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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

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.

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.

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.

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 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.

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.

International audience; Pivotal to projecting the fate of coral reefs is the capacity of reef-building corals to acclimatize and adapt to climate change. Transgenerational plasticity may enable some marine organisms to acclimatize over several generations and it has been hypothesized that epigenetic processes and microbial associations might facilitate adaptive responses. However, current evidence is equivocal and understanding of the underlying processes is limited. Here, we discuss prospects for observing transgenerational plasticity in corals and the mechanisms that could enable adaptive plasticity in the coral holobiont, including the potential role of epigenetics and coral-associated microbes. Well-designed and strictly controlled experiments are needed to distinguish transgenerational plasticity from other forms of plasticity, and to elucidate the underlying mechanisms and their relative importance compared with genetic adaptation.

Coral tissue loss diseases, collectively known as white syndromes (WSs), induce significant mortality on reefs throughout the Indo-Pacific, yet definitive confirmation of WS etiologies remains elusive. In this study, we integrated ecological disease monitoring, bacterial community profiling, in situ visualization of microbe-host interactions, and cellular responses of the host coral through an 18-month repeated-sampling regime. We assert that the observed pathogenesis of WS lesions on acroporid corals at Lizard Island (Great Barrier Reef) is not the result of apoptosis or infection by Vibrio bacteria, ciliates, fungi, cyanobacteria, or helminths. Histological analyses detected helminths, ciliates, fungi, and cyanobacteria in fewer than 25% of WS samples, and helminths and fungi were also observed in 12% of visually healthy samples. The abundances of Vibrio -affiliated sequences (assessed using 16S rRNA amplicon sequencing) did not differ significantly between health states and never exceeded 3.3% of reads in any individual sample. In situ visualization detected Vibrio bacteria only in summer WS lesion samples and revealed no signs of these bacteria in winter disease samples (or any healthy tissue samples), despite continued disease progression year round. However, a 4-fold increase in Rhodobacteraceae -affiliated bacterial sequences at WS lesion fronts suggests that this group of bacteria could play a role in WS pathogenesis and/or serve as a diagnostic criterion for disease differentiation. While the causative agent(s) underlying WSs remains elusive, the microbial and cellular processes identified in this study will help to identify and differentiate visually similar but potentially distinct WS etiologies. IMPORTANCE Over the past decade, a virulent group of coral diseases known as white syndromes have impacted coral reefs throughout the Indian and Pacific Oceans. This article provides a detailed case study of white syndromes to combine disease ecology, high-throughput microbial community profiling, and cellular-scale host-microbe visualization over seasonal time scales. We provide novel insights into the etiology of this devastating disease and reveal new diagnostic criteria that could be used to differentiate visually similar but etiologically distinct forms of white syndrome.

Extremes in seasonal environmental conditions can significantly impact the health and physiological functioning of reef corals, underscoring the need for knowledge of seasonally specific baselines from which to monitor and forecast impending stress. Increases above summertime means in seawater temperature, sunlight intensity, turbidity, or sedimentation may reduce coral immunocompetency and increase disease and bleaching susceptibility. We analyzed temporal patterns in innate immunity parameters over nine time points throughout one year to establish baseline levels from which anomalies might be detected for representative species from three major reef‐building coral families (Acroporidae, Faviidae, and Poritidae). Temporal patterns in both phenoloxidase activity and expression of green fluorescent protein‐like proteins varied among the three families, as did overall constitutive levels. For example, Porites cylindrica had 2.8‐fold higher yearly average levels of phenoloxidase activity than Acropora millepora, which had the lowest levels. In contrast, mean fluorescence was lowest in Acropora millepora and highest in Echinopora mammiformis. Relationships between the potential physical drivers (seasonal variation in seawater temperature, rainfall, salinity) and temporal patterns in these parameters also differed among the three species. For example, phenoloxidase activity was positively correlated with seawater temperature in A. millepora, but negatively correlated in both E. mammiformis and P. cylindrica. Distinctions in constitutive levels and temporal patterns in these parameters among species suggest that corals from these three families have evolved different strategies for investing resources into innate immune parameters. Such differences highlight the need for species‐specific baselines and long‐term assessments to accurately predict coral reef trajectories in rapidly changing environments.

