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Evolutionary tradeoffs between life-history strategies are central to animal evolution. However, because microbes can influence aspects of host physiology, behavior, and resistance to stress or disease, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a highly biodiverse and data-rich host system to test this idea, made more relevant by increases in coral disease outbreaks as a result of anthropogenic changes to climate and reef ecosystems. Identifying factors that determine coral disease susceptibility has therefore become a focus for reef conservation efforts. Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by combining a cross-species coral microbiome survey (the “Global Coral Microbiome Project”) with long-term disease prevalence data at multiple sites. Interpreting these data in their phylogenetic context, we show that microbial dominance and composition predict disease susceptibility. We trace this dominance-disease association to a single putatively beneficial bacterial symbiont,Endozoicomonas, whose relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera. Conversely,Endozoicomonasabundances in coral tissue strongly correlated with high growth rates. These results demonstrate that the evolution of microbial symbiosis in corals correlates with both disease prevalence and growth rate. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbiosis influences animal life-history tradeoffs, and in efforts to use microbes to increase coral growth or disease resistancein-situ.Significance StatementThe evolution of tropical corals, like that of many organisms, involves tradeoffs in life-history strategy. We sought to test whether microbes influence coral life-history traits. Comparative data from a census of modern coral microbes, combined with long term disease surveys in three regions, provide evidence for a correlation between microbiome structure, growth rate, and disease susceptibility during coral evolution. These trends were driven primarily by changes in the relative abundance ofEndozoicomonasin coral tissue microbiomes, suggesting the novel hypothesis thatEndozoicomonasmay allow corals to grow more quickly at the cost of greater vulnerability to disease. Thus, symbiosis with microbes may be an important aspect of animal life-history strategy.

Corals are dependent upon lipids as energy reserves to mount a metabolic response to biotic and abiotic challenges. This study profiled lipids, fatty acids, and microbial communities of healthy and white syndrome (WS) diseased colonies of Acropora hyacinthus sampled from reefs in Western Australia, the Great Barrier Reef, and Palmyra Atoll. Total lipid levels varied significantly among locations, though a consistent stepwise decrease from healthy tissues from healthy colonies (HH) to healthy tissue on WS-diseased colonies (HD; i.e. preceding the lesion boundary) to diseased tissue on diseased colonies (DD; i.e. lesion front) was observed, demonstrating a reduction in energy reserves. Lipids in HH tissues were comprised of high energy lipid classes, while HD and DD tissues contained greater proportions of structural lipids. Bacterial profiling through 16S rRNA gene sequencing and histology showed no bacterial taxa linked to WS causation. However, the relative abundance of Rhodobacteraceae-affiliated sequences increased in DD tissues, suggesting opportunistic proliferation of these taxa. While the cause of WS remains inconclusive, this study demonstrates that the lipid profiles of HD tissues was more similar to DD tissues than to HH tissues, reflecting a colony-wide systemic effect and provides insight into the metabolic immune response of WS-infected Indo-Pacific corals. This project was funded in part by Earthwatch Institute and Mitsubishi Corporation. Scopus

Coral restoration is widely used around the world to address dramatic declines in coral cover; however, very few studies have looked specifically at the temporal response of fish assemblages (i.e. abundance and diversity) to coral restoration. Several critical reef functions and processes are driven by fishes, thereby making their recovery and responses around restoration structures key indicators of success. This study evaluates fish abundance and community composition on restoration plots following 8–12 years of restoration activity, in four locations (two Caribbean and two Indo‐Pacific). Responses were very complex with region‐, site‐, and body size‐specific patterns. Overall, fish abundance only increased in Indo‐Pacific sites where damselfish responded positively to increased coral cover and topographic complexity. Restoration effects on other fish families and particularly on larger bodied reef fish were negative or neutral at all locations. If restoration initiatives are going to substantively improve the condition and recovery of degraded reef fish communities, restoration efforts need to be planned, designed, and monitored based on fish‐specific habitat requirements and locally specific community dynamics.

In the face of unprecedented rates of environmental alterations, the necessity to predict the capacity of corals to respond adaptively in a complex ecological system is becoming increasingly urgent. Recent findings that bleaching-resistant Acropora millepora coral populations have high frequencies of specific alleles provide an opportunity to use spatial mapping of alleles to identify resistant populations. In this study, a Bayesian belief network (BBN) model was developed to predict the spatial distribution of allele frequencies for a specific locus associated with bleaching resistance in response to acute eutrophication during the summertime in A. millepora in the Palm Islands (Great Barrier Reef, Australia). The BBN model enabled the putative responses of populations investigated to be extrapolated to other ‘equivalent’ populations that were previously not surveyed due to constraints of time, cost and logistics. A combination of long-term environmental monitoring data, allele frequency data, expert input and statistical evaluation was used to build the model, with the goal of refining prior beliefs and examining dependencies among environmental variables. The Bayesian simulation approach demonstrates that synergism between highly fluctuating temperatures and high nitrate concentrations may be the primary driver of selection for this locus. Consistently, spatial mapping of predicted allele frequencies reveals the tolerance allele is most likely to be concentrated in populations near the mouths of the Burdekin and Fitzroy Rivers. Corals from these river mouths are good candidates for assisted gene flow initiatives and also to restore reefs that are likely to be affected by eutrophication and ocean warming in the future. This approach opens up new opportunities for more efficient and effective coral reef management and conservation through direct intervention to ensure coral populations have the genetic diversity needed to optimise adaptation to rapid environmental change.

Adult organisms may “prime” their offspring for environmental change through a number of genetic and non-genetic mechanisms, termed parental effects. Some coral species can alter their thermal tolerance by shuffling the proportions of Symbiodinium types within their endosymbiotic communities, but it is unclear if this plasticity can be transferred to offspring in corals that have maternal symbiont transmission. We evaluated symbiont community composition in tagged colonies of Montipora digitata from Orpheus Island, Australia, over two successive annual spawning seasons, the second of which overlapped with the 2016 mass coral bleaching event on the Great Barrier Reef. We applied amplicon sequencing of the ITS2 locus to samples of four families (parent colonies and 10-12 eggs per family) to characterize their potential for symbiont shuffling and to determine if shuffled abundances were preserved in gametes. Symbiont cell densities and photochemical efficiencies of the symbionts’ photosystem II differed significantly among adults in 2016, suggesting differential responses to increased temperatures. Although abundances of the dominant symbiont haplotype, a representative of clade C15, did not differ among families or over time, low-abundance (“background”) ITS2 types differed more among years (2015 vs. 2016) than between life stages (parent vs. offspring). Results indicate that background symbiont shuffling can occur in a canonically ‘stable’ symbiosis, and that such plastic changes to the symbiont community are heritable. To our knowledge, this is the first evidence that shuffled Symbiodinium communities can be inherited by early life-history stages and supports the hypothesis that plastic changes in microbial communities may serve as a mechanism of rapid coral acclimation to changing environmental conditions.

