Noise-induced stress response and hearing loss in goldfish (Carassius auratus)
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 20 October 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: threshold shift, hearing, noise, cortisol, glucose, ABR, recovery, fish, Carassius auratus
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Within the past decade, there has developed an increased awareness that
underwater anthropogenic (human-generated) sounds may be detrimental to marine
organisms by masking the detection of biologically relevant signals and/or
even damaging the exposed animals (NRC,
2000,
2003
). These sounds may be
associated with shipping, dredging, drilling, seismic surveys, sonar,
recreational boating and many other human-made sources. As a result of these
human-generated sounds, ambient noise levels in the ocean are thought to be
growing (NRC, 2003
). Early
estimates by Ross (1993
)
suggest a 10 dB increase from 1950 to 1975 alone or more than a doubling in
noise level. This is likely to have risen further with increases in shipping
and uses of other acoustic sources in parts of the oceans
(NRC, 2003
). Indeed, recent
forecasts by the National Oceanographic and Atmospheric Administration's
Marine Transportation System indicate that foreign oceanborne trade is
expected to double by the year 2020 (US
Department of Transportation, 1999
), and this could result in even
greater ocean noise levels in shipping lanes unless there are dramatic changes
in ship acoustics.
Substantial exposure of fish to acoustical stress is also found in many
aquaculture facilities (Bart et al.,
2001) that are important sources of food, ornamental species and
stock enhancement of wild populations. While considerable effort has been made
to optimize growth of aquaculture species by manipulating many environmental
parameters such as temperature, food quality, photoperiod, water chemistry and
stock density, little or no concern has been directed to determining the
appropriate acoustic environment for optimal growth and development. Rearing
conditions in aquaculture tanks can produce sound levels within the frequency
range of fish hearing that are 20-50 dB higher than in natural habitats
(Bart et al., 2001
). The few
studies that have examined the effects of sound levels on aquaculture species
show that high levels of ambient sound can potentially be detrimental and
result in reduced egg survival and reduced reproductive and growth rates
(Banner and Hyatt, 1973
;
Lagardère, 1982
).
Clearly, these studies need to be replicated and extended to additional
species and include analysis of additional parameters that could be indicative
of the effects of noise on developing fish.
While most research efforts to date, and public interest, have focused on
how underwater noise affects the behavior of marine mammals, the effects of
this noise pollution on fishes have rarely been examined
(Myrberg, 1990; NRC,
2000
,
2003
). It is known that
intense sounds can cause temporary hearing threshold shifts
(Popper and Clark, 1976
;
Scholik and Yan, 2001
) and
damage to the sensory cells of the ears of the few fish species that have been
studied (Enger, 1981
;
Hastings et al., 1996
;
McCauley et al., 2003
).
Besides damage to the inner ear, high levels of background noise may also
create physiological and behavioral stress responses in fishes similar to
those found in mammals (Welch and Welch,
1970
).
In the present study, we investigated the effect of high levels of continuous white noise exposure on the physiological stress levels (measured by plasma cortisol and glucose concentrations) and hearing loss (utilizing the auditory brainstem response technique) of goldfish (Carassius auratus). Our goal was to examine the effects of noise duration on the physiological stress responses and hearing shifts in order to elucidate a potential relationship between hearing loss and noise-induced physiological stress. We also examined the time course of hearing recovery.
In order to examine a broad range of noise exposure durations, we exposed goldfish to noise in two separate sets of experiments - a short-term experiment in which exposure durations ranged from 10 min to 24 h and a long-term experiment that ranged from 1 day to 21 days. We found that intense noise can produce initial physiological stress responses as well as short- and long-term hearing loss in goldfish.
We chose goldfish as a model hearing specialist because of their known
hearing sensitivity and the available literature database about hearing in
this species (Fay and Popper,
1974; Fay, 1988
).
Goldfish are otophysan fishes, which possess Weberian ossicles (modified
cervical vertebrae that abut the ear; von
Frisch, 1938
). These bones acoustically couple movement of the
swim bladder imposed by impinging sound pressure waves to the inner ear,
leading to enhanced hearing sensitivity that includes a broadened frequency
range of hearing and lower auditory thresholds when compared with fishes
without such specializations.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Two sets of experiments were performed to assess the effects of short-term noise exposure. One experiment examined the time course of physiological stress responses, and the other characterized the effect of exposure duration on temporary hearing threshold shifts. In the stress experiment, six fish were noise exposed in each of three 76-liter glass aquaria that were visually isolated from one another. Each tank was randomly assigned an exposure duration time (0 min,10 min or 60 min). In the short-term hearing study, groups of six fish were noise exposed for each of four exposure durations (0 min, 10 min, 1 h or 24 h) in a 19-liter bucket with an underwater speaker resting on the bottom. All work was done under the supervision of the Institutional Animal Care and Use Committee of the University of Maryland.
