A general mechanism of air-borne hearing in Recent and early non-tympanate tetrapods

Abstract

Tetrapod tympanic hearing probably emerged in the Triassic with independent origins in each of the major groups, more than 120 Myr after the water-land transition. During this long period, any auditory sensitivity must have been based on non-tympanic, bone conduction mechanisms. However, bone conduction is a non-specific term describing several different modes of vibration that can stimulate the inner ear. To understand hearing in a non-tympanic ear, we focus on the simplest model: that sound translates the head, i.e., that the head is pushed and pulled by the sound wave, and that this vibration is transduced by the inner ear. Simple translation is the mode of human low-frequency bone conduction sensitivity and translation by underwater sound is also the mode of auditory stimulation for most fishes. It is therefore a straightforward assumption that this may have been the mechanism of hearing in the early tetrapods. According to acoustic theory, the efficiency of translation of an object by sound is determined by its density and ka, the product of the acoustic wavenumber (k) and the radius (a) of the head. Simple finite-element models of translation by sound show that vibration velocities only depend on ka and density (for objects of the same shape and composition) and are almost constant (between 4 and 5 {micro}m/s/Pa depending on shape) for objects with ka<1. We compare sensitivity to sound and to vibrations of the skull in animals lacking tympanic middle ears (snakes, salamanders, earless frogs, and lungfish) and show that the low-frequency air-borne sound sensitivity in these species is largely consistent with a translation mechanism. How translation of the head or body can stimulate the inner ear is most evident in an inertial system like the otolithic/otoconial ears of fish and early tetrapods, but fluid inertia in the inner ear may also generate hydrodynamic waves that can stimulate hair cells in the tetrapod inner ear, providing a mechanism for this simple mode of sound reception to confer hearing in earless animals.