Oxidative stress causes coral bleaching during exposure to elevated temperatures

 Elevated temperatures and solar ultraviolet (UV) radiation have been implicated as recent causes for the loss of symbiotic algae (i.e., bleaching) in corals and other invertebrates with photoautotrophic symbionts. One hypothesized mechanism of coral bleaching involves the production of reduced oxygen intermediates, or toxic oxygen, in the dinoflagellate symbionts and host tissues that subsequently causes cellular damage and expulsion of symbionts. Measurements of photosynthesis in the Caribbean coral Agaricia tenuifolia, taken during temperature-induced stress and exposure to full solar radiation, showed a decrease in photosynthetic performance followed by bleaching. Exposure of corals to exogenous antioxidants that scavenge reactive oxygen species during temperature-induced stress improves maximum photosynthetic capacity to rates indistinguishable from corals measured at the ambient temperature of their site of collection. Additionally, these antioxidants prevent the coral from “ bleaching ” and affect the mechanism of symbiont loss from the coral host. These observations confirm a role for oxidative stress, whether caused by elevated temperatures or exposure to UV radiation, in the bleaching phenomenon. Accepted: 18 October 1996     

Symbiotic specificity,association patterns,and function determine community responses to global changes: defining critical research areas for coral‐Symbiodinium symbioses

Climate change‐driven stressors threaten the persistence of coral reefs worldwide. Symbiotic relationships between scleractinian corals and photosynthetic endosymbionts (genus Symbiodinium) are the foundation of reef ecosystems, and these associations are differentially impacted by stress. Here, we couple empirical data from the coral reefs of Moorea, French Polynesia, and a network theoretic modeling approach to evaluate how patterns in coral‐Symbiodinium associations influence community stability under climate change. To introduce the effect of climate perturbations, we simulate local ‘extinctions’ that represent either the loss of coral species or the ability to engage in symbiotic interactions. Community stability is measured by determining the duration and number of species that persist through the simulated extinctions. Our results suggest that four factors greatly increase coral‐Symbiodinium community stability in response to global changes: (i) the survival of generalist hosts and symbionts maximizes potential symbiotic unions; (ii) elevated symbiont diversity provides redundant or complementary symbiotic functions; (iii) compatible symbiotic assemblages create the potential for local recolonization; and (iv) the persistence of certain traits associate with symbiotic diversity and redundancy. Symbiodinium may facilitate coral persistence through novel environmental regimes, but this capacity is mediated by symbiotic specificity, association patterns, and the functional performance of the symbionts. Our model‐based approach identifies general trends and testable hypotheses in coral‐Symbiodinium community responses. Future studies should consider similar methods when community size and/or environmental complexity preclude experimental approaches.     

Dynamics of lipid and fatty acid composition of shallow-water corals under thermal stress: an experimental approach

Coral bleaching induces changes in lipid and fatty acid composition that result in low lipid content, reducing the likelihood of coral survival. Species-specific differences in the metabolism of lipid reserves may contribute to the differential resistance of corals under acute heat exposures. Here, we examined the dynamics of lipids and fatty acid abundance in corals subjected to short-term heat stress. The stony corals Acropora intermedia, Montipora digitata, and the soft coral Sinularia capitalis all showed a 60–75% decline in both storage and structural lipids. However, S. capitalis and M. digitata exhibited no significant change in the percentages of structural lipids (i.e., polar lipids and sterols) until they had lost 90–95% of their endosymbionts, whereas A. intermedia showed a rapid decline in structural lipids after a 50% loss of symbionts. After a 90–95% loss of symbionts under heat stress, all three corals showed a relative depletion of polyunsaturated fatty acids that had symbiont biomarkers, suggesting that polyunsaturated fatty acids were translocated from the symbiont to the coral host tissue.     

