Within-population variability in coral heat tolerance indicates climate adaptation potential.

Coral reefs are facing unprecedented mass bleaching and mortality events due to marine heatwaves and climate change. To avoid extirpation, corals must adapt. Individual variation in heat tolerance and its heritability underpin the potential for coral adaptation. However, the magnitude of heat tolerance variability within coral populations is largely unresolved. We address this knowledge gap by exposing corals from a single reef to an experimental marine heatwave. We found that double the heat stress dosage was required to induce bleaching in the most-tolerant 10%, compared to the least-tolerant 10% of the population. By the end of the heat stress exposure, all of the least-tolerant corals were dead, whereas the most-tolerant remained alive. To contextualize the scale of this result over the coming century, we show that under an ambitious future emissions scenario, such differences in coral heat tolerance thresholds equate to up to 17 years delay until the onset of annual bleaching and mortality conditions. However, this delay is limited to only 10 years under a high emissions scenario. Our results show substantial variability in coral heat tolerance which suggests scope for natural or assisted evolution to limit the impacts of climate change in the short-term. For coral reefs to persist through the coming century, coral adaptation must keep pace with ocean warming, and ambitious emissions reductions must be realized.

The role of viruses in coral health and disease.

Metagenomic and electron microscopy studies confirm that the coral microbiome contains a rich diversity and abundance of viruses. While there have been no definitive tests of disease causation by viruses in corals, viruses have been implicated as coral pathogens in a number of studies. Growing evidence also indicates that latent viral infections can compromise the algal symbionts under environmental stress and may be involved in the coral bleaching response. Conversely, bacteriophages and archaeal phage viruses are abundant in the microbiome of healthy corals and are likely to be involved in complex ecological networks, genetic material transfer and selective co-evolution within the surface mucus layers and tissues. The relative importance of viral control of bacterial and archaeal populations is unknown, but they are almost certain to be exerting some level of control on the composition and maintenance of the coral microbiome. While rapid leaps in the capability to detect viruses have been made due to advances in metagenomics and bioinformatics, these approaches need now to be integrated with in vitro culture and challenge experiments to assess the functional roles of viruses in health and disease, and it is imperative that interactions with other members of the coral microbiome are taken into account when assessing disease causation.

White syndrome in Acropora muricata: nonspecific bacterial infection and ciliate histophagy.

Selective antibiotic treatment of white syndrome (WS)-affected corals (Acropora muricata) from Fiji was used to identify 3 potential bacterial pathogens of the disease. Interestingly, the suite of bacterial associates of the disease was different to that recently identified using identical primer sets for WS on the GBR and in the Solomon Islands. In addition to the three bacterial pathogenic candidates and as previously shown for WS and more recently for white band disease (WBD) in the Caribbean, all samples of the disease were specifically associated with the histophagous ciliate Philaster lucinda. From the pattern of disease progression and histopathology in relation to the selective elimination of microbial groups, we conclude that these 'white' diseases are a result of a nonspecific bacterial infection and a 'secondary' infection by the P. lucinda ciliate. Although we have not observed the initiation of infection, a nonspecific, multispecies bacterial infection appears to be a corequirement for WS lesion progression and we hypothesize that the bacterial infection occurs initially, weakening the defences of the host to predation by the ciliates. Such ciliate histophagy gives rise to the characteristic white band of denuded coral skeleton that gives these diseases their names. The characteristics of the microbial communities of WBD and WS appear identical, and since the bacterial associates of WS vary geographically (and/or temporally), there appears to be no logical distinction between WS in the Indo-Pacific and WBD in the Caribbean.

Emergent increase in coral thermal tolerance reduces mass bleaching under climate change.

Recurrent mass bleaching events threaten the future of coral reefs. To persist under climate change, corals will need to endure progressively more intense and frequent marine heatwaves, yet it remains unknown whether their thermal tolerance can keep pace with warming. Here, we reveal an emergent increase in the thermal tolerance of coral assemblages at a rate of 0.1 °C/decade for a remote Pacific coral reef system. This led to less severe bleaching impacts than would have been predicted otherwise, indicating adaptation, acclimatisation or shifts in community structure. Using future climate projections, we show that if thermal tolerance continues to rise over the coming century at the most-likely historic rate, substantial reductions in bleaching trajectories are possible. High-frequency bleaching can be fully mitigated at some reefs under low-to-middle emissions scenarios, yet can only be delayed under high emissions scenarios. Collectively, our results indicate a potential ecological resilience to climate change, but still highlight the need for reducing carbon emissions in line with Paris Agreement commitments to preserve coral reefs.

