Mass coral bleaching is increasing in frequency and severity, leading to the loss of coral abundance and diversity. However, some corals are less susceptible to bleaching than others and can provide a model for identifying the physiological and biogeochemical traits that underlie coral resilience to thermal stress. Corals from Eilat in the northern Red Sea do not bleach unless seawater temperatures are sustained at +6⁰C above their average summer maximum. This extreme thermal tolerance qualifies these as super-corals, as most corals bleach when exposed to temperatures that are only +1-2⁰C above their thermal maximum. Here, we conducted a controlled bleaching experiment (+6°C) for 37 days (equivalent to 32-degree heating weeks) on three species of corals from Eilat: Stylophora pistillata, Pocillopora damicornis, and Favia favus. While all three species appeared visibly bleached, their physiological and biogeochemical responses were species-specific. S. pistillata catabolized lipids but still maintained total energy reserves and biomass, while calcification declined. P. damicornis was the least affected by bleaching. It maintained its total energy reserves, biomass, and calcification independent of heterotrophy. Finally, F. favus suffered losses in energy reserves and biomass but still maintained photosynthesis and calcification most likely because of its high baseline heterotrophic capacity. Thus, just like their non-super-coral counterparts, maintaining energy reserves and biomass, and heterotrophic capacity appear to be traits that underlie the thermal tolerance of these super-corals from Eilat. Thus, these super-coral populations could provide viable seed stock for repopulating coral losses on other reefs.

As climate change decimates coral communities on a global scale, effective outplanting of resilient corals will become an increasingly important management tool. This study examined endangered Caribbean coral Acropora cervicornis with three objectives. 1) Determine if there is significant phenotypic plasticity in thermal tolerance, 2) determine if genotypes differ in their degree of plasticity of thermal tolerance, and 3) Identify if acclimatization to higher temperatures affects survival of outplanted coral depending on the environment they are transferred into. To conduct this study, we partnered with the Coral Restoration Foundation (CRF) to acquire fragments of A. cervicornis for both outplanting and land-based tests. To examine the degree of plasticity, fragments of 20 genotypes were exposed to either ambient or elevated temperatures (32o C) after a short acclimation period at either ambient or elevated temperatures. A comparison of lifespan of fragments exposed to different temperatures shows a significant amount of plasticity exists in A. cervicornis and that genotype is a significant factor in determining the degree of plasticity. To test the survivability of treated coral, 10 coral genotypes were outplanted on two reef sites offshore of Key Largo, FL. These corals are being monitored to determine if heat-treated corals have a higher survivability than corals kept at ambient temperature when planted at different reef depths. Identification of plastic genotypes in regard to thermal stress could be used for stocking programs to contribute easily-acclimatized colonies to exposed locations, such as shallow reef crests. Furthermore, an accurate estimation of the limit of phenotypic plasticity within corals will further the understanding of acclimation capacity of coral communities under the changing climate. Prior heat exposure may increase outplant survivability and aid local managers in reef recovery projects, ultimately bolstering active restoration of decimated reef sites.

