Social synchronization of circadian rhythms with a focus on honeybees.

Many animals benefit from synchronizing their daily activities with conspecifics. In this hybrid paper, we first review recent literature supporting and extending earlier evidence for a lack of clear relationship between the level of sociality and social entrainment of circadian rhythms. Social entrainment is specifically potent in social animals that live in constant environments in which some or all individuals do not experience the ambient day-night cycles. We next focus on highly social honeybees in which there is good evidence that social cues entrain the circadian clocks of nest bees and can override the influence of conflicting light-dark cycles. The current understanding of social synchronization in honeybees is consistent with self-organization models in which surrogates of forager activity, such as substrate-borne vibrations and colony volatiles, entrain the circadian clocks of bees dwelling in the dark cavity of the nest. Finally, we present original findings showing that social synchronization is effective even in an array of individually caged callow bees placed on the same substrate and is improved for bees in connected cages. These findings reveal remarkable sensitivity to social time-giving cues and show that bees with attenuated rhythms (weak oscillators) can nevertheless be socially synchronized to a common phase of activity. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Remarkable Sensitivity of Young Honey Bee Workers to Multiple Non-photic, Non-thermal, Forager Cues That Synchronize Their Daily Activity Rhythms.

Honey bees live in colonies containing tens of thousands of workers that coordinate their activities to produce efficient colony-level behavior. In free-foraging colonies, nest bees are entrained to the forager daily phase of activity even when experiencing conflicting light-dark illumination regime, but little is known on the cues mediating this potent social synchronization. We monitored locomotor activity in an array of individually caged bees in which we manipulated the contact with neighbour bees. We used circular statistics and coupling function analyses to estimate the degree of social synchronization. We found that young bees in cages connected to cages housing foragers showed stronger rhythms, better synchronization with each other, higher coupling strength, and a phase more similar to that of the foragers compared to similar bees in unconnected cages. These findings suggest that close distance contacts are sufficient for social synchronization or that cage connection facilitated the propagation of time-giving social cues. Coupling strength was higher for bees placed on the same tray compared with bees at a similar distance but on a different tray, consistent with the hypothesis that substrate borne vibrations mediate phase synchronization. Additional manipulation of the contact between cages showed that social synchronization is better among bees in cages connected with tube with a single mesh partition compared to sealed tubes consistent with the notion that volatile cues act additively to substrate borne vibrations. These findings are consistent with self-organization models for social synchronization of activity rhythms and suggest that the circadian system of honey bees evolved remarkable sensitivity to non-photic, non-thermal, time giving entraining cues enabling them to tightly coordinate their behavior in the dark and constant physical environment of their nests.

Colony Volatiles and Substrate-borne Vibrations Entrain Circadian Rhythms and Are Potential Cues Mediating Social Synchronization in Honey Bee Colonies.

Internal circadian clocks organize animal behavior and physiology and are entrained by ecologically relevant external time-givers such as light and temperature cycles. In the highly social honey bee, social time-givers are potent and can override photic entrainment, but the cues mediating social entrainment are unknown. Here, we tested whether substrate-borne vibrations and hive volatiles can mediate social synchronization in honey bees. We first placed newly emerged worker bees on the same or on a different substrate on which we placed cages with foragers entrained to ambient day-night cycles, while minimizing the spread of volatiles between cages. In the second experiment, we exposed young bees to constant airflow drawn from either a free-foraging colony or a similar-size control hive containing only heated empty honeycombs, while minimizing transfer of substrate-borne vibrations between cages. After 6 days, we isolated each focal bee in an individual cage in an environmental chamber and monitored her locomotor activity. We repeated each experiment 5 times, each trial with bees from a different source colony, monitoring a total of more than 1000 bees representing diverse genotypes. We found that bees placed on the same substrate as foragers showed a stronger phase coherence and a phase more similar to that of foragers compared with bees placed on a different substrate. In the second experiment, bees exposed to air drawn from a colony showed a stronger phase coherence and a phase more similar to that of foragers compared with bees exposed to air from an empty hive. These findings lend credence to the hypothesis that surrogates of activity entrain circadian rhythms and suggest that multiple social cues can act in concert to entrain social insect colonies to a common phase.

Octopamine Underlies the Counter-Regulatory Response to a Glucose Deficit in Honeybees (Apis mellifera).

An animal's internal state is a critical parameter required for adaptation to a given environment. An important aspect of an animal's internal state is the energy state that is adjusted to the needs of an animal by energy homeostasis. Glucose is one essential source of energy, especially for the brain. A shortage of glucose therefore triggers a complex response to restore the animal's glucose supply. This counter-regulatory response to a glucose deficit includes metabolic responses like the mobilization of glucose from internal glucose stores and behavioral responses like increased foraging and a rapid intake of food. In mammals, the catecholamines adrenalin and noradrenalin take part in mediating these counter-regulatory responses to a glucose deficit. One candidate molecule that might play a role in these processes in insects is octopamine (OA). It is an invertebrate biogenic amine and has been suggested to derive from an ancestral pathway shared with adrenalin and noradrenalin. Thus, it could be hypothesized that OA plays a role in the insect's counter-regulatory response to a glucose deficit. Here we tested this hypothesis in the honeybee (Apis mellifera), an insect that, as an adult, mainly feeds on carbohydrates and uses these as its main source of energy. We investigated alterations of the hemolymph glucose concentration, survival, and feeding behavior after starvation and examined the impact of OA on these processes in pharmacological experiments. We demonstrate an involvement of OA in these three processes in honeybees and conclude there is an involvement of OA in regulating a bee's metabolic, physiological, and behavioral response following a phase of prolonged glucose deficit. Thus, OA in honeybees acts similarly to adrenalin and noradrenalin in mammals in regulating an animal's counter-regulatory response.