White noise exposure
All experiments were done using white noise with a bandwidth ranging from
0.1 kHz to 10 kHz at 160-170 dB re 1 µPa total sound pressure level (SPL).
The sound was presented via a Sony MiniDisc player through an
amplifier (5.2 A monoblock; 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. The white noise, which is 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 long- and short-term noise
exposure experiments, with transduction in the tanks having little effect on
the digitally generated flat white noise spectra
(Fig. 1). For the short-term
experiments, the SPL of the noise exposure varied within the bucket from 170
dB re 1 µPa at 1 cm directly above the speaker to 166-169 dB re 1 µPa at
8-14 cm above the speaker. For the long-term experiments, the SPL of the noise
exposure varied slightly within an aquarium, with a maximum (170 dB re 1
µPa) in the center right above the underwater speaker and a minimum
(161-168 dB re 1 µPa) near the sides farthest from the speaker. The SPL of
the control aquaria was in the range of 110-125 dB re 1 µPa. These SPLs are
equivalent to power spectral densities ranging from approximately 80 dB re1
µPa2/Hz (for controls) to 122 dB re 1 µPa2/Hz (for
maximal noise level). Although control and noise-exposed aquaria were in the
same room as 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 air-water interface
(Parvulescu, 1964), very
little sound was heard outside the noise tanks and none of this energy entered
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).
|
Cortisol and glucose assays
Blood plasma cortisol and glucose concentrations are commonly used as
indicators of primary and secondary stress in fishes, with cortisol exhibiting
a more rapid, transient response than glucose
(Mazeaud et al., 1977;
Mazeaud and Mazeaud, 1981
;
Barton et al., 1988
).
Preliminary tests were performed prior to noise-exposure experiments as a
positive control to evaluate cortisol and glucose levels in response to
physiological stress. In these preliminary tests, groups of goldfish
(N=6) were placed in 10 liters of water in a 19-liter bucket. The
control group was left undisturbed for 30 minwhile the treatment group was
exposed to repeated, continuous vibratory stress for 30 min caused by tapping
the bucket.
On each of the experimental days (0-21 days) of the long-term noise-exposure experiment, five fish were removed and bled from the control aquarium first and then from the noise-exposed aquarium. Blood was collected from the caudal vein using heparinized 1-ml 25G 5/8 tuberculin syringes and placed in centrifuge tubes. Each fish was caught singly in a net and removed slowly in an attempt to minimize capture-induced stress in the caught fish and other fish in the aquarium. The fish was bled immediately after capture and then placed in a bucket of water containing a buffered anesthetic, tricaine methanesulfonate (MS-222). It took approximately 7 min to bleed all five fish. Afterwards, the fish were sacrificed by cervical transection, and their inner ears were removed and placed in 4% paraformaldehyde-2% glutaraldehyde fixative for future ultrastructure examination using scanning electron microscopy (SEM).
Blood samples were centrifuged for 10 min at 2200 g and the plasma was then removed and stored at -70°C until analysis. Plasma cortisol, diluted 1:10 in a 0-cortisol standard in order to fit assay sensitivity, was assayed using an enzyme immunoassay (EIA) kit (DSL-10-2000, Diagnostic Systems Laboratories, Inc., Webster, TX, USA) with a four-parameter curve fit for standard curves. Plasma glucose was assayed using a Sigma Infinity glucose kit (Procedure 17-UV; Sigma Diagnostics, St Louis, MO, USA).
For the short-term noise-exposure experiment, one aquarium was randomly chosen for each exposure duration (0 min,10 min and 60 min) and all fish (N=6) were consecutively removed and bled. Blood plasma was then assayed as described for the long-term noise experiment.
Auditory brainstem response (ABR) technique
Auditory thresholds were measured using the auditory brainstem response
(ABR) technique. This is a noninvasive 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
;
Higgs et al., 2001
;
Scholik and Yan, 2001
).
