Abstract:

Coral cover has declined worldwide due to anthropogenic stressors that manifest on both global and local scales. Coral communities that exist in extreme conditions can provide information on how these stressors influence ecosystem structure, with implications for their persistence under future conditions. The Port of Miami is located within an urbanized environment, with active coastal development, as well as commercial shipping and recreational boating activity. Monitoring of sites throughout the Port since 2018 has revealed periodic extremes in temperature, seawater pH, and salinity, far in excess of what have been measured in most coral reef environments. Despite conditions that would kill many reef species, we have documented diverse coral communities growing on artificial substrates at these sites—reflecting remarkable tolerance to environmental stressors. Furthermore, many of the more prevalent species within these communities are now conspicuously absent or in low abundance on nearby reefs, owing to their susceptibility and exposure to stony coral tissue loss disease. Natural reef frameworks, however, are largely absent at the urban sites and while diverse fish communities are documented, it is unlikely that these communities provide the same goods and services as natural reef habitats. Regardless, the existence of these communities indicates unlikely persistence and highlights the potential for coexistence of threatened species in anthropogenic environments, provided that suitable stewardship strategies are in place.

Abstract:

Coral reef ecosystems are experiencing increased rates of carbonate dissolution due to losses in live coral cover coupled with the impacts of ocean acidification (OA) on coral reef calcifiers and bioeroders. While the stimulating effect of OA on bioerosion has been demonstrated experimentally, predominantly in the Pacific, the underlying physiological and molecular mechanisms behind the response are still poorly understood. To address this, we subjected common zooxanthellate (Cliona varians) and azooxanthellate (Pione lampa) Caribbean sponges to pre-industrial (8.15 pH), present-day (8.05 pH), and two future OA scenarios (moderate OA, 7.85 pH; extreme OA, 7.75 pH) and evaluated their physiological and transcriptomic responses. The influence of OA on sponge bioerosion was nonlinear for both species, with the greatest total bioerosion and chemical dissolution rates found in the 7.85 pH treatment, then not increasing further under the more extreme 7.75 pH conditions. A trend towards reduced bioerosion rates in the 7.75 pH treatment occurred regardless of the presence of algal symbionts and suggests that the sponges may become physiologically impaired under prolonged OA exposure, resulting in diminished bioerosion potential. These findings were supported by the RNA-seq analysis, which revealed differentially expressed genes involved in a stress response to OA, in particular, suppressed metabolism. This may indicate that the sponges had reallocated energy resources towards more critical physiological needs in response to OA as a survival mechanism under stressful conditions. These data reveal that while the bioerosion rates of excavating sponges in Caribbean reef ecosystems may increase under moderate OA scenarios, this OA-stimulation may plateau or be lost at extreme end-of-century pH conditions, with implications for the dissolution and long-term persistence of reef habitat structures.

Abstract:

Ocean acidification (OA) threatens coral reef persistence by decreasing calcification and accelerating the dissolution of reef frameworks. The carbonate chemistry of coastal areas where many reefs exist is strongly influenced by the metabolic activity of the underlying benthic community, contributing to high spatiotemporal variability. While characterizing this variability is difficult, it has important implications for the progression of OA and the persistence of the ecosystems. Here, we characterized the carbonate chemistry at 38 permanent stations located along 10 inshore-offshore transects spanning 250 km of the Florida Coral Reef (FCR), which encompass four major biogeographic regions (Biscayne Bay, Upper Keys, Middle Keys, and Lower Keys) and four shelf zones (inshore, mid-channel, offshore, and oceanic). Data have been collected since 2010, with approximately bi-monthly periodicity starting in 2015. Increasing OA, driven by increasing DIC, was detected in the mid-channel, offshore, and oceanic zones in every biogeographic region. In the inshore zone, however, increasing TA counteracted any measurable OA trend. Strong seasonal variability occurred at inshore sites and included periods of both exacerbated and mitigated OA. Seasonality was region-dependent, with greater variability in the Lower and Middle Keys. Elevated pH and aragonite saturation states (Ω_Ar) were observed in the Upper and Middle Keys, which could favor reef habitat persistence in these regions. Offshore reefs in the FCR could be more susceptible to global OA by experiencing open-ocean-like water chemistry conditions. By contrast, higher seasonal variability at inshore reefs could offer a temporary OA refuge during periods of enhanced primary production.

