Millennia-old coral holobiont DNA provides insight into future adaptive trajectories.

Ancient DNA (aDNA) has been applied to evolutionary questions across a wide variety of taxa. Here, for the first time, we utilized aDNA from millennia-old fossil coral fragments to gain new insights into a rapidly declining western Atlantic reef ecosystem. We sampled four Acropora palmata fragments (dated 4215 BCE to 1099 CE) obtained from two Florida Keys reef cores. From these samples, we established that it is possible both to sequence aDNA from reef cores and place the data in the context of modern-day genetic variation. We recovered varying amounts of nuclear DNA exhibiting the characteristic signatures of aDNA from the A. palmata fragments. To describe the holobiont sensu lato, which plays a crucial role in reef health, we utilized metagenome-assembled genomes as a reference to identify a large additional proportion of ancient microbial DNA from the samples. The samples shared many common microbes with modern-day coral holobionts from the same region, suggesting remarkable holobiont stability over time. Despite efforts, we were unable to recover ancient Symbiodiniaceae reads from the samples. Comparing the ancient A. palmata data to whole-genome sequencing data from living acroporids, we found that while slightly distinct, ancient samples were most closely related to individuals of their own species. Together, these results provide a proof-of-principle showing that it is possible to carry out direct analysis of coral holobiont change over time, which lays a foundation for studying the impacts of environmental stress and evolutionary constraints.

The past, present, and future of coral reef growth in the Florida Keys.

Coral-reef degradation is driving global-scale reductions in reef-building capacity and the ecological, geological, and socioeconomic functions it supports. The persistence of those essential functions will depend on whether coral-reef management is able to rebalance the competing processes of reef accretion and erosion. Here, we reconstructed census-based carbonate budgets of 46 reefs throughout the Florida Keys from 1996 to 2019. We evaluated the environmental and ecological drivers of changing budget states and compared historical trends in reef-accretion potential to millennial-scale baselines of accretion from reef cores and future projections with coral restoration. We found that historically, most reefs had positive carbonate budgets, and many had reef-accretion potential comparable to the ~3 mm year-1 average accretion rate during the peak of regional reef building ~7000 years ago; however, declines in reef-building Acropora palmata and Orbicella spp. corals following a series of thermal stress events and coral disease outbreaks resulted in a shift from positive to negative budgets for most reefs in the region. By 2019, only ~15% of reefs had positive net carbonate production. Most of those reefs were in inshore, Lower Keys patch-reef habitats with low water clarity, supporting the hypothesis that environments with naturally low irradiance may provide a refugia from thermal stress. We caution that our estimated carbonate budgets are likely overly optimistic; comparison of reef-accretion potential to measured accretion from reef cores suggests that, by not accounting for the role of nonbiological physical and chemical erosion, census-based carbonate budgets may underestimate total erosion by ~1 mm year-1 (-1.15 kg CaCO3 m-2 year-1 ). Although the present state of Florida's reefs is dire, we demonstrate that the restoration of reef-building corals has the potential to help mitigate declines in reef accretion in some locations, which could allow some key ecosystem functions to be maintained until the threat of global climate change is addressed.

Scale dependence of coral reef oases and their environmental correlates.

Identifying relatively intact areas within ecosystems and determining the conditions favoring their existence is necessary for effective management in the context of widespread environmental degradation. In this study, we used 3766 surveys of randomly selected sites in the United States and U.S. Territories to identify the correlates of sites categorized as "oases" (defined as sites with relatively high total coral cover). We used occupancy models to evaluate the influence of 10 environmental predictors on the probability that an area (21.2-km2 cell) would harbor coral oases defined at four spatial extents: cross-basin, basin, region, and subregion. Across all four spatial extents, oases were more likely to occur in habitats with high light attenuation. The influence of the other environmental predictors on the probability of oasis occurrence were less consistent and varied with the scale of observation. Oases were most likely in areas of low human population density, but this effect was evident only at the cross-basin and subregional extents. At the regional and subregional extents oases were more likely where sea-surface temperature was more variable, whereas at the larger spatial extents the opposite was true. By identifying the correlates of oasis occurrence, the model can inform the prioritization of reef areas for management. Areas with biophysical conditions that confer corals with physiological resilience, as well as limited human impacts, likely support coral reef oases across spatial extents. Our approach is widely applicable to the development of conservation strategies to protect biodiversity and ecosystems in an era of magnified human disturbance.

