Ecology, histopathology, and microbial ecology of a white-band disease outbreak in the threatened staghorn coral Acropora cervicornis.

This study is a multi-pronged description of a temperature-induced outbreak of white-band disease (WBD) that occurred in Acropora cervicornis off northern Miami Beach, Florida (USA), from July to October 2014. We describe the ecology of the disease and examine diseased corals using both histopathology and next-generation bacterial 16S gene sequencing, making it possible to better understand the effect this disease has on the coral holobiont, and to address some of the seeming contradictions among previous studies of WBD that employed either a purely histological or molecular approach. The outbreak began in July 2014, as sea surface temperatures reached 29°C, and peaked in mid-September, a month after the sea surface temperature maximum. The microscopic anatomy of apparently healthy portions of colonies displaying active disease signs appeared normal except for some tissue atrophy and dissociation of mesenterial filaments deep within the branch. Structural changes were more pronounced in visibly diseased fragments, with atrophy, necrosis, and lysing of surface and basal body wall and polyp structures at the tissue-loss margin. The only bacteria evident microscopically in both diseased and apparently healthy tissues with Giemsa staining was a Rickettsiales-like organism (RLO) occupying mucocytes. Sequencing also identified bacteria belonging to the order Rickettsiales in all fragments. When compared to apparently healthy fragments, diseased fragments had more diverse bacterial communities made up of many previously suggested potential primary pathogens and secondary (opportunistic) colonizers. Interactions between elevated seawater temperatures, the coral host, and pathogenic members of the diseased microbiome all contribute to the coral displaying signs of WBD.

Regional coral disease outbreak overwhelms impacts from a local dredge project.

A repeated-measures coral monitoring program established as part of the PortMiami expansion program provided an unparalleled opportunity to quantify the levels of coral mortality that resulted from both local dredging stress and as a result of climate-related bleaching stress and the subsequent outbreak of a white-plague-like disease (WPD) epizootic. By comparing measured rates of coral mortality at 30 sites throughout Miami-Dade County to predicted mortality levels from three different coral mortality scenarios, we were able to evaluate the most likely source of coral mortality at both the local and regional levels during the 2014-2016 coral bleaching and WPD event. These include scenarios that assume (1) local dredging increases coral disease mortality, (2) regional climate-related stress is the proximal driver of coral disease mortality, and (3) local and regional stressors are both responsible for coral disease mortality. Our results show that species-specific susceptibility to disease is the determining factor in 93.3% of coral mortality evaluated throughout Miami-Dade County, whereas local dredging stress only accurately predicted coral mortality levels 6.7% of the time. None of the monitoring locations adjacent to the PortMiami expansion had levels of coral mortality that exceeded predictions when coral community composition was taken into account. The novel result of this analysis is that climate-mediated coral disease mortality was more than an order of magnitude (14x) more deadly than even the largest marine construction project performed in the USA, and that until climate change is addressed, it is likely that local attempts to manage coral resilience will continue to fail.

Clonal diversity impacts coral cover in Acropora cervicornisthickets: Potential relationships between density, growth, and polymorphisms.

As coral reefs decline, cryptic sources of resistance and resilience to stress may be increasingly important for the persistence of these communities. Among these sources, inter- and intraspecific diversity remain understudied on coral reefs but extensively impact a variety of traits in other ecosystems. We use a combination of field and sequencing data at two sites in Florida and two in the Dominican Republic to examine clonal diversity and genetic differentiation of high- and low-density aggregations of the threatened coral Acropora cervicornisin the Caribbean. We find that high-density aggregations called thickets are composed of up to 30 genotypes at a single site, but 47% of genotypes are also found as isolated, discrete colonies outside these aggregations. Genet-ramet ratios are comparable for thickets (0.636) and isolated colonies after rarefaction (0.569), suggesting the composition of each aggregation is not substantially different and highlighting interactions between colonies as a potential influence on structure. There are no differences in growth rate, but a significant positive correlation between genotypic diversity and coral cover, which may be due to the influence of interactions between colonies on survivorship or fragment retention during asexual reproduction. Many polymorphisms distinguish isolated colonies from thickets despite the shared genotypes found here, including putative nonsynonymous mutations that change amino acid sequence in 25 loci. These results highlight intraspecific diversity as a density-dependent factor that may impact traits important for the structure and function of coral reefs.

Unprecedented Disease-Related Coral Mortality in Southeastern Florida.

Anomalously high water temperatures, associated with climate change, are increasing the global prevalence of coral bleaching, coral diseases, and coral-mortality events. Coral bleaching and disease outbreaks are often inter-related phenomena, since many coral diseases are a consequence of opportunistic pathogens that further compromise thermally stressed colonies. Yet, most coral diseases have low prevalence (<5%), and are not considered contagious. By contrast, we document the impact of an extremely high-prevalence outbreak (61%) of white-plague disease at 14 sites off southeastern Florida. White-plague disease was observed near Virginia Key, Florida, in September 2014, and after 12 months had spread 100 km north and 30 km south. The disease outbreak directly followed a high temperature coral-bleaching event and affected at least 13 coral species. Eusmilia fastigiata, Meandrina meandrites, and Dichocoenia stokesi were the most heavily impacted coral species, and were reduced to <3% of their initial population densities. A number of other coral species, including Colpophyllia natans, Pseudodiploria strigosa, Diploria labyrinthiformis, and Orbicella annularis were reduced to <25% of their initial densities. The high prevalence of disease, the number of susceptible species, and the high mortality of corals affected suggests this disease outbreak is arguably one of the most lethal ever recorded on a contemporary coral reef.

Development and application of a video-mosaic survey technology to document the status of coral reef communities.

The recent decline in the condition of coral reef communities worldwide has fueled the need to develop innovative assessment tools to document coral abundance and distribution rapidly and effectively. While most monitoring programs rely primarily on data collected in situ by trained divers, digital photographs and video are used increasingly to extract ecological indicators, provide a permanent visual record of reef condition, and reduce the time that divers spend underwater. In this study, we describe the development and application of a video-based reef survey methodology based on an algorithm for image registration and the estimation of image motion and camera trajectory. This technology was used to construct two-dimensional, spatially accurate, high-resolution mosaics of the reef benthos at a scale of up to 400 m(2). The mosaics were analyzed to estimate the size and percent cover of reef organisms and these ecological indicators of reef condition were compared to similar measurements collected by divers to evaluate the potential of the mosaics as monitoring tools. The ecological indicators collected by trained divers compared favorably with those measured directly from the video mosaics. Five out of the eight categories chosen (hard corals, octocorals, Palythoa, algal turf, and sand) showed no significant differences in percent cover based on survey method. Moreover, no significant differences based on survey method were found in the size of coral colonies. Lastly, the capability to extract the same reef location from mosaics collected at different times proved to be an important tool for documenting change in coral abundance as the removal of even small colonies (<10 cm in diameter) was easily documented. The two-dimensional video mosaics constructed in this study can provide repeatable, accurate measurements on the reef-plot scale that can complement measurements on the colony-scale made by divers and surveys conducted at regional scales using remote sensing tools.