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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., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2024. Published by The Company of Biologists Ltd.)

As climate change increases the rate of environmental change and the frequency and intensity of disturbance events, selective forces intensify. However, given the complicated interplay between plasticity and selection for ecological - and thus evolutionary - outcomes, understanding the proximate signals, molecular mechanisms and the role of environmental history becomes increasingly critical for eco-evolutionary forecasting. To enhance the accuracy of our forecasting, we must characterize environmental signals at a level of resolution that is relevant to the organism, such as the microhabitat it inhabits and its intracellular conditions, while also quantifying the biological responses to these signals in the appropriate cells and tissues. In this Commentary, we provide historical context to some of the long-standing challenges in global change biology that constrain our capacity for eco-evolutionary forecasting using reef-building corals as a focal model. We then describe examples of mismatches between the scales of external signals relative to the sensors and signal transduction cascades that initiate and maintain cellular responses. Studying cellular responses at this scale is crucial because these responses are the basis of acclimation to changing environmental conditions and the potential for environmental 'memory' of prior or historical conditions through molecular mechanisms. To challenge the field, we outline some unresolved questions and suggest approaches to align experimental work with an organism's perception of the environment; these aspects are discussed with respect to human interventions., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2023. Published by The Company of Biologists Ltd.)

In light of the chronic stress and mass mortality reef-building corals face under climate change, it is critical to understand the processes driving reef persistence and replenishment, including coral reproduction and development. Here, we quantified gene expression and sensitivity to ocean acidification across a set of developmental stages in the rice coral, Montipora capitata. Embryos and swimming larvae were exposed to pH treatments of 7.8 (ambient), 7.6 (low) and 7.3 (extreme low) from fertilization to 9 days post-fertilization. Embryo and larval volume, and stage-specific gene expression were compared between treatments to determine the effects of acidified seawater on early development. Although there was no measurable size differentiation between pH treatments at the fertilized egg and prawn chip (9 h post-fertilization) stages, early gastrulae and larvae raised in reduced pH treatments were significantly smaller than those raised in ambient seawater, suggesting an energetic cost to developing under low pH. However, no differentially expressed genes were found until the swimming larval stage. Notably, gene expression patterns of larvae developing at pH 7.8 and pH 7.3 were more similar than those of larvae developing at pH 7.6. Larvae from pH 7.6 showed upregulation of genes involved in cell division, regulation of transcription, lipid metabolism and response to oxidative stress in comparison to the other two treatments. Although low pH appears to increase energetic demands and trigger oxidative stress in larvae, the developmental process is robust to this at a molecular level, with the swimming larval stage reached in all pH treatments., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2022. Published by The Company of Biologists Ltd.)

Although low levels of thermal stress, irradiance and dietary restriction can have beneficial effects for many taxa, stress acclimation remains little studied in marine invertebrates, even though they are threatened by climate change stressors such as ocean acidification. To test the role of life-stage and stress-intensity dependence in eliciting enhanced tolerance under subsequent stress encounters, we initially conditioned pediveliger Pacific geoduck (Panopea generosa) larvae to ambient and moderately elevated PCO2 (920 µatm and 2800 µatm, respectively) for 110 days. Then, clams were exposed to ambient, moderate or severely elevated PCO2 (750, 2800 or 4900 µatm, respectively) for 7 days and, following 7 days in ambient conditions, a 7-day third exposure to ambient (970 µatm) or moderate PCO2 (3000 µatm). Initial conditioning to moderate PCO2 stress followed by second and third exposure to severe and moderate PCO2 stress increased respiration rate, organic biomass and shell size, suggesting a stress-intensity-dependent effect on energetics. Additionally, stress-acclimated clams had lower antioxidant capacity compared with clams under ambient conditions, supporting the hypothesis that stress over postlarval-to-juvenile development affects oxidative status later in life. Time series and stress intensity-specific approaches can reveal life-stages and magnitudes of exposure, respectively, that may elicit beneficial phenotypic variation., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)

The swiftly changing climate presents a challenge to organismal fitness by creating a mismatch between the current environment and phenotypes adapted to historic conditions. Acclimatory mechanisms may be especially crucial for sessile benthic marine taxa, such as reef-building corals, where climate change factors including ocean acidification and increasing temperature elicit strong negative physiological responses such as bleaching, disease and mortality. Here, within the context of multiple stressors threatening marine organisms, I describe the wealth of metaorganism response mechanisms to rapid ocean change and the ontogenetic shifts in organism interactions with the environment that can generate plasticity. I then highlight the need to consider the interactions of rapid and evolutionary responses in an adaptive (epi)genetic continuum. Building on the definitions of these mechanisms and continuum, I also present how the interplay of the microbiome, epigenetics and parental effects creates additional avenues for rapid acclimatization. To consider under what conditions epigenetic inheritance has a more substantial role, I propose investigation into the offset of timing of gametogenesis leading to different environmental integration times between eggs and sperm and the consequences of this for gamete epigenetic compatibility. Collectively, non-genetic, yet heritable phenotypic plasticity will have significant ecological and evolutionary implications for sessile marine organism persistence under rapid climate change. As such, reef-building corals present ideal and time-sensitive models for further development of our understanding of adaptive feedback loops in a multi-player (epi)genetic continuum., Competing Interests: Competing interestsThe author declares no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)

