Depth-dependant response to light of the reef building coral, Pocillopora verrucosa: Implication of oxidative stress

Several environmental factors have been described to trigger bleaching in cnidarian/dinoflagellate endosymbiosis. However, the molecular mechanisms underlying this process still need more investigations. Symbiosis breakdown is known to result from physiological damage to animal host cells and/or symbionts. Cellular oxidation appears to be an essential player in this damage. Indeed, oxidative stress is a direct consequence of increase in irradiance and temperature, the two main environmental factors involved in bleaching. In this study, we examined the role of irradiance in inducing dissociation and oxidative stress in cnidarians and dinoflagellates. We used the bleaching-sensitive scleractinian coral Pocillopora verrucosa in a field cross-transplantation experiment performed between 5 m and 20 m depth at Grande Glorieuse Island (Indian Ocean), a preserved area subject to minimal anthropogenic influence. Cellular damage and increase in antioxidant defense were correlated with bleaching in upward transplanted samples. Downward transplanted colonies presented no associated alterations similar to the controls. We therefore conclude that increasing light induced bleaching via a prooxidative period. Remarkably, the distribution of Symbiodinium over depth was invariant; all colonies were monomorph for clade C, suggesting that bleaching sensitivity of P. verrucosa might not be associated with clade specificity.     

Host Coenzyme Q Redox State Is an Early Biomarker of Thermal Stress in the Coral Acropora millepora

Bleaching episodes caused by increasing seawater temperatures may induce mass coral mortality and are regarded as one of the biggest threats to coral reef ecosystems worldwide. The current consensus is that this phenomenon results from enhanced production of harmful reactive oxygen species (ROS) that disrupt the symbiosis between corals and their endosymbiotic dinoflagellates, Symbiodinium. Here, the responses of two important antioxidant defence components, the host coenzyme Q (CoQ) and symbiont plastoquinone (PQ) pools, are investigated for the first time in colonies of the scleractinian coral, Acropora millepora, during experimentally-induced bleaching under ecologically relevant conditions. Liquid chromatography-mass spectrometry (LC-MS) was used to quantify the states of these two pools, together with physiological parameters assessing the general state of the symbiosis (including photosystem II photochemical efficiency, chlorophyll concentration and Symbiodinium cell densities). The results show that the responses of the two antioxidant systems occur on different timescales: (i) the redox state of the Symbiodinium PQ pool remained stable until twelve days into the experiment, after which there was an abrupt oxidative shift; (ii) by contrast, an oxidative shift of approximately 10% had occurred in the host CoQ pool after 6 days of thermal stress, prior to significant changes in any other physiological parameter measured. Host CoQ pool oxidation is thus an early biomarker of thermal stress in corals, and this antioxidant pool is likely to play a key role in quenching thermally-induced ROS in the coral-algal symbiosis. This study adds to a growing body of work that indicates host cellular responses may precede the bleaching process and symbiont dysfunction.     

Many corals host thermally resistant symbionts in high-temperature habitat

Physiologically distinct lines of dinoflagellate symbionts, Symbiodinium spp., may confer distinct thermal tolerance thresholds on their host corals. Therefore, if a coral can alternately host distinct symbionts, changes in their Symbiodinium communities might allow corals to better tolerate increasing environmental temperatures. However, researchers are currently debating how commonly coral species can host different symbiont types. We sequenced chloroplast 23 s rDNA from the Symbiodinium communities of nine reef-building coral species across two thermally distinct lagoon pools separated by ~500 m. The hotter of these pools reaches 35°C in the summer months, while the other pool’s maximum temperature is 1.5°C cooler. Across 217 samples from nine species, we found a single haplotype in both Symbiodinium clades A and D, but four haplotypes in Symbiodinium clade C. Eight of nine species hosted a putatively thermally resistant member of clade D Symbiodinium at least once, one of which hosted this clade D symbiont exclusively. Of the remaining seven that hosted multiple Symbiodinium types, six species showed higher proportions of the clade D symbiont in the hotter pool. Average percentage rise in the frequency of the clade D symbiont from the hotter to cooler pool was 52% across these six species. Even though corals hosted members of both the genetically divergent clades D and C Symbiodinium, some showed patterns of host–symbiont specificity within clade C. Both Acropora species that hosted clade C exclusively hosted a member of sub-clade C2, while all three Pocillopora species hosted a member of sub-clade C1 (sensu van Oppen et al. 2001). Our results suggest that coral–algal symbioses often conform to particular temperature environments through changes in the identity of the algal symbiont.     

