Tolerance Of Corals Research Articles

Elevated CO2 Has Little Influence on the Bacterial Communities Associated With the pH-Tolerant Coral, Massive Porites spp.

Ocean acidification (OA) as a result of increased anthropogenic CO2 input into the atmosphere carries consequences for all ocean life. Low pH can cause a shift in coral-associated microbial communities of pCO2-sensitive corals, however, it remains unknown whether the microbial community is also influenced in corals known to be more tolerant to high pCO2/low pH. This study profiles the bacterial communities associated with the tissues of the pCO2-tolerant coral, massive Porites spp., from two natural CO2 seep sites in Papua New Guinea. Amplicon sequencing of the hypervariable V3-V4 regions of the 16S rRNA gene revealed that microbial communities remained stable across CO2 seep sites (pH = 7.44–7.85) and adjacent control sites (ambient pH = 8.0–8.1). Microbial communities were more significantly influenced by reef location than pH, with the relative abundance of dominant microbial taxa differing between reefs. These results directly contrast with previous findings that increased CO2 has a strong effect on structuring microbial communities. The stable structure of microbial communities associated with the tissues of massive Porites spp. under high pCO2/low pH conditions confirms a high degree of tolerance by the whole Porites holobiont to OA, and suggest that pH tolerant corals such as Porites may dominate reef assemblages in an increasingly acidic ocean.

Warmer Water Affects Immunity of a Tolerant Reef Coral

Corals are multipartite sedentary organisms, which have evolved complex, physiological networks in order to survive perturbations and environmental fluctuations. However, climate change is warming tropical waters, pushing the limits of coral tolerance and driving global declines. Coral susceptibility to thermal anomalies is variable among species and through time, and directly relates to constituent immunity. Constituent immunity refers to immune activities required to ensure homeostasis, whereas an immune response is acutely heightened immune activity to a perturbation. Understanding the mechanisms behind coral health, and sustained health through adverse conditions, is increasingly important for establishing effective reef conservation and restoration projects. However, most experimental studies of coral health use species that are highly susceptible to thermal events, potentially skewing our understanding. To determine the influence of warmer water on immunity, activities of key coral immune pathways and an antioxidant were compared under ambient (27 oC) and warmer water (32 oC), and between injured and uninjured (control) branches of the tolerant reef coral Porites cylindrica. Three types of phenoloxidase, mono-phenoloxidase, ortho-diphenoloxidase and para-diphenloxidase, indicative of two melanin synthesis pathways (the tyrosinase and laccase-type), and peroxidase were measured at 0 (control), 1, 6, 24, 48 and 168 h post-injury. All four enzymes demonstrated consistent levels of activity under ambient conditions (27 oC), indicating constituent immunity. Upon injury at ambient temperature, all enzyme activities were significantly higher 1 h post-injury as compared to uninjured controls, demonstrating a comprehensive immune response to tissue disruption. Under warmer water, constituent immunity increased through time indicative of immune modulation to maintain homeostasis. However, warmer water, within the non-bleaching summer range, suppressed the immune response to injury, delaying it by 24 hrs. Therefore, upon the environmental cue of warmer water, the tolerant coral P. cylindrica may divert resources away from immune responses (immunosuppression) while enhancing constituent immunity (immune modulation) so as to maintain health through sub-optimal conditions. These changes in immunity with warmer water demonstrates that temperature affects coral immunity and, for this tolerant coral, triggers immune-modulation that may provide cross-tolerance to perturbations more frequent in summer months, such as bleaching and disease.

Variable thermal stress tolerance of the reef-associated symbiont-bearing foraminifera Amphistegina linked to differences in symbiont type