Abstract:

For reef framework to persist, calcium carbonate production by corals and other calcifiers needs to outpace loss due to physical, chemical, and biological erosion. This balance is both delicate and dynamic and is currently threatened by the effects of ocean warming and acidification. Although the protection and recovery of ecosystem functions are at the center of most restoration and conservation programs, decision makers are limited by the lack of predictive tools to forecast habitat persistence under different emission scenarios. To address this, we developed a modeling approach, based on carbonate budgets, that ties species-specific responses to site-specific global change using the latest generation of climate models projections (CMIP6). We applied this model to Cheeca Rocks, an outlier in the Florida Keys in terms of high coral cover, and explored the outcomes of restoration targets scheduled in the coming 20 years at this site by the Mission: Iconic Reefs restoration initiative. Additionally, we examined the potential effects of coral thermal adaptation by increasing the bleaching threshold by 0.25, 0.5, 1 and 2˚C. Regardless of coral adaptative capacity or restoration, net carbonate production at Cheeca Rocks declines heavily once the threshold for the onset of annual severe bleaching is reached. The switch from net accretion to net erosion, however, is significantly delayed by mitigation and adaptation. The maintenance of framework accretion until 2100 and beyond is possible under a decreased emission scenario coupled with thermal adaptation above 0.5˚C. Although restoration initiatives increase reef accretion estimates, Cheeca Rocks will only be able to keep pace with future sea-level rise in a world where anthropogenic CO₂ emissions are reduced. Present results, however, attest to the potential of restoration interventions combined with increases in coral thermal tolerance to delay the onset of mass bleaching mortalities, possibly in time for a low-carbon economy to be implemented and complementary mitigation measures to become effective.

Abstract:

Reef-building corals contain a complex consortium of organisms, a holobiont, which responds dynamically to disease, making pathogen identification difficult. While coral transcriptomics and microbiome communities have previously been characterized, similarities and differences in their responses to different pathogenic sources has not yet been assessed. In this study, we inoculated four genets of the Caribbean branching coral Acropora palmata with a known coral pathogen (Serratia marcescens) and white band disease. We then characterized the coral’s transcriptomic and prokaryotic microbiomes’ (prokaryiome) responses to the disease inoculations, as well as how these responses were affected by a short-term heat stress prior to disease inoculation. We found strong commonality in both the transcriptomic and prokaryiomes responses, regardless of disease inoculation. Differences, however, were observed between inoculated corals that either remained healthy or developed active disease signs. Transcriptomic co-expression analysis identified that corals inoculated with disease increased gene expression of immune, wound healing, and fatty acid metabolic processes. Co-abundance analysis of the prokaryiome identified sets of both healthy-and-disease-state bacteria, while co-expression analysis of the prokaryiomes’ inferred metagenomic function revealed infected corals’ prokaryiomes shifted from free-living to biofilm states, as well as increasing metabolic processes. The short-term heat stress did not increase disease susceptibility for any of the four genets with any of the disease inoculations, and there was only a weak effect captured in the coral hosts’ transcriptomic and prokaryiomes response. Genet identity, however, was a major driver of the transcriptomic variance, primarily due to differences in baseline immune gene expression. Despite genotypic differences in baseline gene expression, we have identified a common response for components of the coral holobiont to different disease inoculations. This work has identified genes and prokaryiome members that can be focused on for future coral disease work, specifically, putative disease diagnostic tools.

Abstract:

Orbicella faveolata, commonly known as the mountainous star coral, is a dominant reef-building species in the Caribbean, but populations have suffered sharp declines since the 1980s due to repeated bleaching and disease-driven mortality. Prior research has shown that inshore adult O. faveolata populations in the Florida Keys are able to maintain high coral cover and recover from bleaching faster than their offshore counterparts. However, whether this origin-specific variation in thermal resistance is heritable remains unclear. To address this knowledge gap, we produced purebred and hybrid larval crosses from O. faveolata gametes collected at two distinct reefs in the Upper Florida Keys, a nearshore site (Cheeca Rocks, CR) and an offshore site (Horseshoe Reef, HR), in two different years (2019, 2021). We then subjected these aposymbiotic larvae to severe (36°C) and moderate (32°C) heat challenges to quantify their thermal tolerance. Contrary to our expectation based on patterns of adult thermal tolerance, HR purebred larvae survived better and exhibited gene expression profiles that were less driven by stress response under elevated temperature compared to purebred CR and hybrid larvae. One potential explanation could be the compromised reproductive output of CR adult colonies due to repeated summer bleaching events in 2018 and 2019, as gametes originating from CR in 2019 contained less storage lipids than those from HR. These findings provide an important counter-example to the current selective breeding paradigm, that more tolerant parents will yield more tolerant offspring, and highlight the importance of adopting a holistic approach when evaluating larval quality for conservation and restoration purposes.