Each fish was restrained in a mesh sling and suspended in a 19-liter plastic bucket filled with water. The fish was suspended so that the top of the head was approximately 3 cm below the water surface and 25 cm above a UW-30 underwater speaker. A reference electrode was placed on the dorsal surface of the fish's head along the midline between the anterior portion of the eyes while a recording electrode was placed on 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
physiology apparatus using SigGen and BioSig software [Tucker-Davis
Technologies (TDT) 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 duration and were gated through a Hanning window - similar to the
conditions of other ABR studies (Higgs et
al., 2001; Mann 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 calibration of each frequency used was done using a
calibrated Model 902 Interocean Systems, Inc. (San Diego, CA, USA) underwater
hydrophone (calibration sensitivity of -195 dB re 1 V/µPa; ±3 dB,
0.02-10 kHz, omnidirectional). Additional details of this ABR protocol have
been previously published (Higgs et al.,
2001
).
Hearing thresholds of the experimental fish were measured after specified durations of noise exposure. For the long-term experiment, these individuals came from the same aquaria as described for the cortisol and glucose assays, but different individuals were used (N=6). Additionally, 21-day-exposed goldfish were allowed to recover in quiet aquaria (<120 dB re 1 µPa), and their hearing thresholds were again measured 7 days and 14 days post-noise exposure.
For the short-term experiment, fish were noise exposed in a 19-liter bucket. For 10 min exposure durations, fish were held in place by the mesh sling described above and exposed in the same bucket from which ABRs were recorded. For 1-24 h duration exposures, fish were exposed in a separate bucket in which they could swim freely. There was no evidence that the fish sought areas of the lowest SPL (closest to the surface) or avoided the underwater speaker. All ABR recordings were started within a few minutes after noise exposure. Fish noise exposed for 24 h (short-term experiment) had their hearing measured immediately after noise exposure and then were allowed to recover in quiet aquaria as in the long-term experiment, except that ABR recordings were made 1, 4, 11 and 18 days after noise exposure.
Statistical analysis
Preliminary analyses of variance (ANOVAs) with treatment (control or noise
exposed) and bleeding order as factors showed that bleeding order had a
significant effect on the physiological stress response of the fish. To
account for this confounding effect on the effects of noise exposure on
goldfish plasma cortisol and glucose, analysis of covariance (ANCOVA) was
used, with noise-exposure duration as a factor and bleeding order as a
covariate. When significant main effects of noise exposure were found,
Wilcoxon signed ranks tests were used to make specific pairwise
comparisons.
The effects of noise exposure and recovery from the exposure on auditory
threshold levels were tested using separate ANOVAs, with duration of exposure
or recovery 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). Regression analysis was used to examine the effects of
noise exposure duration on temporary threshold shifts (TTS).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Noise exposure did not significantly affect cortisol or glucose concentrations in the long-term noise experiment (1-21 days exposure; P<0.10). In the short-term exposure experiment, noise exposure significantly affected plasma cortisol levels (P=0.01) but not glucose levels (P=0.27). Specifically, relative to controls, mean cortisol levels tripled after 10 min of noise exposure and then decreased back to control levels after 60 min of noise exposure (Fig. 2A). Although there was a trend of increasing mean glucose concentrations over the 60 min experimental exposure period, this trend was not statistically significant (Fig. 2B).
|
Effects of noise on auditory thresholds
Goldfish had a bandwidth of auditory sensitivity ranging from 0.1 kHz to 4
kHz and baseline auditory thresholds ranging between 60 dB re 1 µPa and 120
dB re 1 µPa (Fig. 3).
Exposure to the white noise caused an increase in auditory thresholds,
referred to as TTS. These threshold shifts are defined as temporary since they
decreased with time after recovery from noise exposure until thresholds were
similar to pre-noise-exposure levels. Approximately 5 dB TTS were evident
after only 10 min of noise exposure, and TTS increased to approximately 28 dB
after 24 h of exposure (Fig.
