Cardiac performance mirrors the passive thermal tolerance range in the oyster <i>Ostrea edulis</i>

Increasing frequencies of heatwaves threaten marine ectotherm species but not all alike. In exposed habitats, some species rely on a higher capacity for passive tolerance at higher temperatures, thereby extending time-dependent survival limits. Here, we assessed how the involvement of the cardiovascular system in extended tolerance at the margins of the thermal performance curve is dependent on warming rate. We studied organismal and heart tissue cellular responses of the European oyster, Ostrea edulis, challenged by rapid warming (+2°C per hour) and gradual warming (+2°C per 24 h). Starting at 22°C, cardiac activity was monitored as temperature was increased, tracking cardiac performance curves. Hearts were collected at discrete temperatures to determine cardiomyocyte metabolic profiles. Heart rate peaked at a lower Arrhenius breakpoint temperatures (ABT) of 30.5°C under rapid warming versus 33.9°C under gradual warming. However, oysters survived to higher temperatures under rapid than under gradual warming, with half of oysters dying (LT50) by 36.9°C versus 34.8°C, respectively. As rapid warming passed 30°C, heart rate fell and cardiomyocyte metabolic profiles suddenly changed as oysters switched to anaerobic metabolism for survival. By 36°C, severe fluctuations in Krebs cycle-related metabolites accompanied cardiac failure. In contrast, oysters exposed to gradual warming made gradual, extensive adjustments to intracellular metabolic pathways, prolonging aerobic cardiomyocyte metabolism to higher temperatures. This extended survival duration and ABT, beyond which cardiac activity decreased sharply and ceased. Our results emphasize how the rate of warming forces a trade-off between temperature maxima and survival duration, via tissue- and cellular-level impacts. European oysters possess adaptations that enable extended tolerance and survival of intertidal populations.