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.     

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.     

<Emphasis Type="Italic">Symbiodinium</Emphasis> associations with diseased and healthy scleractinian corals

Despite recent advances in identifying the causative agents of disease in corals and understanding the impact of epizootics on reef communities, little is known regarding the interactions among diseases, corals, and their dinoflagellate endosymbionts (Symbiodinium spp.). Since the genotypes of both corals and their resident Symbiodinium contribute to colony-level phenotypes, such as thermotolerance, symbiont genotypes might also contribute to the resistance or susceptibility of coral colonies to disease. To explore this, Symbiodinium were identified using the internal transcribed spacer-2 region of ribosomal DNA from diseased and healthy tissues within individual coral colonies infected with black band disease (BB), dark spot syndrome (DSS), white plague disease (WP), or yellow blotch disease (YB) in the Florida Keys (USA) and the US Virgin Islands. Most of the diseased colonies sampled contained B1, B5a, or C1 (depending on host species), while apparently healthy colonies of the same coral species frequently hosted these types and/or additional symbiont diversity. No potentially “parasitic” Symbiodinium types, uniquely associated with diseased coral tissue, were detected. Within most individual colonies, the same dominant Symbiodinium type was detected in diseased and visually healthy tissues. These data indicate that specific Symbiodinium types are not correlated with the infected tissues of diseased colonies and that DSS and WP onset do not trigger symbiont shuffling within infected tissues. However, few diseased colonies contained clade D symbionts suggesting a negative correlation between hosting Symbiodinium clade D and disease incidence in scleractinian corals. Understanding the influence of Symbiodinium diversity on colony phenotypes may play a critical role in predicting disease resistance and susceptibility in scleractinian corals.     

Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR

Understanding the flexibility of the endosymbioses between scleractinian corals and single‐cell algae of the genus Symbiodinium will provide valuable insights into the future of coral reefs. Here, a real‐time polymerase chain reaction (PCR) assay is presented to accurately determine the cell densities of Symbiodinium clades C and D in the scleractinian coral Acropora millepora, which can be extended to other coral–symbiont associations in the future. The assay targets single‐ to low‐copy genes of the actin family of both the coral host and algal symbiont. Symbiont densities are expressed as the ratio of Symbiodinium cells to each host cell (S/H ratio, error within 30%), but can also be normalized to coral surface area. Greater accuracy in estimating ratios of associations involving multiple clades is achieved compared with previous real‐time PCR assays based on high‐copy ribosomal DNA loci (error within an order of magnitude). Healthy adult A. millepora containing ~1.4 × 10⁶ zooxanthellae per cm² (as determined by haemocytometer counts) had S/H ratios of c. 0.15, i.e. ~15 symbiont cells per 100 host cells. In severely bleached colonies, this ratio decreased to less than 0.005. Because of its capacity to accurately determine both densities and ratios of multiple symbionts within one sample, the assay will open the door for novel research into the mechanisms of symbiont shuffling and switching.     

The distribution of mycosporine-like amino acids (MAAs) and the phylogenetic identity of symbiotic dinoflagellates in cnidarian hosts from the Mexican Caribbean

A survey of 54 species of symbiotic cnidarians that included hydrozoan corals, anemones, gorgonians and scleractinian corals was conducted in the Mexican Caribbean for the presence of mycosporine-like amino acids (MAAs) in the host as well as the Symbiodinium fractions. The host fractions contained relatively simple MAA profiles, all harbouring between one and three MAAs, principally mycosporine-glycine followed by shinorine and porphyra-334 in smaller amounts. Symbiodinium populations were identified to sub-generic levels using PCR-DGGE analysis of the Internal Transcribed Spacer 2 (ITS2) region. Regardless of clade identity, all Symbiodinium extracts contained MAAs, in contrast to the pattern that has been found in cultures of Symbiodinium, where clade A symbionts produced MAAs whereas clade B, C, D, and E symbionts did not. Under natural conditions between one and four MAAs were identified in the symbiont fractions, mycosporine-glycine (λ_max = 310 nm), shinorine (λ_max = 334 nm), porphyra-334 (λ_max = 334 nm) and palythine (λ_max = 320 nm). One sample also contained mycosporine-2-glycine (λ_max = 331 nm). These data suggest that Symbiodinium is restricted to producing five MAAs and there also appears to be a defined order of appearance of these MAAs: mycosporine-glycine followed by shinorine (in one case mycosporine-2-glycine), then porphyra-334 and palythine. Overall, mycosporine-glycine was found in highest concentrations in the host and symbiont extracts. This MAA, unlike many other MAAs, absorbs within the ultraviolet-B range (UVB, 280-320 nm) and is also known for moderate antioxidant properties thus potentially providing protection against the direct and indirect effects of UVR. No depth-dependent changes could be identified due to a high variability of MAA concentrations when all species were included in the analysis. The presence of at least one MAA in all symbiont and host fractions analyzed serves to highlight the importance of MAAs, and in particular the role of mycosporine-glycine, as photoprotectants in the coral reef environment.     

