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.

Two sides of a coin: ecological and chronobiological perspectives of timing in the wild

“…These studies underlined both considerable evolutionary lability of chronobiological traits [76] but also rigid cycles where benefits of rhythmicity are not evident. For example, on the one hand, nearly continuous or ultradian activity has been shown in increasing numbers of species [72]. On the other hand, an increasing number of species is reported to maintain rhythms in seemingly largely arrhythmic environments, for example, caves [77], the deep sea [78] or continuous polar light or darkness [75,79,80].…”

“…For some species, such apparent contradictions arise from individual plasticity (see §4). For example, honeybees are known for their highly precise clocks during the forager stage, but at other stages they may show prolonged intervals of activity with no circadian rhythms [72]. In the absence of circadian behaviour, some pacemakers nevertheless continue to tick in the brains of the bees, even under the tightly regulated physical environment of the hive.…”

“…The proportion of nocturnal species is highest in arid regions and lowest at extremely high latitudes, while crepuscularity (activity during dawn and dusk) is correlated with longer twilight durations. Cathemerality (activity that is spread across day and night) is also more common in cold habitats and under long hours of daylight and twilight in the northern Holarctic region [68,72]. Cathemeral activity, organized in ultradian rhythmicity, is widespread in herbivore mammals, from small voles to horses [71,73].…”

Adaptations to polar life in mammals and birds

“…These unusual aspects of the photoperiod are probably the only unique features of the polar regions, and the adaptations to them are the only ones that make polar biology truly special. It is the photoperiod that gives the polar animals both their clock and their calendar, and a number of reviews have recently outlined our current understanding of how this is achieved (Bloch et al, 2013;Hut et al, 2013;Gwinner and Brandstätter, 2001;Hazlerigg and Simonneaux, 2015;Steiger et al, 2013;Williams et al, 2015). Briefly, information on lighting conditions is received through the eyes and transmitted to the pineal gland, which, in the absence of light, will produce the hormone melatonin.…”

Animal clocks: when science meets nature

“…Bloch et al [20] suggest that activity around the clock with no overt circadian rhythmicity is more common than is currently accepted and may be functionally adaptive for animals living in constant environments or with specific life-history traits such as long migrations or advanced sociality. They further review studies on the possible underlying mechanisms and hypothesize that the complexity of the circadian system enables activity around the clock, while simultaneously keeping vital processes under appropriate circadian regulation.…”