Hearing in Amphibious Marine Mammals

Amphibious marine mammals consist of the pinnipeds (sea lions and fur seals, Family Otariidae; true seals, Family Phocidae; and walruses, Family Odobenidae), sea otters (Family Mustelidae), and polar bears (Family Ursidae). All spend time on land as well as in the water. Consequently, their ears need to function both in air and under water[1]Wartzok, D., & Ketten, D. R. (1999). Marine Mammal Sensory Systems. In J. E. I. Reynolds & S. E. Rommel (Eds.), Biology of Marine Mammals (pp. 117–175). Washington D.C.: Smithsonian Institution Press..

Examples of amphibious marine mammals (left to right). Steller sea lion (Eumetopias jubatus), image credit: NOAA Fisheries. Spotted seal (Phoca vitulina), image credit: Wikimedia. Polar bear (Ursus maritimus), image credit: USGS.

When hearing in air, amphibious marine mammals appear to use the same basic processes as terrestrial mammals. Sound waves enter through the outer ear and vibrate the tympanic membrane and middle ear ossicles. The size and shape of the tympanic membrane and ossicles influence hearing frequency range[2] 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. The Journal of the Acoustical Society of America, 120(6), 3463–3466. https://doi.org/10.1121/1.2372712[3] Nummela, S. (2008). Hearing in aquatic mammals. In J. G. M. Thewissen & S. Nummela (Eds.), Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates (pp. 211-224). Berkeley, CA: University of California Press.. High-frequency versus low frequency hearing is affected by differences in the stiffness and mass of the ossicles.

Underwater hearing capabilities vary among amphibious marine mammals. Sea otters and polar bears have ears that are less specialized for underwater hearing when compared to pinnipeds. The middle and inner ear of pinnipeds function the same in air and under water, but phocid and odobenid (walruses) ears have developed morphological adaptations that characterize them as a unique mammalian ear type[4] Nummela, S. (2008). Hearing in aquatic mammals. In J. G. M. Thewissen & S. Nummela (Eds.), Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates (pp. 211-224). Berkeley, CA: University of California Press.. This ear type includes an inflated auditory bulla, enlarged tympanic membrane, and massive middle ear ossicles that are ten times larger than in terrestrial mammals with a similar skull size[5] 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. The Journal of the Acoustical Society of America, 120(6), 3463–3466. https://doi.org/10.1121/1.2372712.

Phocids (true seals) have muscles and a cartilaginous mechanism that close the external ear canal to water when diving. As described above, phocids also have morphological adaptations that expand their frequency range of hearing in water to at least six octaves, resulting in an underwater hearing ability that rivals fully aquatic mammals[6] Reichmuth, C., Holt, M. M., Mulsow, J., Sills, J. M., & Southall, B. L. (2013). Comparative assessment of amphibious hearing in pinnipeds. Journal of Comparative Physiology A, 199(6), 491–507. https://doi.org/10.1007/s00359-013-0813-y.. Phocids have not lost their aerial hearing capabilities, however, and can hear as well as many terrestrial carnivores. Elephant seals appear to be better at hearing sounds under water than in air, which may in part be due to adaptations of the middle ear to the pressures found at the deep depths to which elephant seals dive[7] Reichmuth, C., Holt, M. M., Mulsow, J., Sills, J. M., & Southall, B. L. (2013). Comparative assessment of amphibious hearing in pinnipeds. Journal of Comparative Physiology A, 199(6), 491–507. https://doi.org/10.1007/s00359-013-0813-y..

Odobenids (walruses) have some of the same morphological adaptations as phocids, but the shape and form of their middle ear ossicles are more similar to that of otariids. The morphology of the ossicles places odobenids in the same hearing category of “other marine carnivores,” separate from the phocids[8]Southall, B. L., Finneran, J. J., Reichmuth, C., Nachtigall, P. E., Ketten, D. R., Bowles, A. E., Ellison, W. T., Nowacek, D. P., & Tyack, P. L. (2019). Marine mammal moise exposure criteria: Updated scientific recommendations for residual hearing effects. Aquatic Mammals, 45(2), 125–232. https://doi.org/10.1578/AM.45.2.2019.125..

