Acoustical stress and hearing sensitivity in fishes: does the linear threshold shift hypothesis hold water?
1 Department of Biology and Center for Comparative and Evolutionary Biology
of Hearing, University of Maryland, College Park, MD 20742, USA
2 Aquatic Pathobiology Program, Department of Veterinary Medicine,
University of Maryland, College Park, MD 20742, USA
3 Neuroscience and Cognitive Science Program, University of Maryland,
College Park, MD 20742, USA
* Author for correspondence (e-mail: mesmith{at}umd.edu)
Accepted 12 July 2004
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Summary |
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Key words: threshold shift, hearing, fish, noise, LINTS, auditory brainstem response, Carassius auratus, Oreochromis niloticus
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Introduction |
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Sounds that are well above those to which an animal is normally exposed are
known to cause temporary changes in hearing capabilities of fishes [i.e.
temporary threshold shifts (TTS); Popper
and Clarke, 1976; Scholik and
Yan, 2001
]. Even louder sounds, or longer exposure to somewhat
quieter sounds, produce damage to the sensory cells of fish ears, as evidenced
in the few fish species that have been studied, and this may lead to permanent
loss of hearing (i.e. permanent threshold shifts;
Enger, 1981
;
Hastings et al., 1996
;
McCauley et al., 2003
). In
addition to causing inner ear damage, high levels of background sound may
create physiological and behavioral stress responses in fishes similar to
those found in mammals (Smith et al.,
2004
).
Mammalian models have long been used to understand the effects of noise on
humans. The results of past studies using mammals show that TTS (noise-exposed
threshold minus control threshold) increase with duration of noise exposure
until an asymptotic threshold shift (ATS) is reached
(Clark, 1991). Once the ATS is
reached for a given sound pressure level (SPL), further noise exposure no
longer increases TTS. The magnitude of the ATS depends upon the SPL of the
exposure noise and increases linearly with SPL above a minimal threshold shift
(Carder and Miller, 1972
).
Although loud sounds were known to induce hearing threshold shifts in
fishes (Scholik and Yan, 2001;
Amoser and Ladich, 2003
;
Smith et al., 2004
), it was
unknown whether fishes exhibit linear threshold shifts with increased SPL, as
is found in mammals. Since water is a far more dense medium for sound
conduction than air, and since the mechanism of hearing in fishes is very
different from that of mammals, it is not intuitive that the relationship
between SPL and TTS in fishes would be the same as that for aerial hearing of
mammals.
In the present study, we tested the hypothesis that noise-induced threshold
shifts in fishes increase linearly with increasing sound pressure differences
(SPD) between the exposure noise and baseline hearing thresholds (referred to
here as the linear threshold shift hypothesis or LINTS hypothesis). To test
this hypothesis, we investigated the effect of intense, continuous white noise
exposure on hearing loss in fish utilizing the auditory brainstem response
(ABR) technique (Corwin et al.,
1982; Kenyon et al.,
1998
). Two species of fish that differ considerably in hearing
sensitivity served as models: goldfish (Carassius auratus; a hearing
specialist) and tilapia (Oreochromis niloticus; a hearing
generalist). The goal was to compare alterations in hearing between species to
elucidate a potential relationship between hearing sensitivity and
susceptibility to acoustic stress.
Although there is a broad continuum in hearing capabilities among various
fish taxa, the terms `hearing specialist' and `hearing generalist' (with
hearing `non-specialist' used as a synonym) are commonly used to describe the
opposite extremes of this continuum. We chose goldfish as a representative
hearing specialist because of their excellent hearing sensitivity and the
considerable data in the literature about their hearing (see
Fay and Popper, 1974;
Fay, 1988
;
Popper et al., 2003
). Goldfish
are otophysan fishes and therefore possess Weberian ossicles (modified
cervical vertebrae that abut the ear; von
Frisch, 1938
) that allow sound pressure waves impinging upon the
swim bladder to be carried directly to the ear, leading to sensitive hearing
(wide-frequency range and relatively low thresholds).
Tilapia, a cichlid, have relatively poor hearing. They have no accessory
structures connecting the swim bladder to the ear, and sound travels through
the ear via bone conduction (Fay
and Popper, 1975). Hearing sensitivity has previously been
characterized for only three other cichlid species African
mouthbreeder (Tilapia macrocephala), oscar (Astronotus
ocellatus) and African cichlid (Tramitichromis intermedius).
Audiograms for these species show that, compared with goldfish, they hear a
smaller bandwidth and at higher thresholds
(Tavolga, 1974
;
Kenyon et al., 1998
;
Ripley et al., 2002
).
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Materials and methods |
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White noise exposure
Fish were exposed to white noise with a bandwidth from 0.1 to 10 kHz. The
sound was generated using a Sony MiniDisc player connected through an
amplifier (5.2 Amonoblock; AudioSource, Portland, OR, USA) to an underwater
speaker (UW-30; Underwater Sound, Inc., Oklahoma City, OK, USA) placed
centrally on the bottom of the aquarium. White noise, defined as having a flat
power spectrum across the entire bandwidth (i.e. all frequencies are presented
at the same SPL), was computer-generated using Igor Pro software (WaveMetrics,
Inc., Lake Oswego, OR, USA). Characteristics of the noise exposure (bandwidth
and SPL) were similar in both short- and long-term noise exposure experiments,
with transduction in the tanks having little effect on the digitally generated
flat, `white noise' spectra (Fig.
1; Smith et al.,
2004). For Experiment 1, 24 h noise exposures were presented at
overall SPLs of either 110 (ambient control), 130, 140 or 160 dB re 1 µPa
to goldfish. These overall SPLs are equivalent to power spectral densities of
approximately 80, 90, 97, 118 and 122 dB re 1 µPa2/Hz, which
were measured using a Brüel and Kjar (Nærum, Denmark) 8103
hydrophone and Type 4223 hydrophone calibrator. Additional 24-h exposure data
from a previous goldfish study (Smith et
al., 2004
) that used a SPL of 170 dB re 1 µPa (124 dB re 1
µPa2/Hz) were compared with the other three SPLs of Experiment
1. For simplicity, in describing the noise to which fish were exposed in the
remainder of this paper, SPL will be given in terms of overall dB re 1 µPa,
instead of the associated power spectral density.
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For Experiment 2, long-term noise exposures of 164170 dB re 1 µPa
were presented to goldfish and tilapia for either 7 days or 2128 days.
