Climate and the latitudinal limits of subtropical reef development.

Climate plays a central role in coral-reef development, especially in marginal environments. The high-latitude reefs of southeast Florida are currently non-accreting, relict systems with low coral cover. This region also did not support the extensive Late Pleistocene reef development observed in many other locations around the world; however, there is evidence of significant reef building in southeast Florida during the Holocene. Using 146 radiometric ages from reefs extending ~ 120 km along Florida's southeast coast, we test the hypothesis that the latitudinal extent of Holocene reef development in this region was modulated by climatic variability. We demonstrate that although sea-level changes impacted rates of reef accretion and allowed reefs to backstep inshore as new habitats were flooded, sea level was not the ultimate cause of reef demise. Instead, we conclude that climate was the primary driver of the expansion and contraction of Florida's reefs during the Holocene. Reefs grew to 26.7° N in southeast Florida during the relatively warm, stable climate at the beginning of the Holocene Thermal Maximum (HTM) ~ 10,000 years ago, but subsequent cooling and increased frequency of winter cold fronts were associated with the equatorward contraction of reef building. By ~ 7800 years ago, actively accreting reefs only extended to 26.1° N. Reefs further contracted to 25.8° N after 5800 years ago, and by 3000 years ago reef development had terminated throughout southern Florida (24.5-26.7° N). Modern warming is unlikely to simply reverse this trend, however, because the climate of the Anthropocene will be fundamentally different from the HTM. By increasing the frequency and intensity of both warm and cold extreme-weather events, contemporary climate change will instead amplify conditions inimical to reef development in marginal reef environments such as southern Florida, making them more likely to continue to deteriorate than to resume accretion in the future.

The timing and causality of ecological shifts on Caribbean reefs.

Caribbean reefs have experienced unprecedented changes in the past four decades. Of great concern is the perceived widespread shift from coral to macroalgal dominance and the question of whether it represents a new, stable equilibrium for coral-reef communities. The primary causes of the shift-grazing pressure (top-down), nutrient loading (bottom-up) or direct coral mortality (side-in)-still remain somewhat controversial in the coral-reef literature. We have attempted to tease out the relative importance of each of these causes. Four insights emerge from our analysis of an early regional dataset of information on the benthic composition of Caribbean reefs spanning the years 1977-2001. First, although three-quarters of reef sites have experienced coral declines concomitant with macroalgal increases, fewer than 10% of the more than 200 sites studied were dominated by macroalgae in 2001, by even the most conservative definition of dominance. Using relative dominance as the threshold, a total of 49 coral-to-macroalgae shifts were detected. This total represents ~35% of all sites that were dominated by coral at the start of their monitoring periods. Four shifts (8.2%) occurred because of coral loss with no change in macroalgal cover, 15 (30.6%) occurred because of macroalgal gain without coral loss, and 30 (61.2%) occurred owing to concomitant coral decline and macroalgal increase. Second, the timing of shifts at the regional scale is most consistent with the side-in model of reef degradation, which invokes coral mortality as a precursor to macroalgal takeover, because more shifts occurred after regional coral-mortality events than expected by chance. Third, instantaneous observations taken at the start and end of the time-series for individual sites showed these reefs existed along a continuum of coral and macroalgal cover. The continuous, broadly negative relationship between coral and macroalgal cover suggests that in some cases coral-to-macroalgae phase shifts may be reversed by removing sources of perturbation or restoring critical components such as the herbivorous sea urchin Diadema antillarum to the system. The five instances in which macroalgal dominance was reversed corroborate the conclusion that macroalgal dominance is not a stable, alternative community state as has been commonly assumed. Fourth, the fact that the loss in regional coral cover and concomitant changes to the benthic community are related to punctuated, discrete events with known causes (i.e. coral disease and bleaching), lends credence to the hypothesis that coral reefs of the Caribbean have been under assault from climate-change-related maladies since the 1970s.

Survivorship and growth in staghorn coral (Acropora cervicornis) outplanting projects in the Florida Keys National Marine Sanctuary.

