Diurnality as an energy-saving strategy: energetic consequences of temporal niche switching in small mammals

Abstract

Endogenous daily (circadian) rhythms allow organisms to anticipate daily changes in the environment. Most mammals are specialized to be active during the night (nocturnal) or day (diurnal). However, typically nocturnal mammals become diurnal when energetically challenged by cold or hunger. The circadian thermo-energetics (CTE) hypothesis predicts that diurnal activity patterns reduce daily energy expenditure (DEE) compared with nocturnal activity patterns. Here, we tested the CTE hypothesis by quantifying the energetic consequences of relevant environmental factors in mice. Under natural conditions, diurnality reduces DEE by 6-10% in energetically challenged mice. Combined with night-time torpor, as observed in mice under prolonged food scarcity, DEE can be reduced by ∼20%. The dominant factor determining the energetic benefit of diurnality is thermal buffering provided by a sheltered resting location. Compared with nocturnal animals, diurnal animals encounter higher ambient temperatures during both day and night, leading to reduced thermogenesis costs in temperate climates. Analysis of weather station data shows that diurnality is energetically beneficial on almost all days of the year in a temperate climate region. Furthermore, diurnality provides energetic benefits at all investigated geographical locations on European longitudinal and latitudinal transects. The reduction of DEE by diurnality provides an ultimate explanation for temporal niche switching observed in typically nocturnal small mammals under energetically challenging conditions. Diurnality allows mammals to compensate for reductions in food availability and temperature as it reduces energetic needs. The optimal circadian organization of an animal ultimately depends on the balance between energetic consequences and other fitness consequences of the selected temporal niche.

Influence of temperature on daily locomotor activity in the crab Uca pugilator

“…Our results obtained under constant temperatures during the cold season are in line with the recently proposed circadian thermoenergetics hypothesis, which postulates that colder ambient temperatures, a decrease in food resources, or other stimuli that lead to an unfavorable energy balance shift activity to the warmer phase of the day [13, 15, 23–24]. This shift in ‘temporal niche’, the 24h temporal distribution of physiological and behavioral processes in a species [23, 25], results in a more favorable energy balance as it leads to rest during the colder part of the day when it is metabolically expensive to sustain high levels of activity.…”

Clocks and meals keep mice from being cool

“…Under these conditions, endogenous circadian rhythms and the timing of food intake are typically synchronized, which would result in daily torpor bouts occurring during the late night and early morning while being inhibited in the early night. This daily rhythm in torpor maximizes the energetic benefit of daily torpor by synchronizing its occurrence with low night-time ambient temperatures (van der Vinne et al, 2015). When food is presented shortly before torpor is expected to occur, torpor is prevented, consistent with a requirement for energetic challenge for daily torpor to occur.…”

The flexible clock: predictive and reactive homeostasis, energy balance and the circadian regulation of sleep–wake timing

“…Because thermal insulation reduces a fraction of the energetic costs required to maintain T b , it will return higher energy savings in absolute terms at low T ambient . Aligning the rest phase with the night and actively foraging during the day is therefore more energy efficient under most natural conditions (van der Vinne et al, 2015a). Nocturnality is therefore energetically costly, as discussed below.…”