There is increasing interest in developing interventions that enhance thermotolerance of restored corals in anticipation of continued climate change. One such method involves controlled bleaching and recovery to manipulate corals algal symbionts in favor of more thermotolerant types. Data from natural bleaching events suggest that disturbed symbiont communities return to their original symbionts over months-years, but the factors influencing the long-term persistence of these symbionts are not well understood. Using real-time PCR, we assessed the longevity of symbiont communities dominated by thermotolerant Symbiodinium trenchii (initially type D1a) in 24 replicate cores from each of 6 colonies of the massive starlet coral (Siderastrea siderea) collected from Emerald Reef, FL following a natural bleaching event. We monitored the symbiont community for three years, including an initial period at control temperatures (7 months at 25-28°C), followed by a thermal challenge applied to a subset of cores (4 weeks at 32-33°C), recovery at control temperatures (1 year), a second thermal challenge applied to all cores (4 weeks at 31-32°C) and a final recovery period (1 year). We found that, under control temperatures, corals containing >1% Symbiodinium clade C rapidly became dominated by these clade (< 4 months). However, corals containing < 1% clade C remained dominated by S. trenchii for >1 year and bleached less severely (measured as declines in symbiont abundance and function [Fv/Fm]) when exposed to heat stress. During both bleaching events, cores with mixed communities experienced shifts in favor of S. trenchii dominance, and cores already dominated by S. trenchii became virtually exclusive on S. trenchii, thereby increasing the long-term persistence of these thermotolerant symbionts. These data suggest that the longevity of S. trenchii communities increases if competing symbionts are reduced below 1%, which may be unlikely to occur across entire colonies because sensitive symbionts likely persist in coral microhabitats (e.g., shaded vertical colony edges) during bleaching events. Instead, these dynamics indicate that the symbiont communities of S. siderea likely persist long-term as complex mosaics whose specific composition in any particular polyp is governed by its history of disturbance and that of its neighbors.

Intervention strategies to create “climate smart” corals for restoration include manipulating the association between corals and their algal symbionts. In adult corals, “stress-hardening” through controlled bleaching and recovery can shift symbiont assemblages in favor of thermally-tolerant Durusdinium (formerly Symbiodinium clade D) and increase thermal tolerance by 1-2°C. We tested methods for manipulating symbiosis in coral recruits using elevated temperature and proximity to adult colonies containing thermally-tolerant Durusdinium to increase symbiont acquisition rates or abundance of Durusdinium. Aposymbiotic Diploria labyrinthiformis recruits from Curaçao were exposed to four experimental treatments: (1) ambient temperature (27°C) and proximity to adult corals predominantly hosting Durusdinium; (2) ambient temperature and proximity to adult corals predominantly hosting Cladocopium (formerly Symbiodinium clade C); (3) elevated temperature (30°C) and proximity to Durusdinium-dominated adults and (4) elevated temperature and proximity to Cladocopium-dominated adults. On average, recruits reared at 30°C experienced a >30% reduction in survivorship compared with those at 27°C. Of the surviving recruits, those exposed to 30°C hosted a greater proportion of Durusdinium (20% of their symbionts) but had fewer symbionts (0.13 per host cell) than those exposed to 27°C, which hosted an average of 11% Durusdinium and 0.27 symbionts per host cell. In addition, at 27°C recruits reared in proximity to Durusdinium-dominated adults hosted three times as many Durusdinium (~17.5%) as those reared with Cladocopium-dominated adults (~5.5%), but there was no significant difference in proportion of Durusdinium based on adult symbiont type at 30°C. This is the first study to investigate how temperature and symbiont availability impacts symbiont acquisition in Caribbean scleractinian coral recruits. Future studies will test the applicability of these findings for different scleractinian species from different source locations. If elevated temperatures and/or proximity to Durusdinium-dominated adults increases the proportion of Durusdinium in recruits, restoration practitioners may choose to rear recruits under these conditions in order to boost their thermal tolerance prior to releasing them onto reefs.