Abstract:

Given that global warming is the greatest threat to coral reefs, coral restoration projects have expanded worldwide with the goal of replenishing habitats whose reef-building corals succumbed to various stressors. In many cases, however, these efforts will be futile if outplanted corals are unable to withstand warmer oceans and an increased frequency of extreme temperature events. Stress-hardening is one approach proposed to increase the thermal tolerance of coral genotypes currently grown for restoration. Previous studies have shown that corals from environments with natural temperature variability experience less bleaching when exposed to thermal stress, though it remains unclear if this localized acclimatization or adaptation to variable temperatures can be operationalized for enhancing restoration efforts. To evaluate this approach, fragments from six source colonies of nursery-raised Caribbean staghorn coral (Acropora cervicornis) were treated with a variable temperature regime (oscillating twice per day from 28 to 31°C) or static temperatures (28°C) in the laboratory for 89 d. Following this, fragments were subjected to a heat-stress assay (32°C) for 2 weeks. Corals treated with variable temperatures manifested signs of severe thermal stress later than static temperature laboratory controls as well as untreated field controls collected from the nursery. Furthermore, there was a stark contrast in the physiological response to heat stress, whereby the laboratory and field control groups had a significantly higher incidence of rapid tissue sloughing and necrosis, while the variable temperature-treated corals succumbed to bleaching more gradually. Overall, our data show that pre-acclimation to a variable temperature regime improves acroporid thermotolerance. As corals continue to be outplanted back onto Florida’s changing reef scape, understanding the molecular mechanisms underlying this enhanced thermal tolerance and its endurance in situ will be critical for future research and restoration applications.

Abstract:

Ocean acidification (OA) is expected to modify the structure and function of coral reef ecosystems by reducing calcification, increasing bioerosion, and altering the physiology of many marine organisms. Much of our understanding of these relationships is based on experiments with static OA treatments, although evidence suggests that the magnitude of diurnal fluctuations in carbonate chemistry may modulate the calcification response to OA. These light-mediated swings in seawater pH are projected to become more extreme with OA, yet their impact on bioerosion remains unknown. We evaluated the influence of diurnal carbonate chemistry variability on the bioerosion rates of two Caribbean sponges: the zooxanthellate Cliona varians and azooxanthellate Cliothosa delitrix. Replicate fragments from multiple colonies of each species were exposed to four precisely controlled pH treatments: contemporary static (8.05 ± 0.00; mean pH ± diurnal pH oscillation), contemporary variable (8.05 ± 0.10), future OA static (7.80 ± 0.00), and future OA variable (7.80 ± 0.10). Significantly enhanced bioerosion rates, determined using buoyant weight measurements, were observed under more variable conditions in both the contemporary and future OA scenarios for C. varians, whereas the same effect was only apparent under contemporary pH conditions for C. delitrix. These results indicate that variable carbonate chemistry has a stimulating influence on sponge bioerosion, and we hypothesize that bioerosion rates evolve non-linearly as a function of pCO₂ resulting in different magnitudes and directions of rate enhancement/reduction between day and night, even with an equal fluctuation around the mean. This response appeared to be intensified by photosymbionts, evident by the consistently higher percent increase in bioerosion rates for photosynthetic C. varians across all treatments. These findings further suggest that more variable natural ecosystems may presently experience elevated sponge bioerosion rates and that the heightened impact of OA enhanced bioerosion on reef habitat could occur sooner than prior predictions.

Abstract:

In an era of global change, the fate and form of reef habitats will depend on shifting assemblages of organisms and their responses to multiple stressors. Multiphyletic assemblages of calcifying and bioeroding species contribute to a dynamic balance between constructive and erosive processes, and reef-framework growth occurs only when calcium-carbonate deposition exceeds erosion. Each contributing species exhibits a unique combination of environmental sensitivities, trophic needs, and competitive abilities, making the net outcome of their habitat-altering behavior difficult to predict. In this study, standardized blocks of clean, massive Porites were placed at six reef sites in the eastern tropical Pacific, in the strongly and more-weakly upwelling Gulfs of Panamá (GoP) and Chiriquí (GoC), respectively. Sites were chosen to characterize the unique thermal and carbonate-chemistry conditions of each gulf. Satellite products were used to examine differences in sea-surface productivity, and surveys were conducted to quantify the abundance of important grazing taxa. After two years in situ, the Porites blocks were collected and scanned using high-resolution computed tomography to volumetrically quantify both endolithic and epilithic habitat alteration. Scan-volumes were further classified into functional groups according to morphology to quantify external bioerosion by fish and sea urchins, as well as the calcifying and bioeroding activity of crustose coralline algae, scleractinian corals, mollusks, annelids, and barnacles. The GoP, which has higher productivity, cooler temperatures, and periodically lower pH conditions, had higher rates of macroboring, but also higher rates of calcification. These unexpectedly higher rates of calcification in the GoP were a result of high recruitment of suspension-feeding taxa, particularly barnacles and vermiform fauna that have poor reef-forming potential. External bioerosion by grazers was the dominant process influencing these dead coral substrates across both gulfs, contributing to higher rates of net erosion in the GoC and underscoring the important roles that urchins and fish play in not just removing algae on reefs, but also eroding reef habitat. Ultimately these findings reveal that the trophic requirements of habitat-altering taxa are closely tied to reef-framework stability, and that environmental conditions conducive to carbonate precipitation are not necessarily those that will lead to habitat persistence.

