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Heat stress can disrupt acid–base homeostasis in reef-building corals and other tropical cnidarians, often leading to cellular acidosis that can undermine organismal function. Temperate cnidarians experience a high degree of seasonal temperature variability, leading us to hypothesize that temperate taxa have more thermally robust pH homeostasis than their tropical relatives. To test this, we investigated how elevated temperature affects intracellular pH and calcification in the temperate coralAstrangia poculata. Clonal pairs were exposed to elevated (30°C) or control (22°C) temperatures for 17 days. Despite causing damage to host tissues and symbiont cells, elevated temperature did not affect intracellular pH or inhibit calcification inA. poculata. These responses contrast with those of tropical cnidarians, which experience cellular acidification and decreased growth during heat stress.Astrangia poculatatherefore appears to have thermally resilient cellular acid–base homeostasis mechanisms, possibly because of adaptation to large seasonal temperature variations. However, we also observed tissue damage and lower egg densities in heat-treated individuals, suggesting that increasingly severe marine heatwaves can still threaten temperate coral fitness. These results provide insight into corals’ nuanced adaptive capacity across latitudes and biological scales. 

Anthropogenic pollution is driving an increase in the frequency and severity of seawater hypoxic events in coastal marine ecosystems. Although hypoxia decreases physiological performance in coral and sea anemone (phylum Cnidaria) larvae, the underlying cellular mechanisms remain unexplored. Here, larvae of the reef-building corals Galaxea fascicularis and Porites astreoides and the estuarine sea anemone Nematostella vectensis were exposed to normoxia or a simulated hypoxic event (6 h at <2 mg dissolved O2 l−1), and their metabolomic response was quantified at the end of the exposure period using targeted liquid chromatography-mass spectrometry. Baseline metabolite profiles (81 amino acids, acylcarnitines, organic acids and nucleotides) were broadly divergent between the three species, with the corals displaying a reliance on nitrogen cycling through amino acid metabolism, whereas N. vectensis relied on nucleotide metabolism. By contrast, several changes in metabolite abundances under hypoxia were shared (e.g. increases in lactate) and suggest the upregulation of glycolysis, lactic acid fermentation and fatty acid β-oxidation as conserved mechanisms for energy production under hypoxia. Changes in these pathways were correlated with adverse physiological outcomes, including conserved declines in swimming behavior and growth. Importantly, life history traits affecting metabolism influenced hypoxia responses. For example, P. astreoides larvae, which possess algal endosymbionts, displayed the least severe metabolic response to hypoxia among these species, possibly owing to symbiont resources. Overall, these findings demonstrate that hypoxia disrupts metabolic performance in coral and sea anemone larvae through conserved and divergent pathways, emphasizing the need to limit drivers of ocean deoxygenation. 

Marine heatwaves are starting to occur several times a decade, yet we do not understand the effect this has on corals across biological scales. This study combines tissue-, organism-, and community-level analyses to investigate the effects of a marine heatwave on reef-building corals. Adjacent conspecific pairs of coral colonies of Montipora capitata and Porites compressa that showed contrasting phenotypic responses (i.e., bleached vs. not bleached) were first identified during a marine heatwave that occurred in 2015 in Kāne’ohe Bay, Hawai‘ i. These conspecific pairs of bleaching-resistant and bleaching-susceptible colonies were sampled for histology and photographed before, during, and after a subsequent marine heatwave that occurred in 2019. Histology samples were quantified for: (i) abundance of mesenterial filaments, (ii) tissue structural integrity, (iii) clarity of epidermis, and (iv) cellular integrity (lack of necrosis/granulation) on a 1–5 scale and averaged for an overall tissue integrity score. Tissue integrity scores revealed a significant decline in overall tissue health during the 2019 heatwave relative to the months prior to the heatwave for individuals of both species, regardless of past bleaching history in 2015 or bleaching severity during the 2019 heatwave. Coral tissue integrity scores were then compared to concurrent colony bleaching severity, which revealed that tissue integrity was significantly correlated with colony bleaching severity and suggests that the stability of the symbiosis is related to host tissue health. Colony partial mortality was also quantified as the cumulative proportion of each colony that appeared dead 2.5 years following the 2019 bleaching event, and tissue integrity during the heatwave was found to be strongly predictive of the extent of partial mortality following the heatwave for M. capitata but not P. compressa, the latter of which suffered little to no mortality. Surprisingly, bleaching severity and partial mortality were not significantly correlated for either species, suggesting that tissue integrity was a better predictor of mortality than bleaching severity in M. capitata. Despite negative effects of heat stress at the tissue- and colony-level, no significant changes in coral cover were detected, indicating resilience at the community level. However, declines in tissue integrity in response to heat stress that are not accompanied by a visible bleaching response may still have long-term consequences for fitness, and this is an important area of future investigation as heat stress is commonly associated with long-term decreases in coral fecundity and growth. Our results suggest that histology is a valuable tool for revealing the harmful effects of marine heatwaves on corals before they are visually evident as bleaching, and may thus improve the predictability of ecosystem changes following climate change-driven heat stress by providing a more comprehensive assessment of coral health. 