Adaptation, acclimatization and symbiont diversity are known to regulate thermal tolerance in corals, but the role of these mechanisms remains poorly constrained in other photosymbioses, such as large benthic foraminifera (LBFs), which are known to bleach at temperatures that are likely to be exceeded in the near future. LBFs inhabit a broad range of shallow-water settings. Within species, differences in thermal tolerance have been found among populations from different habitats, but it is not clear whether such differences occur among LBFs inhabiting similar habitats, but differing in other aspects, such as symbiont type. To this end, we compared responses to thermal stress in specimens from a population of Amphistegina lessonii, an abundant Indo-Pacific species, to specimens of Amphistegina gibbosa, its Atlantic counterpart, from a similar environment but two different water depths (5 and 18 m). Test groups of each species were exposed in a common experiment to three thermal stress scenarios over a four-week period. Growth, respiration, mortality and motility were measured to characterize the holobiont response. Coloration, photosynthesis and chlorophyll a content were measured to determine the response of the endosymbiotic diatoms. The photosymbionts were characterized by genetic fingerprinting. Our results show that, although groups of A. gibbosa were collected from different habitats, their responses were similar, indicating only marginally higher tolerance to thermal peaks in specimens from the shallower site. In contrast, species-specific differences were stronger, with A. lessonii showing higher tolerance to episodic stress and less pronounced impacts of chronic stress on motility, growth and photosymbiont performance. These interspecies variations are consistent with the presence of different and more diverse symbiont assemblages in A. lessonii compared with A. gibbosa. This study demonstrates the importance of considering symbiont diversity in the assessment of intra- and interspecific variations in stress responses in LBFs.

Dynamics of coral-associated microbiomes during a thermal bleaching event.

Coral‐associated microorganisms play an important role in their host fitness and survival. A number of studies have demonstrated connections between thermal tolerance in corals and the type/relative abundance of Symbiodinium they harbor. More recently, the shifts in coral‐associated bacterial profiles were also shown to be linked to the patterns of coral heat tolerance. Here, we investigated the dynamics of Porites lutea‐associated bacterial and algal communities throughout a natural bleaching event, using full‐length 16S rRNA and internal transcribed spacer sequences (ITS) obtained from PacBio circular consensus sequencing. We provided evidence of significant changes in the structure and diversity of coral‐associated microbiomes during thermal stress. The balance of the symbiosis shifted from a predominant association between corals and Gammaproteobacteria to a predominance of Alphaproteobacteria and to a lesser extent Betaproteobacteria following the bleaching event. On the contrary, the composition and diversity of Symbiodinium communities remained unaltered throughout the bleaching event. It appears that the switching and/or shuffling of Symbiodinium types may not be the primary mechanism used by P. lutea to cope with increasing seawater temperature. The shifts in the structure and diversity of associated bacterial communities may contribute more to the survival of the coral holobiont under heat stress.

The Future of Coral Reefs Subject to Rapid Climate Change: Lessons from Natural Extreme Environments

Global climate change and localised anthropogenic stressors are driving rapid declines in coral reef health. In vitro experiments have been fundamental in providing insight into how reef organisms will potentially respond to future climates. However, such experiments are inevitably limited in their ability to reproduce the complex interactions that govern reef systems. Studies examining coral communities that already persist under naturally-occurring extreme and marginal physicochemical conditions have therefore become increasingly popular to advance ecosystem scale predictions of future reef form and function, although no single site provides a perfect analogue to future reefs. Here we review the current state of knowledge that exists on the distribution of corals in marginal and extreme environments, and geographic sites at the latitudinal extremes of reef growth, as well as a variety of shallow reef systems and reef-neighbouring environments (including upwelling and CO2 vent sites). We also conduct a synthesis of the abiotic data that have been collected at these systems, to provide the first collective assessment on the range of extreme conditions under which corals currently persist. We use the review and data synthesis to increase our understanding of the biological and ecological mechanisms that facilitate survival and success under sub-optimal physicochemical conditions. This comprehensive assessment can begin to: (i) highlight the extent of extreme abiotic scenarios under which corals can persist, (ii) explore whether there are commonalities in coral taxa able to persist in such extremes, (iii) provide evidence for key mechanisms required to support survival and/or persistence under sub-optimal environmental conditions, and iv) evaluate the potential of current sub-optimal coral environments to act as potential refugia under changing environmental conditions. Such a collective approach is critical to better understand the future survival of corals in our changing environment. We finally outline priority areas for future research on extreme and marginal coral environments, and discuss the additional management options they may provide for corals through refuge or by providing genetic stocks of stress tolerant corals to support proactive management strategies.