Significant population declines in Acropora cervicornis and A. palmata began in the 1970s and now exceed over 90%. The losses were caused by a combination of coral disease and bleaching, with possible contributions from other stressors, including pollution and predation. Reproduction in the wild by fragment regeneration and sexual recruitment is inadequate to offset population declines. Starting in 2007, the Coral Restoration Foundation™ evaluated the feasibility of outplanting A. cervicornis colonies to reefs in the Florida Keys to restore populations at sites where the species was previously abundant. Reported here are the results of 20 coral outplanting projects with each project defined as a cohort of colonies outplanted at the same time and location. Photogrammetric analysis and in situ monitoring (2007 to 2015) measured survivorship, growth, and condition of 2419 colonies. Survivorship was initially high but generally decreased after two years. Survivorship among projects based on colony counts ranged from 4% to 89% for seven cohorts monitored at least five years. Weibull survival models were used to estimate survivorship beyond the duration of the projects and ranged from approximately 0% to over 35% after five years and 0% to 10% after seven years. Growth rate averaged 10 cm/year during the first two years then plateaued in subsequent years. After four years, approximately one-third of surviving colonies were ≥ 50 cm in maximum diameter. Projects used three to sixteen different genotypes and significant differences did not occur in survivorship, condition, or growth. Restoration times for three reefs were calculated based on NOAA Recovery Plan (NRP) metrics (colony abundance and size) and the findings from projects reported here. Results support NRP conclusions that reducing stressors is required before significant population growth and recovery will occur. Until then, outplanting protects against local extinction and helps to maintain genetic diversity in the wild.

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.

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.

Coral reef baselines: how much macroalgae is natural?

Identifying the baseline or natural state of an ecosystem is a critical step in effective conservation and restoration. Like most marine ecosystems, coral reefs are being degraded by human activities: corals and fish have declined in abundance and seaweeds, or macroalgae, have become more prevalent. The challenge for resource managers is to reverse these trends, but by how much? Based on surveys of Caribbean reefs in the 1970s, some reef scientists believe that the average cover of seaweed was very low in the natural state: perhaps less than 3%. On the other hand, evidence from remote Pacific reefs, ecological theory, and impacts of over-harvesting in other systems all suggest that, historically, macroalgal biomass may have been higher than assumed. Uncertainties about the natural state of coral reefs illustrate the difficulty of determining the baseline condition of even well studied systems.

Is Jamaica a good model for understanding Caribbean coral reef dynamics?

Caribbean reefs have experienced unprecedented changes in the past 40 years. A major hypothesis to explain shifts in reef community composition relates to declining herbivory. This hypothesis was developed largely based on observations of Jamaican reefs from the 1980s onward, but it is widely held to be relevant regionally. We use a region-wide dataset on benthic composition to examine how well the pattern of ecological change on Jamaican reefs is mirrored by other Caribbean reefs. The extent to which macroalgal cover exceeds coral cover on Jamaican reefs is an order of magnitude more extreme than seen elsewhere. We suggest that Jamaican reefs are not representative of the degradation trajectory of Caribbean reefs and management based on the Jamaican experience may not be relevant elsewhere. However, the recovery of Jamaican reefs following the return of urchins gives us hope that Caribbean reefs are more resilient to catastrophic disturbances than previously thought.

Native predators do not influence invasion success of pacific lionfish on Caribbean reefs.

Biotic resistance, the process by which new colonists are excluded from a community by predation from and/or competition with resident species, can prevent or limit species invasions. We examined whether biotic resistance by native predators on Caribbean coral reefs has influenced the invasion success of red lionfishes (Pterois volitans and Pterois miles), piscivores from the Indo-Pacific. Specifically, we surveyed the abundance (density and biomass) of lionfish and native predatory fishes that could interact with lionfish (either through predation or competition) on 71 reefs in three biogeographic regions of the Caribbean. We recorded protection status of the reefs, and abiotic variables including depth, habitat type, and wind/wave exposure at each site. We found no relationship between the density or biomass of lionfish and that of native predators. However, lionfish densities were significantly lower on windward sites, potentially because of habitat preferences, and in marine protected areas, most likely because of ongoing removal efforts by reserve managers. Our results suggest that interactions with native predators do not influence the colonization or post-establishment population density of invasive lionfish on Caribbean reefs.

Catastrophe and the life span of coral reefs.

