Advertisement

Journal of Comparative Physiology A

, Volume 199, Issue 6, pp 491–507 | Cite as

Comparative assessment of amphibious hearing in pinnipeds

  • Colleen Reichmuth
  • Marla M. Holt
  • Jason Mulsow
  • Jillian M. Sills
  • Brandon L. Southall
Original Paper

Abstract

Auditory sensitivity in pinnipeds is influenced by the need to balance efficient sound detection in two vastly different physical environments. Previous comparisons between aerial and underwater hearing capabilities have considered media-dependent differences relative to auditory anatomy, acoustic communication, ecology, and amphibious life history. New data for several species, including recently published audiograms and previously unreported measurements obtained in quiet conditions, necessitate a re-evaluation of amphibious hearing in pinnipeds. Several findings related to underwater hearing are consistent with earlier assessments, including an expanded frequency range of best hearing in true seals that spans at least six octaves. The most notable new results indicate markedly better aerial sensitivity in two seals (Phoca vitulina and Mirounga angustirostris) and one sea lion (Zalophus californianus), likely attributable to improved ambient noise control in test enclosures. An updated comparative analysis alters conventional views and demonstrates that these amphibious pinnipeds have not necessarily sacrificed aerial hearing capabilities in favor of enhanced underwater sound reception. Despite possessing underwater hearing that is nearly as sensitive as fully aquatic cetaceans and sirenians, many seals and sea lions have retained acute aerial hearing capabilities rivaling those of terrestrial carnivores.

Keywords

California sea lion Harbor seal Northern elephant seal Hearing threshold Amphibious hearing Audiogram 

Notes

Acknowledgments

This work was conducted over a period of many years and was supported by the contributions of several individuals. It is important for us to acknowledge that Dr. David Kastak conceived, planned, and conducted much of this research. His long-standing interest in the trade-offs between aerial and underwater hearing in marine mammals stimulated countless discussions, careful experiments, and thoughtful revisions of earlier ideas. Dr. Ronald Schusterman encouraged us during this research and reminded us of the value of viewing science as a self-correcting process. Drs. Bertel Møhl, Jack Terhune, and Patrick Moore influenced this research by sharing their perspectives during early phases of data collection. This research would not have been possible without the participation of many members of our research program at Long Marine Laboratory, especially Amy Bernard, Asila Ghoul, Andrew Rouse, and Brendan Wakefield, and we thank the entire team for their hard work and partnership. Support for this research was provided by the Office of Naval Research through awards N00014-99-1-0164, B00014-02-1-0159, N00014-04-1-0248, and N00014-06-1-0295 and DURIP through award N00014-99-1-0686. This manuscript was improved by the helpful comments of JCP-A Editor Dr. Wolf Hanke and two anonymous reviewers.

Ethical standards

Animal welfare considerations were consistent with the current laws of the United States. Federal authorization for marine mammal research was granted by the National Marine Fisheries Service under scientific research permits 887, 259-1481, 1072-1771, and 14535 to RJ Schusterman and C Reichmuth. The animal protocols associated with this research were reviewed and approved by the US Department of Defense and by the Institutional Animal Care and Use Committee at the University of California Santa Cruz.

Supplementary material

Procedural depiction of an experimental session for the aerial audiogram. Several signal-present trials and control (blank) trials are shown for the harbor seal subject tested in the hemi-anechoic chamber. Signals are 500 ms pure tones with frequency of 400 Hz (MPG 58692 kb)

Procedural depiction of an experimental session for the underwater audiogram. Several signal-present trials and control (blank) trials are shown for the sea lion subject tested in the pool. Signals are 500 ms narrow-band, FM sweeps centered at 800 Hz (MPG 62250 kb)

