larval recruitment. Storms did enhance gene flow among and within reef sites located south of St. Thomas and north of St. Croix. Therefore, populations of clonal marine species with low pelagic dispersion, such as A. cauliformis, may benefit from increased frequency and magnitude of hurricanes for the maintenance of genetic diversity and to combat inbreeding, enhancing the resilience of Caribbean sponge communities to extreme storm events.

Stony coral tissue loss disease induces transcriptional signatures of in situ degradation of dysfunctional Symbiodiniaceae.

Stony coral tissue loss disease (SCTLD), one of the most pervasive and virulent coral diseases on record, affects over 22 species of reef-building coral and is decimating reefs throughout the Caribbean. To understand how different coral species and their algal symbionts (family Symbiodiniaceae) respond to this disease, we examine the gene expression profiles of colonies of five species of coral from a SCTLD transmission experiment. The included species vary in their purported susceptibilities to SCTLD, and we use this to inform gene expression analyses of both the coral animal and their Symbiodiniaceae. We identify orthologous coral genes exhibiting lineage-specific differences in expression that correlate to disease susceptibility, as well as genes that are differentially expressed in all coral species in response to SCTLD infection. We find that SCTLD infection induces increased expression of rab7, an established marker of in situ degradation of dysfunctional Symbiodiniaceae, in all coral species accompanied by genus-level shifts in Symbiodiniaceae photosystem and metabolism gene expression. Overall, our results indicate that SCTLD infection induces symbiophagy across coral species and that the severity of disease is influenced by Symbiodiniaceae identity.

A meta-analysis of the stony coral tissue loss disease microbiome finds key bacteria in unaffected and lesion tissue in diseased colonies.

Stony coral tissue loss disease (SCTLD) has been causing significant whole colony mortality on reefs in Florida and the Caribbean. The cause of SCTLD remains unknown, with the limited concurrence of SCTLD-associated bacteria among studies. We conducted a meta-analysis of 16S ribosomal RNA gene datasets generated by 16 field and laboratory SCTLD studies to find consistent bacteria associated with SCTLD across disease zones (vulnerable, endemic, and epidemic), coral species, coral compartments (mucus, tissue, and skeleton), and colony health states (apparently healthy colony tissue (AH), and unaffected (DU) and lesion (DL) tissue from diseased colonies). We also evaluated bacteria in seawater and sediment, which may be sources of SCTLD transmission. Although AH colonies in endemic and epidemic zones harbor bacteria associated with SCTLD lesions, and aquaria and field samples had distinct microbial compositions, there were still clear differences in the microbial composition among AH, DU, and DL in the combined dataset. Alpha-diversity between AH and DL was not different; however, DU showed increased alpha-diversity compared to AH, indicating that, prior to lesion formation, corals may undergo a disturbance to the microbiome. This disturbance may be driven by Flavobacteriales, which were especially enriched in DU. In DL, Rhodobacterales and Peptostreptococcales-Tissierellales were prominent in structuring microbial interactions. We also predict an enrichment of an alpha-toxin in DL samples which is typically found in Clostridia. We provide a consensus of SCTLD-associated bacteria prior to and during lesion formation and identify how these taxa vary across studies, coral species, coral compartments, seawater, and sediment.

Rapid prototyping for quantifying belief weights of competing hypotheses about emergent diseases.

Emerging diseases can have devastating consequences for wildlife and require a rapid response. A critical first step towards developing appropriate management is identifying the etiology of the disease, which can be difficult to determine, particularly early in emergence. Gathering and synthesizing existing information about potential disease causes, by leveraging expert knowledge or relevant existing studies, provides a principled approach to quickly inform decision-making and management efforts. Additionally, updating the current state of knowledge as more information becomes available over time can reduce scientific uncertainty and lead to substantial improvement in the decision-making process and the application of management actions that incorporate and adapt to newly acquired scientific understanding. Here we present a rapid prototyping method for quantifying belief weights for competing hypotheses about the etiology of disease using a combination of formal expert elicitation and Bayesian hierarchical modeling. We illustrate the application of this approach for investigating the etiology of stony coral tissue loss disease (SCTLD) and discuss the opportunities and challenges of this approach for addressing emergent diseases. Lastly, we detail how our work may apply to other pressing management or conservation problems that require quick responses. We found the rapid prototyping methods to be an efficient and rapid means to narrow down the number of potential hypotheses, synthesize current understanding, and help prioritize future studies and experiments. This approach is rapid by providing a snapshot assessment of the current state of knowledge. It can also be updated periodically (e.g., annually) to assess changes in belief weights over time as scientific understanding increases. Synthesis and applications: The rapid prototyping approaches demonstrated here can be used to combine knowledge from multiple experts and/or studies to help with fast decision-making needed for urgent conservation issues including emerging diseases and other management problems that require rapid responses. These approaches can also be used to adjust belief weights over time as studies and expert knowledge accumulate and can be a helpful tool for adapting management decisions.

