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Coral cover is declining worldwide due to multiple interacting threats. We compared the effects of elevated nutrients and temperature on three Caribbean corals: Acropora cervicornis, Orbicella faveolata, and Siderastrea siderea. Colonies hosting different algal symbionts were exposed to either ambient nutrients (A), elevated NH4 (N), or elevated NH4 + PO4 (N + P) at control temperatures (26 °C) for > 2 months, followed by a 3-week thermal challenge (31.5 °C). A. cervicornis hosted Symbiodinium (S. fitti) and was highly susceptible to the combination of elevated nutrients and temperature. During heat stress, A. cervicornis pre-exposed to elevated nutrients experienced 84%–100% mortality and photochemical efficiency (Fv/Fm) declines of 41–50%. In comparison, no mortality and lower Fv/Fm declines (11–20%) occurred in A. cervicornis that were heat-stressed but not pre-exposed to nutrients. O. faveolata and S. siderea response to heat stress was determined by their algal symbiont community and was not affected by nutrients. O. faveolata predominantly hosted Durusdinium trenchii or Breviolum, but only corals hosting Breviolum were susceptible to heat, experiencing 100% mortality, regardless of nutrient treatment. S. siderea colonies predominantly hosted Cladocopium C1 (C. goreaui), Cladocopium C3, D. trenchii, or variable proportions of Cladocopium C1 and D. trenchii. This species was resilient to elevated nutrients and temperature, with no significant mortality in any of the treatments. However, during heat stress, S. siderea hosting Cladocopium C3 suffered higher reductions in Fv/Fm (41–56%) compared to S. siderea hosting Cladocopium C1 and D. trenchii (17–26% and 10–16%, respectively). These differences in holobiont susceptibility to elevated nutrients and heat may help explain historical declines in A. cervicornis starting decades earlier than other Caribbean corals. Our results suggest that tackling only warming temperatures may be insufficient to ensure the continued persistence of Caribbean corals, especially A. cervicornis. Reducing nutrient inputs to reefs may also be necessary for these iconic coral species to survive.

Intervention strategies to enhance coral resilience include manipulating the association between corals and their algal endosymbionts. While hosting thermotolerant Durusdinium trenchii can increase bleaching thresholds in adults, its effects remain largely unknown during the early life stages of Caribbean corals. Here, we tested if Orbicella faveolata recruits could establish symbiosis with D. trenchii supplied by nearby “donor” colonies and examined the resulting ecological trade-offs to evaluate early Symbiodiniaceae manipulation as a scalable tool for reef restoration. We exposed aposymbiotic recruits to 29°C or 31°C and to fragments of either Montastraea cavernosa (containing Cladocopium) or Siderastrea siderea (containing D. trenchii). After 60 days, recruits reared with D. trenchii donors hosted nearly three times more D. trenchii than those with Cladocopium donors, suggesting that recruits can acquire Symbiodiniaceae from nearby corals of different species. Temperature did not affect D. trenchii uptake. Next, donor colonies were removed and surviving recruits were maintained for three months at ambient temperatures, after which a subset was exposed to a 60-day heat stress trial. Recruits previously reared at 31°C survived twice as long at 34°C as those reared at 29°C, suggesting that pre-exposure to heat can prime recruits to withstand future thermal stress. In addition, recruits hosting primarily D. trenchii survived twice as long at 34°C as those hosting little or no D. trenchii. However, the proportion of D. trenchii hosted was negatively correlated with polyp size and symbiont density, indicating a trade-off between growth (of both host and symbiont) and heat tolerance. These findings suggest that, while donor colonies may be effective sources for seeding coral recruits with thermotolerant symbionts, practitioners will need to balance the likely benefits and costs of these approaches when designing restoration strategies.

Anthropogenic climate change is the biggest threat to coral reefs, but reef restoration efforts are buying time for these ecosystems. Lesion recovery, which can be a determinant of colony survival, is particularly important for restored species. Here, we evaluate lesion recovery of 18 genets of Acropora cervicornis from Florida reefs with different thermal regimes in a temperature challenge experiment. Genets demonstrated significant variability in healing, which greatly slowed under heat stress. Only 35% of fragments healed at 31.5 °C compared to 99% at 28 °C. Donor reef thermal regime significantly influenced lesion recovery under heat stress with corals from warmer reefs demonstrating greater healing than corals from cooler reefs, but did not influence recovery under ambient conditions. These findings should encourage practitioners to utilize rapidly healing genets, avoid fragmentation in high temperatures, and incorporate assisted relocation by moving corals from warmer to cooler reefs, where they might succeed under future climate conditions.

Mesophotic reefs (30‐150 m) have been proposed as potential refugia that facilitate the recovery of degraded shallow reefs following acute disturbances such as coral bleaching and disease. However, because of the technical difficulty of collecting samples, the connectivity of adjacent mesophotic reefs is relatively unknown compared with shallower counterparts. We used genotyping by sequencing to assess fine‐scale genetic structure of Montastraea cavernosa at two sites at Pulley Ridge, a mesophotic coral reef ecosystem in the Gulf of Mexico, and downstream sites along the Florida Reef Tract. We found differentiation between reefs at Pulley Ridge (~68 m) and corals at downstream upper mesophotic depths in the Dry Tortugas (28–36 m) and shallow reefs in the northern Florida Keys (Key Biscayne, ~5 m). The spatial endpoints of our study were distinct, with the Dry Tortugas as a genetic intermediate. Most striking were differences in population structure among northern and southern sites at Pulley Ridge that were separated by just 12km. Unique patterns of clonality and outlier loci allele frequency support these sites as different populations and suggest that the long‐distance horizontal connectivity typical of shallow‐water corals may not be typical for mesophotic systems in Florida and the Gulf of Mexico. We hypothesize that this may be due to the spawning of buoyant gametes, which commits propagules to the surface, resulting in greater dispersal and lower connectivity than typically found between nearby shallow sites. Differences in population structure over small spatial scales suggest that demographic constraints and/or environmental disturbances may be more variable in space and time on mesophotic reefs compared with their shallow‐water counterparts.

Stony coral tissue loss disease (SCTLD) has devastated coral populations along Florida’s Coral Reef and beyond. Although widespread infection and mortality of adult colonies have been documented, no studies have yet investigated the susceptibility of recruits to this disease. Here, we exposed eight-month-old Diploria labyrinthiformis recruits and four-month-old Colpophyllia natans recruits to two sequential doses of SCTLD in the laboratory to track infection and assess potential resilience. Both species began to develop lesions as early as 48 h after exposure began. During the first dose, 59.0% of C. natans recruits lost all tissue (died) within two to eight days of developing lesions, whereas D. labyrinthiformis recruits experienced significantly slower rates of tissue loss and minimal eventual mortality. In C. natans, larger recruits and those fused into groups of multiple genets (chimeras) exhibited the highest survivorship. In contrast, smaller and/or single (ungrouped) recruits had the lowest survivorship (9.9 - 26.5%). After 20 days, a second SCTLD dose was delivered to further test resistance in remaining recruits, and all recruits of both species succumbed within 6 days. Although no recruits showed absolute resistance to SCTLD following repeated exposures, our results provide evidence that interactions between species, size, and chimerism can impact relative resistance. This study represents the first report of SCTLD in Caribbean coral recruits and carries implications for natural species recovery and reef restoration efforts. Additional research on the susceptibility of coral juveniles to SCTLD is urgently needed, to include different species, locations, parents, and algal symbionts, with the goal of assessing relative susceptibility and identifying potential sources of resilience for this critical life history stage.

