BackgroundCoral reefs are facing increasing pressure from natural and anthropogenic stressors that have already caused significant worldwide declines. In January 2010, coral reefs of Florida, United States, were impacted by an extreme cold-water anomaly that exposed corals to temperatures well below their reported thresholds (16°C), causing rapid coral mortality unprecedented in spatial extent and severity.Methodology/Principal FindingsReef surveys were conducted from Martin County to the Lower Florida Keys within weeks of the anomaly. The impacts recorded were catastrophic and exceeded those of any previous disturbances in the region. Coral mortality patterns were directly correlated to in-situ and satellite-derived cold-temperature metrics. These impacts rival, in spatial extent and intensity, the impacts of the well-publicized warm-water bleaching events around the globe. The mean percent coral mortality recorded for all species and subregions was 11.5% in the 2010 winter, compared to 0.5% recorded in the previous five summers, including years like 2005 where warm-water bleaching was prevalent. Highest mean mortality (15%–39%) was documented for inshore habitats where temperatures were <11°C for prolonged periods. Increases in mortality from previous years were significant for 21 of 25 coral species, and were 1–2 orders of magnitude higher for most species.Conclusions/SignificanceThe cold-water anomaly of January 2010 caused the worst coral mortality on record for the Florida Reef Tract, highlighting the potential catastrophic impacts that unusual but extreme climatic events can have on the persistence of coral reefs. Moreover, habitats and species most severely affected were those found in high-coral cover, inshore, shallow reef habitats previously considered the “oases” of the region, having escaped declining patterns observed for more offshore habitats. Thus, the 2010 cold-water anomaly not only caused widespread coral mortality but also reversed prior resistance and resilience patterns that will take decades to recover.

Samples from eight species of corals (Colpophyllia natans, Dendrogyra cylindrus, Diploria labyrinthiformis, Meandrina meandrites, Montastraea cavernosa, Orbicella faveolata, Pseudodiploria strigosa, and Siderastrea siderea) that exhibited gross clinical signs of acute, subacute, or chronic tissue loss attributed to stony coral tissue loss disease (SCTLD) were collected from the Florida Reef Tract during 2016–2018 and examined histopathologically. The hallmark microscopic lesion seen in all eight species was focal to multifocal lytic necrosis (LN) originating in the gastrodermis of the basal body wall (BBW) and extending to the calicodermis, with more advanced lesions involving the surface body wall. This was accompanied by other degenerative changes in host cells such as mucocyte hypertrophy, degradation and fragmentation of gastrodermal architecture, and disintegration of the mesoglea. Zooxanthellae manifested various changes including necrosis (cytoplasmic hypereosinophilia, pyknosis); peripheral nuclear chromatin condensation; cytoplasmic vacuolation accompanied by deformation, swelling, or atrophy; swollen accumulation bodies; prominent pyrenoids; and degraded chloroplasts. Polyhedral intracytoplasmic eosinophilic periodic acid–Schiff-positive crystalline inclusion bodies (∼1–10 μm in length) were seen only in M. cavernosa and P. strigosa BBW gastrodermis in or adjacent to active lesions and some unaffected areas (without surface lesions) of diseased colonies. Coccoidlike or coccobacilloidlike structures (Gram-neutral) reminiscent of microorganisms were occasionally associated with LN lesions or seen in apparently healthy tissue of diseased colonies along with various parasites and other bacteria all considered likely secondary colonizers. Of the 82 samples showing gross lesions of SCTLD, 71 (87%) were confirmed histologically to have LN. Collectively, pathology indicates that SCTLD is the result of a disruption of host–symbiont physiology with lesions originating in the BBW leading to detachment and sloughing of tissues from the skeleton. Future investigations could focus on identifying the cause and pathogenesis of this process.

No abstract

The rapid loss of reef-building corals owing to ocean warming is driving the development of interventions such as coral propagation and restoration, selective breeding and assisted gene flow. Many of these interventions target naturally heat-tolerant individuals to boost climate resilience, but the challenges of quickly and reliably quantifying heat tolerance and identifying thermotolerant individuals have hampered implementation. Here, we used coral bleaching automated stress systems to perform rapid, standardized heat tolerance assays on 229 colonies of Acropora cervicornis across six coral nurseries spanning Florida's Coral Reef, USA. Analysis of heat stress dose–response curves for each colony revealed a broad range in thermal tolerance among individuals (approx. 2.5°C range in F v /F m ED50), with highly reproducible rankings across independent tests ( r = 0.76). Most phenotypic variation occurred within nurseries rather than between them, pointing to a potentially dominant role of fixed genetic effects in setting thermal tolerance and widespread distribution of tolerant individuals throughout the population. The identification of tolerant individuals provides immediately actionable information to optimize nursery and restoration programmes for Florida's threatened staghorn corals. This work further provides a blueprint for future efforts to identify and source thermally tolerant corals for conservation interventions worldwide.

Along the Florida reef tract, stony-coral-tissue-loss disease (SCTLD) has caused extensive mortality of more than 20 scleractinian coral species. The pathogen is unknown, but its epizoology indicates that the disease, facilitated by water currents, has progressed linearly along the tract, affecting reefs at the scale of hundreds of kilometers. To inform ongoing disease mitigation efforts, we examined the small-scale spatial and temporal epidemiology of SCTLD. We established a series of sites in the middle Florida Keys at offshore and inshore locations that had not yet shown signs of SCTLD. We then conducted high-frequency monitoring from February 2018 through September 2019 and documented the onset of SCTLD and its progression through the sites. SCTLD was first observed at one site during early February 2018 and by early March 2018 all sites showed signs of the disease. A dynamic multistate model suggested that disease transmission was independent of coral density and found little evidence of a positive association between a colony showing signs of SCTLD and the condition or distance to its neighboring colonies. The model did, however, indicate that the probability of a colony showing signs of SCTLD increased with increasing colony surface area. These results are consistent with the water-borne transmission of a pathogen that progressed rapidly through the survey area. However, by the end of our survey the progression of SCTLD had slowed, particularly at inshore sites. Many affected colonies no longer exhibited progressive tissue mortality typical of the disease, suggesting the existence of differentially resilient colonies or coral communities, meriting their use for future coral rescue and propagation and disease research. These results are useful for refining ongoing SCTLD mitigation strategies, particularly by determining when disease rates are sufficiently low for direct intervention efforts designed to arrest disease progression on individual coral colonies will be most effective.