Under predicted future ocean conditions, elevated seawater temperatures and ocean acidification (OA) will affect coral simultaneously. Many studies have shown that these conditions can be detrimental to the physiology of both the coral host and its endosymbiotic algae. Moderate nutrient additions, however, may offer some physiological benefits and aid in mitigating elevated temperature and OA stress in corals. We predict that moderate increases in nutrient concentrations will reduce the negative effects of elevated temperature and pCO2 on coral physiology, but that these effects will be species specific. If true, some coastal marine environments may provide refuge to corals in the future. To investigate this, fragments of the two Indo-Pacific corals Acropora millepora and Turbinaria reniformis were grown for 33 days under 8 treatments of a fully factorial experimental design including two seawater temperatures (26.5°C, and 31.5°C), two pCO2 levels (401 μatm, and 760 μatm), and two nutrient levels (low nutrients at 0.4 μmol/L NO3/NO2 and 0.2 μmol/L PO4-3, and moderate nutrients at 3.5 μmol/L NO3/NO2 and 0.3 μmol/L PO4-3). Preliminary results suggest that T. reniformis is resilient under all temperature and pCO2 conditions, with no additional effect of the moderate nutrient addition observed on either the host or the endosymbiont physiology. In contrast, moderate nutrients stimulated the productivity of A. millepora endosymbionts when exposed to the dual stress of elevated temperature and pCO2, but at a cost to host calcification. In addition, isotopic evidence shows that inorganic nitrogen additions are incorporated and recycled between the endosymbiont and the host, and that the N incorporation diminishes under temperature and/or pCO2 stress. Overall, these results suggest that coastal environments with moderate nutrient additions may provide a refuge to the more susceptible A. millepora under predicted future ocean conditions and that the more tolerant T. reniformis is already adapted to future ocean conditions. Therefore, it is important to consider nutrient composition of reefs when developing conservation strategies for Acropora corals.

Cellular stress memory is an important and conserved feature across the tree of life. A growing body of evidence in the literature suggests corals may have a thermal stress memory. Indeed, knowledge of coral stress memory could improve restoration outcomes. To elicit thermal stress memory in the lab, nearshore nursery-reared Acropora cervicornis fragments (n=8 genets) from Broward County, Florida were primed with five distinct thermal exposures, allowed to recover for 8 days, then exposed to a bleaching assay. Symbiont density, chlorophyll, dark-adapted chlorophyll fluorescence, and algal protein content were measured immediately after priming, after the 8-day recovery period, and after bleaching to determine whether priming conferred any bleaching resistance. Our results revealed an increase in bleaching resistance in two priming treatments, however only one treatment was not significantly different from the control group. Perhaps thermal priming of corals may require a priming exposure that is ‘just right’ to confer the maximum benefit to new fragments or outplants. Implications for restoration are discussed.

Rising seawater temperatures are a major threat to coral reefs worldwide, causing coral bleaching events that are occurring annually in some locations and are expected to be annual events globally this century. Corals with high levels of stored energy reserves are known to have increased survival and resilience potential to annual bleaching stress. In this study, we hypothesize that corals that catabolize storage lipids (i.e., triacyglycerols and wax esters) in response to thermal bleaching, but then quickly reassimilate them during recovery will be more resilent to annual bleaching events compared to those that do not. We experimentally bleached three species of Caribbean corals (Porites astreoides, Porites divaricata, and Orbicella faveolata) two years in a row (summer 2009 and 2010) by gradually elevating seawater temperature to 31.5C. We measured concentrations of the following lipid classes using thin layer chromatography: wax esters, triacylglycerols, free fatty acids, cholesterol, and phospholipids. Preliminary results suggest that species had different strategies to respond to environmental change. Overall, O. faveolata and P. divaricata had higher concentrations of storage lipids such as wax esters and triacylglycerols than P. astreoides, in agreement with other studies which show that P. astreoides is the least resilient to repeat bleaching stress of the three species examined. We support prioritization of conservation efforts for O. faveolata and P. divaricata for stock colonies and restoration projects as they are the most likely to survive annual bleaching events of the future. We also found that 1) lipid class composition of O. faveolata was affected by single bleaching, but not repeat bleaching, and those differences were determined by storage lipids; 2) lipid class composition in P. astreoides only changed with repeat bleaching, but not single bleaching with differences also driven by storage lipids; and 3) lipid class composition in P. divaricata was unaffected by single or repeat bleaching. These findings show a complex pattern of acclimation of different species of coral to climate change, which might have important implications for colony assessment and adoption of restoration policies .