3). This log-linear increase exhibited in the short-term
noise-exposure experiment is described by the equation
TTS=27.7(log10D)+4.63 (r2=0.90,
P<0.0001), where TTS was averaged for frequencies between 0.1 kHz
and 2 kHz and D is the duration of noise exposure in days
(Fig. 4). Longer durations of
the long-term noise experiment (7 days and 21 days) produced threshold shifts
similar to that of the 24-h exposure duration, suggesting that an asymptotic
threshold shift (ATS) is reached within 24 h of noise exposure at the sound
levels used in this experiment. In other words, after the duration at which
the ATS is reached, no greater durations of noise exposure will produce
greater TTS. TTS resulting from 7 days and 21 days of exposure were
statistically less than those of 24 h exposures from the short-term noise
experiment (P<0.05). After 7 days of noise exposure, goldfish
exhibited significant mean threshold shifts that were approximately 20 dB
higher than baseline levels. Again, significant TTS occurred at all
frequencies examined (P<0.05). An additional week of noise
exposure (14 days) did not significantly increase the threshold shift. The
goldfish audiograms of this long-term noise-exposure experiment will be
presented elsewhere (M. E. Smith, A. S. Kane and A. N. Popper, unpublished
data).
|
|
In the short-term noise experiment, goldfish exposed to noise for 24 h had significantly lower thresholds one day after exposure when compared to thresholds determined immediately after noise exposure (P<0.0001), but even after 18 days of recovery, goldfish exhibited slightly higher thresholds than preexposure control levels (P<0.0001; Fig. 5).
|
In the long-term experiment, 21-day-exposed goldfish were allowed to recover from noise exposure. For each fish, TTS were averaged across all frequencies tested (0.1-4 kHz). TTS decreased with duration of recovery (from approximately 18 dB immediately after exposure to 0 dB after 2 weeks). After 7 days of recovery, there was still a significant overall effect of noise exposure on hearing thresholds when compared with preexposure controls (P=0.003; Fig. 6), although this difference was not significant for any particular frequency. After 14 days of recovery, auditory thresholds were no longer significantly different from preexposure thresholds (Fig. 6).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
During a stress response, there is an immediate release of catecholamines
followed by the activation of the hypothalamic-pituitary-interrenal axis,
which stimulates the synthesis and secretion of glucocorticoid hormones
(cortisol in teleosts; Schreck et al.,
2001). Our results show that noise exposure can elicit this
physiological cascade rapidly in goldfish (within 10 min) but that the
response is short-lived, with cortisol levels returning to pre-noise-exposure
levels within 1 h. The magnitude of the cortisol response was similar to that
found in other fishes. For example, plasma cortisol levels of rainbow trout,
Onchorynchus mykiss, increased from 29 ng ml-1 to 145 ng
ml-1 after 4 h of confinement
(Pankhurst, 1998
). Two-hour
net confinement resulted in an increase in cortisol levels from <25 ng
ml-1 to approximately 150 ng ml-1 in tilapia
(Oreochromis mossambicus; Nolan
et al., 1999
). The effect of stress on plasma glucose levels in
fishes is more ambiguous. While Nolan et al.
(1999
) found a significant
increase in tilapia cortisol and glucose levels due to confinement, Waring et
al. (1996
) only found a
cortisol effect in turbot (Scophthalmus maximus). Results from the
present study indicate a trend towards increasing plasma glucose values with
time of noise exposure in goldfish during the short-term experiment (0-60
min); however, no trend in either glucose or cortisol was evident in the
long-term experiment.
Two plausible reasons for this lack of a long-term stress effect are that
(1) fish became acclimated to the noise over time and/or (2) noise-induced
damage of the inner ear or nerves creates a threshold shift that effectively
reduces the level of perceived noise. In support of the first explanation,
rapid changes in sound characteristics often stimulate alarm behaviors, and
these changes may elicit stress-like responses much more than does continual
noise exposure. For instance, startle responses in red drum (Sciaenops
ocellatus) larvae are elicited by the onset of an acoustic stimulus, not
continuous exposure (Fuiman et al.,
1999). Physiological adaptation to a continuous stressor is
commonly found in fishes (Schreck,
2000
). For example, salmonids exposed to stressful social or
physical conditions exhibit an initial increase in plasma cortisol but return
to prestress levels within about a week
(Schreck, 1981
).
Although the behavioral response of fishes to noise may be transient, the
damage to their ears may happen quickly and have a longer-lasting effect. For
example, noise-induced damage to the sensory hair cells of codfish (Gadus
morhua) and oscar (Astronotus ocellatus) occurred after only 1 h
of continuous exposure to various frequencies (>180 dB re 1 µPa;
Enger, 1981;
Hastings et al., 1996
).
