Photosymbiosis reduces the environmental stress response under a heat challenge in a facultatively symbiotic coral.

The symbiosis between corals and dinoflagellates of the family Symbiodiniaceae is sensitive to environmental stress. The oxidative bleaching hypothesis posits that extreme temperatures lead to accumulation of photobiont-derived reactive oxygen species ROS, which exacerbates the coral environmental stress response (ESR). To understand how photosymbiosis modulates coral ESRs, these responses must be explored in hosts in and out of symbiosis. We leveraged the facultatively symbiotic coral Astrangia poculata, which offers an opportunity to uncouple the ESR across its two symbiotic phenotypes (brown, white). Colonies of both symbiotic phenotypes were exposed to three temperature treatments for 15 days: (i) control (static 18 °C), (ii) heat challenge (increasing from 18 to 30 °C), and (iii) cold challenge (decreasing from 18 to 4 °C) after which host gene expression was profiled. Cold challenged corals elicited widespread differential expression, however, there were no differences between symbiotic phenotypes. In contrast, brown colonies exhibited greater gene expression plasticity under heat challenge, including enrichment of cell cycle pathways involved in controlling photobiont growth. While this plasticity was greater, the genes driving this plasticity were not associated with an amplified environmental stress response (ESR) and instead showed patterns of a dampened ESR under heat challenge. This provides nuance to the oxidative bleaching hypothesis and suggests that, at least during the early onset of bleaching, photobionts reduce the host's ESR under elevated temperatures in A. poculata.

Phosphorus limitation intensifies heat-stress effects on the potential mutualistic capacity in the coral-derived Symbiodinium.

Coral reef ecosystems have been severely ravaged by global warming and eutrophication. Eutrophication often originates from nitrogen (N) overloading that creates stoichiometric phosphorus (P) limitation, which can be aggravated by sea surface temperature rises that enhances stratification. However, how P-limitation interacts with thermal stress to impact coral-Symbiodiniaceae mutualism is poorly understood and underexplored. Here, we investigated the effect of P-limitation (P-depleted vs. P-replete) superimposed on heat stress (31 °C vs. 25 °C) on a Symbiodinium strain newly isolated from the coral host by a 14-day incubation experiment. The heat and P-limitation co-stress induced an increase in alkaline phosphatase activity and reppressed cell division, photosynthetic efficiency, and expression of N uptake and assimilation genes. Moreover, P limitation intensified downregulation of carbon fixation (light and dark reaction) and metabolism (glycolysis) pathways in heat stressed Symbiodinium. Notably, co-stress elicited a marked transcriptional downregulation of genes encoding photosynthates transporters and microbe-associated molecular patterns, potentially undermining the mutualism potential. This work sheds light on the interactive effects of P-limitation and heat stress on coral symbionts, indicating that nutrient imbalance in the coral reef ecosystem can intensify heat-stress effects on the mutualistic capacity of Symbiodiniaceae.

Symbiosis: Aquatic apicomplexans shedding light on disguised associations.

Aquatic apicomplexans called Corallicolida have been found in tropical and coral-reef settings, infecting many coral species. New data challenge this tropical distribution and expand the corallicolids' range well into the cold temperate. Surprisingly, the sister clade to corallicolids infects only one group of vertebrates - bony fishes.

Coral-reef ecology: Expanding urchin disease threatens ecosystem balance.

Sea urchins are critically important herbivores on coral reefs. A new study shows that a disease that decimated sea urchins in the Caribbean in 2022 has spread to the Red Sea, further threatening coral ecosystems.

Rubble persistence under ocean acidification threatened by accelerated bioerosion and lower-density coral skeletons.