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility

Reef‐building corals are at risk of extinction from ocean warming. While some corals can enhance their thermal limits by associating with dinoflagellate photosymbionts of superior stress tolerance, the extent to which symbiont communities will reorganize under increased warming pressure remains unclear. Here we show that corals in the hottest reefs in the world in the Persian Gulf maintain associations with the same symbionts across 1.5 years despite extreme seasonal warming and acute heat stress (≥35°C). Persian Gulf corals predominantly associated with Cladocopium (clade C) and most also hosted Symbiodinium (clade A) and/or Durusdinium (clade D). This is in contrast to the neighbouring and milder Oman Sea, where corals associated with Durusdinium and only a minority hosted background levels of Cladocopium. During acute heat stress, the higher prevalence of Symbiodinium and Durusdinium in bleached versus nonbleached Persian Gulf corals indicates that genotypes of these background genera did not confer bleaching resistance. Within symbiont genera, the majority of ITS2 rDNA type profiles were unique to their respective coral species, confirming the existence of host‐specific symbiont lineages. Notably, further differentiation among Persian Gulf sites demonstrates that symbiont populations are either isolated or specialized over tens to hundreds of kilometres. Thermal tolerance across coral species was associated with the prevalence of a single ITS2 intragenomic sequence variant (C3gulf), definitive of the Cladocopium thermophilum group. The abundance of C3gulf was highest in bleaching‐resistant corals and at warmer sites, potentially indicating a specific symbiont genotype (or set of genotypes) that may play a role in thermal tolerance that warrants further investigation. Together, our findings indicate that co‐evolution of host–Symbiodiniaceae partnerships favours fidelity rather than flexibility in extreme environments and under future warming.     

Rapid thermal adaptation in photosymbionts of reef‐building corals

Climate warming is occurring at a rate not experienced by life on Earth for 10 s of millions of years, and it is unknown whether the coral‐dinoflagellate (Symbiodinium spp.) symbiosis can evolve fast enough to ensure coral reef persistence. Coral thermal tolerance is partly dependent on the Symbiodinium hosted. Therefore, directed laboratory evolution in Symbiodinium has been proposed as a strategy to enhance coral holobiont thermal tolerance. Using a reciprocal transplant design, we show that the upper temperature tolerance and temperature tolerance range of Symbiodinium C1 increased after ~80 asexual generations (2.5 years) of laboratory thermal selection. Relative to wild‐type cells, selected cells showed superior photophysiological performance and growth rate at 31°C in vitro, and performed no worse at 27°C; they also had lower levels of extracellular reactive oxygen species (exROS). In contrast, wild‐type cells were unable to photosynthesise or grow at 31°C and produced up to 17 times more exROS. In symbiosis, the increased thermal tolerance acquired ex hospite was less apparent. In recruits of two of three species tested, those harbouring selected cells showed no difference in growth between the 27 and 31°C treatments, and a trend of positive growth at both temperatures. Recruits that were inoculated with wild‐type cells, however, showed a significant difference in growth rates between the 27 and 31°C treatments, with a negative growth trend at 31°C. There were no significant differences in the rate and severity of bleaching in coral recruits harbouring wild‐type or selected cells. Our findings highlight the need for additional Symbiodinium genotypes to be tested with this assisted evolution approach. Deciphering the genetic basis of enhanced thermal tolerance in Symbiodinium and the cause behind its limited transference to the coral holobiont in this genotype of Symbiodinium C1 are important next steps for developing methods that aim to increase coral bleaching tolerance.     

Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals?

The bleaching of corals in response to increases in temperature has resulted in significant coral reef degradation in many tropical marine ecosystems. This bleaching has frequently been attributed to photoinhibition of photosynthetic electron transport and the consequent photodamage to photosystem II (PSII) and the production of damaging reactive oxygen species (ROS) in the zooxanthellae (Symbiodinium spp.). However, these events may be because of perturbations of other processes occurring within the zooxanthellae or the host cells, and consequently constitute only secondary responses to temperature increase. The processes involved with the onset of photoinhibition of electron transport, photodamage to PSII and pigment bleaching in coral zooxanthellae are reviewed. Consideration is given to how increases in temperature might lead to perturbations of metabolic processes in the zooxanthellae and/or their host cells, which could trigger events leading to bleaching. It is concluded that production of ROS by the thylakoid photosynthetic apparatus in the zooxanthellae plays a major role in the onset of bleaching resulting from photoinhibition of photosynthesis, although it is not clear which particular ROS are involved. It is suggested that hydrogen peroxide generated in the zooxanthellae may have a signalling role in triggering the mechanisms that result in expulsion of zooxanthellae from corals.     

