Differential spatio-temporal responses of Red Sea coral reef benthic communities to a mass bleaching event.

Understanding how coral reefs respond to disturbances is fundamental to assessing their resistance and resilience, particularly in the context of climate change. Due to the escalating frequency and intensity of coral bleaching events, it is essential to evaluate spatio-temporal responses of coral reef communities to disentangle the mechanisms underlying ecological changes. Here, we used benthic data collected from 59 reefs in the Red Sea over five years (2014-2019), a period that encompasses the 2015/2016 mass bleaching event. Reefs were located within three different geographic regions with different environmental settings: north (Duba; Al Wajh), central (Jeddah; Thuwal), and south (Al Lith; Farasan Banks; Farasan Islands). Coral community responses were region-specific, with communities in the south being more promptly affected than those in the northern and central regions, with hard and soft coral cover dropping drastically in several reefs from around > 40% to < 5% two years after bleaching. Coral bleaching effects were particularly evident in the decrease of cover in branching corals. Overall, we documented a shift towards a dominance of macroalgae, turf algae, and crustose coralline algae (CCA). Using remote sensing data, we analyzed sea surface temperature (SST) regimes at the study sites to infer potential drivers of changes in benthic composition. Both SST and Degree Heating Weeks (DHW) only partially aligned with the responses of benthic communities, highlighting the need for more accurate predictors of coral bleaching in the Red Sea. In times of intense coastal development along Saudi Arabia's Red Sea coast, our study provides crucial baseline information on developments in coral reef community composition, as well as to guide decision-making, namely restoration efforts.

Replayed reef sounds induce settlement of Favia fragum coral larvae in aquaria and field environmentsa).

Acoustic cues of healthy reefs are known to support critical settlement behaviors for one reef-building coral, but acoustic responses have not been demonstrated in additional species. Settlement of Favia fragum larvae in response to replayed coral reef soundscapes were observed by exposing larvae in aquaria and reef settings to playback sound treatments for 24-72 h. Settlement increased under 24 h sound treatments in both experiments. The results add to growing knowledge that acoustically mediated settlement may be widespread among stony corals with species-specific attributes, suggesting sound could be one tool employed to rehabilitate and build resilience within imperiled reef communities.

Polyamine impact on physiology of early stages of reef-building corals-insights from rearing experiments and RNA-Seq analysis.

Polyamines are involved in various functions related to the cellular-level responses. To assess effects of polyamines on marine organisms, rearing experiments and comprehensive gene expression analyses were conducted on Acropora digitifera and Acropora sp.1, representative reef-building corals along the west-central coast of Okinawa, Japan, to evaluate effects of putrescine. Concentrations of putrescine ≥ 1 mM dissolved tissues of juvenile polyps and increased mortality of planula larvae. RNA-Seq analysis of juvenile polyps exposed to putrescine at the stage before effects became visible revealed dynamic fluctuations in gene expression in the putrescine-treated samples, with increased expression of stress-responsive genes (e.g. NAD-dependent protein deacylase sirtuin-6) and the polyamine transporter Slc18b1-like protein. These results also suggest that putrescine affects expression of genes related to ribosomes and translation. This study provides important insights into roles of polyamines and future directions regarding physiological responses of corals.

Regime shift of skeletal δ13C after 1997/1998 El Nino event in Porites coral from Green Island, Taiwan.

The 1997/1998 El Niño event caused mass coral bleaching and mortality in many tropical and subtropical regions, including corals on Green Island, Taiwan, in the northwestern Pacific Ocean. This study analyzed coral carbon isotope ratios (δ13C), oxygen isotope ratios (δ18O), and Sr/Ca ratios for 29 years, including the 1997/1998 El Niño period, to examine how high water temperature events are recorded in coral geochemical indicators. Sr/Ca ratios in coral skeletons from Green Island show the lowest peak, means the highest temperature during the 1997/1998 El Niño period. However, we couldn't observe high-temperature events on δ18O. Furthermore, a negative δ13C shift was observed after El Niño events. The regime shift of δ13C might have been caused by temporal bleaching and/or a decrease in symbiotic algae due to high water temperature stress under the continuous decrease in δ13C in DIC due to the Suess effect.