Abstract:

Since the appearance of stony coral tissue loss disease (SCTLD) on reefs off Miami in 2014, this unprecedented outbreak has spread across the entirety of Florida’s coral reef tract, as well as to many territories throughout the Caribbean. The endemic zone reached the upper Florida Keys by 2016, resulting in partial or complete mortality of coral colonies across numerous species. Disease was first observed at Cheeca Rocks (Islamorada, Florida) in the beginning of 2018, with reports of coral mortality peaking mid-year. The disease was still present at Cheeca Rocks as of March 2020, however, to a lesser degree compared to the initial outbreak. Annual monitoring efforts have been ongoing at Cheeca Rocks since 2012, including repeated benthic photomosaics of a 330 m² survey zone, spanning six replicate sites. As such, a repository of coral community composition data exists for before and after the disease outbreak that was analyzed to assess the impacts of SCTLD on reef communities at an upper Florida Keys inshore reef. Cheeca Rocks is hypothesized to be a resilient reef due to its persistent high coral cover despite its inshore location, which subjects corals to fluctuating water quality and marginal environmental conditions. Coral populations here have been shown to recover from bleaching events and heat stress with minimal coral mortality. Though colonies of coral species characterized as highly and moderately susceptible to SCTLD (e.g., Colpophyllia natans, Diploria labyrinthiformis, Pseudodiploria strigosa, Orbicella annularis, and O. faveolata) suffered mortality as a result of the outbreak with an average loss of 16.42% relative cover by species, the overall impacts on coral cover and community structure were relatively low, contributing to a loss of total coral cover of only 1.65%. Comparison of photomosaic data to other studies indicate Cheeca Rocks may not have been affected as severely as other sites on Florida’s coral reef tract, underlying this site’s potential role in coral resilience to stressors including bleaching events, land-based pollution, and disease epizootics.

Abstract:

Coral reefs are globally in decline and western Atlantic reefs have experienced the greatest losses in live coral cover of any region. The Flower Garden Banks (FGB) in the Gulf of Mexico are high-latitude, remote reefs that are an outlier to this trend, as they have maintained coral cover ≥ 50% since at least 1989. Quantifying the long-term trends in coral growth of key reef-building coral species, and the underlying environmental drivers, leads to a better understanding of local sensitivities to past changes that will ultimately allow us to better predict the future of reef growth at FGB. We obtained coral cores and constructed growth records for two of the most abundant hermatypic coral species at FGB, Pseudodiploria strigosa and Orbicella faveolata. Our records cover 57 yrs of growth for P. strigosa (1957–2013) and 45 yrs for O. faveolata (1970–2014). Linear extension and calcification rates of both species have increased significantly, but skeletal density did not change over the respective time periods. Extension and calcification data of both species combined were negatively correlated with the discharge from the Atchafalaya River, but positively correlated with maximum sea surface temperatures (SST). These data provide evidence that runoff from the Atchafalaya River impacts FGB corals and is a major control on coral growth at FGB. The increase in growth at FGB can be attributed to the significant warming trend in maximum monthly SSTs. Given the warming trend and recent increase in severity of bleaching at FGB, the prognosis is that bleaching events will become more deleterious with time, which will lead to a breakdown in the positive relationship between coral growth and maximum SST. This study provides further evidence that some high-latitude, cooler reef sites have experienced a stimulation in coral growth with ocean warming.