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.     

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.     

Real-time PCR reveals a high incidence of <Emphasis Type="Italic">Symbiodinium </Emphasis>clade D at low levels in four scleractinian corals across the Great Barrier Reef: implications for symbiont shuffling

Reef corals form associations with an array of genetically and physiologically distinct endosymbionts from the genus Symbiodinium. Some corals harbor different clades of symbionts simultaneously, and over time the relative abundances of these clades may change through a process called symbiont shuffling. It is hypothesized that this process provides a mechanism for corals to respond to environmental threats such as global warming. However, only a minority of coral species have been found to harbor more than one symbiont clade simultaneously and the current view is that the potential for symbiont shuffling is limited. Using a newly developed real-time PCR assay, this paper demonstrates that previous studies have underestimated the presence of background symbionts because of the low sensitivity of the techniques used. The assay used here targets the multi-copy rDNA ITS1 region and is able to detect Symbiodinium clades C and D with >100-fold higher sensitivity compared to conventional techniques. Technical considerations relating to intragenomic variation, estimating copy number and non-symbiotic contamination are discussed. Eighty-two colonies from four common scleractinian species (Acropora millepora, Acropora tenuis, Stylophora pistillata and Turbinaria reniformis) and 11 locations on the Great Barrier Reef were tested for background Symbiodinium clades. Although these colonies had been previously identified as harboring only a single clade based on SSCP analyses, background clades were detected in 78% of the samples, indicating that the potential for symbiont shuffling may be much larger than currently thought.     

Highly stable symbioses among western Atlantic brooding corals

The reproductive mode of corals largely determines how zooxanthellae (Symbiodinium spp.) are acquired. Typically, broadcast spawning corals obtain symbionts from the surrounding environment, whereas most brooders transfer symbionts from maternal parent to offspring. Brooding corals are therefore predicted to harbor stable communities of Symbiodinium. This study documents the associations between Symbiodinium spp. and brooding corals in response to seasonal environmental fluctuations. Between March 2002 and December 2005, endosymbiont identity was determined seasonally from replicate colonies (n = 6) of three brooding species, Agaricia agaricites, Porites astreoides and Siderastrea radians, from shallow environments (1–4 m) of the Florida Keys and Bahamas. Symbionts were identified via denaturing gradient gel electrophoresis (DGGE) of the internal transcribed spacer 2 (ITS2) region. No change was detected in the Symbiodinium communities harbored within these brooding colonies. Additionally, no change in symbiosis was observed through a moderate bleaching event, thereby demonstrating that some bleached corals recover without changing symbionts.     

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.

     

The physiological response of reef corals to diel fluctuations in seawater temperature

An opportunity to explore the effects of fluctuating temperatures on tropical scleractinian corals arose when diurnal warming (as large as 4.7 °C) was detected over the rich coral communities found within the back reef of Moorea, French Polynesia. In April and May 2007, experiments were completed to determine the effects of fluctuating temperature on Pocillopora meandrina and Porites rus, and consecutive trials were used to expose them for 13 days to 26 °C, 28 °C (ambient conditions), 30 °C, or a fluctuating treatment ranging from 26 to 30 °C over 24 h. The multivariate response was assessed using maximum dark-adapted quantum yield of PSII (F_V/F_M), Symbiodinium density, chlorophyll-a content, and calcification. In trial 1, multivariate physiology of both species was significantly affected by treatments, with the fluctuating temperature resulting in a 17-45% decline in Symbiodinium density (relative to the ambient) matching that occurring at a constant 30 °C; F_V/F_M, chlorophyll-a content, and calcification, did not differ between the fluctuating and the steady treatments. In contrast, in trial 2 that utilized corals collected two weeks after those used in trial 1, the corals were unaffected by the treatments, likely due to an environment × trial interaction caused by seasonal declines in Symbiodinium density. Together, these results demonstrate that short transgressions to ecologically relevant high and low temperatures can elicit a potentially detrimental response equivalent to that occurring upon exposure to a constant high temperature. The dissimilar responses among dependent variables and consecutive trials underscore the importance of temporal replication and multivariate approaches in coral ecophysiology. It is likely that recent history has a stronger effect on the response of corals to treatments than is currently recognized.     