Coral reefs function as submerged breakwaters providing wave mitigation and flood-reduction benefits for coastal communities. Although the wave-reducing capacity of reefs has been associated with wave breaking and friction, studies quantifying the relative contribution by corals are lacking. To fill this gap, a series of experiments was conducted on a trapezoidal artificial reef model with and without fragments of staghorn coral skeletons attached. The experiments were performed at the University of Miami’s Surge-Structure-Atmosphere-Interaction (SUSTAIN) Facility, a large-scale wind/wave tank, where the influence of coral skeletons on wave reduction under different wave and depth conditions was quantified through water level and wave measurements before and after the reef model. Coral skeletons reduce wave transmission and increase wave-energy dissipation, with the amount depending on the hydrodynamic conditions and relative geometrical characteristics of the reef. The trapezoidal artificial coral reef model was found to reduce up to 98% of the wave energy with the coral contribution estimated to be up to 56% of the total wave-energy dissipation. Depending on the conditions, coral skeletons can thus enhance significantly, through friction, the wave-reducing capability of a reef.

Coral cover is declining worldwide due to multiple interacting threats. We compared the effects of elevated nutrients and temperature on three Caribbean corals: Acropora cervicornis, Orbicella faveolata, and Siderastrea siderea. Colonies hosting different algal types were exposed to either ambient nutrients (A), elevated NH4 (N), or elevated NH4 + PO4 (N+P) at control temperatures (26 °C) for > 2 months, followed by a 3-week thermal challenge (31.5 °C). A. cervicornis hosted Symbiodinium (S. fitti) and was highly susceptible to the combination of elevated nutrients and temperature. During heat stress, A. cervicornis pre-exposed to elevated nutrients experienced 84%-100% mortality and photochemical efficiency (Fv/Fm) declines of 41-50%. In comparison, no mortality and lower Fv/Fm declines (11-20%) occurred in A. cervicornis that were heat-stressed but not pre-exposed to nutrients. O. faveolata and S. siderea response to heat stress was determined by their algal symbiont community and was not affected by nutrients. O. faveolata predominantly hosted Durusdinium trenchii or Breviolum, but only corals hosting Breviolum were susceptible to heat, experiencing 100% mortality, regardless of nutrient treatment. S. siderea colonies predominantly hosted Cladocopium C1 (C. goreaui), Cladocopium C3, D. trenchii, or variable proportions of Cladocopium C1 and D. trenchii. This species was resilient to elevated nutrients and temperature, with no significant mortality in any of the treatments. However, during heat stress, S. siderea hosting Cladocopium C3 suffered higher reductions in Fv/Fm (41-56%) compared to S. siderea hosting Cladocopium C1 and D. trenchii (17-26% and 10-16%, respectively). These differences in holobiont susceptibility to elevated nutrients and heat may help explain historical declines in A. cervicornis starting decades earlier than other Caribbean corals. Our results suggest that tackling only warming temperatures may be insufficient to ensure the continued persistence of Caribbean corals, especially A. cervicornis. Reducing nutrient inputs to reefs may also be necessary for these iconic coral species to survive.

International audience; Maintaining coral reef ecosystems is a social imperative, because so many people depend on coral reefs for food production, shoreline protection, and livelihoods. The survival of reefs this century, however, is threatened by the mounting effects of climate change. Climate mitigation is the foremost and essential action to prevent coral reef ecosystem collapse. Without it, reefs will become extremely diminished within the next 20-30 years. Even with strong climate mitigation, however, existing conservation measures such as marine protected areas and fisheries management are no longer sufficient to sustain the ecosystem and many additional and innovative actions to increase reef resilience must also be taken. In this paper we assess the suite of protections and actions in terms of their potential be effective according to a set of criteria that include effectiveness, readiness, co-benefits and disbenefits. Even with the best scientific innovation, saving coral reefs will require a well-funded, welldesigned, and rapidly executed strategy with political and social commitments at the level of other grand challenges.

Scleractinian corals are the principal builders of coral reefs. These megadiverse ecosystems are declining due to coral mortality from a variety of stressors, including disease. Corals are dependent upon symbiotic dinoflagellates in the family Symbiodiniaceae for phototrophic contributions to their energy budgets. However, suppression of host immunity may be necessary to maintain these intracellular symbioses. To explore the consequences of symbiosis on host immunity, we manipulated symbiont density by increasing nitrogen availability. Replicate cores from four colonies of the Caribbean coral, Orbicella faveolata, were reared in seawater treated with ammonium for one month to increase symbiont density. Corals were then immune-stimulated using lipopolysaccharide and poly I:C. Gene expression was analyzed using RNAseq and symbiont density was quantified (as symbiont:host cell ratio) using quantitative PCR (qPCR). Ammonium treatment had limited positive effects on host immunity. In contrast, increases in symbiont density had large negative effects on host expression of immune-related transcripts. These results suggest links between nutrient enrichment and coral disease may be the result of the effect of increased symbiont density on host immunity, rather than the direct effect of the nutrients. Further study of the trade-offs between symbiont density and immunity may help understand how decreasing water quality and increasing disease will shape future reef communities.

As sea surface temperatures increase worldwide due to climate change, coral bleaching events are becoming more frequent and severe, resulting in reef degradation. Leveraging the inherent ability of reef-building corals to acclimatize to thermal stress via pre-exposure to protective temperature treatments may become an important tool in improving the resilience of coral reefs to rapid environmental change. We investigated whether historical bleaching phenotype, coral host genotype, and exposure to protective temperature treatments would affect the response of the Hawaiian coral Montipora capitata to natural thermal stress. Fragments were collected from colonies that demonstrated different bleaching responses during the 2014-2015 event in Kāne’ohe Bay (O’ahu, Hawai’i) and exposed to four different artificial temperature pre-treatments (and a control at ambient temperature). After recovery, fragments experienced a natural thermal stress event either in laboratory conditions or their native reef environment. Response to thermal stress was quantified by measuring changes in the algal symbionts’ photochemical efficiency, community composition, and relative density. Historical bleaching phenotype was reflected in stable differences in symbiont community composition, with historically bleached corals containing only Cladocopium symbionts and historically non-bleached corals having mixed symbiont communities dominated by Durusdinium. Mixed-community corals lost more Cladocopium than Cladocopium-only corals during the natural thermal stress event, and preferentially recovered with Durusdinium. Laboratory pre-treatments exposed corals to more thermal stress than anticipated, causing photochemical damage that varied significantly by genotype. While none of the treatments had a protective effect, temperature variation during treatments had a significant detrimental effect on photochemical efficiency during the thermal stress event. These results show that acclimatization potential is affected by fine-scale differences in temperature regime, host genotype, and relatively stable differences in symbiont community composition that underpin historical bleaching phenotypes in M. capitata.