Seawater temperature anomalies associated with warming climate have been linked to increases in coral disease outbreaks that have contributed to coral reef declines globally. However, little is known about how seasonal scale variations in environmental factors influence disease dynamics at the level of individual coral colonies. In this study, we applied a multi-state Markov model (MSM) to investigate the dynamics of black band disease (BBD) developing from apparently healthy corals and/or a precursor-stage, termed ‘cyanobacterial patches’ (CP), in relation to seasonal variation in light and seawater temperature at two reef sites around Pelorus Island in the central sector of the Great Barrier Reef. The model predicted that the proportion of colonies transitioning from BBD to Healthy states within three months was approximately 57%, but 5.6% of BBD cases resulted in whole colony mortality. According to our modelling, healthy coral colonies were more susceptible to BBD during summer months when light levels were at their maxima and seawater temperatures were either rising or at their maxima. In contrast, CP mostly occurred during spring, when both light and seawater temperatures were rising. This suggests that environmental drivers for healthy coral colonies transitioning into a CP state are different from those driving transitions into BBD. Our model predicts that (1) the transition from healthy to CP state is best explained by increasing light, (2) the transition between Healthy to BBD occurs more frequently from early to late summer, (3) 20% of CP infected corals developed BBD, although light and temperature appeared to have limited impact on this state transition, and (4) the number of transitions from Healthy to BBD differed significantly between the two study sites, potentially reflecting differences in localised wave action regimes.

In situvisualization of microbial communities within their natural habitats provides a powerful approach to explore complex interactions between microorganisms and their macroscopic hosts. Specifically, the application of fluorescence in situ hybridization (FISH) to simultaneously identify and visualize diverse microbial taxa associated with coral hosts, including symbiotic algae (Symbiodinium), Bacteria, Archaea, Fungi and protists, could help untangle the structure and function of these diverse taxa within the coral holobiont. However, the application of FISH approaches to coral samples is constrained by non-specific binding of targeted rRNA probes to cellular structures within the coral animal tissues (including nematocysts, spirocysts, granular gland cells within the gastrodermis and cnidoglandular bands of mesenterial filaments). This issue, combined with high auto-fluorescence of both host tissues and endosymbiotic dinoflagellates (Symbiodinium), make FISH approaches for analyses of coral tissues challenging. Here we outline the major pitfalls associated with applying FISH to coral samples and describe approaches to overcome these challenges.

Bacterial communities associated with healthy corals produce antimicrobial compounds that inhibit the colonization and growth of invasive microbes and potential pathogens. To date, however, bacteria-derived antimicrobial molecules have not been identified in reef-building corals. Here we report the isolation of an antimicrobial compound produced by Pseudovibrio sp. P12, a common and abundant coral-associated bacterium. This strain was capable of metabolizing dimethylsulfoniopropionate (DMSP), a sulfur molecule produced in high concentrations by reef-building corals and playing a role in structuring their bacterial communities. Bioassay-guided fractionation coupled with nuclear magnetic resonance (NMR) and mass spectrometry (MS), identified the antimicrobial as tropodithietic acid (TDA), a sulfur-containing compound likely derived from DMSP catabolism. TDA was produced in large quantities by Pseudovibrio sp., and prevented the growth of two previously identified coral pathogens, Vibrio coralliilyticus and V. owensii, at very low concentrations (0.5 µg/mL) in agar diffusion assays. Genome sequencing of Pseudovibrio sp. P12 identified gene homologs likely involved in the metabolism of DMSP and production of TDA. These results provide additional evidence for the integral role of DMSP in structuring coral-associated bacterial communities and underline the potential of these DMSP-metabolizing microbes to contribute to coral disease prevention.

International audience; To forecast marine disease outbreaks as oceans warm requires new environmental surveillance tools. We describe an iterative process for developing these tools that combines research, development and deployment for suitable systems. The first step is to identify candidate host–pathogen systems. The 24 candidate systems we identified include sponges, corals, oysters, crustaceans, sea stars, fishes and sea grasses (among others). To illustrate the other steps, we present a case study of epizootic shell disease (ESD) in the American lobster. Increasing prevalence of ESD is a contributing factor to lobster fishery collapse in southern New England (SNE), raising concerns that disease prevalence will increase in the northern Gulf of Maine under climate change. The lowest maximum bottom temperature associated with ESD prevalence in SNE is 128C. Our seasonal outlook for 2015 and long-term projections show bottom temperatures greater than or equal to 128C may occur in this and coming years in the coastal bays of Maine. The tools presented will allow managers to target efforts to monitor the effects of ESD on fishery sustainability and will be iteratively refined. The approach and case example highlight that temperature-based surveillance tools can inform research, monitoring and management of emerging and continuing marine disease threats.

