Ecological and social pressures interfere with homeostatic sleep regulation in the wild
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Evaluation Summary:
This article will be of interest to behavioral ecologists studying activity patterns in wild animals. Using accelerometry, rather than polysomnography, opens up exciting opportunities for studying animal sleep under natural conditions for relatively long periods.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Abstract
Sleep is fundamental to the health and fitness of all animals. The physiological importance of sleep is underscored by the central role of homeostasis in determining sleep investment – following periods of sleep deprivation, individuals experience longer and more intense sleep bouts. Yet, most sleep research has been conducted in highly controlled settings, removed from evolutionarily relevant contexts that may hinder the maintenance of sleep homeostasis. Using triaxial accelerometry and GPS to track the sleep patterns of a group of wild baboons ( Papio anubis ), we found that ecological and social pressures indeed interfere with homeostatic sleep regulation. Baboons sacrificed time spent sleeping when in less familiar locations and when sleeping in proximity to more group-mates, regardless of how long they had slept the prior night or how much they had physically exerted themselves the preceding day. Further, they did not appear to compensate for lost sleep via more intense sleep bouts. We found that the collective dynamics characteristic of social animal groups persist into the sleep period, as baboons exhibited synchronized patterns of waking throughout the night, particularly with nearby group-mates. Thus, for animals whose fitness depends critically on avoiding predation and developing social relationships, maintaining sleep homeostasis may be only secondary to remaining vigilant when sleeping in risky habitats and interacting with group-mates during the night. Our results highlight the importance of studying sleep in ecologically relevant contexts, where the adaptive function of sleep patterns directly reflects the complex trade-offs that have guided its evolution.
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Evaluation Summary:
This article will be of interest to behavioral ecologists studying activity patterns in wild animals. Using accelerometry, rather than polysomnography, opens up exciting opportunities for studying animal sleep under natural conditions for relatively long periods.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
By recording the sleep and movement patterns of a group of baboons (a highly social animal), this study showed that ecological and social pressures affect individuals' sleep patterns. Results highlight the importance of studying animal sleep under natural conditions by using sophisticated electronic tags. The main strength of this paper is that the authors took a novel approach for recording GPS positions and sleep patterns (based on body acceleration) of a group-living species for relatively long periods. The datasets allowed them to examine several important aspects of animal sleep (e.g., the effect of changing sleeping sites and the presence of other group members, testing the sentinel hypothesis). A weakness is that they did not measure sleep directly; however, they are aware of this weakness and …
Reviewer #1 (Public Review):
By recording the sleep and movement patterns of a group of baboons (a highly social animal), this study showed that ecological and social pressures affect individuals' sleep patterns. Results highlight the importance of studying animal sleep under natural conditions by using sophisticated electronic tags. The main strength of this paper is that the authors took a novel approach for recording GPS positions and sleep patterns (based on body acceleration) of a group-living species for relatively long periods. The datasets allowed them to examine several important aspects of animal sleep (e.g., the effect of changing sleeping sites and the presence of other group members, testing the sentinel hypothesis). A weakness is that they did not measure sleep directly; however, they are aware of this weakness and carefully discussed it. I had already provided several comments at pre-submission stage, and the authors revised the manuscript accordingly. Therefore, I only have relatively minor, specific comments.
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Reviewer #2 (Public Review):
A fundamental aspect of sleep is that it is homeostatically regulated. Sleep homeostasis manifests along two dimensions, sleep duration and sleep intensity. Following sleep loss, animals can recover lost sleep by sleeping longer, sleeping deeper, or doing both. In many species, sleep duration can be measured behaviorally (e.g., the animal is immobile in a sleep posture with closed eyes) or electrophysiologically, via measuring brain activity (electroencephalogram, EEG) along with other physiological parameters that change between wakefulness and sleep. Sleep intensity is measured by determining the amount of stimulation needed to awaken an animal. As this method is disruptive to sleep, the quantity (spectral power) of slow waves in the EEG, which correlates with sleep intensity in mammals, is often used to …
Reviewer #2 (Public Review):
A fundamental aspect of sleep is that it is homeostatically regulated. Sleep homeostasis manifests along two dimensions, sleep duration and sleep intensity. Following sleep loss, animals can recover lost sleep by sleeping longer, sleeping deeper, or doing both. In many species, sleep duration can be measured behaviorally (e.g., the animal is immobile in a sleep posture with closed eyes) or electrophysiologically, via measuring brain activity (electroencephalogram, EEG) along with other physiological parameters that change between wakefulness and sleep. Sleep intensity is measured by determining the amount of stimulation needed to awaken an animal. As this method is disruptive to sleep, the quantity (spectral power) of slow waves in the EEG, which correlates with sleep intensity in mammals, is often used to measure sleep intensity.
Most of our understanding about sleep homeostasis is derived from controlled laboratory experiments where ecological pressures are minimized. However, little is known about how animals reconcile ecological pressures for wakefulness with the homeostatic need for sleep. In this paper, the authors used a neck mounted accelerometer and GPS device to characterize the sleep behavior of a troop of baboons living in the wild. Although EEG devices are now being used to record sleep in a variety of animals in the wild (i.e., sloths, sandpipers, owls, and frigatebirds), this method is not suitable for wild baboons, as they would likely attempt to remove the equipment. However, accelerometry can be used to estimate the time spent sleeping in the wild, once validated against either direct measures of sleep behavior (posture, eye state, immobility) or EEG measures of sleep. In the current paper, accelerometry was validated against behavioral measures of sleep obtained with thermal cameras; immobile baboons sitting with the head hung were considered to be asleep.
Using accelerometry, the authors investigated the impact that various ecological factors had on the time spent sleeping. Baboons slept more when spending the night in their preferred trees. They slept less when sleeping in larger groups, apparently due to awakenings of individuals disrupting the sleep of other group members. Indeed, the timing of bouts of sleep and wakefulness were more synchronous within groups sharing the same tree. The time spent sleeping on a given night was not influenced by how much time the baboons spent sleeping the previous night or how much time they were active during the day. As one might expect the baboons to recover lost sleep following a night with less sleep by sleeping longer, the authors suggest that ecological factors interfere with the homeostatic regulation of sleep. The lack of a relationship between the time spent traveling and sleep duration on the following night was also interpreted as evidence for ecological factors interfering with the homeostatic regulation of sleep.
The results support the authors' interpretation if one only considers sleep duration as a means for recovering lost sleep. However, effective sleep homeostasis could have been mediated by modulating sleep intensity. Baboons that lost some sleep on one night might recover this sleep by sleeping deeper, but not longer, on the subsequent night. Without measuring sleep intensity, it is not possible to have a full accounting of the amount of sleep obtained under the various ecological conditions.
Despite this limitation, the authors present a large and unique dataset on the ecology of sleep in highly social animals living in the wild. The finding that baboons sleep less when sleeping in trees with which they are less familiar, illustrates that safe sleep sites are an important resource for animals. The synchrony between bouts of wakefulness and sleep among group members is also interesting, as it suggests that the group does not maximize vigilance by sleeping and waking asynchronously, as some researchers had proposed. In addition, it suggests that a potential cost of sleeping in groups is disrupted sleep. As such, this study adds to our understanding of the ecology of sleep in socially sleeping animals.
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