As the balance between erosional and constructive processes on coral reefs tilts in favor of framework loss under human-induced local and global change, many reef habitats worldwide degrade and flatten. The resultant generation of coral rubble and the beds they form can have lasting effects on reef communities and structural complexity, threatening the continuity of reef ecological functions and the services they provide. To comprehensively capture changing framework processes and predict their evolution in the context of climate change, heavily colonized rubble fragments were exposed to ocean acidification (OA) conditions for 55 days. Controlled diurnal pH oscillations were incorporated in the treatments to account for the known impact of diel carbonate chemistry fluctuations on calcification and dissolution response to OA. Scenarios included contemporary pH (8.05 ± 0.025 diel fluctuation), elevated OA (7.90 ± 0.025), and high OA (7.70 ± 0.025). We used a multifaceted approach, combining chemical flux analyses, mass alteration measurements, and computed tomography scanning images to measure total and chemical bioerosion, as well as chemically driven secondary calcification. Rates of net carbonate loss measured in the contemporary conditions (1.36 kg m-2 year-1) were high compared to literature and increased in OA scenarios (elevated: 1.84 kg m-2 year-1 and high: 1.59 kg m-2 year-1). The acceleration of these rates was driven by enhanced chemical dissolution and reduced secondary calcification. Further analysis revealed that the extent of these changes was contingent on the density of the coral skeleton, in which the micro- and macroborer communities reside. Findings indicated that increased mechanical bioerosion rates occurred in rubble with lower skeletal density, which is of note considering that corals form lower-density skeletons under OA. These direct and indirect effects of OA on chemical and mechanical framework-altering processes will influence the permanence of this crucial habitat, carrying implications for biodiversity and reef ecosystem function.

Effects of water flow and ocean acidification on oxygen and pH gradients in coral boundary layer.

Reef-building corals live in highly hydrodynamic environments, where water flow largely controls the complex chemical microenvironments surrounding them-the concentration boundary layer (CBL). The CBL may be key to alleviate ocean acidification (OA) effects on coral colonies by partially isolating them. However, OA effects on coral CBL remain poorly understood, particularly under different flow velocities. Here, we investigated these effects on the reef-building corals Acropora cytherea, Pocillopora verrucosa, and Porites cylindrica. We preconditioned corals to a control (pH 8.0) and OA (pH 7.8) treatment for four months and tested how low flow (2 cm s-1) and moderate flow (6 cm s-1) affected O2 and H+ CBL traits (thickness, surface concentrations, and flux) inside a unidirectional-flow chamber. We found that CBL traits differed between species and flow velocities. Under OA, traits remained generally stable across flows, except surface pH. In all species, the H+ CBL was thin and led to lower surface pH. Still, low flow thickened H+ CBLs and increased light elevation of surface pH. In general, our findings reveal a weak to null OA modulation of the CBL. Moreover, the OA-buffering capacity by the H+ CBL may be limited in coral species, though low flow could enhance CBL sheltering.

The bioenergetics response of the coral Pocillopora damicornis to temperature changes during its reproduction stage.

Sexual reproduction of reef-building corals is vital for coral reef ecosystem recovery. Corals allocate limited energy to growth and reproduction, when being under environmental disturbance, which ultimately shapes the community population dynamics. In the present study, energetic and physiological parameters of both parental colonies and larvae of the coral Pocillopora damicornis were measured during their reproduction stage under four temperatures; 28 °C (low-temperature acclimation, LA), 29 °C (control temperature, CT), 31 °C (high-temperature acclimation, HA), and 32 °C (heat stress, HS). The results showed temperature changes altered the larvae release timing and fecundity in P. damicornis. Parental colonies exposed to the LA treatment exhibited reduced investment in reproduction and released fewer larvae, while retaining more energy for their development. However, each larva acquired higher energy and symbiont densities enabling survival through longer planktonic periods before settlement. In contrast, parental colonies exposed to the HA treatment had increased investment for reproduction and larvae output, while per larva gained less energy to mitigate the threat of higher temperature. Furthermore, the energy allocation processes restructured fatty acids concentration and composition in both parental colonies and larvae as indicated by shifts in membrane fluidity under adaptable temperature changes. Notably, parental colonies from the HS treatment expended more energy in response to heat stress, resulting in adverse effects, especially after larval release. Our study expands the current knowledge on the energy allocation strategies of P. damicornis and how it is impacted by temperature. Parental colonies employed different energy allocation strategies under distinct temperature regimes to optimize their development and offspring success, but under heat stress, both were compromised. Lipid metabolism is essential for the success of coral reproduction and further understanding their response to heat stress can improve intervention strategies for coral reef conservation in warmer future oceans.

A Semi-Automated Workflow for the Cryopreservation of Coral Sperm to Support Biobanking and Aquaculture.