Inshore coral reefs are experiencing the combined pressures of excess nutrient availability associated with coastal activities and warming seawater temperatures. Both pressures are known to have detrimental effects on the early life history stages of hard corals, but studies of their combined effects on early demographic stages are lacking. We conducted a series of experiments to test the combined effects of nutrient enrichment (three levels) and elevated seawater temperature (up to five levels) on early life history stages of the inshore coral Acropora tenuis, a common species in the Indo-Pacific and Red Sea. Gamete fertilization, larval survivorship and larval settlement were all significantly reduced as temperature increased, but only fertilization was further affected by simultaneous nutrient enrichment. Combined high temperatures and nutrient enrichment affected fertilization in an additive manner, whereas embryo abnormalities increased synergistically. Higher than normal temperatures (32°C) increased coral juvenile growth rates 1.6-fold, but mortality also increased by 50%. The co-occurrence of nutrient enrichment with high temperatures reduced juvenile mortality to 36%, ameliorating temperature stress (antagonistic interaction). Overall, the types of effect (additive vs synergistic or antagonistic) and their magnitude varied among life stages. Gamete and embryo stages were more affected by temperature stress and, in some cases, also by nutrient enrichment than juveniles. The data suggest that coastal runoff events might exacerbate the impacts of warming temperatures on fertilization if these events co-occur during corals spawning. The cumulative impacts of simultaneous exposure to nutrient enrichment and elevated temperatures over all early life history stages increases the likelihood for failure of larval supply and recruitment for this coral species. Our results suggest that improving the water quality of river discharges into coastal areas might help to enhance the thermal tolerances of early life history stages in this common coral species.

In recent decades, coral reef ecosystems have declined to the extent that reefs are now threatened globally. While many water quality parameters have been proposed to contribute to reef declines, little evidence exists conclusively linking specific water quality parameters with increased disease prevalence in situ. Here we report evidence from in situ coral health surveys confirming that chronic exposure to dredging-associated sediment plumes significantly increase the prevalence of white syndromes, a devastating group of globally important coral diseases. Coral health surveys were conducted along a dredging-associated sediment plume gradient to assess the relationship between sedimentation, turbidity and coral health. Reefs exposed to the highest number of days under the sediment plume (296 to 347 days) had two-fold higher levels of disease, largely driven by a 2.5-fold increase in white syndromes, and a six-fold increase in other signs of compromised coral health relative to reefs with little or no plume exposure (0 to 9 days). Multivariate modeling and ordination incorporating sediment exposure level, coral community composition and cover, predation and multiple thermal stress indices provided further confirmation that sediment plume exposure level was the main driver of elevated disease and other compromised coral health indicators. This study provides the first evidence linking dredging-associated sedimentation and turbidity with elevated coral disease prevalence in situ. Our results may help to explain observed increases in global coral disease prevalence in recent decades and suggest that minimizing sedimentation and turbidity associated with coastal development will provide an important management tool for controlling coral disease epizootics.

We investigated the effect of stressors associated with offshore reef-based tourist platforms on the coral immune system. Our findings suggest that stressors associated with platform-related activities, in synergy with seasonal factors, compromise the coral immune system, contributing to the higher coral disease prevalence observed at these locations., Unravelling the contributions of local anthropogenic and seasonal environmental factors in suppressing the coral immune system is important for prioritizing management actions at reefs exposed to high levels of human activities. Here, we monitor health of the model coral Acropora millepora adjacent to a high-use and an unused reef-based tourist platform, plus a nearby control site without a platform, over 7 months spanning a typical austral summer. Comparisons of temporal patterns in a range of biochemical and genetic immune parameters (Toll-like receptor signalling pathway, lectin–complement system, prophenoloxidase-activating system and green fluorescent protein-like proteins) among healthy, injured and diseased corals revealed that corals exhibit a diverse array of immune responses to environmental and anthropogenic stressors. In healthy corals at the control site, expression of genes involved in the Toll-like receptor signalling pathway (MAPK p38, MEKK1, cFos and ATF4/5) and complement system (C3 and Bf) was modulated by seasonal environmental factors in summer months. Corals at reef platform sites experienced additional stressors over the summer, as evidenced by increased expression of various immune genes, including MAPK p38 and MEKK1. Despite increased expression of immune genes, signs of white syndromes were detected in 31% of study corals near tourist platforms in the warmest summer month. Evidence that colonies developing disease showed reduced expression of genes involved in the complement pathway prior to disease onset suggests that their immune systems may have been compromised. Responses to disease and physical damage primarily involved the melanization cascade and GFP-like proteins, and appeared to be sufficient for recovery when summer heat stress subsided. Overall, seasonal and anthropogenic factors may have interacted synergistically to overwhelm the immune systems of corals near reef platforms, leading to increased disease prevalence in summer at these sites.

