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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.

 

Ocean acidification (OA) resulting from anthropogenic CO2 emissions is impairing the reproduction of marine organisms. While parental exposure to OA can protect offspring via carryover effects, this phenomenon is poorly understood in many marine invertebrate taxa. Here, we examined how parental exposure to acidified (pH 7.40) versus ambient (pH 7.72) seawater influenced reproduction and offspring performance across six gametogenic cycles (13 weeks) in the estuarine sea anemone Nematostella vectensis. Females exhibited reproductive plasticity under acidic conditions, releasing significantly fewer but larger eggs compared to ambient females after 4 weeks of exposure, and larger eggs in two of the four following spawning cycles despite recovering fecundity, indicating long-term acclimatization and greater investment in eggs. Males showed no changes in fecundity under acidic conditions but produced a greater percentage of sperm with high mitochondrial membrane potential (MMP; a proxy for elevated motility), which corresponded with higher fertilization rates relative to ambient males. Finally, parental exposure to acidic conditions did not significantly influence offspring development rates, respiration rates, or heat tolerance. Overall, this study demonstrates that parental exposure to acidic conditions impacts gamete production and physiology but not offspring performance in N. vectensis, suggesting that increased investment in individual gametes may promote fitness.

 

Marine heatwaves are occurring more frequently as climate change intensifies, resulting in global mass coral bleaching events several times per decade. Despite the time between marine heatwaves decreasing, there is evidence that reef-building corals can develop increased bleaching resistance across repetitive marine heatwaves. This phenomenon of acclimatization via environmental memory may be an important strategy to ensure coral persistence; however, we still understand very little about the apparent acclimatization or, conversely, sensitization (i.e., stress accumulation or weakening) of reef-building corals to consecutive heatwaves and its implications for the trajectory and resilience of coral reefs. Here, we highlight that not only will some corals become stress hardened via marine heatwaves, but many other individuals will suffer sensitization during repeat heatwaves that further exacerbates their stress response during repeat events and depresses fitness. Under current and predicted climate change, it is necessary to gain a better understanding of the acclimatization vs. sensitization trajectories of different species and individuals on the reef, as well as identify whether changes in bleaching susceptibility relates to physiological acclimatization, trade-offs with other biological processes, and ultimately coral persistence in the Anthropocene.

 

Ocean warming is causing global coral bleaching events to increase in frequency, resulting in widespread coral mortality and disrupting the function of coral reef ecosystems. However, even during mass bleaching events, many corals resist bleaching despite exposure to abnormally high temperatures. While the physiological effects of bleaching have been well documented, the consequences of heat stress for bleaching‐resistant individuals are not well understood. In addition, much remains to be learned about how heat stress affects cellular‐level processes that may be overlooked at the organismal level, yet are crucial for coral performance in the short term and ecological success over the long term. Here we compared the physiological and cellular responses of bleaching‐resistant and bleaching‐susceptible corals throughout the 2019 marine heatwave in Hawai'i, a repeat bleaching event that occurred 4 years after the previous regional event. Relative bleaching susceptibility within species was consistent between the two bleaching events, yet corals of both resistant and susceptible phenotypes exhibited pronounced metabolic depression during the heatwave. At the cellular level, bleaching‐susceptible corals had lower intracellular pH than bleaching‐resistant corals at the peak of bleaching for both symbiont‐hosting and symbiont‐free cells, indicating greater disruption of acid–base homeostasis in bleaching‐susceptible individuals. Notably, cells from both phenotypes were unable to compensate for experimentally induced cellular acidosis, indicating that acid–base regulation was significantly impaired at the cellular level even in bleaching‐resistant corals and in cells containing symbionts. Thermal disturbances may thus have substantial ecological consequences, as even small reallocations in energy budgets to maintain homeostasis during stress can negatively affect fitness. These results suggest concern is warranted for corals coping with ocean acidification alongside ocean warming, as the feedback between temperature stress and acid–base regulation may further exacerbate the physiological effects of climate change.

