Physiological responses to acute warming at the agitation temperature in a temperate shark

Abstract

Thermal tolerance and associated mechanisms are often tested via the critical thermal maximum (CTMax). The agitation temperature is a recently described thermal limit in fishes that has received little mechanistic evaluation. The present study used a temperate elasmobranch fish to test the hypothesis that this thermal tolerance trait is partially set by the onset of declining cardiorespiratory performance and the cellular stress response. Pacific spiny dogfish (Squalus suckleyi) were screened for cardiorespiratory and whole-organism thermal limits to test for associations between thermal performance and tolerance. Then, biochemical markers of secondary stress, aerobic and anaerobic enzyme activities, and molecular markers of cellular stress were determined for various tissues at the agitation temperature, and secondary stress markers were determined at CTMax. In dogfish, the agitation temperature was characterised by increased turning activity within experimental chambers and was equal to the temperature where dogfish exhibited maximum heart rate. Citrate synthase activity increased at the agitation temperature in white muscle relative to unmanipulated dogfish. Further, lactate dehydrogenase activity and accumulated lactate in the plasma and muscle were not affected by acute warming. Cellular stress was apparent in hypothalamus, gill filament, and ventricle, denoted by elevated transcript abundance of hsp70, but not hif1α. Conversely, CTMax was characterised by metabolic acidosis driven by anaerobic lactate production, signifying an increased reliance on anaerobic metabolism between the agitation temperature and CTMax. Together, these data provide partial support for our hypothesis, in that cellular stress, but not declining thermal performance, occurred at the agitation temperature.

Behavioural responses to acute warming precede critical shifts in the cellular and physiological thermal stress responses in fish

“…The agitation temperature of 22.0 ± 1.4 °C from this study falls within this expected range, and the activation of several genes at the agitation treatment temperature, suggests that a shift in the cellular response to temperature occurs at the onset of thermal avoidance behaviour. Similar results were observed in Pacific spiny dogfish ( Squalus suckleyi ) where they showed a cellular stress response occurred at the agitation temperature (Bouyoucos et al, 2023). Morrison et al (2020) showed that CT max generally increased with acclimation temperature in Brook Trout, however, CT max plateaued at acclimation temperatures above 20 °C that coincided with a decrease in hepatosomatic index, and an increase in plasma lactate.…”

“…Studies that assess thermal endpoints can provide a general understanding of when fish display a behavioural reaction to a thermal threshold, however, such studies do not provide insight into sub-organismal responses of the fish. Despite the potential utility of identifying behavioural avoidance responses to thermal stress in fishes, relatively little is known about the physiological mechanisms that coincide with the agitation temperature in fishes (Bouyoucos et al 2023).…”