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The Malleable Middle Ear: An Underappreciated Player in the Evolution of Hearing in Vertebrates

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Insights from Comparative Hearing Research

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 49))

Abstract

The middle ear of tetrapods (limbed vertebrates) originated from nonauditory structures, and has been modified by adaptations arising from the lifestyle of the tetrapods. These accessory structures for the inner ear increased the sensitivity to airborne sound, the frequency range of hearing, and the directionality of the ear. The tympanic middle ear originated independently at least once in every major tetrapod group and a long time after the origin of the tetrapods.

The aim of the chapter is to give an outline of middle ear function and, a comparative overview of tetrapod middle ears and to describe how the middle ear has undergone diverse, major modifications (e.g., in aquatic, fossorial, or ultrasound-sensitive species). In some cases, these modifications even led to a reduction or complete loss of function of the middle ear, leading to decreased auditory sensitivity. These reductions were the result of unrelated, obviously more important, selection pressures.

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References

  • Alexander, R. (1966). Physical aspects of swimbladder function. Biological Review, 41, 141–176.

    CAS  Google Scholar 

  • Arch, V. S., Grafe, T. U., Gridi-Papp, M., & Narins, P. M. (2009). Pure ultrasonic communication in an endemic Bornean frog. Public Library of Science One 4, e5413 doi:10.1371 /journal.pone.0005413.

    Google Scholar 

  • Asher, R.J., Maree, S., Bronner, G., Bennett, N.C., Bloomer, P., Czechowski, P., Meyer, M., & Hofreiter, M. (2010). A phylogenetic estimate for golden moles (Mammalia, Afrotheria, Chrysochloridae). BMC Evolutionary Biology 10, 69.

    PubMed Central  PubMed  Google Scholar 

  • Boistel, R., Aubin, T., Cloetens, P., Langer, M., & Gillet, B. (2011). Whispering to the deaf: Communication by a frog without external vocal sac or tympanum in noisy environments. Public Library of Science One 6(7), e22080 doi:10.1371/journal.pone.0022080.

    CAS  PubMed  Google Scholar 

  • Brazeau, M. D., & Ahlberg, P. E. (2006). Tetrapod-like middle ear architecture in a Devonian fish. Nature 439, 318–321.

    CAS  PubMed  Google Scholar 

  • Chapman, S. C. (2011). Can you hear me now? Understanding vertebrate middle ear development. Frontiers in Biosciences, 16, 1675–1692.

    CAS  Google Scholar 

  • Christensen, C. B., Brandt, C., Christensen-Dalsgaard, J., & Madsen, P. T. (2012). Hearing with an atympanic ear: Good vibration and poor sound pressure detection in royal python (Python regius). Journal of Experimental Biology, 215, 331–342.

    PubMed  Google Scholar 

  • Christensen-Dalsgaard, J. (2005). Directional hearing in non-mammalian tetrapods. In A. N. Popper & R. R. Fay (Eds.), Sound source localization (pp. 67–123). New York: Springer-Verlag.

    Google Scholar 

  • Christensen-Dalsgaard, J. (2011). Vertebrate pressure-gradient receivers. Hearing Research, 273, 37–45.

    PubMed  Google Scholar 

  • Christensen-Dalsgaard, J., & Elepfandt, A. (1995). Biophysics of underwater hearing in the clawed frog, Xenopus laevis. Journal of Comparative Physiology A, 176, 317–324.

    CAS  Google Scholar 

  • Christensen-Dalsgaard, J., & Manley, G. A. (2005). Directionality of the lizard ear. Journal of Experimental Biology, 208, 1209–1217.

    PubMed  Google Scholar 

  • Christensen-Dalsgaard, J., & Carr, C. E. (2008). Evolution of a sensory novelty: The tympanic ears and the associated neural processing. Brain Research Bulletin, 75, 365–370.

    PubMed Central  PubMed  Google Scholar 

  • Christensen-Dalsgaard, J., & Manley, G. A. (2008). Acoustical coupling of lizard eardrums. Journal of the Association for Research in Otolaryngology, 9, 407–416.

