The complex world of honey bee vibrational signaling: A response to Ramsey et al. (2017)

            Ramsey et al. [1] report on the characteristics and temporal distribution of an interesting vibrational signal that they term the “whooping signal”, primarily based upon a long-term study of vibrations recorded by accelerometers placed inside two honey bee (Apis mellifera) colonies, one in France and one in the United Kingdom. The goal of the study, the long-term automated recording and analysis of honey bee vibrational signaling, is worthwhile—but we believe that some of the conclusions drawn by the authors are not well supported, given the evidence.

            Honey bees, particularly the relatively well-studied species, A. mellifera, have a wide variety of vibrational signals that play an important role in organizing and coordinating colony life [2–13]. Understanding the differences between these signals is important. The crux of our criticism rests on how the authors were able to accurately identify and describe signals based largely upon accelerometers implanted inside colonies without additional behavioral data and using signal processing techniques that may not have been sufficient to discriminate between multiple types of vibrational signals. We also believe that they have incorrectly dismissed an interesting and plausible explanation for their results.

            The authors describe the discovery of a new signal, which they call the whooping signal. They state that the whooping signal is “a honeybee vibrational pulse with the same characteristics of what has previously been described as a stop signal” (p 1, [1]). To support the need for this new signal name, they cite different descriptions of what is generally now called the “stop signal” [12,14–16]. The stop signal is a brief vibrational signal, often delivered by waggle dance followers head butting waggle dancers. The stop signal was originally called a begging signal but only rarely elicits food samples [14,17]. However, it is agreed to cause momentary freezing of the signal recipient [3], hence the name “stop signal”. Stop signals have also been called a “brief piping signal” or a “nectar forager pipe” [17,18]. Multiple studies now show that stop signals decrease the number of dance circuits performed by a waggle dancing recipient, thereby inhibiting recruitment [14–17,19] although other functions are certainly possible. Ramsey et al. [1] note that the stop signal has been implicated in re-allocation of tasks within the hive [19] because it is produced by tremble dancers in response to long nectar unloading wait times. With the exception of its possible role in task allocation, all of the other published and currently accepted functions of the stop signal in A. mellifera are consistent with waggle dance inhibition.

            Thus, the objections raised by Ramsey et al. [1] about multiple stop signal contexts and functions (danger at a resource during foraging [15], crowding at a resource during foraging [20], and during consensus-forming hile house-hunting [16]) are not problematic. In fact, the stop signal can be seen as an elegant evolutionary solution that counterbalances the positive feedback of the waggle dance, which itself serves multiple functions by recruiting nestmates for diverse resources: water, nectar, pollen, resin, nest sites, and, in Apis dorsata, migration direction [21–25]. We agree that there is much to be learned about honey bee vibrational signaling and also about the stop signal. However, it is incorrect to imply that the descriptions of what has been called the begging signal or stop signal describe vastly differing phenomena lacking any unifying theme. Below, we detail our main concerns about Ramsey et al. [1].