Metabolic plasticity facilitates a high-latitude life of feast and famine in Arctic char

Summary High northern latitudes experience extreme winters and pronounced environmental variation. Arctic animals possess remarkable and diverse physiological mechanisms to thrive under this variation, but such mechanisms are poorly studied, particularly in the aquatic realm. We combined Arctic field and laboratory experiments to reveal how one of Earth’s most northerly distributed fish species, the Arctic char, seasonally adjusts its metabolism to conserve energy over winter while not feeding and to capitalize on more optimal growth conditions in summer. Laboratory reared Arctic char were fed or food deprived at common summer (8°C) and winter (2°C) temperatures for >120 days. Oxygen consumption rates were assessed as a proxy for rate of aerobic metabolic energy expenditure. Cooling from 8 to 2°C reduced resting aerobic energy expenditure by 35%, while food deprivation independently drove a reduction of 46-50%. Combined, resting energy expenditure was 197% higher under simulated summer (fed at 8°C) than winter conditions (food deprived at 2°C). Reductions in resting energy expenditure with food deprivation were driven, at least in part, by marked tissue-specific decreases in organ size and protein synthesis rates in tissues with central roles in growth and digestion. Wild adult anadromous Arctic char exhibited, seasonal plasticity consistent with our laboratory experiments. Resting energy expenditure at 10°C was 27% higher after summer feeding than in the spring after winter fasting, while liver and digestive organ masses were also markedly reduced overwinter. In contrast, peak aerobic metabolic performance and relative heart mass were largely maintained during food deprivation indicating a protection of systems that support aerobic metabolic capacity. Despite recruiting strategies for substantial energy savings, wild and laboratory reared Arctic char still largely depleted their on-board fat stores with food-deprivation, underscoring that these strategies are essential when food is limited. Given that the Arctic is among the most rapidly changing regions on Earth, temperatures, productivity, and the timing of key seasonal event are all shifting with implications for the efficacy of such strategies for high-latitude animals.