Coral reefs are facing a crisis as the frequency of bleaching events caused by ocean warming increases, resulting in the death of corals on reefs around the world. The subsequent loss of genetic diversity and biodiversity can diminish the ability of coral to adapt to the changing climate, so efforts to preserve existing diversity are essential to maximize the resources available for reef restoration now and in the future. The most effective approach to secure genetics long-term is cryopreservation and biobanking, which permits the frozen storage of living samples at cryogenic temperatures in liquid nitrogen indefinitely. Cryopreservation of coral sperm has been possible since 2012, but the seasonal nature of coral reproduction means that biobanking activities are restricted to just a few nights per year when spawning occurs. Improving the efficiency of coral sperm processing and cryopreservation workflows is therefore essential to maximizing these limited biobanking opportunities. To this end, we set out to optimize cryopreservation processing pathways for coral sperm by building on existing technologies and creating a semi-automated approach to streamline the assessment, handling, and cryopreservation of coral sperm. The process, which combines computer-assisted sperm analysis, barcoded cryovials, and a series of linked auto-datasheets for simultaneous editing by multiple users, improves the efficiency of both sample processing and metadata management in the field. Through integration with cross-cutting research programs such as the Reef Restoration and Adaptation Program in Australia, cryopreservation can play a crucial role in large-scale reef restoration programs by facilitating the genetic management of aquaculture populations, supporting research to enhance thermal tolerance, and preventing the extinction of coral species. The described procedures will be utilized for coral cryopreservation and biobanking practitioners on reefs worldwide and will provide a model for the transition of cryopreservation technologies from research laboratories to large-scale applications.

Coral-seeding devices with fish-exclusion features reduce mortality on the Great Barrier Reef.

Restoration methods that seed juvenile corals show promise as scalable interventions to promote population persistence through anthropogenic warming. However, challenges including predation by fishes can threaten coral survival. Coral-seeding devices with refugia from fishes offer potential solutions to limit predation-driven mortality. In an 8-month field study, we assessed the efficacy of such devices for increasing the survival of captive-reared Acropora digitifera (spat and microfragments) over control devices (featureless and caged). Devices with fish-exclusion features demonstrated a twofold increase in coral survival, while most corals seeded without protection suffered mortality within 48 h. Overall, spat faced more grazing and higher mortality compared to microfragments, and upward-facing corals were more vulnerable than side-facing corals. Grazing-induced mortality varied by site, with lower activity in locations abundant in mat-forming cyanobacteria or Scleractinian corals. Many scraping parrotfish were found feeding on or near the seeded corals; however, bites by Scarus globiceps explained the most site-related variation in grazing. Cyanobacteria may be preferred over corals as a nutritional resource for scraping parrotfish-advancing our understanding of their foraging ecology. Incorporating side-facing refugia in seeding devices and deploying to sites with nutrient-rich food sources for fish are potential strategies to enhance coral survival in restoration programs.

Global impacts of marine heatwaves on coastal foundation species.

With increasingly intense marine heatwaves affecting nearshore regions, foundation species are coming under increasing stress. To better understand their impacts, we examine responses of critical, habitat-forming foundation species (macroalgae, seagrass, corals) to marine heatwaves in 1322 shallow coastal areas located across 85 marine ecoregions. We find compelling evidence that intense, summer marine heatwaves play a significant role in the decline of foundation species globally. Critically, detrimental effects increase towards species warm-range edges and over time. We also identify several ecoregions where foundation species don't respond to marine heatwaves, suggestive of some resilience to warming events. Cumulative marine heatwave intensity, absolute temperature, and location within a species' range are key factors mediating impacts. Our results suggest many coastal ecosystems are losing foundation species, potentially impacting associated biodiversity, ecological function, and ecosystem services provision. Understanding relationships between marine heatwaves and foundation species offers the potential to predict impacts that are critical for developing management and adaptation approaches.

Connectivity modelling identifies sources and sinks of coral recruitment within reef clusters.

