Marine heatwaves (MHWs) have become more common in the past decade as a result of the continuous rise in Earth’s air surface temperatures which is mostly caused by rapidly increasing concentrations of atmospheric carbon dioxide (Horton et al., 2016). MHWs are defined as anomalies in seawater temperatures which are considerably greater than any previous levels that have been used in the past (Marin et al., 2021). The frequency, severity, and duration of MHWs are projected to rise dramatically in a rapidly changing marine environment, causing profoundly ecological and economic repercussions (Wernberg et al., 2023).

Throughout the past 20 years, MHWs have become more severe, recurrent, and longer in coastal ecosystems, especially attacking intertidal zones that support a very productive coastal environment (Masanja et al., 2023; Whalen et al., 2023). The thermal conditions in intertidal regions, specifically in subtidal zones, undergo substantial changes that surpass the fluctuations observed in ocean water temperatures, both in terms of amplitude and variability (Dong et al., 2022). Therefore, when MHWs occur, intertidal species are susceptible to abrupt changes in the environment and exceptionally high temperatures. This can result in a series of interconnected ecological consequence (He et al., 2021; Smith et al., 2023). There has been also a surge in the occurrence, duration, and severity of MHWs in China’s coastal areas (Yao et al., 2020; Li et al., 2023). The Bohai Bay, which is known for its abundant fishing opportunities, has been severely affected by intensifying MHWs events during summertime (Yao et al., 2020). MHWs can potentially have catastrophic effects, such as the bleaching of corals in tropical and subtropical environments, as well as the mass mortality events of marine bivalves on a wide scale (Holbrook et al., 2020; Smith et al., 2023).

Thus, projecting marine organism and ecosystem responses to MHWs is a global ecological problem (Smith et al., 2023). Despite the increasing prevalence of MHWs at an unprecedented rate, there remains significant uncertainty surrounding the response of economically and ecologically relevant organisms to the intensification of MHWs (Garrabou et al., 2022; Smith et al., 2023). MHWs may cause profound impacts at various levels of biological organization on marine bivalves, including hindering metabolism, reducing energy reserves, impairing reproduction, and triggering dysbiosis at the molecular level (Masanja et al., 2023). Encompassing population feedback down to the molecular level can hence provide a more accurate assessment of the effects of MHWs on marine bivalves and their ecosystems. In particular, these observations can be broadly expressed in terms of energy, as energy balance is crucial in determining the ability to tolerate and respond to stress (Sokolova et al., 2012). Indeed, thermal stress can affect various aspects of the allocation of available resources for energy consumption in bivalves, including obtaining energy by consuming food and breaking it down through digestion, as well as energy expenditure through respiration and excretion (Dong et al., 2018; Talevi et al., 2023). During periods of prolonged MHWs events, the intense thermal stress can significantly impact the distribution of energy between crucial physiological processes and functions associated with fitness, as demonstrated in the case of the hard clam Mercenaria mercenaria (Hu et al., 2022) and many other bivalve species (Liu et al., 2023; Shen et al., 2023; Talevi et al., 2023). When marine bivalves are exposed to temperatures that exceed their thermal tolerance limits, they may experience either internal hypoxia or hyperoxia (Lattos et al., 2023; Xu et al., 2023). An important metric for the total energy budget, the scope for growth (SFG), might fall sharply as a consequence of this thermal stress. It is possible to swiftly identify the energy state using the SFG approach, which provides a significant insight into the thermal stress response as a result (Ezgeta-Balić et al., 2011; Filgueira et al., 2011). As far as we know, however, there has been limited research on the physiological energy requirements of marine bivalves in relation to increasing MHWs in intertidal habitats.

The present study aimed at gaining a better understanding of the response of the ecologically and economically hard clam M. mercenaria to intensifying MHWs in the Bohai Sea. We exposed clams to simulated continuous and recurrent scenarios of MHWs. Physiological energetics were then assessed by encompassing the essential energetic processes such as feeding, digesting, respiration, excretion, and the energy budget exemplified by the SFG. Given that many previous studies have shown that intertidal bivalve species can survive in very tough conditions (He et al., 2021; Milan et al., 2023), we hypothesize that M. mercenaria might be able to cope with MHWs that nowadays frequently attack their habitats in the Bohai Sea.

