Criteria for Effects of Anthropogenic Sound on Fishes

Some anthropogenic sounds may affect fishes. These effects may include small changes in behavior that have no long-term consequences, behavioral changes that cause fishes to temporarily or permanently leave feeding or breeding sites or change migration pathways, temporary hearing loss, physiological changes that may affect stress levels, and, with the most intense sounds, result in physical damage to body tissues, or even death [1]Hawkins, A. D., Johnson, C., & Popper, A. N. (2020). How to set sound exposure criteria for fishes. The Journal of the Acoustical Society of America, 147(3), 1762–1777. https://doi.org/10.1121/10.0000907.[2]Popper, A. N., & Hawkins, A. D. (2019). An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes. Journal of Fish Biology, 94(5), 692–713. https://doi.org/10.1111/jfb.13948..

Potential effects of anthropogenic sound on fishes at different distances from the sound source. The actual distances at which different effects might occur depend on the sound level and frequency of the source, the sensitivity of the fish to that signal, and likely many other factors. Note that in the region closest to the source (left), potential effects range from death to behavioral responses, while at the greatest distances (right) behavioral responses may be the only effect. Image credit/copyright: Dr. Arthur Popper.

The actual effects depend on many factors including the type of sound (e.g., shipping noise vs. seismic air gun), the sound level at the fish, and how well the fish hears the sound. While there is considerable concern about sounds that can physically harm fishes, it is clear from recent experiments[3]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. that only the very loudest sounds (see Table 1 below) may potentially cause physical harm or death [4]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: ASA S3/SC1.4 TR-2014 ; a technical report prepared by ANSI-accredited Standards Committee S3/SC1 and registered with ANSI. Springer.[5]Dahl, P. H., Keith Jenkins, A., Casper, B., Kotecki, S. E., Bowman, V., Boerger, C., Dall’Osto, D. R., Babina, M. A., & Popper, A. N. (2020). Physical effects of sound exposure from underwater explosions on Pacific sardines ( Sardinops sagax ). The Journal of the Acoustical Society of America, 147(4), 2383–2395. https://doi.org/10.1121/10.0001064.[6]Jenkins, A. K., Dahl, P. H., Kotecki, S. E., Bowman, V., Casper, B., Boerger, C., & Popper, A. N. (2022). Physical effects of sound exposure from underwater explosions on Pacific mackerel ( Scomber japonicus ): Effects on non-auditory tissues. The Journal of the Acoustical Society of America, 151(6), 3947–3956. https://doi.org/10.1121/10.0011587.. Of far greater likelihood are potential effects on behavior and hearing since they may occur over greater distances from the source.

Criteria Setting

As a result of the concerns about potential effects of anthropogenic sound on fishes, regulators and scientists have been working to develop criteria for sound levels that might result in potential effects[7]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: ASA S3/SC1.4 TR-2014 ; a technical report prepared by ANSI-accredited Standards Committee S3/SC1 and registered with ANSI. Springer. (Table 1).  The most important concern for regulators is that any criteria must be based on the “best available science.”  A challenge in meeting this need is the high diversity of species, anatomy, hearing ability, and behavioral responses of fishes.

In 2014, a committee of scientists and regulators from around the world developed a set of interim criteria for potential effects of sound on fishes. The committee decided to develop different interim criteria for fishes grouped by their hearing ability, rather than develop one set of criteria or develop different criteria for every fish species. It also decided to define criteria for a few representative sources, such as pile driving and shipping, since impacts may be different for continuous vs. impulsive sound. The committee also selected representative effects for which to set criteria (see Table 1 above)[8]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: ASA S3/SC1.4 TR-2014 ; a technical report prepared by ANSI-accredited Standards Committee S3/SC1 and registered with ANSI. Springer.

Table 1 gives an idea of the criteria levels for sounds received by the fish (not at the source, since fishes may be at different distances) for different types of sounds. In cases where there were data, specific criteria were identified. Where there were insufficient data, the committee proposed qualitative distances (near (N), intermediate (I), and far(F)) at which effects might occur.

Criteria for Effects on Behavior

While potential physical effects are important, the likelihood of a behavioral effect is much greater than that of a physical effect. Consequently, there is great interest in developing criteria for behavior. This is a challenge because it is often difficult to observe fish behavior in the wild, especially for pelagic species, such as Atlantic cod and tuna. Behavioral responses of fishes in tanks are not generally sufficient, since animals do not behave in the same way in enclosures as they do in the wild.

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. (Eds.). (2012). The effects of noise on aquatic life. 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 (NCHRP Research Results Digest 363, Project 25-28). National Cooperative Highway Research Program, Transportation Research Board,National Academies Press. http://www.trb.org/Publications/Blurbs/166159.aspx.
  • 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.
  • 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 Astronotusocellatus. The Journal of the Acoustical Society of America, 99(3), 1759–1766. https://doi.org/10.1121/1.414699.
  • 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.
  • Le Prell, C. G., Henderson, D., Fay, R. R., & Popper, A. N. (Eds.). (2012). Noise-induced hearing loss: Scientific advances. Springer.
  • 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.
  • 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.
  • 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., 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.
  • Popper, A. N., & Hastings, M. C. (2009). 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. (2009). 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.
  • Popper, A. N., Hice-Dunton, L., Jenkins, E., Higgs, D. M., Krebs, J., Mooney, A., Rice, A., Roberts, L., Thomsen, F., Vigness-Raposa, K., Zeddies, D., & Williams, K. A. (2022). Offshore wind energy development: Research priorities for sound and vibration effects on fishes and aquatic invertebrates. The Journal of the Acoustical Society of America, 151(1), 205–215. https://doi.org/10.1121/10.0009237.
  • 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.
  • 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.
  • 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.
  • 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:1014266531390.
  • 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.
  • 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.
  • 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.
  • 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.

Cited References

Cited References
1 Hawkins, A. D., Johnson, C., & Popper, A. N. (2020). How to set sound exposure criteria for fishes. The Journal of the Acoustical Society of America, 147(3), 1762–1777. https://doi.org/10.1121/10.0000907.
2 Popper, A. N., & Hawkins, A. D. (2019). An overview of fish bioacoustics and the impacts of anthropogenic sounds on fishes. Journal of Fish Biology, 94(5), 692–713. https://doi.org/10.1111/jfb.13948.
3 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.
4, 7, 8 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: ASA S3/SC1.4 TR-2014 ; a technical report prepared by ANSI-accredited Standards Committee S3/SC1 and registered with ANSI. Springer.
5 Dahl, P. H., Keith Jenkins, A., Casper, B., Kotecki, S. E., Bowman, V., Boerger, C., Dall’Osto, D. R., Babina, M. A., & Popper, A. N. (2020). Physical effects of sound exposure from underwater explosions on Pacific sardines ( Sardinops sagax ). The Journal of the Acoustical Society of America, 147(4), 2383–2395. https://doi.org/10.1121/10.0001064.
6 Jenkins, A. K., Dahl, P. H., Kotecki, S. E., Bowman, V., Casper, B., Boerger, C., & Popper, A. N. (2022). Physical effects of sound exposure from underwater explosions on Pacific mackerel ( Scomber japonicus ): Effects on non-auditory tissues. The Journal of the Acoustical Society of America, 151(6), 3947–3956. https://doi.org/10.1121/10.0011587.