New insights into the dynamics between reef corals and their associated dinoflagellate endosymbionts from population genetic studies

The mutualistic symbioses between reef‐building corals and micro‐algae form the basis of coral reef ecosystems, yet recent environmental changes threaten their survival. Diversity in host‐symbiont pairings on the sub‐species level could be an unrecognized source of functional variation in response to stress. The Caribbean elkhorn coral, Acropora palmata, associates predominantly with one symbiont species (Symbiodinium ‘fitti’), facilitating investigations of individual‐level (genotype) interactions. Individual genotypes of both host and symbiont were resolved across the entire species’ range. Most colonies of a particular animal genotype were dominated by one symbiont genotype (or strain) that may persist in the host for decades or more. While Symbiodinium are primarily clonal, the occurrence of recombinant genotypes indicates sexual recombination is the source of this genetic variation, and some evidence suggests this happens within the host. When these data are examined at spatial scales spanning the entire distribution of A. palmata, gene flow among animal populations was an order of magnitude greater than among populations of the symbiont. This suggests that independent micro‐evolutionary processes created dissimilar population genetic structures between host and symbiont. The lower effective dispersal exhibited by the dinoflagellate raises questions regarding the extent to which populations of host and symbiont can co‐evolve during times of rapid and substantial climate change. However, these findings also support a growing body of evidence, suggesting that genotype‐by‐genotype interactions may provide significant physiological variation, influencing the adaptive potential of symbiotic reef corals to severe selection.     

Microsatellite allele sizes alone are insufficient to delineate species boundaries in Symbiodinium

Symbiodinium are a diverse group of unicellular dinoflagellates that are important nutritional symbionts of reef‐building corals. Symbiodinium putative species (‘types’) are commonly identified with genetic markers, mostly nuclear and chloroplast encoded ribosomal DNA regions. Population genetic analyses using microsatellite loci have provided insights into Symbiodinium biogeography, connectivity and phenotypic plasticity, but are complicated by: (i) a lack of consensus criteria used to delineate inter‐ vs. intragenomic variation within species; and (ii) the high density of Symbiodinium in host tissues, which results in single samples comprising thousands of individuals. To address this problem, Wham & LaJeunesse (2016) present a method for identifying cryptic Symbiodinium species from microsatellite data based on correlations between allele size distributions and nongeographic genetic structure. Multilocus genotypes that potentially do not recombine in sympatry are interpreted as secondary ‘species’ to be discarded from downstream population genetic analyses. However, Symbiodinium species delineations should ideally incorporate multiple physiological, ecological and molecular criteria. This is because recombination tests may be a poor indicator of species boundaries in Symbiodinium due to their predominantly asexual mode of reproduction. Furthermore, discontinuous microsatellite allele sizes in sympatry may be explained by secondary contact between previously isolated populations and by mutations that occur in a nonstepwise manner. Limitations of using microsatellites alone to delineate species are highlighted in earlier studies that demonstrate occasional bimodal distributions of allele sizes within Symbiodinium species and considerable allele size sharing among Symbiodinium species. We outline these issues and discuss the validity of reinterpretations of our previously published microsatellite data from Symbiodinium populations on the Great Barrier Reef (Howells et al. 2013).     

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.     

The Relative Significance of Host–Habitat,Depth, and Geography on the Ecology,Endemism, and Speciation of Coral Endosymbionts in the Genus Symbiodinium

