Sleep deprivation impairs precision of waggle dance signaling in honey bees

Abstract

Sleep is essential for basic survival, and insufficient sleep leads to a variety of dysfunctions. In humans, one of the most profound consequences of sleep deprivation is imprecise or irrational communication, demonstrated by degradation in signaling as well as in receiving information. Communication in nonhuman animals may suffer analogous degradation of precision, perhaps with especially damaging consequences for social animals. However, society-specific consequences of sleep loss have rarely been explored, and no function of sleep has been ascribed to a truly social (eusocial) organism in the context of its society. Here we show that sleep-deprived honey bees (Apis mellifera) exhibit reduced precision when signaling direction information to food sources in their waggle dances. The deterioration of the honey bee's ability to communicate is expected to reduce the foraging efficiency of nestmates. This study demonstrates the impact of sleep deprivation on signaling in a eusocial animal. If the deterioration of signals made by sleep-deprived honey bees and humans is generalizable, then imprecise communication may be one detrimental effect of sleep loss shared by social organisms.dance language | signal precision | recovery sleep | sleep rebound D eprivation of sleep can result in dire consequences to health and to cognitive performance (1-3). When deprived of sleep, humans are susceptible to communication lapses, both when signaling (4, 5) and when receiving (6) information. Human speech performance, such as word fluency and intonation, declines (7). A speaker's voice is sensitive to fatigue (8), with both fundamental frequency and word duration differing in sleep-deprived subjects (9). Speech deterioration is so obvious after sleep deprivation that "rambling, incoherent speech for brief periods" features in a cognitive disorganization scale (10). Although the potential exists for sleep to impact communication in nonhuman animals, we are aware only of studies addressing the role of sleep in song learning in zebra finches (11,12).In the present study, we investigated a possible degradation of social function by testing the effect of sleep deprivation on the precision of signaling in European honey bees (Apis mellifera Linnaeus, 1758). Honey bees regularly inform nestmate workers about the distance and direction to desirable foraging and nestsite locations by performing waggle dances (Fig. 1A), in which the distance to the advertised destination is indicated by the duration of the waggle phase of the dance, and the destination's direction relative to the sun's azimuth is indicated by the angle of the dance relative to the vertical (i.e., dance angle) (Fig. 1A) (13). Imprecision in a bee's performance of the waggle dance could result in degraded transfer of information and a consequent decline in foraging efficiency for vital resources (14, 15).We hypothesized that depriving honey bees of sleep would decrease the precision of their dance's direction and distance information. For directional precision, we predicted t...

Sleeping on the wing

“…Indeed, even when sleeping in flight, sleep was more fragmented and less deep than sleep on land. In contrast with frigatebirds, in animals ranging from insects [92] to humans [93], far shorter periods of sleep restriction and fragmentation [94] have profound adverse effects on their ability to maintain wakefulness and interact adaptively with the environment. People fall asleep while driving a car after losing just a few hours of sleep, even when aware of the dangers and trying to keep themselves awake.…”

The colony environment modulates sleep in honey bee workers

“…5). However, several studies have suggested that honey bees do not compensate for sleep loss by increasing sleep duration; rather, they suggest that bees recover from sleep deprivation by intensifying their later sleep (Beyaert et al, 2012;Hussaini et al, 2009;Klein et al, 2010;Sauer et al, 2004). Moreover, even if young honey bees were compensating for sleep loss by increasing sleep duration, one would predict that 2 days of sleep deprivation will result in a greater sleep rebound than a single day of sleep deprivation, which is not consistent with our findings that sleep duration was similar for bees experiencing the colony environment for 1 or 2 days (Fig.…”

“…From 3 weeks of adult life, honey bee workers typically forage for pollen and nectar outside the hive (Robinson, 1992;Winston, 1987). The sleep behavior of honey bees has been studied both in the natural context of the colony (Kaiser, 1988;Klein and Seeley, 2011;Klein et al, 2008;Klein et al, 2010) and in detailed laboratory studies (Eban-Rothschild and Bloch, 2008;Kaiser, 1988;Sauer et al, 2003). Honey bees exhibit all three behavioral characteristics of sleep: a period of quiescence (Eban-Rothschild and Bloch, 2008;Kaiser, 1988;Sauer et al, 2003;Sauer et al, 2004), an increased response threshold (Eban-Rothschild and Bloch, 2008; Kaiser, 1988;Kaiser and Steiner-Kaiser, 1983) and a homeostatic regulation mechanism (Klein et al, 2010;Sauer et al, 2004).…”

“…The sleep behavior of honey bees has been studied both in the natural context of the colony (Kaiser, 1988;Klein and Seeley, 2011;Klein et al, 2008;Klein et al, 2010) and in detailed laboratory studies (Eban-Rothschild and Bloch, 2008;Kaiser, 1988;Sauer et al, 2003). Honey bees exhibit all three behavioral characteristics of sleep: a period of quiescence (Eban-Rothschild and Bloch, 2008;Kaiser, 1988;Sauer et al, 2003;Sauer et al, 2004), an increased response threshold (Eban-Rothschild and Bloch, 2008; Kaiser, 1988;Kaiser and Steiner-Kaiser, 1983) and a homeostatic regulation mechanism (Klein et al, 2010;Sauer et al, 2004). In honey bee foragers, as in mammals and flies, sleep deprivation impairs learning and memory processes (Beyaert et al, 2012;Hussaini et al, 2009;Klein et al, 2010), and forager bees induced to learn novel navigational tasks sleep longer than control bees (Beyaert et al, 2012).…”

Honeybee linguistics—a comparative analysis of the waggle dance among species of Apis

“…We only decoded waggle phases (the phase of the dance that contains location information) that occurred during 30-s intervals, with the start time of each interval separated by 5 min (starting from the beginning of our video footage). We determined the angles of the waggle phases with the aid of a MATLAB programme that we developed (inspired by a similar approach by Klein et al, 2010). A transparent MATLAB figure was overlaid on an external video player window (SMPlayer) and video was played back at slow speed (usually 1/4 speed).…”