No apparent trade-offs associated with heat tolerance in a reef-building coral.

As marine species adapt to climate change, their heat tolerance will likely be under strong selection. Yet trade-offs between heat tolerance and other life history traits could compromise natural adaptation or assisted evolution. This is particularly important for ecosystem engineers, such as reef-building corals, which support biodiversity yet are vulnerable to heatwave-induced mass bleaching and mortality. Here, we exposed 70 colonies of the reef-building coral Acropora digitifera to a long-term marine heatwave emulation experiment. We tested for trade-offs between heat tolerance and three traits measured from the colonies in situ - colony growth, fecundity, and symbiont community composition. Despite observing remarkable within-population variability in heat tolerance, all colonies were dominated by Cladocopium C40 symbionts. We found no evidence for trade-offs between heat tolerance and fecundity or growth. Contrary to expectations, positive associations emerged with growth, such that faster-growing colonies tended to bleach and die at higher levels of heat stress. Collectively, our results suggest that these corals exist on an energetic continuum where some high-performing individuals excel across multiple traits. Within populations, trade-offs between heat tolerance and growth or fecundity may not be major barriers to natural adaptation or the success of assisted evolution interventions.

Ciliate and bacterial communities associated with White Syndrome and Brown Band Disease in reef-building corals.

White Syndrome (WS) and Brown Band Disease (BrB) are important causes of reef coral mortality for which causal agents have not been definitively identified. Here we use culture-independent molecular techniques (DGGE and clone libraries) to characterize ciliate and bacterial communities in these diseases. Bacterial (16S rRNA gene) and ciliate (18S rRNA gene) communities were highly similar between the two diseases. Four bacterial and nine ciliate ribotypes were observed in both diseases, but absent in non-diseased specimens. Only one of the bacteria, Arcobacter sp. (JF831360) increased substantially in relative 16S rRNA gene abundance and was consistently represented in all diseased samples. Four of the eleven ciliate morphotypes detected contained coral algal symbionts, indicative of the ingestion of coral tissues. In both WS and BrB, there were two ciliate morphotypes consistently represented in all disease lesion samples. Morph1 (JN626268) was observed to burrow into and underneath the coral tissues at the lesion boundary. Morph2 (JN626269), previously identified in BrB, appears to play a secondary, less invasive role in pathogenesis, but has a higher population density in BrB, giving rise to the visible brown band. The strong similarity in bacterial and ciliate community composition of these diseases suggests that they are actually the same syndrome.

Surface flow for colonial integration in reef-building corals.

Reef-building corals are endangered animals with a complex colonial organization. Physiological mechanisms connecting multiple polyps and integrating them into a coral colony are still enigmatic. Using live imaging, particle tracking, and mathematical modeling, we reveal how corals connect individual polyps and form integrated polyp groups via species-specific, complex, and stable networks of currents at their surface. These currents involve surface mucus of different concentrations, which regulate joint feeding of the colony. Inside the coral, within the gastrovascular system, we expose the complexity of bidirectional branching streams that connect individual polyps. This system of canals extends the surface area by 4-fold and might improve communication, nutrient supply, and symbiont transfer. Thus, individual polyps integrate via complex liquid dynamics on the surface and inside the colony.

Levels of immunity parameters underpin bleaching and disease susceptibility of reef corals.

Immunity is a key life history trait that may explain hierarchies in the susceptibility of corals to disease and thermal bleaching, two of the greatest current threats to coral health and the persistence of tropical reefs. Despite their ongoing and rapid global decline, there have been few investigations into the immunity mechanisms of reef-building corals. Variables commonly associated with invertebrate immunity, including the presence of melanin, size of melanin-containing granular cells, and phenoloxidase (PO) activity, as well as concentrations of fluorescent proteins (FPs), were investigated in hard (Scleractinia) and soft (Alcyonacea) corals spanning 10 families from the Great Barrier Reef. Detectable levels of these indicators were present in all corals investigated, although relative investment differed among coral taxa. Overall levels of investment were inversely correlated to thermal bleaching and disease susceptibility. In addition, PO activity, melanin-containing granular cell size, and FP concentration were each found to be significant predictors of susceptibility and thus may play key roles in coral immunity. Correlative evidence that taxonomic (family-level) variation in the levels of these constituent immunity parameters underpins susceptibility to both thermal bleaching and disease indicates that baseline immunity underlies the vulnerability of corals to these two threats. This reinforces the necessity of a holistic approach to understanding bleaching and disease in order to accurately determine the resilience of coral reefs.

