Circadian rhythms in behaviour and physiology are important for animal health and survival. Studies with individually isolated animals in the laboratory have consistently emphasized the dominant role of light for the entrainment of circadian rhythms to relevant environmental cycles. Although in nature interactions with conspecifics are functionally significant, social signals are typically not considered important time-givers for the animal circadian clock. Our results challenge this view. By studying honeybees in an ecologically relevant context and using a massive data set, we demonstrate that social entrainment can be potent, may act without direct contact with other individuals and does not rely on gating the exposure to light. We show for the first time that social time cues stably entrain the clock, even in animals experiencing conflicting photic and social environmental cycles. These findings add to the growing appreciation for the importance of studying circadian rhythms in ecologically relevant contexts.
The insect antennae receive olfactory information from the environment. In some insects, it has been shown that antennal responsiveness is dynamically regulated by circadian clocks. However, it is unknown how general this phenomenon is and what functions it serves. Circadian regulation in honeybee workers is particularly interesting in this regard because they show natural task-related chronobiological plasticity. Forager bees show strong circadian rhythms in behavior and brain gene expression, whereas nurse bees tend brood around-the-clock and have attenuated circadian rhythms in activity and whole-brain gene expression. Here, we tested the hypothesis that there is task-related plasticity in circadian rhythms of antennal responsiveness to odorants in worker honeybees. We used electroantennogram (EAG) to measure the antennal responsiveness of nurses and foragers to general odorants and pheromones around the day. The capacity to track 10-Hz odorant pulses varied with time of day for both task groups but with different phases. The antennal pulse-tracking capacity was higher during the subjective day for the day-active foragers, whereas it was better during the night for around-the-clock active nurses. The task-related phases of pulse-tracking rhythms were similar for all the tested stimuli. We also found evidence for circadian rhythms in the EAG response magnitude of foragers but not of nurses. To the best of our knowledge, these results provide the first evidence for circadian regulation of antennal olfactory responsiveness and odorant pulse-tracking capacity in bees or any other hymenopteran insect. Importantly, our study shows for the first time that the circadian phase of olfactory responsiveness may be socially regulated.
'Nurse' honeybees tend brood around the clock with attenuated or no circadian rhythms, but the brood signals inducing this behavior remain elusive. We first tested the hypothesis that worker circadian rhythms are regulated by brood pheromones. We monitored locomotor activity of individually isolated nurse bees that were exposed to either various doses of larval extract or synthetic brood ester pheromone (BEP). Bees orally treated with larval extract showed attenuated circadian rhythms in one of four tested colonies; a similar but statistically non-significant trend was seen in two additional colonies. Nurse bees treated with synthetic BEP showed rhythm attenuation in one of three tested colonies. Next, we tested the hypothesis that capped brood, which does not require feeding, nevertheless induces around-the-clock activity in nurses. By combining a new protocol that enables brood care by individually isolated nurse bees, detailed behavioral observations and automatic high-resolution monitoring of locomotor activity, we found that isolated nurses tended capped brood around the clock with attenuated circadian rhythms. Bees individually isolated in similar cages but without brood showed strong circadian rhythms in locomotor activity and rest. This study shows for the first time that the need to feed hungry larvae is not the only factor accounting for around-the-clock activity in nurse bees. Our results further suggest that the transition between activity with and without circadian rhythms is not a simple switch triggered by brood pheromones. Around-the-clock tending may enhance brood development and health in multiple ways that include improved larval feeding, thermoregulation or hygienic behavior.
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