Additionally, auditory threshold shifts in fathead minnows (Pimephales
promelas) have been noted after only 1-2 h of noise exposure (142 dB re 1
µPa; Scholik and Yan, 2001
,
2002a
). We found significant
TTS in goldfish after only 10 min of stimulation. Thus, it is possible that
after threshold shifts occurred, the perceived level of the noise and the
resulting physiological stress level were reduced.
While we did not observe long-term physiological stress associated with continuous noise in goldfish, future studies are needed to examine whether loud intermittent or impulsive sounds produce such a response. Such intermittent sounds may more closely represent loud anthropogenic sounds that fish might experience in the wild (e.g. boat traffic, seismic surveys and sonar).
Effects of noise duration and recovery on auditory thresholds
Our control goldfish audiograms are similar to those previously published
in which psychophysical/behavioral methods were utilized
(Fay, 1988), except that our
audiograms have a slightly higher threshold at 200 Hz compared with 100 Hz.
This has been a consistent trend in audiograms obtained using ABR in our lab,
and a similar trend has been found in at least one other lab. Scholik and Yan
(2001
) published baseline
audiograms for fathead minnow (a cyprinid fish, as is goldfish) in which the
mean thresholds at 500 Hz were higher than those at 300 Hz. One possible
explanation for this trend is the ability of fish to use the lateral line to
detect lower frequency vibrations, so that a 100 Hz tone may be detected by a
goldfish's lateral line as well as by the ear, whereas a higher-frequency tone
would only be detected by the ear (Tavolga
and Wodinsky, 1965
). Other researchers examining noise-induced
damage in fish have not performed ABRs at frequencies below 200 Hz, probably
in order to avoid stimulating the lateral line, although in our lab, fishes
exposed to cobalt chloride to selectively ablate the lateral line did not have
ABR thresholds significantly different from controls
(Ramcharitar, 2003
). So,
despite no clear explanation of why thresholds were higher at 200 Hz compared
with 100 Hz for our goldfish, it is important to note that significant
noise-induced threshold shifts occur even at low frequencies.
Noise exposure had a considerable impact on threshold shifts (up to 28 dB)
at all frequencies in goldfish but with shifts being greater where their
hearing sensitivity is best. Popper and Clarke
(1976) examined the effects of
pure tones on threshold shifts in goldfish and found that SPLs of 149 dB re 1
µPa produced threshold shifts of approximately 7-9 dB and 18-27 dB at 500
Hz and 800 Hz, respectively. Thus, TTS were most dramatic at frequencies where
goldfish are more sensitive. Amoser and Ladich
(2003
) exposed goldfish to 158
dB re 1 µPa white noise for 24 h and found greatest hearing loss at 800 Hz
and 1000 Hz. Similarly, the fathead minnow, another hearing specialist,
exhibited approximately 11-20 dB TTS in response to 24 h of 142 dB re 1 µPa
white noise (0.3-4 kHz) exposure (Scholik
and Yan, 2001
) and 8-11 dB TTS in response to 2 h of 142 dB re 1
µPa narrow-bandwidth boat motor noise with a peak frequency near 1.3 kHz
(Scholik and Yan, 2002a
).
These shifts occurred at auditory frequencies where the fathead minnow is most
sensitive. Scholik and Yan
(2001
,
2002a
) did not find
significant, or as strongly significant, TTS at lower (0.3-0.8 kHz) and higher
(2.5-4 kHz) frequencies while we and Amoser and Ladich
(2003
) found significant TTS
across all frequencies. This may be the result of differences between species
or differences in experimental noise SPL and bandwidths.
Significant auditory threshold shifts were evident after only 10 min of
noise exposure in goldfish. Thus, loud sounds can have rapid detrimental
effects on fish hearing as well as on stress levels. This means that even
transient anthropogenic sounds such as boat traffic may affect fishes.