The following is evidence of the physiological energetics of heatwave responses in hard clams. Figure 2 demonstrates a statistically significant CR (p< 0.05). A notable interaction effect exists between temperature and time. This suggests variations in the temporal patterns between the two MHWs scenarios. CR ranged from 0.54 to 1.13 L h^{- 1} g^{- 1}. The P-MHW group showed a downward trend during the 30°C stress, especially on the 35 day of the experiment, which was significantly lower than that the other two experimental groups. Even when the temperature returned to 25°C for one week, it was still significantly lower than that of the control group (p< 0.05). The clearance rate of the R-MHWs group showed a fluctuating trend during the experiment that increased with the onset of heat waves but decreased with the recovery of temperature.

The severity and length of the heatwave and the interaction between these two factors significantly influenced the AE (p< 0.05), as shown in Figure 3 . Absorption efficiency varied over a wide range (39.3-67.0%). Over time, there was an increased first and then decreased under prolonged MHW stress in the P-MHW group, especially on day 35, which was significantly lower than that of other experimental groups (p< 0.05). However, when the temperature was returned to 25°C for one week, it also returned to normal levels. AE of R-MHW group increased during the first thermal stress and decreased after the MHWs disappeared.

Statistically, there is a significant effect of time on RR and a significant interaction effect between temperature and time (p< 0.05; Figure 4 ); Under heat stress, RR of the P-MHW group showed a similar pattern to that of AE, a significant difference was observed between P-MHW and control at day 35. The RR of R-MHW group increased strongly when experiencing the second heat wave stress, which was significantly higher than that of the control group (p< 0.05).

There has been an overall increasing trend in excretion rates across both temperature conditions over time. Statistically, there is a significant main effect of time (p< 0.05; Figure 5 ). However, there were no significant effects of temperature or interaction.

The temporal pattern shows excretion rates increase relatively consistently over time under both persistent and repeated heatwave conditions. The lack of a statistically significant temperature or interaction effect implies that the impact of MHWs on excretion rates is minimal.

There is no clear trend in the O:N ratio over time under either temperature condition. The O:N ratio fluctuates but remains relatively stable. Statistically, no significant main effect of time, temperature, or their interaction exists on the O:N ratio. The lack of a temporal pattern or temperature effect indicates that prolonged exposure to elevated temperatures from marine heatwaves does not impact the O:N ratio. The O:N ratio varies between 10.0 and 14.1 over time in the control and both experimental groups, with no clear directionality. The lack of significant effects implies that hard clams maintain stable oxygen-to-nitrogen waste excretion ratios despite heatwave conditions and over long periods (p > 0.05; Figure 6 ).

According to Figure 7 , there were notable impacts on the potential for growth from the length and interaction with heatwave intensity (p< 0.05). Persistent heatwave exposure (on day 35) resulted in a significant decrease (p< 0.05; Figure 7 ). The SFG values of the P-MHW group were still significantly lower than those of the control and repeated heatwave groups (p<0.05), even after a week of temperature recovery (day 35 and 42).

Given the imminent rise in the occurrence of MHWs, it is crucial to understand the mechanisms by which marine bivalves can recover from MHWs. This understanding is essential in determining their overall response to MHWs. In this study, we examined the physiological energy responses of hard clams as they adapted to continuous and repeated MHWs. Our research indicates that intertidal clams have the ability to withstand and endure marine heatwaves MHWs.

Previous studies on marine bivalves have observed a statistically significant and consistent adaptive ability in the clam’s clearance rate in response to the interaction between temperature and time (Kittner and Riisgård, 2005; Pernet et al., 2007). Riisgård (2001) also noted a similar temporal pattern in the clearance rate at which the clam Ruditapes philippinarum, with an initial decrease followed by a return to normal levels following prolonged exposure to a heat stress. These findings suggest that metabolic adaptation may enable the clearance rate to recover after an initial decrease caused by sudden exposure to high temperatures. Our results align with those of Kittner and Riisgård (2005), who observed a similar adaptation trend in the clearance rates of Mytilus edulis under heat stress. The consistent reaction of different clam species offers compelling evidence of the temporal metabolic adaptation that allows the clearance rate to settle following the initial shock of a heatwave.

Further, the significant decline in absorption efficiency under continuous heatwaves mirrors the patterns reported for other bivalves under thermal stress. For example, Talevi et al. (2023) noted decreasing absorption efficiency in the Manila clam R. philippinarum as heatwave durations increased. They attributed this to potential damage to the clams’ digestive system, hampering food absorption. The current study’s findings match those of Domínguez et al. (2021), who reported impaired absorption efficiency in the Cerastoderma edule after prolonged exposure to elevated temperatures. Comparatively, M. mercenaria appears similarly vulnerable to digestive disruption from metabolic stress during extended heatwaves. However, the absorption efficiency exhibited recovery tendencies once heatwave conditions ended. This suggests the digestive impairment may be reversible once temperatures return to normal ranges.