Coral bleaching is a common stress response to extreme temperatures experienced during marine heatwaves. Bleached corals are left vulnerable without the nutritional support of their algal symbionts, and can often suffer partial or complete mortality. Bleaching-induced mortality is often accompanied by colonization of turf algae over the dead coral skeleton, which can be difficult for corals to regrow over. The Phoenix effect is a phenomenon of rapid recovery of live coral tissue following mortality, which is hypothesized to occurviathe regrowth of tissue from deep within the coral skeleton that expands over the top of dead portions. Here, we found that the Hawaiian coralsPorites compressaandMontipora capitatacan display rapid tissue recovery suggestive of the Phoenix effect. During a marine heatwave that occurred in 2015 in Kāne’ohe Bay, Hawai’i, USA, 237 individuals (including bleached and non-bleached phenotypes) were identified and monitored for mortality and recovery over the next 2–7 years. Nearly 16% ofP. compressaindividuals and 34% ofM. capitataexhibited substantial partial mortality, and approximately half of these affected individuals of each species had bleached during the heatwave. Partial mortality following the 2015 heatwave was followed by turf algae colonization over the exposed skeleton. Of the colonies with substantial mortality, six colonies (10% of affected individuals; fiveP. compressaand oneM. capitata) subsequently recovered to over 90% live coral tissue within 2 years (2017), with an additional three colonies (twoP. compressaand oneM. capitata) recovering within 4 years of the 2015 marine heatwave (2019). We qualify colonies with rapid tissue recovery as those that meet two criteria: (1) substantial partial mortality (≥40%) in the first 12 months following the initial 2015 marine heatwave, and (2) recovery of any amount of live tissue at anytime before 2022. Interestingly, only colonies that had bleached in 2015 exhibited rapid tissue recovery. A consecutive, yet less severe marine heatwave occurred in 2019, and none of the previously recovered colonies observed experienced significant tissue loss, suggesting these individuals remained resilient amidst a secondary heat stress exposure. This phenomenon is an example of remarkable recovery and resilience that may be informative for further study of mechanisms of coral tissue regeneration in two important reef-building coral species. 

Seawater hypoxia is increasing globally and can drive declines in organismal performance across a wide range of marine taxa. However, the effects of hypoxia on early life stages (e.g., larvae and juveniles) are largely unknown, and it is unclear how evolutionary and life histories may influence these outcomes. Here, we addressed this question by comparing hypoxia responses across early life stages of three cnidarian species representing a range of life histories: the reef‐building coralGalaxea fascicularis, a broadcast spawner with horizontal transmission of endosymbiotic algae (family Symbiodiniaceae); the reef‐building coralPorites astreoides, a brooder with vertical endosymbiont transmission; and the estuarine sea anemoneNematostella vectensis, a non‐symbiotic broadcast spawner. Transient exposure of larvae to hypoxia (dissolved oxygen < 2 mg L⁻¹for 6 h) led to decreased larval swimming and growth for all three species, which resulted in impaired settlement for the corals. Coral‐specific responses also included larval swelling, depressed respiration rates, and decreases in symbiont densities and function. These results indicate both immediate and latent negative effects of hypoxia on cnidarian physiology and coral–algal mutualisms specifically. In addition,G. fascicularisandP. astreoideswere sensitized to heat stress following hypoxia exposure, suggesting that the combinatorial nature of climate stressors will lead to declining performance for corals. However, sensitization to heat stress was not observed inN. vectensisexposed to hypoxia, suggesting that this species may be more resilient to combined stressors. Overall, these results emphasize the importance of reducing anthropogenic carbon emissions to limit further ocean deoxygenation and warming. 