Previous studies examining the effect of noise on fish used durations of 1
h (Popper and Clarke, 1976
;
Scholik and Yan, 2001
,
2002b
;
Amoser and Ladich, 2003
). When
duration of noise exposure was log-transformed, the relationship between TTS
and duration was linear for our short-term experiment. This noise duration-TTS
relationship is similar to those found in birds and mammals, except that in
birds and mammals this relationship is more curvilinear, with the rate of TTS
increasing closer to the ATS (Carder and
Miller, 1972
; Saunders and
Dooling, 1974
). In goldfish, we noted a maximal threshold shift at
24 h of noise exposure. By contrast, Scholik and Yan
(2001
) found that fathead
minnows (also hearing specialists) exposed to white noise at 142 dB re 1
µPa reached an ATS after only 2 h of noise exposure. It is possible that
goldfish reach an ATS earlier than the initial 24 h observations made in the
present study. This is supported by lack of overall threshold differences
between goldfish exposed for 12 h and 24 h in Amoser and Ladich's study
(Amoser and Ladich, 2003
). It
is interesting to note that bird and mammal ATS are consistently reached
(using various exposure frequencies and SPL) between exposure durations of 8 h
and 24 h (Mills et al., 1970
;
Carder and Miller, 1972
;
Saunders and Dooling,
1974
).
Surprisingly, goldfish TTS observed in the long-term experiment were less than those for the 24-h-exposed fish. This is probably due to differences in container size between the two sets of experiments. Although the underwater speaker output was the same for both experiments, the 19-liter buckets used for the short-term experiment were smaller than the aquaria used in the long-term study. This put the fish in closer proximity to the underwater speaker in the short-term compared with the long-term experiment, which may have led to higher mean SPL and TTS.
Goldfish exposed to noise for 24 h had 10-20 dB decreases in auditory
thresholds after only 1 day of recovery. Despite this initial improvement,
thresholds did not return to preexposure levels even after 18 days of
recovery. Similarly, fathead minnows exposed to 142 dB re 1 µPa white noise
for 24 h still exhibited significant threshold shifts after 14 days of
recovery (Scholik and Yan,
2001). Longer-term recovery experiments are needed to ascertain
whether or not these smaller long-term shifts are permanent threshold shifts.
No permanent threshold shift has ever been reported for fish. In fact, fathead
minnows exposed for only 2 h had thresholds that returned to control levels
within 6 days postexposure (Scholik and
Yan, 2001
), and goldfish exposed for 12 h or 24 h returned to
control levels within 3 days of recovery
(Amoser and Ladich, 2003
). This
earlier recovery, when compared with the current study, may be due to the
relatively smaller noise SPL and durations used. In the present study,
goldfish exposed to noise for 21 days had auditory thresholds that returned to
control levels after 14 days of recovery, with considerable recovery occurring
within the first 7 days. As described earlier, the probable higher mean SPL
experienced in the short-term compared with the long-term experiment may
explain why full recovery occurred in goldfish exposed for 21 days but not for
those exposed for only 24 h. Thus, the time course of recovery may be
dependent on noise SPL as well as on duration.
Alternatively, since an asymptote of hearing loss was reached within 24 h
of noise exposure, it is possible that physiological and cellular repair
processes began as soon as noise-induced damage occurred and that the time
course of ear repair may be constant, even if noise exposure is continued
beyond the asymptote duration. The reason that continued exposure beyond the
asymptote duration did not produce greater TTS may be that maximal inner ear
hair cell damage occurs within the first 24 h. When hair cells are damaged,
one possible mechanism of repair is that they are extruded to the lumen, and
the supporting cells in the sensory epithelium are triggered to divide and
subsequently differentiate into hair cells and supporting cells
(Bermingham-McDonogh and Rubel,
2003). This process can take several days. For example, after
gentamicin exposure and subsequent hair cell loss, hair cells of the oscar
recovered within 10 days (Lombarte et al.,
1993
). After exposure to intense air-gun signals, pink snapper
(Pagrus auratus) did not exhibit significant hair cell damage 18
hpostexposure but exhibited significant damage 58 days postexposure,
suggesting that the damage and recovery process can take extended periods of
time (McCauley et al., 2003
).
In the current study, the 24-h-exposed fish did not show recovery after 19
days (1 day exposure + 18 days recovery) of the start of the exposure. The
21-day-exposed fish showed recovery 14 days after 21 days of stimulation,
which is 35 days after the start of the noise exposure. Thus, perhaps the bulk
of inner ear damage occurred on the first few exposure days and then at least
19 days are required for complete repair to take place. Thus, sufficient
repair may take 28-35 days, since 21-day-exposed fish did not show
control-level thresholds after 7 days of recovery but did recover after 14
days. Although further noise-induced damage to the inner ear sensory
epithelium may occur with exposure durations longer than 24 h, it is also
possible that hair cells damaged within the first 24 h undergo programmed cell
death followed by extrusion and regeneration (differentiation) of surrounding
supporting cells. These newly developing hair cells may effectively be
protected from further noise-induced damage until they are completely
differentiated.
