Advertisement

Journal of Comparative Physiology A

, Volume 196, Issue 3, pp 165–179 | Cite as

Anatomy and physics of the exceptional sensitivity of dolphin hearing (Odontoceti: Cetacea)

  • Simo Hemilä
  • Sirpa NummelaEmail author
  • Tom Reuter
Review

Abstract

During the past 50 years, the high acoustic sensitivity and the echolocation behavior of dolphins and other small odontocetes have been studied thoroughly. However, understanding has been scarce as to how the dolphin cochlea is stimulated by high frequency echoes, and likewise regarding the ear mechanics affecting dolphin audiograms. The characteristic impedance of mammalian soft tissues is similar to that of water, and thus no radical refractions of sound, nor reflections of sound, can be expected at the water/soft tissue interfaces. Consequently, a sound-collecting terrestrial pinna and an outer ear canal serve little purpose in underwater hearing. Additionally, compared to terrestrial mammals whose middle ear performs an impedance match from air to the cochlea, the impedance match performed by the odontocete middle ear needs to be reversed to perform an opposite match from water to the cochlea. In this paper, we discuss anatomical adaptations of dolphins: a lower jaw collecting sound, thus replacing the terrestrial outer ear pinna, and a thin and large tympanic bone plate replacing the tympanic membrane of terrestrial mammals. The paper describes the lower jaw anatomy and hypothetical middle ear mechanisms explaining both the high sensitivity and the converted acoustic impedance match.

Keywords

Aquatic mammal Acoustic impedance Lower jaw Middle ear model Tympanic bone 

Notes

Acknowledgments

We thank the associate editor Dr. Peter Narins, and two anonymous reviewers for their constructive criticism and helpful suggestions for improving earlier versions of this manuscript. This work was supported by the Academy of Finland (SN), and the Finnish Society of Sciences and Letters (TR).

