By: Antonia DeGroot & Gard Otis
It may come as a surprise to learn that honey bees sleep, and that sleep is a fundamental part of many different aspects of honey bee health.
It is well known how important sleep is for humans, and how sleep deprivation can negatively impact many aspects of our lives. The negative effects of sleep deprivation are remarkably similar in insects (see review by Helfrich-Förster, 2018). But how does sleep deprivation affect honey bees? In order to answer this question, we will break it down into four aspects: i) an introduction to the mechanisms and consequences behind sleep deprivation; ii) how sleep deprivation affects communication; iii) how sleep deprivation affects memory; and iv) speculations and future research directions.
In 1983 the first paper was published that concluded that insects do, in fact, sleep (Kaiser & Steiner-Kaiser, 1983). The researchers determined that when a honey bee is resting, its behaviour is comparable to that of humans, other mammals and birds when they are sleeping (Kaiser, 1988). These behavioral characteristics include a reduction of muscle tone, lowered body temperature, decreased movement and a reaction threshold higher than normal (meaning that it takes a larger stimulus such as sound, movement, or light, to disturb a sleeping bee than it would if that same bee were awake) (Kaiser, 1988). Kaiser & Steiner-Kaiser also determined that bees prefer dark conditions while sleeping, compared to light conditions. This finding indicates that bee sleep is controlled by an internal circadian rhythm, that is, an approximately 24-hour internal clock as they follow a day/night cycle (Kaiser, 1988).
Sauer et al. (2004) compared the behavior of sleep-deprived bees to bees that had experienced a normal amount of rest. To create conditions of sleep deprivation, they placed bees in a glass cylinder that was attached to a tilting device. The device titled every nine seconds in order to disrupt the bees and force them to stay awake for a period of 12 hours. The two ways they determined if a bee was sleeping were the amount of antennal immobility of the bee and the length of time between periods of antennal immobility. Trials were carried out in both light and dark conditions. Sauer et al. determined that after a bee experiences a night of sleep deprivation, the next night if it is left undisturbed, it will exhibit increased periods of antennal immobility compared to undisturbed bees. They had discovered that sleep deprivation in one night leads to enhanced sleep the following night, as the bee apparently attempts to compensate for its previously sleepless night. This sleep “rebound” is similar to how humans and other animals respond when they experience a deficit in the amount or the quality of sleep (Klein et al., 2010; Helfrich-Förster, 2018). The Sauer et al. paper laid the groundwork in understanding that sleep in bees is not simply for the purpose of conserving energy. If it were, bees would not have to make up for a night’s lost sleep; they could simply eat additional food to acquire more energy. Their results indicate that sleep is regulated by physiological processes within the body that maintain normal body functioning (Sauer et al., 2004). This revelation suggests that sleep must affect other behavioural and physiological processes of bees, a topic we examine below.
“When a bee was deprived of sleep the precision of its waggle dances decreased. Specifically it negatively affected the aspect of their dances that depicts direction.”
Bees perform waggle dances to communicate information to their nestmates about the direction and distance to food sources (von Frisch, 1967). The goal of a study conducted by Klein et al. (2010) was to determine if sleep deprivation affected the bees’ performance of waggle dances. In order to create conditions of sleep deprivation, this group of researchers disturbed forager bees by attaching metal tags to them, then placing them in an “insominator,” a device that magnetically jostled the tagged bees for 12 hours. The bees’ dancing and sleep behaviors were then observed for the 48 hours following the operation of the insominator. As a baseline for comparison, the waggle dances of both control and experimental bees were measured beforehand. This study established that when a bee was deprived of sleep, the precision of its waggle dances decreased. Specifically, it negatively affected the aspect of their dances that depicts direction; the angle of the bees’ dances on the comb with respect to gravity became more variable in the sleep-deprived bees. However, precision of the distance information, the duration of the dances, remained unchanged. Klein et al. (2010) hypothesized that conveying directional information is more physiologically or cognitively demanding than conveying information about distance. They concluded that it becomes more difficult for the bees to accurately perform their dances when they are sleep-deprived. These findings have broader significance, as decreased precision in waggle dances reduces the ability of dancing bees to direct their nestmates to food resources, which in turn decreases the foraging efficiency of their colony (Klein et al., 2010).
A study conducted by Beyaert et al., (2012) sought out to determine whether or not the consolidation of novel navigation memory in honey bees is dependent on sleep. The researchers trained a group of bees in a procedure termed a “forced navigation task,” where the bees where trained to a feeder that was located 100 feet away from the hive. Upon the bees arriving at the feeder, they were caught and equipped with a tracking device. They were then transported to a release site that they had not previously visited, located 1970 feet away from the hive, and a different direction than the feeder. The bees were then tracked on their journey back to the hive. In order for the bees to successfully travel from the release site back to the hive, it requires two cognitive processes that encode novel learning: locating their position in their new surroundings, and retrieving memories from their initial flight. After the initial forced navigation task, the bees were then randomly chosen to be in either a sleep-deprived or control group. The experimental group of bees was placed in a vortex located outside of the nest and were gently shaken for eight hours during the night, in order to interfere with their sleep. The control was left undisturbed in the hive during this eight hour period. The next day, the bees were taken back to the release site and their journey back to the hive was recorded once again. The researchers found that the sleep-deprived bees experienced impairment in their consolidation of novel navigation memory. On the first trial 58% of the control bees made it back to the hive compared to 83% on the second trial, indicating that the bees had used newly consolidated navigational memory during the second trial of the experiment. The sleep-deprived bees performed equally in both trials. This demonstrated that bees need sleep to consolidate memories that they are forced to rely on the next day.
