Birds of a feather clock together – sometimes: social synchronization of circadian rhythms

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Abstract

Biological systems use internal circadian clocks to efficiently organize physiological and behavioral activity within the 24-hour time domain. In the absence of time cues, circadian periods vary slightly from 24 hours, but in nature, ambient light serves as the most salient synchronizer for these rhythms, fine-tuning them to exactly 24 hours each day. For some species, social cues can serve to synchronize circadian rhythms in the absence of other time cues or to amplify ambiguous light cues. This has been demonstrated to various degrees in fruit flies, degus, birds, fish, bats, beavers and humans; however, studies in rats and hamsters have shown that social cues are less salient time cues for these species. Social influences on circadian timing might function to tightly organize the social group, thereby decreasing the chances of predation and increasing the likelihood of mating.

Introduction

Circadian rhythms are endogenously generated oscillations in biological function that occur over an approximately 24-hour period and persist when normal daily time cues are absent. One of the most commonly employed circadian indicators, locomotor activity, remains rhythmic in rodents (and other animals) when they are housed in complete darkness for extended periods (even years!). This phenomenon is called a ‘free-running rhythm’ and is typified by a period that is close to, but not exactly, 24 hours in length, causing the behavior to drift out of phase with the real world. In nature, the ambient light cycle acts as a primary zeitgeber (literally time-giver, Ger.) for most organisms. The daily light signal resets circadian rhythms at each cycle, correcting the discrepancy between the free-running period and 24 hours, so that individuals can synchronize (entrain) to the external world. With this synchronicity, the internal clock can assist animals to predict and prepare for changes in the environment.

Although the light cycle is the primary zeitgeber, it is not the only environmental synchronizing influence. Temperature cycles have significant effects in several organisms 1., 2., 3., 4., cyclic food availability resets some rhythms 5., 6., and social cues, including both auditory and olfactory stimuli, contribute to circadian entrainment in some organisms. Levine et al. (2002) [7••] reported recently that fruit flies (Drosophila melanogaster) adjust their circadian rhythms of locomotor activity in response to signals from conspecifics. The flies had a more coherent group rhythm in constant darkness (DD) when housed together than when housed separately. Their individual locomotor activity peaks were more highly correlated after being group-housed in DD for five days in comparison with flies that had been individually housed for the same time period, suggesting that group housing kept them together. Introduction of a small group of arrhythmic flies (or flies with a different initial phase of locomotor activity) into the group housing situation disrupted the group synchrony to a significant degree.

This example underlines the possibility that, under some circumstances, social signals might act to strengthen or supplement light cycle information in synchronizing members of the social group. Such synchronization could facilitate reproduction, protection of individuals from predation, and effective hunting and foraging [8].

In this review, we explore the data in support of, and against, a strong role for social signals in the phase and amplitude control of circadian rhythmicity in a wide variety of animals and also in humans. Clearly, some species are more sensitive to these cues than are others.

Section snippets

Animals

Birds are highly social creatures that rely heavily on vocal communication; therefore, it may not surprising that auditory cues are salient zeitgebers for some birds. Menaker and Eskin [9] showed that behavioral rhythmicity in house sparrows (Passer domesticus) can be entrained by the recorded playback of sparrow song for four hours per day. Three out of ten birds (male and female) clearly entrained to the stimulus and nine out of ten showed some degree of period modulation. A second study by

Humans

Several experiments indicate that human subjects can maintain entrainment to periodic socially related cues in otherwise constant conditions; however, the evidence also suggests that such cues act as relatively weak zeitgebers.

When subjects were housed in light cycles (LD) for four days, then in DD for four days, with the sleep–wake times scheduled by the experimenters, all subjects’ behavioral and physiological rhythms remained entrained as if the former light schedule were still present [37].

Conclusions

It is clear from the existing data that species vary widely in their sensitivity to entrainment by social cues. This is only logical, as social organization among species is as variable as their appearance and lifestyles; some animals are highly dependent on social interactions, whereas, others are fiercely independent. However, in nature, there is an important zeitgeber almost always available — the high amplitude light–dark cycle — and it therefore seems unlikely that social cues play much of

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • of special interest

  • ••

    of outstanding interest

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