References

  1. Aibara R, Welsh JT, Puria S, Goode RL (2001) Human middle-ear sound transfer function and cochlear input impedance. Hear Res 152:100–109CrossRefPubMedGoogle Scholar
  2. Aroyan JL (2001) Three-dimensional modelling of hearing in Delphinus delphis. J Acoust Soc Am 110:3305–3318CrossRefPubMedGoogle Scholar
  3. Au WWL, Moore PWB (1984) Receiving beam patterns and directivity indices of the Atlantic bottlenose dolphin Tursiops truncatus. J Acoust Soc Am 75:255–262CrossRefPubMedGoogle Scholar
  4. Bárány E (1938) A contribution to the physiology of bone conduction. Acta Otolaryngol Suppl (Stockholm) 26:1–223Google Scholar
  5. Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, SunderlandGoogle Scholar
  6. Brill RL, Moore PWB, Helweg DA, Dankiewicz LA (2001) Investigating the dolphin’s peripheral hearing system: acoustic sensitivity about the head and lower jaw. Technical report no. 1865, SPAWAR Systems Center, San Diego, CAGoogle Scholar
  7. Bullock TH, Grinnell AD, Ikezono E, Kameda K, Katsuki Y, Nomoto M, Sato O, Suga N, Yanagisawa K (1968) Electrophysiological studies of central auditory mechanisms in cetaceans. Z Vgl Physiol 59:117–156Google Scholar
  8. Cranford TW (2000) In search of impulse sound sources in odontocetes. In: Au WWL, Popper AN, Fay RR (eds) Hearing by whales and dolphins. Springer, New York, pp 109–155Google Scholar
  9. Cranford TW, Krysl P, Hildebrand JA (2008) Acoustic pathways revealed: simulated sound transmission and reception in Cuvier’s beaked whale (Ziphius cavirostris). Bioinspir Biomim 3:1–10CrossRefGoogle Scholar
  10. Decraemer WF, de La Rochefoucauld O, Dong W, Khanna SM, Dirckx JJJ, Olson ES (2007) Scala vestibule pressure and three-dimensional stapes velocity measured in direct succession in gerbil. J Acoust Soc Am 121:2774–2791CrossRefPubMedGoogle Scholar
  11. Dible SA, Flint JA, Lepper PA (2006) Laser Doppler vibrometry measurement of the lower jaw and teeth of the Atlantic bottlenose dolphin (Tursiops truncatus). In: Proceedings of the 8th European conference on underwater acoustics, Carvoeiro, Portugal, June 2006, pp 12–15Google Scholar
  12. Dible SA, Flint JA, Lepper PA (2009) On the role of periodic structures in the lower jaw of the Atlantic bottlenose dolphin (Tursiops truncatus). Bioinspir Biomim 4:1–9CrossRefGoogle Scholar
  13. Dobbins P (2007) Dolphin sonar—modelling a new receiver concept. Bioinspir Biomim 2:19–29CrossRefPubMedGoogle Scholar
  14. Evans EF (1982a) Functional anatomy of the auditory system. In: Barlow HB, Mollon JD (eds) The senses. Cambridge University Press, London, pp 251–306Google Scholar
  15. Evans EF (1982b) Basic physics and psychophysics of sound. In: Barlow HB, Mollon JD (eds) The senses. Cambridge University Press, London, pp 239–250Google Scholar
  16. Fay RR (1988) Hearing in vertebrates: a psychophysics databook. Hill-Fay Associates, WinnetkaGoogle Scholar
  17. Fleischer G (1978) Evolutionary principles of the mammalian middle ear. Adv Anat Embryol Cell Biol 55:1–70Google Scholar
  18. Flock Å (1971) Sensory transduction in hair cells. In: Loevenstein WR (ed) Handbook of sensory physiology, vol 1. Springer, Berlin, pp 396–441Google Scholar
  19. Fraser FC, Purves PE (1954) Hearing in cetaceans. Bull Br Mus (Nat Hist) Zool 2:103–116Google Scholar
  20. Fraser FC, Purves PE (1960) Anatomy and function of the cetacean ear. Proc R Soc Lond B 152:62–77CrossRefPubMedGoogle Scholar
  21. Gingerich PD, ul-Haq M, Zalmont IS, Khan IH, Malkani MS (2001) Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan. Science 293:2239–2242CrossRefPubMedGoogle Scholar
  22. Goodson AD, Klinowska M (1990) A proposed echolocation receptor for the bottlenose dolphin (Tursiops truncatus): modelling the receive directivity from tooth and lower jaw geometry. In: Thomas JA, Kastelein RA (eds) Sensory abilities of cetaceans. Plenum Press, New York, pp 255–267Google Scholar
  23. Heffner HE, Masterton B (1980) Hearing in Glires: domestic rabbit, cotton rat, house mouse, and kangaroo rat. J Acoust Soc Am 68:1584–1599CrossRefGoogle Scholar