Coral responses to a catastrophic marine heatwave are decoupled from changes in total coral cover at a continental scale.

The services provided by the world's coral reefs are threatened by increasingly frequent and severe marine heatwaves. Heatwave-induced degradation of reefs has often been inferred from the extent of the decline in total coral cover, which overlooks extreme variation among coral taxa in their susceptibility and responses to thermal stress. Here, we provide a continental-scale assessment of coral cover changes at 262 shallow tropical reef sites around Australia, using ecological survey data on 404 coral taxa before and after the 2016 mass bleaching event. A strong spatial structure in coral community composition along large-scale environmental gradients largely dictated how coral communities responded to heat stress. While heat stress variables were the best predictors of change in total coral cover, the pre-heatwave community composition best predicted the temporal beta-diversity index (an indicator of change in community composition over time). Indicator taxa in each coral community differed before and after the heatwave, highlighting potential winners and losers of climate-driven coral bleaching. Our results demonstrate how assessment of change in total cover alone may conceal very different responses in community structure, some of which showed strong regional consistency, and may provide a telling outlook of how coral reefs may reorganize in a warmer future.

Inshore coral reef sediment and turf dynamics unaffected by canopy-forming macroalgae.

Nearshore coral reefs face an increasing abundance of fleshy macroalgae, an indicator of degradation and threat to ecosystem functioning. Removal of macroalgae is proposed to assist coral recovery, though the ecological and physical impacts have not been studied. Nearshore reefs are also confronted with sedimentation stress, influencing reef dynamics including algal turfs, with flow-on impacts to coral recruitment, fish diets, and trophic cascades. In this study, the interplay between macroalgal canopies, sediment deposition and algal turf environments was investigated on the nearshore Great Barrier Reef. Removal of fleshy macroalgae over two years had no significant effect on the amount or composition of sediment deposited on proxy coral (SedPods) and algal turf (TurfPods) surfaces, nor was the height of algal turfs impacted. Deposition on TurfPods was greater with high-energy currents, likely due to retention of sediment within turfs. Therefore, macroalgae removal is unlikely to exacerbate nor alleviate sediment-related stress on benthic communities.

Selective breeding enhances coral heat tolerance to marine heatwaves.

Marine heatwaves are becoming more frequent, widespread and severe, causing mass coral bleaching and mortality. Natural adaptation may be insufficient to keep pace with climate warming, leading to calls for selective breeding interventions to enhance the ability of corals to survive such heatwaves, i.e., their heat tolerance. However, the heritability of this trait-a prerequisite for such approaches-remains unknown. We show that selecting parent colonies for high rather than low heat tolerance increased the tolerance of adult offspring (3-4-year-olds). This result held for the response to both 1-week +3.5 °C and 1-month +2.5 °C simulated marine heatwaves. In each case, narrow-sense heritability (h2) estimates are between 0.2 and 0.3, demonstrating a substantial genetic basis of heat tolerance. The phenotypic variability identified in this population could theoretically be leveraged to enhance heat tolerance by up to 1 °C-week within one generation. Concerningly, selective breeding for short-stress tolerance did not improve the ability of offspring to survive the long heat stress exposure. With no genetic correlation detected, these traits may be subject to independent genetic controls. Our finding on the heritability of coral heat tolerance indicates that selective breeding could be a viable tool to improve population resilience. Yet, the moderate levels of enhancement we found suggest that the effectiveness of such interventions also demands urgent climate action.

Coral Community Composition Linked to Hypoxia Exposure.

