Hearing Loss in Fishes

Intense sounds of short duration or less intense, longer duration sounds may produce a temporary or permanent hearing loss. A temporary decrease in hearing sensitivity involves reversible damage to the inner ear and is called a temporary threshold shift (TTS). A permanent threshold shift (PTS) involves irreversible damage to the inner ear, such as hair cell loss or damage to other inner ear tissues. In many non-fish species, including humans, sounds that kill hair cells results in PTS. However, fishes, including sharks and rays, can replace hair cells lost as a result of exposure to intense sounds or ototoxic drugs[1]Popper, A. N., & Hoxter, B. (1984). Growth of a fish ear: 1. Quantitative analysis of hair cell and ganglion cell proliferation. Hearing Research, 15(2), 133–142. https://doi.org/10.1016/0378-5955(84)90044-3[2]Lombarte, A., Yan, H. Y., Popper, A. N., Chang, J. S., & Platt, C. (1993). Damage and regeneration of hair cell ciliary bundles in a fish ear following treatment with gentamicin. Hearing Research, 64(2), 166–174. https://doi.org/10.1016/0378-5955(93)90002-I[3]Lombarte, A., & Popper, A. N. (1994). Quantitative analyses of postembryonic hair cell addition in the otolithic endorgans of the inner ear of the european hake,merluccius merluccius (gadiformes, teleostei). The Journal of Comparative Neurology, 345(3), 419–428. https://doi.org/10.1002/cne.903450308[4]Popper, A. N., Smith, M. E., Cott, P. A., Hanna, B. W., MacGillivray, A. O., Austin, M. E., & Mann, D. A. (2005). Effects of exposure to seismic airgun use on hearing of three fish species. The Journal of the Acoustical Society of America, 117(6), 3958–3971. https://doi.org/10.1121/1.1904386[5]Popper, A. N., Halvorsen, M. B., Kane, A., Miller, D. L., Smith, M. E., Song, J., Stein, P., & Wysocki, L. E. (2007). The effects of high-intensity, low-frequency active sonar on rainbow trout. The Journal of the Acoustical Society of America, 122(1), 623–635. https://doi.org/10.1121/1.2735115. Moreover, fishes add large numbers of hair cells, as well as repair and replace damaged hair cells, throughout their life. For example, the ear in a juvenile Mediterranean hake may have 5,000 hair cells, whereas an adult may have 2 million. Lastly, regeneration is correlated with a functional recovery of hearing ability[6]Popper, A. N., Halvorsen, M. B., Kane, A., Miller, D. L., Smith, M. E., Song, J., Stein, P., & Wysocki, L. E. (2007). The effects of high-intensity, low-frequency active sonar on rainbow trout. The Journal of the Acoustical Society of America, 122(1), 623–635. https://doi.org/10.1121/1.2735115. As a consequence of the ability to repair and regenerate hair cells, the likelihood of PTS in fishes is considered to be very low.

If a TTS occurs, the magnitude and duration of the hearing impairment depends on multiple variables, such as frequency and intensity of the sound and duration of exposure (see How do you determine if a sound affects a marine animal?). Limited data show some fish species are susceptible to TTS[7]Popper, A. N., Halvorsen, M. B., Kane, A., Miller, D. L., Smith, M. E., Song, J., Stein, P., & Wysocki, L. E. (2007). The effects of high-intensity, low-frequency active sonar on rainbow trout. The Journal of the Acoustical Society of America, 122(1), 623–635. https://doi.org/10.1121/1.2735115. For example, TTS was shown in fathead minnows after exposure to playbacks of boat engine noise at 142 underwater dB for 2 hours[8]Scholik, A. R., & Yan, H. Y. (2002). Effects of boat engine noise on the auditory sensitivity of the fathead minnow, Pimephales promelas. Environmental Biology of Fishes, 63, 203–209. https://doi.org/10.1023/A:1014266531390p, and goldfish developed a TTS after exposure to 166-170 underwater dB of white noise for 10 minutes[9]Smith, M. E., Kane, A., & Popper, A. N. (2004). Acoustical stress and hearing sensitivity in fishes: Does the linear threshold shift hypothesis hold water? Journal of Experimental Biology, 207(20), 3591–3602. https://doi.org/10.1242/jeb.01188. In both studies the length of time required for recovery varied as a function of the exposure frequency and duration[10]Scholik, A. R., & Yan, H. Y. (2001). Effects of underwater noise on auditory sensitivity of a cyprinid fish. Hearing Research, 152(1–2), 17–24. https://doi.org/10.1016/S0378-5955(00)00213-6. It is likely that the frequency and sound levels needed to produce TTS vary widely by species. The data suggests that some species that have enhanced hearing, such as goldfish, catfish, and minnows, are more likely to be subject to TTS than other fishes such as salmon and sunfish[11]Smith, M. E. (2016). Relationship Between Hair Cell Loss and Hearing Loss in Fishes. In A. N. Popper & A. Hawkins (Eds.), The Effects of Noise on Aquatic Life II (Vol. 875, pp. 1067–1074). Springer New York. https://doi.org/10.1007/978-1-4939-2981-8_132.