The effects of multiple stressors on the early life stages of reef-building corals are poorly understood. Elevated temperature is the main physiological driver of mass coral bleaching events, but increasing evidence suggests that other stressors, including elevated dissolved inorganic nitrogen (DIN), may exacerbate the negative effects of thermal stress. To test this hypothesis, we investigated the performance of larvae of Orbicella faveolata and Porites astreoides, two important Caribbean reef coral species with contrasting reproductive and algal transmission modes, under increased temperature and/or elevated DIN. We used a fluorescence-based microplate respirometer to measure the oxygen consumption of coral larvae from both species, and also assessed the effects of these stressors on P. astreoides larval settlement and mortality. Overall, we found that (1) larvae increased their respiration in response to different factors (O. faveolata in response to elevated temperature and P. astreoides in response to elevated nitrate) and (2) P. astreoides larvae showed a significant increase in settlement as a result of elevated nitrate, but higher mortality under elevated temperature. This study shows how microplate respirometry can be successfully used to assess changes in respiration of coral larvae, and our findings suggest that the effects of thermal stress and nitrate enrichment in coral larvae may be species specific and are neither additive nor synergistic for O. faveolata or P. astreoides. These findings may have important consequences for the recruitment and community reassembly of corals to nutrient-polluted reefs that have been impacted by climate change.

Dynamic symbioses with functionally diverse dinoflagellate algae in the genus Symbiodinium may allow some reef corals to alter their phenotypes through ‘symbiont shuffling’, or changes in symbiont community composition. In particular, corals may become more bleaching resistant by increasing the relative abundance of thermally tolerant Symbiodinium in clade D after bleaching. Despite the immediate relevance of this phenomenon to corals living in warming oceans—and to interventions aimed at boosting coral resilience—the mechanisms governing how, why, and when symbiont shuffling occurs are still poorly understood. Here, we performed controlled thermal bleaching and recovery experiments on three species of Caribbean corals hosting mixtures of D1a (S. trenchii) and other symbionts in clades B or C. We show that the degree of symbiont shuffling is related to (1) the duration of stress exposure and (2) the difference in photochemical efficiency (F v /F m) of co-occurring symbionts under stress (i.e., the ‘photochemical advantage’ of one symbiont over the other). The advantage of D1a under stress was greatest in Montastraea cavernosa, intermediate in Siderastrea siderea, and lowest in Orbicella faveolata and correlated positively with the magnitude of shuffling toward D1a. In holobionts where D1a had less of an advantage over co-occurring symbionts (i.e., only slightly higher F v /F m under stress), a longer stress duration was required to elicit commensurate increases in D1a abundance. In fact, across these three coral species, 92.9% of variation in the degree of symbiont shuffling could be explained by the time-integrated photochemical advantage of D1a under heat stress. Although F v /F m is governed by numerous factors that this study is unable to resolve mechanistically, its strong empirical relationship with symbiont shuffling helps elucidate general features that govern this process in reef corals, which will help refine predictions of coral responses to environmental change and inform interventions to manipulate symbiont communities to enhance coral resilience.

Active coral restoration typically involves two interventions: crossing gametes to facilitate sexual larval propagation; and fragmenting, growing, and outplanting adult colonies to enhance asexual propagation. From an evolutionary perspective, the goal of these efforts is to establish self‐sustaining, sexually reproducing coral populations that have sufficient genetic and phenotypic variation to adapt to changing environments. Here, we provide concrete guidelines to help restoration practitioners meet this goal for most Caribbean species of interest. To enable the persistence of coral populations exposed to severe selection pressure from many stressors, a mixed provenance strategy is suggested: genetically unique colonies (genets) should be sourced both locally as well as from more distant, environmentally distinct sites. Sourcing three to four genets per reef along environmental gradients should be sufficient to capture a majority of intraspecies genetic diversity. It is best for practitioners to propagate genets with one or more phenotypic traits that are predicted to be valuable in the future, such as low partial mortality, high wound healing rate, high skeletal growth rate, bleaching resilience, infectious disease resilience, and high sexual reproductive output. Some effort should also be reserved for underperforming genets because colonies that grow poorly in nurseries sometimes thrive once returned to the reef and may harbor genetic variants with as yet unrecognized value. Outplants should be clustered in groups of four to six genets to enable successful fertilization upon maturation. Current evidence indicates that translocating genets among distant reefs is unlikely to be problematic from a population genetic perspective but will likely provide substantial adaptive benefits. Similarly, inbreeding depression is not a concern given that current practices only raise first‐generation offspring. Thus, proceeding with the proposed management strategies even in the absence of a detailed population genetic analysis of the focal species at sites targeted for restoration is the best course of action. These basic guidelines should help maximize the adaptive potential of reef‐building corals facing a rapidly changing environment.

The local environment shapes coral physiology through acclimatization and also selects for genotypes best suited to a particular site. Both acclimatization and selection likely affect the response of corals to future climate change. The local environment is therefore an important factor to consider for restoration ecology. In this study, we exposed Orbicella faveolata from two different locations in Florida (Emerald Reef, near Key Biscayne in the upper Florida Keys, and Truman Harbor near Key West in the lower Florida Keys) that were common-gardened for one month prior to experimentation to four temperature, CO 2 , and food availability treatments (26°C/390 ppm, 26°C/1000 ppm, 31°C/390 ppm, and 31°C/1000 ppm where each of these treatments had fed and unfed components). The goal was to determine how the same species of coral from different locations would respond to projected climate change scenarios. We found that growth (measured as changes in buoyant weight) was highly correlated to source location (i.e., whether the corals came from Emerald Reef or Truman Harbor) and not to parent colony, and growth, symbiont density, chlorophyll a content, and lipid content were highly correlated to feeding regime. These findings show that within a single reef tract, (i.e. the Florida Reef Tract), source location and food availability matter for the physiological outcome of a coral’s stress response, and suggest that an explicit consideration of these effects may be important for management activities such as coral restoration, transplantation, and MPA placement.