Abstract:

Ocean acidification (OA) is impairing the construction of coral reefs while simultaneously accelerating their breakdown. The metabolism of different reef organism assemblages alters seawater pH in different ways, possibly buffering or exacerbating OA impacts. In spite of this, field data relating benthic community structure and seawater pH are sparse. We collected pH time-series data snapshots at 10 m depth from 28 different reefs (n = 13 lagoon, n = 15 fore reef) across 22 Pacific islands, spanning 31° latitude and 90° longitude. Coincident with all deployments, we measured percent cover of the benthic community. On fore reefs, high coral cover (CC) negatively correlated with mean and minimum pH, but positively correlated with pH variability. Conversely, pH minima were positively correlated to coverage of coralline and turf algae. Benthic cover did not correlate with pH in lagoonal reefs. From 0%–100% CC, mean pH and aragonite saturation state (Ωarag) declined −0.081 and −0.51, respectively, while declines in minimum values were greater (Δmin pH = −0.164, Δmin Ωarag = −0.96). Based upon previously published relationships, the mean pH decline from 0%–100% CC would depress coral calcification 7.7%–18.0% and increase biologically-mediated dissolution 13.5%–27.9%, with pH minima depressing dark coral calcification 14.4%–35.2% and increasing biologically-mediated dissolution 31.0%–62.2%. This spatially expansive dataset provides evidence that coral reefs with the highest coral cover may experience the lowest and most extreme pH values with OA.

Abstract:

Although coral reef ecosystems across the globe are in decline due to climate change and other anthropogenic stressors, certain inshore reefs of the Upper Florida Keys reef tract have persisted, with some even thriving, under marginalized conditions. To better understand the molecular basis of the thermotolerance displayed by these corals, a laboratory-based temperature challenge experiment that also featured conspecifics from a more stress-susceptible offshore reef was conducted with the common Caribbean reef-builder Orbicella faveolata, and the proteomes of both the coral hosts and their endosymbiotic dinoflagellate communities were profiled in (1) controls, (2) corals that succumbed to high-temperature stress and bleached, and (3) those that instead acclimated to high temperatures ex situ. Proteomic signatures varied most significantly across temperatures, host genotypes, and Symbiodiniaceae assemblages, and the two eukaryotic compartments of this mutualism exhibited distinct proteomic responses to high temperatures. Both partners maintained high levels of molecular chaperones and other canonical (eukaryotic) stress response (CSR) proteins in all treatments (including controls). Instead, proteins involved in lipid trafficking, metabolism, and photosynthesis played greater roles in the holobionts’ high-temperature responses, and these energy mobilization processes may have sustained the elevated protein turnover rates associated with the constitutively active CSR.

Abstract:

Healthy coral communities can be found on artificial structures (concrete walls and riprap) within the Port of Miami (PoM), Florida. These communities feature an unusually high abundance of brain corals, which have almost entirely vanished from nearby offshore reefs. These corals appear to be thriving in very low-quality waters influenced by dense ship and boat traffic, dredging, and numerous residential and industrial developments. The PoM basin is part of Biscayne Bay, an estuarine environment that experiences frequent freshwater input, high nutrient loading, hypoxia, and acidification. To investigate if there is a molecular basis behind the ability of these corals to persist within these highly “urbanized” waters, we compared whole transcriptome expression profiles from 25 PoM Pseudodiploria strigose colonies against six conspecifics from a nearby offshore reef. We found that the urban corals exhibited higher expression of (1) transcripts encoding pattern-recognition receptors which may allow these corals to better sense and detect food particles and pathogenic invaders, (2) digestive and degradation-associated enzymes, which may suggest an elevated capacity for heterotrophy and pathogen digestion, and (3) transcripts related to innate immunity, defense, and cellular detoxification, which may collectively protect against pathogenic organisms and water pollution impacts. Large ribosomal subunit rRNA gene mapping revealed that P. strigose colonies from the PoM sites predominantly hosted heat-tolerant endosymbionts from the genus Durusdinium, while offshore conspecifics’ communities were dominated by symbionts in the genus Breviolum. These findings reveal transcriptomic plasticity and molecular mechanisms contributing to the persistence of these corals within a highly urbanized habitat.

Abstract:

Naturally acidified environments, such as those caused by volcanic CO₂ venting, reveal how complex coral reef ecosystems may respond to future ocean acidification conditions. Few of these sites have been described worldwide, and only a single such site is known from the Caribbean. Herein, we have characterized an area of volcanic acidification at Mayreau Island, St. Vincent and the Grenadines. Despite localized CO₂ enrichment and gas venting, the surrounding area has high hard and soft coral cover, as well as extensive carbonate frameworks. Twice daily extremes in acidification, in some cases leading to undersaturation of aragonite, are correlated with tidal fluctuations and are likely related to water flow. Corals persisting despite this periodic acidification can provide insights into mechanisms of resilience and the importance of natural pH variability on coral reefs.

