Slumber in a cell: honeycomb used by honey bees for food, brood, heating and sleeping.

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 (Apis mellifera) 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, we 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 noninvasively 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.

Perceived Synchrony of Frog Multimodal Signal Components Is Influenced by Content and Order.

Multimodal signaling is common in communication systems. Depending on the species, individual signal components may be produced synchronously as a result of physiological constraint (fixed) or each component may be produced independently (fluid) in time. For animals that rely on fixed signals, a basic prediction is that asynchrony between the components should degrade the perception of signal salience, reducing receiver response. Male túngara frogs, Physalaemus pustulosus, produce a fixed multisensory courtship signal by vocalizing with two call components (whines and chucks) and inflating a vocal sac (visual component). Using a robotic frog, we tested female responses to variation in the temporal arrangement between acoustic and visual components. When the visual component lagged a complex call (whine + chuck), females largely rejected this asynchronous multisensory signal in favor of the complex call absent the visual cue. When the chuck component was removed from one call, but the robofrog inflation lagged the complex call, females responded strongly to the asynchronous multimodal signal. When the chuck component was removed from both calls, females reversed preference and responded positively to the asynchronous multisensory signal. When the visual component preceded the call, females responded as often to the multimodal signal as to the call alone. These data show that asynchrony of a normally fixed signal does reduce receiver responsiveness. The magnitude and overall response, however, depend on specific temporal interactions between the acoustic and visual components. The sensitivity of túngara frogs to lagging visual cues, but not leading ones, and the influence of acoustic signal content on the perception of visual asynchrony is similar to those reported in human psychophysics literature. Virtually all acoustically communicating animals must conduct auditory scene analyses and identify the source of signals. Our data suggest that some basic audiovisual neural integration processes may be at work in the vertebrate brain.

Robots in the service of animal behavior.

As reading fiction can challenge us to better understand fact, using fake animals can sometimes serve as our best solution to understanding the behavior of real animals. The use of dummies, doppelgangers, fakes, and physical models have served to elicit behaviors in animal experiments since the early history of behavior studies, and, more recently, robotic animals have been employed by researchers to further coax behaviors from their study subjects. Here, we review the use of robots in the service of animal behavior, and describe in detail the production and use of one type of robot - "faux" frogs - to test female responses to multisensory courtship signals. The túngara frog (Physalaemus pustulosus) has been a study subject for investigating multimodal signaling, and we discuss the benefits and drawbacks of using the faux frogs we have designed, with the larger aim of inspiring other scientists to consider the appropriate application of physical models and robots in their research.

Multimodal signal variation in space and time: how important is matching a signal with its signaler?

Multimodal signals (acoustic+visual) are known to be used by many anuran amphibians during courtship displays. The relative degree to which each signal component influences female mate choice, however, remains poorly understood. In this study we used a robotic frog with an inflating vocal sac and acoustic playbacks to document responses of female túngara frogs to unimodal signal components (acoustic and visual). We then tested female responses to a synchronous multimodal signal. Finally, we tested the influence of spatial and temporal variation between signal components for female attraction. Females failed to approach the isolated visual cue of the robotic frog and they showed a significant preference for the call over the spatially separate robotic frog. When presented with a call that was temporally synchronous with the vocal sac inflation of the robotic frog, females did not show a significant preference for this over the call alone; when presented with a call that was temporally asynchronous with vocal sac inflation of the robotic frog, females discriminated strongly against the asynchronous multimodal signal in favor of the call alone. Our data suggest that although the visual cue is neither necessary nor sufficient for attraction, it can strongly modulate mate choice if females perceive a temporal disjunction relative to the primary acoustic signal.

The Curious Connection Between Insects and Dreams.

A majority of humans spend their waking hours surrounded by insects, so it should be no surprise that insects also appear in humans' dreams as we sleep. Dreaming about insects has a peculiar history, marked by our desire to explain a dream's significance and by the tactic of evoking emotions by injecting insects in dream-related works of art, film, music, and literature. I surveyed a scattered literature for examples of insects in dreams, first from the practices of dream interpretation, psychiatry, and scientific study, then from fictional writings and popular culture, and finally in the etymology of entomology by highlighting insects with dream-inspired Latinate names. A wealth of insects in dreams, as documented clinically and culturally, attests to the perceived relevance of dreams and to the ubiquity of insects in our lives.

Sleep deprivation impairs precision of waggle dance signaling in honey bees.

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.

Caste-dependent sleep of worker honey bees.

Sleep is a dynamic phenomenon that changes throughout an organism's lifetime, relating to possible age- or task-associated changes in health, learning ability, vigilance and fitness. Sleep has been identified experimentally in many animals, including honey bees (Apis mellifera). As worker bees age they change castes, typically performing a sequence of different task sets (as 'cell cleaners', 'nurse bees', 'food storers' and 'foragers'). Belonging to a caste could differentially impact the duration, constitution and periodicity of a bee's sleep. We observed individually marked bees within observation hives to determine caste dependent patterns of sleep behavior. We conducted three studies 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 castes we 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 c cleaners and nurse bees exhibited no sleep:wake rhythmicity, food storers and foragers experienced a 24 h 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, our study reveals that the youngest adult bees sleep the most, with all older castes 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.