SPL and duration of noise exposure can affect the magnitude of TTS and the
time to recovery as seen in mammals and birds
(Carder and Miller, 1972;
Saunders and Dooling, 1974
;
Mills et al., 1979
). Despite
the differences in the characteristics of sound conduction in air
versus water and the differences in ear anatomy and hearing
mechanisms in terrestrial vertebrates compared with fishes, the process of
noise-induced auditory threshold shifts seems to be similar in both groups.
Both show fairly linear increases in TTS with noise SPL and duration, followed
by an asymptotic maximal threshold shift. Both show that greater SPLs and
longer durations increase the time to recover to normal hearing levels. Thus,
it is likely that many of the general principles and relationships discovered
in the mammalian hearing literature will be applicable to how loud sounds
affect fishes - for example, the relationship between sensory cell loss and
hearing thresholds (Hamernik et al.,
1989
) and the exposure-equivalent principle
(Ward et al., 1959
).
In summary, our data show that goldfish are susceptible to noise-induced
stress and hearing loss. This is probably the result of their hearing
sensitivity, since `hearing generalists', or fish with higher baseline hearing
thresholds, are less vulnerable to noise-induced hearing loss. For example,
bluegill sunfish (Lepomis machrochirus) and tilapia did not exhibit
threshold shifts in response to intense noise exposure
(Scholik and Yan, 2002b; M. E.
Smith, A. S. Kane and A. N. Popper, unpublished data). This could be because a
certain noise SPL above a fish's baseline hearing threshold must be reached
before a TTS occurs (Hastings et al.,
1996
). Thus, fish with lower baseline audiograms (hearing
specialists) will be more susceptible to noise-induced hearing loss for a
given noise level. Despite the dramatic TTS that resulted from noise exposure,
goldfish were able to recover to normal hearing levels within two weeks of
being exposed to three weeks of noise. This may suggest that fish that have
been exposed to intense anthropogenic underwater noise may not have permanent
physiological or auditory injury.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
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]
Au, W. W. L. and Nachtigall, P. E. (1997). Acoustics of echolocating dolphins and small whales. Mar. Freshw. Behav. Physiol. 29,127 -162.
Banner, A. and Hyatt, M. (1973). Effects of noise on eggs and larvae of two estuarine fishes. Trans. Am. Fish. Soc. 1,134 -136.
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]
Barton, B. A., Schreck, C. B. and Fowler, L. G. (1988). Fasting and diet content affect stress-induced changes in plasma glucose and cortisol in juvenile chinook salmon. Progr. Fish Cult. 50,16 -22.
Bermingham-McDonogh, O. and Rubel, E. (2003). Hair cell regeneration: winging our way towards a sound future. Curr. Opin. Neurobiol. 13,119 -126.[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]
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]
Edds-Walton, P. L. (1997). Acoustic communication signals of mysticete whales. Bioacoustics 8,47 -60.
Engås, A., Løkkeborg, S., Ona, E. and Soldal, A. V. (1996). Effects of seismic shooting on local abundance and catch rates of cod (Gadus morhua) and haddock (Melanogrammus aeglefinus). Can. J. Fish. Aquat. Sci. 53,2238 -2249.[CrossRef]
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. (1988). Hearing in Vertebrates: a Psychophysics Databook. Winnetka, IL: Hill-Fay.
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. (2000). Evolution of hearing in vertebrates: the inner ears and processing. Hear. Res. 149,1 -10.[CrossRef][Medline]
Fuiman, L. A., Smith, M. E. and Malley, V. (1999). Ontogeny of routine swimming speed and startle responses in red drum, with a comparison of responses to acoustic and visual stimuli. J. Fish Biol. 55A,215 -226.[CrossRef]
Hamernik, R. P., Patterson, J. H., Turrentine, G. A. and Ahroon, W. A. (1989). The quantitative relation between sensory cell loss and hearing thresholds. Hear. Res. 38,199 -212.[CrossRef][Medline]
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 Myrberg, A. A. (1983). Hearing and sound communication underwater. In Bioacoustics: A Comparative Approach (ed. B. Lewis), pp.347 -405. London: Academic Press.
