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Research Article
Seismic sensitivity and bone conduction mechanisms enable extratympanic hearing in salamanders
G. Capshaw, D. Soares, J. Christensen-Dalsgaard, C. E. Carr
Journal of Experimental Biology 2020 223: jeb236489 doi: 10.1242/jeb.236489 Published 21 December 2020
G. Capshaw
1Department of Biology, University of Maryland, College Park, MD 20742, USA
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  • For correspondence: gcapshaw@umd.edu
D. Soares
2Department of Biological Sciences, New Jersey Institute of Technology, Newark, NJ 07102, USA
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J. Christensen-Dalsgaard
3Department of Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark
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C. E. Carr
1Department of Biology, University of Maryland, College Park, MD 20742, USA
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ABSTRACT

The tympanic middle ear is an adaptive sensory novelty that evolved multiple times in all 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 probably 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.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: G.C., D.S., J.C.-D., C.E.C.; Methodology: G.C., D.S., J.C.-D., C.E.C.; Software: J.C.-D.; Validation: G.C., J.C.-D.; Formal analysis: G.C., J.C.-D.; Investigation: G.C., D.S., J.C.-D.; Resources: D.S., J.C.-D., C.E.C.; Writing - original draft: G.C.; Writing - review & editing: G.C., D.S., J.C.-D., C.E.C.; Visualization: G.C.; Supervision: D.S., C.E.C.; Project administration: D.S., C.E.C.; Funding acquisition: G.C., D.S., J.C.-D., C.E.C.

  • Funding

    This work was supported by the National Institute on Deafness and Other Communication Disorders (NIDCD/NIH) training grant T32 DC-000046 to the University of Maryland's Center for Comparative and Evolutionary Biology of Hearing, and NIDCD/NIH grant DC-000436 (to C.E.C.), research grants from The Explorer's Club Washington Group (to G.C.) and the American Society of Ichthyologists and Herpetologists (Gaige Award to G.C.), and grants from the Carlsberg Foundation (2009-01-0292 and 2012-01-0662 to J.C.-D.). Deposited in PMC for release after 12 months.

  • Received August 28, 2020.
  • Accepted November 1, 2020.
  • © 2020. Published by The Company of Biologists Ltd
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Keywords

  • Amphibian
  • Auditory
  • Evoked potentials
  • Sound
  • Vibration detection

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Research Article
Seismic sensitivity and bone conduction mechanisms enable extratympanic hearing in salamanders
G. Capshaw, D. Soares, J. Christensen-Dalsgaard, C. E. Carr
Journal of Experimental Biology 2020 223: jeb236489 doi: 10.1242/jeb.236489 Published 21 December 2020
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Research Article
Seismic sensitivity and bone conduction mechanisms enable extratympanic hearing in salamanders
G. Capshaw, D. Soares, J. Christensen-Dalsgaard, C. E. Carr
Journal of Experimental Biology 2020 223: jeb236489 doi: 10.1242/jeb.236489 Published 21 December 2020

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