International audience; Rising sea temperatures are likely to increase the frequency of disease outbreaks affecting reef-building corals through impacts on coral hosts and pathogens. We present and compare climate model projections of temperature conditions that will increase coral susceptibility to disease, pathogen abundance and pathogen virulence. Both moderate (RCP 4.5) and fossil fuel aggressive (RCP 8.5) emissions scenarios are examined. We also compare projections for the onset of disease-conducive conditions and severe annual coral bleaching, and produce a disease risk summary that combines climate stress with stress caused by local human activities. There is great spatial variation in the projections, both among and within the major ocean basins, in conditions favouring disease development. Our results indicate that disease is as likely to cause coral mortality as bleaching in the coming decades. These projections identify priority locations to reduce stress caused by local human activities and test management interventions to reduce disease impacts.

The bacterium Vibrio coralliilyticus has been implicated as the causative agent of coral tissue loss diseases (collectively known as white syndromes) at sites across the Indo-Pacific and represents an emerging model pathogen for understanding the mechanisms linking bacterial infection and coral disease. In this study, we used a mini-Tn7 transposon delivery system to chromosomally label a strain of V. coralliilyticus isolated from a white syndrome disease lesion with a green fluorescent protein gene (GFP). We then tested the utility of this modified strain as a research tool for studies of coral host–pathogen interactions. A suite of biochemical assays and experimental infection trials in a range of model organisms confirmed that insertion of the GFP gene did not interfere with the labeled strain’s virulence. Using epifluorescence video microscopy, the GFP-labeled strain could be reliably distinguished from non-labeled bacteria present in the coral holobiont, and the pathogen’s interactions with the coral host could be visualized in real time. This study demonstrates that chromosomal GFP labeling is a useful technique for visualization and tracking of coral pathogens and provides a novel tool to investigate the role of V. coralliilyticus in coral disease pathogenesis., Human Frontier Science Program (Strasbourg, France) (No. RGY0089RS)

The capacity of reef-building corals to associate with environmentally-appropriate types of endosymbionts from the dinoflagellate genus Symbiodinium contributes significantly to their success at local scales. Additionally, some corals are able to acclimatize to environmental perturbations by shuffling the relative proportions of different Symbiodinium types hosted. Understanding the dynamics of these symbioses requires a sensitive and quantitative method of Symbiodinium genotyping. Electrophoresis methods, still widely utilized for this purpose, are predominantly qualitative and cannot guarantee detection of a background type below 10% of the total Symbiodinium population. Here, the relative abundances of four Symbiodinium types (A13, C1, C3, and D1) in mixed samples of known composition were quantified using deep sequencing of the internal transcribed spacer of the ribosomal RNA gene (ITS-2) by means of Next Generation Sequencing (NGS) using Roche 454. In samples dominated by each of the four Symbiodinium types tested, background levels of the other three types were detected when present at 5%, 1%, and 0.1% levels, and their relative abundances were quantified with high (A13, C1, D1) to variable (C3) accuracy. The potential of this deep sequencing method for resolving fine-scale genetic diversity within a symbiont type was further demonstrated in a natural symbiosis using ITS-1, and uncovered reef-specific differences in the composition of Symbiodinium microadriaticum in two species of acroporid corals (Acropora digitifera and A. hyacinthus) from Palau. The ability of deep sequencing of the ITS locus (1 and 2) to detect and quantify low-abundant Symbiodinium types, as well as finer-scale diversity below the type level, will enable more robust quantification of local genetic diversity in Symbiodinium populations. This method will help to elucidate the role that background types have in maximizing coral fitness across diverse environments and in response to environmental change.