The marked increase in respiration rate of M. mercenaria aligns with previous evidence of bivalves’ metabolic responses to thermal stress. For instance, Trigos et al. (2015) noted significantly elevated respiration in Pinna nobilis under thermal stress. They attributed this to increased energetic costs for ventilation and circulation to manage elevated oxygen demand and respiratory acidosis. Furthermore, the current study’s findings converge with those of Bosch-Belmar et al. (2023), who reported increased respiration rates in the Mediterranean Sponge Chondrilla nucula under experimentally induced heat stress. The comparable responses of varying marine organisms add robustness to the concept of increased respiration as a metabolic adaptation to fulfill elevated energy requirements under thermal stress.

There has been an overall increasing trend in excretion rates across both temperature conditions over time. However, there were no significant effects of temperature or interaction. The temporal pattern shows excretion rates increase relatively consistently over time under both control and heatwave conditions. The lack of a statistically significant temperature or interaction effect implies that the impact of MHWs on excretion rates is minimal. M. mercenaria’s lack of significant change in excretion rate due to thermal stress parallels prior observations in M. edulis (Barrento et al., 2013). This contrasts with studies like those that noted increased excretion in M. edulis (Barrento et al., 2013) and Corbicula fluminea (Xiao et al., 2014) under warming conditions. The variance suggests potential species-specific differences in metabolic responses. However, M. mercenaria’s stable excretion rates align with the findings of Scapharca subcrenata (Jiang et al., 2020) under simulated heat stress. Metabolically, this may indicate the capacity of M. mercenaria to maintain waste excretion rates despite thermal stress without the need for physiological adjustment. Comparatively, this area requires further research across bivalve species to determine adaptation patterns.

The O:N ratio can be a useful indicator for determining the relative contribution of carbohydrate metabolism versus protein catabolism in bivalves. During aerobic respiration, when there is sufficient oxygen available, carbohydrates such as glycogen break down to produce carbon dioxide (CO₂), water (H₂O), and energy. When oxygen levels are low or carbohydrate stores are depleted, bivalves resort to anaerobic respiration or protein breakdown to meet their energy needs. A study on Haliotis discus hannai (Kang et al., 2019) exemplifies this. Because of this, the link between the amount of oxygen to nitrogen and the rise in MHWs suggests that M. mercenaria may be able to use its own energy to deal with physical problems. According to Hu et al. (2022), if the claim that energy supply increases during heatwaves is true, it seems likely that M. mercenaria can easily distribute energy among its different body systems in a way that follows the rules of energy management in stress adaptation and resilience.

The energy balance is crucial in determining the extent to which marine bivalves can withstand, adjust to, and ultimately adapt to heatwaves. Considering the assimilation of energy from food and native nutrients, as well as the energy used in respiration and excretion, the SFG can provide a thorough understanding of M. mercenaria’s probable response to heatwaves. Heatwave exposure to the clams led to a significant reduction in SFG, suggesting that clams under heatwave stress likely redirected their energy resources towards vital physiological functions. This discovery aligns with previous studies conducted on clams subjected to thermal stress Paphia undulata (Han et al., 2008) and R philippinarum (Zhang et al., 2018). These studies indicate that the fast rise in metabolic requirements is the probable cause of the susceptibility of SFG to high temperatures.

This finding suggests that components of the energy budget that are energetically efficient may display versatility. The findings suggest that M. mercenaria may possess the capacity to mitigate physiological effects during heatwaves. Hence, SFG serves as a measure of both the development and reproduction capabilities of organisms, as well as their ability to cope with impending stressors.

Overall, this study shows that hard clams effectively counteract the physiological effects caused by frequent heatwaves. Based on the observation that physiological energies exist, it is feasible to obtain a glance into mechanisms supporting such abilities. Processes that are of utmost relevance in determining the fate of M. mercenaria in a sea that is quickly warming require additional exploration. These processes are particularly important at the most fundamental levels of biological structure, such as the levels of biochemistry and molecular structure. This information will provide insight into the combined impact of biological incursions and global change on intertidal ecosystems.

The original contributions presented in the study are included in the article/ Supplementary Material . Further inquiries can be directed to the corresponding authors.

The manuscript presents research on animals that do not require ethical approval for their study.

JL: Writing – original draft. FM: Writing – review & editing. YL: Writing – review & editing. YG: Writing – review & editing. YD: Writing – review & editing. LZ: Writing – review & editing.