Abstract
Predictions for climate vulnerability of ectotherms have focused on performance-enhancing physiology, even though an organism’s energetic state can also be balanced by lowering resting maintenance costs. Adaptive metabolic depression (hypometabolism) enables animals to endure food scarcity, and physically extreme and variable environmental conditions. Hypometabolism is common in terrestrial and intertidal marine gastropod species, though this physiology and tolerance of environmental change are poorly understood in subtidal benthic gastropods. We investigated oxygen limitation tolerance, hypometabolism and thermal performance in the subtidal, tropical snail Turritella bacillum. Survival, cardiac activity and oxygen debt repayment were determined when oxygen uptake was limited by gill function impairment (air exposure) or exposure to hypoxic seawater. Thermal performance and tolerance were assessed from survival and cardiac performance when heated. The ability of snails to regulate metabolism during oxygen limitation was demonstrated by their tolerance of air exposure (>36 h) and hypoxia (>16 h), rhythmicity and reversibility of bradycardia, and inconsistent anaerobic compensation. Under acute heating, mean heart rate was temperature-insensitive in water and temperature-dependent in air. Converging or peaking of individual heart rates during heating suggest maximization of thermal performance at 38–39°C, whereas survival and heartbeat flatlining suggest an upper thermal limit exceeding 42°C. Snails survived 16 h in seawater at 38°C. Their metabolic regulation complies with the oxygen-limiting, sediment-burrowing lifestyle of the species. Although a tropical organism, the species’ thermal tolerance so far exceeds present habitat temperatures as to question its susceptibility to centennial climate warming. Our findings reveal the importance of knowing the metabolic regulatory capabilities and conserved physiological attributes of species used in climate vulnerability tests. Studies of ectotherm climate vulnerability that identify generalized trends based on physiologically similar animals may be misleading by missing information on physiological diversity.
Highlights
Metabolic rate depression is seen in most metazoan groups, especially among animals that hibernate, estivate or undergo diapause (Storey and Storey, 1990; Guppy and Withers, 1999; Marshall et al, 2011)
Survival and Cardiac Activity All snails (100%) survived air exposure for up to 36 h, though 100% mortality occurred during 48 h exposure
Reduced cardiac activity often signals metabolic depression (Marshall and McQuaid, 1991, 1993, 2011; Marshall et al, 2004), we could not reconcile the heart rate (HR) of T. bacillum snails with their low oxygen uptake rates in air or hypoxic seawater
Summary
Metabolic rate depression (hypometabolism) is seen in most metazoan groups, especially among animals that hibernate, estivate or undergo diapause (Storey and Storey, 1990; Guppy and Withers, 1999; Marshall et al, 2011). Climate vulnerability models for ectotherms focus on the maximization of performance and energy intake relative to temperature, to the exclusion of processes that achieve energetic equilibrium by lowering resting metabolic demand (Brown et al, 2004; Seibel and Drazen, 2007; Sinclair et al, 2016; Huey and Kingsolver, 2019; but for alternatives, see Quévreux and Brose, 2019). To some extent this is understandable as the capability of hypometabolism is limited in many key animal groups, while in others (such as gastropods) its phylogenetic distribution is poorly known. Omitting this aspect of the energy equation challenges the views founded on performance maximization that tropical and marine ectotherms are likely to be especially threatened by climate warming (Deutsch et al, 2008, 2015; Huey et al, 2009; Pinsky et al, 2019)
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