Honey Bees Sleeping
At Night, honey bees pass through a physiological state that is similar to mammalian sleep.
Clarence Collison
“Honey bees are among the first invertebrates for which sleep behavior has been described (Kaiser and Steiner-Kaiser 1983). Honey bee foragers exhibit sleep, both in their natural hive environment, and when isolated individually in the lab. Foragers sleep in a posture characterized by a relaxation of the thorax, head, and antennae. This characteristic posture is associated with a decrease in muscle tonus and body temperature, and an increase in response threshold, measured both neurophysiologically and behaviorally (Kaiser and Steiner-Kaiser 1983; Kaiser 1988). It was further suggested that deep sleep in foragers (determined as periods lacking antennal movements) is correlated with rhythmic electrophysiological activity in the brain, including the mushroom bodies (Schuppe 1995). Foragers deprived of sleep for 12 hours showed a rebound the next day; they increased the duration of antennal immobility, one of the characteristics of sleep in bees (Sauer et al. 2004). This suggests that sleep in foragers is homeostatically regulated. Foragers are relatively old workers, have strong circadian rhythms, and sleep during the night. However, circadian rhythms are not typical to all worker bees; young bees typically perform various in-hive activities around-the-clock, with no circadian rhythms (Crailsheim et al. 1996; Moore et al. 1998). Young bees that are isolated individually, or kept in small groups in constant conditions, have no circadian rhythms in locomotor activity during their first 3-14 days (Moore 2001; Meshi and Bloch 2007). Their around-the-clock pattern of activity raises the question of whether young bees sleep as foragers do. It is possible that young honey bees do not sleep at all, which would make them an exception in the animal kingdom. An alternative hypothesis is that young bees do sleep like foragers, but distribute their sleep throughout the day. A third hypothesis is that young bees sleep, but their sleep is essentially different from that of foragers. In order to distinguish between these hypotheses, Eban-Rothschild and Bloch (2008) characterized the sleep behavior of individually isolated young bees, and compared it to that of sister foragers. Their detailed behavioral observations and analyses of response thresholds lend weight to the third hypothesis. They showed that young honey bees exhibit sleep behavior which is composed of the same stages observed in foragers, but their sleep dynamics differ (Eban-Rothschild and Bloch 2008).”
“At night, honey bees pass through a physiological state that is similar to mammalian sleep. Like sleep in mammals, sleep-like behavior in honey bees is an active process. This is expressed most clearly by spontaneous antennal movements which appear at irregular intervals throughout the night and interrupt episodes of antennal immobility. Sauer et al. 2003 presented a newly developed video technique for the continuous recording of the position and movements of the bee’s antennae. The same technique was used to record head inclination and ventilatory movements. Despite the constancy of the ambient temperature, the magnitudes of antennae-related parameters, as well as head inclination and ventilatory cycle duration, displayed dynamic unimodal time-courses which exhibited a high degree of temporal covariance. The similarity between these time-courses and the nightly time-course of the reaction threshold for a sensory stimulus, investigated previously, indicates that, in honey bees, deepest “sleep” and least ventilatory activity occur at the same time (in the seventh hour of the rest phase) (Sauer et al. 2003).”
“Sleep appears to play an important role in the lives of honey bees, but to understand how and why, it is essential to accurately identify sleep, and to know when and where it occurs. Viewing normally obscured honey bees in their nests would be necessary to calculate the total quantity and quality of sleep and sleep’s relevance to the health and dynamics of a honey bee and its colony. Western honey bees spend much of their time inside cells, and are visible only by the tips of their abdomens when viewed through the walls of an observation hive, or on frames pulled from a typical beehive. Prior studies have suggested that honey bees spend some of their time inside cells resting or sleeping, with ventilatory movements of the abdomen serving as a telltale sign distinguishing sleep from other behaviors. Bouts of abdominal pulses broken by extended pauses (discontinuous ventilation) in an otherwise relatively immobile bee appears to indicate sleep. Can viewing the tips of abdomens consistently and predictably indicate what is happening with the rest of a bee’s body when inserted deep inside a honeycomb cell? To distinguish a sleeping bee from a bee maintaining cells, eating, or heating developing brood, Klein and Busby (2020) used a miniature observation hive with slices of honeycomb turned in cross-section, and filmed the exposed cells with an infrared-sensitive video camera and a thermal camera. Thermal imaging helped us identify heating bees, but simply observing ventilatory movements, as well as larger motions of the posterior tip of a bee’s abdomen was sufficient to non-invasively and predictably distinguish heating and sleeping inside comb cells. Neither behavior is associated with large motions of the abdomen, but heating demands continuous (vs. discontinuous) ventilatory pulsing. Among the four behaviors observed inside cells, sleeping constituted 16.9% of observations. Accuracy of identifying sleep when restricted to viewing only the tip of an abdomen was 86.6%, and heating was 73.0%. Monitoring abdominal movements of honey bees offers anyone with a view of honeycomb the ability to more fully monitor when and where behaviors of interest are exhibited in a bustling nest (Klein and Busby 2020).”
