The myth of the metabolic baseline: how sleep-wake cycles undermine a foundational assumption in organismal biology

Helena Norman, Daphne Cortese, Amelia Munson, Jan Lindstrom, Shaun S Killen

Basal and standard metabolic rates (BMR and SMR) are cornerstones of physiological ecology and are assumed to be relatively fixed intrinsic properties of organisms that represent the minimum energy required to sustain life. However, this assumption is conceptually flawed. Many core maintenance processes underlying SMR are temporally partitioned across sleep and wakefulness and are not continuously active. We argue that instead of representing a singular metabolic state, SMR is better defined as a shifting metabolic mosaic where maintenance functions are distributed unevenly across sleep-wake states. SMR measured during wakefulness will mainly represent ion regulation, thermoregulation, sensory processing, and substrate cycling. In contrast, sleep-measured SMR primarily includes processes upregulated during sleep, including protein synthesis, cellular repair, immune activation, and synaptic plasticity. Our models demonstrate that SMR values measured exclusively during wake or sleep consistently over- or underestimate daily maintenance costs depending on the time spent in specific sleep states and when SMR was measured. In addition, treatment or environmental effects on the costs of specific processes may be entirely missed if metabolic measures occur during the wrong sleep-wake state. The temporal partitioning of maintenance processes suggests that, to date, SMR measurements may have confounded true metabolic variation with individual and species-specific differences in sleep architecture, with implications for the estimation of energy budgets, trait heritability, environmental effects on metabolic rate, and metabolic scaling relationships. We propose redefining organismal maintenance costs as a time-integrated profile of metabolic demands, but also suggest that state-specific SMR measurements are appropriate if the sleep-wake measurement period aligns with that of the behavioural, physiological, or ecological context of interest. Moving beyond the fiction of a constant maintenance baseline would provide more refined insights into the bioenergetic foundations of ecological performance and evolutionary constraints.