Anthropogenic climate change compromises reef growth as a result of increasing temperatures and ocean acidification. Scleractinian corals vary in their sensitivity to these variables, suggesting species composition will influence how reef communities respond to future climate change. Because data are lacking for many species, most studies that model future reef growth rely on uniform scleractinian calcification sensitivities to temperature and ocean acidification. In order to address this knowledge gap, calcification of twelve common and understudied Caribbean coral species was measured for two months under crossed temperatures (27°C, 30.3°C) and CO2 partial pressures (pCO2) (400, 900, 1300 μatm). Mixed effects models of calcification for each species were then used to project community-level scleractinian calcification using Florida Keys reef composition data and IPCC AR5 ensemble climate model data. Three of the four most abundant species, Orbicella faveolata, Montastraea cavernosa, and Porites astreoides, had negative calcification responses to both elevated temperature and pCO2. In the business-as-usual CO2 emissions scenario, reefs with high abundances of these species had projected end-of-century declines in scleractinian calcification of >50% relative to present-day rates. Siderastrea siderea, the other most-common species, was insensitive to both temperature and pCO2 within the levels tested here. Reefs dominated by this species had the most stable end-of-century growth. Under more optimistic scenarios of reduced CO2 emissions, calcification rates throughout the Florida Keys declined

Dredging poses a potential threat to coral reefs, yet quantifying impacts is often difficult due to the large spatial footprint of potential effects and co-occurrence of other disturbances. Here we analyzed in situ monitoring data and remotely-sensed sediment plumes to assess impacts of the 2013–2015 Port of Miami dredging on corals and reef habitat. To control for contemporaneous bleaching and disease, we analyzed the spatial distribution of impacts in relation to the dredged channel. Areas closer to dredging experienced higher sediment trap accumulation, benthic sediment cover, coral burial, and coral mortality, and our spatial analyses indicate that >560,000 corals were killed within 0.5 km, with impacts likely extending over 5–10 km. The occurrence of sediment plumes explained ~60% of spatial variability in measured impacts, suggesting that remotely-sensed plumes, when properly calibrated against in situ monitoring data, can reliably estimate the magnitude and extent of dredging impacts.

Coral populations and structural coral reefs have undergone severe reductions and losses respectively over large parts of the Galapagos Islands during and following the 1982-83 El Nino event. Coral tissue loss amounted to 95% across the Archipelago. Also at that time, all coral reefs in the central and southern islands disappeared following severe degradation and eventual collapse due primarily to intense bioerosion and low recruitment. Six sites in the southern islands have demonstrated low to moderate coral community (scattered colonies, but no carbonate framework) recovery. The iconic pocilloporid reef at Devil's Crown (Floreana Island) experienced recovery to 2007, then severe mortality during a La Nina cooling event, and is again (as of 2017) undergoing rapid recovery. Notable recovery has occurred at the central (Marchena) and northern islands (Darwin and Wolf). Of the 17 structural reefs first observed in the mid-1970s, the single surviving reef (Wellington Reef) at Darwin Island remains in a positive growth mode. The remainder either degraded to a coral community or was lost. Retrospective analyses of the age structure of corals killed in 1983, and isotopic signatures of the skeletal growth record of massive corals suggest the occurrence of robust coral populations during at least a 500-year period before 1983. The greatest potential threats to the recovery and persistence of coral reefs include: ocean warming and acidification, bioerosion, coral diseases, human population growth (increasing numbers of residents and tourists), overfishing, invasive species, pollution, and habitat destruction. Such a diverse spectrum of disturbances, acting alone or in combination, are expected to continue to cause local and archipelago-wide mortality and degradation of the coral reef ecosystem.

Regulating partner abunclance may allow symmotic organisms to mediate interaction outcomes, facilitating adaptive responses to environmental change. To explore the capacity for-adaptive regulation in an ecologically important endosymbiosis, we studied the population dynamics of symbiotic algae in reef-building corals under different abiotic contexts. We found high natural variability in symbiont abundance in corals across reefs, but this variability converged to different symbiont-specific abundances when colonies were maintained under constant conditions. When conditions changed seasonally, symbiont abundance readjusted to new equilibria. We explain these patterns using an a priori model of symbiotic costs and benefits to the coral host, which shows that the observed changes in symbiont abundance are consistent with the maximization of interaction benefit under different environmental conditions. These results indicate that, while regulating symbiont abundance helps hosts sustain maximum benefit in a dynamic environment, spatiotemporal variation in abiotic factors creates a broad range of symbiont abundances (and interaction outcomes) among corals that may account for observed natural variability in performance (e.g., growth rate) and stress tolerance (e.g., bleaching susceptibility). This cost or benefit framework provides a new perspective on the dynamic regulation of reef coral symbioses and illustrates that the dependence of interaction outcomes on biotic and abiotic contexts may be important in understanding how diverse mutualisms respond to environmental change.

Decadal populations changes in four coral taxa and their patterns of association with algal symbionts (Symbiodinium spp. – 10 years of sampling) were examined on Kenyan back reefs over a period of climatic disturbances (1991� 2009). Some of the better surviving taxa, Pavona and Pocillopora, were associated with variable temperature regimes and >50% of sampled colonies in these taxa had some of the more thermally tolerant Symbiodinium in clade D. In contrast, only around 35% of Acropora and no branching forms of Porites contained detectable levels of clade D, and both taxa experienced high levels of thermally-induced mortality and poor recovery. Overall, however the relationship between Symbiodinium clade and population-level success of coral hosts was not strong, and differential success inside and outside fisheries closures suggests that other factors, such as predation on corals, were also influential. Consequently, while Symbiodinium in clade D may contribute to the success of coral hosts across thermal disturbances, multiple ecological factors and additional biological traits also influence their long-term survival.

The growth and survival of reef corals are influenced by their symbiotic algal partners (Symbiodinium spp.), which may be flexible in space and time. Tradeoffs among partnerships exist such that corals with thermotol- erant symbionts (e.g., clade D) resist bleaching but grow more slowly, making the long-term ecosystem-level impacts of different host-symbiont associations uncertain. However, much of this uncertainty is due to limited data regarding these tradeoffs and particularly how they are mediated by the environment. To address this knowledge gap, we measured growth and survival of Pocillopora damicornis with thermally sensitive (clade C) or tolerant (clade D) symbionts at three temperatures over 18-55 weeks. Warming reduced coral growth overall, but altered the tradeoffs associated with symbiont type. While clade D corals grew 35-40 % slower than clade C corals at cooler temperatures (26 C), warming of 1.5-3 C reduced and eliminated this growth disadvantage. These results suggest that although warmer oceans will negatively impact corals, clade D may enhance survival at no cost to growth relative to clade C. Understanding these genotype- environment interactions can help improve modeling efforts and conservation strategies for reefs under global climate change.