A 3,000-year lag between the geological and ecological shutdown of Florida's coral reefs.

The global-scale degradation of coral reefs has reached a critical threshold wherein further declines threaten both ecological functionality and the persistence of reef structure. Geological records can provide valuable insights into the long-term controls on reef development that may be key to solving the modern coral-reef crisis. Our analyses of new and existing coral-reef cores from throughout the Florida Keys reef tract (FKRT) revealed significant spatial and temporal variability in reef development during the Holocene. Whereas maximum Holocene reef thickness in the Dry Tortugas was comparable to elsewhere in the western Atlantic, most of Florida's reefs had relatively thin accumulations of Holocene reef framework. During periods of active reef development, average reef accretion rates were similar throughout the FKRT at ~3 m/ky. The spatial variability in reef thickness was instead driven by differences in the duration of reef development. Reef accretion declined significantly from ~6,000 years ago to present, and by ~3,000 years ago, the majority of the FKRT was geologically senescent. Although sea level influenced the development of Florida's reefs, it was not the ultimate driver of reef demise. Instead, we demonstrate that the timing of reef senescence was modulated by subregional hydrographic variability, and hypothesize that climatic cooling was the ultimate cause of reef shutdown. The senescence of the FKRT left the ecosystem balanced at a delicate tipping point at which a veneer of living coral was the only barrier to reef erosion. Modern climate change and other anthropogenic disturbances have now pushed many reefs past that critical threshold and into a novel ecosystem state, in which reef structures built over millennia could soon be lost. The dominant role of climate in the development of the FKRT over timescales of decades to millennia highlights the potential vulnerability of both geological and ecological reef processes to anthropogenic climate change.

A geological perspective on the degradation and conservation of western Atlantic coral reefs.

Continuing coral-reef degradation in the western Atlantic is resulting in loss of ecological and geologic functions of reefs. With the goal of assisting resource managers and stewards of reefs in setting and measuring progress toward realistic goals for coral-reef conservation and restoration, we examined reef degradation in this region from a geological perspective. The importance of ecosystem services provided by coral reefs-as breakwaters that dissipate wave energy and protect shorelines and as providers of habitat for innumerable species-cannot be overstated. However, the few coral species responsible for reef building in the western Atlantic during the last approximately 1.5 million years are not thriving in the 21st century. These species are highly sensitive to abrupt temperature extremes, prone to disease infection, and have low sexual reproductive potential. Their vulnerability and the low functional redundancy of branching corals have led to the low resilience of western Atlantic reef ecosystems. The decrease in live coral cover over the last 50 years highlights the need for study of relict (senescent) reefs, which, from the perspective of coastline protection and habitat structure, may be just as important to conserve as the living coral veneer. Research is needed to characterize the geological processes of bioerosion, reef cementation, and sediment transport as they relate to modern-day changes in reef elevation. For example, although parrotfish remove nuisance macroalgae, possibly promoting coral recruitment, they will not save Atlantic reefs from geological degradation. In fact, these fish are quickly nibbling away significant quantities of Holocene reef framework. The question of how different biota covering dead reefs affect framework resistance to biological and physical erosion needs to be addressed. Monitoring and managing reefs with respect to physical resilience, in addition to ecological resilience, could optimize the expenditure of resources in conserving Atlantic reefs and the services they provide.

A depth refugium from catastrophic coral bleaching prevents regional extinction.

