Hearing of the African lungfish (Protopterus annectens) suggests underwater pressure detection and rudimentary aerial hearing in early tetrapods

Abstract

In the transition from an aquatic to a terrestrial lifestyle, vertebrate auditory systems have undergone major changes while adapting to aerial hearing. Lungfish are the closest living relatives of tetrapods and their auditory system may therefore be a suitable model of the auditory systems of early tetrapods such as Acanthostega. Therefore, experimental studies on the hearing capabilities of lungfish may shed light on the possible hearing capabilities of early tetrapods and broaden our understanding of hearing across the water-to-land transition. Here, we tested the hypotheses that (i) lungfish are sensitive to underwater pressure using their lungs as pressure-toparticle motion transducers and (ii) lungfish can detect airborne sound. To do so, we used neurophysiological recordings to estimate the vibration and pressure sensitivity of African lungfish (Protopterus annectens) in both water and air. We show that lungfish detect underwater sound pressure via pressure-to-particle motion transduction by air volumes in their lungs. The morphology of lungfish shows no specialized connection between these air volumes and the inner ears, and so our results imply that air breathing may have enabled rudimentary pressure detection as early as the Devonian era. Additionally, we demonstrate that lungfish in spite of their atympanic middle ear can detect airborne sound through detection of sound-induced head vibrations. This strongly suggests that even vertebrates with no middle ear adaptations for aerial hearing, such as the first tetrapods, had rudimentary aerial hearing that may have led to the evolution of tympanic middle ears in recent tetrapods.

Better than fish on land? Hearing across metamorphosis in salamanders

“…By contrast, the lungs of both juvenile and adult awake axolotls contained 2-3 ml air, which, compared with a model of fish swim-bladder vibrations [12], corresponds to a resonance frequency of 4-500 Hz. This finding matches the frequency range where axolotls can detect the sound pressure (figure 3a), suggesting that axolotls sense the underwater sound pressure by detecting the pressure-induced particle motion caused by the air volumes in their lungs, as seen in lungfish [30].…”

“…The high sensitivity is underlined by the fact that thresholds determined by evoked potentials may be 10-30 dB above thresholds determined by single cell recordings or behavioural studies in a variety of animals [39 -41]. Moreover, the low-frequency vibration sensitivity found here is comparable with the vibration sensitivity of lungfish [30,42] in terms of best frequency and sensitivity, but whereas the lungfish vibrogram is U-shaped, the salamander vibrograms were W-shaped, having an additional peak at higher frequencies. In frogs, both the saccule and the amphibian papilla are involved in detection of substrate vibrations: the saccule being most sensitive at frequencies below 100 Hz, and the amphibian papilla to frequencies between 60 and 600 Hz [43][44][45].…”

“…The salamanders had their head resting on a shaker platform 80 cm below a loudspeaker to determine acceleration and sound pressure threshold, respectively. The underwater experiments were conducted in a standing wave tube set-up [30] where an underwater loudspeaker was placed in the bottom of a 2 m long and 30 cm diameter water-filled steel tube with 1 cm thick walls. Sound stimulation created standing waves in the tube and hence the underwater hearing sensitivity could be investigated under different particle motion-to-pressure conditions by changing the measuring depth in the tube.…”

Diversity in Fish Auditory Systems: One of the Riddles of Sensory Biology

“…Prior studies in other taxa demonstrated that fishes can detect sound pressure in the absence of a clear connection ( Figure 12D). This has been shown in the genus Stegastes (family Pomacentridae, damselfishes; Myrberg and Spires, 1980), Gadus (family Gadidae, cods; Sand and Enger, 1973), and recently in the African lungfish Protopterus (family Protopteridae, lungfishes, Christensen et al, 2015). It is assumed that in these families bladder wall oscillations are transmitted to the inner ears via the interjacent tissue (Hawkins, 1986).…”

“…To date it remains elusive how certain inner ear modifications are correlated to certain aspects of auditory abilities. Moreover, only few studies successfully disentangle the detection of the amounts of particle motion and sound pressure in fishes (e.g., Myrberg and Spires, 1980;Christensen et al, 2015).…”