The ability to detect air motions with sensory hairs has evolved repeatedly: insects have filiform hairs, whereas spiders and their close relatives use `trichobothria' – to all intents and purposes sensory hairs, but not homologous to the insect's hairs and, of course, quite different from what we mammals consider as hair. The ability to sense local air motions, or `near-field sounds', serves a variety of purposes, from locating prey by spiders, to locating mates by mosquitoes. A fascinating, if originally subsidiary, potential function is communication within the species. Roger Santer and Eileen Hebets of the University of Nebraska – Lincoln have been investigating this, with the view that communication using near-field sound might turn out to be very widespread among arthropods.
Santer and Hebets used whip spiders – those scary-looking relatives of spiders and scorpions with an enormously extended pair of `antenniform'legs – collected from Florida to build up a convincing demonstration of the deliberate use of near-field sound in communication. When two male whip spiders meet each other, there is not so much a `stand-off' as a `stand very near'. Indeed, each whip spider positions himself so that one of their scary long legs is next to a sensory hair on one of the opposition's regular legs. While, yes, they do occasionally kick each other in the process, this happens sufficiently rarely for direct contact to be unlikely as the means of communication. Once the elongated legs are in position, they vibrate at around 20 Hz with an amplitude of a few millimetres (as observed from high speed video). Such contests can be achieved in complete darkness (so the competitors aren't watching each other), and the vibration display is performed longer by contestant winners than losers, suggesting that the leg-vibrating display conveys information through air movements (though it is not clear what) to resolve the contest.
While these observations alone are highly suggestive, Santer and Hebets took the story a considerable step further. They tuned a `stimulator', an oscillating 200 μm diameter tungsten wire, to replicate the motions of the vibrating leg. By wiggling this pseudo-leg at frequencies ranging from 1 to 120 Hz, while making electrophysiological recordings of the sensory hairs thought to receive information from near-field sounds, they demonstrated that the observed leg-waggling frequencies (around 20 Hz) caused particularly strong and sustained excitation in the sensory hairs. At lower waggling frequencies, there were fewer sensory cell excitations, as each vibration of the pseudo-leg stimulated a constant number of action potentials. At pseudo-leg-waggling frequencies that were too high, the team found a decrease in the sensory signal through time. At realistic leg-waggling frequencies, the sensory hair produced strong, clear signals from which the duration of a leg-waggling bout could be determined. As this is what the behavioural observations had suggested was related to performance in male–male contests, it appears that the leg-waggling frequency and the sensitivity of the air movement-sensing hairs are well matched.
This combination of behavioural and electrophysiological evidence demonstrates that, yes, whip spiders can communicate using the near-field sounds produced by their shaking legs. Given these air movement-sensing hairs turn up very widely across arthropods, Santer and Hebets suggest that similar signalling using near-field sound might actually be quite prevalent. While this will take further work to validate, Santer and Hebets have convincingly ticked the first box of a potentially very long list.