Tropical reef ecosystems are strongly influenced by the composition of coral species, but the factors influencing coral diversity and distributions are not fully understood. Here we demonstrate that large variations in the relative abundance of three major coral species across adjacent Caribbean reef sites are strongly related to their different low O2 tolerances. In laboratory experiments designed to mimic reef conditions, the cumulative effect of repeated nightly low O2 drove coral bleaching and mortality, with limited modulation by temperature. After four nights of repeated low O2, species responses also varied widely, from > 50% bleaching in Acropora cervicornis to no discernable sensitivity of Porites furcata. A simple metric of hypoxic pressure that combines these experimentally derived species sensitivities with high-resolution field data accurately predicts the observed relative abundance of species across three reefs. Only the well-oxygenated reef supported the framework-building hypoxia-sensitive Acropora cervicornis, while the hypoxia-tolerant weedy species Porites furcata was dominant on the most frequently O2-deplete reef. Physiological exclusion of acroporids from these O2-deplete reefs underscores the need for hypoxia management to reduce extirpation risk.

Coral growth along a natural gradient of seawater temperature, pH, and oxygen in a nearshore seagrass bed on Dongsha Atoll, Taiwan.

Coral reefs are facing threats from a variety of global change stressors, including ocean warming, acidification, and deoxygenation. It has been hypothesized that growing corals near primary producers such as macroalgae or seagrass may help to ameliorate acidification and deoxygenation stress, however few studies have explored this effect in situ. Here, we investigated differences in coral growth rates across a natural gradient in seawater temperature, pH, and dissolved oxygen (DO) variability in a nearshore seagrass bed on Dongsha Atoll, Taiwan, South China Sea. We observed strong spatial gradients in temperature (5°C), pH (0.29 pH units), and DO (129 µmol O2 kg-1) across the 1-kilometer wide seagrass bed. Similarly, diel variability recorded by an autonomous sensor in the shallow seagrass measured diel ranges in temperature, pH, and DO of up to 2.6°C, 0.55, and 204 µmol O2 kg-1, respectively. Skeletal cores collected from 15 massive Porites corals growing in the seagrass bed at 4 sites revealed no significant differences in coral calcification rates between sites along the gradients. However, significant differences in skeletal extension rate and density suggest that the dynamic temperature, pH, and/or DO variability may have influenced these properties. The lack of differences in coral growth between sites may be because favorable calcification conditions during the day (high temperature, pH, and DO) were proportionally balanced by unfavorable conditions during the night (low temperature, pH, and DO). Alternatively, other factors were simply more important in controlling coral calcification and/or corals were acclimated to the prevailing conditions at each site.

Capturing fine-scale coral dynamics with a metacommunity modelling framework.

Natural systems exhibit high spatial variability across multiple scales. Models that can capture ecosystem dynamics across space and time by explicitly incorporating major biological mechanisms are crucial, both for management and for ecological insight. In the case of coral reef systems, much focus has been on modelling variability between reefs, despite substantial variability also existing within reefs. We developed C~scape, a coral metacommunity modelling framework that integrates the demography of corals with population-level responses to physical and environmental spatial layers, to facilitate spatiotemporal predictions of coral dynamics across reefs at fine (100s of metres to kilometres) scales. We used satellite-derived habitat maps to modulate community growth spatially, as a proxy for the many interacting physical and environmental factors-e.g., depth, light, wave exposure, temperature, and substrate type-that drive within-reef variability in coral demography. With a case study from the Great Barrier Reef, we demonstrate the model's capability for producing hindcasts of coral cover dynamics and show that overlooking within-reef variability may lead to misleading conclusions about metacommunity dynamics. C~scape provides a valuable framework for exploring a range of management and restoration scenarios at relevant spatial scales.

A generalized numerical model for clonal growth in scleractinian coral colonies.