Regional and local variability in recovery of shallow coral communities: Moorea,French Polynesia and central Great Barrier Reef

Coral communities at Moorea, French Polynesia, and on the Great Barrier Reef (GBR), Australia, were severely depleted by disturbances early in the 1980s. Corals were killed by the predatory starfish Acanthaster planci, by cyclones, and/or by depressed sea level. This study compares benthic community structure and coral population structures on three disturbed reefs (Vaipahu-Moorea; Rib and John Brewer Reefs-GBR) and one undisturbed reef (Davies Reef-GBR) in 1987–89. Moorea barrier reefs had been invaded by tall macrophytes Turbinaria ornata and Sargassum sp., whereas the damaged GBR reefs were colonised by a diverse mixture of short macrophytes, turfs and coralline algae. The disturbed areas had broadly similar patterns of living and dead standing coral, and similar progress in recolonisation, which suggests their structure may converge towards that of undisturbed Davies Reef. Corals occupying denuded areas at Vaipahu, Rib and John Brewer were small (median diameter 5 cm in each case) and sparse (means 4–8 m^-2) compared to longer established corals at Davies Reef (median diameter 9 cm; mean 18 m^-2). At Moorea, damselfish and sea urchins interacted with corals in ways not observed in the GBR reefs. Territories of the damselfish Stegastes nigricans covered much of Moorea's shallow reef top. They had significantly higher diversity and density of post-disturbance corals than areas outside of territories, suggesting that the damselfish exerts some influences on coral community dynamics. Sea urchins on Moorea (Diadema setosum Echinometra mathaei, Echinotrix calamaris) were causing widespread destruction of dead standing coral skeletons. Overall, it appears that the future direction and speed of change in the communities will be explicable more in terms of local than regional processes.     

<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.     

Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea

Disturbances have a critical effect on the structure of natural communities. In this study long-term changes were examined in the reef community at Tiahura Reef, on the northern coast of Moorea, which had been subject to many and varied disturbances over the last 25 years. Tiahura Reef was subject to an outbreak of crown-of-thorns starfish (Acanthaster planci) in 1980–1981, causing significant declines in the abundance of scleractinian corals and butterflyfishes. By 2003, the abundance of corals and butterflyfishes had returned to former levels, but despite this apparent recovery, the species composition of coral communities and butterflyfish assemblages was very different from those recorded in 1979. Ongoing disturbances (including further outbreaks of crown-of-thorns starfish, cyclones, and coral bleaching events) appear to have prevented recovery of many important coral species (notably, Acropora spp.), which has had subsequent effects on the community structure of coral-feeding butterflyfishes. This study shows that recurrent disturbances may have persistent effects on the structure and dynamics of natural communities.     

Recent disturbances augment community shifts in coral assemblages in Moorea, French Polynesia

Coral reefs are often subject to disturbances that can cause enduring changes in community structure and abundance of coral reef organisms. In Moorea, French Polynesia, frequent disturbances between 1979 and 2003 caused marked shifts in taxonomic composition of coral assemblages. This study explores recent changes in live cover and taxonomic structure of coral communities on the north coast of Moorea, French Polynesia, to assess whether coral assemblages are recovering (returning to a previous Acropora-dominated state) or continuing to move towards an alternative community structure. Coral cover declined by 29.7% between July 2003 and March 2009, mostly due to loss of Acropora and Montipora spp. Coral mortality varied among habitats, with highest levels of coral loss on the outer reef slope (7–20 m depth). In contrast, there was limited change in coral cover within the lagoon, and coral cover actually increased on the reef crest. Observed changes in coral cover and composition correspond closely with the known feeding preferences and observed spatial patterns of Acanthaster planci L., though observed coral loss also coincided with at least one episode of coral bleaching, as well as persistent populations of the corallivorous starfish Culcita novaeguineae Muller & Troschel. While climate change poses an important and significant threat to the future structure and dynamics coral reef communities, outbreaks of A. planci remain a significant cause of coral loss in Moorea. More importantly, these recent disturbances have followed long-term shifts in the structure of coral assemblages, and the relative abundance of both Pocillopora and Porites continue to increase due to disproportionate losses of Acropora and Montipora. Moreover, Pocillopora and Porites dominate assemblages of juvenile corals, suggesting that there is limited potential for a return to an Acropora-dominated state, last recorded in 1979.     