Mechanisms of Thermal Tolerance in Reef-Building Corals across a Fine-Grained Environmental Mosaic: Lessons from Ofu, American Samoa

Environmental heterogeneity gives rise to phenotypic variation through a combination of phenotypic plasticity and fixed genetic effects. For reef-building corals, understanding the relative roles of acclimatization and adaptation in generating thermal tolerance is fundamental to predicting future response of coral populations to future climate change. The temperature mosaic in the lagoon of Ofu Island, American Samoa, represents an ideal natural laboratory for studying thermal tolerance in corals. Two adjacent back-reef pools 500 meters apart have different temperature profiles: the highly variable (HV) pool experiences temperatures that range from 24.5°C to 35°C, whereas the moderately variable (MV) pool ranges from 25°C to 32°C. Standardized heat stress tests have shown that corals native to the HV pool have consistently higher levels of bleaching resistance than those in the MV pool. In this review, we summarize research into the mechanisms underlying this variation in bleaching resistance, focusing on the important reef-building genus Acropora. Both acclimatization and adaptation occur strongly and define thermal tolerance differences between pools. Most individual corals shift physiology to become more heat resistant when moved into the warmer pool. Lab based tests show that these shifts begin in as little as a week and are equally sparked by exposure to periodic high temperatures as constant high temperatures. Genome-wide data on gene expression show that a wide variety of genes are co-regulated in expression modules that change expression after experimental heat stress, after acclimatization, and even after short term environmental fluctuations. Population genetic scans have shown associations between a corals’ thermal environmental and its alleles at 100s to 1000s of nuclear genes and no single gene confers strong environmental effects within or between species. Symbionts also tend to differ between pools and species, and the thermal tolerance of a coral is a reflection of individual host genotype and specific symbiont types. We conclude the review by placing this work in the context of parallel research going on in other species, reefs and ecosystems around the world and into the broader framework of reef coral resilience in the face of near future climate change.

Coral physiology and microbiome dynamics under combined warming and ocean acidification.

Rising seawater temperature and ocean acidification threaten the survival of coral reefs. The relationship between coral physiology and its microbiome may reveal why some corals are more resilient to these global change conditions. Here, we conducted the first experiment to simultaneously investigate changes in the coral microbiome and coral physiology in response to the dual stress of elevated seawater temperature and ocean acidification expected by the end of this century. Two species of corals, Acropora millepora containing the thermally sensitive endosymbiont C21a and Turbinaria reniformis containing the thermally tolerant endosymbiont Symbiodinium trenchi, were exposed to control (26.5°C and pCO2 of 364 μatm) and treatment (29.0°C and pCO2 of 750 μatm) conditions for 24 days, after which we measured the microbial community composition. These microbial findings were interpreted within the context of previously published physiological measurements from the exact same corals in this study (calcification, organic carbon flux, ratio of photosynthesis to respiration, photosystem II maximal efficiency, total lipids, soluble animal protein, soluble animal carbohydrates, soluble algal protein, soluble algal carbohydrate, biomass, endosymbiotic algal density, and chlorophyll a). Overall, dually stressed A. millepora had reduced microbial diversity, experienced large changes in microbial community composition, and experienced dramatic physiological declines in calcification, photosystem II maximal efficiency, and algal carbohydrates. In contrast, the dually stressed coral T. reniformis experienced a stable and more diverse microbiome community with minimal physiological decline, coupled with very high total energy reserves and particulate organic carbon release rates. Thus, the microbiome changed and microbial diversity decreased in the physiologically sensitive coral with the thermally sensitive endosymbiotic algae but not in the physiologically tolerant coral with the thermally tolerant endosymbiont. Our results confirm recent findings that temperature-stress tolerant corals have a more stable microbiome, and demonstrate for the first time that this is also the case under the dual stresses of ocean warming and acidification. We propose that coral with a stable microbiome are also more physiologically resilient and thus more likely to persist in the future, and shape the coral species diversity of future reef ecosystems.

High-frequency temperature variability mirrors fixed differences in thermal limits of the massive coral Porites lobata.

