Animal activity around the clock with no overt circadian rhythms: patterns, mechanisms and adaptive value

Abstract

Circadian rhythms are ubiquitous in many organisms. Animals that are forced to be active around the clock typically show reduced performance, health and survival. Nevertheless, we review evidence of animals showing prolonged intervals of activity with attenuated or nil overt circadian rhythms and no apparent ill effects. We show that around-the-clock and ultradian activity patterns are more common than is generally appreciated, particularly in herbivores, in animals inhabiting polar regions and habitats with constant physical environments, in animals during specific life-history stages (such as migration or reproduction), and in highly social animals. The underlying mechanisms are diverse, but studies suggest that some circadian pacemakers continue to measure time in animals active around the clock. The prevalence of around-the-clock activity in diverse animals and habitats, and an apparent diversity of underlying mechanisms, are consistent with convergent evolution. We suggest that the basic organizational principles of the circadian system and its complexity encompass the potential for chronobiological plasticity. There may be trade-offs between benefits of persistent daily rhythms versus plasticity, which for reasons still poorly understood make overt daily arrhythmicity functionally adaptive only in selected habitats and for selected lifestyles.

Keywords: arrhythmic; circadian; evolution; plasticity; sleep; ultradian rhythms.

Figure 1.

Body temperature of a representative free-living male arctic ground squirrel in northern Alaska, USA over one year (upper panel). Sections of body temperature patterns (lower panels) shown in actogram form (double-plotted positive deviations from 24 h mean, time of day on x-axis, sequential days on y-axis, marked as a and b on upper panel). (a) A 10-day section from March, when the animal remains at high body temperatures within the continuously dark burrow for 2–3 weeks while showing no circadian rhythms. (b) A 10-day section from April, after the animal begins above-ground activity and displays robust, diurnal rhythms in body temperature. Details on methodology are provided in [20]. (Online version in colour.)

Figure 2.

Plasticity in circadian rhythms in locomotor activity in bumble-bee (Bombus terrestris) mother queens. (a) A foundress queen that did not lay eggs after her first batch of brood was removed at day 0 developed statistically significant circadian rhythms on day 3 after egg cell removal. (b) A foundress queen that did lay again after her first batch of eggs was removed. This queen showed weak but statistically significant circadian rhythms in the first 4 days but not in the following days. On day 6 (red ring), the queen's cage was inspected and there were no eggs cells. A new egg cup was detected only at a following inspection on day 10 (blue cross). Thus, this queen switched to activity with no circadian rhythms several days before laying again. Shown are double-plotted actograms (see figure 1). Locomotor activity was monitored with a video-based data acquisition system. Adapted from Eban-Rothschild et al. [53].

Figure 3.

Development of spring migratory restlessness in a songbird, the Siberian stonechat (Saxicola torquata Maura). The figure shows a double plot actogram (see figure 1). Although otherwise strictly diurnal, the bird was almost continuously active from late March until mid-May, when the species migrates under natural conditions. For background information see [55].

Figure 4.

Putative mechanisms underlying around-the-clock activity with no circadian rhythms in animals. (a) The pacemakers controlling circadian cycles such as locomotor activity generate normal rhythms but are uncoupled from motor centres (labelled ‘M’) controlling output (top arrow). The internal rhythms may also be masked by potent external or internal factors (including ultradian rhythms generating pacemakers) that influence circadian output (lower arrow). (b) Some or all pacemaker cells are in an arrested state (marked by a horizontal line). (c) Some or all pacemaker cells have dampened amplitude that is below the threshold needed to drive an overt rhythm. (d) Oscillations persist in individual pacemaker cells, but the phases of these cells are desynchronized (depicted by sine waves with different colours), so that the overall signal is dampened. Alternatively, distinct multicellular pacemakers could interact in ways that promote activity around the clock, for example, if they drive activity at different times of day when they are in anti-phase (depicted by the dashed and solid lines).

Figure 5.

The influence of SCN removal on the locomotor activity in common voles (Microtus arvalis). Single plot actograms showing 10-day records of locomotor activity measured by passive infrared detectors. (a) An intact animal. (b) An SCN-lesioned animal. Adapted from Gerkema & Daan [72].