The influence of irradiance on the severity of thermal bleaching in sea anemones that host anemonefish

Entacmaea quadricolor is a geographically widespread species of sea anemone that forms a three-way symbiosis with anemonefish and Symbiodinium. This species dominates the reef substrata at North Solitary Island, Australia, which is located in a region identified as a climate change hot spot. Their geographic location places these anemones under significant threat from rising ocean temperatures, although their upper thermal limit and risk of bleaching are unknown. To address this knowledge gap, anemones were exposed to one of four temperatures (23, 25, 27, or 29°C) and one of two irradiance treatments (high or low light) over 6 days. At moderate temperatures (27°C, 1°C above summer average), anemone bleaching was characterised by symbiont expulsion, while extreme temperatures (29°C) resulted in an additional loss of photosynthetic pigments from within symbionts, and in some cases, host mortality. Irradiance influenced the susceptibility to thermal stress with high light promoting the bleaching response, along with significant reductions in the effective quantum yield of anemone symbionts. The long-term loss of photosystem II photochemical efficiency within in hospite symbionts was observed during exposure to temperatures exceeding the summer average, indicating photosynthetic damage. The resident Symbiodinium, identified as clade C using 28S rRNA gene sequences, therefore represents the partner within the symbiosis that is likely to be most vulnerable to rising seawater temperatures. Results suggest that E. quadricolor is living within approximately 1°C of the upper thermal maximum at the Solitary Islands, and given the predictions for rising seawater temperature on Australia’s east coast, the thermal threshold at which bleaching will occur is expected to be reached and exceeded more frequently in the future.     

Isolation of clonal axenic strains of the symbiotic dinoflagellate Symbiodinium and their growth and host specificity1

The cnidarian‐dinoflagellate mutualism is integral to the survival of the coral‐reef ecosystem. Despite the enormous ecological and economic importance of corals, their cellular and molecular biology and the ways in which they respond to environmental change are still poorly understood. We have been developing a proxy system for examining the coral mutualism in which the dinoflagellate symbiont Symbiodinium is introduced into a clonal population of the host Aiptasia, a small sea anemone closely related to corals. To further develop the tools for this system, we generated five clonal, axenic strains of Symbiodinium and verified the lack of contaminants by growth on rich medium, microscopic examination, and PCR analysis. These strains were assigned to clades A (two strains), B, E, and F based on their chloroplast 23S rDNA sequences. Growth studies in liquid cultures showed that the clade B strain and one of the clade A strains were able to grow photoautotrophically (in light with no fixed carbon), mixotrophically (in light with fixed carbon), or heterotrophically (in dark with fixed carbon). The clade E strain, thought to be free‐living, was able to grow photoautotrophically but not heterotrophically. Infection of an aposymbiotic Aiptasia host with the axenic strains showed consistent patterns of specificity, with only the clade B and one of the clade A strains able to successfully establish symbiosis. Overall, the Aiptasia‐Symbiodinium association represents an important model system for dissecting aspects of the physiology and cellular and molecular biology of cnidarian‐dinoflagellate mutualism and exploring issues that bear directly on coral bleaching.     

FISH-Flow: a quantitative molecular approach for describing mixed clade communities of Symbiodinium

Our understanding of reef corals and their fate in a changing climate is limited by our ability to monitor the diversity and abundance of the dinoflagellate endosymbionts that sustain them. This study combined two well-known methods in tandem: fluorescent in situ hybridization (FISH) for genotype-specific labeling of Symbiodinium and flow cytometry to quantify the abundance of each symbiont clade in a sample. This technique (FISH-Flow) was developed with cultured Symbiodinium representing four distinct clades (based on large subunit rDNA) and was used to distinguish and quantify these types with high efficiency and few false positives. This technique was also applied to freshly isolated symbionts of Orbicella faveolata and Orbicella annularis. Isolates from acutely bleached coral tissues had significantly lower labeling efficiency; however, isolates from healthy tissue had efficiencies comparable to cultured Symbiodinium trials. RNA degradation in bleaching samples may have interfered with labeling of cells. Nevertheless, we were able to determine that, with and without thermal stress, experimental columns of the coral O. annularis hosted a majority of clade B and B/C symbionts on the top and side of the coral column, respectively. We demonstrated that, for cultured Symbiodinium and Symbiodinium freshly isolated from healthy host tissues, the relative ratio of clades could be accurately determined for clades present at as low as 7 % relative abundance. While this method does not improve upon PCR-based techniques in identifying clades at background levels, FISH-Flow provides a high precision, flexible system for targeting, quantifying and isolating Symbiodinium genotypes of interest.     