Abstract:

Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back-to-back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef-building coral Orbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRAD and profiled for algal symbiont abundance and type. O. faveolata at the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerant Durusdinium trenchii (formerly Symbiondinium trenchii) was the dominant endosymbiont type region-wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated by D. trenchii. 2bRAD host genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion of D. trenchii was attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably, D. trenchii was rarely dominant in O. faveolata from the Florida Keys in previous studies, even during bleaching. The region-wide high abundance of D. trenchii was likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys, O. faveolata was most abundant, had the highest bleaching resistance, and contained the most corals dominated by D. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.

Abstract:

Ocean acidification (OA) will result in lower calcification rates for numerous marine taxa, including many species of corals which create important reef habitat. Seawater carbonate chemistry fluctuates over cycles ranging from days to seasons, often driven by biological processes such as respiration and photosynthesis. The magnitude of diel fluctuations varies spatially and may become more pronounced in the future due to OA. Due to technical constraints, OA experiments that incorporate diel variability into treatments are few in number. As a result, the degree to which coral reef organisms are influenced by ambient daily carbonate chemistry variability is poorly understood. Here we describe an experiment conducted in a novel seawater system which can independently manipulate carbonate chemistry in 16 separate aquaria, in real time, allowing precise control of the mean and magnitude of pH oscillations while minimizing pseudoreplication. Five genotypes of the threatened Caribbean coral Acropora cervicornis were subjected to a total of five pH treatments, 7.80 ± 0.20, 7.80 ± 0.10, and 7.80 ± 0.00, as well as 8.05 ± 0.10 and 8.05 ± 0.00. Those corals exposed to variable contemporary conditions (8.05 ± 0.10) calcified faster than those in current and future static treatment levels, which did not significantly differ from each other. Variable contemporary pH also resulted in faster growth rates than highly variable future conditions (7.80 ± 0.20), but were not significantly different than future conditions with the same ±0.10 diel pH oscillation. These findings support the importance of incorporating diel variability into OA experiments and suggest that more variable natural ecosystems may yield higher calcification rates for corals.

Abstract:

Annual coral bleaching events, which are predicted to occur as early as the next decade in the Florida Keys, are expected to cause catastrophic coral mortality. Despite this, there is little field data on how Caribbean coral communities respond to annual thermal stress events. At Cheeca Rocks, an inshore patch reef near Islamorada, Florida, the condition of 4234 coral colonies was followed over 2 years of subsequent bleaching in 2014 and 2015, the two hottest summers on record for the Florida Keys. In 2014, this site experienced 7.7 degree heating weeks (DHW) and, as a result, 38.0% of corals bleached and an additional 36.6% were pale or partially bleached. In situ temperatures in summer of 2015 were even warmer, with the site experiencing 9.5 DHW. Despite the increased thermal stress in 2015, only 12.1% of corals were bleached in 2015, which was 3.1 times less than 2014. Partial mortality dropped from 17.6% of surveyed corals to 4.3% between 2014 and 2015, and total colony mortality declined from 3.4 to 1.9% between years. Total colony mortality was low over both years of coral bleaching with 94.7% of colonies surviving from 2014 to 2016. The reduction in bleaching severity and coral mortality associated with a second stronger thermal anomaly provides evidence that the response of Caribbean coral communities to annual bleaching is not strictly temperature dose dependent and that acclimatization responses may be possible even with short recovery periods. Whether the results from Cheeca Rocks represent an aberration or a true resilience potential is the subject of ongoing research.

Abstract:

The persistence of coral reef frameworks requires that calcium carbonate (CaCO₃) production by corals and other calcifiers outpaces CaCO₃ loss via physical, chemical, and biological erosion. Coral bleaching causes declines in CaCO₃ production, but this varies with bleaching severity and the species impacted. We conducted census-based CaCO₃ budget surveys using the established ReefBudget approach at Cheeca Rocks, an inshore patch reef in the Florida Keys, annually from 2012 to 2016. This site experienced warm-water bleaching in 2011, 2014, and 2015. In 2017, we obtained cores of the dominant calcifying coral at this site, Orbicella faveolata, to understand how calcification rates were impacted by bleaching and how they affected the reef-wide CaCO₃ budget. Bleaching depressed O. faveolata growth and the decline of this one species led to an overestimation of mean (± std. error) reef-wide CaCO₃ production by + 0.68 (± 0.167) to + 1.11 (± 0.236) kg m⁻² year⁻¹ when using the static ReefBudget coral growth inputs. During non-bleaching years, the ReefBudget inputs slightly underestimated gross production by − 0.10 (± 0.022) to − 0.43 (± 0.100) kg m⁻² year⁻¹. Carbonate production declined after the first year of back-to-back bleaching in 2014, but then increased after 2015 to values greater than the initial surveys in 2012. Cheeca Rocks is an outlier in the Caribbean and Florida Keys in terms of coral cover, carbonate production, and abundance of O. faveolata, which is threatened under the Endangered Species Act. Given the resilience of this site to repeated bleaching events, it may deserve special management attention.