    PubMed Central  PubMed  Google Scholar 

  • Christensen-Dalsgaard, J., & Carr, C. E. (2011). Directionality of gecko auditory nerve fibers with free-field stimulation. Association for Research in Otolaryngology, Abstract 463.

    Google Scholar 

  • Christensen-Dalsgaard, J., Brandt, C., Wilson, M., Wahlberg, M., & Madsen, P. T. (2011a). Hearing in the African lungfish, Protopterus Annectens: Preadaptations for pressure hearing in tetrapods? Biology Letters, 7, 139–141.

    PubMed Central  PubMed  Google Scholar 

  • Christensen-Dalsgaard, J., Tang, Y. Z., & Carr, C. E. (2011b). Binaural processing by the gecko auditory periphery. Journal of Neurophysiology, 105, 1992–2004.

    PubMed  Google Scholar 

  • Christensen-Dalsgaard, J., Brandt, C., Willis, K., Christensen, C. B., Ketten, D., Edds-Walton, P., Fay, R. R., Madsen, P. T., & Carr, C. E. (2012). Specialization for underwater hearing by the tympanic middle ear of the turtle, Trachemys scripta elegans. Proceedings of the Royal Society of London B: Biological Sciences, 279, 2816–2824.

    Google Scholar 

  • Clack, J. A. (1997). The evolution of tetrapod ears and the fossil record. Brain Behavior and Evolution, 50, 198–212.

    CAS  Google Scholar 

  • Clack, J. A., & Allin, E. (2004). The evolution of single-and multiple-ossicle ears in fishes and tetrapods. In G. A. Manley, A. N. Popper, & R. R. Fay (Eds.), Evolution of the vertebrate auditory system (pp. 128–163). New York: Springer Science+Business Media.

    Google Scholar 

  • Clack, J. A., Ahlberg, P. E., Finney, S. M., Dominquez-Alonso, P., Robinson, J., & Ketchem, R. A. (2003). A uniquely specialized ear in a very early tetrapod. Nature, 425, 65–69.

    CAS  PubMed  Google Scholar 

  • Coles, R. B., Gower, D. M., Boyd, P. J., & Lewis, D. B. (1982). Acoustic transmission through the head of the common mole, Talpa europaea. Journal of Experimental Biology, 101, 337–341.

    CAS  PubMed  Google Scholar 

  • Decraemer, W. F., & Funnell, W. R. J. (2008). Anatomical and mechanical properties of the tympanic membrane. In B. Ars (Ed.), Chronic otitis media: Pathogenesis-oriented therapeutic management (pp. 51–84). The Hague: Kugler.

    Google Scholar 

  • Feng, A. S., & Christensen-Dalsgaard, J. (2007). Interconnections between the ears in nonmammalian vertebrates. In A. Basbaum, M. Bushnell, D. Smith, G. Beauchamp, S. Firestein, P. Dallos, D. Oertel, R. Masland, T. Albright, J. Kaas, & E. Gardner (Eds.), The Senses: A comprehensive reference (Vol. 3, pp. 217–224). Amsterdam: Elsevier.

    Google Scholar 

  • Feng, A.S., Narins, P.M., Xu, C.H., Lin, W.Y., Yu, Z.L., Qiu, Q., Xu, Z.M., & Shen, J.X. (2006) Ultrasonic communication in frogs. Nature, 440, 333–336.

    Google Scholar 

  • Fleischer, G. (1978). Evolutionary principles of the mammalian middle ear. Advances in Anatomy, Embryology and Cell Biology, 55, 1–70.

    Google Scholar 

  • Friedel, P., Young, B. A., & van Hemmen, J. L. (2008). Auditory localization of ground-borne vibrations in snakes. Physical Review Letters, 100, 048704.

    Google Scholar 

  • Gridi-Papp, M., Feng, A. S., Shen, J.-X., Yu. Z.-L. & Narins, P. M. (2008). Active control of ultrasonic hearing in frogs, Proceedings of the National Academy of Sciencesof the USA, 105, 11013–11018.

    Google Scholar 

  • Gummer, A.W., Smolders, J.W.T., & Klinke, R. (1989). Mechanics of a single-ossicle ear: I. The extra-stapedius of the pigeon. Hearing Research, 39, 1–14.