Goldfish were exposed for 21 days, while tilapia were exposed for 28 days
because goldfish reach an ATS by 1 day
(Smith et al., 2004). Once we
established that there was no difference in ATS for goldfish between days 1
and 21, we terminated the goldfish exposure early (i.e. no differences in TTS
between 21- and 28-day noise-exposed goldfish expected) in order to return the
fish to a quiet and less stressful environment.
In the short-term experiments, the SPL of the noise exposure varied within the bucket from 170 dB re 1 µPa 1 cm directly above the speaker to 166169 dB re 1 µPa at 814 cm above the speaker. The SPL of the noise exposure in the long-term experiments varied slightly within an aquarium, with a maximum (170 dB re 1 µPa) directly above the underwater speaker and minimum (161168 dB re 1 µPa) near the sides of the aquarium furthest from the speaker. The SPL of the control aquarium ranged from 110 to 125 dB re 1 µPa.
Although control and noise-exposed aquaria were in the same room in the
short-term experiments, the SPL of the control aquaria did not change when the
underwater speaker was turned on in the noise-exposed aquaria. Due to the 40
dB loss of sound energy at the airwater interface
(Parvulescu, 1964), relatively
little sound was heard outside of the noise tanks and none of this energy got
into the water of the other tanks in the room. Minor differences, however, may
have occurred between the short- and long-term experiments because of the
smaller volumes of the aquaria and buckets used in the short-term experiment
(i.e. closer proximity between the fish and the underwater speaker compared
with the large long-term aquaria).
Auditory brainstem response (ABR) technique
Hearing thresholds of the experimental fishes were measured on each
specified day of noise exposure (N=56 for controls and
noise-exposed fish for each exposure group) using the auditory brainstem
response (ABR). This technique is a non-invasive method of measuring the
neural activity of the brainstem in response to auditory stimuli and is
commonly used for measuring hearing in fishes and other vertebrates
(Corwin et al., 1982;
Kenyon et al., 1998
). Each
fish was restrained in a mesh sling and suspended underwater in a 19-liter
plastic vessel. The fish was suspended so that the top of the head was
approximately 3 cm below the surface of the water and 25 cm above the
underwater speaker.
A reference electrode was inserted subdermally into the medial dorsal surface of the head between the anterior portion of the eyes while a recording electrode was placed into the dorsal midline surface of the fish approximately halfway between the anterior insertion of the dorsal fin and the posterior edge of the operculae, directly over the brainstem. A ground electrode was placed in the water near the body of the fish.
Sound stimuli were presented and ABR waveforms were collected using a TDT
physiology apparatus using SigGen and BioSig software (Tucker-Davis
Technologies, Inc., Gainesville, FL, USA). Sounds were computer generated
via TDT software and passed through a power amplifier connected to
the underwater speaker. Tone bursts had a 2 ms rise and fall time, were 10 ms
in total duration and were gated through a Hanning window (similar to the
conditions of other ABR studies; e.g. Mann
et al., 2001; Higgs et al.,
2001
). Responses to each tone burst at each SPL were collected
using the BioSig software package, with 400 responses averaged for each
presentation. The SPLs of each presented frequency were confirmed using a
calibrated underwater hydrophone (calibration sensitivity of 195 dB re
1 V/µPa; ±3 dB, 0.0210 kHz, omnidirectional; model 902;
Interocean Systems, Inc., San Diego, CA, USA). Auditory thresholds were
determined by visual inspection of ABRs, as has been done in previous studies.
Additional details of this ABR protocol have been previously published
(Higgs et al., 2001
).
Statistical analysis
For Experiment 1, the effects of noise exposure SPL on fish auditory
threshold levels were tested using analysis of variance (ANOVA) with SPL and
frequency as factors. Tukey's post-hoc test was used to make pairwise
comparisons between specific frequencies when significant main effects were
found (Zar, 1984). In
Experiment 1, regression analysis was used to test for relationships between
noise exposure SPL and the resulting TTS. The threshold shifts were labeled
temporary because goldfish exposed to 170 dB re 1 µPa white noise for 21
days recovered to control hearing levels within two weeks post-noise exposure
(data presented in Smith et al.,
2004
). For this analysis, mean TTS for each SPL was averaged
across five frequencies (400, 600, 800, 1000 and 2000 Hz), so that each point
was calculated using 30 thresholds (N=6 fish x 5 frequencies).
While TTS data for SPLs of 130, 140 and 160 dB re 1 µPa came from
Experiment 1, the raw data for mean TTS at an SPL of 170 dB re 1 µPa are
presented elsewhere (Smith et al.,
2004
).
Regression analysis was also used to test for relationships between SPD (in dB) between the exposure noise and baseline auditory thresholds and TTS in goldfish. Using SPD from baseline auditory thresholds instead of absolute SPL is similar to A-weighting, or measuring perceived sound levels (loudness) in human hearing studies. This relationship between noise SPD from baseline thresholds and TTS is referred to as the LINTS (linear threshold shift) relationship throughout this paper. In these analyses, each data point represents a TTS at a specific frequency, and the variability in the SPD above baseline threshold is due to differences in baseline thresholds across frequencies and not necessarily absolute experimental noise SPL. Analysis of covariance (ANCOVA) was used to examine the effects of frequency on TTS, with SPD above baseline thresholds as the covariate. Before ANCOVA was used, we tested for homogeneity of slopes of the separate regressions for each frequency using ANOVA with SPL, frequency and the interaction between the two factors. An insignificant interaction meant that the assumption of homogeneity of slopes could not be rejected. A similar analysis was used to test for differences in slopes between different SPL.
For Experiment 2, the effects of long-term noise exposure on goldfish and tilapia auditory threshold levels were tested using separate ANOVAs for each exposure duration, with treatment (control or noise exposed) and frequency as factors. Regression analysis was used to test for relationships between SPD from baseline auditory thresholds and TTS using data from Experiment 2 and published data for three other fish species (see Table 1). Separate and pooled regressions were done for hearing generalist and specialist fishes. Regression analysis was also used to examine the LINTS relationship in birds and mammals using published data (Table 1).
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Results |
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There was a statistically significant linear relationship (r2=0.98) between mean TTS (averaged across frequencies) and the SPL of the noise exposure (Fig. 3). The mean TTS was approximately 7 dB for a noise level of 130 dB re 1 µPa and 32 dB at a noise level of 170 dB re 1 µPa. When the mean TTS values at each frequency (instead of the values averaged across frequencies as in Fig. 3) were plotted against the SPD between the noise and baseline hearing thresholds, similar linear relationships were evident (Fig. 4A). When a separate linear regression analysis was done with each of the eight frequencies tested, all had a significantly linear relationship (P<0.0001) that did not significantly differ in slope from one another (P=0.39) but did differ in TTS after accounting for SPD from baseline levels as the covariate (P<0.0001; Fig. 4A).
