Timing Metabolic Depression: Predicting Thermal Stress in Extreme Intertidal Environments

Hui, Tin Yan; Dong, Yun‐wei; Han, Guodong; Lau, Sarah L.Y.; Cheng, Martin C.F.; Meepoka, Chayanid; Ganmanee, Monthon; Williams, Gray A.

doi:10.1086/710339

Cited by 34 publications

(29 citation statements)

References 65 publications

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“…In the rocky intertidal zone, the upper boundaries to vertical distributions are typically set by tolerance to physical factors and lower boundaries by biotic interactions (Connell, 1961). The temporal and spatial pattern of temperature distribution could be exploited over evolutionary time to adjust physiological strategies by responding to critical environmental signals, to actively depress metabolism (Anestis et al, 2007; Hui et al, 2020). These results indicate that the shapes of cTPCs of intertidal species are reflective of the particular environment a species encounters, and that heat‐induced metabolic depression is a physiological adaptation to the extreme thermal stress when exposed to full sun in the splash zone and high shore.…”

Section: Discussionmentioning

confidence: 99%

Physiological determinants of biogeography: The importance of metabolic depression to heat tolerance

Liao

Gao-yang

Wang

et al. 2021

Global Change Biology

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A quantitative understanding of physiological thermal responses is vital for forecasting species distributional shifts in response to climate change. Many studies have focused on metabolic rate as a global metric for analyzing the sublethal effects of changing environments on physiology. Thermal performance curves (TPCs) have been suggested as a viable analytical framework, but standard TPCs may not fully capture physiological responses, due in part to failure to consider the process of metabolic depression. We derived a model based on the nonlinear regression of biological temperature‐dependent rate processes and built a heart rate data set for 26 species of intertidal molluscs distributed from 33°S to ~40°N. We then calculated physiological thermal performance limits with continuous heating using T1false/2H, the temperature at which heart rate is decreased to 50% of the maximal rate, as a more realistic measure of upper thermal limits. Results indicate that heat‐induced metabolic depression of cardiac performance is a common adaptive response that allows tolerance of harsh environments. Furthermore, our model accounted for the high inter‐individual variability in the shape of cardiac TPCs. We then used these TPCs to calculate physiological thermal safety margins (pTSM), the difference between the maximal operative temperature (95th percentile of field temperatures) and T1false/2H of each individual. Using pTSMs, we developed a physiological species distribution model (pSDM) to forecast future geographic distributions. pSDM results indicate that climate‐induced species range shifts are potentially less severe than predicted by a simple correlative SDM. Species with metabolic depression below the optimum temperature will be more thermal resistant at their warm trailing edges. High intraspecific variability further suggests that models based on species‐level vulnerability to environmental change may be problematic. This multi‐scale, mechanistic understanding that incorporates metabolic depression and inter‐individual variability in thermal response enables better predictions about the relationship between thermal stress and species distributions.

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Section: Discussionmentioning

confidence: 99%

Physiological determinants of biogeography: The importance of metabolic depression to heat tolerance

Liao

Gao-yang

Wang

et al. 2021

Global Change Biology

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“…These results indicate that metabolic depression enables the snail to maintain a relatively low metabolic rate for surviving intermediate high temperatures. This capacity is an important physiological adaptation against thermal stress for the species inhabiting the high intertidal zone Hui et al, 2020). These results also imply that anaerobic metabolism should be an important alternative or supplementary source of energy supply for coping with the elevated energy requirements in the face of thermal stress.…”

Section: Anaerobic Metabolism and Metabolic Depression Under Thermal Stressmentioning

confidence: 92%

“…Maintaining an adequate supply of energy to support the cellular stress response as well as normal metabolic requirements is essential for surviving at high temperature. Moreover, high temperature and hypoxia commonly co-occur in intertidal molluscs (Deutsch et al, 2020), and, under these combined stresses, animals either have to maintain a low aerobic metabolic rate or provide energy via anaerobic metabolism (Han et al, 2017;Hui et al, 2020;Meng et al, 2018). According to the cardiac Fig.…”