    CAS  PubMed  Google Scholar 

  • Gyo, K., Aritomo, H., & Goode, R. L. (1987). Measurement of the ossicular vibration ratio in human temporal bones by use of a video measuring system. Acta Oto-Laryngologica, 103, 87–95.

    CAS  PubMed  Google Scholar 

  • Heffner, R. S., & Heffner, H. E. (1992). Evolution of sound localization in mammals. In D. B. Webster, R. R. Fay, & A. N. Popper (Eds.), The evolutionary biology of hearing (pp. 691–715). New York: Springer-Verlag.

    Google Scholar 

  • Helmholtz, H. v. (1868) Die Mechanik der Gehörknöchelchen und des Trommelfelles. Archiv für die gesamte Physiologie des Menschen und der Thiere. Band 1, Max Cohen & Sohn, Bonn 1868, p. 1–61

    Google Scholar 

  • Hemilä, S., Nummela, S., & Reuter, T. (1995). What middle ear parameters tell about impedance matching and high-frequency hearing. Hearing Research, 85, 31–44.

    PubMed  Google Scholar 

  • Hemilä, S., Nummela, S., & Reuter, T. (1999). A model of the odontocete middle ear. Hearing Research, 133, 82–97.

    PubMed  Google Scholar 

  • Heth, G., Frankenberg, E., Raz, A., & Nevo, E. (1987). Vibrational communication in subterranean mole rats (Spalax ehrenbergi). Behavioral Ecology and Sociobiology, 21, 31–33.

    Google Scholar 

  • Hetherington, T. E. (1987). Timing of development of the middle ear of Anura (Amphibia). Zoomorphology, 106, 289–300.

    Google Scholar 

  • Hetherington, T. E. (2008). Comparative anatomy and function of hearing in aquatic amphibians, reptiles, and birds. In J. G. M. Thewissen & S. Nummela (Eds.), Sensory evolution on the threshold (pp. 183–209). Berkeley: University of California Press.

    Google Scholar 

  • Hetherington, T. E., & Lindquist, E. D. (1999). Lung-based hearing in an “earless” anuran amphibian. Journal of Comparative Physiology A, 184, 395–401.

    Google Scholar 

  • Hori, Y., Kawase, T., Hasegawa, J., Sato, T., Yoshida, N., Oshima, T., Suetake, M., & Kobayashi, T. (2006). Audiometry with nasally presented masking noise: Novel diagnostic method for patulous Eustachian tube. Otology and Neurotology, 27, 596–599.

    PubMed  Google Scholar 

  • Jaslow, A. P., Hetherington, T. E., & Lombard, R. E. (1988). Structure and function of the amphibian middle ear. In B. Fritzsch, M. J. Ryan, W. Wilczynski, T. E. Hetherington, & W. Walkowiak (Eds.), The evolution of the amphibian auditory system (pp. 69–91). New York: John Wiley & Sons.

    Google Scholar 

  • Jensen, K. K., Christensen-Dalsgaard, J., Suthers, R., & Larsen, O. N. (2010). A newly discovered superoantero-orbital sinus connecting to the interaural canal may play a role in zebra finch hearing. In 9th International Congress of Neuroethology, Salamanca, poster 31, p. 409.

    Google Scholar 

  • Jørgensen, M. B., & Christensen-Dalsgaard, J. (1997a). Directionality of auditory nerve fiber responses to pure tone stimuli in the grassfrog, Rana temporaria. I. Spike rate responses. Journal of Comparative Physiology A, 180, 493–502.

    Google Scholar 

  • Jørgensen, M. B., & Christensen-Dalsgaard, J. (1997b). Directionality of auditory nerve fiber responses to pure tone stimuli in the grassfrog, Rana temporaria. II. Spike timing. Journal of Comparative Physiology A, 180, 503–511.

    Google Scholar 

  • Jørgensen, M. B., & Kanneworff, M. (1998). Middle ear transmission in the grass frog, Rana temporaria. Journal of Comparative Physiology A, 182, 59–64.