When separate regression analyses were done with each of the four SPLs tested across frequencies, all had a significantly linear relationship (P<0.02; Fig. 4B). There were significant differences in the slopes of these relationships, with slopes for 130 and 170 dB being slightly lower than those of 140 and 160 dB (P<0.01; Fig. 4B). LINTS relationships were more predictive when separated by frequency (Fig. 4A) than by SPL (Fig. 4B), with r2 (coefficient of determination) values ranging from 0.50 to 0.82 and 0.14 to 0.48, respectively.
As mentioned above, TTS varied significantly with frequency. When TTS was plotted against frequency and compared with baseline audiograms, an inverse relationship between baseline thresholds and TTS was evident (Fig. 5); i.e. at frequencies at which goldfish had lower thresholds and more sensitive hearing, TTS produced by constant white noise was generally the greatest, so that the audiogram and TTS curves mirror each other. This mirrored image is not a perfect reflection though, with the greatest TTS occurring at 800 and 1000 Hz whereas goldfish are most sensitive at hearing frequencies of 400 and 600 Hz.
In Experiment 2, distinguishable ABRs were detectable from 100 to 800 Hz for tilapia, with auditory thresholds ranging from 90 to 130 dB re 1 µPa (Fig. 6A). Tilapia exposed to white noise for 7 days did not exhibit auditory thresholds that were significantly different from controls. Tilapia exposed for 28 days did exhibit an overall treatment effect, but this effect was only significant at 800 Hz (P=0.02), where noise-exposed tilapia had thresholds approximately 10 dB higher than controls.
Goldfish, as expected based upon the literature and other studies in our laboratory, had a much broader bandwidth of auditory sensitivity (as described above), with ABRs detectable up to 4 kHz and baseline auditory thresholds ranging between 60 and 120 dB re 1 µPa (Fig. 6B). After 7 days of noise exposure, goldfish had significant threshold shifts that were up to 25 dB higher than baseline levels. Temporary threshold shifts (TTS) occurred at all frequencies examined (P<0.05; Fig. 6B). Two additional weeks of noise exposure (21 days) did not significantly increase the threshold shift. Differences in the effects of constant noise on the auditory thresholds between goldfish and tilapia were notable (Fig. 6). While significant differences between 28-day noise-exposed and control tilapia were small and found at only one frequency, goldfish exhibited considerable threshold shifts after only 7 days of noise exposure.
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Discussion |
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Our experiments are the first to examine the effects of multiple SPLs on
hearing thresholds in fish, and the data show that there is a predictable
relationship between TTS and SPL in goldfish exposed to white noise
(Fig. 3). A previous goldfish
study showed that this TTS is at ATS after 24 h of noise exposure and that
noise exposures of durations greater than 24 h did not show greater TTS
(Smith et al., 2004).
In order to account for frequency-specific TTS, we plotted TTS against the difference between the noise sound pressure and baseline hearing thresholds at specific frequencies (the LINTS relationship; Fig. 7), instead of plotting TTS by absolute SPL as in Fig. 3. Thus, it was possible to focus on the relationship between SPL and TTS alone. The linear relationship between SPD between the noise and baseline thresholds and TTS was significant and similar (i.e. homogeneous slopes) for all the frequencies tested (Fig. 4). Thus, this relationship seems robust for all frequencies within the range of fish hearing.
Another advantage of using the LINTS relationship instead of absolute noise exposure SPL is that even though different studies utilize different species and methodologies and stimulate with sounds of various characteristics (e.g. frequency and SPL; Table 1), the LINTS relationship minimizes these differences and fosters species-wise comparisons. For example, subtracting the baseline hearing threshold from the noise exposure SPL for a particular experiment and/or species standardizes the LINTS relationship so that data from different laboratories and experiments can be compared. Since the LINTS relationship plots SPD (for both TTS and SPD above baseline levels), inter-laboratory differences in absolute SPL calibration of acoustic equipment become less important.
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 baseline hearing threshold is the most sensitive. This
relationship for goldfish is shown in Fig.
5, where the lowest TTS was exhibited where the baseline threshold
was the highest (i.e. 4000 Hz) and the highest TTS was exhibited at
frequencies where the baseline was lowest (i.e. 800 and 1000 Hz). Although
Fig. 5 shows that TTS generally
mirrors the baseline hearing thresholds of goldfish, it is unclear why this
mirrored image is shifted slightly to the right. For example, although
baseline hearing thresholds increase considerably from 1 to 2 kHz, a
corresponding decrease in TTS does not occur between 1 and 2 kHz, but does
between 2 and 4 kHz. One potential explanation for this is the asymmetry of
auditory filters. Both psychophysical and physiological tuning curves of
goldfish are V-shaped, with steep slopes on the right, higher-frequency side
and more gradual slopes on the left, lower-frequency side of the best
frequency (Fay et al., 1978;
Fay and Ream, 1986
). Since
these tuning curves are skewed to the right, this asymmetry may produce
greater TTS on the right side of a frequency being tested. A similar
phenomenon occurs in masking patterns, where, at high intensities of
narrow-band noise maskers, levels of masking are greater to the right of the
center of the noise band (Egan and Hake,
1950
). The frequency specificity of goldfish TTS suggests that
fish may have multiple, narrow-band detection channels that are tuned to
detect specific frequency bandwidths. In support of this hypothesis, the data
from Scholik and Yan (2002a
)
show that fathead minnows (Promelas pimephales) exposed to boat motor
noise with a peak frequency at 1.3 kHz had significant hearing threshold
shifts only at frequencies near the peak noise frequency (1.0, 1.5 and 2.0
kHz), with the greatest TTS occurring at 1.5 kHz. Similarly, the masking
effects of tones in goldfish were greatest at or near the frequency of the
tone (Tavolga, 1974
).
Fish audiograms are generally U-shaped, with higher thresholds at low and
high frequencies and lower thresholds at intermediate frequencies
(Fay, 1988). As a result, the
SPD between a flat spectrum white noise and a baseline threshold of a fish
differs across frequencies and is greatest where hearing sensitivity is the
best. This further suggests that the degree of effect of the noise may not be
uniform for all frequencies, as seems to be the case, at least for LINTS
relationships for hearing specialists. Thus, noise-induced TTS in fish, as
well as sound detection, may be mediated by an auditory filter bank with
multiple peripheral detection filters (i.e. hypothetical detection channels)
operating at each frequency or span of frequencies, with the effects of the
background noise varying across filters.