Disease resistance in coral is mediated by distinct adaptive and plastic gene expression profiles.

Infectious diseases are an increasing threat to coral reefs, resulting in altered community structure and hindering the functional contributions of disease-susceptible species. We exposed seven reef-building coral species from the Caribbean to white plague disease and determined processes involved in (i) lesion progression, (ii) within-species gene expression plasticity, and (iii) expression-level adaptation among species that lead to differences in disease risk. Gene expression networks enriched in immune genes and cytoskeletal arrangement processes were correlated to lesion progression rates. Whether or not a coral developed a lesion was mediated by plasticity in genes involved in extracellular matrix maintenance, autophagy, and apoptosis, while resistant coral species had constitutively higher expression of intracellular protein trafficking. This study offers insight into the process involved in lesion progression and within- and between-species dynamics that lead to differences in disease risk that is evident on current Caribbean reefs.

Experimental transmission of Stony Coral Tissue Loss Disease results in differential microbial responses within coral mucus and tissue.

Stony coral tissue loss disease (SCTLD) is a widespread and deadly disease that affects nearly half of Caribbean coral species. To understand the microbial community response to this disease, we performed a disease transmission experiment on US Virgin Island (USVI) corals, exposing six species of coral with varying susceptibility to SCTLD. The microbial community of the surface mucus and tissue layers were examined separately using a small subunit ribosomal RNA gene-based sequencing approach, and data were analyzed to identify microbial community shifts following disease acquisition, potential causative pathogens, as well as compare microbiota composition to field-based corals from the USVI and Florida outbreaks. While all species displayed similar microbiome composition with disease acquisition, microbiome similarity patterns differed by both species and mucus or tissue microhabitat. Further, disease exposed but not lesioned corals harbored a mucus microbial community similar to those showing disease signs, suggesting that mucus may serve as an early warning detection for the onset of SCTLD. Like other SCTLD studies in Florida, Rhodobacteraceae, Arcobacteraceae, Desulfovibrionaceae, Peptostreptococcaceae, Fusibacter, Marinifilaceae, and Vibrionaceae dominated diseased corals. This study demonstrates the differential response of the mucus and tissue microorganisms to SCTLD and suggests that mucus microorganisms may be diagnostic for early disease exposure.

Investigating the roles of transforming growth factor-beta in immune response of Orbicella faveolata, a scleractinian coral.

Symbiotic relationships range from parasitic to mutualistic, yet all endosymbionts face similar challenges, including evasion of host immunity. Many symbiotic organisms have evolved similar mechanisms to face these challenges, including manipulation of the host's transforming growth factor-beta (TGFß) pathway. Here we investigate the TGFß pathway in scelaractinian corals which are dependent on symbioses with dinoflagellates from the family Symbiodiniaceae. Using the Caribbean coral, Orbicella faveolata, we explore the effects of enhancement and inhibition of the TGFß pathway on host gene expression. Following transcriptomic analyses, we demonstrated limited effects of pathway manipulation in absence of immune stimulation. However, manipulation of the TGFß pathway significantly affects the subsequent ability of host corals to mount an immune response. Enhancement of the TGFß pathway eliminates transcriptomic signatures of host coral immune response, while inhibition of the pathway maintains the response. This is, to our knowledge, the first evidence of an immunomodulatory role for TGFß in a scelaractinian coral. These findings suggest variation in TGFß signaling may have implications in the face of increasing disease prevelance. Our results suggest that the TGFß pathway can modulate tradeoffs between symbiosis and immunity. Further study of links between symbiosis, TGFß, and immunity is needed to better understand the ecological implications of these findings.