Antioxidant plasticity and thermal sensitivity in four types of Symbiodinium sp.

Warmer than average summer sea surface temperature is one of the main drivers for coral bleaching, which describes the loss of endosymbiotic dinoflagellates (genus: Symbiodinium) in reef‐building corals. Past research has established that oxidative stress in the symbiont plays an important part in the bleaching cascade. Corals hosting different genotypes of Symbiodinium may have varying thermal bleaching thresholds, but changes in the symbiont's antioxidant system that may accompany these differences have received less attention. This study shows that constitutive activity and up‐regulation of different parts of the antioxidant network under thermal stress differs between four Symbiodinium types in culture and that thermal susceptibility can be linked to glutathione redox homeostasis. In Symbiodinium B1, C1 and E, declining maximum quantum yield of PSII (F_v/F_m) and death at 33°C were generally associated with elevated superoxide dismutase (SOD) activity and a more oxidized glutathione pool. Symbiodinium F1 exhibited no decline in F_v/F_m or growth, but showed proportionally larger increases in ascorbate peroxidase (APX) activity and glutathione content (GSx), while maintaining GSx in a reduced state. Depressed growth in Symbiodinium B1 at a sublethal temperature of 29°C was associated with transiently increased APX activity and glutathione pool size, and an overall increase in glutathione reductase (GR) activity. The collapse of GR activity at 33°C, together with increased SOD, APX and glutathione S‐transferase activity, contributed to a strong oxidation of the glutathione pool with subsequent death. Integrating responses of multiple components of the antioxidant network highlights the importance of antioxidant plasticity in explaining type‐specific temperature responses in Symbiodinium.     

Photoacclimatory and photoprotective responses to cold versus heat stress in high latitude reef corals

Corals at the world's southernmost coral reef of Lord Howe Island (LHI) experience large temperature and light fluctuations and need to deal with periods of cold temperature (<18°C), but few studies have investigated how corals are able to cope with these conditions. Our study characterized the response of key photophysiological parameters, as well as photoacclimatory and photoprotective pigments (chlorophylls, xanthophylls, and β‐carotene), to short‐term (5‐d) cold stress (~15°C; 7°C below control) in three LHI coral species hosting distinct Symbiodinium ITS2 types, and compared the coral–symbiont response to that under elevated temperature (~29°C; 7°C above control). Under cold stress, Stylophora sp. hosting Symbiodinium C118 showed the strongest effects with regard to losses of photochemical performance and symbionts. Pocillopora damicornis hosting Symbiodinium C100/C118 showed less severe bleaching responses to reduced temperature than to elevated temperature, while Porites heronensis hosting Symbiodinium C111* withstood both reduced and elevated temperature. Under cold stress, photoprotection in the form of xanthophyll de‐epoxidation increased in unbleached P. heronensis (by 178%) and bleached Stylophora sp. (by 225%), while under heat stress this parameter increased in unbleached P. heronensis (by 182%) and in bleached P. damicornis (by 286%). The xanthophyll pool size was stable in all species at all temperatures. Our comparative study demonstrates high variability in the bleaching vulnerability of these coral species to low and high thermal extremes and shows that this variability is not solely determined by the ability to activate xanthophyll de‐epoxidation.     

Exploring Symbiodinium diversity and host specificity in Acropora corals from geographical extremes of Western Australia with 454 amplicon pyrosequencing