If noise-induced TTS were mediated by a single wideband filter, one would
expect TTS to be constant across frequencies, which is not the case for the
data presented here. It is interesting to note that in cod and goldfish,
calculated effective bandwidths of auditory filters increase with frequency
(Fay and Megela Simmons,
1999). In the presence of white noise, larger filter bandwidths
would allow more acoustic energy through to the rest of the auditory system.
This would presumably produce greater TTS at higher frequencies, which is not
what we found, especially at 4000 Hz where TTS was minimal
(Fig. 5). While it is beyond
the results reported here to suggest specific filter mechanisms, future
investigations are needed to examine the relationship between filter
characteristics and TTS in fishes.
The issue of auditory filters in the fish auditory system is quite complex
since filtering can occur at multiple levels in the auditory pathway, both
peripherally and centrally. Although data are available for very few species,
it is known that some species of fish can discriminate between frequencies (as
little as 3% from a given pitch; Dijkgraaf
and Verheijen, 1950; Fay,
1970
), although it is still a matter of debate whether frequency
discrimination is largely controlled by the peripheral or central auditory
system (Enger, 1981
). At the
most peripheral level, mechanical properties of the otoliths and, in the case
of hearing specialists, the swim bladder and Weberian ossicles are likely to
be frequency dependent (Sand and Hawkins,
1973
; Sand and Michelsen,
1978
). At the level of the sensory epithelia, the goldfish saccule
is crudely tonotopically organized, with higher center frequency afferents
originating from the rostral region, while lower center frequency afferents
originate from the caudal region (Furukawa
and Ishii, 1967
). Similarly, the saccular epithelia of the cod
Gadus morhua may also be tonotopically organized. When exposed to an
intense 350-Hz tone, most of the hair cells damaged occurred in the rostral
region of the saccule but, after similar exposure to a 50-Hz tone, most of the
damaged hair cells occurred in the caudal region
(Enger, 1981
).
To date, the only data relating to filters in the primary auditory
afferents of fishes suggest very broad tuning, and just a few filters, across
the hearing bandwidth (Furukawa and Ishii,
1967; Fay, 1974
,
1978
,
1981
). Fay and Ream
(1986
) reported four
non-overlapping categories of saccular nerve fibers (untuned, low-frequency,
mid-frequency and high-frequency) in the goldfish, with the degree of tuning
remaining fairly constant across the goldfish hearing range. Although varying
degrees of spontaneous activity and tuning can be found in the goldfish
saccular afferents, birds and mammals show a more continuous distribution of
fibers with a trend of increased tuning with greater frequencies. This
suggests that the overall level of tuning is greater in other vertebrates
compared with goldfish.
Using reverse correlation analysis to examine filter shapes of afferent
impulse responses, Fay (1997)
found that goldfish filter functions could be classified into two groups; low-
and high-characteristic frequency filters. Both of these groups had similar
characteristics that may reflect hair cell membrane properties, while it was
suggested that differences in the groups were due to differences in hair cell
bundle stiffness and mode of attachment to the otolithic membrane. It is
possible that the characteristics of these two broad filters are responsible
for the frequency dependency of noise-induced TTS in goldfish. The low- and
high-frequency filters have impulse responses that have roll-offs below 200 Hz
and above 1000 Hz, respectively. Similarly, we report TTS that was slightly
lower at 100 and 200 Hz and above 2000 Hz, but TTS was similar at intermediate
frequencies.
Although it is clear that some broad-frequency selectivity can occur at the
level of the auditory periphery (hair cells and their associated primary
afferent neurons), higher order central processing, such as phase-locking in
auditory medullary units (Feng and
Schellart, 1999), is probably necessary to produce the precise
frequency discrimination and narrow critical bands evident from psychophysical
tuning curves of fishes (Hawkins and
Chapman, 1975
; Hawkins and
Johnstone, 1978
). Critical bands are defined as the frequency span
of noise that effectively masks a pure tone stimulus
(Fletcher, 1940
). There is
evidence that narrow critical bands are associated with a wider total
bandwidth and more acute hearing. For example, steep-sided masking functions
are found in goldfish, a hearing specialist
(Tavolga, 1974
), while broader
functions are found in the hearing generalists cod and salmon
(Hawkins and Chapman, 1975
;
Hawkins and Johnstone, 1978
).
These differences in critical bandwidths between hearing specialists and
generalists may be associated with the differential TTS effect of noise
exposure that we found between these two groups of fishes.
LINTS hypothesis in relation to different fish species
Our goldfish audiograms were similar to those published in which
psychophysical/behavioral methods were utilized
(Fay, 1988), with a broad
bandwidth (1004000 Hz) and the most sensitive hearing occurring between
400800 Hz. Tilapia had auditory thresholds that are
3050 dB higher than those of goldfish. They had a small bandwidth of
sensitivity, with ABRs only detectable up to 800 Hz. The absolute auditory
thresholds and the 3050 dB difference between goldfish and tilapia
baseline audiograms found in this study are consistent with previous
comparisons using psychophysical methods
(Tavolga, 1974
). Audiograms
for two other tilapia species, T. macrocephala and T.
intermedius, were similar to our audiograms for O. niloticus,
with a small bandwidth (100800 Hz) and relatively high thresholds
(90135 dB re 1 µPa; Tavolga,
1974
; Ripley et al.,
2002
). The oscar, Astronotus ocellatus, also had
similarly high thresholds but a broader bandwidth (1002000 Hz;
Kenyon et al., 1998
).
Exposure to intense white noise had little effect on tilapia, except that
noise-exposed tilapia had significantly higher thresholds at 800 Hz than
controls. It is unclear why this threshold shift only occurred at 800 Hz but
it is possible that tilapia respond to particle velocity at lower frequencies
but are able to detect sound pressure at 800 Hz. Future experiments are needed
to examine which components of sound (particle motion or pressure) tilapia are
sensitive to over their bandwidth of hearing. Bluegill sunfish (Lepomis
macrochirus), another generalist hearing fish, exhibited a slight, but
not statistically significant, threshold shift after 24 h of white noise
exposure (142 dB re 1 µPa; Scholik and
Yan, 2002b). By contrast, noise exposure produced considerable
threshold shifts (up to 25 dB) in goldfish, but with shifts being greatest
where their hearing sensitivity is greatest (4001000 Hz). Similarly,
the fathead minnow (Pimephales promelas), another hearing specialist,
exhibited approximately 1015 and 20 dB threshold shifts at its most
sensitive auditory frequencies in response to 24 h of white noise exposure and
2 h of boat motor noise with a peak frequency near 1.3 kHz (both 142 dB re 1
µPa), respectively (Scholik and Yan,
2001
,
2002a
).
