Voluntary running in deer mice: speed, distance, energy costs and temperature effects

Abstract

Over the past three decades, exercise and environmental physiologists have painstakingly described the energetics of locomotion in a wide range of animals. In quadrupedal mammals running at near-thermoneutral temperatures, the relationship between metabolic rate and running speed is approximately linear over a broad range of speeds for most species (Taylor et al., 1970(Taylor et al., , 1982, with the slope of the regression of metabolism vs speed inversely related to body mass and the intercept (power output at zero speed) elevated above resting metabolism. Considerably less is known about locomotion energetics at low ambient temperatures, where energy costs of exercise may interact with the need for regulatory thermogenesis. In large mammals such as humans (Brooks and Fahey, 1984), and in birds (e.g. Paladino and King, 1984;Webster and Weathers, 1990), heat produced as a byproduct of exercise can substitute for heat that would otherwise need to be produced by shivering or non-shivering thermogenesis to maintain body temperature in cold conditions. A few studies (Wunder, 1970;Hart, 1971) suggest that in small mammals, exercise and thermogenic costs are largely additive -that is, exercise heat cannot be substituted for thermogenesis, possibly because locomotor movements disrupt pelage insulation or affect peripheral circulation. Completely additive thermogenic and exercise costs could result in increasing constraints on the capacity for sustained exercise as temperature drops, unless maximal power output in The energetics of terrestrial locomotion are of considerable interest to ecologists and physiologists, but nearly all of our current knowledge comes from animals undergoing forced exercise. To explore patterns of energy use and behavior during voluntary exercise, we developed methods allowing nearly continuous measurements of metabolic rates in freely behaving small mammals, with high temporal resolution over periods of several days. We used this approach to examine relationships between ambient temperature (T a ), locomotor behavior and energy costs in the deer mouse, a small mammal that routinely encounters a large range of temperatures in its natural habitat. We tested for individual consistency in running behavior and metabolic traits, and determined how locomotor costs vary with speed and T a . Because of the importance of thermoregulatory costs in small mammals, we checked for substitution of exercise heat for thermostatic heat production at T a below the thermal neutral zone and determined the fraction of the daily energy budget comprising exercise costs.Locomotor behavior was highly variable among individuals but had high repeatability, at least over short intervals. We found few temperature-related changes in speed or distance run, but T a strongly affected energy costs. Partial substitution of exercise heat for thermogenic heat occurred at low T a . This reduced energy expenditure during low-temperature running by 23-37%, but running costs comprised a fairly minor fraction of the energy budget, so th...

Wheel-running activity and energy metabolism in relation to ambient temperature in mice selected for high wheel-running activity

“…DEE was also affected by ambient temperature with a 1.4-fold increase from 20 to 10°C and a 1.5-fold increase from 30 to 20°C. These results are similar to values found in a study in deer mice (Chappell et al 2004) housed at 3, 10 and 25°C. Wheelrunning activity (distance run and running time) was positively correlated with the simultaneously measured DEE.…”

“…COT is related to body mass, with higher costs of transport at higher body mass. In our study as well as previous work by Chappell et al (2004) and Rezende et al (2006), body mass was not a statistically significant predictor of COT. The incremental cost of terrestrial locomotion in relation to body mass can be estimated using the allometry given by Taylor et al in 1982: COT (kJ/km) = 10.7 · mass (kg) 0.684 (Taylor et al 1982), and predicts a slope of 0.92 kJ/km for a 27.6 g animal.…”

“…Maximal running speeds, however, did not significantly vary between temperatures in this study. A study in deer mice likewise provided no evidence for effects of temperature on wheel-running activity (Chappell et al 2004).…”

“…Several studies demonstrate substitution [in White crowned sparrows, Zonotrichia leucophrys gambelii (Paladino and King 1984), potoroo, Potorous tridactylus (Baudinette et al 1993) deer mice, Peromyscus maniculatus (Chappell et al 2004), rat, Rattus novegicus (Arnold et al 1986;Makinen et al 1996)], but there are also results consistent with addition [Kowari, Dasyroides byrnei (MacMillen and Dawson 1986), Chipmunk, Eutamias merriami (Wunder 1970) patas monkey, Erythrocebus patas (Mahoney 1980)]. This discrepancy among studies may well be related to different conditions.…”

Variation in Metabolic Rate among Individuals Is Related to Tissue-Specific Differences in Mitochondrial Leak Respiration

“…However, while a positive correlation between minimum and maximum metabolic rates at the intraspecific level has indeed been found in some contexts Biro and Stamps 2010;Careau et al 2014aCareau et al , 2014b, this is not the case in others (Chappell et al 2004(Chappell et al , 2007Gomes et al 2004;Careau et al 2014b). The mechanisms underlying this purported link are also equivocal, with some studies reporting a positive relationship between metabolic rates and underlying traits such as organ size (Konarzewski and Ksiazek 2013) or mitochondrial density (Norin and Malte 2012), whereas others find no relationship (Selman et al 2001;Chappell et al 2007;Larsen et al 2011;Norin and Malte 2012;Boldsen et al 2013).…”