Otariids (eared seals, including fur seals and sea lions) produce a wide frequency range of sounds and have in-air hearing abilities similar to those of their terrestrial relatives, such as bears[9]Moore, P. W. B., & Schusterman, R. J. (1987). Audiometric assessment of Northern fur seals, Callorhinus ursinus. Marine Mammal Science, 3(1), 31–53. https://doi.org/10.1111/j.1748-7692.1987.tb00150.x.[10]Reichmuth, C., & Southall, B. L. (2012). Underwater hearing in California sea lions (Zalophus californianus): Expansion and interpretation of existing data. Marine Mammal Science, 28(2), 358–363. https://doi.org/10.1111/j.1748-7692.2011.00473.x.[11]Mulsow, J., Reichmuth, C., Gulland, F., Rosen, D. A. S., & Finneran, J. J. (2011). Aerial audiograms of several California sea lions (Zalophus californianus) and Steller sea lions (Eumetopias jubatus) measured using single and multiple simultaneous auditory steady-state response methods. Journal of Experimental Biology, 214(7), 1138–1147. https://doi.org/10.1242/jeb.052837.[12]Mulsow, J., Finneran, J. J., & Houser, D. S. (2011). California sea lion (Zalophus californianus ) aerial hearing sensitivity measured using auditory steady-state response and psychophysical methods. The Journal of the Acoustical Society of America, 129(4), 2298–2306. https://doi.org/10.1121/1.3552882..These pinnipeds also hear well under water, albeit over a narrower frequency range than that of phocids and most fully aquatic mammals[13] Reichmuth, C., Holt, M. M., Mulsow, J., Sills, J. M., & Southall, B. L. (2013). Comparative assessment of amphibious hearing in pinnipeds. Journal of Comparative Physiology A, 199(6), 491–507. https://doi.org/10.1007/s00359-013-0813-y..

Amphibious marine mammals have not necessarily sacrificed aerial hearing abilities for underwater hearing capabilities. More research is needed for amphibious species, especially pinnipeds, to better understand their hearing capabilities.

Additional Links on DOSITS

Additional Resources

  • Computerized Scanning and Imaging Facility at Woods Hole Oceanographic Institution, Image Gallery
  • Fay, R. R., & Wilber, L. A. (1989). Hearing in Vertebrates: A Psychophysics Databook. The Journal of the Acoustical Society of America, 86(5), 2044–2044. https://doi.org/10.1121/1.398550.
  • Ghoul, A., & Reichmuth, C. (2014). Hearing in the sea otter (Enhydra lutris): Auditory profiles for an amphibious marine carnivore. Journal of Comparative Physiology A, 200(11), 967–981. https://doi.org/10.1007/s00359-014-0943-x.
  • Kastelein, R. A., Mosterd, P., van Ligtenberg, C. L., & Verboom, W. C. (1996). Aerial hearing sensitivity tests with a male Pacific walrus (Odobenus rosmarus divergens), in the free field and with headphones. Aquatic Mammals, 22, 81–93.
  • Kastelein, R. A., Mosterd, P., van Santen, B., Hagedoorn, M., & de Haan, D. (2002). Underwater audiogram of a Pacific walrus ( Odobenus rosmarus divergens ) measured with narrow-band frequency-modulated signals. The Journal of the Acoustical Society of America, 112(5), 2173–2182. https://doi.org/10.1121/1.1508783.
  • Pinniped Cognition and Sensory Systems Laboratory, Long Marine Lab, University of California Santa Cruz:

