Loss of coral reef growth capacity to track future increases in sea level.

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.

Performance of Orbicella faveolata larval cohorts does not align with previously observed thermal tolerance of adult source populations.

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.

Role of host genetics and heat-tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming.

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.

Ocean acidification changes the vertical movement of stone crab larvae.

Anthropogenic activities are increasing ocean temperature and decreasing ocean pH. Some coastal habitats are experiencing increases in organic runoff, which when coupled with a loss of vegetated coastline can accelerate reductions in seawater pH. Marine larvae that hatch in coastal habitats may not have the ability to respond to elevated temperature and changes in seawater pH. This study examined the response of Florida stone crab (Menippe mercenaria) larvae to elevated temperature (30°C control and 32°C treatment) and CO2-induced reductions in pH (8.05 pH control and 7.80 pH treatment). We determined whether those singular and simultaneous stressors affect larval vertical movement at two developmental stages. Geotactic responses varied between larval stages. The direction and rate of the vertical displacement of larvae were dependent on pH rather than temperature. Stage III larvae swam upwards under ambient pH conditions, but swam downwards at a faster rate under reduced pH. There was no observable change in the directional movement of Stage V larvae. The reversal in orientation by Stage III larvae may limit larval transport in habitats that experience reduced pH and could pose challenges for the northward dispersal of stone crabs as coastal temperatures warm.

Enhanced macroboring and depressed calcification drive net dissolution at high-CO2 coral reefs.

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.

Ocean acidification alters the otoliths of a pantropical fish species with implications for sensory function.

Ocean acidification affects a wide diversity of marine organisms and is of particular concern for vulnerable larval stages critical to population replenishment and connectivity. Whereas it is well known that ocean acidification will negatively affect a range of calcareous taxa, the study of fishes is more limited in both depth of understanding and diversity of study species. We used new 3D microcomputed tomography to conduct in situ analysis of the impact of ocean acidification on otolith (ear stone) size and density of larval cobia (Rachycentron canadum), a large, economically important, pantropical fish species that shares many life history traits with a diversity of high-value, tropical pelagic fishes. We show that 2,100 µatm partial pressure of carbon dioxide (pCO2) significantly increased not only otolith size (up to 49% greater volume and 58% greater relative mass) but also otolith density (6% higher). Estimated relative mass in 800 µatm pCO2 treatments was 14% greater, and there was a similar but nonsignificant trend for otolith size. Using a modeling approach, we demonstrate that these changes could affect auditory sensitivity including a ∼50% increase in hearing range at 2,100 µatm pCO2, which may alter the perception of auditory information by larval cobia in a high-CO2 ocean. Our results indicate that ocean acidification has a graded effect on cobia otoliths, with the potential to substantially influence the dispersal, survival, and recruitment of a pelagic fish species. These results have important implications for population maintenance/replenishment, connectivity, and conservation efforts for other valuable fish stocks that are already being deleteriously impacted by overfishing.

Restoration and coral adaptation delay, but do not prevent, climate-driven reef framework erosion of an inshore site in the Florida Keys.

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 modelling 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.

Coral persistence despite marginal conditions in the Port of Miami.

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.

Coral reefs in peril in a record-breaking year.

Climate change and its impacts on coral reefs have reached unchartered territory.

Unprecedented early-summer heat stress and forecast of coral bleaching on the Great Barrier Reef, 2021-2022.

The Great Barrier Reef (GBR) is predicted to undergo its sixth mass coral bleaching event during the Southern Hemisphere summer of 2021-2022. Coral bleaching-level heat stress over the GBR is forecast to start earlier than any previous year in the satellite record (1985-present). The National Oceanic and Atmospheric Administration (NOAA) Coral Reef Watch (CRW) near real-time satellite-based heat stress products were used to investigate early-summer sea surface temperature (SST) and heat stress conditions on the GBR during late 2021. As of 14 December 2021, values of instantaneous heat stress (Coral Bleaching HotSpots) and accumulated heat stress over a 12-week running window (Degree Heating Weeks) on the GBR were unprecedented in the satellite record. Further, 89% of GBR satellite reef pixels for this date in 2021 had a positive seven-day SST trend of greater than 0.2 degrees Celsius/week. Background temperatures (the minimum temperature over the previous 29 days) were alarmingly high, with 87% of GBR reef pixels on 14 December 2021 being greater than the maximum SST over that same 29-day period for any year from 1985-2020. The GBR is starting the 2021-2022 summer season with more accumulated heat than ever before, which could have disastrous consequences for the health, recovery, and future of this critical reef system.