Depth and coral cover drive the distribution of a coral macroborer across two reef systems.

Bioerosion, the removal of calcium carbonate from coral frameworks by living organisms, influences a variety of reef features, from their topographic complexity to the net balance of carbonate budgets. Little is known, however, about how macroborers, which bore into reef substrates leaving traces greater than 0.1 mm diameter, are distributed across coral reefs, particularly reef systems with high (>50%) stony coral cover or at mesophotic depths (≥30 m). Here, we present an accurate and efficient method for quantifying macroborer densities from stony coral hosts via image analysis, using the bioeroding barnacle, Lithotrya dorsalis, and its host coral, Orbicella franksi, as a case study. We found that in 2014, L. dorsalis densities varied consistently with depth and host percent cover in two Atlantic reef systems: the Flower Garden Banks (FGB, northwest Gulf of Mexico) and the U.S. Virgin Islands (USVI). Although average barnacle density was nearly 4.5 times greater overall in the FGB than in the USVI, barnacle density decreased with depth in both reef regions. Barnacle density also scaled negatively with increasing coral cover in the study areas, suggesting that barnacle populations are not strictly space-limited in their distribution and settlement opportunities. Our findings suggest that depth and host coral cover, and potentially, local factors may strongly influence the abundance of macroborers, and thus the rate of CaCO3 loss, in a given reef system. Our image analysis method for quantifying macroborers can be standardized across historical and modern reef records to better understand how borers impact host growth and reef health.

Coral reef health response to chronic and acute changes in water quality in St. Thomas, United States Virgin Islands.

It is suspected that land cover alteration on the southern coast of St. Thomas, USVI has increased runoff, degrading nearshore water quality and coral reef health. Chronic and acute changes in water quality, sediment deposition, and coral health metrics were assessed in three zones based upon perceived degree of human influence. Chlorophyll (p<0.0001) and turbidity (p=0.0113) were significantly higher in nearshore zones and in the high impact zone during heavy precipitation. Net sediment deposition and terrigenous content increased in nearshore zones during periods of greater precipitation and port activity. Macroalgae overgrowth significantly increased along a gradient of decreasing water quality (p<0.0001). Coral bleaching in all zones peaked in November with a regional thermal stress event (p<0.0001). However, mean bleaching prevalence was significantly greater in the most impacted zone compared to the offshore zone (p=0.0396), suggesting a link between declining water quality and bleaching severity.

Seasonal Variability in Calorimetric Energy Content of Two Caribbean Mesophotic Corals.

Energetic responses of zooxanthellate reef corals along depth gradients have relevance to the refugia potential of mesophotic coral ecosystems (MCEs). Previous observations suggested that MCEs in the Caribbean are thermally buffered during the warmest parts of the year and occur within or just below the chlorophyll maximum, suggesting abundant trophic resources. However, it is not known if mesophotic corals can maintain constant energy needs throughout the year with changing environmental and biological conditions. The energetic content of tissues from the stony coral species Orbicella faveolata and Agaricia lamarcki was measured on the southern insular shelf of St. Thomas, US Virgin Islands (USVI), using micro-bomb calorimetry. Three sites for each species, at depths of 6m, 25m, 38m and 63m, were selected to capture energetic differences across the major vertical range extent of both species in the USVI-and sampled over five periods from April 2013 to April 2014. Mesophotic colonies of O. faveolata exhibited a significant reduction in energetic content during the month of September 2013 compared to mid-depth and shallow colonies (p = 0.032), whereas A. lamarcki experienced similar energetic variability, but with a significant reduction in energy content that occurred in July 2013 for colonies at sites deeper than 25m (p = 0.014). The results of calorimetric analyses indicate that O. faveolata may be at risk during late summer stress events, possibly due to the timing of reproductive activities. The low-point of A. lamarcki energy content, which may also coincide with reproduction, occurs prior to seasonal stress events, indicating contrasting, species-specific responses to environmental variability on MCEs.

Caribbean mesophotic coral ecosystems are unlikely climate change refugia.

