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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.
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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. |
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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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