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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. 

Coastal seawater hypoxia is increasing in temperate estuaries under global climate change, yet it is unknown how low oxygen conditions affect most estuarine species. We found that hypoxia has increased since the 1990s in an estuary hosting the sea anemoneNematostella vectensis(Jacques Cousteau National Estuarine Research Reserve, New Jersey, USA). AdultN. vectensisbred from anemones collected in this estuary exposed to three consecutive nights of hypoxia (dissolved oxygen = 0.5–1.5 mg L⁻¹for ~12 h night⁻¹) during gametogenesis displayed decreased aerobic respiration rates and biomass, indicating metabolic disruption. Physiological declines were correlated with changes in the expression of genes related to oxygen‐dependent metabolic processes, many of which are targets of hypoxia‐inducible factor 1α (HIF1α), demonstrating the activity of this transcription factor for the first time in this early‐diverging metazoan. The upregulation of genes involved in the unfolded protein response and endoplasmic reticulum and Golgi apparatus homeostasis suggested that misfolded proteins contributed to disrupted physiology. Notably, these responses were more pronounced in females, demonstrating sex‐specific sensitivity that was also observed in reproductive outcomes, with declines in female but not male fecundity following hypoxia exposure. However, sperm from exposed males had higher mitochondrial membrane potential, indicating altered spermatogenesis. Further, crosses performed with gametes from hypoxia‐exposed adults yielded strikingly low developmental success (~2%), yet larvae that did develop displayed similar respiration rates and accelerated settlement compared to controls. Overall, hypoxia depressed fitness inN. vectensisby over 95%, suggesting that even stress‐tolerant estuarine species may be threatened by coastal deoxygenation. 

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. 

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.