Recent back-to-back episodes of heat-induced coral bleaching in Florida and elsewhere have driven the need to test interventions that increase the resilience of restored corals to anticipated future warming. One potential intervention is the application of sublethal doses of bleaching stress to induce compensatory responses in reef corals during recovery that would increase their resistance to subsequent thermal stress (“stress hardening”). We trialed different methods for stress-hardening corals as part of a restoration program in Miami, FL, and used quantitative PCR (qPCR) and chlorophyll fluorometry (I-PAM) to assess changes in the structure and function of algal symbiont communities (Symbiodinium spp.). We tested the effect of high irradiance and the herbicide Diuron (DCMU: 3-(3,4-dichlorophenyl)-1,1-dimethylurea) on the bleaching and recovery of 8 genotypes of the threatened Caribbean staghorn coral Acropora cervicornis. For high light stress, we exposed corals to ~2,000 umol photons/m2/s PAR, which decreased photochemical efficiency (Fv/Fm) and resulted in visible bleaching within 3 weeks. These corals were then allowed to recover in the field and further changes monitored using qPCR. We also tested the effect of short-term exposure (1h, 2h and 6h) to three concentrations of DCMU (0.45mg/L, 4.5mg/L and 41.85mg/L) on coral bleaching and recovery. All concentrations resulted in rapid (< 1 h) decreases in Fv/Fm in A. cervicornis, but these values returned to normal after one day of recovery, suggesting longer exposure times are needed to induce symbiont expulsion. We will report on continued trials using longer DCMU exposure times and the use of subsurface rafts to expose corals to high light in the field. Continued efforts are needed to quickly test the efficacy of low-technology methods of stress hardening corals that can be scaled and incorporated into restoration efforts.

Stress hardening, a technique using controlled stress to induce net positive physiological change, has been proposed as a scalable tool to improve the heat tolerance of nursery-grown corals through bleaching and recovery. Public-facing experiments in the Inventors in Residence Lab at the Phillip and Patricia Frost Museum of Science in Miami, FL, are testing various stress hardening methods using nursery-grown Acropora cervicornis while showcasing coral restoration science to thousands of visitors. These iterative studies include assessing the feasibility of stress hardening using high irradiance while testing which stress and recovery conditions minimize tradeoffs. 165 coral fragments from eight genotypes of A. cervicornis were haphazardly assigned to either a control or a high light treatment (250 or 2000 umol photon m-2s-1) at one of two temperatures (25 or 29.5°C). Following the light stress, bleached corals were allowed to recover at either 25 or 29.5°C in a fully crossed design. Tissue samples, photochemical efficiency, and buoyant weight measurements were taken to assess changes in symbiont community structure (qPCR) and function (I-PAM) and to quantify coral growth. Bleached corals lost approximately 95% of their algal symbionts, with symbiont community function declining more severely at 25 than at 29.5°C. Control corals at 25°C had slower growth rates and lower symbiont abundance and function compared to controls at 29.5°C. While light-stressed corals held at 25°C throughout the study also showed lower total growth and reduced symbiont community function, corals that were light-stressed and recovered at 29.5°C did not show the same significant declines in growth or photochemical efficiency. These results indicate that recovery environment can mitigate potential tradeoffs caused by hormetic approaches such as stress hardening. Exposure of naïve controls and recovered fragments to subsequent stress will elucidate whether stress hardening improves resistance to, or recovery from, bleaching. This pilot study highlights the importance of seasonally timing potential interventions to maximize their net benefit and to maintain restoration efficiency by preserving key physiological functions such as coral growth rate.