Connectivity aids the recovery of populations following disturbances, such as coral bleaching and tropical cyclones. Coral larval connectivity is a function of physical connectivity and larval behaviour. In this study, we used OceanParcels, a particle tracking simulator, with 2D and 3D velocity outputs from a high resolution hydrodynamic-biogeochemical marine model (RECOM) to simulate the dispersal and settlement of larvae from broadcast spawning Acropora corals in the Moore Reef cluster, northern Great Barrier Reef, following the annual spawning events in 2015, 2016 and 2017. 3D velocity simulations showed 19.40-68.80% more links and sinks than those of 2D simulations. Although the patterns of connectivity among sites vary over days and years, coral larvae consistently dispersed from east to west in the cluster domain, with some sites consistently acting as sources or sinks for local larval recruitment. Results can inform coral reef intervention plans for climate change, such as the design of marine protected areas and the deployment of proposed interventions within reef clusters. For example, the wider benefits of interventions (e.g., deployment of heat adapted corals) may be optimised when deployed at locations that are a source of larvae to others within comparable habitats across the reef cluster.

Local adaptation of trophic strategy determined the tolerance of coral Galaxea fascicularis to environmental fluctuations.

The escalation of global change has resulted in heightened frequencies and intensities of environmental fluctuations within coral reef ecosystems. Corals originating from marginal reefs have potentially enhanced their adaptive capabilities in response to these environmental variations through processes of local adaptation. However, the intricate mechanisms driving this phenomenon remain a subject of limited investigation. This study aimed to investigate how corals in Luhuitou reef, a representative relatively high-latitude reef in China, adapt to seasonal fluctuations in seawater temperature and light availability. We conducted a 190-day plantation experiment with the widespread species, Galaxea fascicularis, in Luhuitou local, and from Meiji reef, a typical offshore tropical reef, to Luhuitou as comparison. Drawing upon insights from physiological adaptations, we focused on fatty acid (FA) profiles to unravel the trophic strategies of G. fascicularis to cope with environmental fluctuations from two origins. Our main findings are threefold: 1) Native corals exhibited a stronger physiological resilience compared to those transplanted from Meiji. 2) Corals from both origins consumed large quantities of energy reserves in winter, during which FA profiles of local corals altered, while the change of FA profiles of corals from Meiji was probably due to the excessive consumption of saturated fatty acid (SFA). 3) The better resilience of native corals is related to high levels of functional polyunsaturated fatty acid (PUFA), while insufficient nutrient reserves, possibly due to weak heterotrophic ability, result in the obstruction of the synthesis pathway of PUFA for corals from Meiji, leading to their intolerance to environmental changes. Consequently, we suggest that the tolerance of G. fascicularis to environmental fluctuations is determined by their local adapted trophic strategies. Furthermore, our findings underscore the notion that the rapid adaptation of relatively high-latitude corals to seasonal environmental fluctuations might not be readily attainable for their tropical counterparts within a brief timeframe.

Hurricanes enhance coral connectivity but also superspread coral diseases.

Climate change poses an existential threat to coral reefs. A warmer and more acidic ocean weakens coral ecosystems and increases the intensity of hurricanes. The wind-wave-current interactions during a hurricane deeply change the ocean circulation patterns and hence potentially affect the dispersal of coral larvae and coral disease agents. Here, we modeled the impact of major hurricane Irma (September 2017) on coral larval and stony coral tissue loss disease (SCTLD) connectivity in Florida's Coral Reef. We coupled high-resolution coastal ocean circulation and wave models to simulate the dispersal of virtual coral larvae and disease agents between thousands of reefs. While being a brief event, our results suggest the passage of hurricane Irma strongly increased the probability of long-distance exchanges while reducing larval supply. It created new connections that could promote coral resilience but also probably accelerated the spread of SCTLD by about a month. As they become more intense, hurricanes' double-edged effect will become increasingly pronounced, contributing to increased variability in transport patterns and an accelerated rate of change within coral reef ecosystems.

Sediment source and dose influence the larval performance of the threatened coral Orbicella faveolata.