    Google Scholar 

  • Jørgensen, M. B., Schmitz, B., & Christensen-Dalsgaard, J. (1991). Biophysics of directional hearing in the frog Eleutherodactylus coqui. Journal of Comparative Physiology A, 168, 223–232.

    Google Scholar 

  • Kastak, D., & Schusterman, R. J. (1998). Low-frequency amphibious hearing in pinnipeds: Methods, measurements, noise, and ecology. Journal of the Acoustical Society of America, 103, 2216–2228.

    CAS  PubMed  Google Scholar 

  • Ketten, D. R. (2000) Cetacean Ears. In: Au, W. Fay, R.R. & Popper, A.N. (eds.), Hearing by Whales and Dolphins (pp. 43–108). New York: Springer-Verlag

    Google Scholar 

  • Knudsen, E. I. (2002). Instructed learning in the auditory localization pathway of the barn owl. Nature, 417, 322–328.

    CAS  PubMed  Google Scholar 

  • Konishi, M. (2000). Study of sound localization by owls and its relevance to humans. Comparative Biochemistry and Physiology A, 126, 459–469.

    CAS  Google Scholar 

  • Köppl, C. (1997). Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. Journal of Neuroscience, 17, 3312–3321.

    PubMed  Google Scholar 

  • Köppl, C. (2009). Evolution of sound localization in land vertebrates. Current Biology, 19, R635–R639.

    PubMed  Google Scholar 

  • Kuypers, L. C., Dirckx, J. J. J., Decraemer, W. F., & Timmermans, J.-P. (2005). Thickness of the gerbil tympanic membrane measured with confocal microscopy. Hearing Research, 205, 42–52.

    Google Scholar 

  • Lewis, E. R., & Narins, P. M. (1999). The acoustic periphery of amphibians: Anatomy and physiology. In R. R. Fay & A. N. Popper (Eds.), Comparative hearing: Fish and amphibians (pp. 218–268). New York: Springer-Verlag.

    Google Scholar 

  • Lindquist, E. D., Hetherington, T. E., & Volman, S. (1998). Biomechanical and neurophysiological studies on audition in eared and earless harlequin frogs (Atelopus). Journal of Comparative Physiology A, 183, 265–271.

    CAS  Google Scholar 

  • Luo, Z.-X. (2007). Transformation and diversification in early mammal evolution. Nature, 450, 1011–1019.

    CAS  PubMed  Google Scholar 

  • Luo, Z.-X., Crompton, A. W., & Sun, A.-L. (2001). A new mammaliaform from the Early Jurassic and evolution of mammalian characteristics. Science, 292, 1535–1540.

    CAS  PubMed  Google Scholar 

  • Manley, G. A. (1972a). Frequency response of the ear of the tokay gecko. Journal of Experimental Biology, 181, 159–168.

    CAS  Google Scholar 

  • Manley, G. A. (1972b). Frequency response of the middle ear of geckos. Journal of Comparative Physiology, 81, 251–258.

    Google Scholar 

  • Manley, G. A. (1973). A review of some current concepts of the functional evolution of the ear in terrestrial vertebrates. Evolution, 26, 608–621.

    Google Scholar 

  • Manley, G. A. (1976). Auditory responses from the medulla of the monitor lizard Varanus bengalensis. Brain Research, 102, 329–334.

    Google Scholar 

  • Manley, G. A. (1990). Peripheral hearing mechanisms in reptiles and birds. New York: Springer-Verlag.

    Google Scholar 

  • Manley, G. A. (2010). An evolutionary perspective on middle ears. Hearing Research, 263, 3–8.

    PubMed  Google Scholar 

  • Manley, G. A. (2012). Evolutionary paths to mammalian cochleae. Journal of the Association for Research in Otolaryngology, 13, 733–743.

    PubMed Central  PubMed  Google Scholar 

  • Manley, G. A., & Johnstone, B. M. (1974). Middle-ear function in the guinea pig. Journal of the Acoustical Society of America, 56, 571–576.

    CAS  PubMed  Google Scholar 

  • Manley, G. A., & Köppl, C. (1998). Phylogenetic development of the cochlea and its innervation. Current Opinion in Neurobiology, 8, 468–474.