Abstract:

Sea-level rise (SLR) is predicted to elevate water depths above coral reefs and to increase coastal wave exposure as ecological degradation limits vertical reef growth, but projections lack data on interactions between local rates of reef growth and sea level rise. Here we calculate the vertical growth potential of more than 200 tropical western Atlantic and Indian Ocean reefs, and compare these against recent and projected rates of SLR under different Representative Concentration Pathway (RCP) scenarios. Although many reefs retain accretion rates close to recent SLR trends, few will have the capacity to track SLR projections under RCP4.5 scenarios without sustained ecological recovery, and under RCP8.5 scenarios most reefs are predicted to experience mean water depth increases of more than 0.5 m by 2100. Coral cover strongly predicts reef capacity to track SLR, but threshold cover levels that will be necessary to prevent submergence are well above those observed on most reefs. Urgent action is thus needed to mitigate climate, sea-level and future ecological changes in order to limit the magnitude of future reef submergence.

Abstract:

Staghorn coral, Acropora cervicornis, is a threatened species and the primary focus of western Atlantic reef restoration efforts to date. We compared linear extension, calcification rate, and skeletal density of nursery-raised A. cervicornis branches reared for 6 months either on blocks attached to substratum or hanging from PVC trees in the water column. We demonstrate that branches grown on the substratum had significantly higher skeletal density, measured using computerized tomography, and lower linear extension rates compared to water-column fragments. Calcification rates determined with buoyant weighing were not statistically different between the two grow-out methods, but did vary among coral genotypes. Whereas skeletal density and extension rates were plastic traits that depended on grow-out method, calcification rate was conserved. Our results show that the two rearing methods generate the same amount of calcium carbonate skeleton but produce colonies with different skeletal characteristics and suggest that there is genetically-based variability in coral calcification performance.

Abstract:

Experiments have demonstrated that ocean acidification (OA) conditions projected to occur by the end of the century will slow the calcification of numerous coral species and accelerate the biological erosion of reef habitats (bioerosion). Microborers, which bore holes less than 100 μm diameter, are one of the most pervasive agents of bioerosion and are present throughout all calcium carbonate substrates within the reef environment. The response of diverse reef functional groups to OA is known from real-world ecosystems but, to date, our understanding of the relationship between ocean pH and carbonate dissolution by microborers is limited to controlled laboratory experiments. Here we examine the settlement of microborers to pure mineral calcium carbonate substrates (calcite) along a natural pH gradient at a volcanically acidified reef at Maug, Commonwealth of the Northern Mariana Islands (CNMI). Colonization of pioneer microborers was higher in the lower pH waters near the vent field. Depth of microborer penetration was highly variable both among and within sites (4.2–195.5 μm) over the short duration of the study (3 mo.), and no clear relationship to increasing CO₂ was observed. Calculated rates of biogenic dissolution, however, were highest at the two sites closer to the vent and were not significantly different from each other. These data represent the first evidence of OA-enhancement of microboring flora colonization in newly available substrates and provide further evidence that microborers, especially bioeroding chlorophytes, respond positively to low pH. The accelerated breakdown and dissolution of reef framework structures with OA will likely lead to declines in structural complexity and integrity, as well as possible loss of essential habitat.

Abstract:

Ocean acidification (OA) impacts the physiology of diverse marine taxa; among them corals that create complex reef framework structures. Biological processes operating on coral reef frameworks remain largely unknown from naturally high-carbon-dioxide (CO₂) ecosystems. For the first time, we independently quantified the response of multiple functional groups instrumental in the construction and erosion of these frameworks (accretion, macroboring, microboring, and grazing) along natural OA gradients. We deployed blocks of dead coral skeleton for roughly 2 years at two reefs in Papua New Guinea, each experiencing volcanically enriched CO₂, and employed high-resolution micro-computed tomography (micro-CT) to create three-dimensional models of changing skeletal structure. OA conditions were correlated with decreased calcification and increased macroboring, primarily by annelids, representing a group of bioeroders not previously known to respond to OA. Incubation of these blocks, using the alkalinity anomaly methodology, revealed a switch from net calcification to net dissolution at a pH of roughly 7.8, within Intergovernmental Panel on Climate Change's (IPCC) predictions for global ocean waters by the end of the century. Together these data represent the first comprehensive experimental study of bioerosion and calcification from a naturally high-CO₂ reef ecosystem, where the processes of accelerated erosion and depressed calcification have combined to alter the permanence of this essential framework habitat.