While links between heat stress and coral bleaching are clear and predictive tools for bleaching risk are well advanced, links between heat stress and outbreaks of coral diseases are less well understood. In this study, the effects of accumulated heat stress on tagged colonies of tabular Acropora were monitored over the 2017 austral summer at Beaver Reef, which is located in the central region of the Great Barrier Reef. The initial surveys in midsummer (21 February) coincided with an accumulated heat stress metric of 4.5 °C-weeks, and documented high coral cover (74.0 ± 6.5%), extensive bleaching (71% of all corals displayed bleaching signs) and an outbreak of white syndromes (WSs) (31% of tabular acroporid corals displayed white syndrome signs). Repeat assessments of the impacts of bleaching and disease on these corals provided real-time information to reef managers by tracking the unfolding reef health incident on 100 colonies of Acropora hyacinthus (Dana, 1846), tagged in mid-March and surveyed intermittently until late October 2017. Heat stress increased rapidly on Beaver Reef, peaking at 8.3 °C-weeks on 31 March, which coincided with the highest prevalence of WS recorded in the study. Of the 85 tagged colonies surviving on 31 March, 41 (~ 48%) displayed WS signs, indicating a link between heat stress and WS. When re-surveyed at eight months (24 October), 68 of 100 tagged colonies had suffered whole-colony mortality and only four colonies had not displayed signs of bleaching or disease (WS) in any of our surveys. Overall, coral cover on Beaver Reef was reduced by more than half to 31.0 ± 11.2%. Significant tissue loss due to severe bleaching was observed with up to 20 times greater tissue loss on severely bleached colonies (i.e. categorised as > 50% bleached) compared to mildly/moderately bleached colonies (

Fatty acids (FA) play a vital role in coral physiology, metabolism and stress resistance. Optimal health requires a balance of fatty acids, and more specifically essential polyunsaturated fatty acids (PUFA), for efficient biochemical and physiological functioning. Therefore, it is necessary to fully assess and evaluate the viability of FA as biomarkers for monitoring the health of coral populations. This study explores seasonal and spatial variation in the abundance of 17 FA in the coral Acropora tenuis, along two water quality gradients on the central Great Barrier Reef. Ratios of key FA varied similarly along the two water quality gradients and were highest in corals from comparatively good water quality conditions. Strong differences in PUFA composition were found between wet and dry seasons, with high percentage n-3 PUFA defining the dry seasons (June 2013 and October 2013) and high percentage n-6 PUFA defining the wet seasons (February 2013 and 2014). Saturated FA and monounsaturated FA concentrations varied with season, positively correlated with Symbiodinium density, and had highest concentrations in corals exposed to relatively poor water quality. Overall, results demonstrate that essential FA and their derived ratios support FA as a potential indicator of coral holobiont health; however, strong seasonal variation may negate FA and their derived ratios as water quality indicators.

To investigate plasticity in biochemical and physiological health attributes of corals, identical colony fragments of the coral Acropora tenuis, from two inshore populations, were exposed to native and novel environmental regimes. Variation in global gene expression (GE) and lipid and fatty acid (FA) composition of surviving colony fragments were quantified after four months. Major FA classes, with the exception of short-chain (C18) polyunsaturated fatty acids (PUFA), decreased in concentration when coral fragments were exposed to lower water quality regardless of their source population. In contrast, a strong effect of source population was detected in the GE profiles of all coral fragments and was enriched with genes associated with translation, ribosome biogenesis and ribosome cellular components. One cluster of co-expressed genes positively correlated with multiple individual FA and included genes involved in developmental processes and cellular pathways. This study demonstrates the strong influence of a source effect defining gene expression relating to basic biological functions, including biosynthetic processing, translation and ribosome biogenesis. However, there is plasticity in FA composition and specific genes relating to elevated health and immunity, which can respond to changes in environmental conditions. These findings suggest hope for future corals, if we can reduce anthropogenic water quality stressors.

Coral restoration is increasingly used globally as a management tool to minimize accelerating coral reef degradation resulting from climate change. Yet, the science of coral restoration is still very focused on ecological and technical considerations, impeding the understanding of how coral restoration can be used to improve reef resilience in the context of socio-ecological systems. Here, we visited four well-established coral restoration projects in different regions of the world (Thailand, Maldives, Florida Keys, and US Virgin Islands), and conducted key-informant interviews to characterize local stakeholder's perceptions of the key benefits and limitations associated with restoration efforts. Our results reveal that perceptions around coral reef restoration encompass far more than ecological considerations, and include all four dimensions of sustainability: ecological, social, economic, and governance, suggesting that effective coral restoration should be guided by the principles of sustainability science. Socio-cultural benefits were the most frequently mentioned (72.4% of all respondents), while technical problems were the most common theme for limitations of coral restoration efforts (58.3% of the respondents). Participants also revealed some key points likely to improve the outcomes of coral restoration efforts such as the need to better embrace socio-cultural dimensions in goal setting, evaluate ecological outcomes more broadly, secure long-term funding and improve management and logistics of day to day practices. While we identify several important limitations of coral reef restoration, particularly around amateur workforces and limited involvement of local communities, our results suggest that coral restoration can be used as a powerful conservation education tool to provide hope, enhance agency, promote stewardship and strengthen coral reef conservation strategies.

Research into causative agents underlying coral disease have focused primarily on bacteria, whereas potential roles of viruses have been largely unaddressed. Bacteriophages may contribute to diseases through the lysogenic introduction of virulence genes into bacteria, or prevent diseases through lysis of bacterial pathogens. To identify candidate phages that may influence the pathogenicity of black band disease (BBD), communities of bacteria (16S rRNA) and T4-bacteriophages (gp23) were simultaneously profiled with amplicon sequencing among BBD-lesions and healthy-coral-tissue of Montipora hispida, as well as seawater (study site: the central Great Barrier Reef). Bacterial community compositions were distinct among BBD-lesions, healthy coral tissue and seawater samples, as observed in previous studies. Surprisingly, however, viral beta diversities based on both operational taxonomic unit (OTU)-compositions and overall viral community compositions of assigned taxa did not differ statistically between the BBD-lesions and healthy coral tissue. Nonetheless, relative abundances of three bacteriophage OTUs, affiliated to Cyanophage PRSM6 and Prochlorococcus phages P-SSM2, were significantly higher in BBD-lesions than in healthy tissue. These OTUs associated with BBD samples suggest the presence of bacteriophages that infect members of the cyanobacteria-dominated BBD community, and thus have potential roles in BBD pathogenicity.

Scleractinian corals’ microbial symbionts influence host health, yet how coral microbiomes assembled over evolution is not well understood. We survey bacterial and archaeal communities in phylogenetically diverse Australian corals representing more than 425 million years of diversification. We show that coral microbiomes are anatomically compartmentalized in both modern microbial ecology and evolutionary assembly. Coral mucus, tissue, and skeleton microbiomes differ in microbial community composition, richness, and response to host vs. environmental drivers. We also find evidence of coral-microbe phylosymbiosis, in which coral microbiome composition and richness reflect coral phylogeny. Surprisingly, the coral skeleton represents the most biodiverse coral microbiome, and also shows the strongest evidence of phylosymbiosis. Interactions between bacterial and coral phylogeny significantly influence the abundance of four groups of bacteria–including Endozoicomonas-like bacteria, which divide into host-generalist and host-specific subclades. Together these results trace microbial symbiosis across anatomy during the evolution of a basal animal lineage., Associations between corals and symbiotic microorganisms could be driven by the environment or shared evolutionary history. Here, the authors examine relationships between coral phylogenies and associated microbiomes, finding evidence of phylosymbiosis in microbes from coral skeleton and tissue, but not mucus.