    CAS  PubMed  Google Scholar 

  • Manley, G. A., & Clack, J. A. (2004). An outline of the evolution of vertebrate hearing organs. In G. A. Manley, A. N. Popper, & R. R. Fay (Eds.), Evolution of the vertebrate auditory system (pp. 1–26). New York: Springer Science+Business Media..

    Google Scholar 

  • Manley, G. A., & Kraus, J. E. (2010). Exceptional high-frequency hearing and matched vocalizations in Australian pygopod geckos. Journal of Experimental Biology, 213, 1876–1885.

    PubMed  Google Scholar 

  • Manley, G. A., & Sienknecht, U. J. (2013). The evolution and development of middle ears in land vertebrates. In S. Puria, A. N. Popper, & R. R. Fay (Eds.), The middle ear: Science, otosurgery and technology (pp. 7–30). New York: Springer Science+Business Media.

    Google Scholar 

  • Manley, G. A., Irvine, D. R. F., & Johnstone, B. M. (1972). Frequency response of the bat tympanic membrane. Nature, 237, 112–113.

    Google Scholar 

  • Martin, K. J., Alessi, S. C., Gaspard, J. C., Tucker, A. D., Bauer, G. B., & Mann, D. A. (2012). Underwater hearing in the loggerhead turtle (Caretta caretta): A comparison of behavioral and auditory evoked potential audiograms. Journal of Experimental Biology, 215, 3001–3009.

    PubMed  Google Scholar 

  • Mason, M. J. (2001). Middle ear structures in fossorial mammals: A comparison with non-fossorial species. Journal of Zoology, 255, 467–486.

    Google Scholar 

  • Mason, M. J. (2003). Bone conduction and seismic sensitivity in golden moles (Chrysochloridae). Journal of Zoology, 260, 405–413.

    Google Scholar 

  • Mason, M. J. (2004). The middle ear apparatus of the tuco-tuco Ctenomys sociabilis (Rodentia: Ctenomyidae). Journal of Mammalogy, 85, 797–805.

    Google Scholar 

  • Mason, M. J. (2007). Pathways for sound transmission to the inner ear in amphibians. In P. M. Narins, A. S. Feng, R. R. Fay, & A. N. Popper (Eds.), Hearing and sound communication in amphibians (pp. 147–183). New York: Springer Science+Business Media.

    Google Scholar 

  • Mason, M. J., & Narins, P. M. (2002a). Seismic sensitivity in the desert golden mole (Eremitalpa granti): A review. Journal of Comparative Psychology, 116, 158–163.

    PubMed  Google Scholar 

  • Mason, M. J., & Narins, P. M. (2002b). Vibrometric studies of the middle ear of the bullfrog Rana catesbeiana. II. The operculum. Journal of Experimental Biology, 205, 3167–3176.

    PubMed  Google Scholar 

  • Mertens, R. (1971). Die Rückbildung des Tympanum bei Reptilien und ihre Beziehung zur Lebensweise. Senckenbergiana Biologica, 52, 177–191.

    Google Scholar 

  • Michelsen, A., & Larsen, O. N. (2008). Pressure difference receiving ears. Bioinspiration and Biomimetics, 3, 1–18.

    Google Scholar 

  • Møller, A. R. (1965). An experimental study of the acoustic impedance of the middle ear and its transmission properties. Acta Oto-Laryngologica, 60, 129–148.

    PubMed  Google Scholar 

  • Novacek, M. J. (1977). Aspects of the problem of variation, origin and evolution of the eutherian auditory bulla. Mammal Review, 7, 131–149.

    Google Scholar 

  • Nummela, S. (1995). Scaling of the mammalian middle ear. Hearing Research, 85, 18–30.

    CAS  PubMed  Google Scholar 

  • Nummela, S. (2008). Hearing in aquatic mammals. In J. G. M. Thewissen & S. Nummela (Eds.), Sensory evolution on the threshold (pp. 211–224). Berkeley: University of California Press.

    Google Scholar 

  • Olsson, L., & Hanken, J. (1996). Cranial neural-crest migration and chondrogenic fate in the Oriental fire-bellied toad Bombina orientalis: Defining the ancestral pattern of head development in anuran amphibians. Journal of Morphology, 229, 105–120.

