Widespread scope for coral adaptation under combined ocean warming and acidification.

Reef-building coral populations are at serious risk of collapse due to the combined effects of ocean warming and acidification. Nonetheless, many corals show potential to adapt to the changing ocean conditions. Here we examine the broad sense heritability (H2) of coral calcification rates across an ecologically and phylogenetically diverse sampling of eight of the primary reef-building corals across the Indo-Pacific. We show that all eight species exhibit relatively high heritability of calcification rates under combined warming and acidification (0.23-0.56). Furthermore, tolerance to each factor is positively correlated and the two factors do not interact in most of the species, contrary to the idea of trade-offs between temperature and pH sensitivity, and all eight species can co-evolve tolerance to elevated temperature and reduced pH. Using these values together with historical data, we estimate potential increases in thermal tolerance of 1.0-1.7°C over the next 50 years, depending on species. None of these species are probably capable of keeping up with a high global change scenario and climate change mitigation is essential if reefs are to persist. Such estimates are critical for our understanding of how corals may respond to global change, accurately parametrizing modelled responses, and predicting rapid evolution.

Coping with collapse: Functional robustness of coral-reef fish network to simulated cascade extinction.

Human activities and climate change have accelerated species losses and degradation of ecosystems to unprecedented levels. Both theoretical and empirical evidence suggest that extinction cascades contribute substantially to global species loss. The effects of extinction cascades can ripple across levels of ecological organization, causing not only the secondary loss of taxonomic diversity but also functional diversity erosion. Here, we take a step forward in coextinction analysis by estimating the functional robustness of reef fish communities to species loss. We built a tripartite network with nodes and links based on a model output predicting reef fish occupancy (113 species) as a function of coral and turf algae cover in Southwestern Atlantic reefs. This network comprised coral species, coral-associated fish (site occupancy directly related to coral cover), and co-occurring fish (occupancy indirectly related to coral cover). We used attack-tolerance curves and estimated network robustness (R) to quantify the cascading loss of reef fish taxonomic and functional diversity along three scenarios of coral species loss: degree centrality (removing first corals with more coral-associated fish), bleaching vulnerability and post-bleaching mortality (most vulnerable removed first), and random removal. Degree centrality produced the greatest losses (lowest R) in comparison with other scenarios. In this scenario, while functional diversity was robust to the direct loss of coral-associated fish (R = 0.85), the taxonomic diversity was not robust to coral loss (R = 0.54). Both taxonomic and functional diversity showed low robustness to indirect fish extinctions (R = 0.31 and R = 0.57, respectively). Projections of 100% coral species loss caused a reduction of 69% of the regional trait space area. The effects of coral loss in Southwestern Atlantic reefs went beyond the direct coral-fish relationships. Ever-growing human impacts on reef ecosystems can cause extinction cascades with detrimental consequences for fish assemblages that benefit from corals.

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.

Assisted sexual coral recruits show high thermal tolerance to the 2023 Caribbean mass bleaching event.

Assisted sexual coral propagation, resulting in greater genet diversity via genetic recombination, has been hypothesized to lead to more adaptable and, hence, resilient restored populations compared to more common clonal techniques. Coral restoration efforts have resulted in substantial populations of 'Assisted sexual Recruits' (i.e., juvenile corals derived from assisted sexual reproduction; AR) of multiple species outplanted to reefs or held in in situ nurseries across many locations in the Caribbean. These AR populations provided context to evaluate their relative resilience compared to co-occurring coral populations during the 2023 marine heat wave of unprecedented duration and intensity that affected the entire Caribbean. Populations of six species of AR, most ranging in age from 1-4 years, were surveyed across five regions during the mass bleaching season in 2023 (Aug-Dec), alongside co-occurring groups of corals to compare prevalence of bleaching and related mortality. Comparison groups included conspecific adult colonies as available, but also the extant co-occurring coral assemblages in which conspecifics were rare or lacking, as well as small, propagated coral fragments. Assisted sexual recruits had significantly lower prevalence of bleaching impacts (overall pooled ~ 10%) than conspecific coral populations typically comprised of larger colonies (~ 60-100% depending on species). In addition, small corals derived from fragmentation (rather than sexual propagation) in two regions showed bleaching susceptibility intermediate between AR and wild adults. Overall, AR exhibited high bleaching resistance under heat stress exposure up to and exceeding Degree Heating Weeks of 20°C-weeks. As coral reefs throughout the globe are subject to increasingly frequent and intense marine heatwaves, restoration activities that include sexual reproduction and seeding can make an important contribution to sustain coral populations.