Symbiodinium Photosynthesis in Caribbean Octocorals

Symbioses with the dinoflagellate Symbiodinium form the foundation of tropical coral reef communities. Symbiodinium photosynthesis fuels the growth of an array of marine invertebrates, including cnidarians such as scleractinian corals and octocorals (e.g., gorgonian and soft corals). Studies examining the symbioses between Caribbean gorgonian corals and Symbiodinium are sparse, even though gorgonian corals blanket the landscape of Caribbean coral reefs. The objective of this study was to compare photosynthetic characteristics of Symbiodinium in four common Caribbean gorgonian species: Pterogorgia anceps, Eunicea tourneforti, Pseudoplexaura porosa, and Pseudoplexaura wagenaari. Symbiodinium associated with these four species exhibited differences in Symbiodinium density, chlorophyll a per cell, light absorption by chlorophyll a, and rates of photosynthetic oxygen production. The two Pseudoplexaura species had higher Symbiodinium densities and chlorophyll a per Symbiodinium cell but lower chlorophyll a specific absorption compared to P. anceps and E. tourneforti. Consequently, P. porosa and P. wagenaari had the highest average photosynthetic rates per cm² but the lowest average photosynthetic rates per Symbiodinium cell or chlorophyll a. With the exception of Symbiodinium from E. tourneforti, isolated Symbiodinium did not photosynthesize at the same rate as Symbiodinium in hospite. Differences in Symbiodinium photosynthetic performance could not be attributed to Symbiodinium type. All P. anceps (n = 9) and P. wagenaari (n = 6) colonies, in addition to one E. tourneforti and three P. porosa colonies, associated with Symbiodinium type B1. The B1 Symbiodinium from these four gorgonian species did not cluster with lineages of B1 Symbiodinium from scleractinian corals. The remaining eight E. tourneforti colonies harbored Symbiodinium type B1L, while six P. porosa colonies harbored type B1i. Understanding the symbioses between gorgonian corals and Symbiodinium will aid in deciphering why gorgonian corals dominate many Caribbean reefs.     

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.     

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.     

The genetic identity of dinoflagellate symbionts in Caribbean octocorals

Many cnidarians (e.g., corals, octocorals, sea anemones) maintain a symbiosis with dinoflagellates (zooxanthellae). Zooxanthellae are grouped into clades, with studies focusing on scleractinian corals. We characterized zooxanthellae in 35 species of Caribbean octocorals. Most Caribbean octocoral species (88.6%) hosted clade B zooxanthellae, 8.6% hosted clade C, and one species (2.9%) hosted clades B and C. Erythropodium caribaeorum harbored clade C and a unique RFLP pattern, which, when sequenced, fell within clade C. Five octocoral species displayed no zooxanthella cladal variation with depth. Nine of the ten octocoral species sampled throughout the Caribbean exhibited no regional zooxanthella cladal differences. The exception, Briareum asbestinum, had some colonies from the Dry Tortugas exhibiting the E. caribaeorum RFLP pattern while elsewhere hosting clade B. In the Caribbean, octocorals show more symbiont specificity at the cladal level than scleractinian corals. Both octocorals and scleractinian corals, however, exhibited taxonomic affinity between zooxanthella clade and host suborder.Communicated by R.C. Carpenter     

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.     

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.     

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.     

Phenotypic Variance Predicts Symbiont Population Densities in Corals: A Modeling Approach

Background

We test whether the phenotypic variance of symbionts (Symbiodinium) in corals is closely related with the capacity of corals to acclimatize to increasing seawater temperatures. Moreover, we assess whether more specialist symbionts will increase within coral hosts under ocean warming. The present study is only applicable to those corals that naturally have the capacity to support more than one type of Symbiodinium within the lifetime of a colony; for example, Montastraea annularis and Montastraea faveolata.

Methodology/Principal Findings

The population dynamics of competing Symbiodinium symbiont populations were projected through time in coral hosts using a novel, discrete time optimal–resource model. Models were run for two Atlantic Ocean localities. Four symbiont populations, with different environmental optima and phenotypic variances, were modeled to grow, divide, and compete in the corals under seasonal fluctuations in solar insolation and seawater temperature. Elevated seawater temperatures were input into the model 1.5°C above the seasonal summer average, and the symbiont population response was observed for each location. The models showed dynamic fluctuations in Symbiodinium populations densities within corals. Population density predictions for Lee Stocking Island, the Bahamas, where temperatures were relatively homogenous throughout the year, showed a dominance of both type 2, with high phenotypic variance, and type 1, a high-temperature and high-insolation specialist. Whereas the densities of Symbiodinium types 3 and 4, a high-temperature, low-insolation specialist, and a high-temperature, low-insolation generalist, remained consistently low. Predictions for Key Largo, Florida, where environmental conditions were more seasonally variable, showed the coexistence of generalists (types 2 and 4) and low densities of specialists (types 1 and 3). When elevated temperatures were input into the model, population densities in corals at Lee Stocking Island showed an emergence of high-temperature specialists. However, even under high temperatures, corals in the Florida Keys were dominated by generalists.

Conclusions/Significance

Predictions at higher seawater temperatures showed endogenous shuffling and an emergence of the high-temperature Symbiodinium specialists, even though their phenotypic variance was low. The model shows that sustaining these “hidden” specialists becomes advantageous under thermal stress conditions, and shuffling symbionts may increase the corals'' capacity to acclimatize but not adapt to climatechange–induced ocean warming.