Resting and daily energy expenditures of free-living field voles are positively correlated but reflect extrinsic rather than intrinsic effects

Abstract

Resting metabolic rates at thermoneutral (RMRts) are unexpectedly variable. One explanation is that high RMRts intrinsically potentiate a greater total daily energy expenditure (DEE), but recent work has suggested that DEE is extrinsically defined by the environment, which independently affects RMRt. This extrinsic effect could occur because expenditure is forced upwards in poor habitats or enabled to rise in good habitats. We provide here an intraspecific test for an association between RMRt and DEE that separates intrinsic from extrinsic effects and forcing from enabling effects. We measured the DEE and RMRt of 75 free-living shorttailed field voles at two time points in late winter. Across all sites, there was a positive link between individual variation in RMRt and DEE. This correlation, however, emerged only because of an effect across sites, rather than because of an intrinsic association within sites. We defined site quality from the survivorship of voles at the sites and the time at which they commenced breeding in spring. The associations between DEE͞RMRt and site quality suggested that in February voles in poorer sites had higher energy demands, indicating that DEE was forced upwards, but in March the opposite was true, with higher demands in good sites, indicating that high expenditure was enabled. These data show that daily energy demands are extrinsically defined, with a link to RMRt that is secondary or independent. Both forcing and enabling effects of the environment may pertain at different times of year.T he basal metabolic rate (BMR) is defined as the metabolic rate of a quiescent animal, in the thermoneutral zone, that is neither digesting food nor engaged in reproduction or growth (1). A slightly less rigorously defined measurement, resting metabolic rate at thermoneutral (RMRt), incorporates all of these requirements except that the animal need not be postabsorptive (2). BMR and RMRt are highly variable. This variability is most manifest at the interspecific level, where species that have the same body mass may differ in their RMRts by almost an order of magnitude (3-5). However, intraspecific variation in these traits is also substantial, particularly in small mammals, where individuals of the same body mass may differ by 100% in their BMR or RMRt (6-10).Understanding the nature of these differences is important because RMRt (and BMR) are major components of total energy budgets. Typically in free-living animals, RMRt accounts for Ϸ30-40% of total daily energy demands (11)(12)(13)(14). Because animals must spend time feeding to sustain their daily energy demands, including the component comprising their RMRts, there is presumably selection on animals to minimize this component of their daily energy budgets [to reduce foraging times and exposure to predation or adverse environmental conditions (15) or to allocate the saved energy to the processes of growth and reproduction (16)]. Attempts at understanding why some individual animals have much greater RMRts than others have therefore focused ...

Great ranging associated with greater reproductive investment in mammals

“…A positive interspecific relationship between ranging, food availability, and daily energy budget would also be consistent with the longstanding (26,35), but contentious (36), hypothesis that RMR is positively correlated with food availability, since RMR is both a large component and strong correlate of field metabolic rate (24,26; but see ref. 25). Again, while these examples suggest increased ranging is favored in habitats with increased food availability, our model suggests an increase in ranging and net energy intake can also occur with a decrease in the ratio of B:C (Fig.…”

“…1), which is relatively inflexible for an individual but may be labile over evolutionary time. This hypothesis could be tested with data on daily energy budgets for wild populations (24,25,33) or laboratory comparisons of maximum daily metabolic rate (12,23).…”

“…Laboratory and field studies have provided critical insight into foraging energetics and ecology within various species. Comparative efforts, using doubly labeled water (24,25,33) or similar techniques to measure foraging costs and benefits in a common currency of metabolic energy are necessary to understand how these speciesspecific strategies evolve.…”

“…23). Since normal daily energy expenditure approaches this limit in wild populations, with field metabolic rates of 2-4ϫ resting metabolism (24)(25)(26), a zero-sum system apparently prevails, in which increasing the energy spent on travel decreases the energy available for maintenance and reproduction (2) (Fig. 1A).…”

Long-term effects of manipulated natal brood size on metabolic rate in zebra finches

“…We measured SMR in resting post-absorptive birds at night, but at a temperature below the lower critical temperature. SMR constitutes a large part of total energy consumption, and is highly variable within populations (Speakman et al 2003). What causes this variation is poorly understood, but SMR is a repeatable trait (e.g.…”