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.

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.

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.

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.

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.

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.

Severe cold-water bleaching of a deep-water reef underscores future challenges for Mesophotic Coral Ecosystems.

Elevated sea surface temperatures are causing an increase in coral bleaching events worldwide, and represent an existential threat to coral reefs. Early studies of Mesophotic Coral Ecosystems (MCEs) highlighted their potential as thermal refuges for shallow-water coral species in the face of predicted 21st century warming. However, recent genetic evidence implies that limited ecological connectivity between shallow- and deep-water coral communities inhibits their effectiveness as refugia; instead MCEs host distinct endemic communities that are ecologically significant in and of themselves. In either scenario, understanding the response of MCEs to climate change is critical given their ecological significance and widespread global distribution. Such an understanding has so far eluded the community, however, because of the challenges associated with long-term field monitoring, the stochastic nature of climatic events that drive bleaching, and the paucity of deep-water observations. Here we document the first observed cold-water bleaching of a mesophotic coral reef at Clipperton Atoll, a remote Eastern Tropical Pacific (ETP) atoll with high coral cover and a well-developed MCE. The severe bleaching (>70 % partially or fully bleached coral cover at 32 m depth) was driven by an anomalously shallow thermocline, and highlights a significant and previously unreported challenge for MCEs. Prompted by these observations, we compiled published cold-water bleaching events for the ETP, and demonstrate that the timing of past cold-water bleaching events in the ETP coincides with decadal oscillations in mean zonal wind strength and thermocline depth. The latter observation suggests any future intensification of easterly winds in the Pacific could be a significant concern for its MCEs. Our observations, in combination with recent reports of warm-water bleaching of Red Sea and Indian Ocean MCEs, highlight that 21st century MCEs in the Eastern Pacific face a two-pronged challenge: warm-water bleaching from above, and cold-water bleaching from below.

Natural coral recovery despite negative population growth.

Demographic processes that ensure the recovery and resilience of marine populations are critical as climate change sends an increasing proportion on a trajectory of decline. Yet for some populations, recovery potential remains high. We conducted annual monitoring over 9 years (2012-2020) to assess the recovery of coral populations belonging to the genus Pocillopora. These populations experienced a catastrophic collapse following a severe typhoon in 2009. From the start of the monitoring period, high initial recruitment led to the establishment of a juvenile population that rapidly transitioned to sexually mature adults, which dominated the population within 6 years after the disturbance. As a result, coral cover increased from 1.1% to 20.2% during this time. To identify key demographic drivers of recovery and population growth rates (λ), we applied kernel-resampled integral projection models (IPMs), constructing eight successive models to examine annual change. IPMs were able to capture reproductive traits as key demographic drivers over the initial 3 years, while individual growth was a continuous key demographic driver throughout the entire monitoring period. IPMs further detected a pulse of reproductive output subsequent to two further Category 5 typhoon events during the monitoring period, exemplifying key mechanisms of resilience for coral populations impacted by disturbance. Despite rapid recovery, (i.e., increased coral cover, individual colony growth, low mortality), IPMs estimated predominantly negative values of λ, indicating a declining population. Indeed, while λ translates to a change in the number of individuals, the recovery of coral populations can also be driven by an increase in the size of surviving colonies. Our results illustrate that accumulating long-term data on historical dynamics and applying IPMs to extract demographic drivers are crucial for future predictions that are based on comprehensive and robust understandings of ecological change.