  24. Hemilä S, Nummela S, Reuter T (1995) What middle ear parameters tell about impedance matching and high frequency hearing. Hear Res 85:31–44CrossRefPubMedGoogle Scholar
  25. Hemilä S, Nummela S, Reuter T (1999) A model of the odontocete middle ear. Hear Res 133:82–97CrossRefPubMedGoogle Scholar
  26. Hemilä S, Nummela S, Reuter T (2001) Modelling whale audiograms: effects of bone mass on high-frequency hearing. Hear Res 151:221–226CrossRefPubMedGoogle Scholar
  27. Hemilä S, Nummela S, Berta A, Reuter T (2006) High-frequency hearing in phocid and otariid pinnipeds: an interpretation based on inertial and cochlear constraints. J Acoust Soc Am 120:3463–3466CrossRefPubMedGoogle Scholar
  28. Henson OW Jr (1974) Comparative anatomy of the middle ear. In: Keidel WD, Neff WD (eds) Handbook of sensory physiology. Auditory system, vol V/1. Springer, Berlin, pp 39–110Google Scholar
  29. Houser DS, Finneran J, Carder D, van Bonn W, Smith C, Hoh C, Mattrey R, Ridgway S (2004) Structural and functional imaging of bottlenose dolphin (Tursiops truncatus) cranial anatomy. J Exp Biol 207:3657–3665CrossRefPubMedGoogle Scholar
  30. Hudspeth AJ (1989) How the ear’s works work. Nature 341:397–404CrossRefPubMedGoogle Scholar
  31. Hyrtl J (1845) Vergleichend-anatomische Untersuchungen über das innere Gehörorgan des Menschen und der Säugethiere. Verlag von Friedrich Ehrlich, PragueGoogle Scholar
  32. Jacobs DW, Hall JD (1972) Auditory thresholds of a fresh water dolphin, Inia geoffrensis Blainville. J Acoust Soc Am 51:530–533CrossRefGoogle Scholar
  33. Johnson CS (1967) Sound detection thresholds in marine mammals. In: Tavolga WN (ed) Marine bio-acoustics II. Pergamon Press, Oxford, pp 247–260Google Scholar
  34. Kastelein RA, Bunskoek P, Hagedoorn M, Au WWL, de Haan D (2002) Audiogram of a harbor porpoise (Phocoena phocoena) measured with narrow-band frequency-modulated signals. J Acoust Soc Am 112:334–344CrossRefPubMedGoogle Scholar
  35. Kastelein RA, Bunskoek P, Hagedoorn M, Au WWL, de Haan D (2003) Audiogram of a striped dolphin (Stenella coeruleoalba). J Acoust Soc Am 113:1130–1137CrossRefPubMedGoogle Scholar
  36. Kellogg R (1938) Adaptation of structure to function in whales. Publ Carnegie Inst Wash 501:649–682Google Scholar
  37. Kellogg WN (1958) Echo ranging in the porpoise. Science 128:982–988CrossRefPubMedGoogle Scholar
  38. Ketten DR (1992) The marine mammal ear: specializations for aquatic audition and echolocation. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 717–754Google Scholar
  39. Ketten DR (2000) Cetacean ears. In: Au WWL, Popper AN, Fay RR (eds) Hearing by whales and dolphins. Springer, New York, pp 43–108Google Scholar
  40. Khanna SM, Tonndorf J (1972) Tympanic membrane vibrations in cats studied by time-averaged holography. J Acoust Soc Am 51:1904–1920CrossRefPubMedGoogle Scholar
  41. Koopman HN, Zahorodny ZP (2008) Life history constrains biochemical development in the highly specialized odontocete echolocation system. Proc R Soc Lond 275:2327–2334CrossRefGoogle Scholar
  42. Lillie DG (1910) Observations on the anatomy and general biology of some members of the larger Cetacea. Proc Zool Soc Lond 1910:769–792Google Scholar
  43. Ljungblad DK, Scoggins PD, Gilmartin WG (1982) Auditory thresholds of a captive Eastern Pacific bottle-nosed dolphin, Tursiops spp. J Acoust Soc Am 72:1726–1929CrossRefPubMedGoogle Scholar
  44. Luo ZX (1998) Homology and transformation of cetacean ectotympanic structures. In: Thewissen JGM (ed) The emergence of whales: evolutionary patterns in the origin of Cetacea. Plenum Press, New York, pp 269–301Google Scholar
  45. Lynch TJ III, Nedzelnitsky V, Peake WT (1982) Input impedance of the cochlea in cat. J Acoust Soc Am 72:108–130CrossRefPubMedGoogle Scholar
  46. McCormick JG, Wever EG, Palin J, Ridgway SH (1970) Sound conduction in the dolphin ear. J Acoust Soc Am 48:1418–1428CrossRefPubMedGoogle Scholar
  47. Møhl B, Au WWL, Pawloski J, Nachtigall PE (1999) Dolphin hearing: relative sensitivity as a function of point of application of a contact sound source in the jaw and head region. J Acoust Soc Am 105:3421–3424CrossRefPubMedGoogle Scholar