Photogrammetry as a tool to improve ecosystem restoration.

Ecosystem restoration has been practiced for over a century and is increasingly supported by the emergent applied science of restoration ecology. A prerequisite for successful ecosystem restoration is determining meaningful and measurable goals. This requires tools to monitor success in a standardized way. Photogrammetry uses images to reconstruct landscapes and organisms in three dimensions, enabling non-invasive measurement of key success indicators with unprecedented accuracy. We propose photogrammetry can improve restoration success by: (i) facilitating measurable goals; (ii) innovating and standardizing indicators of success; and (iii) standardizing monitoring. While the case we present is specific to coral reefs, photogrammetry has enormous potential to improve restoration practice in a wide range of ecosystems.

Coral mucus: the properties of its constituent mucins.

The gel-forming properties of mucus are closely related to its functioning; although there is limited information available relating to coral mucus gels. The present study investigates coral mucus glycoprotein using rheological methods. We demonstrate the presence of a high-molecular-weight polymeric glycoprotein similar to that found in vertebrates, capable of forming a gel. The milked mucus exuded mostly from the oral cavity of corals is not a gel; however, it does show a tendency to form a gel upon concentration. Such results indicate the potential for corals to produce two different kinds of mucus, each potentially capable of performing different functions.

Equistatin and equinatoxin gene expression is influenced by environmental temperature in the sea anemone Actinia equina.

We examined the gene expression levels of equinatoxin and equistatin in the sea anemone Actinia equina, when reared at varying environmental temperatures for five months. Both genes were significantly downregulated at 10 °C compared to 16 °C but showed no significant change at 22 °C. This provides the first evidence of an effect of temperature on gene expression, but with no effect of increasing temperatures such as those predicted due to climate change.

Do reef corals age?

Hydra is emerging as a model organism for studies of ageing in early metazoan animals, but reef corals offer an equally ancient evolutionary perspective as well as several advantages, not least being the hard exoskeleton which provides a rich fossil record as well as a record of growth and means of ageing of individual coral polyps. Reef corals are also widely regarded as potentially immortal at the level of the asexual lineage and are assumed not to undergo an intrinsic ageing process. However, putative molecular indicators of ageing have recently been detected in reef corals. While many of the large massive coral species attain considerable ages (>600 years) there are other much shorter-lived species where older members of some populations show catastrophic mortality, compared to juveniles, under environmental stress. Other studies suggestive of ageing include those demonstrating decreased reproduction, increased susceptibility to oxidative stress and disease, reduced regeneration potential and declining growth rate in mature colonies. This review aims to promote interest and research in reef coral ageing, both as a useful model for the early evolution of ageing and as a factor in studies of ecological impacts on reef systems in light of the enhanced effects of environmental stress on ageing in other organisms.

Evolutionary conservation of the antimicrobial function of mucus: a first defence against infection.

Mucus layers often provide a unique and multi-functional hydrogel interface between the epithelial cells of organisms and their external environment. Mucus has exceptional properties including elasticity, changeable rheology and an ability to self-repair by re-annealing, and is therefore an ideal medium for trapping and immobilising pathogens and serving as a barrier to microbial infection. The ability to produce a functional surface mucosa was an important evolutionary step, which evolved first in the Cnidaria, which includes corals, and the Ctenophora. This allowed the exclusion of non-commensal microbes and the subsequent development of the mucus-lined digestive cavity seen in higher metazoans. The fundamental architecture of the constituent glycoprotein mucins is also evolutionarily conserved. Although an understanding of the biochemical interactions between bacteria and the mucus layer are important to the goal of developing new antimicrobial strategies, they remain relatively poorly understood. This review summarises the physicochemical properties and evolutionary importance of mucus, which make it so successful in the prevention of bacterial infection. In addition, the strategies developed by bacteria to counteract the mucus layer are also explored.

