Limits to Sustainable Metabolic Rate during Transient Exposure to Low Temperatures in Short-Tailed Field Voles (Microtus agrestis)

Abstract

We exposed short-tailed field voles, Microtus agrestis, to transient decreases in ambient temperature to evaluate the limits of their sustainable metabolic rates. We predicted that voles exposed to transient low temperatures would elevate their food intake until they reached some alimentary limit and thereafter they would withdraw reserves. During short-term (24-h) exposure to temperatures below the lower critical temperature (25° C) daily food intake actually decreased significantly to a minimum of 1.51 ± 0.41 g at 10° C but was greater at 5° and -5° C. Weight loss (g) increased significantly with decreasing temperature; however, at 5° C vole mass increased. During more prolonged exposure for 4 d, food intake increased significantly with the duration of cold exposure (5° and 15° C) to a maximum on days 3 and 4. In a separate experiment voles were randomly exposed for 3-d intervals to a range of temperatures from 20° to 5° C and were returned to 25° C for 3 d between exposures. Both food intake and weight loss increased significantly with decreasing temperature; voles gained mass at 20° and 25° C. There was 40% mortality in voles exposed to -5° C for 24 h (n = 10). When voles were exposed to 5° C for 6 d before they were exposed to -5° C, there was zero mortality at -5° C for 12 d (n = 6). The basal metabolism (BMR) of voles before transient cold exposure, 1.71 ± 0.41 mL · min⁻¹, was not significantly different from that of the same voles after transient cold exposure (2.17 ± 0.71 mL min⁻¹). Maximum food intake at 5°C (5.67 ± 1.45 g · d⁻¹) represented 1.7 times BMR, which is considerably lower than the limit on alimentary uptake of seven times BMR previously suggested. Our results suggest that the voles were using a strategy of energy minimization during transient cold exposure that combined increased energy intake with body reserve utilization. However, the duration of cold exposure had a profound effect on this strategy. The mortality data in this species at low temperatures combined with levels of food intake relative to BMR suggest that sustainable metabolic rate is not limited by constraints imposed centrally by the alimentary system but rather by constraints at the sites of energy utilization.