Effects of Intense Sounds on the Ear of Fishes

Over the past several years there has been considerable interest generated in the impact of human-generated (anthropogenic) sounds on the ears of animals. It is widely known that intense sounds and certain drugs will damage the sensory cells of the ears of mammalian species, and the concern is that similar sounds will impair hearing in wild animals. Related to this is the increase in the presence of anthropogenic sounds in the environment. This has been of particular interest for its impact on marine mammals, where the concern is that human-generated sounds from a variety of underwater activities may impair the survival of a number of species (see NRC 2000).

While the major interest in the impact of anthropogenic sounds in the marine environment concerns mammals, it is now appreciated that these sounds may also impact the lives of fishes and other organisms as well as marine mammals. However, the extent of data on the effects of intense sounds on fishes is only poorly known. At the same time, several results from the Popper lab are germane to the topic.

One of the very few direct studies on the impact of intense sounds on the ear of fishes was done in collaboration between the Popper lab and the lab of Dr. Mardi Hastings at the Ohio State University. In this study (Hastings et al., 1996) we investigated the effect of high intensity on the ears of the oscar, Astronotus oscellatus. We found that sounds that were lower than 180 dB (re 1 µPa) and sounds that were not on continuously had no apparent impact on the sensory cells of the ear. However, when we subjected fish to 180 dB signals 300-Hz pure tones for four continuous hours, and then examined the ears after four days, there was some damage to the sensory cells of the lagena. This is shown in the figure to the right. In this scanning electron micrograph from the lagena, the top figure shows a low power view of the whole macula. The area within the square is shown in the lower SEM. The lower picture shows that there has been some loss of ciliary bundles resulting from the high acoustic stimulation.

While damage was found in a number of specimens, it did not show up unless the animals were allowed to live for several days, suggesting that damage takes a while to be visible. While these data are highly suggestive that damage may result from long-term intense sounds, there are several caveats on these data. First, it is not known if data from this freshwater fish can be extrapolated to other species. Second, how significant is this damage in terms of sound detection, and would damage of this low magnitude impact the survival of a fish? Third, it is important to note that the fish in this study were kept close to the sound source, and it is unlikely that fish in the wild would be exposed to four-hours of continuous sound and stay in the vicinity of the sound for the full time. Another significant question is whether the hair cells that are damaged would regenerate. As we have shown in other studies, sensory cells in the ears of fish do regenerate after treatment with ototoxic drugs, and this might mean that the hair cells in fishes would also regenerate after damage by intense sounds. Thus, while there may be some damage shortly after sound stimulation, will this have a long-term impact on fish? Of course, during the time that damage is present, and before any regeneration, fishes may be at a disadvantage in terms of detecting predators and prey, and so their survival may be impacted.

Another recent study (Smith et al., in review) in the Popper lab examined the relationship between baseline hearing thresholds and noise level on temporary threshold shifts in fish hearing capabilities. It has been well documented in the mammalian literature that temporary threshold shifts reach an asymptote after a specific duration of noise exposure. These asymptotic threshold shifts (ATS) increase linearly with sound intensity. We examined whether this linear threshold shift relationship is valid for other hearing vertebrates (fish and birds).

Specifically, we tested the hypothesis that noise-induced threshold shifts in fish increase linearly with increasing sound pressure levels (SPL) above baseline thresholds (the linear threshold shift or LINTS hypothesis). To test this hypothesis we investigated the effect of intense continuous white noise exposure on the hearing loss of two species that vary considerably in hearing sensitivity- goldfish, Carassius auratus (a hearing specialist), and tilapia, Oreochromis niloticus, (a hearing generalist). The goal was to compare these hearing effects between species to elucidate a potential relationship between hearing sensitivity and susceptibility to acoustic stress.

