Peak Sustained Metabolic Rate and Its Individual Variation in Cold-Stressed Mice

Abstract

Is long-term sustained metabolic rate (SusMR) subject to a ceiling value? If so, what physiological or evolutionary factors impose that ceiling, and is the ceiling value independent of the type of energy stress? We determined food intake and daily digestible energy intake (DEI) as measures of SusMR, and resting metabolic rate (RMR), in mice that were energy stressed by being maintained at cold ambient temperatures. We compared these values with those from previous studies of mice that were energy stressed by peak lactation. We also measured intestinal brush-border nutrient uptakes, body lean and fat masses, and masses of the small intestine, heart, kidneys, and liver. Even with ad lib. quantities of a high-fat diet available, mice could not survive at temperatures below -15° C. Body mass declined at low temperatures because of depletion of body fat reserves. Food intake increased 2.5-fold, RMR 1.5-fold, and masses of the small intestine, heart, and kidneys by 30%-70% with a decrease in temperature from 23° C to -15° C. Intestinal hypertrophy served to restore the reserve capacity of intestinal nutrient transporters that would otherwise have been swamped by the increased food intake. The values reached by sustained metabolic scope (SusMR/RMR), food intake, and intestinal mass were still considerably below those of lactating mice, even though mice at temperatures below -15° C died in the presence of excess food. Thus, intestinal capacity was not the ultimate reason for an inability to survive at lower temperatures. Analysis of individual variation showed that those mice with unusually high food intake, DEI, or RMR tended to have unusually large hearts, kidneys, and intestines. Those organs are essentialfor high energy budgets (reflected in high DEIs), but they also incur large maintenance costs themselves (reflected in high RMRs).