Spatial heterogeneity in environmental characteristics can drive adaptive differentiation when contrasting environments exert divergent selection pressures. This environmental and genetic heterogeneity can substantially influence population and community resilience to disturbance events. Here, we investigated corals from the highly variable back-reef habitats of Ofu Island in American Samoa that thrive in thermal conditions known to elicit widespread bleaching and mortality elsewhere. To investigate the relative importance of acclimation versus site of origin in shaping previously observed differences in coral tolerance limits at Ofu Island, specimens of the common Indo-Pacific coral Porites lobata from locations with differing levels of thermal variability were acclimated to low and high thermal variation in controlled common garden aquaria. Overall, there were minimal effects of the acclimation exposure. Corals native to the site with the highest level of daily variability grew fastest, regardless of acclimation treatment. When exposed to lethal thermal stress, corals native to both variable sites contained elevated levels of heat shock proteins and maintained photosynthetic performance for 1-2 days longer than corals from the stable environment. Despite being separated by <5 km, there was significant genetic differentiation among coral colonies (FST=0.206, P<0.0001; nuclear ribosomal DNA), whereas Symbiodiniaceae were all Cladocopium sp. (ITS type C15). Our study demonstrates consistent signatures of adaptation in growth and stress resistance in corals from naturally thermally variable habitats, suggesting that differences in the amount of thermal variability may be an important contributor to adaptive differentiation in reef-building corals.

Mesopredator trophodynamics on thermally stressed coral reefs

Ecosystems are becoming vastly modified through disturbance. In coral reef ecosystems, the differential susceptibility of coral taxa to climate-driven bleaching is predicted to shift coral assemblages towards reefs with an increased relative abundance of taxa with high thermal tolerance. Many thermally tolerant coral species are characterised by low structural complexity, with reduced habitat niche space for the small-bodied coral reef fishes on which piscivorous mesopredators feed. This study used a patch reef array to investigate the potential impacts of climate-driven shifts in coral assemblages on the trophodynamics of reef mesopredators and their prey communities. The ‘tolerant’ reef treatment consisted only of coral taxa of low susceptibility to bleaching, while ‘vulnerable’ reefs included species of moderate to high thermal vulnerability. ‘Vulnerable’ reefs had higher structural complexity, and the fish assemblages that established on these reefs over 18 months had higher species diversity, abundance and biomass than those on ‘tolerant’ reefs. Fish assemblages on ‘tolerant’ reefs were also more strongly influenced by the introduction of a mesopredator (Cephalopholis boenak). Mesopredators on ‘tolerant’ reefs had lower lipid content in their muscle tissue by the end of the 6-week experiment. Such sublethal energetic costs can compromise growth, fecundity, and survivorship, resulting in unexpected population declines in long-lived mesopredators. This study provides valuable insight into the altered trophodynamics of future coral reef ecosystems, highlighting the potentially increased vulnerability of reef fish assemblages to predation as reef structure declines, and the cost of changing prey availability on mesopredator condition.

ENSO Weather and Coral Bleaching on the Great Barrier Reef, Australia

AbstractThe most devastating mass coral bleaching has occurred during El Niño events, with bleaching reported to be a direct result of increased sea surface temperatures (SSTs). However, El Niño itself does not cause SSTs to rise in all regions that experience bleaching. Nor is the upper ocean warming trend of 0.11°C per decade since 1971, attributed to global warming, sufficient alone to exceed the thermal tolerance of corals. Here we show that weather patterns during El Niño that result in reduced cloud cover, higher than average air temperatures and higher than average atmospheric pressures, play a crucial role in determining the extent and location of coral bleaching on the world's largest coral reef system, the World Heritage Great Barrier Reef (GBR), Australia. Accordingly, synoptic‐scale weather patterns and local atmosphere‐ocean feedbacks related to El Niño–Southern Oscillation (ENSO) and not large‐scale SST warming due to El Niño alone and/or global warming are often the cause of coral bleaching on the GBR.

The contribution of microbial biotechnology to mitigating coral reef degradation.

The decline of coral reefs due to anthropogenic disturbances is having devastating impacts on biodiversity and ecosystem services. Here we highlight the potential and challenges of microbial manipulation strategies to enhance coral tolerance to stress and contribute to coral reef restoration and protection.

Engineering Strategies to Decode and Enhance the Genomes of Coral Symbionts.

