Reef Endemism,Host Specificity and Temporal Stability in Populations of Symbiotic Dinoflagellates from Two Ecologically Dominant Caribbean Corals

Background

The dinoflagellate genus Symbiodinium forms symbioses with numerous protistan and invertebrate metazoan hosts. However, few data on symbiont genetic structure are available, hindering predictions of how these populations and their host associations will fair in the face of global climate change.

Methodology/Principal Findings

Here, Symbiodinium population structure from two of the Caribbean''s ecologically dominant scleractinian corals, Montastraea faveolata and M. annularis, was examined. Tagged colonies on Florida Keys and Bahamian (i.e., Exuma Cays) reefs were sampled from 2003–2005 and their Symbiodinium diversity assessed via internal transcribed spacer 2 (ITS2) rDNA and three Symbiodinium Clade B-specific microsatellite loci. Generally, the majority of host individuals at a site harbored an identical Symbiodinium ITS2 “type” B1 microsatellite genotype. Notably, symbiont genotypes were largely reef endemic, suggesting a near absence of dispersal between populations. Relative to the Bahamas, sympatric M. faveolata and M. annularis in the Florida Keys harbored unique Symbiodinium populations, implying regional host specificity in these relationships. Furthermore, within-colony Symbiodinium population structure remained stable through time and environmental perturbation, including a prolonged bleaching event in 2005.

Conclusions/Significance

Taken together, the population-level endemism, specificity and stability exhibited by Symbiodinium raises concerns about the long-term adaptive capacity and persistence of these symbioses in an uncertain future of climate change.     

Transmission Mode Predicts Specificity and Interaction Patterns in Coral-Symbiodinium Networks

Most reef-building corals in the order Scleractinia depend on endosymbiotic algae in the genus Symbiodinium for energy and survival. Significant levels of taxonomic diversity in both partners result in numerous possible combinations of coral-Symbiodinium associations with unique functional characteristics. We created and analyzed the first coral-Symbiodinium networks utilizing a global dataset of interaction records from coral reefs in the tropical Indo-Pacific and Atlantic Oceans for 1991 to 2010. Our meta-analysis reveals that the majority of coral species and Symbiodinium types are specialists, but failed to detect any one-to-one obligate relationships. Symbiont specificity is correlated with a host’s transmission mode, with horizontally transmitting corals being more likely to interact with generalist symbionts. Globally, Symbiodinium types tend to interact with only vertically or horizontally transmitting corals, and only a few generalist types are found with both. Our results demonstrate a strong correlation between symbiont specificity, symbiont transmission mode, and community partitioning. The structure and dynamics of these network interactions underlie the fundamental biological partnership that determines the condition and resilience of coral reef ecosystems.     

Horizontal transmission of Symbiodinium cells between adult and juvenile corals is aided by benthic sediment

Of all reef-building coral species, 80–85 % initially draw their intracellular symbionts (dinoflagellates of the genus Symbiodinium) from the environment. Although Symbiodinium cells are crucial for the growth of corals and the formation of coral reefs, little is known about how corals first encounter free-living Symbiodinium cells. We report how the supply of free-living Symbiodinium cells to the benthos by adult corals can increase the rate of horizontal symbiont acquisition for conspecific recruits. Three species of newly settled aposymbiotic (i.e., symbiont-free) corals were maintained in an open aquarium system containing: sterilized sediment and adult coral fragments combined; adult coral fragments alone; sterilized sediment alone; or seawater at Heron Island, Great Barrier Reef, Australia. In all instances, the combination of an adult coral and sediment resulted in the highest symbiont acquisition rates by juvenile corals (up to five-fold greater than seawater alone). Juvenile corals exposed to individual treatments of adult coral or sediment produced an intermediate acquisition response (<52 % of recruits), and symbiont acquisition from unfiltered seawater was comparatively low (<20 % of recruits). Additionally, benthic free-living Symbiodinium cells reached their highest densities in the adult coral + sediment treatment (up to 1.2 × 10⁴ cells mL⁻¹). Our results suggest that corals seed microhabitats with free-living Symbiodinium cells suitable for many coral species during the process of coral recruitment.

     

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.     