Scleractinian corals have demonstrated the ability to shuffle their endosymbiotic dinoflagellate communities (genus Symbiodinium) during periods of acute environmental stress. This has been proposed as a mechanism of acclimation, which would be increased by a diverse and flexible association with Symbiodinium. Conventional molecular techniques used to evaluate Symbiodinium diversity are unable to identify genetic lineages present at background levels below 10%. Next generation sequencing (NGS) offers a solution to this problem and can resolve microorganism diversity at much finer scales. Here we apply NGS to evaluate Symbiodinium diversity and host specificity in Acropora corals from contrasting regions of Western Australia. The application of 454 pyrosequencing allowed for detection of Symbiodinium operational taxonomic units (OTUs) occurring at frequencies as low as 0.001%, offering a 10 000‐fold increase in sensitivity compared to traditional methods. All coral species from both regions were overwhelmingly dominated by a single clade C OTU (accounting for 98% of all recovered sequences). Only 8.5% of colonies associated with multiple clades (clades C and D, or C and G), suggesting a high level of symbiont specificity in Acropora assemblages in Western Australia. While only 40% of the OTUs were shared between regions, the dominance of a single OTU resulted in no significant difference in Symbiodinium community structure, demonstrating that the coral‐algal symbiosis can remain stable across more than 15° of latitude and a range of sea surface temperature profiles. This study validates the use of NGS platforms as tools for providing fine‐scale estimates of Symbiodinium diversity and can offer critical insight into the flexibility of the coral‐algal symbiosis.     

VARIABILITY IN THE PRIMARY SITE OF PHOTOSYNTHETIC DAMAGE IN SYMBIODINIUM SP. (DINOPHYCEAE) EXPOSED TO THERMAL STRESS1

Exposure to elevated temperature is known to cause photosynthetic inhibition in the coral symbiont Symbiodinium sp. Through the use of the artificial electron acceptor, methyl viologen, this study identified how reduced photosynthetic capacity occurs as a result of inhibition up‐ and/or downstream of ferredoxin in Symbiodinium sp. in hospite and in culture. Heterogeneity between coral species and symbiont clades was identified in the thermal sensitivity of photosynthesis in the symbionts of the scleractinian corals Stylophora pistillata and Pocillopora damicornis, as well as among Symbiodinium cultures of clades A, B, and C. The in hospite symbionts of S. pistillata and the cultured clade C Symbiodinium both exhibited similar patterns in that their primary site of thermal inhibition occurred downstream of ferredoxin at 32°C. In contrast, the primary site of thermal inhibition occurred upstream of ferredoxin in clades A and B at 32°C, while at 34°C, all samples showed combined up‐ and downstream inhibition. Although clade C is common to both P. damicornis and S. pistillata, the manner of thermal inhibition was not consistent when observed in hospite. Results showed that there is heterogeneity in the primal site of thermal damage in Symbiodinium among coral species and symbiont clades.     

Change in algal symbiont communities after bleaching,not prior heat exposure,increases heat tolerance of reef corals

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.     

The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: correlations with host and the history of ocean thermal stress

Spatially intimate symbioses, such as those between scleractinian corals and unicellular algae belonging to the genus Symbiodinium, can potentially adapt to changes in the environment by altering the taxonomic composition of their endosymbiont communities. We quantified the spatial relationship between the cumulative frequency of thermal stress anomalies (TSAs) and the taxonomic composition of Symbiodinium in the corals Montipora capitata, Porites lobata, and Porites compressa across the Hawaiian archipelago. Specifically, we investigated whether thermally tolerant clade D Symbiodinium was in greater abundance in corals from sites with high frequencies of TSAs. We recovered 2305 Symbiodinium ITS2 sequences from 242 coral colonies in lagoonal reef habitats at Pearl and Hermes Atoll, French Frigate Shoals, and Kaneohe Bay, Oahu in 2007. Sequences were grouped into 26 operational taxonomic units (OTUs) with 12 OTUs associated with Montipora and 21 with Porites. Both coral genera associated with Symbiodinium in clade C, and these co‐occurred with clade D in M. capitata and clade G in P. lobata. The latter represents the first report of clade G Symbiodinium in P. lobata. In M. capitata (but not Porites spp.), there was a significant correlation between the presence of Symbiodinium in clade D and a thermal history characterized by high cumulative frequency of TSAs. The endogenous community composition of Symbiodinium and an association with clade D symbionts after long‐term thermal disturbance appear strongly dependent on the taxa of the coral host.     