Species intolerant of changing climate might avoid extinction within refugia buffered from extreme conditions. Refugia have been observed in the fossil record but are not well documented or understood on ecological time scales. Using a 37-year record from the eastern Pacific across the two most severe El Niño events on record (1982-1983 and 1997 1998) we show how an exceptionally thermally sensitive reef-building hydrocoral, Millepora intricata, twice survived catastrophic bleaching in a deeper-water refuge (> 11 m depth). During both events, M. intricata was extirpated across its range in shallow water, but showed recovery within several years, while two other hydrocorals without deep-water populations were driven to regional extinction. Evidence from the subfossil record in the same area showed shallow-water persistence of abundant M. intricata populations from 5000 years ago, through severe El Niño-Southern Oscillation cycles, suggesting a potential depth refugium on a millennial timescale. Our data confirm the deep refuge hypothesis for corals under thermal stress.

Upwelling, climate change, and the shifting geography of coral reef development.

The eastern tropical Pacific is oceanographically unfavorable for coral-reef development. Nevertheless, reefs have persisted there for the last 7000 years. Rates of vertical accretion during the Holocene have been similar in the strong-upwelling Gulf of Panamá (GoP) and the adjacent, weak-upwelling Gulf of Chiriquí (GoC); however, seasonal upwelling in the GoP exacerbated a climate-driven hiatus in reef development in the late Holocene. The situation is now reversed and seasonal upwelling in the GoP currently buffers thermal stress, creating a refuge for coral growth. We developed carbonate budget models to project the capacity of reefs in both gulfs to keep up with future sea-level rise. On average, the GoP had significantly higher net carbonate production rates than the GoC. With an estimated contemporary reef-accretion potential (RAP) of 5.5 mm year-1, reefs in the GoP are projected to be able to keep up with sea-level rise if CO2 emissions are reduced, but not under current emissions trajectories. With an estimated RAP of just 0.3 mm year-1, reefs in the GoC are likely already unable to keep up with contemporary sea-level rise in Panamá (1.4 mm year-1). Whereas the GoP has the potential to support functional reefs in the near-term, our study indicates that their long-term persistence will depend on reduction of greenhouse gases.

The potential for coral reef restoration to mitigate coastal flooding as sea levels rise.

The ability of reefs to protect coastlines from storm-driven flooding hinges on their capacity to keep pace with sea-level rise. Here, we show how and whether coral restoration could achieve the often-cited goal of reversing the impacts of coral-reef degradation to preserve this essential function. We combined coral-growth measurements and carbonate-budget assessments of reef-accretion potential at Buck Island Reef, U.S. Virgin Islands, with hydrodynamic modeling to quantify future coastal flooding under various coral-restoration, sea-level rise, and storm scenarios. Our results provide guidance on how restoration of Acropora palmata, if successful, could mitigate the most extreme impacts of coastal flooding by reversing projected trajectories of reef erosion and allowing reefs to keep pace with the ~0.5 m of sea-level rise expected by 2100 with moderate carbon-emissions reductions. This highlights the potential long-term benefits of pursuing coral-reef restoration alongside climate-change mitigation to support the persistence of essential coral-reef ecosystem services.

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.

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.

A revised Holocene coral sea-level database from the Florida reef tract, USA.