A strong earthquake in the western Caribbean in 2009 had a catastrophic impact on uncemented, unconsolidated coral reefs in the central sector of the shelf lagoon of the Belizean barrier reef. In a set of 21 reef sites that had been observed prior to the earthquake, the benthic assemblages of 10 were eradicated, and one was partially damaged, by avalanching of their slopes. Ecological dynamics that had played out over the previous 23 years, including the mass mortalities of two sequentially dominant coral species and a large increase in the cover of an encrusting sponge, were instantaneously rendered moot in the areas of catastrophic reef-slope failure. Because these prior dynamics also determined the benthic composition and resilience of adjacent sections of reef that remained intact, the history of disturbance prior to the earthquake will strongly influence decadal-scale recovery in the failed areas. Geological analysis of the reef framework yielded a minimum return time of 2000-4000 years for this type of high-amplitude event. Anthropogenic degradation of ecosystems must be viewed against the backdrop of long-period, natural catastrophes, such as the impact of strong earthquakes on uncemented, lagoonal reefs.

Severe 2010 cold-water event caused unprecedented mortality to corals of the Florida reef tract and reversed previous survivorship patterns.

BACKGROUND: Coral 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 FINDINGS: Reef 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/SIGNIFICANCE: The 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.

Changing patterns of microhabitat utilization by the threespot damselfish, Stegastes planifrons, on Caribbean reefs.

BACKGROUND: The threespot damselfish, Stegastes planifrons (Cuvier), is important in mediating interactions among corals, algae, and herbivores on Caribbean coral reefs. The preferred microhabitat of S. planifrons is thickets of the branching staghorn coral Acropora cervicornis. Within the past few decades, mass mortality of A. cervicornis from white-band disease and other factors has rendered this coral a minor ecological component throughout most of its range. METHODOLOGY/PRINCIPAL FINDINGS: Survey data from Jamaica (heavily fished), Florida and the Bahamas (moderately fished), the Cayman Islands (lightly to moderately fished), and Belize (lightly fished) indicate that distributional patterns of S. planifrons are positively correlated with live coral cover and topographic complexity. Our results suggest that species-specific microhabitat preferences and the availability of topographically complex microhabitats are more important than the abundance of predatory fish as proximal controls on S. planifrons distribution and abundance. CONCLUSIONS/SIGNIFICANCE: The loss of the primary microhabitat of S. planifrons-A. cervicornis-has forced a shift in the distribution and recruitment of these damselfish onto remaining high-structured corals, especially the Montastraea annularis species complex, affecting coral mortality and algal dynamics throughout the Caribbean.

Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs.

Many marine scientists have concluded that coral reefs are moving toward or are locked into a seaweed-dominated state. However, because there have been no regional- or global-scale analyses of such coral reef "phase shifts," the magnitude of this phenomenon was unknown. We analyzed 3581 quantitative surveys of 1851 reefs performed between 1996 and 2006 to determine the frequency, geographical extent, and degree of macroalgal dominance of coral reefs and of coral to macroalgal phase shifts around the world. Our results indicate that the replacement of corals by macroalgae as the dominant benthic functional group is less common and less geographically extensive than assumed. Although we found evidence of moderate local increases in macroalgal cover, particularly in the Caribbean, only 4% of reefs were dominated by macroalgae (i.e., > 50% cover). Across the Indo-Pacific, where regional averages of macroalgal cover were 9-12%, macroalgae only dominated 1% of the surveyed reefs. Between 1996 and 2006, phase shift severity decreased in the Caribbean, did not change in the Florida Keys and Indo-Pacific, and increased slightly on the Great Barrier Reef due to moderate coral loss. Coral reef ecosystems appear to be more resistant to macroalgal blooms than assumed, which has important implications for reef management.

One-third of reef-building corals face elevated extinction risk from climate change and local impacts.

The conservation status of 845 zooxanthellate reef-building coral species was assessed by using International Union for Conservation of Nature Red List Criteria. Of the 704 species that could be assigned conservation status, 32.8% are in categories with elevated risk of extinction. Declines in abundance are associated with bleaching and diseases driven by elevated sea surface temperatures, with extinction risk further exacerbated by local-scale anthropogenic disturbances. The proportion of corals threatened with extinction has increased dramatically in recent decades and exceeds that of most terrestrial groups. The Caribbean has the largest proportion of corals in high extinction risk categories, whereas the Coral Triangle (western Pacific) has the highest proportion of species in all categories of elevated extinction risk. Our results emphasize the widespread plight of coral reefs and the urgent need to enact conservation measures.