Environmental symbiont acquisition may not be the solution to warming seas for reef-building corals

Background

Coral reefs worldwide are in decline. Much of the mortality can be attributed to coral bleaching (loss of the coral''s intracellular photosynthetic algal symbiont) associated with global warming. How corals will respond to increasing oceanic temperatures has been an area of extensive study and debate. Recovery after a bleaching event is dependent on regaining symbionts, but the source of repopulating symbionts is poorly understood. Possibilities include recovery from the proliferation of endogenous symbionts or recovery by uptake of exogenous stress-tolerant symbionts.

Methodology/Principal Findings

To test one of these possibilities, the ability of corals to acquire exogenous symbionts, bleached colonies of Porites divaricata were exposed to symbiont types not normally found within this coral and symbiont acquisition was monitored. After three weeks exposure to exogenous symbionts, these novel symbionts were detected in some of the recovering corals, providing the first experimental evidence that scleractinian corals are capable of temporarily acquiring symbionts from the water column after bleaching. However, the acquisition was transient, indicating that the new symbioses were unstable. Only those symbiont types present before bleaching were stable upon recovery, demonstrating that recovery was from the resident in situ symbiont populations.

Conclusions/Significance

These findings suggest that some corals do not have the ability to adjust to climate warming by acquiring and maintaining exogenous, more stress-tolerant symbionts. This has serious ramifications for the success of coral reefs and surrounding ecosystems and suggests that unless actions are taken to reverse it, climate change will lead to decreases in biodiversity and a loss of coral reefs.     

Bleaching as a pathogenic response in scleractinian corals, evidenced by high concentrations of apoptotic and necrotic zooxanthellae

The study of symbiont cells lost from bleached scleractinian corals Acropora hyacinthus, Favites complanata, and Porites solida and octocorals Sarcophyton ehrenbergi, Sinularia sp., and Xenia sp. using flow cytometry shows that Symbiodinium die from either apoptosis or necrosis. Despite the majority of lost Symbiodinium cells being viable at 28 °C, the predominance of apoptotic and necrotic symbiont cells at higher temperatures indicates that the proportion of live cells decreases with increasing temperature. This implies that reinfection of corals at high temperatures by Symbiodinium lost from scleractinian corals may be less frequent than previously described, since many of the symbiont cells exhibit nonreversible symptoms of approaching cell death. The fraction of viable Symbiodinium cells lost from S. ehrenbergi, Xenia sp., and Sinularia at 32 °C was greater than that at 28 °C. At 34 °C, the fraction of viable cells lost from S. ehrenbergi and Xenia sp. fell but not from Sinularia sp., which suggests that their symbionts have higher temperature tolerances. Thus, Symbiodinium from octocorals may represent “pools” of genetically resistant symbionts available for reinfection of other reef organisms. This has been proposed previously for Symbiodinium in some scleractinian corals, but this is the first evidence for such, particularly for an octocoral. Many of the viable cells, determined using Trypan blue staining techniques, are in fact actually undergoing apoptosis or necrosis, when examined using Annexin V-fluor and propidium iodide staining profiles. The characterization of more apoptotic and necrotic cells than viable cells is critical, as this indicates that the loss of Symbiodinium cells cannot be beneficial to other bleached corals for symbiotic reassociation.     

Flexible associations between Pocillopora corals and Symbiodinium limit utility of symbiosis ecology in defining species

Corals in the genus Pocillopora are the primary framework builders of eastern tropical Pacific (ETP) reefs. These corals typically associate with algal symbionts (genus Symbiodinium) in clade C and/or D, with clade D associations having greater thermal tolerance and resistance to bleaching. Recently, cryptic "species" delineations within both Pocillopora and Symbiodinium have been suggested, with host–symbiont specificity used as a supporting taxonomic character in both genera. In particular, it has been suggested that three lineages of Pocillopora (types 1–3) exist in the ETP, of which type 1 is the exclusive host of heat-tolerant Symbiodinium D1. This host specificity has been used to support the species name "Symbiodinium glynni" for this symbiont. To validate these host–symbiont relationships and their taxonomic utility, we identified Pocillopora types and their associated Symbiodinium at three sites in the ETP. We found greater flexibility in host–symbiont combinations than previously reported, with both Pocillopora types 1 and 3 able to host and be dominated by Symbiodinium in clade C or D. The prevalence of certain combinations did vary among sites, showing that a gradient of specificity exists which may be mediated by evolutionary relationships and environmental disturbance history. However, these results limit the utility of apparent host–symbiont specificity (which may have been a result of undersampling) in defining species boundaries in either corals or Symbiodinium. They also suggest that a greater diversity of corals may benefit from the thermal tolerance of clade D symbionts, affirming the need to conserve Pocillopora across its entire geographic and environmental range.     