Bacterial community structure associated with white band disease in the elkhorn coral Acropora palmata determined using culture-independent 16S rRNA techniques.

Culture-independent molecular (16S ribosomal RNA) techniques showed distinct differences in bacterial communities associated with white band disease (WBD) Type I and healthy elkhorn coral Acropora palmata. Differences were apparent at all levels, with a greater diversity present in tissues of diseased colonies. The bacterial community associated with remote, non-diseased coral was distinct from the apparently healthy tissues of infected corals several cm from the disease lesion. This demonstrates a whole-organism effect from what appears to be a localised disease lesion, an effect that has also been recently demonstrated in white plague-like disease in star coral Montastraea annularis. The pattern of bacterial community structure changes was similar to that recently demonstrated for white plague-like disease and black band disease. Some of the changes are likely to be explained by the colonisation of dead and degrading tissues by a micro-heterotroph community adapted to the decomposition of coral tissues. However, specific ribosomal types that are absent from healthy tissues appear consistently in all samples of each of the diseases. These ribotypes are closely related members of a group of alpha-proteobacteria that cause disease, notably juvenile oyster disease, in other marine organisms. It is clearly important that members of this group are isolated for challenge experiments to determine their role in the diseases.

Baseline coral disease surveys within three marine parks in Sabah, Borneo.

Two of the most significant threats to coral reefs worldwide are bleaching and disease. However, there has been a scarcity of research on coral disease in South-East Asia, despite the high biodiversity and the strong dependence of local communities on the reefs in the region. This study provides baseline data on coral disease frequencies within three national parks in Sabah, Borneo, which exhibit different levels of human impacts and management histories. High mean coral cover (55%) and variable disease frequency (mean 0.25 diseased colonies m(-2)) were found across the three sites. Highest disease frequency (0.44 diseased colonies per m(2)) was seen at the site closest to coastal population centres. Bleaching and pigmentation responses were actually higher at Sipadan, the more remote, offshore site, whereas none of the other coral diseases detected in the other two parks were detected in Sipadan. Results of this study offer a baseline dataset of disease in these parks and indicate the need for continued monitoring, and suggest that coral colonies in parks under higher anthropogenic stressors and with lower coral cover may be more susceptible to contracting disease.

Microbial communities associated with healthy and White syndrome-affected Echinopora lamellosa in aquaria and experimental treatment with the antibiotic ampicillin.

Prokaryotic and ciliate communities of healthy and aquarium White Syndrome (WS)-affected coral fragments were screened using denaturing gradient gel electrophoresis (DGGE). A significant difference (R = 0.907, p < 0.001) in 16S rRNA prokaryotic diversity was found between healthy (H), sloughed tissue (ST), WS-affected (WSU) and antibiotic treated (WST) samples. Although 3 Vibrio spp were found in WS-affected samples, two of these species were eliminated following ampicillin treatment, yet lesions continued to advance, suggesting they play a minor or secondary role in the pathogenesis. The third Vibrio sp increased slightly in relative abundance in diseased samples and was abundant in non-diseased samples. Interestingly, a Tenacibaculum sp showed the greatest increase in relative abundance between healthy and WS-affected samples, demonstrating consistently high abundance across all WS-affected and treated samples, suggesting Tenacibaculum sp could be a more likely candidate for pathogenesis in this instance. In contrast to previous studies bacterial abundance did not vary significantly (ANOVA, F2, 6 = 1.000, p = 0.422) between H, ST, WSU or WST. Antimicrobial activity (assessed on Vibrio harveyi cultures) was limited in both H and WSU samples (8.1% ±8.2 and 8.0% ±2.5, respectively) and did not differ significantly (Kruskal-Wallis, χ2 (2) = 3.842, p = 0.146). A Philaster sp, a Cohnilembus sp and a Pseudokeronopsis sp. were present in all WS-affected samples, but not in healthy samples. The exact role of ciliates in WS is yet to be determined, but it is proposed that they are at least responsible for the neat lesion boundary observed in the disease.

Algae as reservoirs for coral pathogens.