References

  • Nachtigall, P. E., Supin, A. Y., Amundin, M., Roken, B., Moller, T., Mooney, T. A., Taylor, K. A., & Yuen, M. (2007). Polar bear, Ursus maritimus, hearing measured with auditory evoked potentials. Journal of Experimental Biology, 210(7), 1116–1122. https://doi.org/10.1242/jeb.02734.
  • Owen, M., & Bowles, A. (2011). In-air auditory psychophysics and the management of a threatened carnivore, the polar bear (Ursus maritimus). International Journal of Comparative Psychology, 24, 244–254.
  • Smodlaka, H., Khamas, W. A., Jungers, H., Pan, R., Al‐Tikriti, M., Borovac, J. A., Palmer, L., & Bukac, M. (2019). A novel understanding of Phocidae hearing adaptations through a study of Northern elephant seal ( Mirounga angustirostris ) ear anatomy and histology. The Anatomical Record, 302(9), 1605–1614. https://doi.org/10.1002/ar.24026.

Cited References   [ + ]

1. Wartzok, D., & Ketten, D. R. (1999). Marine Mammal Sensory Systems. In J. E. I. Reynolds & S. E. Rommel (Eds.), Biology of Marine Mammals (pp. 117–175). Washington D.C.: Smithsonian Institution Press.
2, 5. 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. The Journal of the Acoustical Society of America, 120(6), 3463–3466. https://doi.org/10.1121/1.2372712
3. Nummela, S. (2008). Hearing in aquatic mammals. In J. G. M. Thewissen & S. Nummela (Eds.), Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates (pp. 211-224). Berkeley, CA: University of California Press.
4. Nummela, S. (2008). Hearing in aquatic mammals. In J. G. M. Thewissen & S. Nummela (Eds.), Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates (pp. 211-224). Berkeley, CA: University of California Press.
6. Reichmuth, C., Holt, M. M., Mulsow, J., Sills, J. M., & Southall, B. L. (2013). Comparative assessment of amphibious hearing in pinnipeds. Journal of Comparative Physiology A, 199(6), 491–507. https://doi.org/10.1007/s00359-013-0813-y.
7, 13. Reichmuth, C., Holt, M. M., Mulsow, J., Sills, J. M., & Southall, B. L. (2013). Comparative assessment of amphibious hearing in pinnipeds. Journal of Comparative Physiology A, 199(6), 491–507. https://doi.org/10.1007/s00359-013-0813-y.
8. Southall, B. L., Finneran, J. J., Reichmuth, C., Nachtigall, P. E., Ketten, D. R., Bowles, A. E., Ellison, W. T., Nowacek, D. P., & Tyack, P. L. (2019). Marine mammal moise exposure criteria: Updated scientific recommendations for residual hearing effects. Aquatic Mammals, 45(2), 125–232. https://doi.org/10.1578/AM.45.2.2019.125.
9. Moore, P. W. B., & Schusterman, R. J. (1987). Audiometric assessment of Northern fur seals, Callorhinus ursinus. Marine Mammal Science, 3(1), 31–53. https://doi.org/10.1111/j.1748-7692.1987.tb00150.x.
10. Reichmuth, C., & Southall, B. L. (2012). Underwater hearing in California sea lions (Zalophus californianus): Expansion and interpretation of existing data. Marine Mammal Science, 28(2), 358–363. https://doi.org/10.1111/j.1748-7692.2011.00473.x.
11. Mulsow, J., Reichmuth, C., Gulland, F., Rosen, D. A. S., & Finneran, J. J. (2011). Aerial audiograms of several California sea lions (Zalophus californianus) and Steller sea lions (Eumetopias jubatus) measured using single and multiple simultaneous auditory steady-state response methods. Journal of Experimental Biology, 214(7), 1138–1147. https://doi.org/10.1242/jeb.052837.
12. Mulsow, J., Finneran, J. J., & Houser, D. S. (2011). California sea lion (Zalophus californianus ) aerial hearing sensitivity measured using auditory steady-state response and psychophysical methods. The Journal of the Acoustical Society of America, 129(4), 2298–2306. https://doi.org/10.1121/1.3552882.