Sleeping on the wing

Abstract

Wakefulness enables animals to interface adaptively with the environment. Paradoxically, in insects to humans, the efficacy of wakefulness depends on daily sleep, a mysterious, usually quiescent state of reduced environmental awareness. However, several birds fly non-stop for days, weeks or months without landing, questioning whether and how they sleep. It is commonly assumed that such birds sleep with one cerebral hemisphere at a time (i.e. unihemispherically) and with only the corresponding eye closed, as observed in swimming dolphins. However, the discovery that birds on land can perform adaptively despite sleeping very little raised the possibility that birds forgo sleep during long flights. In the first study to measure the brain state of birds during long flights, great frigatebirds ( Fregata minor ) slept, but only during soaring and gliding flight. Although sleep was more unihemispheric in flight than on land, sleep also occurred with both brain hemispheres, indicating that having at least one hemisphere awake is not required to maintain the aerodynamic control of flight. Nonetheless, soaring frigatebirds appeared to use unihemispheric sleep to watch where they were going while circling in rising air currents. Despite being able to engage in all types of sleep in flight, the birds only slept for 0.7 h d −1 during flights lasting up to 10 days. By contrast, once back on land they slept 12.8 h d −1 . This suggests that the ecological demands for attention usually exceeded that afforded by sleeping unihemispherically. The ability to interface adaptively with the environment despite sleeping very little challenges commonly held views regarding sleep, and therefore serves as a powerful system for examining the functions of sleep and the consequences of its loss.

Local Aspects of Avian Non-REM and REM Sleep

“…Several avian species engage in long, non-stop flights: bar-tailed godwits ( Limosa lapponica baueri ) fly from Alaska to New Zealand in 8.1 days spanning 11,690 km of sustained flight (Gill et al, 2009); great frigatebirds fly around the Indian Ocean for up to 2 months without landing on the water (Weimerskirch et al, 2016); and Alpine swifts ( Tachymarptis melba ) and Common swifts ( Apus apus ) can fly for 200 and 300 days, respectively (Liechti et al, 2013; Hedenström et al, 2016). Many other birds also make multiday, non-stop flights (reviewed in Rattenborg, 2017). The discovery that dolphins can swim in a coordinated manner during unihemispheric sleep and ducks can switch to asymmetric sleep when needed on the ground, led to the assumption that flying birds maintain aerodynamic control and navigation by sleeping with one eye open (Rattenborg, 2017).…”

“…Many other birds also make multiday, non-stop flights (reviewed in Rattenborg, 2017). The discovery that dolphins can swim in a coordinated manner during unihemispheric sleep and ducks can switch to asymmetric sleep when needed on the ground, led to the assumption that flying birds maintain aerodynamic control and navigation by sleeping with one eye open (Rattenborg, 2017).…”

To sleep or not to sleep: neuronal and ecological insights

“…Unihemispheric sleep enables the individual to simultaneously engage in two otherwise mutually exclusive tasks; sleep and attention [51]. Mallard ducks ( Anas platyrhynchos ) undergo unihemispheric sleep while under the risk of predation [52,53], and other birds during long flights [54 • ]. Marine mammals show unihemispheric sleep [55] allowing them to keep swimming and breathing, and taking continuous care of young.…”

“…For example, whether individuals with a higher capacity to stay awake and suppress their sleep to favor motivational processes (such as mate seeking) will show disadvantages in other aspects (such as attentional processes). In addition, it would be of interest to examine whether reward-related ecologically-relevant demands (such as mate seeking), that reduce or fragment sleep, result in minor negative consequences on animal physiology as compared to stressful or lab-induced sleep disturbances [54 • ]. Future studies comparing the consequences of sleep/wake disturbances under different naturalistic environments should increase our understanding of the evolution of sleep/wake cycles.…”

Coevolving advances in animal flight and aerial robotics

“…Finally, a mostly overlooked specialization in animal flight is that birds can sleep on the wing. Rattenborg [5] offers a critical introduction in this poorly understood aerial behaviour and shows how great frigatebirds sleep in unexpected ways and for remarkably small amounts of time. This ability offers new inspiration for managing situational awareness and information processing in flying robots.…”