Abstract:

Rising anthropogenic CO₂ in the atmosphere is accompanied by an increase in oceanic CO₂ and a concomitant decline in seawater pH. This phenomenon, known as ocean acidification (OA), has been experimentally shown to impact the biology and ecology of numerous animals and plants, most notably those that precipitate calcium carbonate skeletons, such as reef-building corals. Volcanically acidified water at Maug, Commonwealth of the Northern Mariana Islands (CNMI) is equivalent to near-future predictions for what coral reef ecosystems will experience worldwide due to OA. We provide the first chemical and ecological assessment of this unique site and show that acidification-related stress significantly influences the abundance and diversity of coral reef taxa, leading to the often-predicted shift from a coral to an algae-dominated state. This study provides field evidence that acidification can lead to macroalgae dominance on reefs.

Abstract:

The calcification and extension rates of two species of scleractinian coral (Montastraea cavernosa, Porites astreoides) were measured in corals experimentally transplanted to paired inshore and offshore locations in the Upper, Middle, and Lower Florida Keys from 2010 to 2011. Growth rates were compared with respect to 1) shelf location, 2) species, 3) region, and 4) temperature. Transplanted corals on inshore reefs generally calcified less than those at paired offshore sites, but these differences were only significant in a few cases. This difference in growth is likely because of two thermal stress events that occurred inshore, but not offshore, as growth records from cores of P. astreoides revealed significantly higher extension and calcification inshore from 2001–2013. The core data confirmed that the years 2010–2012 were a period of depressed growth inshore. Calcification and extension rates of the experimental corals were not statistically different between M. cavernosa and P. astreoides within a given site. The only exceptions were that calcification was higher in M. cavernosa at the Middle Keys inshore site. The Middle Florida Keys sites had the lowest rates of calcification, supporting the hypothesis that the influence of Florida Bay waters in this region contributes to poor reef development. Mean calcification rates negatively correlated with metrics of cold stress in M. cavernosa and heat stress in P. astreoides. The lack of a significant correlation between heat stress and mean calcification in M. cavernosa may help explain this species persistence on today's reefs. Maximum calcification and mean extension, however, were negatively correlated with maximum running 30-day mean temperature, showing that the growth of M. cavernosa is not completely insensitive to warm water stress. The ‘weedy’ life-history strategy of P. astreoides may compensate for the sensitivity of calcification rates to heat stress reported here, allowing this species to maintain the stable populations that have been observed throughout Florida and the wider Caribbean.

Abstract:

Coral reefs along the Florida Keys portion of the Florida Reef Tract (FRT) have undergone a dramatic decline since the 1980s. Since the 1997-98 El Niño event, coral cover on offshore reefs of the FRT has been ≤ 5% and continues to decline. Mortality of the framework-constructing coral in the Orbicella (formerly Montastraea) annularis species complex has driven this recent loss in overall coral cover. One exception to this decline occurred on the inshore patch reefs of the Florida Keys, where coral cover has remained relatively high. We examined the growth and calcification of Orbicella faveolata, an ecologically important subspecies of the O. annularis complex, at both an inshore and offshore reef site representing this dichotomy of present-day coral cover. The period examined (2004-2013) encompasses the Caribbean-wide 2005 mass coral bleaching, the 2009-10 catastrophic cold-water bleaching, and a warm-water bleaching event in 2011. Extension and calcification rates were higher inshore every year from 2004-2013 except when there were thermal stress events that solely impacted inshore reefs (2009-10, 2011-12). Inshore growth rates recovered quickly from cold and warm-water stress. These higher calcification rates and their quick recovery after thermal stress are likely important factors in the persistence of high coral cover inshore.

Abstract:

Anthropogenic CO₂ is causing warming and ocean acidification. Coral reefs are being severely impacted, yet confusion lingers regarding how reefs will respond to these stressors over this century. Since the 1982–1983 El Niño–Southern Oscillation warming event, the persistence of reefs around the Galápagos Islands has differed across an acidification gradient. Reefs disappeared where pH  < 8.0 and aragonite saturation state (Ω_arag)  ≤ 3 and have not recovered, whereas one reef has persisted where pH  > 8.0 and Ω_arag  > 3. Where upwelling is greatest, calcification by massive Porites is higher than predicted by a published relationship with temperature despite high CO₂, possibly due to elevated nutrients. However, skeletal P/Ca, a proxy for phosphate exposure, negatively correlates with density (R = −0.822, p < 0.0001). We propose that elevated nutrients have the potential to exacerbate acidification by depressing coral skeletal densities and further increasing bioerosion already accelerated by low pH.