Low net carbonate accretion characterizes Florida's coral reef.

Coral reef habitat is created when calcium carbonate production by calcifiers exceeds removal by physical and biological erosion. Carbonate budget surveys provide a means of quantifying the framework-altering actions of diverse assemblages of marine species to determine net carbonate production, a single metric that encapsulates reef habitat persistence. In this study, carbonate budgets were calculated for 723 sites across the Florida Reef Tract (FRT) using benthic cover and parrotfish demographic data from NOAA's National Coral Reef Monitoring Program, as well as high-resolution LiDAR topobathymetry. Results highlight the erosional state of the majority of the study sites, with a trend towards more vulnerable habitat in the northern FRT, especially in the Southeast Florida region (- 0.51 kg CaCO3 m-2 year-1), which is in close proximity to urban centers. Detailed comparison of reef types reveals that mid-channel reefs in the Florida Keys have the highest net carbonate production (0.84 kg CaCO3 m-2 year-1) and indicates that these reefs may be hold-outs for reef development throughout the region. This study reports that Florida reefs, specifically their physical structure, are in a net erosional state. As these reefs lose structure, the ecosystem services they provide will be diminished, signifying the importance of increased protections and management efforts to offset these trends.

Poorly cemented coral reefs of the eastern tropical Pacific: possible insights into reef development in a high-CO2 world.

Ocean acidification describes the progressive, global reduction in seawater pH that is currently underway because of the accelerating oceanic uptake of atmospheric CO(2). Acidification is expected to reduce coral reef calcification and increase reef dissolution. Inorganic cementation in reefs describes the precipitation of CaCO(3) that acts to bind framework components and occlude porosity. Little is known about the effects of ocean acidification on reef cementation and whether changes in cementation rates will affect reef resistance to erosion. Coral reefs of the eastern tropical Pacific (ETP) are poorly developed and subject to rapid bioerosion. Upwelling processes mix cool, subthermocline waters with elevated pCO(2) (the partial pressure of CO(2)) and nutrients into the surface layers throughout the ETP. Concerns about ocean acidification have led to the suggestion that this region of naturally low pH waters may serve as a model of coral reef development in a high-CO(2) world. We analyzed seawater chemistry and reef framework samples from multiple reef sites in the ETP and found that a low carbonate saturation state (Omega) and trace abundances of cement are characteristic of these reefs. These low cement abundances may be a factor in the high bioerosion rates previously reported for ETP reefs, although elevated nutrients in upwelled waters may also be limiting cementation and/or stimulating bioerosion. ETP reefs represent a real-world example of coral reef growth in low-Omega waters that provide insights into how the biological-geological interface of coral reef ecosystems will change in a high-CO(2) world.

Surface Water CO2 variability in the Gulf of Mexico (1996-2017).

Approximately 380,000 underway measurements of sea surface salinity, temperature, and carbon dioxide (CO2) in the Gulf of Mexico (GoM) were compiled from the Surface Ocean CO2 Atlas (SOCAT) to provide a comprehensive observational analysis of spatiotemporal CO2 dynamics from 1996 to 2017. An empirical orthogonal function (EOF) was used to derive the main drivers of spatial and temporal variability in the dataset. In open and coastal waters, drivers were identified as a biological component linked to riverine water, and temperature seasonality. Air-sea flux estimates indicate the GoM open (- 0.06 ± 0.45 mol C m-2 year-1) and coastal (- 0.03 ± 1.83 mol C m-2 year-1) ocean are approximately neutral in terms of an annual source or sink for atmospheric CO2. Surface water pCO2 in the northwest and southeast GoM open ocean is increasing (1.63 ± 0.63 µatm  year-1 and 1.70 ± 0.14 µatm year-1, respectively) at rates comparable to those measured at long-term ocean time-series stations. The average annual increase in coastal CO2 was 3.20 ± 1.47 µatm year-1 for the northwestern GoM and 2.35 ± 0.82 µatm year-1 for the west Florida Shelf. However, surface CO2 in the central (coastal and open) GoM, which is influenced by Mississippi and Atchafalaya River outflow, remained fairly stable over this time period.

Resilience in carbonate production despite three coral bleaching events in 5 years on an inshore patch reef in the Florida Keys.

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.