Projected increases in sea surface temperatures will exceed corals' ability to withstand heat stress within this century. Experimental evolution of cultured symbionts (Symbiodiniaceae) at high temperatures followed by reintroduction into corals can enhance coral heat tolerance. Several studies have selected for enhanced tolerance in Cladocopium goreaui (C1) over multiple time scales and then compared the performance of coral juveniles infected with the heat-tolerant C1 selected strain (SS) to the performance of juveniles infected with the C1 wild type (WT). To derive lessons about host benefits when symbionts are experimentally selected, here we compare the performance of SS- and WT-juveniles after 21 cell generations of heat selection versus longer periods (73–131) in recently published experiments. After 21 generations, we found rapid improvement in heat tolerance of SS through an overall shift in the mean tolerance to temperature. This did not translate to improved growth and survivorship of the coral. Specifically, survival did not differ significantly between juveniles of Acropora tenuis hosting WT versus SS at any temperature. Juveniles infected with WT exhibited greater skeletal growth than those infected with SS at 27 and 31°C but not at 32.5°C. SS-juvenile symbiont cell densities increased significantly at 27°C relative to SS-juveniles in the 31 and 32.5°C. Photosynthetic efficiencies in SS-juveniles were higher compared to WT-juveniles at 31°C, equal at 27°C, and lower at 32.5°C. These results suggest that selection over longer generation (>130) times will be needed to confer host benefits and will be dependent on the stability of this association being maintained in nature.

The discovery of multi-species synchronous spawning of scleractinian corals on the Great Barrier Reef in the 1980s stimulated an extraordinary effort to document spawning times in other parts of the globe. Unfortunately, most of these data remain unpublished which limits our understanding of regional and global reproductive patterns. The Coral Spawning Database (CSD) collates much of these disparate data into a single place. The CSD includes 6178 observations (3085 of which were unpublished) of the time or day of spawning for over 300 scleractinian species in 61 genera from 101 sites in the Indo-Pacific. The goal of the CSD is to provide open access to coral spawning data to accelerate our understanding of coral reproductive biology and to provide a baseline against which to evaluate any future changes in reproductive phenology., info:eu-repo/semantics/published

Diseases of tropical reef organisms is an intensive area of study, but despite significant advances in methodology and the global knowledge base, identifying the proximate causes of disease outbreaks remains difficult. The dynamics of infectious wildlife diseases are known to be influenced by shifting interactions among the host, pathogen, and other members of the microbiome, and a collective body of work clearly demonstrates that this is also the case for the main foundation species on reefs, corals. Yet, among wildlife, outbreaks of coral diseases stand out as being driven largely by a changing environment. These outbreaks contributed not only to significant losses of coral species but also to whole ecosystem regime shifts. Here we suggest that to better decipher the disease dynamics of corals, we must integrate more holistic and modern paradigms that consider multiple and variable interactions among the three major players in epizootics: the host, its associated microbiome, and the environment. In this perspective, we discuss how expanding the pathogen component of the classic host-pathogen-environment disease triad to incorporate shifts in the microbiome leading to dysbiosis provides a better model for understanding coral disease dynamics. We outline and discuss issues arising when evaluating each component of this trio and make suggestions for bridging gaps between them. We further suggest that to best tackle these challenges, researchers must adjust standard paradigms, like the classic one pathogen-one disease model, that, to date, have been ineffectual at uncovering many of the emergent properties of coral reef disease dynamics. Lastly, we make recommendations for ways forward in the fields of marine disease ecology and the future of coral reef conservation and restoration given these observations.

Coral restoration is rapidly becoming a mainstream strategic reef management response to address dramatic declines in coral cover worldwide. Restoration success can be defined as enhanced reef functions leading to improved ecosystem services, with multiple benefits at socio-ecological scales. However, there is often a mismatch between the objectives of coral restoration programs and the metrics used to assess their effectiveness. In particular, the scales of ecological benefits currently assessed are typically limited in both time and space, often being limited to short-term monitoring of the growth and survival of transplanted corals. In this paper, we explore reef-scale responses of coral assemblages to restoration practices applied in four well-established coral restoration programs. We found that hard coral cover and structural complexity were consistently greater at restored compared to unrestored (degraded) sites. However, patterns in coral diversity, coral recruitment, and coral health among restored, unrestored, and reference sites varied across locations, highlighting differences in methodologies among restoration programs. Altogether, differences in program objectives, methodologies, and the state of nearby coral communities were key drivers of variability in the responses of coral assemblages to restoration. The framework presented here provides guidance to improve qualitative and quantitative assessments of coral restoration efforts and can be applied to further understanding of the role of restoration within resilience-based reef management.

Increases in the frequency of perturbations that drive coral community structure, such as severe thermal anomalies and high intensity storms, highlight the need to understand how coral communities recover following multiple disturbances. We describe the dynamics of cover and assemblage composition of corals on exposed inshore reefs in the Palm Islands, central Great Barrier Reef, over 19 years encapsulating major disturbance events such as the severe bleaching event in 1998 and Cyclone Yasi in 2011, along with other minor storm and heat stress events. Over this time, 47.8% of hard coral cover was lost, with a concomitant shift in coral assemblage composition due to taxon-specific rates of mortality during the disturbances, and asymmetric recovery in the aftermath thereof. High recruitment rates of some broadcast-spawning corals, particularly corymbose Acropora spp., even in the absence of adult colonies, indicate that a strong external larval supply replenished the stocks. Conversely, the time required for recovery of slow-growing coral morphologies and life histories was longer than the recurrence times of major disturbances. With interludes between bleaching and cyclones predicted to decrease, the probability of another severe disturbance event before coral cover and assemblage composition approximates historical levels suggests that reefs will continue to erode.

This manuscript was improved by constructive comments from the Responsible Editor and 2 anonymous reviewers. This study was supported by the Endeavour International and JCU Postgraduate Research Scholarship to K.M.Q., the Australian Research Council grant, through the ARC Centre of Excellence for Coral Reef Studies, to B.L.W., and by funding from the Australian Institute of Marine Science to L.K.B.