In an experiment performed by Hussaini et al., (2009) sleep deprivation conditions were created by placing bees on an instrument called a “vortex”. The vortex shook the bee at 100-120 rpm every five minutes, for a period of 15 hours, in order to keep the bees awake. The bees were trained in a learning procedure known as “classical conditioning.” In classical conditioning, a “conditioned stimulus,” in this case an odour, is presented and rewarded with an unconditioned stimulus to which the bees normally respond, in this case sugar water. When bees were presented with the sugar water immediately after being exposed to the odour, they learned to associate the two stimuli so that in subsequent trials they usually stretched out their tongues upon receiving the odor alone. After the bees were conditioned, the researchers then tested to see if there was a significant difference between extinction memory in sleep-deprived versus rested bees. Extinction memory is defined as the process in which a previously conditioned response (in this case, the extension of the tongue to the odour) is performed by the subject, without the being given the reward afterwards (in this case, the sugar water) (Hussaini et al., 2009). Therefore, a new memory is formed (Hussaini et al., 2009). The new memory is what happens when the conditioned stimulus (odour) is given in the absence of the reward (Hussaini et al., 2009). This process takes place as the subject learns to uncouple a response from the previously conditioned stimulus (Hussaini et al., 2009). After a series of experiments, the researchers discovered that the sleep-deprived bees had significantly reduced scores for extinction learning compared to rested bees (Hussaini et al., 2009). However, this phenomenon was not detected in trials that measured acquisition memory- the initial conditioning during which they learn to respond to the odor (Hussaini et al., 2009).
“Sleep-deprived bees experienced impairment in their consolidation of novel navigation memory.”
The general consensus today is that bees can become stressed by a variety of environmental sources, including parasites, pesticides and nutritional deficiencies resulting from modern agricultural methods (Goulson et al., 2015). One of the most negative consequences of stress is a lowered immune function, which contributes to bees being more susceptible to other stressors which, in turn, can lead to shortened bee longevity and colony population decline (Goulson et al., 2015). This can be dangerous as it may cause colony disruptions from which bees cannot recover. The research is clear that combined stress negatively impacts honey bees. Is it possible that disruption and deprivation of sleep contributes to the combined stresses weighing on bees? A specific situation where bees may experience sleep deprivation is during relocation. Every February in the United States, more than a million hives of bees are transported via trucks across the country to California for the purpose of almond pollination. Some colonies are moved five or more times per year to pollinate various crops and take advantage of honey flows. A study by Nelson and Jay (1989) found that when hives were transported 14 km (9 miles) to a new location, they experienced a 23% greater loss in colony population compared to colonies that were not moved (i.e., control hives). Bees in the colonies that were moved were also much more likely to drift from their new location (Nelson & Jay, 1989). Did loss of sleep contribute to this loss of bees after their hives were moved? Does the stress of sleep deprivation contribute to the reduction in the size of bees’ brood-food glands that has been documented following their transport (Anh et al., 2012)? Does loss of sleep during long-distance transportation of colonies contribute to greater “oxidative stress” an internal imbalance that can damage cells and contribute to a reduction in immune function (Simone-Finstrom et al., 2016)? If loss of sleep contributes to a decline in immune function, does that help to explain why Nosema infections increase following hive movement (Zhu et al., 2014)?
In conclusion, sleep deprivation is detrimental to honey bees for a variety of reasons. There are many unanswered questions concerning the degree to which trucking hives from one place to another affects sleep and affects colony health. Further study of the consequences of sleep deprivation is likely to yield interesting links between colony health and beekeeping practices such as migratory beekeeping.
References
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Helfrich-Förster, C. 2017. Sleep in insects. Annual Review of Entomology 63: 69-86. doi.org/10.1146/annurev-ento-020117-043201
Hussaini, S., Bogusch, L., Landgraf, T., and Menzel, B. 2009. Sleep deprivation affects extinction but not acquisition memory in honeybees. Learning and Memory. 16: 698-705.
Kaiser, W. 1988. Busy bees need rest, too: behavioural and electromyographical sleep signs in honey bees. Journal of Comparative Physiology.163: 565-584.
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von Frisch, K. 1967. The dance language and orientation of bees. Cambridge: The Belknap Press of Harvard University Press
Zhu, X., Zhou, S., and Huang, Z. 2014. Transportation and pollination service increase abundance and prevalence of Nosema cerane in honey bees (Apis mellifera). Journal of Apiculture Research. 53(4): 469-471.