“As worker bees age they change tasks, typically performing a sequence of different task sets (as ‘cell cleaners’, ‘nurse bees’, ‘food storers’ and ‘foragers’). Belonging to different task groups could differentially impact the duration, constitution, and periodicity of a bee’s sleep. Individually marked bees were observed within observation hives to determine task-dependent patterns of sleep behavior. Three studies were conducted to investigate the duration and periodicity of sleep when bees were outside comb cells, as well as duration of potential sleep when bees were immobile inside cells. All four worker task groups that were examined exhibited a sleep state. As bees aged and changed tasks, however, they spent more time and longer uninterrupted periods in a sleep state outside cells but spent less time and shorter uninterrupted periods immobile inside cells. Although cell cleaners and nurse bees exhibited no sleep:wake rhythmicity, food storers and foragers experienced a 24 hour sleep:wake cycle, with more sleep and longer unbroken bouts of sleep during the night than during the day. If immobility within cells is an indicator of sleep, this study reveals that the youngest adult bees sleep the most, with all older task groups sleeping the same amount. This in-cell potential sleep may compensate for what would otherwise indicate an exceptional increase of sleep in an aging animal (Klein et al. 2008).”
“Honey bees face variables such as temperature and position of resources within their colony’s nest that may impact their sleep. Klein et al. (2014) mapped sleep behavior and temperature of worker bees and produced maps of their nest’s comb contents as the colony grew and contents changed. By following marked bees, they discovered that individuals slept in many locations, but bees of different tasks groups slept in different areas of the nest relative to position of the brood and surrounding temperature. Older worker bees generally slept outside cells, closer to the perimeter of the nest, in colder regions, and away from uncapped brood. Younger worker bees generally slept inside cells and closer to the center of the nest and spent more time asleep than awake when surrounded by uncapped brood. The average surface temperature of sleeping foragers was lower than the surface temperature of their surroundings (Klein et al. 2014).”
“Honey bee foragers shift their work schedules, but how flexible they are in the timing of sleep as they shift the timing of work is unknown, despite the importance of colony-level plasticity in the face of a changing environment. Klein and Seeley (2011) hypothesized that sleep schedules of foragers are not fixed and instead vary depending on the time when food is available. They trained bees to visit a food source made available for several hours in the early morning (AM) or several hours in the late afternoon (PM), then monitored their sleep behavior for 24 hours after training, specifically comparing their sleep during the AM and PM periods previously designated as training periods. Following AM training, honey bee foragers slept more during the afternoon than during the morning, but following PM training, the same bees ‘slept in’ the next morning, and so slept more in the morning than in the afternoon. Although foragers did not change the total amount of time devoted to each of their behaviors (including sleep), the timing of their sleep did change. Thus, plasticity in timing of foraging was matched by plasticity in timing of sleep. The apparent correlation between the timing patterns of foraging and sleeping demonstrates temporal plasticity of sleep under ecologically realistic conditions (Klein and Seeley 2011).”
“Rest at night in forager honey bees meets essential criteria of sleep. This study reports the effect of a 12-hour total sleep deprivation (SD) by forced activity on the behavior of these bees. The behavior of sleep-deprived bees was compared with that of control bees under LD [periodic alternation between light (L) and darkness (D)] 12:12 hours. Sleep deprivation for 12 hours during the first D period resulted in a significant difference with respect to the parameter ‘hourly amount of antennal immobility between sleep-deprived and control bees during the remaining L and D periods. This difference did not occur in the L period following the deprivation night, but rather it became obvious at the beginning of the following D period. The increase of the amount of antennal immobility in sleep-deprived bees was accompanied by an increase of the duration of episodes of antennal immobility. Moreover, the latency from lights off to the first episode of antennal immobility lasting 20 seconds or longer (deep sleep latency) tended to be shorter in sleep-deprived than in control bees. Disturbing the bees during the day (L period) did not result in such differences between disturbed and control bees. Highest reaction thresholds in sleeping honey bees occur during long episodes of antennal immobility. Sauer et al. (2004) concluded that honey bees compensate a sleep deficit by intensification (deepening) of the sleep process and thus that sleep in honey bees, like that in other arthropods and mammals, is controlled by regulatory mechanisms.”