The LINTS hypothesis predicts that, for a given intensity of sound, more
sensitive species will be more prone to TTS than less sensitive species. The
difference in the effects of noise exposure between goldfish and tilapia is
probably due to the relationship between the noise SPL and the varying
baseline auditory thresholds between the two species. To test this hypothesis,
the TTS at each frequency was plotted against the difference between the noise
SPL and the SPL of the baseline audiogram for goldfish and tilapia (present
study) and for bluegill sunfish and fathead minnow (from Scholik and Yan,
2001,
2002b
), goldfish and the
catfish Pimelodus pictus (Amoser
and Ladich, 2003
).
With all five species, the resulting linear relationship between TTS and SPD above baseline threshold is TTS=0.23(SPD)2.44 (r2=0.62, P<0.0001; Fig. 7). A separate regression was done with hearing specialists only (goldfish, fathead minnows and catfish) since the hearing generalist species (bluegill and tilapia) did not exhibit significant TTS (except for a 10 dB shift at 800 Hz observed in tilapia). This regression was also significantly linear [TTS=0.24(SPL)3.17; r2=0.53, P<0.0001]. Mean TTS increased from fathead minnow to catfish to goldfish (all hearing specialists), which also corresponded with increasing experimental noise exposure SPLs of 142, 159 and 170 dB re 1 µPa, respectively (Table 1). All individual hearing specialist species had a significant regression relationship (P<0.05), while generalist species did not and could not be properly evaluated since TTS did not occur.
Experiments with higher noise levels will be needed to ascertain whether the LINTS relationship is valid for hearing generalists. At 60 dB above the baseline threshold for tilapia, the linear relationship obtained using the other four species predicts that tilapia would exhibit a mean TTS of approximately 11 dB. It is interesting to note, however, that at the one frequency at which a significant TTS occurred (800 Hz) in tilapia, the threshold shift was approximately 10 dB, i.e. near the predicted value (Fig. 7).
A possible reason why tilapia did not exhibit threshold shifts in response
to 170 dB re 1 µPa white noise, whereas goldfish did, is that a certain SPD
above a baseline threshold must be reached before hearing loss occurs. Because
baseline thresholds for tilapia are 2050 dB higher than those of
goldfish, one might predict that a 2050 dB greater SPL (i.e.
190220 dB re 1 µPa) will be required to produce the same threshold
shifts as found in goldfish exposed to 170 dB re 1 µPa. Anthropogenic sound
sources such as some SONARS and seismic air gun arrays produce sound levels of
such intensities close to the source (NRC,
2000). Such SPLs would be difficult and dangerous to achieve in
the laboratory, but higher SPLs than those tested here are needed to examine
whether the LINTS relationship is only valid with hearing specialist fish or
whether, given sufficient noise SPL, hearing generalists, or even
intermediate-hearing species, will also exhibit a similar TTS.
In the LINTS relationships for fish species shown in Fig. 7, within-species variance in SPD from baseline thresholds is only due to the shape of the audiogram for each species since each was only exposed to one experimental SPL. This supports the view that fish are more prone to hearing loss at frequencies where they are most sensitive. All hearing specialists (goldfish, fathead minnows and catfish) had significant LINTS regressions when plotted individually, suggesting that this relationship is valid, at least for hearing specialists.
The prediction that better hearing species will be more prone to TTS from a
specific noise SPL than poor hearing species also holds for birds. Canaries
(Serinus canaria) and zebrafinches (Taenopyga guttata) were
less sensitive to noise-induced basilar papillae damage and threshold shifts
than more sensitive species such as quail (Coturnix coturnix
japonica) and budgerigars (Melopsittacus undulates;
Ryals et al., 1999).
The LINTS hypothesis in relation to different taxa
To compare LINTS relationships between hearing specialist fish and other
taxa, regression analysis was also done using published data for birds and
mammals (Table 1;
Fig. 8).Despite differences in
experimental protocols used in the previously published studies, all
vertebrate taxa for which there are sufficient hearing studies showed
significant linear relationships between the noise SPD above baseline hearing
thresholds and the resulting threshold shift (P<0.001). The slope
of this relationship was greatest for mammals, intermediate for birds and
least for fishes. On this multi-taxon level, the LINTS hypothesis predicts
that, for a given noise SPL, taxa with more sensitive hearing will be more
likely to exhibit noise-induced threshold shifts than less sensitive taxa.
This seems to be the case for mammals, birds and fishes, with TTS being
greatest for mammals, intermediate for birds and least for fishes, for a
specific SPL above baseline thresholds. Thus, a greater SPD between the noise
exposure and the baseline hearing threshold is required in fishes to achieve a
TTS similar to that found in mammals.
This is probably due to differences in mechanisms of sound detection and/or
in the structure of the ear between groups. While the ears of fishes respond
directly to the particle motion of a sound field, either through direct
stimulation of the otolith end organs or via a pressure detecting
device such as the swim bladder (Popper
and Fay, 1999), birds and mammals possess a tympanic membrane and
middle ear bones that amplify sounds impinging the tympanic membrane. Such
specializations affect how efficiently the energy from a noise of specific SPL
is transferred from the animal periphery to the inner ear.
If the TTS we report for goldfish is directly related to damage of inner
ear hair cells, then the difference in slopes of the LINTS relationships
between fish, birds and mammals may be due to differences in susceptibility to
noise-induced hair cell damage. The LINTS relationship plots TTS as a function
of SPL above baseline hearing thresholds. Experimentally, these SPL are
usually measured outside of the body of an animal. Such measurements may not
accurately reflect the amount of energy actually reaching the inner ear. For
example, the resonance of the external ear of humans can increase the SPL at
the tympanic membrane by 1520 dB at 2.5 kHz
(Weiner and Ross, 1946).
Additionally, the middle ear bones act as an impedance transformer to minimize
losses of sound energy associated with transmission from the air to cochlear
fluids. According to Nedzelnitsky
(1980
), the transfer function
of the middle ear shows a peak gain of
30 dB at 1 kHz. Most importantly,
the mammalian cochlea acts as an active amplifier, with a gain of up to 60 dB
(Viergever and Diependaal,
1986
).
