Tutorial: Fishes – Hearing Loss
Exposure to intense sounds can cause a permanent or temporary hearing loss. Some anthropogenic sounds may cause temporary threshold shift (TTS), depending on a number of variables including the frequency and intensity of the sound, duration of exposure, etc. (see How do you determine if a sound affects a marine animal?). The physiological basis for TTS can involve reversible damage to the hair cells of the inner ear.
Fishes are susceptible to TTS. For example, fathead minnows experienced TTS after exposure to playback of boat engine noise at 142 underwater dB for 2 hours, whereas goldfish exhibited a TTS after exposure to 166-170 underwater dB of white noise for 10 minutes. In both studies, hearing returned to normal, but the length of time required for recovery varied as a function of the frequency of the sound and duration of exposure. It is likely that the actual sound levels needed to produce TTS will vary widely, and even differ by species.
Physical hair cell damage has been observed in several fish species following exposure to intense sounds. Hair cells were lost in goldfish after exposure to white noise at 170 underwater dB for 48·hours and monitored for 8·days after exposure. Scientists found that the hair cell loss was accompanied by TTS. However, after 7 days hearing thresholdsreturned to normal and the damaged hair cells started to be replaced.
In contrast to the effects seen in the above studies, caged rainbow trout, channel catfish, and hybrid sunfish exposed to a US Navy SURTASS LFA sound source (maximum received level of 193 underwater dB) for 324 or 628 seconds did not show exposure-related damage in the inner ear and other tissues, while both rainbow trout and channel catfish (but not the hybrid sunfish, largemouth bass, or yellow perch) showed small TTS for several days after exposure.
Additionally, exposure-related damage was not observed when these fish were exposed to mid-frequency signals (maximum received level 210 underwater dB) for 15 seconds. The duration and level of exposure to sonars in this study were much longer than would be encountered by fish exposed to sonar in the ocean.
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), although several species showed TTS that recovered within 18 hours of the exposure.
Many species, including humans, exposed to sounds longer and louder than those that result in TTS may experience permanent threshold shift (PTS). PTS occurs when hair cells die and are not replaced. In contrast, fishes, including sharks and rays, can replace hair cells lost as a result of exposure to intense sounds or ototoxic drugs. Moreover, fishes add large numbers of hair cells, as well as repair and replace damaged hair cells, throughout life. For example, a small 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. As a consequence of the ability to repair and regenerate hair cells, the likelihood of PTS in fishes is considered to be very low.
Effects of Sound Tutorial Sections:
- Popper, A. N., Halvorsen, M. B., Kane, E., Miller, D. D., Smith, M. E., Song, J. Stein, P., and Wysocki, L. E. 2007, “The effects of high-intensity, low-frequency active sonar on rainbow trout.” J. Acoust. Soc. Am., 122:623-635.
- Scholik, A.R. and 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.
- Smith, M.E., Kane, A.S. and Popper, A.N. 2004, “Acoustical stress and hearing sensitivity in fishes: does the linear threshold shift hypothesis hold water?” Journal of Experimental Biology 207: 3591-3602.
- Scholik, A.R. and Yan, H.Y. 2001, “Effects of underwater noise on auditory sensitivity of a cyprinid fish.”Hearing Research 152: 17-24.
- Smith , M.E., Coffin, A.B., Miller, D.L. and Popper, A.N. 2006, “Anatomical and functional recovery of the goldfish (Carassius auratus) ear following noise exposure.” The Journal of Experimental Biology. 209, 4193-4202.
- Halvorsen, M. B., Zeddies, D. G., Ellison, W. T., Chicoine, D. R., and Popper, A. N. 2012, “Effects of mid-frequency active sonar on fish hearing.” J. Acoust. Soc. Am., 131:599-607. DOI: 10.1121/1.3664082.
- Halvorsen, M. B., Zeddies, D. G., Chicoine, D., and Popper, A. N. 2013, “Effects of low frequency naval sonar exposure on three species of fish.” JASA Express Letters, 134(2), EL206-210.