Dinoflagellates in the genus Symbiodinium are among the most abundant and important group of eukaryotic microbes found in coral reef ecosystems. Recent analyses conducted on various host cnidarians indicated that Symbiodinium assemblages in the Caribbean Sea are genetically and ecologically diverse. In order to further characterize this diversity and identify processes important to its origins, samples from six orders of Cnidaria comprising 45 genera were collected from reef habitats around Barbados (eastern Caribbean) and from the Mesoamerican barrier reef off the coast of Belize (western Caribbean). Fingerprinting of the ribosomal internal transcribed spacer 2 identified 62 genetically different Symbiodinium. Additional analyses of clade B Symbiodinium using microsatellite flanker sequences unequivocally characterized divergent lineages, or “species,” within what was previously thought to be a single entity (B1 or B184). In contrast to the Indo-Pacific where host-generalist symbionts dominate many coral communities, partner specificity in the Caribbean is relatively high and is influenced little by the host’s apparent mode of symbiont acquisition. Habitat depth (ambient light) and geographic isolation appeared to influence the bathymetric zonation and regional distribution for most of the Symbiodinium spp. characterized. Approximately 80% of Symbiodinium types were endemic to either the eastern or western Caribbean and 40–50% were distributed to compatible hosts living in shallow, high-irradiance, or deep, low-irradiance environments. These ecologic, geographic, and phylogenetic patterns indicate that most of the present Symbiodinium diversity probably originated from adaptive radiations driven by ecological specialization in separate Caribbean regions during the Pliocene and Pleistocene periods.     

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

Mutualistic organisms can be particularly susceptible to climate change stress, as their survivorship is often limited by the most vulnerable partner. However, symbiotic plasticity can also help organisms in changing environments by expanding their realized niche space. Coral–algal (Symbiodinium spp.) symbiosis exemplifies this dichotomy: the partnership is highly susceptible to ‘bleaching’ (stress‐induced symbiosis breakdown), but stress‐tolerant symbionts can also sometimes mitigate bleaching. Here, we investigate the role of diverse and mutable symbiotic partnerships in increasing corals' ability to thrive in high temperature conditions. We conducted repeat bleaching and recovery experiments on the coral Montastraea cavernosa, and used quantitative PCR and chlorophyll fluorometry to assess the structure and function of Symbiodinium communities within coral hosts. During an initial heat exposure (32 °C for 10 days), corals hosting only stress‐sensitive symbionts (Symbiodinium C3) bleached, but recovered (at either 24 °C or 29 °C) with predominantly (>90%) stress‐tolerant symbionts (Symbiodinium D1a), which were not detected before bleaching (either due to absence or extreme low abundance). When a second heat stress (also 32 °C for 10 days) was applied 3 months later, corals that previously bleached and were now dominated by D1a Symbiodinium experienced less photodamage and symbiont loss compared to control corals that had not been previously bleached, and were therefore still dominated by Symbiodinium C3. Additional corals that were initially bleached without heat by a herbicide (DCMU, at 24 °C) also recovered predominantly with D1a symbionts, and similarly lost fewer symbionts during subsequent thermal stress. Increased thermotolerance was also not observed in C3‐dominated corals that were acclimated for 3 months to warmer temperatures (29 °C) before heat stress. These findings indicate that increased thermotolerance post‐bleaching resulted from symbiont community composition changes, not prior heat exposure. Moreover, initially undetectable D1a symbionts became dominant only after bleaching, and were critical to corals' resilience after stress and resistance to future stress.     

The susceptibility and resilience of corals to thermal stress: adaptation,acclimatization or both?

Coral reefs are threatened with worldwide decline from multiple factors, chief among them climate change ( Hughes et al. 2003 ; Hoegh‐Guldberg et al. 2007 ). The foundation of coral reefs is an endosymbiosis between coral hosts and their resident photosynthetic dinoflagellates (genus Symbiodinium) and this partnership (or holobiont) is exquisitely sensitive to temperature stress. The primary response to hyperthermic stress is coral bleaching, which is the loss of symbionts from coral tissues—the collapse of the symbiosis ( Weis 2008 ). Bleaching can result in increased coral mortality which can ultimately lead to severely compromised reef health ( Hoegh‐Guldberg et al. 2007 ). Despite this grim picture of coral bleaching and reef degradation, coral susceptibility to stress and bleaching is highly variable ( Coles & Brown 2003 ). There is enormous interest in discovering the factors that determine susceptibility in order to help us predict if and how corals will survive a period of rapid global warming. In this issue, Barshis et al. (2010) examine the ecophysiological and genetic basis for differential responses to stress in Porites lobata in American Samoa. They combine a reciprocal transplant experimental design between two neighbouring, but very different reef environments with state‐of‐the‐art physiological biomarkers and molecular genetic markers for both partners to tease apart the contribution of environmental and fixed influences on stress susceptibility. Their results suggest the presence of a fixed, rather than environmental effect on expression of ubiquitin conjugates, one key marker for physiological stress response. In addition, the authors show genetic differentiation in host populations between the two sites suggesting strong selection for physiological adaptation to differing environments across small geographic distances. These conclusions point the study of coral resilience and susceptibility in a new direction.     