The effects of turbidity and sedimentation stress on early life stages of corals are poorly understood, particularly in Atlantic species. Dredging operations, beach nourishment, and other coastal construction activities can increase sedimentation and turbidity in nearby coral reef habitats and have the potential to negatively affect coral larval development and metamorphosis, reducing sexual reproduction success. In this study, we investigated the performance of larvae of the threatened Caribbean coral species Orbicella faveolata exposed to suspended sediments collected from a reef site in southeast Florida recently impacted by dredging (Port of Miami), and compared it to the performance of larvae exposed to sediments collected from the offshore, natal reef of the parent colonies. In a laboratory experiment, we tested whether low and high doses of each of these sediment types affected the survival, settlement, and respiration of coral larvae compared to a no-sediment control treatment. In addition, we analyzed the sediments used in the experiments with 16S rRNA gene amplicon sequencing to assess differences in the microbial communities present in the Port versus Reef sediments, and their potential impact on coral performance. Overall, only O. faveolata larvae exposed to the high-dose Port sediment treatment had significantly lower survival rates compared to the control treatment, suggesting an initial tolerance to elevated suspended sediments. However, significantly lower settlement rates were observed in both Port treatments (low- and high-dose) compared to the control treatment one week after exposure, suggesting strong latent effects. Sediments collected near the Port also contained different microbial communities than Reef sediments, and higher relative abundances of the bacteria Desulfobacterales, which has been associated with coral disease. We hypothesize that differences in microbial communities between the two sediments may be a contributing factor in explaining the observed differences in larval performance. Together, these results suggest that the settlement success and survival of O. faveolata larvae are more readily compromised by encountering port inlet sediments compared to reef sediments, with potentially important consequences for the recruitment success of this species in affected areas.

Biodiversity of macroalgae does not differentially suppress coral performance: The other side of a biodiversity issue.

Hundreds of studies now document positive relationships between biodiversity and critical ecosystem processes, but as ecological communities worldwide shift toward new species configurations, less is known regarding how the biodiversity of undesirable species will shape the functioning of ecosystems or foundation species. We manipulated macroalgal species richness in experimental field plots to test whether and how the identity and diversity of competing macroalgae affected the growth, survival, and microbiome of a common coral in Mo'orea, French Polynesia. Compared to controls without algal competitors, coral growth was significantly suppressed across three macroalgal monocultures, a polyculture of the same three macroalgae, and plots containing inert seaweed mimics; coral mortality was limited and did not differ significantly among treatments. One macroalga suppressed coral growth significantly less than the other two, but none differed from the inert mimic in terms of coral suppression. The composition, dispersion, and diversity of coral microbiomes in treatments with live macroalgae or inert plastic mimics did not differ from controls experiencing no competition. Microbiome composition differed between two macroalgal monocultures and a monoculture versus plastic mimics, but no other microbiome differences were observed among macroalgal or mimic treatments. Together, these findings suggest that algal diversity does not alter harmful impacts of macroalgae on coral performance, which could be accounted for by physical structure alone in these field experiments. While enhancing biodiversity is a recognized strategy for promoting desirable species, it would be worrisome if biodiversity also enhanced the negative impacts of undesirable species. We documented no such effects in this investigation.

Do cold water corals provide an essential habitat for Helicolenus dactylopterus (Delaroche, 1809) in the Northwest Africa?

Cold water corals (CWC) provide habitats for many organisms including demersal fish. Bottom trawl observations have indicated a co-occurrence of the fish Helicolenus dactylopterus with CWC reefs, but a detailed understanding of this relation is lacking. To better understand the nature of this relation we have analyzed 85 video-lines from ROV dives conducted at 25-1700 m depth off Morocco, Mauritania, and Senegal in 2020 and 2021. We annotated abundance, size, and behavior of the 552 specimens observed (32% juveniles and 68% adults), of these 82% occurred in CWC habitats at 400-600 m depth. Both juveniles and adults were observed standing on the seafloor. Our observations are discussed considering available knowledge on feeding ecology and life cycle of H. dactylopterus. Our findings show that CWC provides an essential habitat for this species at least during parts of its lifecycle, however, more behavioral studies are needed for an in-depth understanding of this association.

Effects of macroalgae and sea urchin grazing pressure on zoantharians growth under laboratory conditions.

In the context of ocean warming, thermophilic organisms such as zoantharians are expanding and altering shallow benthic habitats. Here, a four-month laboratory experiment was performed to examine the influence of three types of macroalgae morphotypes common in the Canary Islands (turf algae, Lobophora spp., and crustose coralline algae) on the growth of two zoantharian species, Palythoa caribaeorum and Zoanthus pulchellus. Additionally, the grazing effects of echinoids Diadema africanum and Paracentrotus lividus were assessed as facilitators of substrate colonization by means of controlling macroalgae cover. Colony and algal coverages were measured at the beginning, middle and end of the experiment, and increments were calculated. Results indicated a general decrease in zoantharian colony sizes in contact with different algal types in the absence of sea urchins. However, P. caribaeorum colonies showed significant growth in the presence of D. africanum, highlighting the ecological importance of sea urchins in zoantharian population proliferation and subsequent community modification. This study represents the first investigation into zoantharian-macroalgae interactions under controlled conditions.