359_2013_813_MOESM3_ESM.pdf (133 kb)
The psychometric functions associated with aerial auditory thresholds for the harbor seal subject (Sprouts) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 20 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 132 kb)
359_2013_813_MOESM4_ESM.pdf (136 kb)
The psychometric functions associated with aerial auditory thresholds for the northern elephant seal subject (Burnyce) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 20 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 135 kb)
359_2013_813_MOESM5_ESM.pdf (137 kb)
The psychometric functions associated with aerial auditory thresholds for the California sea lion subject (Rio) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 20 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 137 kb)
359_2013_813_MOESM6_ESM.pdf (86 kb)
The psychometric functions associated with underwater auditory thresholds for the harbor seal subject (Sprouts) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 1 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 85 kb)
359_2013_813_MOESM7_ESM.pdf (128 kb)
The psychometric functions associated with underwater auditory thresholds for the California sea lion subject (Ronan) at each test frequency. The X-axis of each plot shows the sound pressure level in dB re 1 μPa. The Y-axis shows the percent correct detection on signal-present trials during MCS testing. Probit analysis was used to fit the psychometric function to the observed proportion of correct detections at each stimulus level. An inverse prediction (not shown) was then used to determine the threshold, defined as the 50 % correct detection probability (depicted by the dotted lines) (PDF 128 kb)