  48. Møhl B, Wahlberg M, Madsen PT, Heerfordt A, Lund A (2003) The monopulsed nature of sperm whale clicks. J Acoust Soc Am 114:1143–1154CrossRefPubMedGoogle Scholar
  49. Møller AR (1974) Function of the middle ear. In: Keidel WD, Neff WD (eds) Handbook of sensory physiology. Auditory system, vol V/1. Springer, Berlin, pp 491–517Google Scholar
  50. Mooney TA, Nachtigall PE, Castellote M, Taylor KA, Pacini AF, Esteban J-A (2008) Hearing pathways and directional sensitivity of the beluga whale, Delphinapterus leucas. J Exp Mar Biol Ecol 362:108–116CrossRefGoogle Scholar
  51. Morell M, DeGollada E, van der Schaar M, Alonso JM, Delory E, López A, Dewez A, André M (2007) Comparative morphometry of odontocete ears through computerized tomography. J Mar Biol Assoc UK 87:69–76CrossRefGoogle Scholar
  52. Nachtigall PE, Supin AY (2008) A false killer whale adjusts its hearing when it echolocates. J Exp Biol 211:1714–1718CrossRefPubMedGoogle Scholar
  53. Nachtigall PE, Lemonds DW, Roitblat HL (2000) Psychoacoustic studies of dolphin and whale hearing. In: Au WWL, Popper AN, Fay RR (eds) Hearing by whales and dolphins. Springer, New York, pp 330–363Google Scholar
  54. Neff WD, Hind JE (1955) Auditory thresholds of the cat. J Acoust Soc Am 27:480–483CrossRefGoogle Scholar
  55. Norris KS (1964) Some problems of echolocation in cetaceans. In: Tavolga WN (ed) Marine bio-acoustics. Pergamon Press, New York, pp 317–336Google Scholar
  56. Norris KS (1968) The evolution of acoustic mechanisms in odontocete cetaceans. In: Drake ET (ed) Evolution and environment. Yale University Press, New Haven, pp 297–324Google Scholar
  57. Norris KS (1980) Peripheral sound processing in odontocetes. In: Busnel RG, Fish JR (eds) Animal sonar systems. Plenum Press, New York, pp 495–509Google Scholar
  58. Nummela S (1995) Scaling of the mammalian middle ear. Hear Res 85:18–30CrossRefPubMedGoogle Scholar
  59. Nummela S (1997) Scaling and modeling the mammalian middle ear. Comments Theor Biol 4:387–412Google Scholar
  60. Nummela S (2008) Hearing in aquatic mammals. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, San Diego, pp 211–224Google Scholar
  61. Nummela S (2009) Hearing. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals, 2nd edn. Academic Press, San DiegoGoogle Scholar
  62. Nummela S, Reuter T, Hemilä S, Holmberg P, Paukku P (1999a) The anatomy of the killer whale middle ear (Orcinus orca). Hear Res 133:61–70CrossRefPubMedGoogle Scholar
  63. Nummela S, Wägar T, Hemilä S, Reuter T (1999b) Scaling of the cetacean middle ear. Hear Res 133:71–81CrossRefPubMedGoogle Scholar
  64. Nummela S, Thewissen JGM, Bajpai S, Hussain ST, Kumar K (2004a) Eocene evolution of whale hearing. Nature 430:776–778CrossRefPubMedGoogle Scholar
  65. Nummela S, Kosove JE, Lancaster TE, Thewissen JGM (2004b) Lateral mandibular wall thickness in Tursiops truncatus: variation due to sex and age. Mar Mamm Sci 20:491–497CrossRefGoogle Scholar
  66. Nummela S, Thewissen JGM, Bajpai S, Hussain ST, Kumar K (2007) Sound transmission in archaic and modern whales: anatomical adaptations for underwater hearing. Anat Rec 290A:716–733CrossRefGoogle Scholar
  67. Oliver D (2008) Prestin. In: Dallos P, Oertel D (eds) The senses: a comprehensive reference. Audition, vol 3. Elsevier, Amsterdam, pp 309–317Google Scholar
  68. Peake WT, Rosowski JJ, Lynch TJ III (1992) Middle-ear transmission: acoustic versus ossicular coupling in cat and human. Hear Res 57:245–268CrossRefPubMedGoogle Scholar
  69. Phillips DP, Calford MB, Pettigrew JD, Aitkin LM, Semple MN (1982) Directionality of sound pressure transformation at the cat’s pinna. Hear Res 8:13–28CrossRefPubMedGoogle Scholar
  70. Rauschmann MA, Huggenberger S, Kossatz LS, Oelschläger HA (2006) Head morphology in perinatal dolphins: a window into phylogeny and ontogeny. J Morphol 267:1295–1315CrossRefPubMedGoogle Scholar
  71. Reysenbach de Haan FW (1957) Hearing in whales. Acta Otolaryngol Suppl 134:1–114PubMedGoogle Scholar
  72. Ridgway SH (2000) The auditory central nervous system of dolphins. In: Au WWL, Popper AN, Fay RR (eds) Hearing by whales and dolphins. Springer, New York, pp 273–293Google Scholar