    Google Scholar 

  • O’Shea, T. J., & Poché, L. B., Jr. (2006). Aspects of underwater sound communication in Florida manatees (Trichechus manatus latirostris). Journal of Mammalogy, 87, 1061–1071.

    Google Scholar 

  • Patterson, W. C. (1966). Hearing in the turtle. Journal of Auditory Research, 6, 453–464.

    Google Scholar 

  • Pickles, J. O. (2008). An introduction to the physiology of hearing (p. 19). Bingley, UK: Emerald Press.

    Google Scholar 

  • Pinder, A. C., & Palmer, A. R. (1983). Mechanical properties of the frog ear: Vibration measurements under free- and closed-field acoustic conditions. Proceedings of the Royal Society of London B: Biological Sciences, 219, 371–396.

    CAS  PubMed  Google Scholar 

  • Popper, A. N., & Fay, R. R. (2011). Rethinking sound detection by fishes. Hearing Research, 273, 25–36.

    PubMed  Google Scholar 

  • Puria, S., & Steele, C. (2010). Tympanic-membrane and malleus–incus-complex co-adaptations for high-frequency hearing in mammals. Hearing Research, 263, 183–190.

    PubMed  Google Scholar 

  • Ridgway, S., Wever, E., McCormick, J., Palin, J., & Anderson, J. (1969). Hearing in the giant sea turtle, Chelonia mydas. Proceedings of the National Academy of Sciences of the USA 64, 884–890.

    CAS  PubMed  Google Scholar 

  • Rosowski, J. (1994). Outer and middle ears. In R. R. Fay & A. N. Popper (Eds.), Comparative hearing: Mammals (pp. 172–247). New York: Springer-Verlag.

    Google Scholar 

  • Rosowski, J. J. (1996). Models of external- and middle-ear function. In H. L. Hawkins, T. A. McMullen, A. N. Popper, & R. R. Fay (Eds.), Auditory computation (pp. 15–61). New York: Springer-Verlag.

    Google Scholar 

  • Rosowski, J. J., Peake, W. T., Lynch, T.J., III, Leong, R., & Weiss, T. F. (1985). A model for signal transmission in an ear having hair cells with free-standing stereocilia. II. Macromechanical stage. Hearing Research, 20, 139–155.

    CAS  PubMed  Google Scholar 

  • Ruggero, M.A., & Temchin, A. (2002). The roles of the external, middle, and inner ears in determining the bandwidth of hearing. Proceedings of the National Academy of Sciences of the USA, 99, 13206–13210.

    CAS  PubMed  Google Scholar 

  • Sanes, D. H., Reh, T. A., & Harris, W. A. (2005). Development of the nervous system (2nd ed.). Burlington: Academic Press.

    Google Scholar 

  • Saunders, J., Duncan, R. K., Doan, D. E., & Werner, Y. L. (2000). The middle ear of reptiles and birds. In R. J. Dooling, R. R. Fay, & A. N. Popper (Eds.), Comparative hearing: Birds and reptiles (pp. 13–69). New York: Springer-Verlag.

    Google Scholar 

  • Segall, W. (1970). Morphological parallelisms of the bulla and auditory ossicles in some insectivores and marsupials. Fieldiana Zoology, 51, 169–205.

    Google Scholar 

  • Shaikh, D., Hallam, J., Christensen-Dalsgaard, J., & Zhang, L. (2009). A Braitenberg lizard: Continuous phonotaxis with a lizard ear model. In Lecture Notes in Computer Science (5602, pp. 439–448)., New York: Springer Science+Business Media.

    Google Scholar 

  • Sienknecht, U. J. (2013). Developmental origin and fate of middle ear structures. Hearing Research, 301, 19–26.

    Google Scholar 

  • Szpir, M. R., Sento, S., & Ryugo, D. K. (1990). Central projections of cochlear nerve fibers in the alligator lizard. Journal of Comparative Neurology, 295, 530–547.

    CAS  PubMed  Google Scholar 

  • Takechi, M., & Kuratani, S. (2010). History of studies on mammalian middle ear evolution: A comparative morphological and developmental perspective. Journal of Experimental Zoology (Molecular and Developmental Evolution), 314B, 417–433.

