Seismic sensitivity and bone conduction mechanisms enable extratympanic hearing in salamanders

Abstract

The tympanic middle ear is an adaptive sensory novelty that evolved multiple times in all of the major terrestrial tetrapod groups to overcome the impedance mismatch generated when aerial sound encounters the air-skin boundary. Many extant tetrapod species have lost their tympanic middle ears, yet they retain the ability to detect airborne sound. In the absence of a functional tympanic ear, extratympanic hearing may occur via the resonant qualities of air-filled body cavities, sensitivity to seismic vibration, and/or bone conduction pathways to transmit sound from the environment to the ear. We used auditory brainstem response recording and laser vibrometry to assess the contributions of these extratympanic pathways for airborne sound in atympanic salamanders. We measured auditory sensitivity thresholds in eight species and observed sensitivity to low frequency sound and vibration from 0.05-1.2 kHz and 0.02-1.2 kHz, respectively. We determined that sensitivity to airborne sound is not facilitated by the vibrational responsiveness of the lungs or mouth cavity. We further observed that, although seismic sensitivity likely contributes to sound detection under naturalistic scenarios, airborne sound stimuli presented under experimental conditions did not produce vibrations detectable to the salamander ear. Instead, threshold-level sound pressure is sufficient to generate translational movements in the salamander head, and these sound-induced head vibrations are detectable by the acoustic sensors of the inner ear. This extratympanic hearing mechanism mediates low frequency sensitivity in vertebrate ears that are unspecialized for the detection of aerial sound pressure, and may represent a common mechanism for terrestrial hearing across atympanic tetrapods.