Coral species-specific loss and physiological legacy effects are elicited by an extended marine heatwave.

Marine heatwaves are increasing in frequency and intensity, with potentially catastrophic consequences for marine ecosystems such as coral reefs. An extended heatwave and recovery time-series that incorporates multiple stressors and is environmentally realistic can provide enhanced predictive capacity for performance under climate change conditions. We exposed common reef-building corals in Hawai'i, Montipora capitata and Pocillopora acuta, to a 2-month period of high temperature and high PCO2 conditions or ambient conditions in a factorial design, followed by 2 months of ambient conditions. High temperature, rather than high PCO2, drove multivariate physiology shifts through time in both species, including decreases in respiration rates and endosymbiont densities. Pocillopora acuta exhibited more significantly negatively altered physiology, and substantially higher bleaching and mortality than M. capitata. The sensitivity of P. acuta appears to be driven by higher baseline rates of photosynthesis paired with lower host antioxidant capacity, creating an increased sensitivity to oxidative stress. Thermal tolerance of M. capitata may be partly due to harboring a mixture of Cladocopium and Durusdinium spp., whereas P. acuta was dominated by other distinct Cladocopium spp. Only M. capitata survived the experiment, but physiological state in heatwave-exposed M. capitata remained significantly diverged at the end of recovery relative to individuals that experienced ambient conditions. In future climate scenarios, particularly marine heatwaves, our results indicate a species-specific loss of corals that is driven by baseline host and symbiont physiological differences as well as Symbiodiniaceae community compositions, with the surviving species experiencing physiological legacies that are likely to influence future stress responses.

The dispersant Corexit 9500 and (dispersed) oil are lethal to coral endosymbionts.

Endosymbionts (Symbiodiniaceae) play a vital role in the health of corals. Seawater pollution can harm these endosymbionts and dispersants used during oil spill cleanup can be extremely toxic to these organisms. Here, we examined the impact of oil and a specific dispersant, Corexit-9500, on two representative endosymbionts - Symbiodinium and Cladocopium - from the Southwestern endemic coral Mussismilia braziliensis. The survival and photosynthetic potential of the endosymbionts decreased dramatically after exposure to the dispersant and oil by ~25 % after 2 h and ~50 % after 7 days. Low concentrations of dispersant (0.005 ml/l) and dispersed oil (Polycyclic Aromatic Hydrocarbons, 1132 µg/l; Total Petroleum Hydrocarbons, 595 µg/l) proved highly toxic to both Symbiodinium and Cladocopium. These levels triggered a reduction in growth rate, cell size, and cell wall thickness. After a few hours of exposure, cellular organelles were damaged or destroyed. These acute toxic effects underline the fragile nature of coral endosymbionts.

AI-2 quorum sensing signal disrupts coral symbiotic homeostasis and induces host bleaching.

Symbiotic microorganisms play critical ecophysiological roles that facilitate the maintenance of coral health. Currently, information on the gene and protein pathways contributing to bleaching responses is lacking, including the role of autoinducers. Although the autoinducer AI-1 is well understood, information on AI-2 is insufficient. Here, we observed a 3.7-4.0 times higher abundance of the AI-2 synthesis gene luxS in bleached individuals relative to their healthy counterparts among reef-building coral samples from the natural environment. Laboratory tests further revealed that AI-2 contributed significantly to an increase in coral bleaching, altered the ratio of potential probiotic and pathogenic bacteria, and suppressed the antiviral activity of specific pathogenic bacteria while enhancing their functional potential, such as energy metabolism, chemotaxis, biofilm formation and virulence release. Structural equation modeling indicated that AI-2 influences the microbial composition, network structure, and pathogenic features, which collectively contribute to the coral bleaching status. Collectively, our results offer novel potential strategies for coral conservation based on a signal manipulation approach.