Mutualistic organisms can be particularly susceptible to climate change stress, as their survivorship is often limited by the most vulnerable partner. However, symbiotic plasticity can also help organisms in changing environments by expanding their realized niche space. Coral–algal (Symbiodinium spp.) symbiosis exemplifies this dichotomy: the partnership is highly susceptible to ‘bleaching’ (stress-induced symbiosis breakdown), but stress-tolerant symbionts can also sometimes mitigate bleaching. Here, we investigate the role of diverse and mutable symbiotic partnerships in increasing corals' ability to thrive in high temperature conditions. We conducted repeat bleaching and recovery experiments on the coral Montastraea cavernosa, and used quantitative PCR and chlorophyll fluorometry to assess the structure and function of Symbiodinium communities within coral hosts. During an initial heat exposure (32 °C for 10 days), corals hosting only stress-sensitive symbionts (Symbiodinium C3) bleached, but recovered (at either 24 °C or 29 °C) with predominantly (>90%) stress-tolerant symbionts (Symbiodinium D1a), which were not detected before bleaching (either due to absence or extreme low abundance). When a second heat stress (also 32 °C for 10 days) was applied 3 months later, corals that previously bleached and were now dominated by D1a Symbiodinium experienced less photodamage and symbiont loss compared to control corals that had not been previously bleached, and were therefore still dominated by Symbiodinium C3. Additional corals that were initially bleached without heat by a herbicide (DCMU, at 24 °C) also recovered predominantly with D1a symbionts, and similarly lost fewer symbionts during subsequent thermal stress. Increased thermotolerance was also not observed in C3-dominated corals that were acclimated for 3 months to warmer temperatures (29 °C) before heat stress. These findings indicate that increased thermotolerance post-bleaching resulted from symbiont community composition changes, not prior heat exposure. Moreover, initially undetectable D1a symbionts became dominant only after bleaching, and were critical to corals' resilience after stress and resistance to future stress.

Survival trajectories for coral reefs under climate change may depend in part on shifts in the composition of their algal symbiont communities (Symbiodinium spp.). Shifts favoring thermotolerant symbionts have been recorded in response to mass bleaching events but rarely tracked through time. A 10 yr monitoring study of Symbiodinium in a variety of Kenyan corals assessed their variability through time, across coral taxa and between sites, and their relationship to environmental conditions. Coral genera varied significantly in their propensity to host thermo- tolerant symbionts of Symbiodinium clade D, with some genera becoming dominated by clade D at annual maximum temperatures of 32°C but others showing clade D only rarely at 35°C. High annual maximum temperatures, high standard deviation, positive skewness and positive kurtosis characterized sites where clade D was common. In corals whose symbiont communities were ther- mally labile (e.g. Pocillopora) an increase in maximum annual temperature from 30 to 35°C resulted in 3- to 4-fold increases in dominance by clade D. There was no directional change in symbiont communities over the study period, but there was evidence for a ~6 yr decline in the inci- dence of mixed (C + D) communities following the 1998 bleaching event. These data illustrate how acute and chronic thermal stress caused by oceanographic and tidal oscillations interact to pro- duce highly dynamic symbiotic communities. The clade D niche is a function of the environment and host taxon and, through a variety of mechanisms, is expected to expand with climate warm- ing. Corals from warm and variable conditions represent conservation priorities because they establish a niche for these symbionts in contemporary reef environments.

Reef corals are sensitive to thermal stress, which induces coral bleaching (the loss of algal symbionts), often leading to coral mortality. However, corals hosting certain symbionts (notably Symbiodinium in clade D) resist bleaching when exposed to high temperatures. To determine if these symbionts are also cold tolerant, we exposed corals hosting either Symbiodinium C3 or D1a to incremental warming (+1°C week−1 to 35°C) and cooling (−1°C week−1 to 15°C), and measured photodamage and symbiont loss. During warming to 33°C, C3-corals were photodamaged and lost >99% of symbionts, while D1a-corals experienced photodamage but did not bleach. During cooling, D1a-corals suffered more photodamage than C3-corals but still did not bleach, while C3-corals lost 94% of symbionts. These results indicate that photodamage does not always lead to bleaching, suggesting alternate mechanisms exist by which symbionts resist bleaching, and helping explain the persistence of D1a symbionts on recently-bleached reefs, with implications for the future of these ecosystems.

Coral reefs of the eastern tropical Pacific (ETP) are unique in being the only reef region in the world that has experienced multiple episodes of mass coral bleaching while also being exposed to chronically depressed aragonite saturation states as a result of regional upwelling. These characteristics make them ideal case studies for the continued effects of climate change on coral reefs, and in particular for the responses of reef corals and their dinoflagellate algal symbionts (Symbiodinium spp.) to combined climate stressors. As a result, the diversity, distribution and stability of Symbiodinium in ETP corals have been studied since the mid-1990s, shortly after contemporary molecular methods to identify Symbiodinium were first developed. ETP reefs have been instrumental in the discovery that certain members of Symbiodinium in clade D impart bleaching resistance to their coral hosts. In the ETP, clade D is represented by a single symbiont type (D1, also referred to as S. glynni), which has been shown to be tolerant of both episodic El Nino-driven high temperature stress (e.g., 1997 in the Gulf of Chiriqui, Panama), and low temperature stress during an unusually cold winter (e.g., 2008 in Baja California, Mexico). Virtually all studies in the region have focused on corals in the genus Pocillopora, which is both the dominant reef-building genus and the most symbiotically diverse, being the only coral genus in the ETP that routinely hosts heat tolerant D1 symbionts at high abundance. There is debate over the mechanisms by which D1 becomes dominant on pocilloporid reefs, with evidence for both differential mortality of corals, and dynamic change in symbiont communities in response to thermal history and/or disturbance. The relative importance of these two mechanisms is likely to be critical in determining reef survival trajectories over the coming century, as is the degree to which non-pocilloporid corals in the region can associate with, or become dominated by, D1. Dynamic change in symbiont communities may allow corals to survive recurrent bleaching events if stepwise increases in the abundance of D1 following each bleaching event allow these thermotolerant symbionts to accumulate. However, controlled experiments and continued monitoring are required to resolve the debate over symbiont stability versus lability, and there may be significant differences in coral response across the region. Finally, understanding whether different Symbiodinium can alter coral response to high CO2 or depressed aragonite saturation state (Ωarag) remains a priority research area for the region, especially given the potential for strong interactions between Ωarag, coral growth, and symbiont community structure.

Understanding the factors that influence coral susceptibility to thermally induced bleaching may aid reef management efforts. Now corals with high symbiont cell densities are shown to be more susceptible to bleaching, indicating that environmental conditions which increase symbiont densities—such as nutrient pollution—could exacerbate climate-induced coral bleaching.

Some reef-building corals have been shown to respond to environmental change by shifting the composition of their algal symbiont (genus Symbiodinium ) communities. These shifts have been proposed as a potential mechanism by which corals might survive climate stressors, such as increased temperatures. Conventional molecular methods suggest this adaptive capacity may not be widespread because few (∼25%) coral species have been found to associate with multiple Symbiodinium clades. However, these methods can fail to detect low abundance symbionts (typically less than 10–20% of the total algal symbiont community). To determine whether additional Symbiodinium clades are present, but are not detected using conventional techniques, we applied a high-resolution, real-time PCR assay to survey Symbiodinium (in clades A–D) from 39 species of phylogenetically and geographically diverse scleractinian corals. This survey included 26 coral species thought to be restricted to hosting a single Symbiodinium clade (‘symbiotic specialists’). We detected at least two Symbiodinium clades (C and D) in at least one sample of all 39 coral species tested; all four Symbiodinium clades were detected in over half (54%) of the 26 symbiotic specialist coral species. Furthermore, on average, 68 per cent of all sampled colonies within a given coral species hosted two or more symbiont clades. We conclude that the ability to associate with multiple symbiont clades is common in scleractinian (stony) corals, and that, in coral–algal symbiosis, ‘specificity’ and ‘flexibility’ are relative terms: specificity is rarely absolute. The potential for reef corals to adapt or acclimatize to environmental change via symbiont community shifts may therefore be more phylogenetically widespread than has previously been assumed.