  73. Ridgway SH, Carder DA, Kamolnick T, Smith RR, Schlundt CE, Elsberry WR (2001) Hearing and whistling in the deep sea: depth influences whistle spectra but does not attenuate hearing by white whales (Delphinapterus leucas) (Odontoceti, Cetacea). J Exp Biol 204:3829–3841PubMedGoogle Scholar
  74. Rosowski JJ (1992) Hearing in transitional mammals: predictions from the middle-ear anatomy and hearing capabilities of extant mammals. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 615–631Google Scholar
  75. Rosowski JJ (1994) Outer and middle ears. In: Fay RR, Popper AN (eds) Comparative hearing: mammals. Springer, New York, pp 172–247Google Scholar
  76. Rosowski JJ, Graybeal A (1991) What did Morganucodon hear? Zool J Linn Soc 101:131–168CrossRefGoogle Scholar
  77. Rosowski JJ, Carney LH, Lynch TJ III, Peake WT (1986) The effectiveness of the external and middle ears in coupling acoustic power into the cochlea. In: Allen JB, Hall JL, Hubbard A, Neely ST, Tubis A (eds) Peripheral auditory mechanisms. Springer, New York, pp 3–12Google Scholar
  78. Ruggero MA, Temchin AN (2002) The roles of external, middle, and inner ears in determining the bandwidth of hearing. Proc Natl Acad Sci USA 99:13206–13210CrossRefPubMedGoogle Scholar
  79. Ruggero MA, Rich NC, Robles L, Shivapuja BG (1990) Middle-ear response in the chinchilla and its relationship to mechanics at the case of the cochlea. J Acoust Soc Am 87:1612–1629CrossRefPubMedGoogle Scholar
  80. Russell IJ (2008) Cochlear receptor potentials. In: Dallos P, Oertel D (eds) The senses: a comprehensive reference. Audition, vol 3. Elsevier, Amsterdam, pp 319–358Google Scholar
  81. Sassu R, Cozzi B (2007) The external and middle ear of the striped dolphin Stenella coerulealba (Meyen 1833). Anat Histol Embryol 36:197–201CrossRefPubMedGoogle Scholar
  82. Schuknecht HF (1993) Pathology of the ear, 2nd edn. Lea & Febiger, PhiladelphiaGoogle Scholar
  83. Starck D (1979) Vergleichende Anatomie der Wirbeltiere: auf evolutionsbiologischer Grundlage. Das Skeletsystem, vol 2. Springer, BerlinGoogle Scholar
  84. Stenfelt S, Hato N, Goode RL (2002) Factors contributing to bone conduction: the middle ear. J Acoust Soc Am 111:947–959CrossRefPubMedGoogle Scholar
  85. Supin AY, Popov VV, Mass AM (2001) The sensory physiology of aquatic mammals. Kluwer, BostonGoogle Scholar
  86. Szymanski MD, Bain DE, Kiehl K, Pennington S, Wong S, Henty KR (1999) Killer whale (Orcinus orca) hearing: auditory brainstem response and behavioral audiograms. J Acoust Soc Am 106:1134–1141CrossRefPubMedGoogle Scholar
  87. Thewissen JGM, Hussain ST (1993) Origin of underwater hearing in whales. Nature 361:444–445CrossRefPubMedGoogle Scholar
  88. Thewissen JGM, Williams EM, Roe LJ, Hussain ST (2001) Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 413:277–281CrossRefPubMedGoogle Scholar
  89. Thomas J, Chun N, Au W, Pugh K (1988) Underwater audiogram of a false killer whale (Pseudorca crassidens). J Acoust Soc Am 84:936–940CrossRefPubMedGoogle Scholar
  90. Thomas JA, Moss CF, Vater M (eds) (2004) Echolocation in bats and dolphins. The University of Chicago Press, ChicagoGoogle Scholar
  91. Urick RJ (1975) Principles of underwater sound. McGraw-Hill, New YorkGoogle Scholar
  92. Wartzok D, Ketten DR (1999) Marine mammal sensory systems. In: Reynolds JE III, Rommel SA (eds) Biology of marine mammals. Smithsonian Institution Press, Washington, DC, pp 117–175Google Scholar
  93. Wever EG, McCormick JG, Palin J, Ridgway SH (1971) Cochlea of the dolphin, Tursiops truncatus: the basilar membrane. Proc Natl Acad Sci USA 68:2708–2711CrossRefPubMedGoogle Scholar
  94. White MJ Jr, Norris J, Ljungblad D, Baron K, di Sciara G (1978) Auditory thresholds in two beluga whales (Delphinapterus leucas). HSWRI Technical Report No 78-109. Hubbs Marine Research Institute, San Diego, CAGoogle Scholar
  95. Zwislocki JJ (1975) The role of the external and middle ear in sound transmission. In: Tower DB (ed) The nervous system. Human communication and its disorders, vol 3. Raven Press, New York, pp 45–55Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of BiosciencesUniversity of HelsinkiHelsinkiFinland

Personalised recommendations