Elevated sea surface temperatures from a severe and prolonged El Niño event (2014–2016) fueled by climate change have resulted in mass coral bleaching (loss of dinoflagellate photosymbionts, Symbiodinium spp., from coral tissues) and subsequent coral mortality, devastating reefs worldwide. Genetic variation within and between Symbiodinium species strongly influences the bleaching tolerance of corals, thus recent papers have called for genetic engineering of Symbiodinium to elucidate the genetic basis of bleaching-relevant Symbiodinium traits. However, while Symbiodinium has been intensively studied for over 50 years, genetic transformation of Symbiodinium has seen little success likely due to the large evolutionary divergence between Symbiodinium and other model eukaryotes rendering standard transformation systems incompatible. Here, we integrate the growing wealth of Symbiodinium next-generation sequencing data to design tailored genetic engineering strategies. Specifically, we develop a testable expression construct model that incorporates endogenous Symbiodinium promoters, terminators, and genes of interest, as well as an internal ribosomal entry site from a Symbiodinium virus. Furthermore, we assess the potential for CRISPR/Cas9 genome editing through new analyses of the three currently available Symbiodinium genomes. Finally, we discuss how genetic engineering could be applied to enhance the stress tolerance of Symbiodinium, and in turn, coral reefs.

Restricted gene flow and local adaptation highlight the vulnerability of high-latitude reefs to rapid environmental change.

Global climate change poses a serious threat to the future health of coral reef ecosystems. This calls for management strategies that are focused on maximizing the evolutionary potential of coral reefs. Fundamental to this is an accurate understanding of the spatial genetic structure in dominant reef-building coral species. In this study, we apply a genotyping-by-sequencing approach to investigate genome-wide patterns of genetic diversity, gene flow, and local adaptation in a reef-building coral, Pocillopora damicornis, across 10 degrees of latitude and a transition from temperate to tropical waters. We identified strong patterns of differentiation and reduced genetic diversity in high-latitude populations. In addition, genome-wide scans for selection identified a number of outlier loci putatively under directional selection with homology to proteins previously known to be involved in heat tolerance in corals and associated with processes such as photoprotection, protein degradation, and immunity. This study provides genomic evidence for both restricted gene flow and local adaptation in a widely distributed coral species, and highlights the potential vulnerability of leading-edge populations to rapid environmental change as they are locally adapted, reproductively isolated, and have reduced levels of genetic diversity.

Shifting paradigms in restoration of the world's coral reefs.

Many ecosystems around the world are rapidly deteriorating due to both local and global pressures, and perhaps none so precipitously as coral reefs. Management of coral reefs through maintenance (e.g., marine-protected areas, catchment management to improve water quality), restoration, as well as global and national governmental agreements to reduce greenhouse gas emissions (e.g., the 2015 Paris Agreement) is critical for the persistence of coral reefs. Despite these initiatives, the health and abundance of corals reefs are rapidly declining and other solutions will soon be required. We have recently discussed options for using assisted evolution (i.e., selective breeding, assisted gene flow, conditioning or epigenetic programming, and the manipulation of the coral microbiome) as a means to enhance environmental stress tolerance of corals and the success of coral reef restoration efforts. The 2014-2016 global coral bleaching event has sharpened the focus on such interventionist approaches. We highlight the necessity for consideration of alternative (e.g., hybrid) ecosystem states, discuss traits of resilient corals and coral reef ecosystems, and propose a decision tree for incorporating assisted evolution into restoration initiatives to enhance climate resilience of coral reefs.

Air exposure of coral is a significant source of dimethylsulfide (DMS) to the atmosphere

Corals are prolific producers of dimethylsulfoniopropionate (DMSP). High atmospheric concentrations of the DMSP breakdown product dimethylsulfide (DMS) have been linked to coral reefs during low tides. DMS is a potentially key sulfur source to the tropical atmosphere, but DMS emission from corals during tidal exposure is not well quantified. Here we show that gas phase DMS concentrations (DMSgas) increased by an order of magnitude when three Indo-Pacific corals were exposed to air in laboratory experiments. Upon re-submersion, an additional rapid rise in DMSgas was observed, reflecting increased production by the coral and/or dissolution of DMS-rich mucus formed by the coral during air exposure. Depletion in DMS following re-submersion was likely due to biologically-driven conversion of DMS to dimethylsulfoxide (DMSO). Fast Repetition Rate fluorometry showed downregulated photosynthesis during air exposure but rapid recovery upon re-submersion, suggesting that DMS enhances coral tolerance to oxidative stress during a process that can induce photoinhibition. We estimate that DMS emission from exposed coral reefs may be comparable in magnitude to emissions from other marine DMS hotspots. Coral DMS emission likely comprises a regular and significant source of sulfur to the tropical marine atmosphere, which is currently unrecognised in global DMS emission estimates and Earth System Models.