Coral bleaching indices and thresholds for the Florida Reef Tract, Bahamas, and St. Croix, US Virgin Islands.

It is well established that elevated sea temperatures cause widespread coral bleaching, yet confusion lingers as to what facet of extreme temperatures is most important. Utilizing long-term in situ datasets, we calculated nine thermal stress indices and tested their effectiveness at segregating bleaching years a posteriori for multiple reefs on the Florida Reef Tract. The indices examined represent three aspects of thermal stress: (1) short-term, acute temperature stress; (2) cumulative temperature stress; and (3) temperature variability. Maximum monthly sea surface temperature (SST) and the number of days >30.5 degrees C were the most significant; indicating that cumulative exposure to temperature extremes characterized bleaching years. Bleaching thresholds were warmer for Florida than the Bahamas and St. Croix, US Virgin Islands reflecting differences in seasonal maximum SST. Hind-casts showed that monthly mean SST above a local threshold explained all bleaching years in Florida, the Bahamas, and US Virgin Islands.

Elevated Colonization of Microborers at a Volcanically Acidified Coral Reef.

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.

Rapid Recent Warming of Coral Reefs in the Florida Keys.

Coral reef decline in the Florida Keys has been well-publicized, controversial, and polarizing owing to debate over the causative agent being climate change versus overfishing. The recurrence of mass bleaching in 2014, the sixth event since 1987, prompted a reanalysis of temperature data. The summer and winter of 2014 were the warmest on record. The oldest known in-situ temperature record of any coral reef is from Hens and Chickens Reef (H&C) in the Florida Keys, which showed significant warming from 1975-2014. The average number of days ≥31.5 and 32(o)C per year increased 2670% and 2560%, respectively, from the mid-1990 s to present relative to the previous 20 years. In every year after 1992 and 1994, maximum daily average temperatures exceeded 30.5 and 31°C, respectively. From 1975-1994, temperatures were <31 °C in 61% of years, and in 44% of the years prior to 1992 temperatures were <30.5 °C. The measured rate of warming predicts the start of annual bleaching between 2020 and 2034, sooner than expected from climate models and satellite-based sea temperatures. These data show that thermal stress is increasing and occurring on a near-annual basis on Florida Keys reefs due to ocean warming from climate change.

Ocean acidification refugia of the Florida Reef Tract.

Ocean acidification (OA) is expected to reduce the calcification rates of marine organisms, yet we have little understanding of how OA will manifest within dynamic, real-world systems. Natural CO(2), alkalinity, and salinity gradients can significantly alter local carbonate chemistry, and thereby create a range of susceptibility for different ecosystems to OA. As such, there is a need to characterize this natural variability of seawater carbonate chemistry, especially within coastal ecosystems. Since 2009, carbonate chemistry data have been collected on the Florida Reef Tract (FRT). During periods of heightened productivity, there is a net uptake of total CO(2) (TCO(2)) which increases aragonite saturation state (Ω(arag)) values on inshore patch reefs of the upper FRT. These waters can exhibit greater Ω(arag) than what has been modeled for the tropical surface ocean during preindustrial times, with mean (± std. error) Ω(arag)-values in spring = 4.69 (±0.101). Conversely, Ω(arag)-values on offshore reefs generally represent oceanic carbonate chemistries consistent with present day tropical surface ocean conditions. This gradient is opposite from what has been reported for other reef environments. We hypothesize this pattern is caused by the photosynthetic uptake of TCO(2) mainly by seagrasses and, to a lesser extent, macroalgae in the inshore waters of the FRT. These inshore reef habitats are therefore potential acidification refugia that are defined not only in a spatial sense, but also in time; coinciding with seasonal productivity dynamics. Coral reefs located within or immediately downstream of seagrass beds may find refuge from OA.

Hurricanes benefit bleached corals.

Recent, global mass-mortalities of reef corals due to record warm sea temperatures have led researchers to consider global warming as one of the most significant threats to the persistence of coral reef ecosystems. The passage of a hurricane can alleviate thermal stress on coral reefs, highlighting the potential for hurricane-associated cooling to mitigate climate change impacts. We provide evidence that hurricane-induced cooling was responsible for the documented differences in the extent and recovery time of coral bleaching between the Florida Reef Tract and the U.S. Virgin Islands during the Caribbean-wide 2005 bleaching event. These results are the only known scenario where the effects of a hurricane can benefit a stressed marine community.