Life history strategy of Tubastraea spp. corals in an upwelling area on the Southwest Atlantic: growth, fecundity, settlement, and recruitment.

Over the past few decades, corals of the genus Tubastraea have spread globally, revealing themselves to be organisms of great invasive capacity. Their constant expansion on the Brazilian coast highlights the need for studies to monitor the invasion process. The growth, fecundity, settlement, and data on the coverage area of three co-occurring Tubastraea species in the 2015-2016 period were related to temperature variation and light irradiance on the rocky shores of Arraial do Cabo, Rio de Janeiro. Hence, this study sought to understand and compare the current invasion scenario and characteristics of the life history strategy of sun coral species based on environmental variables, considering the uniqueness of this upwelling area in the southwestern Atlantic. For that, we evaluate the fecundity, settlement, and growth rates of corals by carrying out comparative studies between species over time and correlating them with the variables temperature and irradiance, according to seasonality. Field growth of colonies was measured every two months during a sample year. Monthly collections were performed to count reproductive oocytes to assess fecundity. Also, quadrats were scrapped from an area near a large patch of sun coral to count newly attached coral larvae and used years later to assess diversity and percentage coverage. Results showed that corals presented greater growth during periods of high thermal amplitude and in months with below-average temperatures. Only Tubastraea sp. had greater growth and polyp increase in areas with higher light incidence, showing a greater increase in total area compared to all the other species analyzed. Despite the observed affinity with high temperatures, settlement rates were also higher during the same periods. Months with low thermal amplitude and higher temperature averages presented high fecundity. While higher water temperature averages showed an affinity with greater coral reproductive activity, growth has been shown to be inversely proportional to reproduction. Our study recorded the most significant coral growth for the region, an increase in niche, high annual reproductive activity, and large area coverage, showing the ongoing adaptation of the invasion process in the region. However, lower temperatures in the region affect these corals' reproductive activity and growth, slowing down the process of introduction into the region. To better understand the advantages of these invasion strategies in the environment, we must understand the relationships between them and the local community that may be acting to slow down this colonization process.

Highest ocean heat in four centuries places Great Barrier Reef in danger.

Mass coral bleaching on the Great Barrier Reef (GBR) in Australia between 2016 and 2024 was driven by high sea surface temperatures (SST)1. The likelihood of temperature-induced bleaching is a key determinant for the future threat status of the GBR2, but the long-term context of recent temperatures in the region is unclear. Here we show that the January-March Coral Sea heat extremes in 2024, 2017 and 2020 (in order of descending mean SST anomalies) were the warmest in 400 years, exceeding the 95th-percentile uncertainty limit of our reconstructed pre-1900 maximum. The 2016, 2004 and 2022 events were the next warmest, exceeding the 90th-percentile limit. Climate model analysis confirms that human influence on the climate system is responsible for the rapid warming in recent decades. This attribution, together with the recent ocean temperature extremes, post-1900 warming trend and observed mass coral bleaching, shows that the existential threat to the GBR ecosystem from anthropogenic climate change is now realized. Without urgent intervention, the iconic GBR is at risk of experiencing temperatures conducive to near-annual coral bleaching3, with negative consequences for biodiversity and ecosystems services. A continuation on the current trajectory would further threaten the ecological function4 and outstanding universal value5 of one of Earth's greatest natural wonders.

Coral Sr/Ca-SST reconstruction from Fiji extending to ~1370 CE reveals insights into the Interdecadal Pacific Oscillation.