The identity and diversity of algal symbionts (Symbiodinium spp.) in reef corals is thought to influence to the resilience of reef ecosystems to climate change, and varies depending on coral species, environmental conditions, and biogeography. We examined these factors by surveying corals along a latitudinal gradient in Western Australia on reefs connected north to south by the warm-water Leeuwin Current. We used the internal transcribed spacer-2 (ITS-2) region of ribosomal DNA to characterize Symbiodinium communities in 19 species of reef coral (in 16 genera) from trop- ical Dampier (20.5° S) to temperate Dunsborough (33.5° S). We documented a high number of novel ITS-2 types in Symbiodinium clades B (1 type) and C (14 types) as well as 7 previously reported ITS- 2 types in clades B, C, and D. In addition, we compared symbiont distributions with Giovanni's OBIG MODIS-Aqua satellite temperature data set and found that the putatively thermotolerant Symbiodi- nium ITS-2 type D1a was more frequently detected in 'chronically warm' tropical sites than at 'chron- ically cool' temperate sites, while clade B symbiont types showed the reverse pattern, being found in certain corals at the southernmost sites. Symbiodinium type D1a was generally most abundant at Dampier, where bleaching had occurred 1 mo prior to sampling, although some variation by host taxa was observed. The diverse and novel Symbiodinium communities documented here may be a result of (1) the variable environmental histories of the study sites, (2) the apparent genetic divergence within this genus resulting from the relative isolation of Western Australian reefs, and/or (3) the fre- quent transport of symbionts (in hospite or free-living) from Indo-Malay reefs to Western Australia via the Leeuwin Current. These results indicate that understudied reefs in remote and isolated areas may contain Symbiodinium diversity that has not been reported previously.

Reef corals are examples of metazoans that engage in mutualisms with a variety of microorganisms, including dinoflagellates, Bacteria, Archaea, and viruses. The high adaptive capacity of these microbial symbionts can be co-opted by their coral hosts, and various emergent traits of these associations, such as thermotolerance, are undergoing strong selection due to climate change. This selection may spur the rise of microbial 'disaster taxa': opportunistic, cosmopolitan generalists that can proliferate and increase host survivorship following disturbances. Coral bleaching (a stress-induced loss of dinoflagellates) constitutes one type of catastrophic disturbance for resident symbiont communities, and opens novel patches of host for colonization by microbial disaster taxa. Moreover, the compartmentalization of microbial symbionts within coral polyps reduces their effective population size and thus facilitates the spread of disaster taxa during times of environmental change. These phenomena suggest that, despite widespread loss of coral cover as a result of climate disturbances, the potential spread of resilient microbial disaster taxa in surviving colonies can have important implications for coral reef persistence over the coming decades.

Surveys of microsatellite variation show that genetic diversity has largely recovered in two reef-building corals, Pocillopora damicornis and Seriatopora hystrix (Scleractinia: Pocilloporidae), on reefs which were decimated by the eruption of the volcano Krakatau in 1883. Assignment methods and gene flow estimates indicate that the recolonization of Krakatau occurred mainly from the closest upstream reef system, Pulau Seribu, but that larval input from other regions has also occurred. This pattern is clearer in S. hystrix, which is traditionally the more dispersal-limited species. Despite these observed patterns of larval dispersal, self-recruitment appears to now be the most important factor in supplying larvae to coral populations in Krakatau. This suggests that the colonization of devastated reefs can occur quickly through larval dispersal; however, their survival requires local sources of larvae for self-recruitment. This research supports the observation that the recovery of genetic diversity in coral reef animals can occur on the order of decades and centuries rather than millennia. Conservation measures aimed at sustaining coral reef populations in Krakatau and elsewhere should include both the protection of upstream source populations for larval replenishment should disaster occur as well as the protection of large adult colonies to serve as local larval sources.

Since the early 1980s, episodes of coral reef bleaching and mortality, due primarily to climate-induced ocean warming, have occurred almost annually in one or more of the world's tropical or subtropical seas. Bleaching is episodic, with the most severe events typically accompanying coupled ocean–atmosphere phenomena, such as the El Nino-Southern Oscillation (ENSO), which result in sustained regional elevations of ocean temperature. Using this extended dataset (25+ years), we review the short- and long-term ecological impacts of coral bleaching on reef ecosystems, and quantitatively synthesize recovery data worldwide. Bleaching episodes have resulted in catastrophic loss of coral cover in some locations, and have changed coral community structure in many others, with a potentially critical influence on the maintenance of biodiversity in the marine tropics. Bleaching has also set the stage for other declines in reef health, such as increases in coral diseases, the breakdown of reef framework by bioeroders, and the loss of critical habitat for associated reef fishes and other biota. Secondary ecological effects, such as the concentration of predators on remnant surviving coral populations, have also accelerated the pace of decline in some areas. Although bleaching severity and recovery have been variable across all spatial scales, some reefs have experienced relatively rapid recovery from severe bleaching impacts. There has been a significant overall recovery of coral cover in the Indian Ocean, where many reefs were devastated by a single large bleaching event in 1998. In contrast, coral cover on western Atlantic reefs has generally continued to decline in response to multiple smaller bleaching events and a diverse set of chronic secondary stressors. No clear trends are apparent in the eastern Pacific, the central-southern-western Pacific or the Arabian Gulf, where some reefs are recovering and others are not. The majority of survivors and new recruits on regenerating and recovering coral reefs have originated from broadcast spawning taxa with a potential for asexual growth, relatively long distance dispersal, successful settlement, rapid growth and a capacity for framework construction. Whether or not affected reefs can continue to function as before will depend on: (1) how much coral cover is lost, and which species are locally extirpated; (2) the ability of remnant and recovering coral communities to adapt or acclimatize to higher temperatures and other climatic factors such as reductions in aragonite saturation state; (3) the changing balance between reef accumulation and bioerosion; and (4) our ability to maintain ecosystem resilience by restoring healthy levels of herbivory, macroalgal cover, and coral recruitment. Bleaching disturbances are likely to become a chronic stress in many reef areas in the coming decades, and coral communities, if they cannot recover quickly enough, are likely to be reduced to their most hardy or adaptable constituents. Some degraded reefs may already be approaching this ecological asymptote, although to date there have not been any global extinctions of individual coral species as a result of bleaching events. Since human populations inhabiting tropical coastal areas derive great value from coral reefs, the degradation of these ecosystems as a result of coral bleaching and its associated impacts is of considerable societal, as well as biological concern. Coral reef conservation strategies now recognize climate change as a principal threat, and are engaged in efforts to allocate conservation activity according to geographic-, taxonomic-, and habitat-specific priorities to maximize coral reef survival. Efforts to forecast and monitor bleaching, involving both remote sensed observations and coupled ocean–atmosphere climate models, are also underway. In addition to these efforts, attempts to minimize and mitigate bleaching impacts on reefs are immediately required. If significant reductions in greenhouse gas emissions can be achieved within the next two to three decades, maximizing coral survivorship during this time may be critical to ensuring healthy reefs can recover in the long term.