Abstract Variable temperature regimes that expose corals to sublethal heat stress have been recognized as a mechanism to increase coral thermal tolerance and lessen coral bleaching. However, there is a need to better understand which thermal regimes maximize coral stress hardening. Here, standardized thermal stress assays were used to determine the relative thermal tolerance of three divergent genera of corals (Acropora,Pocillopora,Porites) originating from six reef sites representing an increasing gradient of annual mean diel temperature fluctuations of 1–3 °C day⁻¹. Bleaching severity and dark-acclimated photochemical yield (i.e.,F_v/F_m) were quantified following exposure to five temperature treatments ranging from 23.0 to 36.3 °C. The greatest thermal tolerance (i.e.,F_v/F_meffective dose 50) was found at the site with intermediate mean diel temperature variability (2.2 °C day⁻¹), suggesting there is an optimal priming exposure that leads to maximal thermal tolerance. Interestingly,AcroporaandPocilloporaoriginating from the least thermally variable regimes (< 1.3 °C day⁻¹) had lower thermal tolerance than corals from the most variable sites (> 2.8 °C day⁻¹), whereas the opposite was true forPorites, suggesting divergent responses across taxa. Remarkably, comparisons across global studies revealed that the range in coral thermal tolerance uncovered in this study across a single reef (< 5 km) were as large as differences observed across vast latitudinal gradients (300–900 km). This finding indicates that local gene flow could improve thermal tolerance between habitats. However, as climate change continues, exposure to intensifying marine heatwaves is already compromising thermal priming as a mechanism to enhance coral thermal tolerance and bleaching resistance. 

Climate change threatens the survival of symbiotic cnidarians by causing photosymbiosis breakdown in a process known as bleaching. Direct effects of temperature on cnidarian host physiology remain difficult to describe because heatwaves depress symbiont performance, leading to host stress and starvation. The symbiotic sea anemone Exaiptasia diaphana provides an opportune system to disentangle direct versus indirect heat effects on the host, as it can survive indefinitely without symbionts. We tested the hypothesis that heat directly impairs cnidarian physiology by comparing symbiotic and aposymbiotic individuals of two laboratory subpopulations of a commonly used clonal strain of E. diaphana, CC7. We exposed anemones to a range of temperatures (ambient, +2°C, +4°C and +6°C) for 15–18 days, then measured their symbiont population densities, autotrophic carbon assimilation and translocation, photosynthesis, respiration and host intracellular pH (pHi). Symbiotic anemones from the two subpopulations differed in size and symbiont density and exhibited distinct heat stress responses, highlighting the importance of acclimation to different laboratory conditions. Specifically, the cohort with higher initial symbiont densities experienced dose-dependent symbiont loss with increasing temperature and a corresponding decline in host photosynthate accumulation. In contrast, the cohort with lower initial symbiont densities did not lose symbionts or assimilate less photosynthate when heated, similar to the response of aposymbiotic anemones. However, anemone pHi decreased at higher temperatures regardless of cohort, symbiont presence or photosynthate translocation, indicating that heat consistently disrupts cnidarian acid–base homeostasis independent of symbiotic status or mutualism breakdown. Thus, pH regulation may be a critical vulnerability for cnidarians in a changing climate. 