Graph shows the amount of TTS at different frequencies when goldfish were exposed to different sound levels of white noise. Hearing sensitivity (threshold) got poorer as the noise level increased. Fishes with minimal noise exposure, at 110 dB, showed almost no threshold shift, while fishes exposed to 160 dB noise showed considerable hearing loss at all frequencies tested. Adapted with permission from Smith et al. 2004.

There are correlations for TTS and physical hair cell damage when fishes are exposed to intense sounds[12]Smith, M. E., Kane, A., & Popper, A. N. (2004). Noise-induced stress response and hearing loss in goldfish (Carassius auratus). Journal of Experimental Biology, 207(3), 427–435. https://doi.org/10.1242/jeb.00755[13]Smith, M. E., Coffin, A. B., Miller, D. L., & Popper, A. N. (2006). Anatomical and functional recovery of the goldfish (Carassius auratus) ear following noise exposure. Journal of Experimental Biology, 209(21), 4193–4202. https://doi.org/10.1242/jeb.02490. However, in a study with goldfish, hearing thresholds returned to normal and the damaged hair cells were replaced after seven days[14]Smith, M. E., Coffin, A. B., Miller, D. L., & Popper, A. N. (2006). Anatomical and functional recovery of the goldfish (Carassius auratus) ear following noise exposure. Journal of Experimental Biology, 209(21), 4193–4202. https://doi.org/10.1242/jeb.02490.

Images of the saccular sensory epithelium of goldfish. The cells are stained with a fluorescent dye (“labeled”) so they look white under the microscope. In control animals (not shown) the images would look like A, with the surfaces covered evenly with labeled sensory cells. Figures A and C are from the rostral (front) end of the epithelium while B and C are from the caudal (back) end. A and B were from goldfish exposed to 100 Hz and show far more loss of sensory cells in the caudal end of the epithelium than the rostral. In contrast, in fish exposed to 2000 Hz, there is much more loss of sensory cells in the rostral (C) than caudal (D) end. Scale bars = 50 µm. (Reprinted from Smith, M.E., Schuck, J.B., Gilley, R.R., and Rogers, B.D. 2011. Structural and functional effects of acoustic exposure in goldfish: evidence for tonotopy in the teleost saccule. BMC Neuroscience 12:19, Doi:10.1186/1471-2202-12-19.)

In several controlled exposure studies, multiple species in cages were exposed to a US Navy SURTASS LFA sound source in a lake (received level of 193 underwater dB) for 324 or 628 seconds. Rainbow trout and channel catfish, but not hybrid sunfish, largemouth bass, or yellow perch, showed small TTS for several days after exposure[15]Halvorsen, M. B., Zeddies, D. G., Chicoine, D., & Popper, A. N. (2013). Effects of low-frequency naval sonar exposure on three species of fish. The Journal of the Acoustical Society of America, 134(2), EL205–EL210. https://doi.org/10.1121/1.4812818[16]Popper, A. N., Halvorsen, M. B., Kane, A., Miller, D. L., Smith, M. E., Song, J., Stein, P., & Wysocki, L. E. (2007). The effects of high-intensity, low-frequency active sonar on rainbow trout. The Journal of the Acoustical Society of America, 122(1), 623–635. https://doi.org/10.1121/1.2735115[17]Halvorsen, M. B., Zeddies, D. G., Ellison, W. T., Chicoine, D. R., & Popper, A. N. (2012). Effects of mid-frequency active sonar on hearing in fish. The Journal of the Acoustical Society of America, 131(1), 599–607. https://doi.org/10.1121/1.3664082. However, none of the fishes showed exposure-related damage in the inner ear and other body tissues[18]Halvorsen, M. B., Zeddies, D. G., Ellison, W. T., Chicoine, D. R., & Popper, A. N. (2012). Effects of mid-frequency active sonar on hearing in fish. The Journal of the Acoustical Society of America, 131(1), 599–607. https://doi.org/10.1121/1.3664082. In an additional study, catfish and rainbow trout were exposed to mid-frequency active (MFA) sonar signals (maximum received level 210 underwater dB) for 15 seconds. Some catfish, but not rainbow trout, showed temporary hearing loss, but no damage to other tissues[19]Kane, A. S., Song, J., Halvorsen, M. B., Miller, D. L., Salierno, J. D., Wysocki, L. E., Zeddies, D., & Popper, A. N. (2010). Exposure of fish to high-intensity sonar does not induce acute pathology. Journal of Fish Biology, 76(7), 1825–1840. https://doi.org/10.1111/j.1095-8649.2010.02626.x.