Coral reefs, vital ecosystems supporting diverse marine life, are primarily shaped by the clonal expansion of coral colonies. Although the principles of coral clonal growth, involving polyp division for spatial extension, are well-understood, numerical modelling efforts are notably scarce in the literature. In this article, we present a parsimonious numerical model based on the cloning of polyps, using five key parameters to simulate a range of coral shapes. The model is agent-based, where each polyp represents an individual. The colony's surface expansion is dictated by the growth mode parameter (s), guiding the preferred growth direction. Varying s facilitates the emulation of diverse coral shapes, including massive, branching, cauliflower, columnar and tabular colonies. Additionally, we introduce a novel approach for self-regulatory branching, inspired by the intricate mesh-like canal system and internode regularity observed in Acropora species. Through a comprehensive sensitivity analysis, we demonstrate the robustness of our model, paving the way for future applications that incorporate environmental factors, such as light and water flow. Coral colonies are known for their high plasticity, and understanding how individual polyps interact with each other and their surroundings to create the reef structure has been a longstanding question in the field. This model offers a powerful framework for studying these interactions, enabling a future implementation of environmental factors and the possibility of identifying the key mechanisms influencing coral colonies' morphogenesis.

Climate adaptive loci revealed by seascape genomics correlate with phenotypic variation in heat tolerance of the coral Acropora millepora.

One of the main challenges in coral reef conservation and restoration is the identification of coral populations resilient under global warming. Seascape genomics is a powerful tool to uncover genetic markers potentially involved in heat tolerance among large populations without prior information on phenotypes. Here, we aimed to provide first insights on the role of candidate heat associated loci identified using seascape genomics in driving the phenotypic response of Acropora millepora from New Caledonia to thermal stress. We subjected 7 colonies to a long-term ex-situ heat stress assay (4 °C above the maximum monthly mean) and investigated their physiological response along with their Symbiodiniaceae communities and genotypes. Despite sharing similar thermal histories and associated symbionts, these conspecific individuals differed greatly in their tolerance to heat stress. More importantly, the clustering of individuals based on their genotype at heat-associated loci matched the phenotypic variation in heat tolerance. Colonies that sustained on average lower mortality, higher Symbiodiniaceae/chlorophyll concentrations and photosynthetic efficiency under prolonged heat stress were also the closest based on their genotypes, although the low sample size prevented testing loci predictive accuracy. Together these preliminary results support the relevance of coupling seascape genomics and long-term heat stress experiments in the future, to evaluate the effect size of candidate heat associated loci and pave the way for genomic predictive models of corals heat tolerance.

Thermal tolerance traits of individual corals are widely distributed across the Great Barrier Reef.

Adaptation of reef-building corals to global warming depends upon standing heritable variation in tolerance traits upon which selection can act. Yet limited knowledge exists on heat-tolerance variation among conspecific individuals separated by metres to hundreds of kilometres. Here, we performed standardized acute heat-stress assays to quantify the thermal tolerance traits of 709 colonies of Acropora spathulata from 13 reefs spanning 1060 km (9.5° latitude) of the Great Barrier Reef. Thermal thresholds for photochemical efficiency and chlorophyll retention varied considerably among individual colonies both among reefs (approximately 6°C) and within reefs (approximately 3°C). Although tolerance rankings of colonies varied between traits, the most heat-tolerant corals (i.e. top 25% of each trait) were found at virtually all reefs, indicating widespread phenotypic variation. Reef-scale environmental predictors explained 12-62% of trait variation. Corals exposed to high thermal averages and recent thermal stress exhibited the greatest photochemical performance, probably reflecting local adaptation and stress pre-acclimatization, and the lowest chlorophyll retention suggesting stress pre-sensitization. Importantly, heat tolerance relative to local summer temperatures was the greatest on higher latitude reefs suggestive of higher adaptive potential. These results can be used to identify naturally tolerant coral populations and individuals for conservation and restoration applications.

Predicting 3D and 2D surface area of corals from simple field measurements.