Cyclone Yasi, one of the most severe tropical storms on record, crossed the central Great Barrier Reef (GBR) in February 2011, bringing wind speeds of up to 285 km hr⁻¹ and wave heights of at least 10 m, and causing massive destruction to exposed reefs in the Palm Island Group. Following the cyclone, mean (± S.E.) hard coral cover ranged from just 2.1 (0.2) % to 5.3 (0.4) % on exposed reefs and no reproductively mature colonies of any species of Acropora remained. Although no fragments of Acropora were found at impacted exposed sites following the cyclone, small juvenile colonies of Acropora (

The effects of temperature and light on the breakdown of the coral-Symbiodinium symbiosis are well documented but current understanding of their roles during initial uptake and establishment of symbiosis is limited. In this study, we investigate how temperature and light affect the uptake of the algal symbionts, ITS1 types C1 and D, by juveniles of the broadcast-spawning corals Acropora tenuis and A. millepora. Elevated temperatures had a strong negative effect on Symbiodinium uptake in both coral species, with corals at 31 °C showing as little as 8% uptake compared to 87% at 28 °C. Juveniles in high light treatments (390 µmol photons m(-2) s(-1)) had lower cell counts across all temperatures, emphasizing the importance of the light environment during the initial uptake phase. The proportions of the two Symbiodinium types taken up, as quantified by a real time PCR assay using clade C- and D-specific primers, were also influenced by temperature, although variation in uptake dynamics between the two coral species indicates a host effect. At 28 °C, A. tenuis juveniles were dominated by C1 Symbiodinium, and while the number of D Symbiodinium cells increased at 31 °C, they never exceeded the number of C1 cells. In contrast, juveniles of A. millepora had approximately equal numbers of C1 and D cells at 28 °C, but were dominated by D at 30 °C and 31 °C. This study highlights the significant role that environmental factors play in the establishment of coral-Symbiodinium symbiosis and provides insights into how potentially competing Symbiodinium types take up residence in coral juveniles.

Background: Corals, like many other marine invertebrates, lack a mature allorecognition system in early life history stages. Indeed, in early ontogeny, when corals acquire and establish associations with various surface microbiota and dinoflagellate endosymbionts, they do not efficiently distinguish between closely and distantly related individuals from the same population. However, very little is known about the molecular components that underpin allorecognition and immunity responses or how they change through early ontogeny in corals. Methodology/Principal Findings: Patterns in the expression of four putative immune response genes (apextrin, complement C3, and two CELIII type lectin genes) were examined in juvenile colonies of Acropora millepora throughout a six-month post-settlement period using quantitative real-time PCR (qPCR). Expression of a CELIII type lectin gene peaked in the fourth month for most of the coral juveniles sampled and was significantly higher at this time than at any other sampling time during the six months following settlement. The timing of this increase in expression levels of putative immune response genes may be linked to allorecognition maturation which occurs around this time in A.millepora. Alternatively, the increase may represent a response to immune challenges, such as would be involved in the recognition of symbionts (such as Symbiodinium spp. or bacteria) during winnowing processes as symbioses are fine-tuned. Conclusions/Significance: Our data, although preliminary, are consistent with the hypothesis that lectins may play an important role in the maturation of allorecognition responses in corals. The co-expression of lectins with apextrin during development of coral juveniles also raises the possibility that these proteins, which are components of innate immunity in other invertebrates, may influence the innate immune systems of corals through a common pathway or system. However, further studies investigating the expression of these genes in alloimmune-challenged corals are needed to further clarify emerging evidence of a complex innate immunity system in corals.

In sessile modular marine invertebrates, chimeras can originate from fusions of closely settling larvae or of colonies that come into contact through growth or movement. While it has been shown that juveniles of brooding corals fuse under experimental conditions, chimera formation in broadcast spawning corals, the most abundant group of reef corals, has not been examined. This study explores the capacity of the broadcast spawning coral Acropora millepora to form chimeras under experimental conditions and to persist as chimeras in the field. Under experimental conditions, 1.5-fold more larvae settled in aggregations than solitarily, and analyses of nine microsatellite loci revealed that 50 per cent of juveniles tested harboured different genotypes within the same colony. Significantly, some chimeric colonies persisted for 23 months post-settlement, when the study ended. Genotypes within persisting chimeric colonies all showed a high level of relatedness, whereas rejecting colonies displayed variable levels of relatedness. The nearly threefold greater sizes of chimeras compared with solitary juveniles, from settlement through to at least three months, suggest that chimerism is likely to be an important strategy for maximizing survival of vulnerable early life-history stages of corals, although longer-term studies are required to more fully explore the potential benefits of chimerism.