References

  1. Babushina Ye S (1979) Localization by the dolphin of the source of tonal and pulse signals in water and in air. Vestnik Leningradskogo Universiteta Biologiva 3:119–121Google Scholar
  2. Babushina Ye S, Zaslavskii GL, Yurkevich LI (1991) Air and underwater hearing characteristics of the northern fur seal: audiograms, frequency and differential thresholds. Biophysics 36:909–913Google Scholar
  3. Branstetter BK, Finneran JJ (2008) Comodulation masking release in bottlenose dolphins (Tursiops truncatus). J Acoust Soc Am 124:625–633PubMedCrossRefGoogle Scholar
  4. Brüel and Kjær (2008) Technical documentation: hand-held analyzers types 2250 and 2270. Brüel and Kjær, Sound and Vibration Measurement A/S, NærumGoogle Scholar
  5. Cornsweet TN (1962) The staircase method in psychophysics. Am J Psychol 75:485–491PubMedCrossRefGoogle Scholar
  6. Finneran JJ (2003) An integrated computer-controlled system for marine mammal auditory testing. SSC, San Diego, CA, 102 pGoogle Scholar
  7. Finneran JJ, Schlundt CE (2007) Underwater sound pressure variation and bottlenose dolphin (Tursiops truncatus) hearing thresholds in a small pool. J Acoust Soc Am 122:606–614PubMedCrossRefGoogle Scholar
  8. Finneran JJ, Carder DA, Ridgway SH (2002) Low-frequency acoustic pressure, velocity, and intensity thresholds in a bottlenose dolphin (Tursiops truncatus) and white whale (Delphinapterus leucas). J Acoust Soc Am 111:447–456PubMedCrossRefGoogle Scholar
  9. Finney DJ (1971) Probit analysis, 3rd edn. Cambridge UP, CambridgeGoogle Scholar
  10. Fobes JL, Smock CC (1981) Sensory capacities of marine mammals. Psychol Bull 89:288–307PubMedCrossRefGoogle Scholar
  11. Gelfand SA (2001) Essentials of audiology, 2nd edn. Thieme, New YorkGoogle Scholar
  12. Gerstein ER, Gerstein L, Forsythe SE, Blue JE (1999) The underwater audiogram of the West Indian manatee (Trichechus manatus). J Acoust Soc Am 105:3575–3583PubMedCrossRefGoogle Scholar
  13. Heffner HE (1983) Hearing in large and small dogs: absolute thresholds and size of the tympanic membrane. Behav Neurosci 97:310–318CrossRefGoogle Scholar
  14. Heffner RS, Heffner HE (1985a) Hearing range of the domestic cat. Hear Res 19:85–88PubMedCrossRefGoogle Scholar
  15. Heffner RS, Heffner HE (1985b) Hearing in mammals: the least weasel. J Mammal 66:745–755CrossRefGoogle Scholar
  16. 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 120:3463–3466PubMedCrossRefGoogle Scholar
  17. Houser DS, Crocker DE, Reichmuth C, Mulsow J, Finneran JJ (2007) Auditory evoked potentials in northern elephant seals (Mirounga angustirostris). Aquat Mamm 33:110–121CrossRefGoogle Scholar
  18. Houser DS, Crocker DE, Finneran JJ (2008) Click-evoked potentials in a large marine mammal, the adult male northern elephant seal (Mirounga angustirostris). J Acoust Soc Am 124:44–47PubMedCrossRefGoogle Scholar
  19. Johnson CS (1967) Sound detection thresholds in marine mammals. In: Tavolga WN (ed) Marine bio-acoustics, vol 2. Pergamon Press, Oxford, pp 247–260Google Scholar
  20. Kastak D, Schusterman RJ (1998) Low-frequency amphibious hearing in pinnipeds: methods, measurements, noise, and ecology. J Acoust Soc Am 103:2216–2228PubMedCrossRefGoogle Scholar
  21. Kastak D, Schusterman RJ (1999) In-air and underwater hearing sensitivity of a northern elephant seal (Mirounga angustirostris). Can J Zool 77:1751–1758Google Scholar
  22. Kastak D, Schusterman RJ (2002) Changes in auditory sensitivity with depth in a free-diving California sea lion (Zalophus californianus). J Acoust Soc Am 112:329–333PubMedCrossRefGoogle Scholar
  23. Kastelein RA, Nieuwstraten SH, Staal C, van Ligtenberg CL, Versteegh D (1997) Low-frequency aerial hearing of a harbor porpoise (Phocoena phocoena). In: Read AJ, Wiepkema PR, Nachtigall PE (eds) The biology of the harbor porpoise. De Spil Publishers, Woerden, pp 295–312Google Scholar
  24. 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 112:334–344PubMedCrossRefGoogle Scholar
  25. Kastelein RA, Wensveen PJ, Hoek L, Verboom WC, Terhune JM (2009) Underwater detection of tonal signals between 0.125 and 100 kHz by harbor seals (Phoca vitulina). J Acoust Soc Am 125:1222–1229PubMedCrossRefGoogle Scholar
  26. Kelly JB, Kavanagh GL, Dalton JCH (1986) Hearing in the ferret (Mustela putorius): thresholds for pure tone detection. Hear Res 24:269–275PubMedCrossRefGoogle Scholar