- Kane, A.S., Song, J., Halvorsen, M.B., Miller,D.L., Salierno, J.D., Wysocki, L.E., Zeddies, D., and Popper, A.N. 2010, “Exposure of fish to high-intensity sonar does not induce acute pathology.” Journal of fish biology. 76, 1825-1840.
- Song, J., Mann, D. A., Cott, P. A., Hanna, B. W., and Popper, A. N. 2008, “The inner ears of northern Canadian freshwater fishes following exposure to seismic air gun sounds.” J. Acoust. Soc. Am., 124: 1360-1366.
- Popper, A.N., Smith, M.E., Cott, P.A., Hanna, B.W., MacGillivray, A.O., Austin, M.E., and Mann, D.A. 2005, “Effects of exposure to seismic airgun use on hearing of three fish species.” Journal of the Acoustical Society of America 117(6): 3958-3971.
- Popper, A.N., and Hoxter, B. 1984, “Growth of a fish ear: 1. Quantitative analysis of sensory hair cell and ganglion cell proliferation.” Hearing Research 15: 133142.
- Lombarte, A., Yan, H.Y., Popper, A.N., Chang, J.C., and Platt, C. 1993, “Damage and regeneration of hair cell ciliary bundles in a fish ear following treatment with gentamicin.” Hearing Research 66: 166-174.
- Lombarte, A., and 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)” Journal of Comparative Neurology 345: 419-428.
- Fay, R.R. and Popper, A.N. 2000, “Evolution of hearing in vertebrates: The inner ears and processing.” Hearing Research 149: 1-10.
- Halvorsen, M.B., Casper, B.M., Woodley, C.M., Carlson, T.J., and Popper, A.N. 2011, “Predicting and mitigating hydroacoustic impacts on fish from pile installations.” NCHRP Research Results Digest 363, Project 25-28, National Cooperative Highway Research Program, Transportation Research Board, National Academy of Sciences, Washington, D.C. (Link)
- Hastings, M.C., Popper, A.N., Finneran, J.J. and 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” Journal of the Acoustical Society of America 99(3): 1759-1766.
- Le Prell, C. G., Henderson, D., Fay, R. R., and Popper, A. N. (eds). 2012, “Noise-Induced Hearing Loss: Scientific Advances.”Springer Science and Business Media, LLC, New York.
- McCauley, R.D., Fewtrell, J. and Popper, A.N. 2003, “High intensity anthropogenic sound damages fish ears.” Journal of the Acoustical Society of America 113(1): 638-642.
- Popper A.N., and Hastings, M.C. 2009, “The effects of anthropogenic sources of sounds on fishes.” Journal of Fish Biology. 25, 455-489.
- Popper, A.N, and Hastings, M.C. 2009, “The effects of human-generated sound on fish.” Integrative Zoology. 4, 43-52.
- Popper, A.N., Fewtrell, J., Smith, M.E. and McCauley, R.D. 2003/04, “Anthropogenic sound: Effects on the behavior and physiology of fishes.” Marine Technology Society Journal 37(4): 35-40.
- Smith, M.E., Kane, A.S. and Popper, A.N. 2004, “Noise-induced stress response and hearing loss in goldfish (Carassius auratus)” Journal of Experimental Biology 207: 427-435.
- Wysocki, L.E. and F. Ladich 2005, “Hearing in fishes under noise conditions.” Journal of the Association for Research Otolaryngology. 6(1): 28-36.
- Popper, A.N., Hawkins, A.D., Fay, R.R., Mann, D., Bartol, S., Carlson, T., Coombs, S., Ellison, W.T., Gentry, R., Halvorsen, M.B., Løkkeborg, S., Rogers, P., Southall, B.L., Zeddies, D., Tavolga, W.N. 2014, “Sound Exposure Guidelines for Fishes and Sea Turtles: A Technical Report prepared by ANSI-Accredited Standards Committee S3/SC1 and registered with ANSI.” ASA S3/SC1.4 TR-2014. Springer and ASA Press, Cham, Switzerland.
- Popper, A. N. and Hawkins, A. (eds). 2012, “The Effects of Noise on Aquatic Life.” Springer Science and Business Media, LLC, New York.