Marine Biology, 159 (1), ISSN:0025-3162, ISSN:1432-1793

Coral disease has emerged over recent decades as a significant threat to coral reef ecosystems, with declines in coral cover and diversity of Caribbean reefs providing an example of the potential impacts of disease at regional scales. If similar trends are to be mitigated or avoided on reefs worldwide, a deeper understanding of the factors underlying the origin and spread of coral diseases and the steps that can be taken to prevent, control, or reduce their impacts is required. In recent years, an increased focus on coral microbiology and the application of classic culture techniques and emerging molecular technologies has revealed several coral pathogens that could serve as targets for novel coral disease diagnostic tools. The ability to detect and quantify microbial agents identified as indicators of coral disease will aid in the elucidation of disease causation and facilitate coral disease detection and diagnosis, pathogen monitoring in individuals and ecosystems, and identification of pathogen sources, vectors, and reservoirs. This information will advance the field of coral disease research and contribute knowledge necessary for effective coral reef management. This paper establishes the need for sensitive and specific molecular-based coral pathogen detection, outlines the emerging technologies that could serve as the basis of a new generation of coral disease diagnostic assays, and addresses the unique challenges inherent to the application of these techniques to environmentally derived coral samples.

Background: Declining water quality coupled with the effects of climate change are rapidly increasing coral diseases on reefs worldwide, although links between coral diseases and environmental parameters remain poorly understood. This is the first study to document a correlation between coral disease and water quality on an inshore reef. Methodology/Principal Findings: The temporal dynamics of the coral disease atramentous necrosis (AN) was investigated over two years within inshore populations of Montipora aequituberculata in the central Great Barrier Reef, in relation to rainfall, salinity, temperature, water column chlorophyll a, suspended solids, sedimentation, dissolved organic carbon, and particulate nitrogen, phosphorus and organic carbon. Overall, mean AN prevalence was 10-fold greater during summer wet seasons than winter dry seasons. A 2.5-fold greater mean disease abundance was detected during the summer of 2009 (44 ± SE 6.7 diseased colonies per 25 m2), when rainfall was 1.6-fold greater than in the summer of 2008. Two water quality parameters explained 67% of the variance in monthly disease prevalence in a Partial Least Squares regression analysis; disease abundance was negatively correlated with salinity (R2 = −0.6) but positively correlated with water column particulate organic carbon concentration (R2 = 0.32). Seasonal temperature patterns were also positively correlated with disease abundance, but explained only a small portion of the variance. Conclusions/Significance: The results suggest that rainfall and associated runoff may facilitate seasonal disease outbreaks, potentially by reducing host fitness or by increasing pathogen virulence due to higher availability of nutrients and organic matter. In the future, rainfall and seawater temperatures are likely to increase due to climate change which may lead to decreased health of inshore reefs.

Sessile animals, like corals, frequently suffer physical injury from a variety of sources, thus wound-healing mechanisms that restore tissue integrity and prevent infection are vitally important for defence. Despite the ecological importance of reef-building corals, little is known about the cells and processes involved in wound healing in this group or in phylogenetically basal metazoans in general. A histological investigation into wound healing of the scleractinian coral Porites cylindrica at 0 h, 6 h, 24 h and 48 h after injury revealed differences in cellular components between injured and healthy tissues. Cell counts of the obligate endosymbiont, Symbiodinium, and melanin volume fraction analysis revealed rapid declines in both Symbiodinium abundance and tissue cross-sectional area occupied by melanin-containing granular cells after injury. Four phases of wound healing were identified, which are similar to phases described for both vertebrates and invertebrates. The four phases included (i) plug formation via the degranulation of melanin-containing granular cells; (ii) immune cell infiltration (inflammation); (iii) granular tissue formation (proliferation); and (iv) maturation. This study provides detailed documentation of the processes involved in scleractinian wound healing for the first time and further elucidates the roles of previously-described immune cells, such as fibroblasts. These results demonstrate the conservation of wound healing processes from anthozoans to humans.