Goldfish and tilapia were exposed to white noise from 0.1 to 4 kHz at 164-170 dB (re: 1 µPa) for either 0 (control), 7, 21 (for goldfish), or 28 d (for tilapia) in 600-L aquaria. Auditory thresholds were measured using the auditory brainstem response (ABR). This technique is a noninvasive method of measuring the whole brain response to auditory stimuli and is commonly used for measuring hearing in fishes and other vertebrates.

 
  Figure 1. Auditory thresholds of tilapia (left) and goldfish (right) after 7, 21 or 28 days of white noise exposure. ABRs were detectable from 100 to 800 Hz for tilapia. Tilapia exposed for 28 d exhibited an overall treatment effect, but this effect was only significant at 800 Hz (P=0.02). ABRs were detectable up to 4 kHz in goldfish. In contrast to tilapia, goldfish had significant threshold shifts at all frequencies after only 7 d of noise exposure. After 7 d, further noise exposure did not produce greater threshold shifts, suggesting an asymptote had been reached. Thresholds returned to baseline levels after 14 d of recovery from noise exposure.
 
  Figure 2 (left). Relationship between TTS and noise SPL above baseline levels in four fish species (bluegill and tilapia are hearing generalists, minnows and goldfish are hearing specialists). Sunfish and minnow data are from Scholik & Yan 2001, 2002b. A significant linear relationship exists for all species, for hearing specialists alone, but not for hearing generalists alone. Thus, it is unclear if the LINTS hypothesis is valid for only hearing specialist fishes or whether the SPL was simply not great enough for TTS in generalists.

Figure 3 (right). Relationship between TTS and noise SPL above baseline levels in fish, birds, and mammals. Regression relationships were significant for all taxa, with slopes increasing from fish to birds to mammals. Sources of data are provided on a separate table below. Even though different noise-induced TTS researchers utilize different species and methodologies, and stimulate with sound of various characteristics (e.g. frequency, duration, SPL; Table 1), subtracting the species’ baseline hearing threshold from the noise exposure SPL for each experiment standardizes the LINTS relationship and allows easy comparison between species.


Our results show that noise differentially affects two teleost species that differ in hearing sensitivity and also confirms the hypothesis that hearing specialists are more greatly affected by noise exposure than are hearing generalists. While tilapia were minimally affected by 28 d of noise-exposure, goldfish exhibited significant TTS after 7 d of noise-exposure. The difference can be explained by a linear relationship between TTS and SPL above the fish’s baseline threshold. We suggest that the reason that tilapia did not exhibit threshold shifts in response to 170 db re: 1µPa white noise and goldfish did, is that TTS (and perhaps hearing damage) only occurs when noise is a certain SPL above the fish’s baseline. Because baseline thresholds for tilapia are 20-50 dB higher than those of goldfish, one might expect 20-50 dB greater SPLs (190-220 dB re: 1µPa) would be required to produce the same threshold shifts as found in goldfish exposed to 170 db re: 1µPa. This linear threshold shift (LINTS) hypothesis needs to be tested with more teleost species and a broader range of noise SPLs, but may become a useful tool for researchers examining how anthropogenic sounds might affect fishes. Such a linear relationship for teleosts is consistent with results for birds and mammals, but greater underwater SPLs are required to induce a comparable TTS as found in birds and mammals in air.

The LINTS relationship is robust and is predictive on many different levels. On the level of an individual animal, it predicts that, when stimulated with white noise, the threshold shift will be greatest at frequencies where the animal’s baseline hearing threshold is the lowest. Both hearing specialists (goldfish and fathead minnows) had significant LINTS regressions when plotted alone, suggesting that this relationship was true, at least for hearing specialists. Tilapia and bluegill did not exhibit a significant LINTS regression when plotted alone, but this relationship was not testable in these hearing generalists since no TTS occurred at any frequency (except 10 dB shift at 800 Hz for tilapia). On the next higher level of prediction, the LINTS hypothesis predicts that, for a given intensity of sound, more sensitive species will be more prone to TTS than less sensitive species. This was the case in comparing our specialist and generalist teleost species, and in comparing fish with mammals and birds.



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