It is important to note that even though there was some TTS in the sonar studies, all of the exposures tested were longer and louder than would be encountered by free ranging fish. The scientists concluded that it is not likely that these sonars would do any harm to fishes.

Similarly, in a study to test the effects of exposure to seismic airguns, devices used in geological exploration and search for oil and gas underwater, it was found that there was no damage to the ears of five different species of fish in the MacKenzie River Delta (Canada)[20]Song, J., Mann, D. A., Cott, P. A., Hanna, B. W., & Popper, A. N. (2008). The inner ears of Northern Canadian freshwater fishes following exposure to seismic air gun sounds. The Journal of the Acoustical Society of America, 124(2), 1360–1366. https://doi.org/10.1121/1.2946702, although several species showed TTS that recovered within 18 hours of the exposure. In another seismic study, it was shown that there was no damage to the ears or other body tissues of lake sturgeon and paddlefish exposed to a single blast from an airgun in Lake Sakagawea (North Dakota)[21]Popper, A. N., Smith, M. E., Cott, P. A., Hanna, B. W., MacGillivray, A. O., Austin, M. E., & Mann, D. A. (2005). Effects of exposure to seismic airgun use on hearing of three fish species. The Journal of the Acoustical Society of America, 117(6), 3958–3971. https://doi.org/10.1121/1.1904386

Similarly, in a study to test the effects

Additional Links on DOSITS

Additional Resources

  • Wysocki. (2005). Hearing in Fishes under Noise Conditions. Journal of the Association for Research in Otolaryngology, 6(1), 28. https://doi.org/10.1007/s10162-004-2427-0
  • Popper, A. N., Hawkins, A. D., Fay, R. R., Mann, D., Bartol, S., Carlson, T., … Tavolga, W. N. (2014). Sound exposure guidelines for fishes and sea turtles: ASA S3/SC1.4 TR-2014 ; a technical report prepared by ANSI-accredited Standards Committee S3/SC1 and registered with ANSI. Cham, Switzerland: Springer.
  • Popper, A. N., & Hawkins, A. D. (Eds.). (2012). The effects of noise on aquatic life. New York: Springer.

References

  • Fay, R. R., & Popper, A. N. (2000). Evolution of hearing in vertebrates: the inner ears and processing. Hearing Research, 149(1–2), 1–10. https://doi.org/10.1016/S0378-5955(00)00168-4
  • Halvorsen, M. B., Casper, B. M., Woodley, C. M., Carlson, T. J., & Popper, A. N. (2011). Predicting and mitigating hydroacoustic impacts on fish from pile installations (No. NCHRP Research Results Digest 363, Project 25-28). Washington, D.C.: National Cooperative Highway Research Program, Transportation Research Board,National Academies Press. Retrieved from http://www.trb.org/Publications/Blurbs/166159.aspx<
  • Hastings, M. C., Popper, A. N., Finneran, J. J., & Lanford, P. J. (1996). Effects of low‐frequency underwater sound on hair cells of the inner ear and lateral line of the teleost fish Astronotus ocellatus. The Journal of the Acoustical Society of America, 99(3), 1759–1766. https://doi.org/10.1121/1.414699
  • Le Prell, C. G., Henderson, D., Fay, R. R., & Popper, A. N. (Eds.). (2012). Noise-induced hearing loss: scientific advances. New York, NY: Springer.
  • McCauley, R. D., Fewtrell, J., & Popper, A. N. (2003). High intensity anthropogenic sound damages fish ears. The Journal of the Acoustical Society of America, 113(1), 638–642. https://doi.org/10.1121/1.1527962
  • Popper, A. N., Fewtrell, J., Smith, M. E., & McCauley, R. D. (2003). Anthropogenic Sound: Effects on the Behavior and Physiology of Fishes. Marine Technology Society Journal, 37(4), 35–40. https://doi.org/10.4031/002533203787537050
  • Popper, A. N., & Hastings, M. C. (2009a). The effects of anthropogenic sources of sound on fishes. Journal of Fish Biology, 75(3), 455–489. https://doi.org/10.1111/j.1095-8649.2009.02319.x
  • Popper, A. N., & Hastings, M. C. (2009b). The effects of human-generated sound on fish. Integrative Zoology, 4(1), 43–52. https://doi.org/10.1111/j.1749-4877.2008.00134.x