Black band disease (BBD) is a virulent coral disease, and although its microbiology has been studied extensively, the aetiology of BBD remains poorly understood. Here we used aquaria and field experiments to determine if feeding on BBD lesions by corallivorous fishes influences disease progression rates. Although selective predation on lesions was observed in both controlled laboratory experiments and field-based observations, we found no evidence that fish feeding either reduced or enhanced progression rates of BBD. Variability in disease progression rates in the field was explained by variation among coral colonies (24.46%) and among sample days (37.77%) rather than by predation treatment (

Global increases in coral disease prevalence have been linked to ocean warming through changes in coral-associated bacterial communities, pathogen virulence and immune system function. However, the interactive effects of temperature and pathogens on the coral holobiont are poorly understood. Here, we assessed three compartments of the holobiont (host, Symbiodinium and bacterial community) of the coral Montipora aequituberculata challenged with the pathogen Vibrio coralliilyticus and the commensal bacterium Oceanospirillales sp. under ambient (27°C) and elevated (29.5 and 32°C) seawater temperatures. Few visual signs of bleaching and disease development were apparent in any of the treatments, but responses were detected in the holobiont compartments. V. coralliilyticus acted synergistically and negatively impacted the photochemical efficiency of Symbiodinium at 32°C, while Oceanospirillales had no significant effect on photosynthetic efficiency. The coral, however, exhibited a minor response to the bacterial challenges, with the response towards V. coralliilyticus being significantly more pronounced, and involving the prophenoloxidase-activating system and multiple immune system-related genes. Elevated seawater temperatures did not induce shifts in the coral-associated bacterial community, but caused significant gene expression modulation in both Symbiodinium and the coral host. While Symbiodinium exhibited an antiviral response and upregulated stress response genes, M. aequituberculata showed regulation of genes involved in stress and innate immune response processes, including immune and cytokine receptor signalling, the complement system, immune cell activation and phagocytosis, as well as molecular chaperones. These observations show that M. aequituberculata is capable of maintaining a stable bacterial community under elevated seawater temperatures and thereby contributes to preventing disease development.

Coral reef restoration initiatives are burgeoning in response to the need for novel management strategies to address dramatic global declines in coral cover. However, coral restoration programs typically lack rigor and critical evaluation of their effectiveness. A review of 83 peer-reviewed papers that used coral transplantation for reef restoration reveals that growth and survival of coral fragments were the most widely used indicators of restoration success, with 88% of studies using these two indicators either solely (55%) or in combination with a limited number of other ecological factors (33%). In 53% of studies, reef condition was monitored for 1 year or less, while only 5% of reefs were monitored for more than 5 years post-transplantation. These results highlight that coral reef restoration science has focused primarily on short-term experiments to evaluate the feasibility of techniques for ecological restoration and the initial establishment phase post-transplantation, rather than on longer-term outcomes for coral reef communities. Here, we outline 10 socioecological indicators that comprehensively evaluate the effectiveness of coral reef restoration across the four pillars of sustainability (i.e. environmental, sociocultural, governance, and economic contributions to sustainable communities). We recommend that evaluations of the effectiveness of coral restoration programs integrate ecological indicators with sociocultural, economic, and governance considerations. Assessing the efficacy of coral restoration as a tool to support reef resilience will help to guide future efforts and ensure the sustainable maintenance of reef ecosystem goods and services.

This study explores how plasticity in biochemical attributes, used as indicators of health and condition, enables the coral Acropora tenuis to respond to differing water quality regimes in inshore regions of the Great Barrier Reef. Health attributes were monitored along a strong and weak water quality gradient, each with three reefs at increasing distances from a major river source. Attributes differed significantly only along the strong gradient; corals grew fastest, had the least dense skeletons, highest symbiont densities and highest lipid concentrations closest to the river mouth, where water quality was poorest. High nutrient and particulate loads were only detrimental to skeletal density, which decreased as linear extension increased, highlighting a trade-off. Our study underscores the importance of assessing multiple health attributes in coral reef monitoring. For example, autotrophic indices are poor indicators of coral health and condition, but improve when combined with attributes like lipid content and biomass.

Bacterial diversity associated with corals has been studied extensively, however, localization of bacterial associations within the holobiont is still poorly resolved. Here we provide novel insight into the localization of coral-associated microbial aggregates (CAMAs) within tissues of the coral Acropora hyacinthus. In total, 318 and 308 CAMAs were characterized via histological and fluorescent in situ hybridization (FISH) approaches respectively, and shown to be distributed extensively throughout coral tissues collected from five sites in Japan and Australia. The densities of CAMAs within the tissues were negatively correlated with the distance from the coastline (i.e. lowest densities at offshore sites). CAMAs were randomly distributed across the six coral tissue regions investigated. Within each CAMA, bacterial cells had similar morphological characteristics, but bacterial morphologies varied among CAMAs, with at least five distinct types identified. Identifying the location of microorganisms associated with the coral host is a prerequisite for understanding their contributions to fitness. Localization of tissue-specific communities housed within CAMAs is particularly important, as these communities are potentially important contributors to vital metabolic functions of the holobiont.

Interactions between corals and their associated microbial communities (Symbiodiniaceae and prokaryotes) are key to understanding corals' potential for and rate of acclimatory and adaptive responses. However, the establishment of microalgal and bacterial communities is poorly understood during coral ontogeny in the wild. We examined the establishment and co‐occurrence between multiple microbial communities using 16S rRNA (bacterial) and ITS2 rDNA (Symbiodiniaceae) gene amplicon sequencing in juveniles of the common coral, Acropora tenuis, across the first year of development. Symbiodiniaceae communities in juveniles were dominated by Durusdinium trenchii and glynnii (D1 and D1a), with lower abundances of Cladocopium (C1, C1d, C50, and Cspc). Bacterial communities were more diverse and dominated by taxa within Proteobacteria, Cyanobacteria, and Planctomycetes. Both communities were characterized by significant changes in relative abundance and diversity of taxa throughout the year. D1, D1a, and C1 were significantly correlated with multiple bacterial taxa, including Alpha‐, Deltra‐, and Gammaproteobacteria, Planctomycetacia, Oxyphotobacteria, Phycisphaerae, and Rhizobiales. Specifically, D1a tended to associate with Oxyphotobacteria and D1 with Alphaproteobacteria, although these associations may represent correlational and not causal relationships. Bioenergetic modeling combined with physiological measurements of coral juveniles (surface area and Symbiodiniaceae cell densities) identified key periods of carbon limitation and nitrogen assimilation, potentially coinciding with shifts in microbial community composition. These results demonstrate that Symbiodiniaceae and bacterial communities are dynamic throughout the first year of ontology and may vary in tandem, with important fitness effects on host juveniles., We characterized the establishment and maintenance of bacterial and Symbiodiniaceae communities in the coral Acropora tenuis across the first year of juvenile ontogeny, identifying potentially key co‐occurrence patterns using network modeling. Bioenergetic modeling combined with physiological measurements of coral juveniles (surface area and Symbiodiniaceae cell densities) identified periods of carbon limitation and nitrogen assimilation, potentially coinciding with shifts in microbial community composition. These dynamic communities vary in tandem with important fitness effects on host juvenile corals.