Establishment of Coral–Algal Symbiosis Requires Attraction and Selection

Coral reef ecosystems are based on coral–zooxanthellae symbiosis. During the initiation of symbiosis, majority of corals acquire their own zooxanthellae (specifically from the dinoflagellate genus Symbiodinium) from surrounding environments. The mechanisms underlying the initial establishment of symbiosis have attracted much interest, and numerous field and laboratory experiments have been conducted to elucidate this establishment. However, it is still unclear whether the host corals selectively or randomly acquire their symbionts from surrounding environments. To address this issue, we initially compared genetic compositions of Symbiodinium within naturally settled about 2-week-old Acropora coral juveniles (recruits) and those in the adjacent seawater as the potential symbiont source. We then performed infection tests using several types of Symbiodinium culture strains and apo-symbiotic (does not have Symbiodinium cells yet) Acropora coral larvae. Our field observations indicated apparent preference toward specific Symbiodinium genotypes (A1 and D1-4) within the recruits, despite a rich abundance of other Symbiodinium in the environmental population pool. Laboratory experiments were in accordance with this field observation: Symbiodinium strains of type A1 and D1-4 showed higher infection rates for Acropora larvae than other genotype strains, even when supplied at lower cell densities. Subsequent attraction tests revealed that three Symbiodinium strains were attracted toward Acropora larvae, and within them, only A1 and D1-4 strains were acquired by the larvae. Another three strains did not intrinsically approach to the larvae. These findings suggest the initial establishment of corals–Symbiodinium symbiosis is not random, and the infection mechanism appeared to comprise two steps: initial attraction step and subsequent selective uptake by the coral.     

The Roles and Interactions of Symbiont,Host and Environment in Defining Coral Fitness

Background

Reef-building corals live in symbiosis with a diverse range of dinoflagellate algae (genus Symbiodinium) that differentially influence the fitness of the coral holobiont. The comparative role of symbiont type in holobiont fitness in relation to host genotype or the environment, however, is largely unknown. We addressed this knowledge gap by manipulating host-symbiont combinations and comparing growth, survival and thermal tolerance among the resultant holobionts in different environments.

Methodology/Principal Findings

Offspring of the coral, Acropora millepora, from two thermally contrasting locations, were experimentally infected with one of six Symbiodinium types, which spanned three phylogenetic clades (A, C and D), and then outplanted to the two parental field locations (central and southern inshore Great Barrier Reef, Australia). Growth and survival of juvenile corals were monitored for 31–35 weeks, after which their thermo-tolerance was experimentally assessed. Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness. Furthermore, coral-algal associations were established with symbiont types belonging to clades A, C and D, but three out of four symbiont types belonging to clade C failed to establish a symbiosis. Associations with clade A had the lowest fitness and were unstable in the field. Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.

Conclusions/Significance

These results highlight the complex interactions that occur between the coral host, the algal symbiont, and the environment to shape the fitness of the coral holobiont. An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.     

Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef)

The abundance and distribution of free-living dinoflagellates in the genus Symbiodinium have important implications for the ecology of coral reefs, determining both the symbionts available to newly recruited corals and symbiont types available for uptake by adult corals during environmental stress. However, little is known about where symbiotic dinoflagellates reside outside the host, due to the difficulty of capturing and detecting unicellular organisms in the marine environment. This study presents a successful protocol for sampling Symbiodinium from both the benthos and the water column. Comparisons of two detection methods for enumerating Symbiodinium indicated that conventional microscope analysis is accurate and more efficient when estimating Symbiodinium densities in sediment samples, while an automated particle counter (FlowCAM) was more efficient in detecting cells in the water column where densities are low. Symbiodinium densities were found to be relatively high (1000–4000 cells/mL) in sediment samples and much lower (up to 80 cells/mL) in the water column, indicating that the free-living form resides mainly in the benthos. Symbiodinium densities were found to be highly variable spatially, differing significantly between two reef locations. Within sites, elevated densities of Symbiodinium along reef margins combined with significant decreases in densities one meter away from the reef, suggest that cells aggregate within the reef habitat.     

Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades

Many reef-building corals form symbioses with dinoflagellates from the diverse genus Symbiodinium. There is increasing evidence of functional significance to Symbiodinium diversity, which affects the coral holobiont''s response to changing environmental conditions. For example, corals hosting Symbiodinium from the clade D taxon exhibit greater resistance to heat-induced coral bleaching than conspecifics hosting the more common clade C. Yet, the relatively low prevalence of clade D suggests that this trait is not advantageous in non-stressful environments. Thus, clade D may only be able to out-compete other Symbiodinium types within the host habitat when conditions are chronically stressful. Previous studies have observed enhanced photosynthesis and fitness by clade C holobionts at non-stressful temperatures, relative to clade D. Yet, carbon-centered metrics cannot account for enhanced growth rates and patterns of symbiont succession to other genetic types when nitrogen often limits reef productivity. To investigate the metabolic costs of hosting thermally tolerant symbionts, we examined the assimilation and translocation of inorganic ¹⁵N and ¹³C in the coral Acropora tenuis experimentally infected with either clade C (sub-type C1) or D Symbiodinium at 28 and 30 °C. We show that at 28 °C, C1 holobionts acquired 22% more ¹⁵N than clade D. However, at 30 °C, C1 symbionts acquired equivalent nitrogen and 16% less carbon than D. We hypothesize that C1 competitively excludes clade D in hospite via enhanced nitrogen acquisition and thus dominates coral populations despite warming oceans.     

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.     

Trans-generational specificity within a cnidarian–algal symbiosis

Ocean warming and other anthropogenic stresses threaten the symbiosis between tropical reef cnidarians and their dinoflagellate endosymbionts (Symbiodinium). Offspring of many cnidarians acquire their algal symbionts from the environment, and such flexibility could allow corals to respond to environmental changes between generations. To investigate the effect of both habitat and host genotype on symbiont acquisition, we transplanted aposymbiotic offspring of the common Caribbean octocoral Briareum asbestinum to (1) an environmentally different habitat that lacked B. asbestinum and (2) an environmentally similar habitat where local adults harbored Symbiodinium phylotypes that differed from parental colonies. Symbiont acquisition and establishment of symbioses over time was followed using a within-clade DNA marker (23S chloroplast rDNA) and a within-phylotype marker (unique alleles at a single microsatellite locus). Early in the symbiosis, B. asbestinum juveniles harbored multiple symbiont phylotypes, regardless of source (parent or site). However, with time (~4 yr), offspring established symbioses with the symbiont phylotype dominant in the parental colonies, regardless of transplant location. Within-phylotype analyses of the symbionts revealed a similar pattern, with offspring acquiring the allelic variant common in symbionts in the parental population regardless of the environment in which the offspring was reared. These data suggest that in this host species, host–symbiont specificity is a genetically determined trait. If this level of specificity is widespread among other symbiotic cnidarians, many cnidarian–algal symbioses may not be able to respond to rapid, climate change-associated environmental changes by means of between-generation switching of symbionts.     

Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf

The symbiotic association of corals and unicellular algae of the genus Symbiodinium in the southern Persian/Arabian Gulf (PAG) display an exceptional heat tolerance, enduring summer peak temperatures of up to 36 °C. As yet, it is not clear whether this resilience is related to the presence of specific symbiont types that are exclusively found in this region. Therefore, we used molecular markers to identify the symbiotic algae of three Porites species along >1000 km of coastline in the PAG and the Gulf of Oman and found that a recently described species, Symbiodinium thermophilum, is integral to coral survival in the southern PAG, the world''s hottest sea. Despite the geographic isolation of the PAG, we discovered that representatives of the S. thermophilum group can also be found in the adjacent Gulf of Oman providing a potential source of thermotolerant symbionts that might facilitate the adaptation of Indian Ocean populations to the higher water temperatures expected for the future. However, corals from the PAG associated with S. thermophilum show strong local adaptation not only to high temperatures but also to the exceptionally high salinity of their habitat. We show that their superior heat tolerance can be lost when these corals are exposed to reduced salinity levels common for oceanic environments elsewhere. Consequently, the salinity prevailing in most reefs outside the PAG might represent a distribution barrier for extreme temperature-tolerant coral/Symbiodinium associations from the PAG.     