Different responses of scleractinian coral Acropora pruinosa from Weizhou Island during extreme high temperature events

Ecological surveys observe coral “winners” and “losers” in global coral bleaching events. However, the key contributors to holobiont tolerance and interactions between symbionts remain unclear. Herein, we compared bleaching and unbleaching Acropora pruinosa corals from Weizhou Island, during an extreme high-temperature event in the northern South China Sea in 2020. We found the dominant Symbiodiniaceae subclade in the bleaching and unbleaching corals to be C1; however, the density of Symbiodiniaceae in the latter was significantly higher than that in the former. Additionally, the symbiotic bacteria α diversity in the unbleaching coral was significantly higher than that in the bleaching coral, with a reorganized bacterial community structure. Core microbiome analyses revealed 55 bacterial core operational taxonomic units (OTUs), of which 10 were significantly differentially enriched between the two coral groups. The significantly enriched bacterial core OTUs in the unbleaching coral were primarily nitrogen cycling related, while those enriched in the bleaching coral were associated with antimicrobial activity. RNA-Seq analyses revealed that significantly upregulated genes in the bleaching coral were primarily associated with diseases and autophagy, while those in the unbleaching coral were associated with immune defense and maintenance of the symbiotic relationship between corals and symbionts. We propose that the differences in tolerance of A. pruinosa result from the cooperation between coral host, Symbiodiniaceae, and symbiotic bacteria. In extreme high-temperature events, unbleaching corals may maintain stable symbiotic relationships by increasing the diversity of symbiotic bacteria, regulating the structure of the symbiotic bacteria community, improving the interaction between coral host and symbiont and enhancing host immunity, thus avoiding coral bleaching. This study illuminates the relationship between the coral symbiont and tolerance differences of coral holobionts, providing new insights for further exploration into the adaptability of scleractinian corals in the context of global warming.

     

Do fluctuating temperature environments elevate coral thermal tolerance?

In reef corals, much research has focused on the capacity of corals to acclimatize and/or adapt to different thermal environments, but the majority of work has focused on distinctions in mean temperature. Across small spatial scales, distinctions in daily temperature variation are common, but the role of such environmental variation in setting coral thermal tolerances has received little attention. Here, we take advantage of back-reef pools in American Samoa that differ in thermal variation to investigate the effects of thermally fluctuating environments on coral thermal tolerance. We experimentally heat-stressed Acropora hyacinthus from a thermally moderate lagoon pool (temp range 26.5–33.3°C) and from a more thermally variable pool that naturally experiences 2–3 h high temperature events during summer low tides (temp range 25.0–35°C). We compared mortality and photosystem II photochemical efficiency of colony fragments exposed to ambient temperatures (median: 28.0°C) or elevated temperatures (median: 31.5°C). In the heated treatment, moderate pool corals showed nearly 50% mortality whether they hosted heat-sensitive (49.2 ± 6.5% SE; C2) or heat-resistant (47.0 ± 11.2% SE; D) symbionts. However, variable pool corals, all of which hosted heat-resistant symbionts, survived well, showing low mortalities (16.6 ± 8.8% SE) statistically indistinguishable from controls held at ambient temperatures (5.1–8.3 ± 3.3–8.3% SE). Similarly, moderate pool corals hosting heat-sensitive algae showed rapid rates of decline in algal photosystem II photochemical efficiency in the elevated temperature treatment (slope = −0.04 day⁻¹ ± 0.007 SE); moderate pool corals hosting heat-resistant algae showed intermediate levels of decline (slope = −0.039 day⁻¹ ± 0.007 SE); and variable pool corals hosting heat-resistant algae showed the least decline (slope = −0.028 day⁻¹ ± 0.004 SE). High gene flow among pools suggests that these differences probably reflect coral acclimatization not local genetic adaptation. Our results suggest that previous exposure to an environmentally variable microhabitat adds substantially to coral–algal thermal tolerance, beyond that provided by heat-resistant symbionts alone.     

Discordant coral–symbiont structuring: factors shaping geographical variation of Symbiodinium communities in a facultative zooxanthellate coral genus,Oculina