Disease is an emerging threat to coral reef ecosystems worldwide, highlighting the need to understand how environmental conditions interact with coral immune function and associated microbial communities to affect holobiont health. Increased coral disease incidence on reefs adjacent to permanently moored platforms on Australia's Great Barrier Reef provided a unique case study to investigate environment–host–microbe interactions in situ . Here, we evaluate coral-associated bacterial community (16S rRNA amplicon sequencing), immune function (protein-based prophenoloxidase-activating system), and water quality parameters before, during and after a disease event. Over the course of the study, 31% of tagged colonies adjacent to platforms developed signs of white syndrome (WS), while all control colonies on a platform-free reef remained visually healthy. Corals adjacent to platforms experienced significant reductions in coral immune function. Additionally, the corals at platform sites that remained visually healthy throughout the study had reduced bacterial diversity compared to healthy colonies at the platform-free site. Interestingly, prior to the observation of macroscopic disease, corals that would develop WS had reduced bacterial diversity and significantly greater community heterogeneity between colonies compared to healthy corals at the same location. These results suggest that activities associated with offshore marine infrastructure impacts coral immunocompetence and associated bacterial community, which affects the susceptibility of corals to disease.

Ocean acidification (OA) as a result of increased anthropogenic CO2 input into the atmosphere carries consequences for all ocean life. Low pH can cause a shift in coral-associated microbial communities of pCO2-sensitive corals, however, it remains unknown whether the microbial community is also influenced in corals known to be more tolerant to high pCO2/low pH. This study profiles the bacterial communities associated with the tissues of the pCO2-tolerant coral, massive Porites spp., from two natural CO2 seep sites in Papua New Guinea. Amplicon sequencing of the hypervariable V3-V4 regions of the 16S rRNA gene revealed that microbial communities remained stable across CO2 seep sites (pH = 7.44–7.85) and adjacent control sites (ambient pH = 8.0–8.1). Microbial communities were more significantly influenced by reef location than pH, with the relative abundance of dominant microbial taxa differing between reefs. These results directly contrast with previous findings that increased CO2 has a strong effect on structuring microbial communities. The stable structure of microbial communities associated with the tissues of massive Porites spp. under high pCO2/low pH conditions confirms a high degree of tolerance by the whole Porites holobiont to OA, and suggest that pH tolerant corals such as Porites may dominate reef assemblages in an increasingly acidic ocean.

Predicted increases in sea-surface temperatures due to climate change are likely to alter the physiology of marine organisms and ultimately influence the distribution and abundance of their populations. The consequences of increased temperatures for marine species, including decreased survival and altered rates of development, growth and settlement, are well known and often attributed to imbalances between energy supply and demand. To test this hypothesis, we calibrated the effect of temperature on rates of survival and lipid depletion for larvae of the common stony coral Acropora tenuis over a 7 °C temperature range. Temperature had a pronounced, linearly increasing effect on larval mortality, with a sixfold decrease in median survival time. Contrary to expectation, however, temperature had a quasi-parabolic effect on lipid use; rates declined as temperatures either increased above or decreased below the ambient temperature at the time of spawning. This contrasts with previous work suggesting that increased energy depletion is the cause of larval mortality at higher temperatures. Our results highlight the sensitivity of coral larvae to temperature and have implications for dispersal potential because fewer larvae will survive to disperse. Such projected declines in connectivity among coral populations are likely to undermine reef resilience.

Despite the ecological significance of the relationship between reef-building corals and intracellular photosynthetic dinoflagellates of the genus Symbiodinium, very little is known about the molecular mechanisms involved in its establishment. Indeed, microarray-based analyses point to the conclusion that host gene expression is largely or completely unresponsive during the establishment of symbiosis with a competent strain of Symbiodinium. In this study, the use of Illumina RNA-Seq technology allowed detection of a transient period of differential expression involving a small number of genes (1073 transcripts

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).

Emerging infectious diseases are contributing to global declines in coral reef ecosystems, highlighting a growing need for aetiological knowledge to develop effective management strategies. In this review, we focus on black band disease (BBD), one of the most virulent diseases and the only polymicrobial disease so far known to affect corals. A multipartite microbial consortium dominated by Cyanobacteria, but also including sulfur-cycling bacteria, other bacterial groups and members of the Archaea and Eukarya, forms a sulfide-rich anaerobic mat that migrates across the surface of coral colonies, killing the underlying tissues. The polymicrobial nature of the disease challenges classic aetiological approaches to unravelling disease causation. Here, we synthesize current knowledge on the range of pathogens forming the microbial consortium with recent studies on the transmission, biogeochemistry and environmental drivers of BBD to develop a conceptual model of BBD pathogenesis. The model illustrates how the development of BBD virulence factors is linked to a cascade of microbial community shifts and associated functional roles that progressively develop the microbial consortium from comparatively benign cyanobacterial patches to virulent BBD lesions. This review showcases how an approach that integrates multiple key aspects of the disease provides insights essential to elucidating the aetiology of BBD.

Diazotrophic bacteria are instrumental in generating biologically usable forms of nitrogen by converting abundant dinitrogen gas (N-2) into available forms, such as ammonium. Although nitrogen is crucial for coral growth, direct observation of associations between diazotrophs and corals has previously been elusive. We applied fluorescence in situ hybridization (FISH) and nanoscale secondary ion mass spectrometry to observe the uptake of N-15-enriched diazotrophic Vibrio sp. isolated from Acropora millepora into conspecific coral larvae. Incorporation of Vibrio sp. cells was observed in coral larvae after 4-h incubation with enriched bacteria. Uptake was restricted to the aboral epidermis of larvae, where Vibrio cells clustered in elongated aggregations. Other bacterial associates were also observed in epidermal areas in FISH analyses. Although the fate and role of these bacteria requires additional investigation, this study describes a powerful approach to further explore cell associations and nutritional pathways in the early life stages of the coral holobiont.

Aquaculture of coral offers an alternative to wild harvest for the ornamental trade and shows considerable promise for restoring reefs and preserving biodiversity. Here, we compare advantages and disadvantages of asexually derived fragments versus sexually derived propagules and in situ versus ex situ nursery phases for the ornamental trade and reef restoration. Asexual propagules, sourced from a donor coral colony that is cut into smaller parts and attached to artificial substrate, are most commonly used. The most suitable corals are typically branching species, although fragments from species with other growth forms can be successful, albeit slower growing. Sexually derived propagules are collected from the wild or from colonies in aquaria during spawning, with an artificial substrate provided for settlement. The timing of spawning is known for many broadcast spawning corals, but opportunities for collection of gametes are generally limited to only once or a few times per year. Brooding species with multiple periods of larval release provide better options for culture of sexually derived propagules. Propagation techniques have developed considerably over the past 20 years, yielding faster growth rates, reduced mortality and reduced detachment from substrates. Simple and cost–effective propagation techniques can be used to restore denuded reefs, preserve endangered species, provide live corals to the international ornamental trade, enable livelihood diversification for coastal communities and provide experimental materials for marine research. This review provides a comprehensive synthesis of recent developments in aquaculture propagation techniques for the purpose of ornamental trade and coral reef restoration, including asexual and sexual propagation, nursery and transplantation stages.