Patterns of Symbiodinium (Dinophyceae) diversity and assemblages among diverse hosts and the coral reef environment of Lizard Island,Australia

Large‐scale environmental disturbances may impact both partners in coral host–Symbiodinium systems. Elucidation of the assembly patterns in such complex and interdependent communities may enable better prediction of environmental impacts across coral reef ecosystems. In this study, we investigated how the community composition and diversity of dinoflagellate symbionts in the genus Symbiodinium were distributed among 12 host species from six taxonomic orders (Actinaria, Alcyonacea, Miliolida, Porifera, Rhizostoma, Scleractinia) and in the reef water and sediments at Lizard Island, Great Barrier Reef before the 3rd Global Coral Bleaching Event. 454 pyrosequencing of the ITS2 region of Symbiodinium yielded 83 operational taxonomic units (OTUs) at a 97% similarity cut‐off. Approximately half of the Symbiodinium OTUs from reef water or sediments were also present in symbio. OTUs belonged to six clades (A‐D, F‐G), but community structure was uneven. The two most abundant OTUs (100% matches to types C1 and A3) comprised 91% of reads and OTU C1 was shared by all species. However, sequence‐based analysis of these dominant OTUs revealed host species specificity, suggesting that genetic similarity cut‐offs of Symbiodinium ITS2 data sets need careful evaluation. Of the less abundant OTUs, roughly half occurred at only one site or in one species and the background Symbiodinium communities were distinct between individual samples. We conclude that sampling multiple host taxa with differing life history traits will be critical to fully understand the symbiont diversity of a given system and to predict coral ecosystem responses to environmental change and disturbance considering the differential stress response of the taxa within.     

New Species of Closely Related Endosymbiotic Dinoflagellates in the Greater Caribbean have Niches Corresponding to Host Coral Phylogeny

Symbiotic dinoflagellates in the genus Breviolum (formerly Symbiodinium Clade B) dominate coral communities in shallow waters across the Greater Caribbean. While some formally described species exist, mounting genetic, and ecological evidence indicate that numerous more comprise this genus, many of which are closely related. To test this, colonies of common reef‐building corals were sampled across a large geographical range. Phylogenetic and population genetic markers then used to examine evolutionary divergence and delineate boundaries of genetic recombination. Three new candidate species were distinguished by fixed differences in nucleotide sequences from nuclear and chloroplast DNA. Population connectivity was evident within each lineage over thousands of kilometers, however, substantial genetic structure persisted between lineages co‐occurring within sampling locations, signifying reproductive isolation. While geographically widespread with overlapping distributions, each species is ecologically distinct, exhibiting specific mutualisms with phylogenetically distinct coral hosts. Moreover, significant differences in mean cell sizes provide some morphological evidence substantiating formal species distinctions. In providing evidence that satisfies the biological, phylogenetic, ecological, and morphological species concepts, we classify and formally name Breviolum faviinorum n. sp., primarily associated with Caribbean corals belonging to the Caribbean subfamily Faviinae; B. meandrinium n. sp., associated with corals belonging to the family Meandrinidae; and B. dendrogyrum n. sp., a symbiont harbored exclusively by the threatened coral Dendrogyra cylindrus. These findings support the primary importance of niche diversification (i.e. host habitat) in the speciation of symbiotic dinoflagellates.     