The effect of temperature stress on coral–<Emphasis Type="Italic">Symbiodinium</Emphasis> associations containing distinct symbiont types

Several studies have demonstrated that the temperature tolerance of scleractinian reef-building corals is controlled, in part, by hosting physiologically distinct symbiotic algae. We investigated the thermal tolerance of coral–algal associations within seven common species of reef-building corals hosting distinct Symbiodinium sub-clades collected from Heron Island during experimentally induced bleaching conditions. During experimental heating, photosynthetic fitness was assessed by the dark-adapted yield of PSII (F _v/F _m), and excitation pressure across PSII (Q _m) of each coral–algal association using pulse amplitude modulation fluorometry. The onset of bleaching was determined by the measurement of Symbiodinium cell density. Using the ribosomal internal transcribed spacer 2 (ITS-2) region, we showed that Symbiodinium type–coral host associations were temporally and spatially conserved in a high proportion of the colonies sampled within each species. Generally, the species Acropora millepora, Platygyra daedalea, Acropora aspera and Acropora formosa contained Symbiodinium ITS-2 type C3, whereas the species Montipora digitata, Porites cylindrica and Porites lutea contained Symbiodinium type C15. Bleaching susceptibility showed some association with Symbiodinium type, but further research is required to confirm this. Corals hosting C3 Symbiodinium displayed higher reductions in F _v/F _m during heating compared to their C15 counterparts, irrespective of host species. However, a corresponding reduction in Symbiodinium density was not observed. Nonetheless, A. aspera and A. formosa showed significant reductions in Symbiodinium density relative to controls. This correlated with large increases in Q _m and decreases in F _v/F _m in heated explants. Our results suggest a range of bleaching susceptibilities for the coral species investigated, with A. aspera and A. formosa showing the greatest susceptibility to bleaching and M. digitata showing the lowest bleaching susceptibility. The data provide strong evidence for distinct differences in temperature tolerance between C3 and C15 Symbiodinium types when in-hospite; however, future studies addressing the confounding effect of host species would help to confirm this.     

Coscinaraea marshae corals that have survived prolonged bleaching exhibit signs of increased heterotrophic feeding

Colonies of Coscinaraea marshae corals from Rottnest Island, Western Australia have survived for more than 11 months in various bleached states following a severe heating event in the austral summer of 2011. These colonies are situated in a high-latitude, mesophotic environment, which has made their long-term survival of particular interest as such environments typically suffer from minimal thermal pressures. We have investigated corals that remain unbleached, moderately bleached, or severely bleached to better understand potential survival mechanisms utilised in response to thermal stress. Specifically, Symbiodinium (algal symbiont) density and genotype, chlorophyll-a concentrations, and δ¹³C and δ¹⁵N levels were compared between colonies in the three bleaching categories. Severely bleached colonies housed significantly fewer Symbiodinium cells (p < 0.05) and significantly reduced chlorophyll-a concentrations (p < 0.05), compared with unbleached colonies. Novel Symbiodinium clade associations were observed for this coral in both severely and moderately bleached colonies, with clade C and a mixed clade population detected. In unbleached colonies, only clade B was observed. Levels of δ¹⁵N indicate that severely bleached colonies are utilising heterotrophic feeding mechanisms to aid survival whilst bleached. Collectively, these results suggest that these C. marshae colonies can survive with low symbiont and chlorophyll densities, in response to prolonged thermal stress and extended bleaching, and increase heterotrophic feeding levels sufficiently to meet energy demands, thus enabling some colonies to survive and recover over long time frames. This is significant as it suggests that corals in mesophotic and high-latitude environments may possess considerable plasticity and an ability to tolerate and adapt to large environmental fluctuations, thereby improving their chances of survival as climate change impacts coral ecosystems worldwide.     

Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments

Studying the mechanisms that enable coral populations to inhabit spatially varying thermal environments can help evaluate how they will respond in time to the effects of global climate change and elucidate the evolutionary forces that enable or constrain adaptation. Inshore reefs in the Florida Keys experience higher temperatures than offshore reefs for prolonged periods during the summer. We conducted a common garden experiment with heat stress as our selective agent to test for local thermal adaptation in corals from inshore and offshore reefs. We show that inshore corals are more tolerant of a 6‐week temperature stress than offshore corals. Compared with inshore corals, offshore corals in the 31 °C treatment showed significantly elevated bleaching levels concomitant with a tendency towards reduced growth. In addition, dinoflagellate symbionts (Symbiodinium sp.) of offshore corals exhibited reduced photosynthetic efficiency. We did not detect differences in the frequencies of major (>5%) haplotypes comprising Symbiodinium communities hosted by inshore and offshore corals, nor did we observe frequency shifts (‘shuffling’) in response to thermal stress. Instead, coral host populations showed significant genetic divergence between inshore and offshore reefs, suggesting that in Porites astreoides, the coral host might play a prominent role in holobiont thermotolerance. Our results demonstrate that coral populations inhabiting reefs <10‐km apart can exhibit substantial differences in their physiological response to thermal stress, which could impact their population dynamics under climate change.