Background: Chimeras are organisms containing tissues or cells of two or more genetically distinct individuals, and are known to exist in at least nine phyla of protists, plants, and animals. Although widespread and common in marine invertebrates, the extent of chimerism in wild populations of reef corals is unknown. Methodology/Principal Findings: The extent of chimerism was explored within two populations of a common coral, Acropora millepora, on the Great Barrier Reef, Australia, by using up to 12 polymorphic DNA microsatellite loci. At least 2% and 5% of Magnetic Island and Pelorus Island populations of A. millepora, respectively, were found to be chimeras (3% overall), based on conservative estimates. A slightly less conservative estimate indicated that 5% of colonies in each population were chimeras. These values are likely to be vast underestimates of the true extent of chimerism, as our sampling protocol was restricted to a maximum of eight branches per colony, while most colonies consist of hundreds of branches. Genotypes within chimeric corals showed high relatedness, indicating that genetic similarity is a prerequisite for long-term acceptance of non-self genotypes within coral colonies. Conclusions/Significance: While some brooding corals have been shown to form genetic chimeras in their early life history stages under experimental conditions, this study provides the first genetic evidence of the occurrence of coral chimeras in the wild and of chimerism in a broadcast spawning species. We hypothesize that chimerism is more widespread in corals than previously thought, and suggest that this has important implications for their resilience, potentially enhancing their capacity to compete for space and respond to stressors such as pathogen infection.

Background: Reef-building corals live in symbiosis with a diverse range of dinoflagellate algae ( genus Symbiodinium) that differentially influence the fitness of the coral holobiont. The comparative role of symbiont type in holobiont fitness in relation to host genotype or the environment, however, is largely unknown. We addressed this knowledge gap by manipulating host-symbiont combinations and comparing growth, survival and thermal tolerance among the resultant holobionts in different environments.Methodology/Principal Findings: Offspring of the coral, Acropora millepora, from two thermally contrasting locations, were experimentally infected with one of six Symbiodinium types, which spanned three phylogenetic clades (A, C and D), and then outplanted to the two parental field locations (central and southern inshore Great Barrier Reef, Australia). Growth and survival of juvenile corals were monitored for 31-35 weeks, after which their thermo-tolerance was experimentally assessed. Our results showed that: (1) Symbiodinium type was the most important predictor of holobiont fitness, as measured by growth, survival, and thermo-tolerance; (2) growth and survival, but not heat-tolerance, were also affected by local environmental conditions; and (3) host population had little to no effect on holobiont fitness. Furthermore, coral-algal associations were established with symbiont types belonging to clades A, C and D, but three out of four symbiont types belonging to clade C failed to establish a symbiosis. Associations with clade A had the lowest fitness and were unstable in the field. Lastly, Symbiodinium types C1 and D were found to be relatively thermo-tolerant, with type D conferring the highest tolerance in A. millepora.Conclusions/Significance: These results highlight the complex interactions that occur between the coral host, the algal symbiont, and the environment to shape the fitness of the coral holobiont. An improved understanding of the factors affecting coral holobiont fitness will assist in predicting the responses of corals to global climate change.

Algal endosymbionts of the genus Symbiodinium play a key role in the nutrition of reef building corals and strongly affect the thermal tolerance and growth rate of the animal host. This study reports that (14)C photosynthate incorporation into juvenile coral tissues was doubled in Acropora millepora harbouring Symbiodinium C1 compared with juveniles from common parentage harbouring Symbiodinium D in a laboratory experiment. Rapid light curves performed on the same corals revealed that the relative electron transport rate of photosystem II (rETR(MAX)) was 87% greater in Symbiodinium C1 than in Symbiodinium D in hospite. The greater relative electron transport through photosystem II of Symbiodinium C1 is positively correlated with increased carbon delivery to the host under the applied experimental conditions (r (2) = 0.91). This may translate into a competitive advantage for juveniles harbouring Symbiodinium C1 under certain field conditions, since rapid early growth typically limits mortality. Both symbiont types exhibited severe reductions in (14)C incorporation during a 10-h exposure to the electron transport blocking herbicide diuron (DCMU), confirming the link between electron transport through PSII and photosynthate incorporation within the host tissue. These findings advance the current understanding of symbiotic relationships between corals and their symbionts, providing evidence that enhanced growth rates of juvenile corals may result from greater translocation of photosynthates from Symbiodinium C1.