Functional genomic analysis of corals from natural CO2‐seeps reveals core molecular responses involved in acclimatization to ocean acidification

Little is known about the potential for acclimatization or adaptation of corals to ocean acidification and even less about the molecular mechanisms underpinning these processes. Here, we examine global gene expression patterns in corals and their intracellular algal symbionts from two replicate population pairs in Papua New Guinea that have undergone long‐term acclimatization to natural variation in pCO₂. In the coral host, only 61 genes were differentially expressed in response to pCO₂ environment, but the pattern of change was highly consistent between replicate populations, likely reflecting the core expression homeostasis response to ocean acidification. Functional annotations highlight lipid metabolism and a change in the stress response capacity of corals as key parts of this process. Specifically, constitutive downregulation of molecular chaperones was observed, which may impact response to combined climate change‐related stressors. Elevated CO₂ has been hypothesized to benefit photosynthetic organisms but expression changes of in hospite Symbiodinium in response to acidification were greater and less consistent among reef populations. This population‐specific response suggests hosts may need to adapt not only to an acidified environment, but also to changes in their Symbiodinium populations that may not be consistent among environments, adding another challenging dimension to the physiological process of coping with climate change.     

Cryptic diversity hides host and habitat specialization in a gorgonian‐algal symbiosis

Shallow water anthozoans, the major builders of modern coral reefs, enhance their metabolic and calcification rates with algal symbionts. Controversy exists over whether these anthozoan–algae associations are flexible over the lifetimes of individual hosts, promoting acclimative plasticity, or are closely linked, such that hosts and symbionts co‐evolve across generations. Given the diversity of algal symbionts and the morphological plasticity of many host species, cryptic variation within either partner could potentially confound studies of anthozoan‐algal associations. Here, we used ribosomal, organelle and nuclear sequences, along with microsatellite variation, to study the relationship between lineages of a common Caribbean gorgonian and its algal symbionts. The gorgonian Eunicea flexuosa is a broadcast spawner, composed of two recently diverged, genetically distinct lineages largely segregated by depth. We sampled colonies of the two lineages across depth gradients at three Caribbean locations. We find that each host lineage is associated with a unique Symbiodinium B1/184 phylotype. This relationship between host and symbiont is maintained when host colonies are reciprocally transplanted, although cases of within phylotype switching were also observed. Even when the phylotypes of both partners are present at intermediate depths, the specificity between host and symbiont lineages remained absolute. Unrecognized cryptic diversity may mask host‐symbiont specificity and change the inference of evolutionary processes in mutualistic associations. Symbiotic specificity thus likely contributes to the ecological divergence of the two partners, generating species diversity within coral reefs.     

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

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

Symbiont acquisition strategy drives host–symbiont associations in the southern Great Barrier Reef

Coral larvae acquire populations of the symbiotic dinoflagellate Symbiodinium from the external environment (horizontal acquisition) or inherit their symbionts from the parent colony (maternal or vertical acquisition). The effect of the symbiont acquisition strategy on Symbiodinium-host associations has not been fully resolved. Previous studies have provided mixed results, probably due to factors such as low sample replication of Symbiodinium from a single coral host, biogeographic differences in Symbiodinium diversity, and the presence of some apparently host-specific symbiont lineages in coral with either symbiont acquisition strategies. This study set out to assess the effect of the symbiont acquisition strategy by sampling Symbiodinium from 10 coral species (five with a horizontal and five with a vertical symbiont acquisition strategy) across two adjacent reefs in the southern Great Barrier Reef. Symbiodinium diversity was assessed using single-stranded conformational polymorphism of partial nuclear large subunit rDNA and denaturing gradient gel electrophoresis of the internal transcribed spacer 2 region. The Symbiodinium population in hosts with a vertical symbiont acquisition strategy partitioned according to coral species, while hosts with a horizontal symbiont acquisition strategy shared a common symbiont type across the two reef environments. Comparative analysis of existing data from the southern Great Barrier Reef found that the majority of corals with a vertical symbiont acquisition strategy associated with distinct species- or genus-specific Symbiodinium lineages, but some could also associate with symbiont types that were more commonly found in hosts with a horizontal symbiont acquisition strategy.     