Section: Anaerobic Metabolism and Metabolic Depression Under Thermal Stressmentioning

confidence: 99%

Temperature adaptations of the thermophilic snail Echinolittorina malaccana: insights from metabolomic analysis

Chen

Wang

Liao

et al. 2021

Journal of Experimental Biology

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The periwinkle snail Echinolittorina malaccana, whose upper lethal temperature is near 55°C, is one of the most heat-tolerant eukaryotes known. We conducted a multi-level investigation, including cardiac physiology, enzyme activity, and targeted and untargeted metabolomic analysis, that elucidated a spectrum of adaptations to extreme heat. All systems examined showed heat intensity-dependent responses. Under moderate heat stress (from 37 to 45°C) the snail depressed cardiac activity and entered a state of metabolic depression. The global metabolomic analyses and enzymatic analysis showed that the depressed metabolic state under moderate heat stress entailed production of metabolites characteristic of oxygen-independent pathways of ATP generation (lactate and succinate), which suggests that anaerobic metabolism was the main energy supply pathway under heat stress (from 37 to 52°C). The metabolomic analyses also revealed alterations in glycerophospholipid metabolism under extreme heat stress of 52°C, which likely reflected adaptive changes to maintain membrane structure. Small molecular mass organic osmolytes (glycine betaine, choline, and carnitine) showed complex changes in concentration that were consistent with a role of these protein-stabilizing solutes in protection of the proteome under heat stress. This thermophilic species thus can deploy a wide array of adaptive strategies to acclimatize to extremely high temperatures.

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“…Similarly, the saltmarsh crustacean Sphaeroma rugicauda tends to switch to temperature-independent metabolism during exposure to high temperatures in summer months (Marsden, 1979). This strategy allows conservation of respiratory substrates/oxygen that would otherwise be used to meet elevated metabolic demands during severe thermal stress, which will likely occur if the environmental temperature exceeds the critical physiological temperature (Hui et al, 2020). The depression of metabolism in T. crenata under oxygen undersaturation naturally occurs during the night and is paralleled by a marked thermal insensitivity, when respiration by autotrophs reduces water oxygen saturation in mangroves, seagrasses and coral reefs (Giomi et al, 2019).…”

Section: Flexible Metabolic Performance In Heterogeneous Environmentmentioning

confidence: 99%

Dissolved Oxygen in Heterogeneous Environments Dictates the Metabolic Rate and Thermal Sensitivity of a Tropical Aquatic Crab

et al. 2021

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Oxygen availability, together with water temperature, greatly varies in coastal habitats, especially in those characterized by elevated primary production. In this study, we investigate the combined role of dissolved oxygen and temperature on the thermal physiological response of the mud crab Thalamita crenata living in an equatorial system of coastal habitats. We sampled temperature, oxygen and salinity in T. crenata habitats, mangrove creeks and fringes and seagrass meadows, at Gazi Bay (Kenya). We found that seagrass meadows exhibited higher temperature and oxygen saturation than the mangrove habitats during the day, creating conditions of oxygen supersaturation. By investigating the effect of different levels of oxygen saturation on the thermal response of T. crenata, we demonstrated that the respiratory physiology of this ectotherm has a pronounced resistance to heat, directly influenced by the amount of dissolved oxygen in the water. Under low oxygen saturation levels, the mud crab significantly reduced its metabolism, becoming temperature-independent. This result shows that aquatic species can modulate their thermal response in a stringent dependency with water oxygen saturation, corroborating previous findings on the thermal response of T. crenata under supersaturation. This contribution provides further support for the need to adopt an ecologically-relevant approach to forecast the effect of climate change on marine ectothermal species.

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Timing Metabolic Depression: Predicting Thermal Stress in Extreme Intertidal Environments

Cited by 34 publications

References 65 publications

Physiological determinants of biogeography: The importance of metabolic depression to heat tolerance

Physiological determinants of biogeography: The importance of metabolic depression to heat tolerance

Temperature adaptations of the thermophilic snail Echinolittorina malaccana: insights from metabolomic analysis

Dissolved Oxygen in Heterogeneous Environments Dictates the Metabolic Rate and Thermal Sensitivity of a Tropical Aquatic Crab

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