Inactivity and the Passive Slowing Effect of Cold on Resting Metabolism as the Primary Drivers of Energy Savings in Overwintering Fishes

Abstract

Winter dormancy is a seasonal survival strategy common among temperate ectotherms, characterized by inactivity, fasting, and low metabolic rates. Previous reports of metabolic rate depression (MRD) in winter-dormant ectotherms, including many fishes, may result from confounding influences of temperature-dependent variation in activity on metabolic rate measurements. We hypothesize that, as demonstrated recently in the winter-dormant cunner (Tautogolabrus adspersus), inactivity and the passive physicochemical (Arrhenius) effect of cold on standard metabolic rate (SMR) are the common primary mechanisms underlying the low metabolic rates among winter-dormant fishes. Using automated video tracking, we investigated threshold temperatures for winter dormancy onset (major reductions in activity, increased sheltering, and fasting) in four phylogenetically-diverse teleost species reported to be winter dormant: cunner, pumpkinseed sunfish (Lepomis gibbosus), American eel (Anguilla rostrata), and mummichog (Fundulus heteroclitus). All species showed large activity and feeding reductions, but the magnitude of change and dormancy threshold temperature was species-specific. We propose that a continuum of overwintering responses exists among fishes from dormant to lethargic to active. The relationship between activity and metabolic rate was then measured using video-recorded automated respirometry during acute cooling and following cold acclimation in pumpkinseed, mummichog, and eel. In all species, activity and metabolic rate were strongly correlated at all temperatures, and cooling caused reduced activity and metabolic rate. When variation in activity was controlled for across temperatures spanning the dormancy thresholds, the thermal sensitivity of metabolic rate including SMR indicated the predominance of passive physicochemical influences (mean Q10<3.5), rather than active MRD. Activity reductions and physicochemical slowing of metabolism due to cold appear to be the primary energy saving mechanisms in overwintering fishes.