Symbiodinium genotypic and environmental controls on lipids in reef building corals

Background

Lipids in reef building corals can be divided into two classes; non-polar storage lipids, e.g. wax esters and triglycerides, and polar structural lipids, e.g. phospholipids and cholesterol. Differences among algal endosymbiont types are known to have important influences on processes including growth and the photobiology of scleractinian corals yet very little is known about the role of symbiont types on lipid energy reserves.

Methodology/Principal Findings

The ratio of storage lipid and structural lipid fractions of Scott Reef corals were determined by thin layer chromatography. The lipid fraction ratio varied with depth and depended on symbiont type harboured by two corals (Seriatopora hystrix and Pachyseris speciosa). S. hystrix colonies associated with Symbiodinium C1 or C1/C# at deep depths (>23 m) had lower lipid fraction ratios (i.e. approximately equal parts of storage and structural lipids) than those with Symbiodinium D1 in shallow depths (<23 m), which had higher lipid fraction ratios (i.e. approximately double amounts of storage relative to structural lipid). Further, there was a non-linear relationship between the lipid fraction ratio and depth for S. hystrix with a modal peak at ∼23 m coinciding with the same depth as the shift from clade D to C types. In contrast, the proportional relationship between the lipid fraction ratio and depth for P. speciosa, which exhibited high specificity for Symbiodinium C3 like across the depth gradient, was indicative of greater amounts of storage lipids contained in the deep colonies.

Conclusions/Significance

This study has demonstrated that Symbiodinium exert significant controls over the quality of coral energy reserves over a large-scale depth gradient. We conclude that the competitive advantages and metabolic costs that arise from flexible associations with divergent symbiont types are offset by energetic trade-offs for the coral host.     

Interseasonal and interspecies diversities of <Emphasis Type="Italic">Symbiodinium</Emphasis> density and effective photochemical efficiency in five dominant reef coral species from Luhuitou fringing reef,northern South China Sea

Although it is well established that different coral species have different susceptibilities to thermal stress, the reasons behind this variation are still unclear. In this study, 384 samples across five dominant coral species were collected seasonally between September 2013 and August 2014 at Luhuitou fringing reef in Sanya, Hainan Island, northern South China Sea, and their algal symbiont density and effective photochemical efficiency (Φ _PSII) were measured. The results indicated that both the Symbiodinium density and Φ _PSII of corals were subject to significant interspecies and seasonal variations. Stress-tolerant coral species, including massive Porites lutea and plating Pavona decussata, had higher symbiont densities but lower Φ _PSII compared to the vulnerable branching species of Acropora over the course of all four seasons. Seasonally, coral symbiont densities were the lowest during winter, while during the same period, Φ _PSII of corals was at the highest point. Further analysis suggested that dissolved inorganic nutrients and upwelling in the reef area were probably responsible for the observed seasonal variations in symbiont density. The fact that Porites lutea has the lowest Φ _PSII during all four seasons is likely related to their symbionts’ lower capacity to provide required photosynthates for calcification. These results suggest that a coral’s thermal tolerance is primarily and positively dependent on its symbiont density and is less related to its effective photochemical efficiency.     

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.     

Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event

Reef corals are sentinels for the adverse effects of rapid global warming on the planet''s ecosystems. Warming sea surface temperatures have led to frequent episodes of bleaching and mortality among corals that depend on endosymbiotic micro-algae (Symbiodinium) for their survival. However, our understanding of the ecological and evolutionary response of corals to episodes of thermal stress remains inadequate. For the first time, we describe how the symbioses of major reef-building species in the Caribbean respond to severe thermal stress before, during and after a severe bleaching event. Evidence suggests that background populations of Symbiodinium trenchi (D1a) increased in prevalence and abundance, especially among corals that exhibited high sensitivity to stress. Contrary to previous hypotheses, which posit that a change in symbiont occurs subsequent to bleaching, S. trenchi increased in the weeks leading up to and during the bleaching episode and disproportionately dominated colonies that did not bleach. During the bleaching event, approximately 20 per cent of colonies surveyed harboured this symbiont at high densities (calculated at less than 1.0% only months before bleaching began). However, competitive displacement by homologous symbionts significantly reduced S. trenchi''s prevalence and dominance among colonies after a 2-year period following the bleaching event. While the extended duration of thermal stress in 2005 provided an ecological opportunity for a rare host-generalist symbiont, it remains unclear to what extent the rise and fall of S. trenchi was of ecological benefit or whether its increased prevalence was an indicator of weakening coral health.