Metabolic Regulation, Oxygen Limitation and Heat Tolerance in a Subtidal Marine Gastropod Reveal the Complexity of Predicting Climate Change Vulnerability

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.

Microclimate drives intraspecific thermal specialization: conservation perspectives in freshwater habitats

“…On a short time scale, M. etrusca appears to periodically aestivate, purportedly to avoid the prolonged exposure to high water temperatures. We suggest that during this phase, M. etrusca undergoes to short-term metabolic adjustment (likely hypometabolism as described by Marshall and McQuaid, 2020 ). As a matter of fact, individuals are observed active in the water across every season ( Bartolini et al , 2017 ).…”

“…Aestivation is the behaviour of withdrawal into the shell, which associates with aerobic hypometabolism (adaptive, as compared to metabolic depression, which implies either an adaptive or a capacity limited response; e.g. Marshall and McQuaid, 2020 ). Under severe environmental conditions, snails can even switch to anaerobic facultative metabolism while aestivating (e.g.…”

Thermal fluctuations independently modulate physiological plasticity and the dynamics of the gut microbiome in a tropical rocky shore oyster

“…For high-shore intertidal ectotherms, metabolic depression is an adaptive response that allows them to cope with extreme and stressful thermal conditions (Hui et al, 2020; Marshall et al, 2011; Sokolova and Pörtner, 2001). This physiological adjustment is a common signal that the animal is under thermal stress and acts as a strategy to conserve energy required for critical functions during normal metabolic resumption (i.e., less stressful thermal conditions; Hand and Hardewig, 1996; Marshall and McQuaid, 2020). Metabolic depression is also known to be an important mechanism to reduce/avoid the over-production of harmful ROS that results from the rapid increase in metabolic demands under elevated temperatures (Abele et al, 2002; Storey and Storey, 2004).…”

An evolutionary estuarine incursion: molecular differentiation and niche separation in BorneanIndothaissnails (Rapaninae, Muricidae)

“…The relatively high nucleotide diversity of I. gradata, which is far more abundant than the other species, aligns with its capacity to establish relatively large populations. The success of this species in highly variable estuarine environments must partly relate to its physiological plasticity, specifically its capacity to regulate energy metabolism and adjust feeding and reproduction in ways appropriate to changes in the environmental conditions (Marshall, 2009;Proum et al, 2017;Marshall & McQuaid, 2020). A population with a larger and more variable gene pool has a greater potential for local adaptation and habitat diversification.…”