The southwestern tropical Pacific is a key center for the Interdecadal Pacific Oscillation (IPO), which regulates global climate. This study introduces a groundbreaking 627-year coral Sr/Ca sea surface temperature reconstruction from Fiji, representing the IPO's southwestern pole. Merging this record with other Fiji and central tropical Pacific records, we reconstruct the SST gradient between the southwestern and central Pacific (SWCP), providing a reliable proxy for IPO variability from 1370 to 1997. This reconstruction reveals distinct centennial-scale temperature trends and insights into Pacific-wide climate impacts and teleconnections. Notably, the 20th century conditions, marked by simultaneous basin-scale warming and weak tropical Pacific zonal-meridional gradients, deviate from trends observed during the past six centuries. Combined with model simulations, our findings reveal that a weak SWCP gradient most markedly affects IPO-related rainfall patterns in the equatorial Pacific. Persistent synchronous western and central Pacific warming rates could lead to further drying climate across the Coral Sea region, adversely affecting Pacific Island nations.

Feeding biology of crown-of-thorns seastars across sites differing in Acropora availability.

Crown-of-thorns seastars (COTS, Acanthaster spp.) are a major contributor to coral mortality across the Indo-Pacific and can cause extensive reef degradation. The diet preferences of COTS can influence coral community structure by predation on fast-growing genera such as Acropora and avoidance of rare coral genera. In non-outbreaking populations, this preference can increase species diversity. The feeding biology of Acanthaster cf. solaris was compared at two sites (Shark Alley and Second Lagoon) on One Tree Island reef, located in the southern Great Barrier Reef, to determine whether the availability of Acropora influences differences in COTS movement, feeding preference and feeding rates within the same reef system. Acanthaster cf. solaris were tracked daily for five days across both sites, with measurements of movement, feeding scars and coral composition recorded over this time. While Shark Alley and Second Lagoon have similar live coral cover (40 and 44 % respectively), Shark Alley has significantly lower Acropora availability than Second Lagoon (2 vs 32 %). The feeding rate of COTS was significantly different between Shark Alley and Second Lagoon (259.8 and 733.8 cm2 of coral per day, respectively), but did not differ between seastar size (25-40 cm and >40 cm). Acanthaster cf. solaris showed preference for Pocillopora, Seriatopora, Acropora and Isopora and an avoidance of Porites at both sites. The results suggest that for coral reef sites where Acropora is not dominant, COTS outbreaks may be less likely to initiate, with comparatively low feeding rates found in comparison to coral reefs where Acropora is dominant.

Long-term exposure to climbazole may affect the health of stress-tolerant coral Galaxea fascicularis.

The persistence of coral reefs globally is threatened by various forms of chemical pollution. Climbazole, an azole antibacterial agent extensively utilized in pharmaceuticals and personal care products (PPCPs) in everyday life, has been detected in various environment media and proved to have significant adverse effects on aquatic organism. However, the effects of climbazole on coral remain largely unknown. Therefore, in this study, we conducted a 42-day investigation to examine the effects of varying concentrations of climbazole on Galaxea fascicularis (G. fascicularis), a stress-tolerant coral species. Our investigations included coral color observations, physiological experiments, and assessments of microbial diversity. The results showed that, after 42 days of exposure, the coral color in the treatment group exposed to 100 µg/L climbazole significantly decreased by one color category on the reference chart (D6 shifted to D5), while there was no change in the control group. This was accompanied by an increase in oxidative stress and a decrease in photosynthetic capacity in coral specimens. Additionally, there was a notable alteration in microbial diversity, resulting in reduced community stability. Elevated levels of climbazole (100 µg/L) stress led to an increased abundance of potentially pathogenic bacteria such as unclassified Erysipelotrichaceae. However, at an environmentally relevant concentration of 1 µg/L, climbazole decreased the photosynthetic efficiency and induced oxidative stress in the stress-tolerant coral G. fascicularis, while not significantly impacting the microbial community diversity of the coral. The findings of our study have important implications for the protection and management of nearshore coral reefs and offer essential data for ecological risk assessment of climbazole.