Skeletal records of community-level bleaching in Porites corals from Palau

Tropical Pacific sea surface temperature is projected to rise an additional 2–3 °C by the end of this century, driving an increase in the frequency and intensity of coral bleaching. With significant global coral reef cover already lost due to bleaching-induced mortality, efforts are underway to identify thermally tolerant coral communities that might survive projected warming. Massive, long-lived corals accrete skeletal bands of anomalously high density in response to episodes of thermal stress. These “stress bands” are potentially valuable proxies for thermal tolerance, but to date their application to questions of community bleaching history has been limited. Ecological surveys recorded bleaching of coral communities across the Palau archipelago during the 1998 and 2010 warm events. Between 2011 and 2015, we extracted skeletal cores from living Porites colonies at 10 sites spanning barrier reef and lagoon environments and quantified the proportion of stress bands present in each population during bleaching years. Across Palau, the prevalence of stress bands tracked the severity of thermal stress, with more stress bands occurring in 1998 (degree heating weeks = 13.57 °C-week) than during the less severe 2010 event (degree heating weeks = 4.86 °C-week). Stress band prevalence also varied by reef type, as more corals on the exposed barrier reef formed stress bands than did corals from sheltered lagoon environments. Comparison of Porites stress band prevalence with bleaching survey data revealed a strong correlation between percent community bleaching and the proportion of colonies with stress bands in each year. Conversely, annual calcification rates did not decline consistently during bleaching years nor did annually resolved calcification histories always track interannual variability in temperature. Our data suggest that stress bands in massive corals contain valuable information about spatial and temporal trends in coral reef bleaching and can aid in conservation efforts to identify temperature-tolerant coral reef communities.

Different Stress Tolerances of Juveniles of the Coral Acropora tenuis Associated with Clades C1 and D Symbiodinium.

Ikuko Yuyama, Takashi Nakamura, Tomihiko Higuchi, and Michio Hidaka (2016) Reef-building corals are often associated with multiple clades of symbiotic dinoflagellate Symbiodinium spp., where the relative composition of Symbiodinium can alter the phylogenetic properties (e.g., stress responsiveness, growth rate) of the host coral. The genus Symbiodinium contains nine clades, some of which behave differently in response to strong light and/or temperature stresses, for example, clade D Symbiodinium are thermally tolerant. However, previous studies are based on corals present in the field, and it is possible that the corals used in previous experiments did not contain single Symbiodinium clades. For an accurate assessment of the effects of each Symbiodinium clade on host thermal stress resistance, monoclonal cultures of clades C1 and D were inoculated into aposymbiotic juvenile polyps. Photosynthetic efficiency (maximum quantum yield: F v /F m) showed a decline at 30°C than at 25°C in both clades. Symbiodinium clade C1 showed a consistently higher rETRmax with larger fluctuations than clade D, with a lower survival rate of juveniles during thermal stress treatment. Under strong light exposure, corals containing clade C1 showed a greater decline in F v /F m (-74%), compared to decline in corals associated with clade D (-50%) after 3 hours. This is the first study to assess stress tolerances of juvenile corals in association with the monoclonal Symbiodinium clades C and D, and our results indicated greater tolerance of corals associated with clade D to strong light (500 μmol m-2 s-1). However, it is difficult to determine the impact of high-temperature stress on coral-algae symbiosis from photosynthetic activity. At high temperatures, clade C1 Symbiodinium exhibited high photosynthetic activity, but host survival rates were higher in corals associated with clade D Symbiodinium. Since clade C1 has a relatively high photosynthetic activity under high temperatures, clade C1 symbiosis at high temperatures might have a negative impact on corals compared with clade D.

Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures.