  27. 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 717–750CrossRefGoogle Scholar
  28. Killion MC (1978) Revised estimate of minimum audible pressure: where is the “missing 6 dB”? J Acoust Soc Am 63:1501–1508PubMedCrossRefGoogle Scholar
  29. Liebschner A, Hanke W, Miersch L, Dehnhardt G (2005) Sensitivity of a tucuxi (Sotalia fluviatilis guianensis) to airborne sound. J Acoust Soc Am 117:436–441PubMedCrossRefGoogle Scholar
  30. Lipatov NV (1992) Underwater hearing in seals: the role of the outer ear. In: Thomas JA, Kastelein RA, Supin AY (eds) Marine mammal sensory systems. Plenum Press, New York, pp 249–256CrossRefGoogle Scholar
  31. Møhl B (1968a) Auditory sensitivity of the common seal in air and water. J Aud Res 8:27–38Google Scholar
  32. Møhl B (1968b) Hearing in seals. In: Harrison RJ, Hubbard RC, Peterson RS, Rice CE, Schusterman RJ (eds) The behavior and physiology of pinnipeds. Appleton-Century-Crofts, New York, pp 172–195Google Scholar
  33. Mooney TA, Yamamoto M, Branstetter BK (2012) Hearing in cetaceans: from natural history to experimental biology. Adv Mar Biol 63:197–246PubMedCrossRefGoogle Scholar
  34. Moore PWB, Schusterman RJ (1987) Audiometric assessment of northern fur seals, Callorhinus ursinus. Mar Mamm Sci 3:31–53CrossRefGoogle Scholar
  35. Mulsow J, Reichmuth C (2007) Electrophysiological assessment of temporal resolution in pinnipeds. Aquat Mamm 33:122–131CrossRefGoogle Scholar
  36. Mulsow JL, Reichmuth C (2010) Psychophysical and electrophysiological aerial audiograms of a Steller sea lion (Eumetopias jubatus). J Acoust Soc Am 127:2692–2701PubMedCrossRefGoogle Scholar
  37. Mulsow J, Finneran JJ, Houser DS (2011) California sea lion (Zalophus californianus) aerial hearing sensitivity measured using auditory steady-state response and psychophysical methods. J Acoust Soc Am 129:2298–2306PubMedCrossRefGoogle Scholar
  38. Mulsow J, Houser DS, Finneran JJ (2012a) Underwater psychophysical audiogram of a young male California sea lion (Zalophus californianus). J Acoust Soc Am 131:4182–4187PubMedCrossRefGoogle Scholar
  39. Mulsow J, Reichmuth C, Houser D, Finneran JJ (2012b) Auditory evoked potential measurement of hearing sensitivity in pinnipeds. In: Popper AN, Hawkins A (eds) The effects of noise on aquatic life. Springer, Berlin, pp 73–76CrossRefGoogle Scholar
  40. 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, Berkeley, pp 211–231Google Scholar
  41. Nummela S, Thewissen JGM (2008) The physics of sound in air and water. In: Thewissen JGM, Nummela S (eds) Sensory evolution on threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 175–181Google Scholar
  42. Parvin SJ, Nedwell JR (1995) Underwater sound perception and the development of an underwater noise weighting scale. Underw Tech 21:12–19CrossRefGoogle Scholar
  43. Ramprashad F (1975) Aquatic adaptations in the ear of the harp seal Pagophilus groenlandicus (Erxleben, 1777). Rapp P-v Reun Cons Int Explor Mer 169:102–111Google Scholar
  44. Reichmuth C, Southall BL (2012) Underwater hearing in California sea lions (Zalophus californianus): expansion and interpretation of existing data. Mar Mamm Sci 28:358–363CrossRefGoogle Scholar
  45. Reichmuth C, Ghoul A, Southall BL (2012) Temporal processing of low-frequency sounds by seals (L). J Acoust Soc Am 132:2147–2150PubMedCrossRefGoogle Scholar
  46. Repenning CA (1972) Underwater hearing in seals: Functional morphology. In: Harrison RJ (ed) Functional anatomy of marine mammals, vol 1. Academic Press, London, pp 307–331Google Scholar
  47. Richardson WJ, Greene CR, Malme CI, Thomson DH (1995) Marine mammals and noise. Academic, San DiegoGoogle Scholar
  48. Robinson PW, Costa DP, Crocker DE, Gallo-Reynoso JP, Champange CD, Fowler MA, Goetsch C, Goetz KT, Hassrick JL, Huckstadt LA, Kuhn CE, Maresh JL, Maxwell SM, McDonald BI, Peterson SH, Simmons SE, Teutschel NM, Villegas-Amtmann S, Yoda K (2012) Foraging behavior and success of a mesopelagic predator in the northeast Pacific Ocean: insights from a data-rich species, the northern elephant seal. PLoS ONE 7:e36728PubMedCrossRefGoogle Scholar
  49. Schusterman RJ (1974a) Auditory sensitivity of a California sea lion to airborne sound. J Acoust Soc Am 56:1248–1251PubMedCrossRefGoogle Scholar
