Hearing with an atympanic ear: good vibration and poor sound-pressure detection in the royal python, Python regius

Brandt

Willis

et al. 2012

Proc. R. Soc. B.

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Turtles, like other amphibious animals, face a trade-off between terrestrial and aquatic hearing. We used laser vibrometry and auditory brainstem responses to measure their sensitivity to vibration stimuli and to airborne versus underwater sound. Turtles are most sensitive to sound underwater, and their sensitivity depends on the large middle ear, which has a compliant tympanic disc attached to the columella. Behind the disc, the middle ear is a large air-filled cavity with a volume of approximately 0.5 ml and a resonance frequency of approximately 500 Hz underwater. Laser vibrometry measurements underwater showed peak vibrations at 500-600 Hz with a maximum of 300 mm s 21 Pa 21 , approximately 100 times more than the surrounding water. In air, the auditory brainstem response audiogram showed a best sensitivity to sound of 300-500 Hz. Audiograms before and after removing the skin covering reveal that the cartilaginous tympanic disc shows unchanged sensitivity, indicating that the tympanic disc, and not the overlying skin, is the key sound receiver. If air and water thresholds are compared in terms of sound intensity, thresholds in water are approximately 20-30 dB lower than in air. Therefore, this tympanic ear is specialized for underwater hearing, most probably because sound-induced pulsations of the air in the middle ear cavity drive the tympanic disc.

Section: Discussionmentioning

confidence: 99%

Specialization for underwater hearing by the tympanic middle ear of the turtle,Trachemys scripta elegans

Brandt

Willis

et al. 2012

Proc. R. Soc. B.

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“…The neurophysiological experiments in air were conducted in a combined acceleration and sound pressure setup previously described (Christensen et al, 2012). To minimize the vibrational noise coupling from the floor, the shaker was put on a 60×60 cm iso-plate passive isolation system (PTT600600, Thorlabs), four passive isolation mounts (PWA075, Thorlabs) and successive layers of flagstone and styrofoam.…”

Section: Experimental Setup and Calibrationmentioning

confidence: 99%

“…They may therefore be hypothesized to be unable to detect aerial sound pressure. However, vibration sensitivity has been shown to enable atympanic vertebrates such as snakes and likely also salamanders to sense airborne sound through detection of sound-induced head vibrations (Christensen et al, 2012;Christensen et al, 2015). It is therefore possible that lungfish are also able to sense airborne sound via a similar mechanism.…”

Section: Introductionmentioning

confidence: 99%

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

Christensen

Journal of Experimental Biology

Madsen

2015

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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.

“…Data collection and analyses were made using MATLAB and RPVDSEX v. 72 (TDT). Both sound and vibrational background noise levels were measured and quantified in octave levels to provide a conservative measure of the potential masking noise [29].…”

Section: (A) Metamorphosismentioning

confidence: 99%

Better than fish on land? Hearing across metamorphosis in salamanders

Christensen

Lauridsen

et al. 2015

Proc. R. Soc. B.

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Early tetrapods faced an auditory challenge from the impedance mismatch between air and tissue in the transition from aquatic to terrestrial lifestyles during the Early Carboniferous (350 Ma). Consequently, tetrapods may have been deaf to airborne sounds for up to 100 Myr until tympanic middle ears evolved during the Triassic. The middle ear morphology of recent urodeles is similar to that of early 'lepospondyl' microsaur tetrapods, and experimental studies on their hearing capabilities are therefore useful to understand the evolutionary and functional drivers behind the shift from aquatic to aerial hearing in early tetrapods. Here, we combine imaging techniques with neurophysiological measurements to resolve how the change from aquatic larvae to terrestrial adult affects the ear morphology and sensory capabilities of salamanders. We show that air-induced pressure detection enhances underwater hearing sensitivity of salamanders at frequencies above 120 Hz, and that both terrestrial adults and fully aquatic juvenile salamanders can detect airborne sound. Collectively, these findings suggest that early atympanic tetrapods may have been pre-equipped to aerial hearing and are able to hear airborne sound better than fish on land. When selected for, this rudimentary hearing could have led to the evolution of tympanic middle ears.