Coral reefs are globally threatened by climate change-related ocean warming and ocean acidification (OA). To date, slow-response mechanisms such as genetic adaptation have been considered the major determinant of coral reef persistence, with little consideration of rapid-response acclimatization mechanisms. These rapid mechanisms such as parental effects that can contribute to trans-generational acclimatization (e.g. epigenetics) have, however, been identified as important contributors to offspring response in other systems. We present the first evidence of parental effects in a cross-generational exposure to temperature and OA in reef-building corals. Here, we exposed adults to high (28.9°C, 805 µatm P(CO2)) or ambient (26.5°C, 417 µatm P(CO2)) temperature and OA treatments during the larval brooding period. Exposure to high treatment negatively affected adult performance, but their larvae exhibited size differences and metabolic acclimation when subsequently re-exposed, unlike larvae from parents exposed to ambient conditions. Understanding the innate capacity corals possess to respond to current and future climatic conditions is essential to reef protection and maintenance. Our results identify that parental effects may have an important role through (1) ameliorating the effects of stress through preconditioning and adaptive plasticity, and/or (2) amplifying the negative parental response through latent effects on future life stages. Whether the consequences of parental effects and the potential for trans-generational acclimatization are beneficial or maladaptive, our work identifies a critical need to expand currently proposed climate change outcomes for corals to further assess rapid response mechanisms that include non-genetic inheritance through parental contributions and classical epigenetic mechanisms., (© 2015. Published by The Company of Biologists Ltd.)

Regulating intracellular pH (pHi) is critical for optimising the metabolic activity of corals, yet the mechanisms involved in pH regulation and the buffering capacity within coral cells are not well understood. Our study investigated how the presence of symbiotic dinoflagellates affects the response of pHi to PCO2-driven seawater acidification in cells isolated from Pocillopora damicornis. Using the fluorescent dye BCECF-AM, in conjunction with confocal microscopy, we simultaneously characterised the pHi response in host coral cells and their dinoflagellate symbionts, in symbiotic and non-symbiotic states under saturating light, with and without the photosynthetic inhibitor DCMU. Each treatment was run under control (pH 7.8) and CO2-acidified seawater conditions (decreasing pH from 7.8 to 6.8). After 105 min of CO2 addition, by which time the external pH (pHe) had declined to 6.8, the dinoflagellate symbionts had increased their pHi by 0.5 pH units above control levels when in the absence of DCMU. In contrast, in both symbiotic and non-symbiotic host coral cells, 15 min of CO2 addition (0.2 pH unit drop in pHe) led to cytoplasmic acidosis equivalent to 0.3-0.4 pH units irrespective of whether DCMU was present. Despite further seawater acidification over the duration of the experiment, the pHi of non-symbiotic coral cells did not change, though in host cells containing a symbiont cell the pHi recovered to control levels when photsynthesis was not inhibited. This recovery was negated when cells were incubated with DCMU. Our results reveal that photosynthetic activity of the endosymbiont is tightly coupled with the ability of the host cell to recover from cellular acidosis after exposure to high CO2/low pH., (© 2014. Published by The Company of Biologists Ltd.)

To understand the effects of global climate change on reef-building corals, a thorough investigation of their physiological mechanisms of acclimatization is warranted. However, static temperature manipulations may underestimate the thermal complexity of the reefs in which many corals live. For instance, corals of Houbihu, Taiwan, experience changes in temperature of up to 10°C over the course of a day during spring-tide upwelling events. To better understand the phenotypic plasticity of these corals, a laboratory-based experiment was conducted whereby specimens of Seriatopora hystrix from an upwelling reef (Houbihu) and conspecifics from a non-upwelling reef (Houwan) were exposed to both a stable seawater temperature (26°C) regime and a regime characterized by a 6°C fluctuation (23-29°C) over a 12 h period for 7 days. A suite of physiological and molecular parameters was measured in samples of both treatments, as well as in experimental controls, to determine site of origin (SO) and temperature treatment (TT) responses. Only chlorophyll a (chl a) concentration and growth demonstrated the hypothesized trend of higher levels when exposed to a TT that mimicked SO conditions. In contrast, chl a, maximum dark-adapted quantum yield of photosystem II (F(v)/F(m)), and Symbiodinium ribulose-1,5-bisphosphate carboxylase/oxygenase (rbcL), photosystem I (psI, subunit III) and phosphoglycolate phosphatase (pgpase) mRNA expression demonstrated significant TT effects. Specifically, levels of these response variables were higher in samples exposed to a variable temperature regime, suggesting that S. hystrix may acclimate to fluctuating temperatures by increasing its capacity for photosynthesis.