Although hearing specialist fishes such as goldfish detect sound
via their swim bladder, and swim bladder motion is transmitted to the
inner ear through the Weberian ossicles, no data exist on the actual transfer
function of the swim bladder and/or Weberian ossicles. Based upon our current
knowledge of the morphology of Weberian ossicles, there is no reason to think
that potential amplification of sound by the swim bladder and ossicles
approximates the magnitude of the peripheral amplification in mammals. Thus,
the difference in the LINTS slopes between fish, birds and mammals may simply
be a function of efficiency of sound conduction to the ear for a given sound
level. An assumption of this hypothesis is that hair cells operate similarly
in fish, birds and mammals. This is probably a safe assumption since it is
generally believed that all vertebrate hair cells have fundamental
characteristics in common and function according to similar principles
(Popper and Fay, 1999). For
example, the most sensitive inner ear afferents of goldfish can detect otolith
particle motion as small as 0.1 nm (Fay,
1984
). This displacement sensitivity is similar to the threshold
of displacement in the guinea pig (0.2 nm;
Allen, 1997
), suggesting that
the physiological processes of transduction are similar in fish and
mammals.
In mammals, there is a relationship between hair cell loss and hearing
loss. For example, tuning curves of cat auditory nerve fibers were elevated
following noise and kanamycin exposure
(Liberman and Dodds, 1984).
Differences in the shape of these tuning curves were dependent upon specific
damage to the hair cells of the organ of Corti (i.e. whether inner, outer or
both hair cell types were damaged). Although there have been reports of fish
hair cells being damaged by exposure to sound or ototoxic drugs, no data are
yet available on the relationship between hair cell loss and hearing loss in
fishes.
Effects of noise duration and recovery
In Experiment 2, goldfish auditory thresholds returned to control levels
after 14 days of recovery, with considerable recovery occurring within the
first 7 days. It remains to be tested whether the recovery from hearing loss
was due to repair of mildly damaged hair cells or replacement of hair cells
that were destroyed. Four species of birds exposed to noise showed
considerable threshold shifts and hair cell damage immediately following
exposure, but over time both threshold shifts and hair cell numbers recovered
(Ryals et al., 1999). The
difficulty in making a correlation between hearing and hair cell recovery in
fishes arises because the only hair cell regeneration data available for
fishes come from studies using ototoxic drugs in which hearing was never
tested and there have been no comparable studies using acoustic trauma. Hair
cell ciliary bundle replacement appeared to be complete 10 days after maximal
gentamicin-induced hair cell damage in the oscar
(Lombarte et al., 1993
).
Similarly, mitotic activity suggesting hair cell regeneration was found in
adult quail 10 days after noise exposure
(Ryals and Rubel, 1988
).
After only 2 h of white noise exposure (142 dB re 1 µPa), fathead
minnows had thresholds that returned to control levels, but after 24 h of
exposure, thresholds were still significantly elevated after 14 days
(Scholik and Yan, 2001). Thus,
although goldfish and fathead minnows are both cyprinids and hearing
specialists, there appear to be species-specific differences in recovery time
from acoustic stimulation, although it is impossible at this point to rule out
subtle experimental differences as also contributing to the differences in
recovery time between species. Species-specific differences in recovery from
acoustic trauma have also been reported for birds
(Ryals et al., 1999
).
Duration of noise exposure (7 or 21/28 days) did not significantly affect
thresholds of goldfish in Experiment 2 because the ATS had already occurred.
In an additional short-term experiment, goldfish exhibited significant
threshold shifts after only 10 min of noise exposure and reached an ATS by 24
h of exposure (Smith et al.,
2004). This asymptotic relationship between duration of exposure
and hearing threshold shifts is well documented for mammals
(Clark, 1991
). Duration of
exposure can also affect time to recovery in mammals
(Mills et al., 1979
). While we
found that goldfish hearing recovered 14 days after a 21-day noise exposure,
further experiments are needed to understand the relationship between exposure
time and recovery time. A more thorough examination of the effects of
noise-exposure duration on TTS and recovery of goldfish hearing is provided
elsewhere (Smith et al.,
2004
).
Importance
The LINTS hypothesis is valid for underwater noise-induced TTS in some
fishes, as it is in aerial noise-induced TTS in land vertebrates. This
relationship standardizes TTS data from different studies for comparison. The
LINTS relationship is valid across different frequencies and SPLs and multiple
fish species and predicts, based on species-specific baseline thresholds, that
some species will exhibit TTS in response to a certain SPL of noise exposure,
while other species will not. Noise differentially affects species that differ
in hearing sensitivity and confirms intuition that a given noise exposure
would affect hearing specialists more than hearing generalists. The
differential threshold shifts between bluegill sunfish and goldfish can be
explained by a linear relationship between TTS and SPD above the fish's
baseline threshold, but the data for tilapia do not seem to fit LINTS
predictions. This LINTS hypothesis needs to be tested with more teleost
species and a broader range of noise SPLs. Such a linear relationship for
teleosts is consistent with what is found for birds and mammals, but greater
underwater SPLs are required to induce a comparable threshold shift as in
birds and mammals in air.
The LINTS relationship has potential utility in attempting to mitigate the
effects of anthropogenic underwater noise, although it would also need to be
determined for impulsive and repetitive sounds rather than continuous noise,
as used in these experiments and as experienced by fishes in aquaculture and
other similar facilities. Once a general LINTS relationship is agreed upon for
fishes, if a single relationship exists for all species that exhibit
noise-induced hearing loss, the expected TTS of a previously unstudied species
for a specified noise exposure (e.g. by an air gun) is only dependent upon the
species' audiogram. If unknown, an audiogram can be readily attained using the
ABR technique. This type of interpolation would be especially useful for the
impacts of extremely loud sounds that are difficult to produce in the
laboratory. McCauley et al.
(2003) found that fish caged
in the vicinity of seismic survey sounds exhibited severe inner ear damage.
Similar field experiments using intense sound are needed to examine how such
intense sounds affect fish hearing thresholds.
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Alder, J. A., Poje, C. P. and Saunders, J. C. (1993). Recovery of auditory function and structure in the chick after two intense pure tone exposures. Hear. Res. 71,214 -224.[CrossRef][Medline]
Allen, J. B. (1997). OHCs shift the excitation pattern via BM tension. In Diversity in Auditory Mechanics (ed. E. R. Lewis, G. R. Long, R. F. Lyon, P. M. Narins, C. R. Steele and E. Hecht-Poinar), pp. 167-175. Singapore: World Scientific Press.