Understanding the factors that help shape the association between corals and their algal symbionts, zooxanthellae (Symbiodinium), is necessary to better understand the functional diversity and acclimatization potential of the coral host. However, most studies focus on tropical zooxanthellate corals and their obligate algal symbionts, thus limiting our full comprehension of coral–algal symbiont associations. Here, we examine algal associations in a facultative zooxanthellate coral. We survey the Symbiodinium communities associated with Oculina corals in the western North Atlantic and the Mediterranean using one clade-level marker (psbA coding region) and three fine-scale markers (cp23S–rDNA, b7sym15 flanking region, and b2sym17). We ask whether Oculina spp. harbor geographically different Symbiodinium communities across their geographic range and, if so, whether the host’s genetics or habitat differences are correlated with this geographical variation. We found that Oculina corals harbor different Symbiodinium communities across their geographical range. Of the habitat differences (including chlorophyll a concentration and depth), sea surface temperature is better correlated with this geographical variation than the host’s genetics, a pattern most evident in the Mediterranean. Our results suggest that although facultative zooxanthellate corals may be less dependent on their algal partners compared to obligate zooxanthellate corals, the Symbiodinium communities that they harbor may nevertheless reflect acclimatization to environmental variation among habitats.

     

Host tolerance,not symbiont tolerance,determines the distribution of coral species in relation to their environment at a Central Pacific atoll

Tolerance of environmental variables differs between corals and their dinoflagellate symbionts (Symbiodinium spp.), controlling the holobiont’s (host and symbiont combined) resilience to environmental stress. However, the ecological role that environmental variables play in holobiont distribution remains poorly understood. We compared the drivers of symbiont and coral species distributions at Palmyra Atoll, a location with a range of reef environments from low to high sediment concentrations (1–52 g dry weight m⁻² day⁻¹). We observed uniform holobiont partnerships across the atoll (e.g. Montipora spp. with Symbiodinium type C15 at all sites). Multivariate analysis revealed that field-based estimates of settling sediment predominantly explained the spatial variation of coral species among sites (P < 0.01). However, none of the environmental variables measured (sedimentation, temperature, chlorophyll concentration, salinity) affected symbiont distribution. The discord between environmental variables and symbiont distributions suggests that the symbionts are physiologically tolerant of the variable environmental regime across this location and that the distribution of different host–symbiont combinations present is largely dependent on coral rather than Symbiodinium physiology. The data highlight the importance of host tolerance to environmental stressors, which should be considered simultaneously with symbiont sensitivity when considering the impact of variations in environmental conditions on coral communities.     

Associational refuges among corals mediate impacts of a crown-of-thorns starfish Acanthaster planci outbreak Indirect positive interactions in communities

Interactions among coral populations can moderate the impact of coral predator outbreaks, enhancing community resilience and recovery. This study used predator-exclusion cages and neighbour removals in a field experiment to test how indirect interactions between populations of three coral taxa, Acropora, Pocillopora, and Porites, influenced their survival during an outbreak of the crown-of-thorns starfish, Acanthaster planci, in Moorea, French Polynesia. High densities of corals enhanced survival by generating associational refuges: physical structures that impeded Acanthaster and protected corals, and by simple density-dependent prey dilution that reduced predation rates. Acanthaster showed feeding preferences, resulting in varying intensities of predation on corals, which (1) influenced the type and strength of the associational refuge among corals and (2) resulted in significant loss of the competitive dominants to the benefit of the competitive inferiors. The result was a set of indirect positive interactions (IPIs) that prevented Acanthaster from eradicating Acropora and may have enhanced Porites, a relatively weak competitor among corals. IPIs probably play a key role in many ecosystems, especially in coral reefs in which corals act as engineer species, to reduce impacts of perturbations and enhance community resilience. This study illustrates the importance of IPIs in community regulation with a new conceptual model.     

Modulation of Light-Enhancement to Symbiotic Algae by Light-Scattering in Corals and Evolutionary Trends in Bleaching

Calcium carbonate skeletons of scleractinian corals amplify light availability to their algal symbionts by diffuse scattering, optimizing photosynthetic energy acquisition. However, the mechanism of scattering and its role in coral evolution and dissolution of algal symbioses during “bleaching” events are largely unknown. Here we show that differences in skeletal fractal architecture at nano/micro-lengthscales within 96 coral taxa result in an 8-fold variation in light-scattering and considerably alter the algal light environment. We identified a continuum of properties that fall between two extremes: (1) corals with low skeletal fractality that are efficient at transporting and redistributing light throughout the colony with low scatter but are at higher risk of bleaching and (2) corals with high skeletal fractality that are inefficient at transporting and redistributing light with high scatter and are at lower risk of bleaching. While levels of excess light derived from the coral skeleton is similar in both groups, the low-scatter corals have a higher rate of light-amplification increase when symbiont concentration is reduced during bleaching, thus creating a positive feedback-loop between symbiont concentration and light-amplification that exposes the remaining symbionts to increasingly higher light intensities. By placing our findings in an evolutionary framework, in conjunction with a novel empirical index of coral bleaching susceptibility, we find significant correlations between bleaching susceptibility and light-scattering despite rich homoplasy in both characters; suggesting that the cost of enhancing light-amplification to the algae is revealed in decreased resilience of the partnership to stress.     