“Even though sleep-like behavior has been studied in honey bees, the relationship between sleep and memory formation has not been explored. Hussaini et al. (2009) described a new approach to address the question if sleep in bees, like in other animals, improves memory consolidation. Restrained bees were observed by a web camera, and their antennal activities were used as indicators of sleep. They found that the bees sleep more during the dark phase of the day compared with the light phase. Sleep phases were characterized by two distinct patterns of antennal activities: symmetrical activity, more prominent during the dark phase; and asymmetrical activity, more common during the light phase. Sleep-deprived bees showed rebound the following day, confirming effective deprivation of sleep. After appetitive conditioning of the bees to various olfactory stimuli, they observed their sleep. Bees conditioned to odor with sugar reward showed lesser sleep compared with bees that were exposed to either reward alone or air alone. Next, they asked whether sleep deprivation affects memory consolidation. While sleep deprivation had no effect on retention scores after odor acquisition, retention for extinction learning was significantly reduced, indicating that consolidation of extinction memory but not acquisition memory was affected by sleep deprivation.”
“Honey bees can signal the destination of a food source with a waggle dance, but when sleep-restricted, dancers perform directionally less precise dances (Klein et al. 2010).” “Klein et al. (2018) analysed dance follower behavior with respect to a dance’s directional precision and whether or not the dancer had been sleep-restricted. Followers were more likely to switch dances if following an imprecise dance and more likely to exit the nest if following a precise dance. Followers were also more likely to exit the nest after following a dance composed of more iterations (waggle phases), but only if the dancer was sleep-restricted. Bees appeared to follow fewer waggle phases of a dance that was less precise, but, again, only if the dancer was sleep-restricted. Following fewer waggle phases has been shown to decrease a bee’s flight accuracy, so results suggest that cues associated with sleep loss could affect a follower’s foraging success.”
References
Crailsheim, K., N. Hrassnigg and A. Stabentheiner 1996. Diurnal behavioural differences in forager and nurse honey bees (Apis mellifera carnica Pollm). Apidologie 27: 235-244.
Eban-Rothschild, A.D. and G. Bloch 2008. Differences in the sleep architecture of forager and young honeybees (Apis mellifera). J. Exp. Biol. 211: 2408-2416.
Hussaini, S.A., L. Bogusch, T. Landgraf and R. Menzel 2009. Sleep deprivation affects extinction but not acquisition memory in honeybees. Learn. Mem. 16: 698-705.
Kaiser, W.J. 1988. Busy bees need rest, too. J. Comp. Physiol. A. 163: 565-584.
Kaiser, W.J. and J. Steiner-Kaiser 1983. Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect. Nature 301: 707-709.
Klein, B.A. and M.K. Busby 2020. Slumber in a cell: honeycomb used by honey bees for food, brood, heating…and sleeping. PeerJ 8: e9583 https://doi.org/10.7717/peerj.9583
Klein, B.A. and T.D. Seeley 2011. Work or sleep? Honey bee foragers opportunistically nap during the day when forage is not available. Anim. Behav. 82: 77-83.
Klein, B.A., K.M. Olzsowy, A. Klein, K.M. Saunders and T,D. Seeley 2008. Caste-dependent sleep of worker honey bees. J. Exp. Biol. 211: 3028-3040.
Klein, B.A., A. Klein, M.K. Wray, U.G. Mueller and T.D. Seeley 2010. Sleep deprivation impairs precision of waggle dance signaling in honey bees. Proc. Natl. Acad. Sci. USA 107: 22705-22709.
Klein, B.A., M. Stiegler, A. Klein, and J. Tautz 2014. Mapping sleeping bees within their nest: spatial and temporal analysis of worker honey bee sleep. PLoS ONE 9(7): e102316 https://doi.org/10.1371/journal.pone.0102316
Klein, B.A., M. Vogt, K. Unrein and D.M. Reineke 2018. Followers of honey bee waggle dancers change their behaviour when dancers are sleep-restricted or perform imprecise dances. Anim. Behav. 146: 71-77.
Meshi, A. and G. Bloch 2007. Monitoring circadian rhythms of individual honey bees in a social environment reveals social influences on postembryonic ontogeny of activity rhythms. J. Biol. Rhythms 22: 343-355.
Moore, D. 2001. Honey bee circadian clocks: behavioral control from individual workers to whole-colony rhythms. J. Insect Physiol. 47: 843-857.
Moore, D., J.E. Angel, I.M. Cheeseman, S.E. Fahrbach and G.E. Robinson 1998. Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav. Ecol. Sociobiol. 43: 147-160.
Sauer., S., M. Kinkelin, E. Herrmann and W. Kaiser 2003. The dynamics of sleep-like behavior in honey bees. J. Comp. Physiol. A 189:599-607.
Sauer, S., E. Herrmann and W. Kaiser 2004. Sleep deprivation in honey bees. J. Sleep Res. 13: 145-152.
Schuppe, H. 1995. Rhythmic brain activity in sleeping bees. Wien Med. Wochenschr. 145: 463- 464.
Clarence Collison is an Emeritus Professor of Entomology and Department Head Emeritus of Entomology and Plant Pathology at Mississippi State University, Mississippi State, MS.