The structural architecture of coral reefs is a known predictor of species richness, fish biomass and reef resilience. At a smaller scale, three-dimensional (3D) surface area of corals is a fundamental determinant of physical and biological processes. Quantifying the 3D surface area of corals has applications for a broad range of scientific disciplines, including carbonate production estimates, coral predation studies, and assessments of reef growth. Here, we present morphotaxon-specific conversion metrics to estimate total 3D surface area and projected 2D surface area of individual colonies from simple field measurements of colony maximum diameter. Underwater photogrammetry techniques were used to quantify surface area and estimate conversion metrics. Bayesian models showed strong non-linear (power) relationships between colony maximum diameter and both total 3D surface area and projected 2D surface area for 13 out of 15 morphotaxa. This study presents a highly resolved and efficient method for obtaining critical surface area assessments of corals for various applications, including assessments of biotic surface area, tissue biomass, calcification rates, coral demographic rates, and reef restoration monitoring.

The stony coral Fimbriaphyllia (Euphyllia) ancora's reproductive strategy involves a sex change every year.

A sex change phenomenon was reported in some free-living, non-sessile coral species of the Family Fungiidae. However, there are no reports describing sex change in sessile colonial species. Timing and cellular processes of sex change are also unclear in corals. Here, we report sex change of the colonial coral, Fimbriaphyllia ancora, and its cellular process. Of 26 colonies monitored at Nanwan Bay, southern Taiwan, about 70% changed their sex every year after annual spawning for least 3-4 consecutive years, i.e., colonies that were male two years ago became female last year, and male again this year. The remaining 30% were permanently male or female. Sex-change and non-sex-change colonies grew in close proximity or even side-by-side. No significant differences were found in colony size between sex-change and non-sex-change colonies. Histological analysis showed that, in female-to-male sex change, small oocytes were present up to 3 months in some gonads after spawning and disappeared by 5 months. This suggests that sex change occurred 4-5 months after spawning. In contrast, in male-to-female sex change, oocytes appeared weeks after sperm release and in most gonads by 3 months, suggesting that male-to-female sex change occurred 0-3 months after sperm release.

The role of mesoscale-driven connectivity patterns in coral recovery around Moorea and Tahiti, French Polynesia.

Coral reefs are declining due to anthropogenic warming. Nonetheless, some have recovered quickly from repeated bleaching events. Coral recovery depends on adaptation capabilities, fishing pressure, overall number of stressors, reef conditions before the event, and degree of connectivity. Coral reefs that are connected to many others can receive viable larvae and regain coverage faster. Around Moorea and Tahiti, within the Society Islands of French Polynesia, coral cover has regained its previous levels rapidly, despite several mass bleaching events over the past three decades. Here it is explored whether the connectivity with distant reefs may support such recovery by modeling the transport of coral larvae around the islands over 28 years. Ocean currents enable connectivity with the Tuamotu Islands, ~ 250 km to the northeast, that act as sources to Moorea and Tahiti for pelagic larval durations of three weeks or longer. The circulation around Moorea and Tahiti is very dynamic; mesoscale eddies can also halt the connectivity with the Tuamotu Islands and sporadically transport larvae from reefs to the west and southeast instead. With many undisturbed coral reefs within a 300 km radius and strong mesoscale variability, a dynamic, long-range connectivity may explain the recovery of reefs around Moorea and Tahiti.

Gene expression plasticity governing symbiosis during natural coral bleaching.

The increasing global frequency and severity of coral bleaching events, driven by the loss of endosymbiotic algae, pose a significant threat to these vital ecosystems. However, gene expression plasticity offers a potential mechanism for rapid and effective acclimatization to environmental changes. We employed dual transcriptomics to examine the gene expression profile of Seriatopora hystrix, an ecologically important scleractinian coral, across healthy, mildly bleached, and severely bleached colonies collected from the waters of Likupang, North Sulawesi, Indonesia. Our analysis revealed that coral bleaching is associated with gene plasticity in calcium signaling and focal adhesion within coral hosts, as well as with endoplasmic reticulum stress in symbionts. Notably, we identified specific genes associated with innate immunity that were predominantly overexpressed in mildly bleached coral hosts. This overexpression implies that high expression plasticity of these key genes might contribute to bleaching resistance and the preservation of the host-symbiont relationship. Our findings offer a detailed insight into the dynamics of bleaching resistance in S. hystrix, shedding light on the variability of bleaching risks in Indonesian reefs and underscoring the coral's ability to utilize gene expression plasticity for immediate survival and potential long-term adaptation to climate changes.