Ocean acidification (OA) as a result of increased anthropogenic CO2 input into the atmosphere carries consequences for all ocean life. Low pH can cause a shift in coral-associated microbial communities of pCO2-sensitive corals, however, it remains unknown whether the microbial community is also influenced in corals known to be more tolerant to high pCO2/low pH. This study profiles the bacterial communities associated with the tissues of the pCO2-tolerant coral, massive Porites spp., from two natural CO2 seep sites in Papua New Guinea. Amplicon sequencing of the hypervariable V3-V4 regions of the 16S rRNA gene revealed that microbial communities remained stable across CO2 seep sites (pH = 7.44–7.85) and adjacent control sites (ambient pH = 8.0–8.1). Microbial communities were more significantly influenced by reef location than pH, with the relative abundance of dominant microbial taxa differing between reefs. These results directly contrast with previous findings that increased CO2 has a strong effect on structuring microbial communities. The stable structure of microbial communities associated with the tissues of massive Porites spp. under high pCO2/low pH conditions confirms a high degree of tolerance by the whole Porites holobiont to OA, and suggest that pH tolerant corals such as Porites may dominate reef assemblages in an increasingly acidic ocean.

The majority of corals acquire their photo-endosymbiont Symbiodinium from environmental sources anew each generation. Despite the critical role that environmental availability of Symbiodinium plays in the potential for corals to acclimate and adapt to changing environments, little is known about the diversity of free-living Symbiodinium communities and how variation in these communities influences uptake and in hospite communities in juvenile corals. Here we characterize Symbiodinium community diversity in sediment samples collected from eight reefs representing latitudinal and cross-shelf variation in water quality and temperature regimes. Sediment-associated Symbiodinium communities were then compared to in hospite communities acquired by A. tenuis and A. millepora juveniles following 11 – 145 days of experimental exposure to sediments from each of the reefs. Communities associated with juveniles and sediments differed substantially, with sediments harbouring four times more unique OTUs than juveniles (1125 OTUs vs. 271). Moreover, only 10.6% of these OTUs were shared between juveniles and sediments, indicating selective uptake by acroporid juveniles. The diversity and abundance of Symbiodinium types differed among sediment samples from different temperature and water quality environments. Symbiodinium communities acquired by juveniles also differed among the sediment treatments, despite juveniles having similar parentage. Moreover, Symbiodinium communities displayed different rates of infection, mortality, and photochemical efficiencies, important traits for coral fitness. This study demonstrates that the biogeography of free-living Symbiodinium types found within sediment reservoirs follows patterns along latitudinal and water quality environmental gradients on the Great Barrier Reef. We also demonstrate a bipartite strategy for Symbiodinium uptake by juvenile corals of two horizontally-transmitting acroporid species, whereby uptake is selective within the constraints of environmental availability.

Infectious diseases not regulated by host density, such as vector-borne diseases, have the potential to drive population declines and extinctions. Here we test the vector potential of the snail Drupella sp. and butterflyfish Chaetodon plebeius for two coral diseases, black band (BBD) and brown band (BrB) disease. Drupella transmitted BrB to healthy corals in 40% of cases immediately following feeding on infected corals, and even in 12% of cases 12 and 24 hours following feeding. However, Drupella was unable to transmit BBD in either transmission treatment. In a field experiment testing the vector potential of naturally-occurring fish assemblages, equivalent numbers of caged and uncaged coral fragments became infected with either BrB, BBD or skeletal eroding band, indicating that corallivorous fish were unlikely to have caused transmission. In aquaria, C. plebeius did not transmit either BBD or BrB, even following extended feeding on both infected and healthy nubbins. A literature review confirmed only four known coral disease vectors, all invertebrates, corroborating our conclusion that polyp-feeding fishes are unlikely to be vectors of coral diseases. This potentially because polyp-feeding fishes produce shallow lesions, not allowing pathogens to invade coral tissues. In contrast, corallivorous invertebrates that create deeper feeding scars increase pathogens transmission.

Parks and protected areas have been instrumental in reducing anthropogenic sources of damage in terrestrial and aquatic environments. Pathogen invasion often succeeds physical wounding and injury, yet links between the reduction of damage and the moderation of disease have not been assessed. Here, we examine the utility of no-take marine reserves as tools for mitigating diseases that affect reef-building corals. We found that sites located within reserves had fourfold reductions in coral disease prevalence compared to non-reserve sites (80 466 corals surveyed). Of 31 explanatory variables assessed, coral damage and the abundance of derelict fishing line best explained differences in disease assemblages between reserves and non-reserves. Unexpectedly, we recorded significantly higher levels of disease, coral damage, and derelict fishing line in non-reserves with fishing gear restrictions than in those without gear restrictions. Fishers targeting stocks perceived to be less depleted, coupled with enhanced site access from immediately adjacent boat moorings, may explain these unexpected patterns. Significant correlations between the distance from mooring sites and prevalence values for a ciliate disease known to infest wounded tissue (r = −0.65), coral damage (r = −0.64), and the abundance of derelict fishing line (r = −0.85) corroborate this interpretation. This is the first study to link disease with recreational use intensity in a park, emphasizing the need to evaluate the placement of closures and their direct relationship to ecosystem health. Since corals are modular, ecological processes that govern reproductive and competitive fitness are frequently related to colony surface area therefore, even low levels of cumulative tissue loss from progressing diseases pose significant threats to reef coral persistence. Disease mitigation through reductions in physical injury in areas where human activities are concentrated is another mechanism by which protected areas may improve ecosystem resilience in a changing climate.

Mounting evidence of cryptic species in a wide range of taxa highlights the need for careful analyses of population genetic data sets to unravel within-species diversity from potential interspecies relationships. Here, we use microsatellite loci and hierarchical clustering analysis to investigate cryptic diversity in sympatric and allopatric (separated by 450 km) populations of the widespread coral Seriatopora hystrix on the Great Barrier Reef. Structure analyses delimited unique genetic clusters that were confirmed by phylogenetic and extensive population-level analyses. Each of four sympatric yet distinct genetic clusters detected within S. hystrix demonstrated greater genetic cohesion across regional scales than between genetic clusters within regions (10 km). Moreover, the magnitude of genetic differentiation between different clusters (0.620 G"ST ) was similar to the difference between S. hystrix clusters and the congener S. caliendrum (mean G"ST 0.720). Multiple lines of evidence, including differences in habitat specificity, mitochondrial identity, Symbiodinium associations and morphology, corroborate the nuclear genetic evidence that these distinct clusters constitute different species. Hierarchical clustering analysis combined with more traditional population genetic methods provides a powerful approach for delimiting species and should be regularly applied to ensure that ecological and evolutionary patterns interpreted for single species are not confounded by the presence of cryptic species.

Recurrent disturbances on coral reefs that cause injuries, like predation and storm damage, and elevated seawater temperatures reduce coral fitness and immunocompetence. An effective immune response is essential to prevent disease and enhance colony survival. To evaluate how elevated seawater temperatures affect the coral immune response following injury, fragments of Acropora aspera were exposed to ambient (27–29°C) or elevated (32–33.5°C) seawater temperatures for 8 days and subsequently experimentally injured. Expression patterns for 15 immune genes 24 h post-injury revealed that most genes involved in the Toll-like receptor pathway were unaffected by elevated seawater temperatures. Exceptions to this pattern were cFos and cJun, which were upregulated and likely played a role in repair processes, and TRAF-6 and NFκB, which were downregulated suggesting reduced immune function. Components of the complement system were upregulated (millectin, C3) or downregulated (Bf, Tx60, apextrin) in corals at high temperatures. However, corals that also sustained injury, showed normal Tx60 and apextrin expression, suggesting roles in the wounding response. Overall, basal expression levels of immune genes are sufficient to mount a response to injury in the short term, and the immune response of A. aspera following injury is not significantly affected by minor elevations in seawater temperatures.

