Snakes hear by detection of sound-induced skull vibrations Good vibration and poor sound pressure detection in royal python (Python regius) Christian Bech Christensen1, Jakob Christensen-Dalsgaard2, Christian Brandt2 and Peter Teglberg Madsen1 1 Zoophysiology, Department of Bioscience, Aarhus University, Denmark. 2 Institute of Biology, University of Southern Denmark, Denmark. Introduction Corresponding author: [email protected] www.marinebioacoustics.com Snakes lack both an outer ear and a tympanic middle ear which is found in most terrestrial vertebrates. Matching the impedance of air and inner ear fluids, the tympanic middle ear enable response to the pressure component of sound by enhancing pressure to particle motion transformation. Snakes therefore appear unable to detect sound pressure and generally insensitive to airborne sound. The connection of the middle ear bone to the jaw bones in snakes, however, suggests acute vibration sensitivity. It has therefore been hypothesized that the high vibration sensitivity enable snakes to hear aerial 2,3 sounds by detecting the sound induced substrate vibrations . CT scan of Python Head: Mandible, Quadrate, Collumella, Inner Ear Space and Sacculus Hypotheses In this study we test the two hypotheses: 1) Snakes are sensitive to sound pressure 2) Snakes are sensitive to vibrations, but cannot hear the sound pressure per se. Methods Results Vibration sensitivity was highest at 80 and 120 Hz (Figure R1), with an average sensitivity of -54 dB re 1 m/s rms1. Sound pressure sensitivity was highest at 160 Hz (Figure R2) with an average sensitivity of 78 dB re 20 µPa rms1. 2 Vibrogram Experimental setup. The setup was placed in anechoic room to minimize acoustic noise and reflections. The speaker was suspended from strings from the ceiling to minimize direct coupling of vibrational noise. Swing and shaker were placed on consecutive layers of mineral wool and flag stones to minimize vibrational noise from the floor and within a Faraday cage to minimize electrical noise. Python in setup. [Photo: Christian Bech Christensen] Figure R1: Vibrogram of Python regius. Individual thresholds (•), Total octave noise of all three directions (x). Substrate Vibrations Figure R3: Sound-induced substrate vibrations (SV). SV induced by sound ( ), SV induced by vibration ( ) and Total octave noise (x). SV induced by threshold level sound pressure were above vibration thresholds at 80 Hz only, at all other frequencies they were below vibration thresholds. Audiogram Figure R2: Audiogram of Python regius. Individual thresholds (•), Octave noise (x). Head Vibrations Figure R4: Sound-induced head vibrations (HV). HV induced by sound ( ), HV induced by vibration ( ) and Total octave noise (x). Overall head vibrations induced by thres-hold level sound were above or equal to head vibrations induced by threshold level vibrations at all frequencies except at 500 Hz. Conclusion Pythons, and possibly all snakes, can hear, but with the loss of a functional outer and middle ear they lost effective pressure hearing. Instead snakes have maintained or developed vibration sensitivity as good as that found in any terrestrial vertebrate, enabling them to maintain insensitive sound detection via sound induced head vibrations. Acknowledgements: The study was funded by the Oticon Foundation (CBC), by the Danish Natural Science Research Council (JCD and PTM) and by the Carlsberg Foundation (JCD). We thank H. Lauridsen and M. Pedersen for skilled support and CT scannings. We also wish to thank K. Beedholm for helpful discussions and critique during experiments and B. Young and C. Carr for most helpful critique. References: 1 Christensen, C.B., Christensen-Dalsgaard, J., Brandt, C. and Madsen, P.T. (2012). Hearing with an atympanic ear: good vibration and poor sound pressure detection in the royal python, Python regius. Journal of Experimental Biology 215: 331-342. 2 Hartline, P. H. (1971). Physiological basis for detection of sound and vibration in snakes. Journal Experimental Biology 54: 349-371. 3 Wever, E. G. and Vernon, J. A. (1960). The problem of hearing in snakes. J. Aud. Res. 1: 77-83.
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