Amoser, S. and Ladich, F. (2003). Diversity in noise-induced temporary hearing loss in otophysine fishes. J. Acoust. Soc. Am. 113,2170 -2179.[CrossRef][Medline]
Bart, A. N., Clark, J., Young, J. and Zohar, Y. (2001). Underwater ambient noise measurements in aquaculture systems: a survey. Aquacult. Eng. 25, 99-110.[CrossRef]
Campo, P., Subramaniam, M. and Henderson, D. (1991). The effect of "conditioning" exposures on hearing loss from traumatic exposure. Hear. Res. 55,195 -200.[CrossRef][Medline]
Canlon, B., Miller, J., Flock, A. and Borg, E. (1987). Pure tone overstimulation changes the micromechanical properties of the inner hair cell stereocilia. Hear. Res. 30,65 -72.[CrossRef][Medline]
Carder, H. M. and Miller, J. D. (1972). Temporary threshold shifts from prolonged exposure to noise. J. Speech Hear. Res. 15,603 -623.[Medline]
Clark, W. W. (1991). Recent studies of temporary threshold shift (TTS) and permanent threshold shift (PTS) in animals. J. Acoust. Soc. Am. 90,155 -163.[Medline]
Corwin, J. T., Bullock, T. H. and Schweitzer, J. (1982). The auditory brainstem response in five vertebrate classes. Electroencephalogr. Clin. Neurophysiol. 54,629 -641.[CrossRef][Medline]
Dijkgraaf, S. and Verheijen, F. (1950). Neue Versuche über das Tonunterscheidungsvermögen der Elritze. Z. Verg. Physiol. 34,248 -256.
Egan, J. P. and Hake, H. W. (1950). On the masking pattern of a simple auditory stimulus. J. Acoust. Soc. Am. 22,622 -630.
Enger, P. S. (1981). Frequency discrimination in teleosts central or peripheral? In Hearing and Sound Communication in Fishes (ed. W. N. Tavolga, A. N. Popper and R. R. Fay), pp. 243-255. New York: Springer-Verlag.
Fay, R. R. (1970). Auditory frequency discrimination in the goldfish (Carassius auratus). J. Comp. Physiol. Pyschol. 73,175 -180.
Fay, R. R. (1974). Sound reception and processing in the carp, saccular potentials. Comp. Biochem. Physiol. A 49,29 -42.[CrossRef][Medline]
Fay, R. R. (1978). Coding of information in single auditory nerve fibers of the goldfish. J. Acoust. Soc. Am. 63,136 -146.[Medline]
Fay, R. R. (1981). Coding of acoustic information in the eighth nerve. In Hearing and Sound Communication in Fishes (ed. W. N. Tavolga, A. N. Popper and R. R. Fay), pp.189 -221. New York: Springer-Verlag.
Fay, R. R. (1984). The goldfish ear codes the axis of particle motion in three dimensions. Science 225,951 -953.[Medline]
Fay, R. R. (1988). Hearing in Vertebrates: a Psychophysics Databook. Winnetka, IL: Hill-Fay.
Fay, R. R. (1997). Frequency selectivity of saccular afferents of the goldfish revealed by REVCOR analysis. In Diversity in Auditory Mechanics (ed. E. R. Lewis, G. R. Long, R. F. Lyon, P. M. Narins, C. R. Steele and E. Hecht-Poinar), pp.69 -75. Singapore: World Scientific Press.
Fay, R. R. and Megela Simmons, A. (1999). The sense of hearing in fishes and amphibians. In Comparative Hearing: Fish and Amphibians (ed. R. R. Fay and A. N. Popper), pp.269 -318. New York: Springer-Verlag.
Fay, R. R. and Popper, A. N. (1974). Acoustic stimulation of the goldfish (Carassius auratus). J. Exp. Biol. 61,243 -260.[Medline]
Fay, R. R. and Popper, A. N. (1975). Modes of stimulation of the teleost ear. J. Exp. Biol. 62,379 -388.[Abstract]
Fay, R. R. and Popper, A. N. (2000). Evolution of hearing in vertebrates: the inner ears and processing. Hear. Res. 149,1 -10.[CrossRef][Medline]
Fay, R. R. and Ream, T. J. (1986). Acoustic response and tuning in saccular nerve fibers of the goldfish (Carassius auratus). J. Acoust. Soc. Am. 79,1883 -1895.[Medline]
Fay, R. R., Ahroon, W. A. and Orawski, A. A. (1978). Auditory masking patterns in the goldfish (Carassius auratus): psychophysical tuning curves. J. Exp. Biol. 74,83 -100.[Abstract]
Feng, A. S. and Schellart, N. A. M. (1999). Central auditory processing in fish and amphibians. In Comparative Hearing: Fish and Amphibians (ed. R. R. Fay and A. N. Popper), pp. 218-268. New York: Springer-Verlag.
Fletcher, H. (1940). Auditory patterns. Rev. Mod. Phys. 12,47 -65.[CrossRef]
Furukawa, T. and Ishii, Y. (1967).
Neurophysiological studies on hearing in goldfish. J.
Neurophysiol. 30,1377
-1403.
Hastings, M. C., Popper, A. N., Finneran, J. J. and Lanford, P. J. (1996). Effect of low frequency underwater sound on hair cells of the inner ear and lateral line of the teleost fish Astronotus ocellatus. J. Acoust. Soc. Am. 99,1759 -1766.[Medline]
Hawkins, A. D. and Chapman, C. J. (1975). Masked auditory thresholds in the cod Gadus morhua L. J. Comp. Physiol. A 103,209 -226.
Hawkins, A. D. and Johnstone, A. D. F. (1978). The hearing of the Atlantic salmon, Salmo salar. J. Fish. Biol. 13,655 -673.
Higgs, D. M., Souza, M. J., Wilkins, H. R., Presson, J. C. and Popper, A. N. (2001). Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio). J. Assoc. Res. Otolaryngol. 3, 174-184.
Kenyon, T. N., Ladich, F. and Yan, H. Y. (1998). A comparative study of hearing ability in fishes; the auditory brainstem response approach. J. Comp. Physiol. A 182,307 -318.[Medline]
Kryter, K. D. (1985). The Effects of Noise on Man. Orlando, FL: Academic Press.