Disease is increasingly recognized as a threat to coral reef ecosystems, particularly in the light of increasing anthropogenic disturbances that disrupt important symbiotic partnerships within the coral holobiont. White syndromes (WSs) are a prevalent group of coral diseases in the Indo-Pacific region that have been the focus of an increasing number of investigations over the past decade. Here, we summarize the current state of knowledge on WSs, advocate the use of established standardized criteria to describe disease lesions at gross and cellular levels to move the field forward, and highlight potential erroneous characterization of underlying causes that hinders ongoing progress in coral disease research. We argue for retention of the general term WSs for Indo-Pacific cases of tissue loss lacking distinguishing macroscopic signs and with unknown aetiologies, but erection of more specific names once standardized criteria are met. Recent advances in WS disease pathology, microbial ecology, physiology, ecology and environmental drivers are discussed and the need for greater application of interdisciplinary approaches is emphasized. Following recent widespread reports of WSs on coral reefs, a clear, concise perspective is needed to provide a focus for further research and avoid confusion in the study of this virulent group of diseases.

Corals wrapped in plastic Coral reefs provide vital fisheries and coastal defense, and they urgently need protection from the damaging effects of plastic waste. Lamb et al. surveyed 159 coral reefs in the Asia-Pacific region. Billions of plastic items were entangled in the reefs. The more spikey the coral species, the more likely they were to snag plastic. Disease likelihood increased 20-fold once a coral was draped in plastic. Plastic debris stresses coral through light deprivation, toxin release, and anoxia, giving pathogens a foothold for invasion. Science , this issue p. 460

The majority of corals acquire their photo-endosymbiont Symbiodinium from environmental sources anew each generation. Despite the critical role that environmental availability of Symbiodinium plays in the potential for corals to acclimate and adapt to changing environments, little is known about the diversity of free-living Symbiodinium communities and how variation in these communities influences uptake and in hospite communities in juvenile corals. Here we characterize Symbiodinium community diversity in sediment samples collected from eight reefs representing latitudinal and cross-shelf variation in water quality and temperature regimes. Sediment-associated Symbiodinium communities were then compared to in hospite communities acquired by A. tenuis and A. millepora juveniles following 11 – 145 days of experimental exposure to sediments from each of the reefs. Communities associated with juveniles and sediments differed substantially, with sediments harbouring four times more unique OTUs than juveniles (1125 OTUs vs. 271). Moreover, only 10.6% of these OTUs were shared between juveniles and sediments, indicating selective uptake by acroporid juveniles. The diversity and abundance of Symbiodinium types differed among sediment samples from different temperature and water quality environments. Symbiodinium communities acquired by juveniles also differed among the sediment treatments, despite juveniles having similar parentage. Moreover, Symbiodinium communities displayed different rates of infection, mortality, and photochemical efficiencies. This study demonstrates that the biogeography of free-living Symbiodinium types found within sediment reservoirs follows patterns along latitudinal and water quality environmental gradients on the Great Barrier Reef. We also demonstrate a bipartite strategy for Symbiodinium uptake by juvenile corals of two horizontally-transmitting acroporid species, whereby uptake is selective within the constraints of environmental availability.

Determining the extent to which Symbiodinium communities in corals are inherited versus environmentally acquired is fundamental to understanding coral resilience and to predicting coral responses to stressors like warming oceans that disrupt this critical endosymbiosis. We examined the fidelity with which Symbiodinium communities in the brooding coral Seriatopora hystrix are vertically transmitted and the extent to which communities are genetically regulated, by genotyping the symbiont communities within 60 larvae and their parents (9 maternal and 45 paternal colonies) using high-throughput sequencing of the ITS2 locus. Unexpectedly, Symbiodinium communities associated with brooded larvae were distinct from those within parent colonies, including the presence of types not detected in adults. Bayesian heritability (h2) analysis revealed that 33% of variability in larval Symbiodinium communities was genetically controlled. Results highlight flexibility in the establishment of larval symbiont communities and demonstrate that symbiont transmission is not exclusively vertical in brooding corals. Instead, we show that Symbiodinium transmission in S. hystrix involves a mixed-mode strategy, similar to many terrestrial invertebrate symbioses. Also, variation in the abundances of common Symbiodinium types among adult corals suggests that microhabitat differences influence the structure of in hospite Symbiodinium communities. Partial genetic regulation coupled with flexibility in the environmentally acquired component of Symbiodinium communities implies that corals with vertical transmission, like S. hystrix, may be more resilient to environmental change than previously thought.

Determining the extent to whichSymbiodiniumcommunities in corals are inherited versus environmentally-acquired is fundamental to understanding coral resilience and to predicting coral responses to stressors like warming oceans that disrupt this critical endosymbiosis. We examined the fidelity with whichSymbiodiniumcommunities in the brooding coralSeriatopora hystrixare vertically transmitted and the extent to which communities are genetically regulated, by genotyping 60 larvae and their parents (9 maternal and 45 paternal colonies) using high throughput sequencing of the ITS-2 locus. Unexpectedly,Symbiodiniumcommunities associated with brooded larvae were distinct from those within parent colonies, including the presence of types not detected in adults. Bayesian heritability (h2) analysis revealed that 33% of variability in larvalSymbiodiniumcommunities was genetically controlled. Results highlight flexibility in the establishment of larval communities and overturn the paradigm that symbiont transmission is exclusively vertical in brooding corals. Instead, we show thatSymbiodiniumtransmission inS. hystrixinvolves a mixed-mode strategy, similar to many terrestrial invertebrate symbioses. Also, variation in the abundances of commonSymbiodiniumtypes among adult communities suggests that microhabitat differences influence the structure ofin hospite Symbiodiniumcommunities. Partial genetic regulation coupled with flexibility in the environmentally-acquired component of larvalSymbiodiniumcommunities implies that corals with vertical transmission, likeS. hystrix,may be more resilient to environmental change than previously thought.

The dinoflagellate-coral partnership influences the coral holobiont’s tolerance to thermal stress and bleaching. However, the comparative roles of host genetic versus environmental factors in determining the composition of this symbiosis are largely unknown. Here we quantify the heritability of the initial Symbiodinium communities for two broadcast-spawning corals with different symbiont transmission modes: Acropora tenuis has environmental acquisition, whereas Montipora digitata has maternal transmission. Using high throughput sequencing of the ITS-2 region to characterize communities in parents, juveniles and eggs, we describe previously undocumented Symbiodinium diversity and dynamics in both corals. After one month of uptake in the field, Symbiodinium communities associated with A. tenuis juveniles were dominated by A3, C1, D1, A-type CCMP828, and D1a in proportional abundances conserved between experiments in two years. M. digitata eggs were predominantly characterized by C15, D1, and A3. In contrast to current paradigms, host genetic influences accounted for a surprising 29% of phenotypic variation in Symbiodinium communities in the horizontally-transmitting A. tenuis, but only 62% in the vertically-transmitting M. digitata. Our results reveal hitherto unknown flexibility in the acquisition of Symbiodinium communities and substantial heritability in both species, providing material for selection to produce partnerships that are locally adapted to changing environmental conditions.