    Google Scholar 

  • Tonndorf, J. (1972). Bone conduction. In J. V. Tobias (Ed.), Foundations of modern auditory theory, (Vol. 2, pp. 195–237). New York: Academic Press.

    Google Scholar 

  • Tonndorf, J., & Khanna, S. M. (1970). The role of the tympanic membrane in middle ear transmission. Annals of Otology Rhinology and Laryngology, 79, 743–754.

    CAS  Google Scholar 

  • Tonndorf, J., & Khanna, S. M. (1972). Tympanic-membrane vibrations in human cadaver ears studied by time-averaged holography. Journal of the Acoustical Society of America, 52, 1221–1233.

    CAS  PubMed  Google Scholar 

  • Tubelli, A. A., Zosuls, A., Ketten, D. R., Yamato, M., & Mountain, D. C. (2012). A prediction of the minke whale (Balaenoptera acutorostrata) middle-ear transfer function. Journal of the Acoustical Society of America, 132, 3263–3272.

    PubMed  Google Scholar 

  • van Bergeijk, W. A. (1966). Evolution of the sense of hearing in vertebrates. American Zoologist, 6, 371–377.

    PubMed  Google Scholar 

  • Vorobyeva, E., & Smirnov, S. (1987). Characteristic features in the formation of anuran sound-conducting systems. Journal of Morphology, 192, 1–11.

    Google Scholar 

  • Vossen, C., Christensen-Dalsgaard, J., & van Hemmen, J. L. (2010). Analytical model of internally coupled ears. Journal of the Acoustical Society of America, 128, 909–918.

    PubMed  Google Scholar 

  • Walkowiak, W. (1980). The coding of auditory signals in the torus semicircularis of the fire-bellied toad and the grass frog: Responses to simple stimuli and to conspecific calls. Journal of Comparative Physiology, 138, 131–148.

    Google Scholar 

  • Werner, Y. L. (2003). Mechanical leverage in the middle ear of the American bullfrog, Rana catesbeiana. Hearing Research, 175, 54–65.

    PubMed  Google Scholar 

  • Werner, Y. L., & Igic, P. G. (2002). The middle ear of gekkonoid lizards: Interspecific variation of structure in relation to body size and to auditory sensitivity. Hearing Research, 167, 33–45.

    PubMed  Google Scholar 

  • Wever, E. G. (1978). The reptile ear. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Wever, E. G. (1985). The amphibian ear. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Wever, E. G., & Gans, C. (1973). The ear in Amphisbaenia (Reptilia); further anatomical observations. Journal of Zoology, 171, 189–206.

    Google Scholar 

  • Willis, K.L., Christensen-Dalsgaard, J., Ketten, D. R., & Carr, C. E. (2013). Middle ear cavity morphology is consistent with an aquatic origin for testudines. Public Library of Science ONE 8, e54086. doi:10.1371/journal.pone.0054086.

    CAS  PubMed  Google Scholar 

  • Wood, J. L., Hughes, A. J., Mercer, K. J., & Chapman, S. C. (2010). Analysis of chick (Gallus gallus) middle ear columella formation. BMC Developmental Biology, 10, 16.

    PubMed Central  PubMed  Google Scholar 

  • Yamato, M., Ketten, D. R., Arruda, J., Craemer, S., & Moore, K. (2012). The auditory anatomy of the minke whale (Balaenoptera acutorostrata): A potential fatty sound reception pathway in a baleen whale. The Anatomical Record, 295, 991–998.

    PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank John Rosowski for comments on an earlier version of this chapter.

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Correspondence to Jakob Christensen-Dalsgaard .

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Christensen-Dalsgaard, J., Manley, G.A. (2013). The Malleable Middle Ear: An Underappreciated Player in the Evolution of Hearing in Vertebrates. In: Köppl, C., Manley, G., Popper, A., Fay, R. (eds) Insights from Comparative Hearing Research. Springer Handbook of Auditory Research, vol 49. Springer, New York, NY. https://doi.org/10.1007/2506_2013_33

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