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

Oliver Siehler,Guy Bloch,Shuo Wang

doi:10.3389/fphys.2021.789773

Oliver Siehler, Guy Bloch + Show 1 more

Open Access

https://doi.org/10.3389/fphys.2021.789773

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Abstract

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.

Highlights

Circadian clocks are endogenous pacemakers capable of autonomously generating rhythms of about a day (∼24 h)
We found that after 7 days, the phase difference between young bees and foragers was smaller for the connected compared to the unconnected bees (Figures 3A,B)
We combined a tightly controlled lab assay and a new pipeline to assess social synchronization of activity rhythms among honey bee foragers and young bees, each isolated in a separate monitoring cage

Summary

Introduction

Circadian clocks are endogenous pacemakers capable of autonomously generating rhythms of about a day (∼24 h). Ambient light and temperature cycles, which are influenced by the sun position, are considered the most important environmental cues entraining circadian clocks (known as “time-givers,” or “zeitgebers” in German). The notion that the sun is the pivotal source for entraining cues is consistent with the view that circadian clocks have evolved to adjust the biology of organisms on Earth to predicted daily fluctuations in their environment. There has been significant progress in research on the mechanisms and entrainment by diet and feeding cycles (e.g., López-Olmeda, 2017; Tomioka and Matsumoto, 2019; Lewis et al, 2020). Additional cues that may entrain circadian rhythms stem from social interactions between individuals of the same species (for a recent review Siehler et al, 2021)

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