When foraging honey bees find a source of food, they return to their hive and perform a “waggle dance” to communicate the location of the food source to their hive mates. The waggle dance is performed on a platform near the entrance to the hive, and consists of visual signals, as well as sounds produced by wing movements and vibrations of the abdomen.
New research by team from the Graduate School of Bioagricultural Sciences at Nagoya University, Japan, in collaboration with researchers from the University of Iowa’s Department of Biological Sciences, shows that mechanoreceptors called Johnson’s organs, in the honey bee’s antennae, are exquisitely tuned to the frequencies made by air particle movements generated by the movements of the dancing bee. The findings are published online today, in the journal PLoS One.
In the study, transmission electron microscope was used to examine the ultrastructure of the honey bee’s Johnson’s organ. At the end of the honey bee’s antennae are segmented structures called flagella. These are highly sensitive movement detectors, which respond to displacements of the flagellar tip of just 20 nanometres (20 billionths of a metre) that occur in response to movements of air. These movements are detected by the Johnson’s organs, which, in the honey bee, are found in the second segment of the antenna (the pedicel), within the joint between the flagellum and the basal region of the antenna (the scape).
In the honey bee, the Johnson’s organ consists of a highly organized array of 300-320 sensory units called scolopidia. The entire array is attached to about 50 “knobs”, which are arranged in the cuticle around the circumference of the pedicel. Each of the cuticular knobs (labelled ‘K’ in the diagram below) is attached to 3-10 scolopidia, by fibres which extend down into the Johnson’s organ. The ends of the fibres are attached to a spindle-shaped cage formed by a scolopale cell (SC); inside the cage are the dendrites of 3 sensory neurons.
Thus, the movements of air particles cause mechanical vibrations in the flagellum (the third, and most distal segment of the antennae), which displace the cuticular knobs on the outer surface of the pedicel. These vibrations are transmitted along the fibres and into the cage formed by the scolapale cell, where they are transduced into electrical signals by the sensory neurons. The action potentials generated by these neurons travel down the cells’ axons to the mechanosensory region of the brain, where they undergo further auditory processing.
The researchers then carried out electrophysiological recordings so that the responses of the Johnson’s organ neurons to stimulation could be observed. They designed various auditory stimuli; one consisted of 100 millisecond tones with a frequency of 50-1,000 Hertz (Hz, cycles per second), another consisted of four 20 millisecond pulses with a frequency of 265 Hz, corresponding to the sounds produced by a bee performing the waggle dance. Microelectrodes were inserted into the Johnson’s organ, at the joint between the scape and the pedicel (marked by an arrow in the scanning electron micrograph of highest magnification), the recordings were played back, and the sound-evoked potentials measured.
It was found that the antennae of mature worker bees are most sensitive to sounds with a frequency of between 250-300 Hz, and that the frequency and timing of the flagellar vibrations are accurately translated into the neural responses of the sensory cells in the Johnson’s organ. The worker bees’ hearing is therefore perfectly tuned to detect the movements of other bees, and the auditory system is ideal for listening in on the sounds made by other workers performing a dance no more than several millimetres away.
However, it was also found that the sensitivity of the Johnson’s organ was dependent on the age of the bee – only older workers are able to detect the sounds made by a waggle dance. In a hive, different castes of bees perform different roles. Young worker bees feed the queen and the larvae, middle-aged workers perform housekeeping (or, rather, hive-keeping) duties and store food, and only the older workers forage for food. The hearing of the honey bee matures with age, such that only workers old enough to forage for food can detect the sounds of the waggle dance.
Tsujiuchi, S., et al (2007). Dynamic range compression in the honey bee auditory system toward waggle dance sounds. PLoS One 2: e234. doi:10.1371/journal.pone.0000234. [Full text]