Understanding the potential for coral adaptation to warming seas is complicated by interactions between symbiotic partners that define stress responses and the difficulties of tracking selection in natural populations. To overcome these challenges, we characterized the contribution of both animal host and symbiotic algae to thermal tolerance in corals that have already experienced considerable warming on par with end-of-century projections for most coral reefs. Thermal responses in Platygyra daedalea corals from the hot Persian Gulf where summer temperatures reach 36°C were compared with conspecifics from the milder Sea of Oman. Persian Gulf corals had higher rates of survival at elevated temperatures (33 and 36°C) in both the nonsymbiotic larval stage (32-49% higher) and the symbiotic adult life stage (51% higher). Additionally, Persian Gulf hosts had fixed greater potential to mitigate oxidative stress (31-49% higher) and their Symbiodinium partners had better retention of photosynthetic performance under elevated temperature (up to 161% higher). Superior thermal tolerance of Persian Gulf vs. Sea of Oman corals was maintained after 6-month acclimatization to a common ambient environment and was underpinned by genetic divergence in both the coral host and symbiotic algae. In P.daedalea host samples, genomewide SNP variation clustered into two discrete groups corresponding with Persian Gulf and Sea of Oman sites. Symbiodinium within host tissues predominantly belonged to ITS2 rDNA type C3 in the Persian Gulf and type D1a in the Sea of Oman contradicting patterns of Symbiodinium thermal tolerance from other regions. Our findings provide evidence that genetic adaptation of both host and Symbiodinium has enabled corals to cope with extreme temperatures in the Persian Gulf. Thus, the persistence of coral populations under continued warming will likely be determined by evolutionary rates in both, rather than single, symbiotic partners.

Hsp60 expression profiles in the reef-building coral Seriatopora caliendrum subjected to heat and cold shock regimes

Climate changes have increased the intensity/frequency of extreme thermal events, which represent serious threats to the health of reef-building corals. Since the vulnerability of corals exposed to thermal stresses are related to their ability to regulate Heat shock proteins (Hsps), we have analyzed together the time related expression profiles of the mitochondrial Hsp60 and the associated changes in tissue pigmentation in Seriatopora caliendrum subjected to 48 h of heat and cold treatments characterized by moderate (±2 °C) and severe (±6 °C) shocks. For the first time, an Hsp60 response was observed in a scleractinian coral exposed to cold stresses. Furthermore, the Hsp60 modulations and the changes in the tissue coloration were found to be specific for each treatment. A strong down-regulation at the end of the treatments was observed following both the severe shocks, but only the severe heat stress led to bleaching in concert with the lowest levels of Hsp60, suggesting that a severe heat shock can be more deleterious than an exposure to a severe cold temperature. On the contrary, a moderate cold stress seems to be more harmful than a moderate temperature increase, which could allow coral acclimation. Our results can provide a potential framework for understanding the physiological tolerance of corals under possible future climate changes.

Limits to the thermal tolerance of corals adapted to a highly fluctuating, naturally extreme temperature environment.

Naturally extreme temperature environments can provide important insights into the processes underlying coral thermal tolerance. We determined the bleaching resistance of Acropora aspera and Dipsastraea sp. from both intertidal and subtidal environments of the naturally extreme Kimberley region in northwest Australia. Here tides of up to 10 m can cause aerial exposure of corals and temperatures as high as 37 °C that fluctuate daily by up to 7 °C. Control corals were maintained at ambient nearshore temperatures which varied diurnally by 4-5 °C, while treatment corals were exposed to similar diurnal variations and heat stress corresponding to ~20 degree heating days. All corals hosted Symbiodinium clade C independent of treatment or origin. Detailed physiological measurements showed that these corals were nevertheless highly sensitive to daily average temperatures exceeding their maximum monthly mean of ~31 °C by 1 °C for only a few days. Generally, Acropora was much more susceptible to bleaching than Dipsastraea and experienced up to 75% mortality, whereas all Dipsastraea survived. Furthermore, subtidal corals, which originated from a more thermally stable environment compared to intertidal corals, were more susceptible to bleaching. This demonstrates that while highly fluctuating temperatures enhance coral resilience to thermal stress, they do not provide immunity to extreme heat stress events.