Cited References

Cited References
1 Popper, A. N., & Hoxter, B. (1984). Growth of a fish ear: 1. Quantitative analysis of hair cell and ganglion cell proliferation. Hearing Research, 15(2), 133–142. https://doi.org/10.1016/0378-5955(84)90044-3
2 Lombarte, A., Yan, H. Y., Popper, A. N., Chang, J. S., & Platt, C. (1993). Damage and regeneration of hair cell ciliary bundles in a fish ear following treatment with gentamicin. Hearing Research, 64(2), 166–174. https://doi.org/10.1016/0378-5955(93)90002-I
3 Lombarte, A., & Popper, A. N. (1994). Quantitative analyses of postembryonic hair cell addition in the otolithic endorgans of the inner ear of the european hake,merluccius merluccius (gadiformes, teleostei). The Journal of Comparative Neurology, 345(3), 419–428. https://doi.org/10.1002/cne.903450308
4 Popper, A. N., Smith, M. E., Cott, P. A., Hanna, B. W., MacGillivray, A. O., Austin, M. E., & Mann, D. A. (2005). Effects of exposure to seismic airgun use on hearing of three fish species. The Journal of the Acoustical Society of America, 117(6), 3958–3971. https://doi.org/10.1121/1.1904386
5, 6, 7, 16 Popper, A. N., Halvorsen, M. B., Kane, A., Miller, D. L., Smith, M. E., Song, J., Stein, P., & Wysocki, L. E. (2007). The effects of high-intensity, low-frequency active sonar on rainbow trout. The Journal of the Acoustical Society of America, 122(1), 623–635. https://doi.org/10.1121/1.2735115
8 Scholik, A. R., & Yan, H. Y. (2002). Effects of boat engine noise on the auditory sensitivity of the fathead minnow, Pimephales promelas. Environmental Biology of Fishes, 63, 203–209. https://doi.org/10.1023/A:1014266531390p
9 Smith, M. E., Kane, A., & Popper, A. N. (2004). Acoustical stress and hearing sensitivity in fishes: Does the linear threshold shift hypothesis hold water? Journal of Experimental Biology, 207(20), 3591–3602. https://doi.org/10.1242/jeb.01188
10 Scholik, A. R., & Yan, H. Y. (2001). Effects of underwater noise on auditory sensitivity of a cyprinid fish. Hearing Research, 152(1–2), 17–24. https://doi.org/10.1016/S0378-5955(00)00213-6
11 Smith, M. E. (2016). Relationship Between Hair Cell Loss and Hearing Loss in Fishes. In A. N. Popper & A. Hawkins (Eds.), The Effects of Noise on Aquatic Life II (Vol. 875, pp. 1067–1074). Springer New York. https://doi.org/10.1007/978-1-4939-2981-8_132
12 Smith, M. E., Kane, A., & Popper, A. N. (2004). Noise-induced stress response and hearing loss in goldfish (Carassius auratus). Journal of Experimental Biology, 207(3), 427–435. https://doi.org/10.1242/jeb.00755
13, 14 Smith, M. E., Coffin, A. B., Miller, D. L., & Popper, A. N. (2006). Anatomical and functional recovery of the goldfish (Carassius auratus) ear following noise exposure. Journal of Experimental Biology, 209(21), 4193–4202. https://doi.org/10.1242/jeb.02490
15 Halvorsen, M. B., Zeddies, D. G., Chicoine, D., & Popper, A. N. (2013). Effects of low-frequency naval sonar exposure on three species of fish. The Journal of the Acoustical Society of America, 134(2), EL205–EL210. https://doi.org/10.1121/1.4812818
17, 18 Halvorsen, M. B., Zeddies, D. G., Ellison, W. T., Chicoine, D. R., & Popper, A. N. (2012). Effects of mid-frequency active sonar on hearing in fish. The Journal of the Acoustical Society of America, 131(1), 599–607. https://doi.org/10.1121/1.3664082
19 Kane, A. S., Song, J., Halvorsen, M. B., Miller, D. L., Salierno, J. D., Wysocki, L. E., Zeddies, D., & Popper, A. N. (2010). Exposure of fish to high-intensity sonar does not induce acute pathology. Journal of Fish Biology, 76(7), 1825–1840. https://doi.org/10.1111/j.1095-8649.2010.02626.x
20 Song, J., Mann, D. A., Cott, P. A., Hanna, B. W., & Popper, A. N. (2008). The inner ears of Northern Canadian freshwater fishes following exposure to seismic air gun sounds. The Journal of the Acoustical Society of America, 124(2), 1360–1366. https://doi.org/10.1121/1.2946702
21 Popper, A. N., Smith, M. E., Cott, P. A., Hanna, B. W., MacGillivray, A. O., Austin, M. E., & Mann, D. A. (2005). Effects of exposure to seismic airgun use on hearing of three fish species. The Journal of the Acoustical Society of America, 117(6), 3958–3971. https://doi.org/10.1121/1.1904386