The coral reefs and mangrove habitats of the south Florida region have long been used in sea-level studies for the western Atlantic because of their broad geographic extent and composition of sea-level tracking biota. The data from this region have been used to support several very different Holocene sea-level reconstructions (SLRs) over the years. However, many of these SLRs did not incorporate all available coral-based data, in part because detailed characterizations necessary for inclusion into sea-level databases were lacking. Here, we present an updated database comprised of 303 coral samples from published sources that we extensively characterized for the first time. The data were carefully screened by evaluating and ranking the visual taphonomic characteristics of every dated sample within the database, which resulted in the identification of 134 high-quality coral samples for consideration as suitable sea-level indicators. We show that our database largely agrees with the most recent SLR for south Florida over the last ∼7,000 years; however, the early Holocene remains poorly characterized because there are few high-quality data spanning this period. Suggestions to refine future Holocene SLRs in the region are provided including filling spatial and temporal data gaps of coral samples, particularly from the early Holocene, as well as constructing a more robust peat database to better constrain sea-level variability during the middle to late Holocene. Our database and taphonomic-ranking protocol provide a framework for researchers to evaluate data-selection criteria depending on the robustness of their sea-level models.

Upwelling buffers climate change impacts on coral reefs of the eastern tropical Pacific.

Corals of the eastern tropical Pacific live in a marginal and oceanographically dynamic environment. Along the Pacific coast of Panamá, stronger seasonal upwelling in the Gulf of Panamá in the east transitions to weaker upwelling in the Gulf of Chiriquí in the west, resulting in complex regional oceanographic conditions that drive differential coral-reef growth. Over millennial timescales, reefs in the Gulf of Chiriquí recovered more quickly from climatic disturbances compared with reefs in the Gulf of Panamá. In recent decades, corals in the Gulf of Chiriquí have also had higher growth rates than in the Gulf of Panamá. As the ocean continues to warm, however, conditions could shift to favor the growth of corals in the Gulf of Panamá, where upwelling may confer protection from high-temperature anomalies. Here we describe the recent spatial and temporal variability in surface oceanography of nearshore environments in Pacific Panamá and compare those conditions with the dynamics of contemporary coral-reef communities during and after the 2016 coral-bleaching event. Although both gulfs have warmed significantly over the last 150 yr, the annual thermal maximum in the Gulf of Chiriquí is increasing faster, and ocean temperatures there are becoming more variable than in the recent past. In contrast to historical trends, we found that coral cover, coral survival, and coral growth rates were all significantly higher in the Gulf of Panamá. Corals bleached extensively in the Gulf of Chiriquí following the 2015-2016 El Niño event, whereas upwelling in the Gulf of Panamá moderated the high temperatures caused by El Niño, allowing the corals largely to escape thermal stress. As the climate continues to warm, upwelling zones may offer a temporary and localized refuge from the thermal impacts of climate change, while reef growth in the rest of the eastern tropical Pacific continues to decline.

Climate Change, Coral Loss, and the Curious Case of the Parrotfish Paradigm: Why Don't Marine Protected Areas Improve Reef Resilience?

Scientists have advocated for local interventions, such as creating marine protected areas and implementing fishery restrictions, as ways to mitigate local stressors to limit the effects of climate change on reef-building corals. However, in a literature review, we find little empirical support for the notion of managed resilience. We outline some reasons for why marine protected areas and the protection of herbivorous fish (especially parrotfish) have had little effect on coral resilience. One key explanation is that the impacts of local stressors (e.g., pollution and fishing) are often swamped by the much greater effect of ocean warming on corals. Another is the sheer complexity (including numerous context dependencies) of the five cascading links assumed by the managed-resilience hypothesis. If reefs cannot be saved by local actions alone, then it is time to face reef degradation head-on, by directly addressing anthropogenic climate change-the root cause of global coral decline.

ENSO drove 2500-year collapse of eastern Pacific coral reefs.

Cores of coral reef frameworks along an upwelling gradient in Panamá show that reef ecosystems in the tropical eastern Pacific collapsed for 2500 years, representing as much as 40% of their history, beginning about 4000 years ago. The principal cause of this millennial-scale hiatus in reef growth was increased variability of the El Niño-Southern Oscillation (ENSO) and its coupling with the Intertropical Convergence Zone. The hiatus was a Pacific-wide phenomenon with an underlying climatology similar to probable scenarios for the next century. Global climate change is probably driving eastern Pacific reefs toward another regional collapse.