Three to six-month-old juveniles of Acropora tenuis, A. millepora and Pocillopora acuta were experimentally co-exposed to nutrient enrichment and suspended sediments (without light attenuation or sediment deposition) for 40days. Suspended sediments reduced survivorship of A. millepora strongly, proportional to the sediment concentration, but not in A. tenuis or P. acuta juveniles. However, juvenile growth of the latter two species was reduced to less than half or to zero, respectively. Additionally, suspended sediments increased effective quantum yields of symbionts associated with A. millepora and A. tenuis, but not those associated with P. acuta. Nutrient enrichment did not significantly affect juvenile survivorship, growth or photophysiology for any of the three species, either as a sole stressor or in combination with suspended sediments. Our results indicate that exposure to suspended sediments can be energetically costly for juveniles of some coral species, implying detrimental longer-term but species-specific repercussions for populations and coral cover.

Phytoplankton-bacteria interactions drive the surface ocean sulfur cycle and local climatic processes through the production and exchange of a key compound: dimethylsulfoniopropionate (DMSP). Despite their large-scale implications, these interactions remain unquantified at the cellular-scale. Here we use secondary-ion mass spectrometry to provide the first visualization of DMSP at sub-cellular levels, tracking the fate of a stable sulfur isotope (34S) from its incorporation by microalgae as inorganic sulfate to its biosynthesis and exudation as DMSP, and finally its uptake and degradation by bacteria. Our results identify for the first time the storage locations of DMSP in microalgae, with high enrichments present in vacuoles, cytoplasm and chloroplasts. In addition, we quantify DMSP incorporation at the single-cell level, with DMSP-degrading bacteria containing seven times more 34S than the control strain. This study provides an unprecedented methodology to label, retain, and image small diffusible molecules, which can be transposable to other symbiotic systems. DOI: http://dx.doi.org/10.7554/eLife.23008.001, eLife digest Sulfur is an essential element for many organisms and environmental processes. Every year, organisms including microalgae produce more than one billion tons of a sulfur-containing compound called DMSP. Some of this DMSP is released into seawater, where it acts as a key nutrient for microscopic organisms and as a foraging cue to attract fish. DMSP is also the precursor of a gas that helps to form clouds. Despite DMSP’s potential large-scale effects, it is still not clear what role it plays in the organisms that produce it, or how it is transferred from the microalgae that produce it to the bacteria that use it. It is thought that DMSP could potentially protect the cells from sudden changes in the amount of salt in the seawater (salinity) or from other damage, such as oxidative stress – a build-up of harmful chemicals inside cells. In a controlled setting using artificial seawater, Raina et al. used high-resolution imaging and chemical analysis to track the journey of DMSP from microalgae to recipient bacteria. The results show that similar to land plants, algae store DMSP in the compartments that regulate cell pressure and photosynthesis. The presence of DMSP in these locations also supports its proposed role in protecting cells from changes in salinity or oxidative damage. A future step will be to identify the genes involved in producing DMSP in microalgae. This knowledge could be used to create mutants that are either incapable of producing this molecule or that overproduce it. In combination with the high-resolution imaging techniques described here, this will allow researchers to fully understand the role that DMSP plays in these organisms. DOI: http://dx.doi.org/10.7554/eLife.23008.002

Here we describe an efficient and effective technique for rearing sexually-derived coral propagules from spawning through larval settlement and symbiont uptake with minimal impact on natural coral populations. We sought to maximize larval survival while minimizing expense and daily husbandry maintenance by experimentally determining optimized conditions and protocols for gamete fertilization, larval cultivation, induction of larval settlement by crustose coralline algae, and inoculation of newly settled juveniles with their dinoflagellate symbiont Symbiodinium. Larval rearing densities at or below 0.2 larvae mL−1 were found to maximize larval survival and settlement success in culture tanks while minimizing maintenance effort. Induction of larval settlement via the addition of a ground mixture of diverse crustose coralline algae (CCA) is recommended, given the challenging nature of in situ CCA identification and our finding that non settlement-inducing CCA assemblages do not inhibit larval settlement if suitable assemblages are present. Although order of magnitude differences in infectivity were found between common Great Barrier Reef Symbiodinium clades C and D, no significant differences in Symbiodinium uptake were observed between laboratory-cultured and wild-harvested symbionts in each case. The technique presented here for Acropora millepora can be adapted for research and restoration efforts in a wide range of broadcast spawning coral species.

Coral reproduction is vulnerable to both declining water quality and warming temperatures, with simultaneous exposures likely compounding the negative impact of each stressor. We investigated how early life processes of the coral Acropora tenuis respond to increasing levels of suspended sediments in combination with temperature or organic nutrients. Fertilization success and embryo development were more sensitive to suspended sediments than to high temperatures or nutrient enrichment, while larval development (after acquisition of cilia) and settlement success were predominantly affected by thermal stress. Fertilization success was reduced 80% by suspended sediments, and up to 24% by temperature, while the addition of nutrients to suspended sediments had no further impact. Larval survivorship was unaffected by any of these treatments. However, settlement success of larvae developing from treatment-exposed embryos was negatively affected by all three stressors (e.g. up to 55% by suspended sediments), while exposure only during later larval stages predominantly responded to temperature stress. Environmentally relevant levels of suspended sediments and temperature had the greatest impacts, affecting more processes than the combined impacts of sediments and nutrients. These results suggest that management strategies to maintain suspended sediments at low concentrations during coral spawning events will benefit coral recruitment, especially with warming climate.

The dinoflagellate-coral partnership influences the coral holobiont’s tolerance to thermal stress and bleaching. However, the comparative roles of host genetic versus environmental factors in determining the composition of this symbiosis are largely unknown. Here we quantify the heritability of the initialSymbiodiniumcommunities for two broadcast-spawning corals with different symbiont transmission modes:Acropora tenuishas environmental acquisition, whereasMontipora digitatahas maternal transmission. Using high throughput sequencing of the ITS-2 region to characterize communities in parents, juveniles and eggs, we describe previously undocumentedSymbiodiniumdiversity and dynamics in both corals. After one month of uptake in the field,Symbiodiniumcommunities associated withA. tenuisjuveniles were dominated by A3, C1, D1, A-type CCMP828, and D1a in proportional abundances conserved between experiments in two years.M. digitataeggs were predominantly characterized by C15, D1, and A3. In contrast to current paradigms, host genetic influences accounted for a surprising 29% of phenotypic variation inSymbiodiniumcommunities in the horizontally-transmittingA. tenuis, but only 62% in the vertically-transmittingM. digitata. Our results reveal hitherto unknown flexibility in the acquisition ofSymbiodiniumcommunities and substantial heritability in both species, providing material for selection to produce partnerships that are locally adapted to changing environmental conditions.