  50. Schusterman RJ (1974b) Low false-alarm rates in signal detection by marine mammals. J Acoust Soc Am 55:845–848PubMedCrossRefGoogle Scholar
  51. Schusterman RJ, Balliet RF, Nixon J (1972) Underwater audiogram of the California sea lion by the conditioned vocalization technique. J Exp Anal Behav 17:339–350PubMedCrossRefGoogle Scholar
  52. Schusterman RJ, Kastak D, Levenson DH, Reichmuth CJ, Southall BL (2000) Why pinnipeds don’t echolocate. J Acoust Soc Am 107:2256–2264PubMedCrossRefGoogle Scholar
  53. Siler W (1969) Near-and far fields in a marine environment. J Acoust Soc Am 46:483–484CrossRefGoogle Scholar
  54. Southall BL, Schusterman RJ, Kastak D (2000) Masking in three pinnipeds: underwater, low-frequency critical ratios. J Acoust Soc Am 108:1322–1326PubMedCrossRefGoogle Scholar
  55. Southall BL, Schusterman RJ, Kastak D (2003) Masking in three pinnipeds: aerial critical ratios and direct critical bandwidth measurements. J Acoust Soc Am 114(3):1660–1666PubMedCrossRefGoogle Scholar
  56. Southall BLS, Schusterman RJ, Kastak D, Reichmuth Kastak C (2005) Reliability of underwater hearing thresholds. Acoust Res Lett Onl 6:243–249CrossRefGoogle Scholar
  57. Southall BL, Bowles AE, Ellison WT, Finneran JJ, Gentry RL, Greene CR, Kastak D, Ketten DK, Miller JH, Nachtigall PE, Richardson WJ, Thomas JA, Tyack PL (2007) Marine mammal noise exposure criteria: initial scientific recommendations. Aquat Mamm 33:412–521CrossRefGoogle Scholar
  58. Stebbins WC (1970) Principles of animal psychophysics. In: Stebbins WC (ed) Animal psychophysics: the design and conduct of sensory experiments. Appleton-Century-Crofts, New York, pp 1–19CrossRefGoogle Scholar
  59. Supin AY, Popov VV, Mass AM (2001) The sensory physiology of aquatic mammals. Kluwer Academic Publishers, BostonCrossRefGoogle Scholar
  60. Terhune JM (1988) Detection thresholds of a harbour seal to repeated underwater high-frequency, short-duration sinusoidal pulses. Can J Zool 66:1578–1582CrossRefGoogle Scholar
  61. Terhune JM (1991) Masked and unmasked pure tone detection thresholds of a harbour seal listening in air. Can J Zool 69:2059–2066CrossRefGoogle Scholar
  62. Terhune JM, Ronald K (1971) The harp seal, Pagophilus groenlandicus (Erxleben 1777). X. The air audiogram. Can J Zool 49:385–390PubMedCrossRefGoogle Scholar
  63. Terhune JM, Ronald K (1972) The harp seal, Pagophilus groenlandicus (Erxleben 1777). III. The underwater audiogram. Can J Zool 50:565–569PubMedCrossRefGoogle Scholar
  64. Thomas J, Chun N, Au W, Pugh K (1988) Underwater audiogram of a false killer whale (Pseudorca crassidens). J Acoust Soc Am 84:936–940PubMedCrossRefGoogle Scholar
  65. Turnbull SD, Terhune JM (1990) White noise and pure tone masking of pure tone thresholds of a harbor seal listening in air and underwater. Can J Zool 68:2090–2097CrossRefGoogle Scholar
  66. Wainwright WN (1958) Comparison of hearing thresholds in air and in water. J Acoust Soc Am 30:1025–1029CrossRefGoogle Scholar
  67. Wartzok D, Ketten DR (1999) Marine mammal sensory systems. In: Reynolds JE III, Rommel SA (eds) Biology of marine mammals. Smithsonian Institute, Washington, D.C., pp 117–175Google Scholar
  68. Watkins WA, Wartzok D (1985) Sensory biophysics of marine mammals. Mar Mamm Sci 3:219–260CrossRefGoogle Scholar
  69. Wolski LF, Anderson RC, Bowles AE, Yochem PK (2003) Measuring hearing in the harbor seal (Phoca vitulina): comparison of behavioral and auditory brainstem response techniques. J Acoust Soc Am 113:629–637PubMedCrossRefGoogle Scholar
  70. Yost WA (2000) Fundamentals of hearing: an introduction, 4th edn. Academic Press, San DiegoGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Colleen Reichmuth
    • 1
  • Marla M. Holt
    • 2
  • Jason Mulsow
    • 3
  • Jillian M. Sills
    • 4
  • Brandon L. Southall
    • 1
    • 5
  1. 1.Long Marine Laboratory, Institute of Marine SciencesUniversity of California Santa CruzSanta CruzUSA
  2. 2.Conservation Biology Division, Northwest Fisheries Science CenterNational Marine Fisheries Service, National Oceanic and Atmospheric AdministrationSeattleUSA
  3. 3.National Marine Mammal FoundationSan DiegoUSA
  4. 4.Long Marine Laboratory, Department of Ocean SciencesUniversity of California Santa CruzSanta CruzUSA
  5. 5.SEA Inc.AptosUSA

Personalised recommendations