Reciprocal transplant experiments of the corals Pocillopora eydouxi Milne Edwards & Haime and Porites lobata Dana were carried out for an 18-month period from September 2004 to March 2006 between two back reef pools on Ofu Island, American Samoa, to test environmental versus genetic effects on skeletal growth rates. Skeletal growth of P. eydouxi showed environmental but not genetic effects, resulting in doubling of growth in Pool 300 compared with Pool 400. There were no environmental or genetic effects on skeletal growth of P. lobata. Pool 300 had more frequent and longer durations of elevated seawater temperatures than Pool 400, characteristics likely to decrease rather than increase skeletal growth. Pool 300 also had higher nutrient levels and flow velocities than Pool 400, characteristics that may increase skeletal growth. However, higher nutrient levels would be expected to increase skeletal growth in both species, but there was no difference between the pools in P. lobata growth. P. eydouxi is much more common in high-energy environments than P. lobata; thus the higher flow velocities in Pool 300 than in Pool 400 may have positively affected skeletal growth of P. eydouxi while not having a detectable effect on P. lobata. The greater skeletal growth of P. eydouxi in Pool 300 occurred despite the presence of clade D zooxanthellae in several source colonies in Pool 300, a genotype known to result in greater heat resistance but slower skeletal growth. Increased skeletal growth rates in higher water motion may provide P. eydouxi a competitive advantage in shallow, high-energy environments where competition for space is intense.

The ability of reef corals to adapt or acclimatize to projected climate change is a critical, but controversial, question in contemporary coral reef science and conservation. Much research has focused on whether or not corals are able to flexibly associate with diverse symbionts ('zooxanthel- lae') whose different physiologies may impart greater resistance to environmental extremes. Goulet (2006; Mar Ecol Prog Ser 321:1-7) concluded that most coral species only host zooxanthellae from a single Symbiodinium clade, and that these symbionts do not change in response to environmental disturbance, disease, or temperature stress. We re-evaluate her data and show that: (1) almost two-thirds of the coral species investigated have been severely undersampled (N ≤ 5); (2) more than three-quarters of the scleractinian (stony) coral species sampled more adequately (N > 10) host mul- tiple Symbiodinium clades, or multiple types within a clade; (3) scleractinian corals are more flexible than octocorals; (4) almost all scleractinian coral families can host more than one symbiont clade. Moreover, the molecular approaches used by many studies are likely to have underestimated Sym- biodinium diversity, because they are unable to detect symbionts at low abundance and because they cannot distinguish between closely related types. In addition, various other studies show that: (1) scleractinian corals commonly host multiple symbiont types within a Symbiodinium clade; (2) symbiont communities in scleractinian corals are dynamic; (3) 'cryptic' symbiont taxa found at low abundance within colonies are unlikely to be molecular artifacts. We suggest that the majority of scleractinian coral species, including virtually all of the dominant reef-building taxa, can be found hosting multiple symbiont types, even at the clade level. This flexibility is important in under- standing the past evolutionary success of these species and their future survival trajectories in the face of projected climate change.

Coral reefs are subjected globally to a variety of natural and anthropogenic stressors that often act synergistically. Today, reversing ongoing and future coral reef degradation presents significant challenges and countering this negative trend will take considerable efforts and investments. Scientific knowledge can inform and guide the requisite decision-making process and offer practical solutions to the problem of protection as the effects of climate change exacerbate. However, implementation of solutions presently lags far behind the pace required to reverse global declines, and there is a need for an urgent and significant step-up in the extent and range of strategies being implemented. In this paper, we consider scientific frontiers in natural and social science research that can help build stronger support for reef management and improve the efficacy of interventions. We cover various areas including: (1) enhancing the case for reef conservation and management, (2) dealing with local stressors on reefs, (3) addressing global climate change impacts, (4) and reviewing various approaches to the governance of coral reefs. In sum, we consider scientific frontiers in natural and social science that will require further attention in coming years as managers’ work towards building stronger support for reef management and improve the efficacy of local interventions.

Reef corals (and other marine invertebrates and protists) are hosts to a group of exceptionally diverse dinoflagellate symbionts in the genus Symbiodinium. These symbionts are critical components of coral reef ecosystems whose loss during stress-related “bleaching” events can lead to mass mortality of coral hosts and associated collapse of reef ecosystems. Molecular studies have shown these partnerships to be more flexible than previously thought, with different hosts and symbionts showing varying degrees of specificity in their associations. Further studies are beginning to reveal the systematic, ecological, and biogeographic underpinnings of this flexibility. Unusual symbionts normally found only in larval stages, marginal environments, uncommon host taxa, or at latitudinal extremes may prove critical in understanding the long-term resilience of coral reef ecosystems to environmental perturbation. The persistence of bleaching-resistant symbiont types in affected ecosystems, and the possibility of recombination among different partners following bleaching, may lead to significant shifts in symbiont community structure and elevations of future bleaching thresholds. Monitoring symbiont communities worldwide is essential to understanding the long-term response of reefs to global climate change because it will help resolve current controversy over the timescales over which symbiont change might occur. Symbiont diversity should be explicitly incorporated into the design of coral reef Marine Protected Areas (MPAs) where resistance or resilience to bleaching is a consideration.

Summary Reef-building corals are vulnerable to heat stress and are facing widespread losses due to climate change. A new study shows that coral heat tolerance can result from selection on a suite of genes to maintain genetic flexibility.

The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others. However, these interaction outcomes may also depend on partner abundance, with differences in the total number of symbionts changing the net benefit to the coral host, depending on the particular environmental conditions. We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses. This density-dependent framework suggests that corals may regulate the size of their symbiont pool to match microhabitat-specific optima, which may contribute to the high spatiotemporal variability in symbiont abundance observed within and among colonies and reefs. Differences in symbiont standing stock may subsequently explain variation in energetics, growth, reproduction, and stress susceptibility, and may mediate the impacts of environmental change on these outcomes. However, the importance of symbiont abundance has received relatively little recognition, possibly because commonly-used metrics based on surface area (e.g., symbiont cells cm(-2)) may be only weakly linked to biological phenomena and are difficult to compare across studies. We suggest that normalizing symbionts to biological host parameters, such as units of protein or numbers of host cells, will more clearly elucidate the functional role of symbiont abundance in reef coral symbioses. In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.