The severe loss of hard coral cover over the past 30 years has prompted an interest in reef restoration by transplanting coral fragments. However, not all coral transplants are equally successful and the ecological conditions necessary for transplant resiliency in the face of disturbances are not well understood. To address this lack of knowledge, we combined a long-term reef community census with a longitudinal study of coral transplant survival on fifteen reefs in the middle Florida Keys. A total of 276 coral fragments of five species were transplanted along permanent transects and photographed quarterly from June 2013 to June 2018. During this period, two species of coral transplants were exposed to two acute thermal stress events (2014, 2015) and four species endured a category four hurricane (2017). In general, Siderastrea siderea showed higher resiliency to bleaching compared to Porites asteroides. Of all the abiotic and biotic factors measured, the amount of Dictyota spp. algae present was the factor that best explained individual variance in the propensity for bleaching. Porites asteroides, Siderastrea radians, and Orbicella faveolata had the highest survival after a physical disturbance with more than 50% of transplants surviving. Acropora cervicornis transplants were most susceptible to physical disturbance with only 16% survival. The complexity of the reef directly surrounding the coral transplant influenced the survival of A. cervicornis and O. faveolata corals, but not P. asteroides or S. radians transplants. Local topography and species composition rather than regional characteristics, such as depth, distance to shore, and visibility, explained more variation in coral resiliency. These results suggest some species are more resilient to thermal stress while others are more resilient to physical disturbance and local conditions may be the best predictors of transplant success.

Coral reefs are being severely damaged worldwide. Coral restoration has been implemented to ameliorate such degradation and increase coral cover. In the last decade restoration of branching corals have been widely implemented and popularized that even non-expert citizens do it globally. Yet there are still scientific gaps that may accelerate the restoration process and increase the probability of success in the long-term. We tested whether coral populations are locally adapted, so that when transplanted to different habitats incur in increased mortality rates. We found that in the ESA threated Orbicella species, populations are adapted across depths and an increased in depth of just 5 meters sparks an increased mortality of 25% for O. annularis. O. franksi when transplanted shallower (3 m) does however remarkably well with no-mortality. We also found that the robustness of O. franksi in shallow environments is related to a faster photo-physiological adjustment to brighter environments. On the contrary, O. annularis in deep areas reaches extremely low excitation pressures that compromise algal photosynthesis and the coral-algal symbiosis. Our compilation of studies using reciprocal transplants suggests adaptation in reef anthozoans is a common phenomenon. Even under similar survivorship rates, the physiological compensation of being in a new foreign habitat decreases coral performance. Our results highlight the need to match donor and transplanted sites to increase coral yield during coral restoration. In slow growing species (< 3 cm/yr) such in Orbicella incorporating habitat information to increase the likelihood of restoration success is of greatest importance as measuring the effects of restoration may take as long as couple of decades.

Over the past 30 years we have lost 50% of corals worldwide. With climate change projections increasing over time, it is estimated that only 10% of corals will survive past 2050. Therefore, we must intervene to establish a foundation of resilient corals that allow our reefs to have a future. In 2015, we spearheaded novel research aimed at accelerating natural selection to enhance stress tolerance in corals (i.e. human- assisted evolution). Starting with the most thermal stress resistant corals, we tested emerging methods such as 1) selective breeding, 2) inducing acclimatization and 3) modifying symbioses. We selectively bred and sequenced the genomes of two of the main reef-building coral species in Kane’ohe Bay (Montipora capitata and Porites compressa), induced acclimatization in three coral species, and inoculated corals with thermal tolerant symbionts. Now we are taking the first steps to incorporate resilient coral stocks into restoration efforts to enhance long-term effectiveness, thereby increasing return on investment and offsetting the risk of losing important ecosystem services. We will identify coral stocks that are more resilient to thermal stress, grow them in in situ nurseries, and propagate them at three locations near O’ahu, Hawaii. Partners include National Oceanic and Atmospheric Administration (federal), Hawai’i State Department of Land and Natural Resources (state) and Malama Maunalua (non-profit). We will restore at least 5 acres (0.6 acres of live coral) using experimental plots to directly enhance coastal protection while determining whether restoration with resilient corals enhances future outcomes. The ultimate goal is to develop a best practices model for effective restoration that can be scaled up for greatest impact.