Benthic algae are associated with coral death in the form of stress and disease. It's been proposed that they release exudates, which facilitate invasion of potentially pathogenic microbes at the coral-algal interface, resulting in coral disease. However, the original source of these pathogens remains unknown. This study examined the ability of benthic algae to act as reservoirs of coral pathogens by characterizing surface associated microbes associated with major Caribbean and Indo-Pacific algal species/types and by comparing them to potential pathogens of two dominant coral diseases: White Syndrome (WS) in the Indo-Pacific and Yellow Band Disease (YBD) in the Caribbean. Coral and algal sampling was conducted simultaneously at the same sites to avoid spatial effects. Potential pathogens were defined as those absent or rare in healthy corals, increasing in abundance in healthy tissues adjacent to a disease lesion, and dominant in disease lesions. Potentially pathogenic bacteria were detected in both WS and YBD and were also present within the majority of algal species/types (54 and 100% for WS and YBD respectively). Pathogenic ciliates were associated only with WS and not YBD lesions and these were also present in 36% of the Indo-Pacific algal species. Although potential pathogens were associated with many algal species, their presence was inconsistent among replicate algal samples and detection rates were relatively low, suggestive of low density and occurrence. At the community level, coral-associated microbes irrespective of the health of their host differed from algal-associated microbes, supporting that algae and corals have distinctive microbial communities associated with their tissue. We conclude that benthic algae are common reservoirs for a variety of different potential coral pathogens. However, algal-associated microbes alone are unlikely to cause coral death. Initial damage or stress to the coral via other competitive mechanisms is most likely a prerequisite to potential transmission of these pathogens.

Evidence of melanoma in wild marine fish populations.

The increase in reports of novel diseases in a wide range of ecosystems, both terrestrial and marine, has been linked to many factors including exposure to novel pathogens and changes in the global climate. Prevalence of skin cancer in particular has been found to be increasing in humans, but has not been reported in wild fish before. Here we report extensive melanosis and melanoma (skin cancer) in wild populations of an iconic, commercially-important marine fish, the coral trout Plectropomus leopardus. The syndrome reported here has strong similarities to previous studies associated with UV induced melanomas in the well-established laboratory fish model Xiphophorus. Relatively high prevalence rates of this syndrome (15%) were recorded at two offshore sites in the Great Barrier Reef Marine Park (GBRMP). In the absence of microbial pathogens and given the strong similarities to the UV-induced melanomas, we conclude that the likely cause was environmental exposure to UV radiation. Further studies are needed to establish the large scale distribution of the syndrome and confirm that the lesions reported here are the same as the melanoma in Xiphophorus, by assessing mutation of the EGFR gene, Xmrk. Furthermore, research on the potential links of this syndrome to increases in UV radiation from stratospheric ozone depletion needs to be completed.

Development of bacterial biofilms on artificial corals in comparison to surface-associated microbes of hard corals.

Numerous studies have demonstrated the differences in bacterial communities associated with corals versus those in their surrounding environment. However, these environmental samples often represent vastly different microbial micro-environments with few studies having looked at the settlement and growth of bacteria on surfaces similar to corals. As a result, it is difficult to determine which bacteria are associated specifically with coral tissue surfaces. In this study, early stages of passive settlement from the water column to artificial coral surfaces (formation of a biofilm) were assessed. Changes in bacterial diversity (16S rRNA gene), were studied on artificially created resin nubbins that were modelled from the skeleton of the reef building coral Acropora muricata. These models were dip-coated in sterile agar, mounted in situ on the reef and followed over time to monitor bacterial community succession. The bacterial community forming the biofilms remained significantly different (R = 0.864 p<0.05) from that of the water column and from the surface mucus layer (SML) of the coral at all times from 30 min to 96 h. The water column was dominated by members of the α-proteobacteria, the developed community on the biofilms dominated by γ-proteobacteria, whereas that within the SML was composed of a more diverse array of groups. Bacterial communities present within the SML do not appear to arise from passive settlement from the water column, but instead appear to have become established through a selection process. This selection process was shown to be dependent on some aspects of the physico-chemical structure of the settlement surface, since agar-coated slides showed distinct communities to coral-shaped surfaces. However, no significant differences were found between different surface coatings, including plain agar and agar enhanced with coral mucus exudates. Therefore future work should consider physico-chemical surface properties as factors governing change in microbial diversity.