 

Climate change threatens symbiotic cnidarians’ survival 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 vs. indirect heat effects on the host, since 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, +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.

 

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.

 

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.

 

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. 

Increasing ocean temperatures threaten coral reefs globally, but corals residing in habitats that experience high thermal variability are thought to be better adapted to survive climate-induced heat stress. Here, we used long-term ecological observations and in situ temperature data from Heron Island, southern Great Barrier Reef to investigate how temperature dynamics within various thermally variable vs. thermally stable reef habitats change during a marine heatwave and the resulting consequences for coral community survival. During the heatwave, thermally variable habitats experienced larger surges in daily mean and maxima temperatures compared to stable sites, including extreme hourly incursions up to 36.5 °C. The disproportionate increase in heat stress in variable habitats corresponded with greater subsequent declines in hard coral cover, including a three-times greater decline within the thermally variable Reef Flat (70%) and Deep Lagoon (83%) than within thermally stable habitats along sheltered and exposed areas of the reef slope (0.3–19%). Interestingly, the thermally variable Reef Crest experienced comparatively small declines (26%), avoiding the most severe tidal ponding and resultant heat stress likely due to proximity to the open ocean equating to lower seawater residence times, greater mixing, and/or increased flow. These results highlight that variable thermal regimes, and any acclimatization or adaptation to elevated temperatures that may lead to, do not necessarily equate to protection against bleaching and mortality during marine heatwaves. Instead, thermally stable habitats that have greater seawater exchange with the open ocean may offer the most protection to corals during the severe marine heatwaves that accompany a changing climate. 

Across diverse taxa, sublethal exposure to abiotic stressors early in life can lead to benefits such as increased stress tolerance upon repeat exposure. This phenomenon, known as hormetic priming, is largely unexplored in early life stages of marine invertebrates, which are increasingly threatened by anthropogenic climate change. To investigate this phenomenon, larvae of the sea anemone and model marine invertebrateNematostella vectensiswere exposed to control (18 °C) or elevated (24 °C, 30 °C, 35 °C, or 39 °C) temperatures for 1 h at 3 days post-fertilization (DPF), followed by return to control temperatures (18 °C). The animals were then assessed for growth, development, metabolic rates, and heat tolerance at 4, 7, and 11 DPF. Priming at intermediately elevated temperatures (24 °C, 30 °C, or 35 °C) augmented growth and development compared to controls or priming at 39 °C. Indeed, priming at 39 °C hampered developmental progression, with around 40% of larvae still in the planula stage at 11 DPF, in contrast to 0% for all other groups. Total protein content, a proxy for biomass, and respiration rates were not significantly affected by priming, suggesting metabolic resilience. Heat tolerance was quantified with acute heat stress exposures, and was significantly higher for animals primed at intermediate temperatures (24 °C, 30 °C, or 35 °C) compared to controls or those primed at 39 °C at all time points. To investigate a possible molecular mechanism for the observed changes in heat tolerance, the expression of heat shock protein 70 (HSP70) was quantified at 11 DPF. Expression of HSP70 significantly increased with increasing priming temperature, with the presence of a doublet band for larvae primed at 39 °C, suggesting persistent negative effects of priming on protein homeostasis. Interestingly, primed larvae in a second cohort cultured to 6 weeks post-fertilization continued to display hormetic growth responses, whereas benefits for heat tolerance were lost; in contrast, negative effects of short-term exposure to extreme heat stress (39 °C) persisted. These results demonstrate that some dose-dependent effects of priming waned over time while others persisted, resulting in heterogeneity in organismal performance across ontogeny following priming. Overall, these findings suggest that heat priming may augment the climate resilience of marine invertebrate early life stagesviathe modulation of key developmental and physiological phenotypes, while also affirming the need to limit further anthropogenic ocean warming.