Liberman, M. C. and Dodds, L. W. (1984). Single-neuron labeling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves. Hear. Res. 16, 55-74.[CrossRef][Medline]
Lombarte, A., Yan, H. Y., Popper, A. N., Chang, J. S. and Platt, C. (1993). Damage and regeneration of hair cell ciliary bundles in a fish ear following treatment with gentamicin. Hear. Res. 64,166 -174.[CrossRef][Medline]
Mann, D. A., Higgs, D. M., Tavolga, W. N., Souza, M. J. and Popper, A. N. (2001). Ultrasound detection by clupeiform fishes. J. Acoust. Soc. Am. 109,3048 -3054.[CrossRef][Medline]
McCauley, R. D., Fewtrell, J. and Popper, A. N. (2003). High intensity anthropogenic sound damages fish ears. J. Acoust. Soc. Am. 113,1 -5.[CrossRef]
Melnick, W. (1976). Human asymptotic threshold shift. In Effects of Noise on Hearing (ed. D. Henderson, R. P. Hamernik, D. S. Dosanjh and J. H. Mills), pp.277 -289. New York: Raven Press.
Mills, J. H., Gengel, R. W., Watson, C. S. and Miller, J. D. (1970). Temporary changes of the auditory system due to exposure to noise for one or two days. J. Acoust. Soc. Am. 48,524 -530.[Medline]
Mills, J. H., Gilbert, R. M. and Adkins, W. Y. (1979). Temporary threshold shifts in humans exposed to octave bands of noise for 16 to 24 h. J. Acoust. Soc. Am. 65,1238 -1248.[Medline]
Myrberg, A. A., Jr (1990). The effects of man-made noise on the behavior of marine animals. Environ. Int. 16,575 -586.[CrossRef]
Nedzelnitsky, V. (1980). Sound pressures in the basal turn of the cat cochlea. J. Acoust. Soc. Am. 68,1676 -1689.[Medline]
NRC (National Research Council) (2000). Marine Mammals and Low Frequency Sound: Progress Since 1944. Washington, DC: National Academy.
Parvulescu, A. (1964). Problems of propagation and processing. In Marine BioAcoustics (ed. W. N. Tavolga), pp. 87-100. Oxford: Pergamon Press.
Popper, A. N. (2003). Effects of anthropogenic sound on fishes. Fisheries 28, 24-31.
Popper, A. N. and Clarke, N. L. (1976). The auditory system of the goldfish (Carassius auratus): effects of intense acoustic stimulation. Comp. Biochem. Physiol. A 53,11 -18.[Medline]
Popper, A. N. and Fay, R. R. (1999). The auditory periphery in fishes. In Comparative Hearing: Fish and Amphibians (ed. R. R. Fay and A. N. Popper), pp.43 -100. New York: Springer-Verlag.
Popper, A. N., Fay, R. R., Platt, C. and Sand, O. (2003). Sound detection mechanisms and capabilities of teleost fishes. In Sensory Processing in Aquatic Environments (ed. S. P. Collin and N. J. Marshall), pp. 3-38. New York: Springer-Verlag.
Pugliano, F. A., Pribitikin, E. and Saunders, J. C. (1993). Growth of evoked-potential amplitude in neonatal chicks exposed to intense sound. Act. Oto-Laryngol. 113, 18-25.
Ripley, J. L., Lobel, P. S. and Yan, H. Y. (2002). Correlations of sound production with hearing sensitivity in the Lake Malawi cichlid Tramitichromis intermedius.Bioacoustics 12,238 -240.
Ryals, B. M., Dooling, R. J., Westbrook, E., Dent, M. L., MacKenzie, A. and Larsen, O. N. (1999). Avian species differences in susceptibility to noise exposure. Hear. Res. 131,71 -88.[CrossRef][Medline]
Ryals, B. M. and Rubel, E. W. (1988). Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240,1774 -1776.[Medline]
Sand, O. and Hawkins, A. D. (1973). Acoustic properties of the cod swimbladder. J. Exp. Biol. 58,797 -820.
Sand, O. and Michelsen, A. (1978). Vibration measurement of the perch otolith. J. Comp. Physiol. 123, 85-89.
Saunders, J. C., Hills, J. H. and Miller, J. D. (1977). Threshold shift in chinchilla from daily exposure to noise for six hours. J. Acoust. Soc. Am. 61,558 -570.[Medline]
Scholik, A. R. and Yan, H. Y. (2001). Effects of underwater noise on auditory sensitivity of a cyprinid fish. Hear. Res. 152,17 -24.[CrossRef][Medline]
Scholik, A. R. and Yan, H. Y. (2002a). Effects of boat engine noise on the auditory sensitivity of the fathead minnow, Pimephales promelas. Environ. Biol. Fish. 63,203 -209.[CrossRef]
Scholik, A. R. and Yan, H. Y. (2002b). The effects of noise on the auditory sensitivity of the bluegill sunfish, Lepomis macrochirus. Comp. Biochem. Physiol. A 133, 43-52.
Smith, M. E., Kane, A. S. and Popper, A. N.
(2004). Noise-induced stress response and hearing loss in
goldfish (Carassius auratus). J. Exp. Biol.
207,427
-435.
Tavolga, W. N. (1974). Signal/noise ratio and the critical band in fishes. J. Acoust. Soc. Am. 55,1323 -1333.[Medline]
Viergever, M. A. and Diependaal, R. J. (1986). Quantitative validation of cochlear models using the Liouville-Green approximation. Hear. Res. 21, 1-15.[CrossRef][Medline]
von Frisch, K. (1938). The sense of hearing in fish. Nature 141,8 -11.
Ward, W. D. (1975). Studies in Asymptotic TTS. Aerospace Medical Specialists Meeting, Advisory Group for Aerospace Research and Development (AGARD). Toronto, Canada: North Atlantic Treaty Organization (NATO).
Weiner, F. M. and Ross, D. A. (1946). The pressure distribution in the auditory canal in a progressive sound field. J. Acoust. Soc. Am. 18,401 -408.
Welch, B. L. and Welch, A. S. (ed.) (1970). Physiological Effects of Noise. New York: Plenum Press.
Zar, J. H. (1984). Biostatistical Analysis. 2nd edition. Englewood Cliffs, NJ: Prentice-Hall.
Zelick, R., Mann, D. and Popper, A. N. (1999). Acoustic communication in fishes and frogs. In Comparative Hearing: Fish and Amphibians (ed. R. R. Fay and A. N. Popper), pp.363 -411. New York: Springer-Verlag.