Latent virus‐like infections are present in a diverse range of Symbiodinium spp. (Dinophyta)

Coral reefs are increasingly threatened by disease outbreaks, which affect the coral animal and/or its algal symbionts (Symbiodinium spp.) and can cause mass mortalities. Currently around half of the recognized coral diseases have unknown causative agents. While many of the diseases are thought to be bacterial in origin, there is growing evidence that viruses may play a role. In particular, it appears that viruses may infect the algal symbionts, causing breakdown of the coral‐algal mutualism. In this study, we screened a wide range of Symbiodinium cultures in vitro for the presence of latent viral infections. Using flow cytometry and electron microscopy, we found that many types of Symbiodinium apparently harbor such infections, and that the type of putative virus varied within and among host types. Furthermore, the putative viral infections could be induced via abiotic stress and cause host cell lysis and population decline. If similar processes occur in Symbiodinium cells in hospite, they may provide an explanation for some of the diseases affecting corals and other organisms forming symbioses with these algae.     

Ecological Inferences from a deep screening of the Complex Bacterial Consortia associated with the coral,Porites astreoides

The functional role of the bacterial organisms in the reef ecosystem and their contribution to the coral well‐being remain largely unclear. The first step in addressing this gap of knowledge relies on in‐depth characterization of the coral microbial community and its changes in diversity across coral species, space and time. In this study, we focused on the exploration of microbial community assemblages associated with an ecologically important Caribbean scleractinian coral, Porites astreoides, using Illumina high‐throughput sequencing of the V5 fragment of 16S rRNA gene. We collected data from a large set of biological replicates, allowing us to detect patterns of geographical structure and resolve co‐occurrence patterns using network analyses. The taxonomic analysis of the resolved diversity showed consistent and dominant presence of two OTUs affiliated with the order Oceanospirillales, which corroborates a specific pattern of bacterial association emerging for this coral species and for many other corals within the genus Porites. We argue that this specific association might indicate a symbiotic association with the adult coral partner. Furthermore, we identified a highly diverse rare bacterial ‘biosphere’ (725 OTUs) also living along with the dominant bacterial symbionts, but the assemblage of this biosphere is significantly structured along the geographical scale. We further discuss that some of these rare bacterial members show significant association with other members of the community reflecting the complexity of the networked consortia within the coral holobiont.     

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.     

Rapid thermal adaptation in photosymbionts of reef‐building corals

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

Evaluating Methods for Transplanting Endangered Elkhorn Corals in the Virgin Islands

Restoration of rare corals is desirable and restoration projects are fairly common, but scientific evaluation of this approach is limited. We tested several techniques for transplant and restabilization of Acropora palmata (the elkhorn coral), an ecologically important Caribbean coral whose populations have suffered severe declines. In rough weather, fragments break‐off colonies of branching corals like A. palmata as a normal form of asexual reproduction. We transplanted naturally produced coral fragments from remnant populations to nearby restoration sites. Untouched control fragments at the donor site died faster and grew slower than fragments attached to the reef, so attaching fragments to the reef is beneficial. Transplanted fragments grew and died at a rate similar to fragments left at the donor site (both groups were attached to the reef), so there were no effects of moving fragments or differences in habitat quality between donor and restoration sites. Growth and survival were similar using four methods of attaching fragments to the reef: cable ties, two types of epoxy resin, and hydrostatic cement. Corals sometimes compete with the macroalgae that dominate degraded reefs, and clearing surrounding algae improved the growth of fragments. After 4 years, transplanted fragments grew to 1,450 cm² in area and so were potentially sexually active. Because the methods tested are simple and cheap, they could be used by volunteer recreational divers to restore locally extirpated A. palmata populations or to enhance reefs where natural recovery is slow.     

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

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