International audience; : The deep reef refugia hypothesis proposes that deep reefs can act as local recruitment sources for shallow reefs following disturbance. To test this hypothesis, nine polymorphic DNA microsatellite loci were developed and used to assess vertical connectivity in 583 coral colonies of the Caribbean depth-generalist coral Montastraea cavernosa. Samples were collected from three depth zones (≤10, 15-20 and ≥25 m) at sites in Florida (within the Upper Keys, Lower Keys and Dry Tortugas), Bermuda, and the U.S. Virgin Islands. Migration rates were estimated to determine the probability of coral larval migration from shallow to deep and from deep to shallow. Finally, algal symbiont (Symbiodinium spp.) diversity and distribution were assessed in a subset of corals to test whether symbiont depth zonation might indicate limited vertical connectivity. Overall, analyses revealed significant genetic differentiation by depth in Florida, but not in Bermuda or the U.S. Virgin Islands, despite high levels of horizontal connectivity between these geographic locations at shallow depths. Within Florida, greater vertical connectivity was observed in the Dry Tortugas compared to the Lower or Upper Keys. However, at all sites, and regardless of the extent of vertical connectivity, migration occurred asymmetrically, with greater likelihood of migration from shallow to intermediate/deep habitats. Finally, most colonies hosted a single Symbiodinium type (C3), ruling out symbiont depth zonation of the dominant symbiont type as a structuring factor. Together, these findings suggest that the potential for shallow reefs to recover from deep-water refugia in M. cavernosa is location-specific, varying among and within geographic locations likely as a consequence of local hydrology.

Managing coral reefs for resilience to climate change is a popular concept but has been difficult to implement because the empirical scientific evidence has either not been evaluated or is sometimes unsupportive of theory, which leads to uncertainty when considering methods and identifying priority reefs. We asked experts and reviewed the scientific literature for guidance on the multiple physical and biological factors that affect the ability of coral reefs to resist and recover from climate disturbance. Eleven key factors to inform decisions based on scaling scientific evidence and the achievability of quantifying the factors were identified. Factors important to resistance and recovery, which are important components of resilience, were not strongly related, and should be assessed independently. The abundance of resistant (heat-tolerant) coral species and past temperature variability were perceived to provide the greatest resistance to climate change, while coral recruitment rates, and macroalgae abundance were most influential in the recovery process. Based on the 11 key factors, we tested an evidence-based framework for climate change resilience in an Indonesian marine protected area. The results suggest our evidence-weighted framework improved upon existing un-weighted methods in terms of characterizing resilience and distinguishing priority sites. The evaluation supports the concept that, despite high ecological complexity, relatively few strong variables can be important in influencing ecosystem dynamics. This is the first rigorous assessment of factors promoting coral reef resilience based on their perceived importance, empirical evidence, and feasibility of measurement. There were few differences between scientists' perceptions of factor importance and the scientific evidence found in journal publications but more before and after impact studies will be required to fully test the validity of all the factors. The methods here will increase the feasibility and defensibility of including key resilience metrics in evaluations of coral reefs, as well as reduce costs. Adaptation, marine protected areas, priority setting, resistance, recovery.

Corals in the Arabian/Persian Gulf endure summer temperatures of up to 36 °C, making them ideal subjects to study the mechanisms underlying thermal tolerance. Unexpectedly, we found the “generalist” Symbiodinium clade C3 to be the prevalent symbiont among seven coral species from Abu Dhabi (UAE) waters. Moreover, C3 represented the only dominant symbiont type in Porites spp. from this region. The “thermotolerant” symbionts D1a and C15 were not encountered, indicating that the association with these symbionts cannot be the sole reason for the heat tolerance of Gulf corals. The association of Porites lobata with specific symbiont types (C3 vs. C15) in samples from habitats with very different temperature regimes (Abu Dhabi vs. Fiji) remained unaffected by laboratory culture. During temperature stress experiments specimens from both locations strongly downregulated green fluorescent protein (GFP)-like pigments. However, the Abu Dhabi samples were less prone to bleaching and showed lower mortality.

Mass coral reef bleaching and mortality as a result of prolonged seawater warming following the 1997–1998 El Nino-Southern Oscillation forced a change in conservation priorities in assessing threats to the health of coral reefs worldwide. By some estimates, approximately one sixth of the world’s coral reefs was destroyed over a single 9-month period during the 1997–1998 bleaching event (Wilkinson 2000). Most of this destruction occurred in the Indian Ocean, where prolonged elevations of sea surface temperature were maintained by prevailing currents that pooled warm water in the western Indo-Pacific. In most cases, coral reef destruction equated to a dramatic reduction in live coral cover on these reefs (e.g., McClanahan 2000; Loch et al. 2002), but it is noteworthy that even the most severely affected reefs maintained significant pockets of live coral scattered throughout their original distributions. Moreover, many coral reef ecosystems that suffered extensive bleaching (e.g., parts of the Caribbean and Great Barrier Reef) did not experience significant eventual mortality (Wilkinson 2002). Consequently, coral reef recovery has in many places been more rapid than initially expected, particularly in the western Pacific. Although 1997–1998 clearly represents an annus horribilis for many coral reefs worldwide, the destruction it witnessed may not be as irreversible or as cumulative as originally thought. How resistant and/or resilient were reef corals (and coral reefs) to this event? How might resistance and resilience change over time in response to rising temperatures and recurrent bleaching episodes? To what extent can we expect the destruction and recovery patterns of 1997–1998 to be common features of reef bleaching and mortality in the years to come?

Biodiversity stabilizes ecosystem functioning in small-scale, short-term experiments, but do such findings scale up to the larger world? A global study of fossil reefs from the past 500 million years suggests they do.

The bleaching of coral reefs, in which symbiotic algae are lost from reef-building invertebrates, is usually considered to be a drastic and damaging response to adverse environmental conditions1,2. Here I report results from transplant experiments involving different combinations of coral host and algal symbiont that support an alternative view, in which bleaching offers a high-risk ecological opportunity for reef corals to rid themselves rapidly of suboptimal algae and to acquire new partners. This strategy could be an advantage to coral reefs that face increasingly frequent and severe episodes of mass bleaching as a result of projected climate change2,3.

The long-term response of coral reefs to climate change depends on the ability of reef-building coral symbioses to adapt or acclimatize to warmer temperatures, but there has been no direct evidence that such a response can occur. Here we show that corals containing unusual algal symbionts that are thermally tolerant and commonly associated with high-temperature environments are much more abundant on reefs that have been severely affected by recent climate change. This adaptive shift in symbiont communities indicates that these devastated reefs could be more resistant to future thermal stress, resulting in significantly longer extinction times for surviving corals than had been previously assumed.