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.

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.

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.

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.

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.

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.

Corals use similar immune cells and wound-healing processes as those of higher organisms.

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.

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.

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.

Vertical distribution and diel patterns of zooplankton abundance and biomass at Conch Reef, Florida Keys (USA).

Zooplankton play an important role in the trophic dynamics of coral reef ecosystems. Detailed vertical and temporal distribution and biomass of zooplankton were evaluated at four heights off the bottom and at six times throughout the diel cycle over a coral reef in the Florida Keys (USA). Zooplankton abundance averaged 4396 +/- 1949 SD individuals m(-3), but temporal and spatial distributions varied for individual zooplankton taxa by time of day and by height off the bottom. Copepods comprised 93-96% of the abundance in the samples. Taxon-based zooplankton CHN values paired with abundance data were used to estimate biomass. Average daily biomass ranged from 3.1 to 21.4 mg C m(-3) and differed by both height off the bottom and by time of day. While copepods were the numerically dominant organisms, their contribution to biomass was only 35% of the total zooplankton biomass. Our findings provide important support for the new emerging paradigm of how zooplankton are distributed over reefs.

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.

The bacterial ecology of a plague-like disease affecting the Caribbean coral Montastrea annularis.

The bacterial communities associated with the Caribbean coral Montastrea annularis showing tissue lesions indicative of a White Plague (WP)-like disease were investigated. Two molecular screening techniques using bacterial 16S rDNA genes were used and demonstrated distinct differences between the bacterial communities of diseased and non-diseased coral tissues, and also in relation to the proximity of tissue lesions on diseased corals. Differences between non-diseased corals and the apparently healthy tissues remote from the tissue lesion in affected corals indicates a 'whole coral' response to a relatively small area of infection with a perturbation in the normal microbial flora occurring prior to the onset of visible signs of disease. These whole organism changes in the microbial flora may serve as a bioindicator of environmental stress and disease. There were striking similarities between the 16S rDNA sequence composition associated with the WP-like disease studied here and that previously reported in association with black band disease (BBD) in coral. Similarities included the presence of a potential pathogen, an alpha-proteobacterium identified as the causal agent of juvenile oyster disease (JOD). The WP-like disease studied here is apparently different to WP Type ii because the bacterial species previously identified as the causal agent of WP Type ii was not detected, although the symptoms of the two diseases are similar.

Characterization of the bacterial consortium associated with black band disease in coral using molecular microbiological techniques.

The bacterial community associated with black band disease (BBD) of the scleractinian corals Diploria strigosa, Montastrea annularis and Colpophyllia natans was examined using culture-independent techniques. Two complementary molecular screening techniques of 16S rDNA genes [amplified 16S ribosomal DNA restriction analysis (ARDRA) of clone libraries and denaturing gradient gel electrophoresis (DGGE)] were used to give a comprehensive characterization of the community. Findings support previous studies indicating low bacterial abundance and diversity associated with healthy corals. A single cyanobacterial ribotype was present in all the diseased samples, but this was not the same as that identified from Phormidium corallyticum culture isolated from BBD. The study confirms the presence of Desulfovibrio spp. and sulphate-reducing bacteria that have previously been associated with the BBD consortium. However, the species varied between diseased coral samples. We found no evidence of bacteria from terrestrial, freshwater or human sources in any of the samples. We report the presence of previously unrecognized potential pathogens [a Cytophaga sp. and an alpha-proteobacterium identified as the aetiological agent of juvenile oyster disease (JOD)] that were consistently present in all the diseased coral samples. The molecular biological approach described here gives an increasingly comprehensive and more precise picture of the bacterial population associated with BBD. To understand the pathogenesis of BBD, our attention should be focused on the pervasive ribotypes identified in this study (the Cyanobacterium sp., the Cytophaga sp. and the JOD pathogen).