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]
Lagardère, J. P. (1982). Effects of noise on growth and reproduction of Crangon crangon in rearing tanks. Mar. Biol. 71,177 -185.
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., Tavolga, W., Souza, M. and Popper, A. N. (2001). Ultrasound detection by clupeiform fishes. J. Acoust. Soc. Am. 109,3048 -3054.[CrossRef][Medline]
Mazeaud, M. M. and Mazeaud, F. (1981). Adrenergic response to stress in fish. In Stress in Fish (ed. A. D. Pickering), pp. 49-75. London: Academic Press.
Mazeaud, M. M., Mazeaud, F. and Donaldson, E. H. (1977). Stress resulting from handling in fish: primary and secondary effects. Trans. Am. Fish. Soc. 106,201 -212.
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]
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]
Nolan, D. T., Op't Veld, R. L. J. M., Balm, P. H. M. and Wendelaar Bonga, S. E. (1999). Ambient salinity modulates the response of tilapia, Oreochromis mossambicus (Peters), to net confinement. Aquaculture 177,297 -309.[CrossRef]
NRC (2000). Marine Mammals and Low Frequency Sound: Progress Since 1944. Washington, DC: National Academy Press.
NRC (2003). Ocean Noise and Marine Mammals. Washington, DC: National Academy Press.
Pankhurst, N. W. (1998). Further evidence of the equivocal effects of cortisol on in vitro steroidogenesis by ovarian follicles of rainbow trout, Oncorhynchus mykiss. Fish Physiol. Biochem. 19,315 -323.[CrossRef]
Parvulescu, A. (1964). Problems of propagation and processing. In Marine BioAcoustics (ed. W. N. Tavolga), pp. 87-100. Oxford: Pergamon Press.
Pearson, W. H., Skalski, J. R. and Malme, C. I. (1992). Effects of sounds from a geophysical survey device on behavior of captive rockfish (Sebastes spp.). Can. J. Fish. Aquat. Sci. 49,1343 -1356.
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.
Ramcharitar, J. (2003).Structure-function relations in the inner ears of Western Atlantic Sciaenid fishes . Ph.D. Dissertation. University of Maryland, College Park, MD, USA.
Ross, D. (1993). On ocean underwater ambient noise. Acoust. Bull. 18,5 -8.
Saunders, J. C. and Dooling, R. J. (1974). Noise-induced threshold shift in the parakeet (Melopsittacus undulatus). Proc. Natl. Acad. Sci. USA 71,1962 -1965.[Abstract]
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.
Schreck, C. B. (1981). Stress and compensation in teleostean fishes: response to social and physical factors. In Stress and Fish (ed. A. D. Pickering), pp.295 -321. London: Academic Press.
Schreck, C. B. (2000). Accumulation and long-term effects of stress in fish. In The Biology of Animal Stress - Basic Principles and Implications for Animal Welfare (ed. G. P. Moberg and J. A. Mench), pp. 147-158. New York: CABI Publishing.
Schreck, C. B., Contreras-Sanchez, W. and Fitzpatrick, M. S. (2001). Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture 197, 3-24.[CrossRef]
Schwarz, A. L. and Greer, G. L. (1984). Responses of Pacific herring, Clupea harengus pallasi, to some underwater sounds. Can. J. Fish. Aquat. Sci. 41,1183 -1192.
Tavolga, W. N. and Wodinsky, J. (1965). Auditory capacities in fishes: threshold variability in the blue-striped grunt Haemulon sciurus. Anim. Behav. 13,301 -311.[Medline]
US Department of Transportation (1999). An Assessment of The U.S. Marine Transportation System. A Report To Congress. Washington: US Department of Transportation.
von Frisch, K. (1938). The sense of hearing in fish. Nature 141,8 -11.
Ward, W. D., Glorig, A. and Sklar, D. L. (1959). Temporary threshold shift produced by intermittent exposure to noise. J. Acoust. Soc. Am. 31,791 -794.
Waring, C. P., Stagg, R. M. and Poxton, M. G. (1996). Physiological responses to handling in the turbot. J. Fish Biol. 48,161 -173.[CrossRef]
Welch, B. L. and Welch, A. S. (ed.) (1970). Physiological Effects of Noise. New York: Plenum Press.
Zar, J. H. (1984). Biostatistical Analysis. Second 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.