An energetic conundrum: contradictory relationship between energetic state and heat tolerance during progressive air exposure in a tropical high-shore gastropod

High-shore intertidal gastropods experience energy-demanding thermo-dehydrative stressful conditions during air emersion, related to their vertical position and the habitat heterogeneity. Simultaneously, these gastropods are forced to downregulate metabolism when resting in air to limit dehydration and ensure energetic homeostasis under conditions of constrained food (energy) intake, due to prolonged inactivity. We investigated this apparent conundrum by studying the temporal patterning of metabolic depression and the influence of depressed metabolism on heat tolerance of the tropical high-shore snail, Planaxis sulcatus, during progressive air emersion. We compared cardiac thermal performance (a proxy for metabolic performance) of snails pre-exposed to different periods of air emersion (field fresh, 5 d and 10 d) and different levels of dehydration and heat stress, mimicking naturally sunned or shaded resting habitats. Compared to early air emersion, long resting periods under benign (shaded) conditions suppressed cardiac thermal performance and elevated heat tolerance, responses mostly not modified by dehydration or heat stress. Cardiac (energetic) suppression was temporally idiosyncratic among individuals, becoming more uniform with longer air emersion. Reanalyzed data comparing higher and lower metabolic (energetic) states across the treatments showed greater heat tolerance in lower-energetic snails. The apparent energetic conundrum of simultaneously needing to support energetically-demanding protective heat tolerance and energetically-conserving metabolic depression can be explained by an early highly energy-demanding preparatory stage, which hardens snails for the duration of aestivation, irrespective of the resting habitat conditions. Our observed temporal patterning of metabolism provides an excellent framework for molecular and cellular investigation of high-shore snails.