The future of coral reefs in a warming world depends on corals’ ability to recover from bleaching, the loss of their symbiotic dinoflagellate algae (Symbiodiniaceae) during marine heatwaves. Heat-tolerant symbiont species can remain in symbiosis during heat stress, but often provide less photosynthate to the host than heat-sensitive species under ambient conditions. Understanding how heat stress changes the dynamics of this tradeoff between stress tolerance and mutualism contribution is crucial for predicting coral success under climate change. To test how symbiont resource allocation affects coral recovery from heat stress, we exposed the coral Montipora capitata hosting either heat-sensitive Cladocopium C31 (C) or heat-tolerant Durusdinium glynnii (D) to heat stress. D regained symbiont density and photochemical efficiency faster after heat treat- ment than C, but symbiont recovery did not restore coral biomass or calcification rates to pre-bleaching levels in the initial recovery period. D populations also contributed less photosynthate to the host relative to C, even during heat stress. Further, higher-density symbiont populations of both species retained more photosynthate than lower-density populations, and corals receiving less photosynthate exhibited reduced calcification rates and lower intracellular pH. This is the first evidence that symbiont density and carbon translocation are negatively related, and the first to establish a link between Symbiodiniaceae carbon translocation and coral cellular homeostasis. Together, these results suggest the energy demand of symbiont regrowth after bleaching reduces their mutualism contribution and can thus delay host recovery. Reestablishing a beneficial endos- ymbiosis imposes additional costs as holobionts overcome stress, and may explain latent mortality among coral populations after alleviation of heat stress in the field. 

Most stony corals liberate their gametes into the water column via broadcast spawning, where fertilization hinges upon the activation of directional sperm motility. Sperm from gonochoric and hermaphroditic corals display distinct morphological and molecular phenotypes, yet it is unknown whether the signalling pathways controlling sperm motility are also distinct between these sexual systems. Here, we addressed this knowledge gap using the gonochoric, broadcast spawning coralAstrangia poculata. We found that cytosolic alkalinization of sperm activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), which is required for motility. Additionally, we demonstrate for the first time in any cnidarian that sAC activity leads to protein kinase A (PKA) activation, and that PKA activity contributes to sperm motility activation. Ultrastructures ofA. poculatasperm displayed morphological homology with other gonochoric cnidarians, and sAC exhibited broad structural and functional conservation across this phylum. These results indicate a conserved role for pH-dependent sAC-cAMP-PKA signalling in sperm motility across coral sexual systems, and suggest that the role of this pathway in sperm motility may be ancestral in metazoans. Finally, the dynamics of this pH-sensitive pathway may play a critical role in determining the sensitivity of marine invertebrate reproduction to anthropogenic ocean acidification. 

Increasingly frequent marine heatwaves are devastating coral reefs. Corals that survive these extreme events must rapidly recover if they are to withstand subsequent events, and long-term survival in the face of rising ocean temperatures may hinge on recovery capacity and acclimatory gains in heat tolerance over an individual’s lifespan. To better understand coral recovery trajectories in the face of successive marine heatwaves, we monitored the responses of bleaching-susceptible and bleaching-resistant individuals of two dominant coral species in Hawai’i,Montipora capitataandPorites compressa, over a decade that included three marine heatwaves. Bleaching-susceptible colonies ofP. compressaexhibited beneficial acclimatization to heat stress (i.e., less bleaching) following repeat heatwaves, becoming indistinguishable from bleaching-resistant conspecifics during the third heatwave. In contrast, bleaching-susceptibleM. capitatarepeatedly bleached during all successive heatwaves and exhibited seasonal bleaching and substantial mortality for up to 3 y following the third heatwave. Encouragingly, bleaching-resistant individuals of both species remained pigmented across the entire time series; however, pigmentation did not necessarily indicate physiological resilience. Specifically,M. capitatadisplayed incremental yet only partial recovery of symbiont density and tissue biomass across both bleaching phenotypes up to 35 mo following the third heatwave as well as considerable partial mortality. Conversely,P. compressaappeared to recover across most physiological metrics within 2 y and experienced little to no mortality. Ultimately, these results indicate that even some visually robust, bleaching-resistant corals can carry the cost of recurring heatwaves over multiple years, leading to divergent recovery trajectories that may erode coral reef resilience in the Anthropocene.