Not-so-mutually beneficial coral symbiosis.

The partnership between corals and their intracellular algal symbionts has long been a textbook example of a mutually beneficial association. Here I argue that this view has been made obsolete by a steady accumulation of evidence over the past three decades. The coral-algal relationship is perhaps better viewed as one of domestication - think of it like a cattle farm, in which the coral is the farmer and the algae are the cows. I synthesize old and new evidence in support of this updated view and highlight remaining knowledge gaps, the largest of which continues to be the natural history of algal symbionts.

Changing disturbance regimes, material legacies, and stabilizing feedbacks: Dead coral skeletons impair key recovery processes following coral bleaching.

Ecosystem responses to disturbance depend on the nature of the perturbation and the ecological legacies left behind, making it critical to understand how climate-driven changes in disturbance regimes modify resilience properties of ecosystems. For coral reefs, recent increases in severe marine heat waves now co-occur with powerful storms, the historic agent of disturbance. While storms kill coral and remove their skeletons, heat waves bleach and kill corals but leave their skeletons intact. Here, we explored how the material legacy of dead coral skeletons modifies two key ecological processes that underpin coral reef resilience: the ability of herbivores to control macroalgae (spatial competitors of corals), and the replenishment of new coral colonies. Our findings, grounded by a major bleaching event at our long-term study locale, revealed that the presence of structurally complex dead skeletons reduced grazing on turf algae by ~80%. For macroalgae, browsing was reduced by >40% on less preferred (unpalatable) taxa, but only by ~10% on more preferred taxa. This enabled unpalatable macroalgae to reach ~45% cover in 2 years. By contrast, herbivores prevented macroalgae from becoming established on adjacent reefs that lacked skeletons. Manipulation of unpalatable macroalgae revealed that the cover reached after 1 year (~20%) reduced recruitment of corals by 50%. The effect of skeletons on juvenile coral growth was contingent on the timing of settlement relative to the disturbance. If corals settled directly after bleaching (before macroalgae colonized), dead skeletons enhanced colony growth by 34%, but this benefit was lost if corals colonized dead skeletons a year after the disturbance once macroalgae had proliferated. These findings underscore how a material legacy from a changing disturbance regime can alter ecosystem resilience properties by disrupting key trophic and competitive interactions that shape post-disturbance community dynamics.

A portable multi-taxa phenotyping device to retrieve physiological performance traits.

Organismal phenotyping to identify fitness traits is transforming our understanding of adaptive responses and ecological interactions of species within changing environments. Here we present a portable Multi-Taxa Phenotyping (MTP) system that can retrieve a suite of metabolic and photophysiological parameter across light, temperature, and/or chemical gradients, using real time bio-optical (oxygen and chlorophyll a fluorescence) measurements. The MTP system integrates three well-established technologies for the first time: an imaging Pulse Amplitude Modulated (PAM) chlorophyll a fluorometer, custom-designed well plates equipped with optical oxygen sensors, and a thermocycler. We demonstrate the ability of the MTP system to distinguish phenotypic performance characteristics of diverse aquatic taxa spanning corals, mangroves and algae based on metabolic parameters and Photosystem II dynamics, in a high-throughput capacity and accounting for interactions of different environmental gradients on performance. Extracted metrics from the MTP system can not only provide information on the performance of aquatic taxa exposed to differing environmental gradients, but also provide predicted phenotypic responses of key aquatic organisms to environmental change. Further work validating how rapid phenotyping tools such as the MTP system predict phenotypic responses to long term environmental changes in situ are urgently required to best inform how these tools can support management efforts.