Deeper coral reefs experience reduced temperatures and light and are often shielded from localized anthropogenic stressors such as pollution and fishing. The deep reef refugia hypothesis posits that light-dependent stony coral species at deeper depths are buffered from thermal stress and will avoid bleaching-related mass mortalities caused by increasing sea surface temperatures under climate change. This hypothesis has not been tested because data collection on deeper coral reefs is difficult. Here we show that deeper (mesophotic) reefs, 30-75 m depth, in the Caribbean are not refugia because they have lower bleaching threshold temperatures than shallow reefs. Over two thermal stress events, mesophotic reef bleaching was driven by a bleaching threshold that declines 0.26 °C every +10 m depth. Thus, the main premise of the deep reef refugia hypothesis that cooler environments are protective is incorrect; any increase in temperatures above the local mean warmest conditions can lead to thermal stress and bleaching. Thus, relatively cooler temperatures can no longer be considered a de facto refugium for corals and it is likely that many deeper coral reefs are as vulnerable to climate change as shallow water reefs.

Environmental conditions influence tissue regeneration rates in scleractinian corals.

Natural and anthropogenic factors may influence corals' ability to recover from partial mortality. To examine how environmental conditions affect lesion healing, we assessed several water quality parameters and tissue regeneration rates in corals at six reefs around St. Thomas, US Virgin Islands. We hypothesized that sites closer to developed areas would have poor water quality due to proximity to anthropogenic stresses, which would impede tissue regeneration. We found that water flow and turbidity most strongly influenced lesion recovery rates. The most impacted site, with high turbidity and low flow, recovered almost three times slower than the least impacted site, with low turbidity, high flow, and low levels of anthropogenic disturbance. Our results illustrate that in addition to lesion-specific factors known to affect tissue regeneration, environmental conditions can also control corals' healing rates. Resource managers can use this information to protect low-flow, turbid nearshore reefs by minimizing sources of anthropogenic stress.

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.

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.

Disease incidence is related to bleaching extent in reef-building corals.

Recent outbreaks of coral bleaching and disease have contributed to substantial declines in the abundance of reef-building coral. Significant attention has been paid to both phenomena in order to determine their effect on reef trajectories. Although each is positively correlated with high temperatures, few studies have explored the potential links between bleaching and disease. A longitudinal study of corals in the Florida Keys was therefore conducted during the 2005 Caribbean bleaching event to quantify bleaching extent and disease incidence in corals, and to determine whether they were related or if they acted as discrete phenomena. These data indicated that overall, a positive correlation exists between bleaching extent and disease incidence. However, the specific interactions between these two phenomena varied among disease bleaching combinations. Montastraea faveolata colonies with greater bleaching intensities later developed white plague (WP) infections. Meanwhile, Siderastrea siderea colonies with dark spot disease (DS) bleached more extensively than apparently healthy colonies. Finally, bleaching and black band disease (BB) co-occurred on Colpophyllia natans throughout the bleaching event. WP, BB, and bleaching are each independently capable of changing the structure of coral populations through loss of living tissue, and DS is an important indicator of reef health. Understanding the dynamics of how these mortality sources interact is critical to understanding mortality patterns and predicting how reef communities will respond to future events.

Dynamics and impact of the coral disease white plague: insights from a simulation model.

Coral disease is playing a significant role in structuring today's coral reef communities. While monitoring programs document declines associated with coral disease, there is a lack of tools that can test hypotheses of disease incidence and control. Here, we describe a modeling tool developed to test hypotheses about the spread and impact of white plague disease in diverse coral populations distributed across heterogeneous reef landscapes. The model Simulation of Infected Corals (SICO) was based on the dynamics of white plague over the course of 6 yr of monitoring on the fore-reefs of Little Cayman (Cayman Islands, British West Indies). A pattern-oriented modeling approach using a genetic algorithm was used to calibrate model parameters that describe disease introduction, transmissibility, and host susceptibility. Simulation patterns most accurately reflected patterns observed at study sites when disease was introduced at regular intervals and was transmissible within a limited area. Projecting forward in time, coral cover tended to drop precipitously until colonies were so sparse that disease transmission among colonies was rare. A sensitivity analysis of disease parameters indicated that the effect of changing disease parameters depended on the type of coral community, but that in communities dominated by susceptible species, local preventative measures were generally more effective than treatment measures in limiting disease impact.