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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. 

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. 

Abstract 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.