Development of coral and zooxanthella‐specific microsatellites in three species of Pocillopora (Cnidaria,Scleractinia) from French Polynesia

Since the building of coral reefs results from the association of corals and zooxanthellae, their intracellular algal symbionts, genetic markers for both organisms are essential for studying the contribution of their respective dispersal to the resilience of endangered reef ecosystems. Very few microsatellites have been obtained in corals thus far. Here we report the successful cloning of six polymorphic microsatellites (allele number: 5–15) from Pocillopora verrucosa, P. meandrina and P. damicornis. Four of them amplified coral, and two amplified zooxanthella DNA.     

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.     

Coral bleaching is linked to the capacity of the animal host to supply essential metals to the symbionts

Massive coral bleaching events result in extensive coral loss throughout the world. These events are mainly caused by seawater warming, but are exacerbated by the subsequent decrease in nutrient availability in surface waters. It has therefore been shown that nitrogen, phosphorus or iron limitation contribute to the underlying conditions by which thermal stress induces coral bleaching. Generally, information on the trophic ecology of trace elements (micronutrients) in corals, and on how they modulate the coral response to thermal stress is lacking. Here, we demonstrate for the first time that heterotrophic feeding (i.e. the capture of zooplankton prey by the coral host) and thermal stress induce significant changes in micro element concentrations and isotopic signatures of the scleractinian coral Stylophora pistillata. The results obtained first reveal that coral symbionts are the major sink for the heterotrophically acquired micronutrients and accumulate manganese, magnesium and iron from the food. These metals are involved in photosynthesis and antioxidant protection. In addition, we show that fed corals can maintain high micronutrient concentrations in the host tissue during thermal stress and do not bleach, whereas unfed corals experience a significant decrease in copper, zinc, boron, calcium and magnesium in the host tissue and bleach. In addition, the significant increase in δ⁶⁵Cu and δ⁶⁶Zn signature of symbionts and host tissue at high temperature suggests that these isotopic compositions are good proxy for stress in corals. Overall, present findings highlight a new way in which coral heterotrophy and micronutrient availability contribute to coral resistance to global warming and bleaching.     

Phylogenetically Diverse Denitrifying and Ammonia-Oxidizing Bacteria in Corals Alcyonium gracillimum and Tubastraea coccinea

To date, the association of coral–bacteria and the ecological roles of bacterial symbionts in corals remain largely unknown. In particular, little is known about the community components of bacterial symbionts of corals involved in the process of denitrification and ammonia oxidation. In this study, the nitrite reductase (nirS and nirK) and ammonia monooxygenase subunit A (amoA) genes were used as functional markers. Diverse bacteria with the potential to be active as denitrifiers and ammonia-oxidizing bacteria (AOB) were found in two East China Sea corals: stony coral Alcyonium gracillimum and soft coral Tubastraea coccinea. The 16S rRNA gene library analysis demonstrated different communities of bacterial symbionts in these two corals of the same location. Nitrite reductase nirK gene was found only in T. coccinea, while both nirK and nirS genes were detected in A. gracillimum, which might be the result of the presence of different bacterial symbionts in these two corals. AOB rather than ammonia-oxidizing archaea were detected in both corals, suggesting that AOB might play an important role in the ammonia oxidation process of the corals. This study indicates that the coral bacterial symbionts with the potential for nitrite reduction and ammonia oxidation might have multiple ecological roles in the coral holobiont, which promotes our understanding of bacteria-mediated nitrogen cycling in corals. To our knowledge, this study is the first assessment of the community structure and phylogenetic diversity of denitrifying bacteria and AOB in corals based on nirK, nirS, and amoA gene library analysis.     

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.