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Superorganism inhibitory communication

There is strong evidence that a vibrational signal, the honey bee “stop signal” (Nieh 1993; Lau and Nieh 2010, McCollough and Nieh 2015, and Tan et al. 2016) inhibits the waggle dance. This inhibition reduces recruitment to a specific food location when the signal sender is attacked by a food competitor or potential predator at that location (Nieh 2010). Modeling demonstrates that this can significantly increase the efficiency of food exploitation by allowing the colony to reallocate its foraging labor away from food sources where foragers are endangered (Johnson and Nieh 2010). This discovery provides one of the most sophisticated examples of inhibitory signaling in a superorganism. Thus, as in intra- and inter-cellular communication, negative feedback may play an important, though currently underappreciated, role in self-organizing behaviors within superorganisms.

Most recently, Tan et al. (2016) have shown that this stop signal also exists in the Asian honey bee species, Apis cerana, and is evidently functionally referential. Larger and more dangerous hornets elicit stop signals with a higher fundamental frequency and such higher frequency signals are more effective at inhibiting waggle dancing than lower frequency signals. Interestingly, it is known that the closely related European honey bee, Apis mellifera, is more sensitive (has a lower freezing response threshold) for higher frequency signals. In addition, A. cerana stop signals also appear to encode the attack context, with longer duration signals corresponding to the more dangerous situation of hornets attacking the nest as compared to hornets attacking foragers far away from the colony.

In the video below, you will see and hear three stop signals produced by A. cerana. The waggle dancer does not stop, in this case, until after it has received the third stop signal. This illustrate how stop signals increase the probability of a receiver response but do not always immediately stop waggle dancing.

The video below was produced by UCSD television and provides a narrated introduction on the stop signal.

In the video below, the honey bee (Apis mellifera) in the upper left of the screen is moving down and using her head to butt against the bee in the center (this bee is painted with violet and white dots on her thorax). Simultaneously, she produces a short pulse of sound which is the stop signal. This signal has the effect of causing the receiver to either stop waggle dancing or to reduce the number of waggle dance circuits that she would perform. In this video, the receiver is still unloading her collected nectar to other bees who will concentrate it to produce honey. This video is repeated twice.

The high speed video below, filmed by Heather Bell, shows a waggle dancing honey bee receiving a stop signal at normal speed and then slowed down. The waggle dancer is towards the bottom of the screen and the stop signaler is at 3:00. She butts her head against the waggle dancer.

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References

Please note: The copyright of these articles (with the exception of Open Access articles) is with their respective publishers. By downloading an article, you agree to limit the use of the pdf file to printing of single copies for personal research and study. You may not modify the files in any way, or to use them for commercial purposes.

Johnson BR, Nieh JC (2010) Modeling the adaptive role of negative signaling in honey bee intraspecific competition. Journal of Insect Behavior 23: 459-471

Lau CW, Nieh JC (2010) Honey bee stop-signal production: temporal distribution and effect of feeder crowding. Apidologie 41: 87-95

Nieh JC (2010) A negative feedback signal is triggered by peril and curbs honey bee recruitment. Current Biology 20: 1-6

Nieh JC (1993) The stop signal of honey bees: Reconsidering its message. Behavioral Ecology and Sociobiology 33: 51-56